Ovarian Cancer Surgery Case File

Ovarian Cancer Surgery Case File

Eugene C. Toy, MD, Konrad P. Harms, MD, Keith O. Reeves, MD, Cristo Papasakelariou, MD, FACOG

Case 17

A 58-year-old G3P3 Caucasian woman presents to your office complaining that, “I look like I am 6 months pregnant.” She gives a 6-month history of early satiety and increasing abdominal girth. She has lost 15 lb (6.8 kg) over the same time period and has noted a change in bowel habits with increasing constipation and diarrhea. She noticed some shortness of breath over the last few weeks. She reports no significant past medical history and has never had surgery. She has always had normal Papanicolaou (Pap) smears and underwent normal physiologic menopause without complications at age 52. She had a mammogram 2 years ago and has never had a colonoscopy. Her family history is noncontributory.

On physical examination, her abdomen is distended and no masses are palpable. She has a positive abdominal fluid wave. Pelvic examination reveals a normal appearing cervix and a palpable mass along the right adnexa that is more prominent on rectovaginal examination. Her stool guaiac is positive.

Her internist ordered a CT scan of the abdomen and pelvis. A large volume of ascites is noted. Additional findings include omental caking and an 8-cm complex mass partially compressing the sigmoid colon.

➤ What additional evaluation/treatment is needed prior to surgical intervention?

➤ What is your most likely diagnosis?

➤ What type of surgery should she undergo?

ANSWERS TO CASE 17:

Ovarian Cancer Surgery

Summary: This is a 58-year-old G3P3 woman with a pelvic mass, ascites, weight loss, and bowel symptoms whose most likely diagnosis is ovarian cancer.

➤ Additional preoperative evaluation/treatment: Check complete blood count (CBC), comprehensive metabolic panel, chest x-ray, electrocardiogram (ECG), and cancer antigen 125 (CA-125). Given patient’s age and CT findings, she should have a colonoscopy prior to surgical intervention.

➤ Most likely diagnosis: Ovarian cancer.

➤ Type of surgery: She should undergo exploratory laparotomy with the goal of optimal cytoreduction.

ANALYSIS

Objectives

1. Recognize the symptoms of ovarian cancer.
2. Be familiar with requirements of optimal cytoreduction and surgical staging in patients with early- and advanced-stage ovarian cancer.
3. Describe stage I cancer and fertility preservation.
4. Describe tumors of low malignant potential (LMP) and the possible need for staging.
5. Describe the management of adnexal masses during pregnancy.

Considerations

This is a 58-year-old Caucasian G3P3 woman with symptoms suggestive of ovarian cancer. Symptoms associated with ovarian cancer include pelvic/abdominal pain, urinary urgency, increased abdominal size, and early satiety.

In the preoperative evaluation, the physician should at a minimum, obtain a CBC, comprehensive metabolic panel, chest x-ray, and ECG for women older than 50 years. Thrombocytosis is seen in 22% of patients with ovarian cancer, which may be associated with advanced-stage disease. Serum electrolytes and liver function tests may identify underlying medical conditions which need correction

prior to surgery. A chest x-ray should be performed preoperatively to evaluate for pulmonary metastases and pleural effusions. A screening colonoscopy is an important part of the preoperative evaluation if significant bowel complaints are noted, for example, change in stool caliber or an increase in constipation, or if the physical examination or CT scan suggests the possibility of a primary bowel carcinoma. A CA-125 level should be drawn preoperatively to serve as a baseline level for follow-up if ovarian carcinoma is found.

The goal of cytoreductive surgery is the removal of the maximum amount of tumor possible to enhance the effectiveness of subsequent chemotherapy. Current practice parameters suggest that optimal cytoreduction means that there is no residual disease greater than 1 cm (cumulative). Primary surgical cytoreduction typically includes a total abdominal hysterectomy, bilateral salpingo-oophorectomy, omentectomy, pelvic and para-aortic lymph node dissection, and resection of any metastatic foci. Cytoreduction surgery may commonly include splenectomy, bowel resection, resection of metastatic peritoneal and diaphragmatic implants, and, rarely, liver resection and cholecystectomy.1-3 Optimal cytoreduction may not be feasible in patients with extra-abdominal metastases or with extensive disease in the hepatic parenchyma or porta hepatis, along the root of the small bowel mesentery, or in patients with bulky suprarenal lymphatic disease.4 Preoperative imaging may assist in the decision to proceed with primary surgery or neoadjuvant chemotherapy.

APPROACH TO

Suspected Ovarian Cancer

DEFINITIONS

CYTOREDUCTIVE SURGERY: The surgical process by which as much of the bulk of malignant tissue as possible is removed. Debulking is considered optimal when the largest residual tumor mass is less than 1 cm.

CANCER ANTIGEN 125: A protein that is found on the surface of most epithelial ovarian cancer cells, as well as peritoneal and fallopian tube carcinomas. An elevated serum level may indicate possible ovarian malignancy although in a premenopausal woman, there are conditions that can falsely elevate the CA-125 such as endometriosis, pregnancy, uterine fibroids, or pelvic inflammatory disease. A level exceeding 35 mcg/mL is considered elevated.

INTRAPERITONEAL CHEMOTHERAPY: Chemotherapy administered directly into the peritoneal cavity rather than intravenously.

NEOADJUVANT CHEMOTHERAPY: The use of chemotherapy prior to surgery to chemically debulk the cancer and make subsequent surgery less complicated and increase the chance of optimal cytoreduction. However, whether or not neoadjuvant chemotherapy improves overall survival is still controversial.

CLINICAL APPROACH

Most patients with ovarian cancer will present with advanced-stage disease, as currently, there is no proven way to detect early disease. Many patients present with pelvic or abdominal pain, early satiety, and increased abdominal girth for several months preceding diagnosis. A recent study showed that when affected women were carefully questioned, many of them reported having the above symptoms for at least 12 days out of each month during the 12 months prior to diagnosis: 60% of those with early-stage invasive disease and 79% of those with advanced-stage invasive disease. While all of these symptoms are nonspecific when they occur with increasing frequency and severity, they merit an evaluation for possible ovarian cancer.5

Etiology

Epidemiologic association with increased risk of ovarian cancer includes early menarche, late menopause, low parity, infertility, the use of perineal talc, and consumption of galactose. The use of oral contraceptives for at least 5 years and history of a tubal ligation are associated with a decreased risk. The use of fertility-enhancing medications has not been definitively associated with an increased risk.

Hereditary ovarian cancer is associated with BRCA1 gene mutations, located on chromosome 17. The risk to develop ovarian cancer can be as high as 28% to 44% in patients from these high-risk families. Another gene, BRCA2, located on chromosome 13, is associated with a smaller proportion of ovarian cancers. The risk of development of ovarian cancer for BRCA2 mutation carriers approaches 27%.6 A third important syndrome is the Lynch syndrome, also known as hereditary nonpolyposis colon cancer syndrome (HNPCC). Patients with Lynch syndrome have a higher-thanexpected risk to develop either endometrial and ovarian cancers or colon cancer. Thus, affected patients with a strong family history of ovarian or breast cancer should undergo genetic counseling and testing. Those found to have a deleterious mutation may choose to reduce their risk for developing cancer by undergoing prophylactic salpingo-oophorectomy after completion of childbearing. Patients who desire to retain their childbearing potential may opt to take birth control pills, which decreases the risk of ovarian cancer.

Diagnosis

The diagnosis of ovarian cancer is ideally made by obtaining tissue for histologic examination (see Figure 17–1 in a patient who presented with an adnexal mass undergoing laparoscopy). Although surgical evaluation for a persistent adnexal mass is preferred, there are clinical scenarios that may contraindicate surgery. For example, patients with multiple medical problems deemed unfit for cytoreduction surgery may opt to undergo needle biopsy for tissue diagnosis, thoracentesis, or paracentesis for cytologic diagnosis. Subsequently, these patients may be considered for neoadjuvant chemotherapy if cancer is diagnosed.

Patients diagnosed with apparent Stage I (no obvious metastatic cancer outside of the ovary) invasive ovarian carcinoma need comprehensive surgical staging as the risk of undetected metastatic disease is high. Comprehensive surgical staging includes hysterectomy with bilateral salpingo-oophorectomy,

Figure 17–1. A large cystic ovarian mass is noted on laparoscopy. (Courtesy of Dr. Cristo Papasakelariou.)

omentectomy, and pelvic and para-aortic lymphadenectomy. A biopsy is done to evaluate any clinically suspicious area in the abdominal cavity. If no abnormality is readily visible, random biopsies are taken from the bladder peritoneum, bilateral pelvic sidewall, posterior cul-de-sac, bilateral paracolic gutters, and from each side of the undersurface of the diaphragm. Collection of peritoneal washings for cytologic examination is also done.

Early Cancer in Women Desiring Fertility Patients with early-stage ovarian cancer who desire future fertility present a unique group of patients for the gynecologic oncologist. A conservative approach, preserving the uterus and contralateral ovary, may be used if the likelihood of cure is not compromised while preserving reproductive potential. Comprehensive surgical staging in this group of patients is of utmost import. As a definitive diagnosis based on frozen section diagnosis may be difficult, these patients accept the risk that further surgical procedures may be necessary based on final histologic diagnosis. Generally, these patients may opt to undergo hysterectomy and removal of the contralateral ovary at the completion of childbearing.7,8

Low Malignant Potential Patients with a low malignant potential (LMP) or borderline tumor have a much better prognosis than patients with invasive ovarian cancers. Surgical staging is important for these patients because 5% of patients with borderline tumors diagnosed on frozen section analysis

Table 17–1 FIGO STAGING FOR PRIMARY OVARIAN CANCER

Stage I: Limited to ovaries Stage IA: Limited to one ovary, no tumor on external surface, capsule intact. Stage IB: Limited to both ovaries, no tumor on external surface, capsule intact. Stage IC: Tumor stage IA or IB but with tumor on the surface of one or both ovaries or capsule rupture or ascites positive for malignancy or with positive peritoneal washings.   Stage II: Involving one or both ovaries, limited to pelvis Stage IIA: Extension or metastases to uterus and/or fallopian tubes. Stage IIB: Extension to other pelvic tissue. Stage IIC: Tumor either stage IIA or IIB but with tumor on the surface of one or both ovaries or capsule rupture or ascites positive for malignancy or with positive peritoneal washings.   Stage III: Extension beyond true pelvis Stage IIIA: Involving one or both ovaries grossly limited to pelvis with negative nodes but histologically confirmed microscopic seeding of abdominal peritoneal surfaces.   Negative nodes. Stage IIIB: Involving one or both ovaries with histologically confirmed implants of abdominal peritoneal surfaces, none greater than 2 cm. Negative nodes. Stage IIIC: Abdominal implants greater than 2 cm in diameter and/or positive retroperitoneal or inguinal nodes.   Stage IV: Distant metastases If pleural effusion is present, cytologic diagnosis is necessary for a patient to be staged as having stage IV disease. Parenchymal disease is also allotted to this stage. Extraperitoneal disease is also included in stage IV.

Abbreviation: FIGO, International Federation of Gynecology and Obstetrics.

may have true invasive carcinoma upon final pathologic diagnosis. However, patients who have a final pathologic diagnosis of low malignant potential have an excellent 5-year survival rate of 99% for stage I and 92% for stages II and III (see Table 17–1 for ovarian cancer staging). Even for patients with advanced-stage disease, adjuvant therapy is not recommended because it has not been shown to improve survival. Approximately 10% of patients will develop recurrent disease, which is often managed by repeat surgical removal of recurrent lesions with careful pathologic evaluation for progression to invasive carcinoma.9,10

Ovarian Cancer in Pregnancy Patients diagnosed during the first trimester of pregnancy with an adnexal mass, measuring 6 cm or greater, merit close observation. Most of these masses will resolve by the second trimester. However, up to 28% of patients with a persistent mass may develop acute symptoms, necessitating emergent surgery. Thus, a reasonable management schema is to surgically evaluate persistent masses between 15 and 19 weeks’ of gestation. Among patients who undergo surgery during pregnancy, common findings are a dermoid cyst or serous cystadenoma; the chance of finding a malignant tumor is low, usually less than 5%. Waiting beyond 23 weeks increases the risk of adverse pregnancy outcomes, including preterm delivery. The decision to perform either laparoscopic or open surgery during pregnancy depends on the individual patient’s clinical situation and the ability of her surgeon.11

Treatment

The initial treatment for ovarian cancer is optimal cytoreduction as survival is clearly improved with lower volume of residual disease. This step cannot be overemphasized, and meticulous care and sufficient time should be devoted to the removal of cancer to maximize the patient’s outcome. After maximal cytoreduction, adjuvant chemotherapy with a platinum-based regimen is the standard. Intraperitoneal chemotherapy has recently been shown to improve median overall survival when compared to intravenous chemotherapy in advanced-stage ovarian cancer patients. In this trial conducted by the Gynecologic Oncology Group (2006), patients received IV paclitaxel (135 mg/m2) over 24 hours, then intraperitoneal cisplatin (100 mg/m2) on day 2 and intraperitoneal paclitaxel (60 mg/m2) on day 8 every 3 weeks for six cycles. Although only 42% of patients were able to complete all six cycles of intraperitoneal chemotherapy due to complications, the intraperitoneal chemotherapy group had a 16-month increase in median overall survival. Patients undergoing intraperitoneal therapy reported a decreased quality of life when compared to patients undergoing conventional intravenous chemotherapy, but these differences equalized at 1 year following treatment. For patients who are not ideal candidates for intraperitoneal chemotherapy, chemotherapy with intravenous carboplatin (starting dose area under the curve [AUC] = 5-6 mg/mL • min) and paclitaxel (175 mg/m2) every 3 weeks for six cycles is given.12

Surgical Approach

Surgery for ovarian cancer is almost universally approached through a vertical skin incision, whose length may be extended as the need arises. After entry into the abdomen, peritoneal washings are obtained and sent for cytologic evaluation. If ascites is present, this is collected and sent in lieu of washings. Systematic exploration of the abdominal cavity is performed to evaluate the extent of disease and the plan for resection of disease. Careful assessment is important for prognostic purposes, plan for the surgical resection, and later consideration for adjuvant therapy. In addition to evaluation of the pelvic organs, particular attention is paid to the surfaces of the diaphragm bilaterally, the mesentery of the small bowel, and the retroperitoneal lymphatic nodes.

For patients not interested in future fertility, surgery includes removal of the uterus, bilateral tubes and ovaries, omentum, and pelvic and para-aortic lymph nodes. For patients with widespread peritoneal metastases, removal of metastatic disease is achieved to enable optimal cytoreduction (largest residual disease < 1 cm). Commonly, the sigmoid colon and ovarian masses are coalesced into one large tumor mass for which surgical planes are not found. In this case, a retroperitoneal approach to remove en bloc all affected organs is taken as the planes of dissection are often still preserved in this area despite massive intra-abdominal disease.

The omentum is often infiltrated and thickened with tumor. This “omental cake” can be dissected from the underlying transverse colon and stomach and removed. Bowel resection and reanastomosis are done to enable optimal cytoreduction. Disease on peritoneal surfaces may be removed by a technique referred to as “peritoneal stripping.” This stripping technique may be done also for tumor plaques on the diaphragm in which case inadvertent entry into the thoracic cavity and resultant pneumothorax is an uncommon, but not rare, complication.

Lymphadenectomy is performed for staging from the level of the renal veins, past the bifurcation of the aorta and iliac vessels and until the circumflex vein as the vessels enter the inguinal canal. Enlarged nodes are removed as part of cytoreduction. Often, identifying the avascular areas of the pelvis, for example, the pararectal and paravesical spaces, makes surgery easier. Identifying the course of the ureter is important to avoid injury, especially when there is significant disease distorting pelvic anatomy.

At the end of the surgery, the abdomen is closed using a mass closure, such as the Smead-Jones technique or its various modifications. The strength of the closure is critical due to the patient likely having recurrence of ascites, and possible delayed wound healing such as due to malnutrition. Good technique is important to prevent infectious or dehiscence wound complications that may delay adjuvant chemotherapy.

Complications

When operating in the deep pelvis, injury to vascular structures and massive blood loss are possible. In anticipation of blood loss and need for transfusion, a type and cross match should be done prior to surgery. The planned procedure is discussed with the anesthesiologist so that adequate lines and monitoring equipment are available for emergent use. Intraoperatively, if a vessel injury occurs, pressure is quickly applied with either a sponge stick or the surgeon’s hand. Subsequently, a clamp may be used to obtain hemostasis and the vessel repaired.

Entry into the intestinal tract is a common occurrence, either intentionally or inadvertently, as part of surgery for ovarian cancer. Prompt recognition of inadvertent entry is the key to prevention of further complications, including abscess and fistula formation. Serosal tears and small luminal entry are easily repaired with sutures. Occasionally, larger injury may necessitate resection and reanastomosis of the normal bowel segments.

Ureteral injury is best avoided by tracing the normal course of the ureters in the retroperitoneal space within the medial leaf of the broad ligament. For patients with distorted retroperitoneal anatomy (eg, patients with previous retroperitoneal dissection, severe endometriosis, or renal anomalies), preoperative ureteral stenting may assist the surgeon by allowing intraoperative palpation of the course of the ureters when visualization is impossible. Obvious injury is repaired intraoperatively. However, simple ureteral stenting will allow most small injuries to heal spontaneously. Occasionally, late injury due to devascularization of the ureters may not present until more than 1 week after surgery.

The risk of postoperative complications increases with the extent of surgery and the comorbidities of the patient. Fever and ileus are frequent occurrences, as are urinary tract and wound complications. Anemia is common, both from the disease process and surgical blood loss. Blood loss greater than 1 L occurs in as many as 20% of patients.

Thromboembolic disease is a common complication of surgery. Postoperative ovarian cancer patients have all three characteristics identified as Virchow triad: hypercoagulability due to the cancer, vessel wall injury, and stasis from the surgical procedure itself. Pre- and postoperative DVT prophylaxis is critically important. There are many published guidelines for the use of sequential compression devices and heparin, both unfractionated and low-molecular weight. For the postoperative cancer patients, heparin in the immediate postoperative period is preferred. Extended thromboprophylaxis after hospital discharge is recommended in selected high-risk patients, for example, those with past history of DVT or a hypercoagulable state.13

Splenectomy is often part of cytoreduction for disease in the upper abdomen. Complications include pancreatic injury and pancreatic pseudocyst formation as the spleen lies in proximity to the pancreas. Most patients will also have a transient leukocytosis and thrombocytosis. Ideally, 14 days prior to a planned splenectomy, the patient will undergo preoperative immunization for Haemophilus influenzae, Streptococcus pneumoniae, and Neisseria meningitidis as asplenic patients have increased risk of infection from these encapsulated organisms. Postoperative immunization may also be done 14 days after surgery.14

Comprehension Questions

17.1 A 25-year-old nulligravida woman undergoes exploratory laparotomy and left salpingo-oophorectomy for an adnexal mass. Frozen section analysis shows a borderline serous tumor. The rest of the abdomen and pelvis is grossly normal. Which of the following is an appropriate intraoperative management?

A. Close the abdomen as she is interested in fertility and await final histologic diagnosis.

B. Proceed with total abdominal hysterectomy and remove the contralateral tube and ovary.

C. Proceed with surgical staging without removing the uterus and contralateral ovary.

D. Biopsy the contralateral ovary and remove the ovary if abnormal.

17.2 Which of the following statements is correct for a patient who has a BRCA1 mutation?

A. Prophylactic bilateral salpingo-oophorectomy is indicated after completion of childbearing.

B. The patient has an 80% lifetime risk of developing ovarian cancer.

C. If the patient is interested in delaying future fertility, oral contraceptive usage may increase her risk of developing ovarian cancer.

D. She has a mutation on chromosome 11.

17.3 A 21-year-old at 9 weeks’ of gestation presents for her first prenatal examination. You diagnose an adnexal mass measuring 6 cm with complex features. She is completely asymptomatic. Which of the following is an appropriate management for this patient?

A. Expectant management with serial ultrasounds.

B. Immediate laparotomy and unilateral salpingo-oophorectomy.

C. No further evaluation; the adnexal mass is most likely a corpus luteum and should resolve.

D. Immediate laparoscopic evaluation with plans for conversion to laparotomy if a cancer is suspected.

17.4 A 22-year-old G0 woman recently had surgery for a left adnexal mass and underwent a unilateral salpingo-oophorectomy. The other ovary appeared normal during the case. Final pathology revealed a serous tumor of low malignant potential. What is the next management step?

A. Immediate exploratory laparotomy and staging.

B. Immediate operative laparoscopy with staging.

C. Observation and close follow-up.

D. Immediate exploratory laparotomy with a total abdominal hysterectomy and removal of contralateral adnexa.

ANSWERS

17.1 C. Surgical staging is appropriate as a frozen section diagnosis of a borderline (LMP) tumor carries approximately 5% risk of upstaging to an invasive carcinoma on final histologic examination. Random biopsy of a grossly normal contralateral ovary is not indicated because it is unlikely to find microscopic foci of tumor, but may lead to complications such as bleeding, necessitating removal of a normal ovary. Removal of the uterus or the remaining ovary is not indicated if the patient is interested in future fertility.

17.2 B. The BRCA1 mutation is an autosomal dominant mutation located on chromosome 17. This mutation confers up to an 80% lifetime risk of development of breast cancer and a 28% to 44% lifetime

risk of developing ovarian cancer. Current recommendations include the use of oral contraceptives for women who are interested in future fertility to decrease the risk of developing ovarian cancer, and prophylactic bilateral salpingo-oophorectomy after completion of childbearing. Other recommendations for carriers include increased breast surveillance and gynecologic surveillance of the ovaries with serial ultrasounds and measurement of CA-125. Even after prophylactic oophorectomy, there is a risk of developing peritoneal carcinoma; thus, continued gynecologic surveillance is mandatory.

17.3 A. A pregnant patient with an asymptomatic adnexal mass needs follow-up. This is most easily done with serial ultrasounds. Immediate surgical evaluation is not indicated unless the patient is symptomatic. If the mass persists at 15 to 19 weeks’ gestation, surgical evaluation either with laparoscopy or laparotomy for a mass greater than 6 cm is reasonable even if the patient is asymptomatic. With a large mass, there is a risk of torsion and acute pain later in pregnancy, which may lead to adverse pregnancy outcomes.

17.4 C. Recent studies have shown that survival and outcome for patients with low malignant potential tumors of the ovary are not dependent on surgical staging. As she has not completed childbearing, she needs observation and close follow-up but does not require repeat surgery for staging.

Clinical Pearls

See Table 1-2 for definition of level of evidence and strength of recommendation

➤ Patients who have a strong family history of breast and/or ovarian cancer should undergo genetic counseling and possible testing for BRCA1 and BRCA2. Risk-reducing salpingo-oophorectomy should be offered to these patients once they have completed childbearing (Level A).

➤ The goal of surgical staging is to leave minimal disease residual. Optimal cytoreduction means that there is no residual cancer mass of larger than 1 cm (Level A).

➤ Adjuvant therapy with intraperitoneal chemotherapy has recently been shown to increase survival in patients with ovarian cancer (Level A).

➤ Patients who present with less than a 1-year history of pelvic/abdominal pain, urinary urgency, and early satiety occurring more than 12 d/mo merit an evaluation for ovarian cancer (Level B).

➤ Consider surgery for pregnant patients with growing or persistent adnexal masses of larger than 6 cm at 15 to 19 weeks (Level C).

REFERENCES

1. Chen LM, Leuchter RS, Lagasse LD. Splenectomy and surgical cytoreduction for ovarian cancer. Gynecol Oncol. 2000;77:362-368. 

2. Eisenhauer EL, Abu-Rustum NR, Sonoda Y, et al. The addition of extensive upper abdominal surgery to achieve optimal cytoreduction improves survival in patients with Stage IIIC-IV epithelial ovarian cancer. Gynecol Oncol. 2006;103:1083-1090. 

3. Eisenkop SM, Spirtos NM, Lin WC. Splenectomy in the context of primary cytoreductive operations for advanced epithelial ovarian cancer. Gynecol Oncol. 2006;100:344-348. 

4. Chi DS, Eisenhauer DL, Lang J, et al. What is the optimal goal of primary cytoreductive surgery for bulky stage IIIC epithelial ovarian carcinoma? Gynecol Oncol. 2006;103:559-564. 

5. Goff BA, Mandel LS, Drescher CW, et al. Development of an ovarian cancer symptom index: possibilities for earlier detection. Cancer. 2007;109:221-227. 

6. King MC, Marks JH, Mandell JB for the New York Breast Cancer Study Group. Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2. Science. 2003;302:643-646. 

7. Rao GG, Skinner EN, Gehrig PA, Duska LR, Miller DS, Schorge JO. Fertilitysparing surgery for ovarian low malignant potential tumors. Gynecol Oncol. 2005;98:263-266. 

8. Schilder JM, Thompson AM, DePriest PD, et al. Outcome of reproductive age women with Stage IA or IC invasive epithelial ovarian cancer treated with fertilitysparing therapy. Gynecol Oncol. 2002;87:1-877. 

9. Ayhan A, Guven ESG, Guven S, Kucukali T. Recurrence and prognostic factors in borderline ovarian tumors. Gynecol Oncol. 2005;98:439-445. 

10. Wingo SN, Knowles LM, Carrick KS, Miller DS, Schorge JO. Retrospective cohort study of surgical staging for ovarian low malignant potential tumors. Am J Obstet Gynecol. 2006;194:20-22. 

11. Stany MP, Elkas JC. Laparoscopy for adnexal masses in pregnancy? Contemporary OB/Gyn. 2007;52:44-49. 

12. Armstrong DK, Bundy B, Wenzel L, et al. Intraperitoneal cisplatin and paclitaxel in ovarian cancer. N Engl J Med. 2006;354:34-43. 

13. Kakkar AK. Prevention of venous thromboembolism in the cancer surgical patient. J Clin Oncol. 2009;27:4881-4884. 14. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5753a6.htm. Accessed December 17, 2009.

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