1216 Obesity Surgery, 14, 2004 © FD-Communications Inc.

Obesity Surgery, 14, 1216-1221

Background: Ovarian disease is common in obesewomen and is usually not screened during routinepreoperative evaluation in patients undergoingbariatric surgery. Consequently, surgeons mayencounter previously undiagnosed adnexal tumorsduring bariatric operations.The aim of this study is toreport our experience with incidental ovarian tumorsin patients during Roux-en-Y gastric bypass(RYGBP).

Methods: Prospectively collected data on all con-secutive patients undergoing RYGBP for clinicallysignificant obesity from July 1998 to September 2003were reviewed for patients with incidental gynecolog-ical tumors. Details of operative treatment and out-comes are reported herein.

Results: 460 women underwent RYGBP during thestudy period. 52 (11%) had a previous hysterectomyand/or bilateral oophorectomy and were excludedfrom the study. 12 ovarian masses, median tumor size11 cm (range 4-65 cm) were found in 10 women (2.5%)during 6 open and 4 laparoscopic RYGBPs. Mean agewas 40±9 years and mean BMI was 58±12 kg/m2.Resection of 9 benign cystic lesions and 2 malignantlesions was undertaken. One patient with polycysticovary syndrome did not undergo resection. TheRYGBP was completed in all but 2 patients who, byappearance and intraoperative frozen biopsy, had evi-dence of malignancy. No additional morbidity resultedfrom the added gynecological procedure. Based onthese results, an algorithm for the treatment of inci-dental gynecological tumors is suggested.

Conclusions: Although infrequent, incidental ovariantumors may be discovered in patients undergoingbariatric surgery, emphasizing the importance of thor-ough exploration of the abdominal cavity. Consult-ation with a gynecologist is warranted in most

instances, and treatment should be on a patient-by-patient basis, especially in women of child-bearingage.

Key words: Morbid obesity, gastric bypass, adnexal mass,ovarian cyst, ovarian carcinoma, polycystic ovary syn-drome

Introduction

Obesity has become an epidemic throughout mostof the developed world. According to the NationalCenter for Health Statistics (NCHS) and Center forDisease Control (CDC), the prevalence of obesity inthe United States has doubled in adults and tripledin children over the last 20 years.1 Weight-loss regi-mens, medications, and behavioral treatment, whichinclude modifying eating, activity, and thinkinghabits that contribute to patients' weight problemshave resulted in disappointing sustainable weightloss.2,3 Operative treatment has been recognized asthe only effective treatment for clinically significantobesity and its related co-morbidities. Roux-en-Ygastric bypass (RYGBP) is the procedure of choiceand the most commonly performed weight-lossoperation in North America.

Obesity is among the clinical features of womenwith polycystic ovary syndrome (PCOS), which isthe most common cause of anovulatory infertilityaffecting up to 10% of women of reproductiveage.4,5 Compared to non-obese women, patientswith a body mass index (BMI) >30 kg/m2 are atgreater risk of ovarian cancer (odds ratio = 1.15;

Management of Incidental Ovarian Tumors inPatients Undergoing Gastric Bypass

Rodrigo Gonzalez, MD; Krista Haines, BA; Scott F. Gallagher, MD;Geremy Sanders, MD; Mitchel Hoffman, MD*; Michel M. Murr, MD

Interdisciplinary Obesity Treatment Group, Departments of Surgery and Gynecologic Oncology*,University of South Florida Health Sciences Center, Tampa, FL, USA

Reprint requests to: Michel M. Murr, MD, FACS, Director ofBariatric Surgery, University of South Florida College ofMedicine, c/o Tampa General Hospital, PO Box 1289, Tampa, FL33601, USA. Fax: (813) 844-1920; e-mail: mmurr@hsc.usf.edu

95%CI = 1.44 to 2.64).6 Furthermore, higher BMI isassociated with increased risk for death from ovar-ian cancer.7

Routine preoperative screening for ovarian dis-ease is not common in women undergoing bariatricsurgery; consequently, surgeons may encounter apreviously undiagnosed adnexal mass during rou-tine abdominal exploration. As such, surgeons per-forming bariatric procedures should be familiar withidentification and management of ovarian tumors.The aim of this study is to report our experience inmanaging patients with incidental ovarian tumorsfound during RYGBP. We will review herein ourexperience with and decision-making process forboth benign and malignant ovarian tumors encoun-tered during planned RYGBP.

Methods

This study was approved by the Institutional ReviewBoard at The University of South Florida College ofMedicine and was performed in accordance withHIPAA regulations. Prospectively collected data onall patients undergoing bariatric surgery for clini-cally significant obesity from July 1998 toSeptember 2003 at our institution were reviewed.Indications for RYGBP were based on criteriaestablished by the NIH Consensus Conference in1991,1 including a BMI ≥40 kg/m2, or BMI >35kg/m2 with obesity-related co-morbidities. Patientsunderwent a standardized preoperative physical,nutritional, and psychological evaluation.

Regardless of the surgical approach, either openor laparoscopic, we routinely undertake abdominalexploration and visualization of pelvic organs. In allcases of finding an adnexal mass, intraoperativeconsultation with a gynecologist is made. The age ofthe patient, desire for child-bearing, size and natureof the mass, and the risk for malignancy are takeninto consideration. Depending on the nature of themass, a cystectomy, an oophorectomy, a total hys-terectomy with unilateral or bilateral salpingo-ophorectomy, or no intervention at all was under-taken. Laparoscopic cases were converted to open inthe case of finding a mass suspicious or verified byintraoperative frozen section as being malignant.Any decision involving resection of one or both

ovaries was explained to and consented by a familymember.

Results

From July 1998 to September 2003, we undertook460 bariatric procedures in women with clinicallysevere obesity. Fifty-two patients (11%) had a pre-vious hysterectomy and/or bilateral oophorectomyand were excluded from the study. We discovered12 previously undiagnosed adnexal masses duringabdominal exploration in 10 of the remaining 408patients (2.5%). Mean age was 40 ± 9 years, andmean BMI was 58 ± 12 kg/m2. Median tumor sizewas 11 cm (range 4-65 cm). Two of the patients hadmalignant tumors, for an overall incidental ovarianmalignancy rate in our patient population of 0.5%.Table 1 summarizes the patients' characteristics,tumor characteristics, and operative treatment.

In one patient undergoing laparoscopic RYGBP,both ovaries were significantly enlarged and had amulticystic and hyperthecotic appearance (Figure1). The patient was noted to be hirsute, with findingsconsistent with PCOS; therefore, no further resec-tional treatment was recommended.

In both patients undergoing RYGBP with ovariancysts <6 cm in diameter, the decision to remove theovary containing the cyst was made given thepatients' age and history of previous tubal ligationimplying no further wishes for child-bearing. Thedecision was discussed with and consented by theirfamilies.

A small amount of ascites was found in the cul-de-sac upon laparoscopic inspection of the abdomi-nal cavity in a postmenopausal patient with a largetumor implant of malignant characteristics locatedin the omentum. The fluid was aspirated and sub-mitted for cytological examination, and a 20-cmtumor mass was resected along with the surroundingomentum. Consent for bilateral removal of normal-appearing ovaries was obtained from her husband.

In all patients where RYGBP was completed,resection of the adnexal mass resulted in no addedmorbidity to the original operation. All patientswere counseled on intraoperative findings andreferred for follow-up by their gynecologist.

Management of Incidental Gynecological Findings

Obesity Surgery, 14, 2004 1217

Gonzalez et al

1218 Obesity Surgery, 14, 2004

Discussion

Throughout the general population, bariatricsurgery is undertaken more often in women than inmen. With the increasing prevalence of obesity indeveloped countries, the number of clinically severeobese women undergoing weight-loss surgery hasincreased exponentially over the last few years. Inaddition to many other diseases, obesity is associ-ated with increased likelihood of developing ovariantumors. Because ovarian tumors are more difficultto detect on physical examination of obese womenand because such patients are not routinely screenedfor gynecological disorders preoperatively, bariatricsurgeons may discover ovarian tumors intraopera-tively. We report our experience in managing 12incidental ovarian masses discovered in 10 patientsundergoing RYGBP in our institution. There was noadditional morbidity due to the treatment of thesetumors.

All patients were managed by surgeons and gyne-cologists according to an algorithm for the treatmentof incidental ovarian tumors described herein(Figure 2). A gynecology consult was made as soonas an ovarian tumor was discovered. The considera-tions in the treatment algorithm included whetherthe patient was premenopausal, and the appearance

and the size of the tumor mass. In premenopausalpatients, further specific intervention was consid-ered in the case of tumors suspicious of malignancyor cysts >6 cm. On the other hand, postmenopausalwomen underwent staging or cytoreduction for asuspicious tumor or cysts >3 cm. Regardless of theintraoperative management, all patients werereferred for follow-up with a gynecologist.

Table 1. Clinical characteristics, tumor information, and surgical procedure in all patients with ovarian masses discov-ered during abdominal exploration prior to performing a Roux-en-Y gastric bypass

Approach Age BMI Side Size Appearance Procedure RYGBP Final pathology(kg/m2) (cm) completed?

Open 49 79 right 4 cyst Right SO yes follicular cyst26 57 right 65 cyst Right SO yes follicular cyst37 66 left 8 cyst Left SO yes cystadenoma33 52 right 20 cyst Right SO yes cystadenoma48 61 bilateral 5 & 5 cyst Bilateral SO yes corpus

luteum cyst50 58 right 15 cyst Right SO no carcinoma

Laparoscopic 50 67 right 10 cyst Right SO yes mesothelial cyst

36 45 left 12 cyst Left SO yes follicular cyst29 46 bilateral 10 & 12 PCOS No resection yes ------------

Converted to open 51 47 left 20 hard/irregular Bilateral SO no metastatic + omentectomy adenocarcinoma

BMI = body mass index; RYGBP = Roux-en-Y gastric bypass; SO= salpingo-ophorectomy; PCOS= Polycystic ovarysyndrome

Figure 1. Large bilateral cysts (arrows) in a patient under-going laparoscopic Roux-en-Y gastric bypass. Findingswere consistent with polycystic ovarian syndrome and nofurther treatment was recommended intraoperatively.

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Obesity Surgery, 14, 2004 1219

Alteration in endogenous hormones due to excessadiposity is one proposed mechanism by which obe-sity may predispose to some types of gynecologicalmalignancies. Women with high BMI during lateadolescence may be at increased risk of infertility,which in turn has been associated with increasedrisk for ovarian cancer. In addition, weight gain dur-ing adulthood and obesity in postmenopausalwomen increase circulating endogenous estrogens.

According to a recently published study,8 womenwho were overweight or obese during adolescenceor young adulthood have an increased risk of ovar-ian cancer (relative risk [RR]= 1.56) compared tonon-obese women. This was not the case in olderobese women, who were only found to be at higherrisk of endometrial cancer. In addition, mortalityfrom ovarian cancer is higher among overweight(RR= 1.16) and obese women (RR= 1.26) comparedwith women with BMI <25 kg/m2.9 However, theuse of postmenopausal estrogens modifies the asso-ciation between BMI and mortality from ovariancancer. Two recently published studies found obe-sity and height to be independently associated withovarian cancer mortality.8,9 This was later corrobo-rated by Fairfield and colleagues,10 who found thatwomen with greater BMI at age 18 had a two-foldincrease in premenopausal ovarian cancer risk.Nevertheless, these investigators found no evidenceof an association between increase in BMI during

adulthood and ovarian cancer risk. Gynecological tumors are usually asymptomatic

and therefore difficult to diagnose until they becomequite large, especially in obese patients. Evenmalignant ovarian tumors rarely produce significantsymptoms until the disease is advanced. Bimanualpelvic examination has marked limitations for eval-uating pelvic disorders in obese patients, resultingin significant inaccuracy in palpating the adnexa.11

Transvaginal ultrasound, the best method to evalu-ate the ovaries in these women, is not routinely per-formed in patients undergoing bariatric surgery. Inaddition, many bariatric patients exceed weightrestrictions of most CT scan and MRI equipment.Therefore, although relatively infrequent, patientsundergoing bariatric surgery may present with inci-dental adnexal masses, underscoring the importanceof intraoperative abdominal exploration. Regardlessof the operative approach (open or laparoscopic)surgeons should perform an exploration of theabdominal cavity and the pelvic region to identifyany incidental findings that may require furthertreatment.

Less than 10% of ovarian masses in women <30years old are malignant compared to over 50% inwomen older than 50 years. Functional ovariancysts such as corpus luteal and follicular cysts arecaused by ovulation, and, therefore, do not occur inpostmenopausal women. When a small (<6 cm indiameter) cystic mass is encountered in pre-menopausal women, it is likely to be due to a func-tional cyst, as was the case in two of the women inthe present series. Resection of these cystic lesionsis generally unnecessary and may compromisefuture fertility. The majority of large benign cysticand solid ovarian tumors replace the gonadal tissueas they grow, and, therefore, oophorectomy is oftenindicated. Management is based on the age of thepatient, history and desire of the patient for futurechild-bearing, as well as the size and gross appear-ance of the mass. Consultation with a gynecologistcan be helpful in the assessment of these patients.

PCOS is the most common cause of anovulatoryinfertility, affecting 4% to 6% of women duringreproductive age. The PCOS is associated with obe-sity and is characterized by hyperandrogenism,anovulation leading to infertility, and menstrualirregularities. Growing evidence links this syn-drome to insulin resistance and compensatory

Figure 2. Treatment algorithm for patients with incidentalovarian masses, taking into consideration the patient, sizeand nature of the mass, and the risk for malignancy.

OVARIAN TUMOUR

Consultation with agynecologist

Suspicioustumor

orCyst >6 cm

Follow-up with agynecologist

• Cytology• Frozen section• Cystectomy/oophorectomy

Follow-up with agynecologist

Stagingor

cytoreduction

Suspicioustumor

orCyst >3 cm

Isthe patient pre-menopausal?

yes no

no no

yes yes

malignant

Gonzalez et al

1220 Obesity Surgery, 14, 2004

hyperinsulinemia. Weight loss has been shown toimprove both menstrual cycles and insulin resis-tance in women with PCOS;12 therefore, resectionmay not be necessary (i.e., to reduce hyperandro-genism) in patients undergoing RYGBP, becausemost patients will sustain considerable weight loss,with likely resolution of insulin resistance andreturn of ovulation.

Of all female genital tract tumors, ovarian carci-noma carries the worst prognosis, which is related tothe fact that it is usually diagnosed at a late stage,and is not amenable to screening.13 In contrast tocervical cancer, ovarian cancer does not have a well-defined precursor lesion, thus limiting the opportu-nity to identify early stage disease. Intraoperativefindings consistent with invasive ovarian malig-nancy include bilateral nodular ovarian masses,adherence to adjacent organs, surface excrescences,ascites, peritoneal implants, hemorrhage, and necro-sis. Sensitivity and specificity of intraoperativefrozen section are 93% and 99% for malignant ovar-ian tumors and 98% and 93% for benign tumors,respectively,14 which is higher than those of tumormarkers and preoperative ultrasound examination.15

Therefore, it is recommended to perform an intra-operative frozen section examination in patientswith ovarian tumors to rule out the possibility ofinvasive carcinoma. If clinically early invasive car-cinoma is found, careful staging is important todetermine whether adjuvant chemotherapy will beneeded. The hallmark of operative management ofadvanced ovarian cancer is cytoreduction.

The decision to proceed with bilateral salpingo-ophorectomy in premenopausal women for thetreatment of incidentally found ovarian cancershould not be taken lightly in the absence of aninformed discussion and consent by the patient. Inextreme situations, the bariatric surgeon and gyne-cologist may elect to postpone definitive resectionaltreatment for the future so that an informed consentprocess can be executed with the patient herself.

Conclusion

We recommend routine exploration of the abdomi-nal cavity of patients, especially women, duringbariatric operations. Half of the women with an inci-

dental ovarian mass have functional cysts. Such pre-menopausal women must be evaluated in light ofage, size and nature of the mass, as well as desire forfuture child-bearing. Intraoperative consultationwith a gynecologist is essential to ensure completeevaluation of gynecological disorders that generalsurgeons have become less familiar with by virtueof training and specialization. This is especiallyimportant in young women and in cases wheremalignancy is suspected, so that appropriate intra-operative staging can be done. No additional mor-bidity resulted from the added gynecological proce-dure undertaken to manage these tumors.

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(Received May 27, 2004; accepted August 16, 2004)