Ovarian cancer is a disease that requires complex surgical management. Surgery is required to make a definitive diagnosis and to determine stage and extent of adjuvant chemotherapy dosing and duration. In advanced-stage disease, surgical cytoreduction is the most critical factor affecting prognosis.1,2 Surgical specialty, surgeon volume, and hospital volume have all been associated with higher optimal cytoreduction rates.3–8 It has been shown that women with ovarian cancer who receive an initial surgical procedure by a gynecologic oncologist will have a significantly higher likelihood of receiving National Comprehensive Cancer Network guideline therapy, optimal cytoreduction, and overall survival.3–8 Unfortunately, recent studies have shown that for 30–50% of women with ovarian cancer, their surgeons are neither gynecologic oncologists nor high-volume surgeons.4,5,7,8 In one study of hospital discharge data from 10,432 admissions, 25.2% of women received surgery from providers who managed only one ovarian cancer case per year and 48.3% underwent surgery by providers who perform fewer than 10 procedures per year.5
One of the contributing factors to gynecologic oncologists not performing initial surgical management is that the diagnosis of ovarian cancer is often not diagnosed before surgery. To address this, the American College of Obstetricians and Gynecologists has published criteria for referral of women with pelvic masses at high risk for ovarian cancer to a gynecologic oncologist.9 Women considered a high risk for harboring an ovarian cancer include those with one of the following: a complex ovarian mass, ascites, elevated CA 125, fixation or nodularity of the mass or both, or evidence of distant metastasis. The current management and referral practices to gynecologic oncologists from primary care physicians and obstetrician–gynecologists (ob-gyns) in the United States is largely unknown. Our goal was to identify these referral practices and the factors associated with referral of a woman with a suspected ovarian mass to a gynecologic oncologist.
MATERIALS AND METHODS
Our study sample included 3,200 physicians aged 64 and younger practicing in office or hospital settings in the United States, with equal numbers from the primary specialties of family medicine, general internal medicine, and obstetrics and gynecology. Of these, 200 received a pilot version of our questionnaire. The remaining 3,000 received the final version of the questionnaire.
The physicians were sampled randomly from the 72,241 family physicians, 77,007 general internists, and 28,929 ob-gyns listed in the August 2008 American Medical Association (AMA) Physician Masterfile. The study was approved by the University of Washington Human Subjects Division.
We developed a 12-page mail survey booklet that examined physicians' care for women's health and posed numerous questions about physician demographics, practice characteristics, attitudes, beliefs, sources of information, and cancer experience.10 The questionnaire asked how physicians would manage a patient with an adnexal mass suspicious for ovarian cancer. The vignette featured a 57-year-old woman who complained of right lower quadrant pain and bloating for 3 weeks. A pelvic examination revealed a right adnexal mass. A pelvic ultrasound examination revealed a 10-cm right adnexal mass with solid and cystic components and increased vascularity of the solid components by Doppler. There was a moderate amount of ascites. We varied the patient's race (African American, white), and insurance (Medicaid, private). Physicians were asked to indicate their course of action in caring for the patient. Physicians were given choices and instructed to check all that applied. These choices included consult with another physician, refer for evaluation by another physician, perform surgery, observe and repeat ultrasound examination in 6 weeks, and order more tests. The respondents were asked to indicate the physician specialty to which they would refer or consult. Ob-gyns who performed surgery were asked to list the type of surgery to be performed and indicate whether another physician would be involved with the surgery (if the latter, we asked for the physician specialty).
Physicians were assigned randomly to one of the four versions of the vignette based on the four variable patient factors. To optimize response, we conducted the survey using the Total Design Method11 with modification, entailing two 2-day priority mailings, a midpoint reminder postcard or thank you note, a $20 bill with the first mailing, and an encouraging handwritten note from the principal investigator with the second mailing.
The study outcome for family medicine or internal medicine physicians revealed whether or not the physician self-reported referral to or consultation with a gynecologic oncologist. The study outcome for ob-gyns revealed whether or not they performed surgery, which factors were associated with performing surgery, and which surgical procedures were recommended. Patients' characteristics were race and insurance. These were assigned evenly to surveyed physicians.
Physician demographics included age (the survey year  minus year of birth), sex from the AMA Physician Masterfile, and race and ethnicity from the questionnaire. We used the primary physician specialty recorded on the survey. When two of the specialties of interest (family medicine, general internal medicine, obstetrics and gynecology) were recorded, we used the one that agreed with the specialty in the AMA Physician Masterfile.
Other physician characteristics included years in practice (2008 minus year graduated from medical school); involvement in clinical teaching; board certification; the average number of outpatients seen weekly; location in an urban, large rural, or small or isolated small rural area (based on Rural Urban Commuting Area codes linked by physician mailing ZIP code from the AMA Physician Masterfile)12; Census Division of physician mailing address; primary practice setting (eg, office practice, community health center); and practice type (eg, solo, group practice). We measured attitude toward risk-taking13,14 and malpractice concern15 by using modified published measures.13–15 We measured physicians' nonprofessional experience with cancer: none; experience with family or close friend or coworker only; and the physician's own cancer experience.
We used responses from both the pilot and main surveys to ensure the largest sample size. Of the 3,200 surveyed physicians, we sequentially excluded 33 duplicates, 95 undeliverable surveys, 19 retired, disabled, or deceased respondents, and 11 not practicing or on leave, resulting in 3,042 sample physicians. Of these, 1,878 (61.7%) responded. We then further excluded 200 physicians who did not provide outpatient care to women, 71 working in settings that did not provide outpatient or primary care (eg, emergency rooms), 10 that reported specialties other than the three included in this study, and 23 in residency or fellowship training. After exclusions, the overall study sample included 1,574 respondents.
We compared respondents and nonrespondents on the variables available through the AMA Masterfile and found differences in the response rate by present employment type (P=.02). Respondents and nonrespondents were distributed across the different present employment categories as follows: group practice, 69.3% compared with 63.6%; self employed 17.7% compared with 22.2%; government, 6.9% compared with 7.0%; and other, 6.1% compared with 7.2%, respectively. We found no difference in response rate by physician specialty, sex, or age.
We first described demographic, practice, and other characteristics of the internal medicine physicians, family practice physicians, and ob-gyns. We used SUDAAN 10.0 to compare physicians' unadjusted rates of self-reported recommending consultation or referral (family practice and internal medicine) or surgery (ob-gyn) by patient, physician, and practice characteristics. Multivariable logistic regression analysis identified the patient, physician, and practice characteristics that were independently and significantly associated with consultation or referral to a gynecologic oncologist for family practice and internal medicine physicians or conduction of surgery for ob-gyns at the P≤.05 level.
We first entered all patient characteristics into the regression model, and then used stepwise modeling to enter physician and practice characteristics that were significant at the P≤.05 level in the unadjusted analysis. We were able to evaluate geographic practice location at two levels (urban compared with rural) or three levels (urban compared with large rural compared with remote or small rural) and in the logistic regression used the variable with the best model fit. Because consultation or referral and conduction of surgery are common outcomes, we calculated risk ratios based on predicted marginals within SUDAAN.16
The physician and practice characteristics of the weighted respondent sample are shown in Table 1. The majority of physicians were white, and a just fewer than half were female. Almost half of physicians had been in practice for more than 20 years and approximately one quarter were in solo practice. More than 50% of family practice physicians, 34% of internal medicine physicians, and 47% of ob-gyns saw more than 90 patients per week.
When asked to indicate the next steps in management of a patient with a suspicious adnexal mass, 99% of family practice and internal medicine physicians indicated that they would refer or consult with another physician (Table 2). None of the physicians reported that they would observe and repeat the ultrasound examination and approximately 1% would only order more tests. There were significant differences in referral, consultation, or referral and consultation practices between family practice and internal medicine physicians. Referral, consultation, or both with a gynecologic oncologist was recommended by 39.3% of family practice and 51.0% of internal medicine physicians (P=.01). Of the ob-gyns, 66.3% indicated that they would refer or consult with another physician rather than conduct their own surgery, and for 96.0%, referral, consultation, or both was with a gynecologic oncologist (Table 3). Overall, 33.7% of the ob-gyn participants indicated that they would perform surgery on the patient themselves. The majority of ob-gyns who would perform surgery also indicated they would involve a gynecologic oncologist in the procedure (83.7%). The most common procedure recommended was removal of the mass and staging (if needed) in 64.4% of cases, but more than 30% of ob-gyn surgeons did not indicate that staging would be part of their surgical management (data not shown).
Table 4 shows the unadjusted patient and physician characteristics associated with referral or consultation with a gynecologic oncologist for family practice and internal medicine physicians. The only patient factor associated with referral was private insurance for family practice physicians. Physician characteristics associated with gynecologic oncology involvement for this group included age, female sex, board certification, fewer years in practice, fewer number of patients seen per week, and lower fear of malpractice. For internal medicine physicians, the significant factors were board certification, group practice, fewer number of patients, involvement in clinical teaching, and urban practice location.
Table 5 shows the unadjusted factors associated with primary surgical management by ob-gyns. The only factors significantly associated with performing surgery included geographic location and Census division.
Table 6 shows the results of the multivariable regression analysis examining factors significantly associated with family practice and internal medicine physicians who would refer to or consult with a gynecologic oncologist. Factors associated with not referring to or consulting included patients having Medicaid insurance (family practice), a weekly average number of patients more than 91 (family practice and internal medicine), male sex (family practice), a rural practice location (internal medicine), and solo practice (internal medicine).
We also evaluated the factors associated with ob-gyns who conducted primary surgical management (Table 7). The multivarible regression analysis confirmed the unadjusted findings. Physicians in small, remote, or small and remote rural practices were significantly more likely than those in urban and large rural practice locations to perform primary surgical management. Among Census divisions, Mid-Atlantic, East North Central, West South Central, and Pacific divisions all had higher primary surgery rates compared with the Mountain division.
Ovarian cancer is the most lethal of the gynecologic cancers with approximately 14,000 deaths from the disease per year.17 Overall 5-year survival rates are only 40% because the majority of women present with advanced-stage disease. Unfortunately, screening has not been shown to reduce the morbidity or mortality from ovarian cancer.18,19 Optimizing treatment, especially appropriate surgical therapy, is currently the most effective strategy for improving ovarian cancer outcomes. Despite the importance of surgical treatment, U.S. population-based studies show that up to half of women with ovarian cancer do not receive treatment from centers or surgeons who are likely to provide the best opportunity for guideline-recommended therapy.3–8 Our study suggests that national referral practices may play a role in why such a significant number of patients do not receive surgery in optimal settings.
Our study found that overall fewer than 50% of primary care physicians refer women with suspected ovarian cancer directly to gynecologic oncologists. Among primary care physicians, those in family practice were significantly less likely than internal medicine counterparts to refer to gynecologic oncologists. However, nearly all those who did not refer directly to a gynecologic oncologist referred instead to ob-gyns. As with other cancers, such as breast and colorectal cancers,20,21 we found that private insurance status was associated with recommendation for referral to specialists, in this case gynecologic oncologists, but only for the family practice physicians. Race, unlike in many other studies, was not a factor in predicting direct referral to gynecologic oncologists.22
In 2002 the American College of Obstetricians and Gynecologists published a comment opinion defining the role of the generalist ob-gyn in the early detection of ovarian cancer.9 Referral to gynecologic oncologists is recommended when women have a suspicious mass, ascites, elevated CA 125, or evidence of metastatic disease. In our study, the obstetricians and gynecologists indicated that in two thirds of cases they would refer a patient with suspected malignancy to a gynecologic oncologist. In the one third of gynecologists who perform primary surgery, 83.7% indicated that they would involve a gynecologic oncologist in the surgery. This suggests that the majority of patients should be receiving their care from a gynecologic oncologist considering that more than 94% of internists and family practitioners report referring patients with suspected ovarian cancer to either a gynecologic oncologist or an ob-gyn. However, population-based studies contradict this finding and suggest that a sizable portion of women with ovarian cancer, in fact, are not receiving surgery from surgeons or in centers that optimize their care.3–8 In addition, population-based studies suggest that approximately one third of ovarian cancer patients do not receive comprehensive surgery.5 This problem is not unique to ovarian cancer and is found with other malignancies, such as colorectal, breast, and prostate cancers.20–23
Reasons that ovarian cancer patients do not get referred on to high-volume centers or gynecologic oncologists are probably diverse. Clearly, gynecologists understand that in the setting of likely malignancy, referral to or involvement of a gynecologic oncologist is indicated, as almost all of those surveyed responded that they would include a gynecologic oncologist in some way in the care of the patient. However, several factors may deter these ob-gyns from referring to their specialist colleagues. First, patients may be reluctant to leave their communities for care. In this study, ob-gyns practicing in rural locations were significantly less likely to report including a gynecologic oncologist in the hypothetical patient's care. However, in our survey we did not inquire the proximity of the nearest gynecologic oncologist. Second, studies have shown that financial incentives can have a strong effect on the decision to perform surgery, which in turn will affect referral to an alternative physician. Patients with fee-for-service rather than capitated insurance were found to have 78% higher surgery rates.24 In another study of cataract surgery in St. Louis where capitation was introduced to a network of optometrists and ophthalmologists, the cataract surgery rate decreased by nearly 50% despite a stable physician and patient population.25
There are limitations to this study as the results are based on physician self-report and these findings do not mirror what has been found in population-based investigations of patterns of care of women with ovarian cancer.3–8 The response rate of the survey was quite good at 61.7%; however, these results may not be generalizable to the 38.3% of physicians who did not respond to the survey, although, with the exception of present employment, the respondents and nonrespondents were similar.
This study evaluates physician-reported referral patterns for women with findings suspicious for ovarian cancer. Specialty is a primary factor influencing referral to gynecologic oncologists, with two thirds of gynecologists, 51.0% of internists, and 39.3% of family practitioners reporting that they would refer directly to these specialists and an additional 84% of the remaining gynecologists reporting involvement of a gynecologic oncologist in the patient's surgery. And with more than 90% of internists and family physicians reporting referral to either an ob-gyn or a gynecologic oncologist, the majority of these patients should be receiving care from a gynecologic oncologist. Yet studies suggest that many patients do not receive this care, and there are high rates of noncomprehensive surgery and non—guideline-recommended therapy in the United States. Promoting direct referral of women with suspicious ovarian masses to gynecologic oncologists may be the best way to improve compliance with therapeutic guidelines.
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© 2011 by The American College of Obstetricians and Gynecologists. Published by Wolters Kluwer Health, Inc. All rights reserved.
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