Obstetrics & Gynecology:
Influence of the Gynecologic Oncologist on the Survival of Ovarian Cancer Patients
Chan, John K. MD1; Kapp, Daniel S. MD, PhD3; Shin, Jacob Y. BA2; Husain, Amreen MD2; Teng, Nelson N. MD, PhD2; Berek, Jonathan S. MD, MMS2; Osann, Kathryn PhD4; Leiserowitz, Gary S. MD5; Cress, Rosemary D. DrPH6; O'Malley, Cynthia PhD6
From the 1Division of Gynecologic Oncology, Department of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Francisco School of Medicine, University of California, San Francisco Comprehensive Cancer Center, San Francisco, California; 2Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, 3Division of Radiation Therapy, Department of Radiation Oncology, Stanford University School of Medicine, Stanford Cancer Center, Stanford, California; 4Division of Hematology and Oncology, Department of Medicine, Chao Family Comprehensive Cancer Center, University of California, Irvine–Medical Center, Orange, California; 5Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, University of California, Davis–Medical Center, Davis, California; and 6Northern California Cancer Center, Sacramento and Fremont, California.
The collection of cancer incidence data used in this study was supported by the California Department of Health Services as part of the statewide cancer reporting program mandated by California Health and Safety Code Section 103885; the National Cancer Institute's Surveillance, Epidemiology and End Results Program under contract N01-PC-35136 awarded to the Northern California Cancer Center, contract N01-PC-35139 awarded to the University of Southern California, and contract N02-PC-15105 awarded to the Public Health Institute; and the Centers for Disease control and Prevention's National Program of Cancer Registries, under agreement #U55/CCR921930-02 awarded to the Public Health Institute. The ideas and opinions expressed herein are those of the author(s) and endorsement by the State of California, Department of Health Services, the National Cancer Institute, and the Centers for Disease Control and Prevention or their contractors and subcontractors is not intended nor should be inferred.
Corresponding author: John K. Chan, MD, Division of Gynecologic Oncology, Department of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Francisco School of Medicine, University of California, San Francisco Comprehensive Cancer Center, 1600 Divisadero Street, Box 1702, San Francisco, CA 94143-1702; e-mail: firstname.lastname@example.org.
OBJECTIVE: To estimate the influence of gynecologic oncologists on the treatment and outcome of patients with ovarian cancer.
METHODS: Data were obtained from California Cancer Registry from 1994 to 1996. Kaplan-Meier and Cox proportional hazard methods were used for analyses.
RESULTS: Of 1,491 patients, the median age was 65 years (range: 13–100). Only 34.1% received care by gynecologic oncologists (group A) while 65.9% were treated by others (group B). Women in group A were more affluent (P<.001), were more educated (P=.036), were classified as white-collar employees (P=.128), and lived in urban regions (P<.001) compared with group B. Patients who saw gynecologic oncologists were more likely to have surgery as their initial treatment (91.9% versus 69.1%; P<.001), present with advanced (stage III-IV) cancers (78.2% versus 70.5%; P<.001), have more grade 3 tumors (61.7% versus 39.9%; P=.048), and receive chemotherapy (90.0% versus 70.1%; P<.001). Women in group B had a fourfold higher risk of having unstaged cancers (8.0% versus 2.1%; P<.001). The 5-year disease-specific survival of group A patients was 38.6% compared with 30.3% in group B (P<.001). On multivariable analysis, early stage, lower grade, and treatment by gynecologic oncologists were independent prognostic factors for improved survival. After adjusting for surgery and chemotherapy, there was no improvement in survival associated with care by gynecologic oncologists (hazard ratio=0.90, 95% confidence interval 0.78–1.03; P=.133).
CONCLUSION: In this study of 1,491 women, those who were treated by gynecologic oncologists were more likely to undergo primary staging surgery and receive chemotherapy. Stage, grade of disease, and treatment by gynecologic oncologists were important prognosticators.
LEVEL OF EVIDENCE: II
The standard treatment for patients diagnosed with an epithelial ovarian cancer involves primary surgical staging surgery, with or without adjuvant chemotherapy. The roles of primary surgery include diagnosis, staging, and tumor cytoreduction in advanced disease. Evidence-based guidelines for referring women with pelvic masses suspicious for ovarian cancers to gynecologic oncologists have been established jointly by Society of Gynecologic Oncologists and the American College of Obstetricians and Gynecologists (ACOG).1 Although these recommendations advocate referral to physicians with adequate skills for surgery and treatment, further investigations are warranted to determine the potential influence of these specialists on the survival of patients with ovarian cancer.
Prior studies have demonstrated a survival benefit for patients with ovarian cancer associated with subspecialty care.2–8 However, many of these studies have been limited by a small number of patients, lack of information on stage of disease, tumor grade, adjuvant chemotherapy, and possible selection bias reporting from single academic institutions. More importantly, the majority of studies did not provide a multivariable analysis controlling for all other important prognosticators, in particular, primary surgery, chemotherapy, or both.9 Few studies have evaluated the role of the gynecologic oncologist in ovarian cancer treatment on a population level. In a prior population-based study, women who were seen by gynecologic oncologists, compared with other specialists, were more likely to receive appropriate staging, cytoreductive surgery, and adjuvant chemotherapy.10,11 Others also stated that it was the care instituted by the gynecologic oncologists that was the most predictive factor for improved survival.7,10 However, another population-based study did not show a distinct survival advantage between those who received care from a specialist versus those who did not.5,10 These studies were limited to selected populations and did not provide detailed information on the primary surgery and chemotherapy. It is difficult to estimate the precise role of the gynecologic oncologist and the interaction between various treatment factors associated with subspecialty training. It is possible that the survival advantage may be even more profound for those who had their initial surgery and adjuvant chemotherapy administered by a subspecialist.
In this current population-based study of 1,491 patients, we estimated the independent significance of gynecologic oncologists on the treatment and outcome of women with invasive epithelial ovarian cancer using a multivariable model controlling for clinicopathologic and treatment factors including surgery and adjuvant chemotherapy. More specifically, we identified underlying treatments rendered by the gynecologic oncologists that may affect survival.
MATERIALS AND METHODS
The study population included women residing in Northern California who were diagnosed with primary invasive epithelial ovarian cancer from January 1, 1994, to December 31, 1996. The study subjects were identified within a surveillance region of 10.5 million people by using three population-based databases from the California Cancer Registry. The majority of the data were initially extracted from hospital registry information. These data were subsequently validated by death certificates, physician offices, and radiation oncology centers. All studies were approved by the Northern California Cancer Center, Public Health Institute, and State of Health and Human Services Agency. Treatment data were supplemented through physician surveys and medical reviews. The study was considered exempt by the Stanford University Research compliance office. Details on the data collection have been described in a prior report.11
Race/ethnicity was categorized into four groups: non-Hispanic White (white), non-Hispanic Black (black), non-Hispanic Asian/other (Asian), and Hispanic. Geographical regions were defined as Sacramento, rural Northern California, and a reference group of the urban San Francisco/San Jose Bay Area (SF). Census-based socioeconomic measures were assigned to each patient by linking the patient's address at the time of diagnosis with the census block group socioeconomic characteristics. Using the race-specific measures for each block group, we created dichotomous variables to classify each neighborhood as low/not low education, low/not low income, and “blue-collar”/“white collar.” These census-based socioeconomic measures are commonly employed in public health research and have been validated in prior studies in the San Francisco Bay area.12
All patients were diagnosed with invasive epithelial ovarian cancer and found to have International Federation of Gynecology and Obstetrics stage IC or higher disease. International Federation of Gynecology and Obstetrics stage was derived from procedures used by Surveillance, Epidemiology, and End Results (SEER) extent of disease. Histologic cell types were categorized into the following categories: serous, mucinous, endometrioid, clear cell, and other. Women with low malignant potential ovarian tumors, germ cell, stromal, and other non-epithelial histologies were excluded. Moreover, all patients survived at least 12 days after diagnosis and were considered candidates for adjuvant chemotherapy.
A patient was classified as having seen a gynecologic oncologist if any of her physicians were members of the Society of Gynecologic Oncology. Because chemotherapy is typically given in an outpatient setting, registry treatment data were supplemented with data from a physician survey and medical record review. Chemotherapy was dichotomized as yes/no. Follow-up data, including the date and cause of death or censoring, were obtained through linkage with Vital Statistics.10
Survival time was measured in months from the time of diagnosis until death or censoring. The outcome variable was death from ovarian cancer; deaths from other or unknown causes were censored at the time of death. Pearson's χ2 test was used to evaluate associations between factors and risk of death. Survival analyses and predictors of outcome were analyzed using Kaplan-Meier and Cox proportional hazard methods. Statistical analyses were performed using SPSS 14.0 (SPSS, Inc., Chicago, IL).
Patient demographics of 1,491 women with epithelial ovarian cancer included in the study are shown in Table 1. The median age at diagnosis was 65 years (range 13 to 100 years). One thousand one hundred seventy-two women were white (78.6%), 128 (8.6%) Hispanic, 111 (7.4%) Asian, and 67 (4.5%) were black. There were 786 (52.7%) women classified as affluent and 705 (47.3%) women as nonaffluent. One thousand one hundred eleven (74.5%) patients were classified to be more educated while 380 (25.5%) were less educated. Nine hundred thirty-three (62.6%) were white-collar compared with 558 (37.4%) blue-collar workers. Two hundred eighty-six (19.2%) patients were from the San Francisco region, 368 (24.7%) from Sacramento, 268 (18.0%) from rural northern California, and 569 (38.2%) from the Santa Clara region. During the study, from 1994 to 1996, there has been an increase in the proportion of patients treated by gynecologic oncologists (27.9% to 35.6%; P<.001). One hundred forty-three (9.6%) were stage IC, 168 (11.3%) stage II, 669 (44.9%) stage III, 421 (28.2%) stage IV, and 90 (6.0%) were unstaged. There were 80 (5.4%) patients with grade 1 disease, 248 (16.6%) with grade 2, 706 (47.3%) grade 3, and 457 (30.7%) women with unknown grade of disease. Detailed clinicopathologic information is provided in Table 2.
The study group was dichotomized based on treatment by gynecologic oncologists. Only 34.1% received care by gynecologic oncologists (group A) while 65.9% were treated by others (group B). The median age of patients in group A was 62 years compared with 68 years in group B. Women in group A were found to reside in more affluent (60.9% versus 48.5%; P<.001), more educated (77.8% versus 72.8%; P=.036), white-collar (65.2% versus 61.2%; P=.128) and urban neighborhoods (88.4% versus 78.7%; P<.001) compared with group B. Furthermore, more patients in group A than group B underwent primary surgery (91.9% versus 69.1%; P<.001), presented with advanced (stage III-IV) cancers (78.2% versus 70.5%; P<.001), had grade 3 tumors (61.7% versus 39.9%; P=.048), and were more likely to receive chemotherapy (90.0% versus 70.1%; P<.001) (Table 2). Women in group B had a fourfold higher risk of having unstaged cancers (8.0% versus 2.1%; P<.001).
The 5-year disease-specific survivals of the entire study based on age, race, socioeconomic factors, region, and year of diagnosis are shown in Table 3. The 5-year disease-specific survival of patients with stage IC, II, III, and IV was 71.0%, 55.8%, 32.9%, and 14.3%, respectively (P<.001) (Table 4, Fig. 1). Women with grades 1, 2, and 3 disease had 5-year disease-specific survivals of 67.0%, 46.6%, and 33.0%, respectively (P<.001). Patients who underwent primary surgery had an improved survival compared with those who did not undergo primary surgery (40.6% versus 7.4%; P<.001). Furthermore, chemotherapy treatment was also associated with an improved survival in the overall study group (36.4% versus 22.1%; P<.001) (Table 4).
The survival of patients who were seen by a gynecologic oncologist (group A) was 38.6% compared with 30.3% in those who did not receive care by a gynecologic oncologist (group B) (P<.001) (Fig. 2). This survival advantage of group A patients was most notable in those with stage III-IV disease (31.0% versus 22.5%; P<.001) with a nonsignificant survival improvement in early-stage disease (66.3% versus 61.1%; P=.157) (Fig. 2B and C). Furthermore, grade 3 patients in group A showed an improved survival compared with those in group B (37.1% versus 29.6%; P=.005). Care from a gynecologic oncologist was also associated with an improved survival after adjusting for year of diagnosis and socioeconomic factors including income, level of education, and occupation (Table 3).
On multivariable analysis, younger age, early stage, lower grade, and treatment by gynecologic oncologists were found to be significant prognostic factors for improved survival. (Table 5). In view of the relationship between care by a gynecologic oncologist and use of primary surgery and chemotherapy, we performed an additional multivariable model accounting for these factors. After adjusting for primary surgery and chemotherapy, there remains a nonstatistically significant improvement in survival associated with care by gynecologic oncologists (hazard ratio=0.90, 95% confidence interval [CI] 0.78–1.03; P=.133) (Table 6). An additional multivariable analysis was performed to determine factors associated with receiving chemotherapy. Controlling for factors such as age, stage, and grade of disease, treatment by a gynecologic oncologist was significantly associated with patients receiving chemotherapy (odds ratio 2.35, 95% CI 1.67–3.32). Similarly, a multivariable analysis controlling for age, stage, and grade of disease revealed that treatment by a gynecologic oncologist was significantly associated with the patient undergoing surgery (odds ratio 2.38, 95% CI 1.60–3.54). In fact, the patients who did not undergo primary surgery by a gynecologist and did not receive chemotherapy had a 5-year disease-specific survival of only 7.1% in contrast to 41.0% in those who received multimodality treatment under the care of gynecologic oncologists (P<.001).
Although most retrospective studies2,7,13–16 have demonstrated a survival benefit associated with ovarian cancer surgery performed by gynecologic oncologists, some have not shown that treatment by gynecologic oncologists is an independent prognostic factor for improved survival.10 In this current study, our objective was to determine the potential survival benefits for patients with ovarian cancer treated by gynecologic oncologists adjusted for clinicopathologic and treatment factors. In this population-based study, we proposed to identify those specific treatments rendered by the gynecologic oncologists that lead to the improved outcome.
Our data suggest that patients who saw a gynecologic oncologist underwent more primary surgery for their cancer (91.9% versus 69.1%; P<.001). Of the 509 patients cared for by gynecologic oncologists in our study, 97.9% of the patients had staging information. On the other hand, those who did not receive care by a gynecologic oncologist had a fourfold higher risk of being unstaged. Furthermore, of the patients who had staging information, the proportion of patients with advanced-stage disease treated by a gynecologic oncologist was 78.2% compared with only 70.5% in those treated by others (P<.001). Previously reported studies have demonstrated that surgery under the care of a gynecologic oncology specialist resulted in more complete staging and tumor debulking.2,5,7,8,15,16,18–22 In summary, surgery performed by gynecologic oncologists: 1) decreased recurrence rate and improved survival in early-stage cancers after comprehensive staging surgeries,3,22,23 and 2) improved the median survival associated with increased rates of optimal cytoreduction in advanced disease.9,15,18,24,25 Despite the bias that gynecologic oncologist–treated patients with more advanced-stage and higher-grade cancers, these high-risk patients had a better disease-specific survival. Furthermore, there may be a bias in which patients with more serious comorbidities are referred to tertiary care centers with gynecologic oncologists while the healthier women remain in the community hospitals.
Given that a large number of patients with high-risk disease treated by non–gynecologic oncologists did not receive chemotherapy, our data suggests that some physicians without subspecialty training in ovarian cancer may not appreciate the risk of recurrence and failure in this aggressive cancer. We found that a significantly higher proportion of patients underwent chemotherapy in the group treated by a gynecologic oncologist (90.0% versus 70.1%; P<.001). A recent study by O'Malley et al10 found that more than 20% of young (less than 55 years) patients with high-risk early-stage ovarian cancer did not receive appropriate chemotherapy according to standard treatment guidelines. These authors also found that those who visited gynecologic oncologists were more likely to receive chemotherapy. In this current analysis, patients who received chemotherapy and saw a gynecologic oncologist had a 5-year disease-free survival rate of 39.1% compared with 34.7% in those who received chemotherapy and did not have treatment by a gynecologic oncologist (P<.001) (Table 4).
Of note, our multivariable analysis showed a survival benefit associated with gynecologic oncologist care after adjusting for age, stage, and grade of disease (Table 5). These findings may be explained by the fact that the gynecologic oncologists significantly impacted the outcomes of patients with ovarian cancer by using aggressive treatments including debulking surgery and adjuvant chemotherapy. Thus, after accounting for these specific treatments rendered by the gynecologic oncologist, such as primary surgery, comprehensive staging, cytoreductive operations, and recommendation for adjuvant chemotherapy, the effect of the gynecologic oncologist loses significance in the second multivariable model (Table 6), suggesting that the influence of the gynecologic oncologist is partially accounted for by surgery and chemotherapy. Previous studies that have adjusted for these prognostic variables have also shown a residual survival benefit when patients are referred to gynecologic oncologists.18,26 It is possible that the gynecologic oncologist's understanding of the biology and natural history of this cancer may ultimately result in management recommendations that impact the survival and quality of care in patients with ovarian cancer.
The strengths of our study include the large number of patients representative of the general population from multiple academic and community institutions. The collection of data from various hospitals and large number of physicians with different training enables us to better evaluate the significance of subspecialty training on the outcome of patients with ovarian cancer. To supplement the registry data on treatment, questionnaires were sent to the patients' attending physician to ask whether the patient received chemotherapy. In this analysis, our multivariate model accounts for potential confounders such as demographic, clinicopathologic, and treatment information such as race, socioeconomic background, surgical staging, and adjuvant chemotherapy data. However, our study was limited by the lack of information on the comprehensive surgical staging, extent of cytoreductive surgery, residual disease after primary surgery, perioperative morbidities associated with aggressive surgery, and the rate of loss to follow-up. However, others have shown that the presence or absence of gynecologic oncologists intraoperatively was the most significant covariate for the probability of attaining optimal cytoreduction and the aggressive surgical approach was associated with more periopertaive morbidities.2 Others have not found an increase in morbidity despite more extensive surgery including intestinal anastomosis, urologic procedures, and lymphadenectomy to increase cytoreduction for advanced disease.27,28 In addition, we do not have detailed information on the specific type and number of cycles of chemotherapy, and the physician specialist who administered the chemotherapy.
In this large population-based study, our initial multivariate model showed that consultation by a gynecologic oncologist was associated an improved disease-specific survival. More specifically, these patients were more likely to undergo primary surgery with appropriate staging and receive chemotherapy. After accounting for standard treatments, there was no improvement in survival associated with subspecialist care. The thorough understanding of the natural progression of this aggressive cancer by a subspecialty trained physician may ultimately impact the outcome of these patients. Future studies are warranted to identify specific gynecologic oncologists and/or centers of excellence whose patients have particularly good outcomes. Through these analyses, useful strategies for outcome improvement may be defined.
In summary, our study showed that the combination of primary surgery and chemotherapy positively influences survival in patients with ovarian cancer. Moreover, gynecologic oncologists are more likely to provide this care. Although there has been a trend toward an increase in referral to gynecologic oncologists during the study period, only a minority of women received treatment by gynecologic oncologists in this population-based analysis. Additional studies are required to identify the reasons for this lack of referral which may include impediments such as poor access to care, inaccurate preoperative evaluation, lack of knowledge about standard treatments and survival advantages provided by the subspecialists. Therefore, further patient and physician education are needed to assure that patients with ovarian cancer are appropriately referred to subspecialists to achieve high-quality comprehensive care for this aggressive cancer. With an increased emphasis on evidence-based guidelines and enhanced awareness of these recommendations, we hope that the clinical management of ovarian cancer will change and the outcomes of patients ovarian cancer will improve.
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