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Research

ONCOLOGY

www. AJOG.org

The risk of diagnostic hysteroscopy in women with endometrial cancer
Jennifer E. Soucie, MD, MSc; Pamela A. Chu, MD, MBA; Sue Ross, PhD; Tom Snodgrass, BSc (Hons); Stephen L. Wood, MD, MSc
OBJECTIVE : We sought to evaluate whether hysteroscopy in patients

with endometrial cancer had an effect on disease stage or mortality.
STUDY DESIGN: This was a retrospective cohort analysis of data linked

group (P ϭ .38). There was also no difference in death rates, 13.2% vs 15.2% (P ϭ .25), or in the proportion of women dying of female genital organ cancer, 46.1% vs 42.1% (P ϭ .53), respectively.
CONCLUSION: Hysteroscopy is not associated with a higher rate of

between a registry of women diagnosed with endometrial cancer and physician billing data on hysteroscopy.
RESULTS: A 99.8% match rate was obtained. Eighty-five percent of

cases had complete data on staging. Of these 1972 cases, 672 (34.1%) had undergone hysteroscopy. There was no difference in stage III disease between the hysteroscopy (7.1%) vs no hysteroscopy (6.5%)

stage III disease or mortality. It allows for accurate diagnosis with direct visualization and biopsy, and should be considered a safe diagnostic tool. Key words: endometrial cancer, hysteroscopy, mortality, stage

Cite this article as: Soucie JE, Chu PA, Ross S, et al. The risk of diagnostic hysteroscopy in women with endometrial cancer. Am J Obstet Gynecol 2012;207:71.e1-5.

ysteroscopy is widely used for the diagnosis of endometrial hyperplasia or carcinoma. The sensitivity has been estimated to be 86.4%.1 In comparison, Pipelle endometrial biopsies have been reported to have a sensitivity of 6783.5%.2,3 It has also been shown that hysteroscopically guided curettage has higher accuracy than dilatation and curettage (D&C) alone.4 However, concern exists that the introduction of high-pressure gas or fluid into the uterine cavity, to produce distension, could facilitate the dissemination of malignant cells in

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patients with endometrial cancer. It has been found that the distention medium can begin draining transcervically and transtubally when pressures reach approximately 100-150 mm Hg. Thus, in the patient with endometrial cancer, there is the theoretical possibility that malignant cells might be dispersed into the fallopian tubes and the abdominal cavity following hysteroscopy.5 The evidence associating peritoneal dissemination with hysteroscopy and ultimately its possible effect on endometrial cancer mortality outcomes is inconclusive.6-16

This study was undertaken to evaluate whether preoperative hysteroscopy performed in patients with endometrial cancer had an effect on subsequent surgical staging, and ultimately mortality. It is a retrospective cohort analysis of data on women who had been diagnosed with endometrial cancer over a period of 10 years (1997 through 2006).

M ATERIALS AND M ETHODS
Sources of data for this study were the Alberta Cancer Registry and physician billing data from Alberta Health and Wellness. The Alberta Cancer Registry captures data on all patients diagnosed with a cancer that is identified by the International Classification for Diseases for Oncology. Data on women with endometrial cancer were retrieved from the registry from Jan. 1, 1997, through Dec. 31, 2006. This start time was chosen principally because the Alberta Cancer Registry had undergone a number of coding changes prior to this time period. It was not until 1997 that endometrioid adenocarcinoma was differentiated from other more aggressive nonadenocarcinoma histologic types, such as, clear cell and papillary serous. A second benefit to this time period was the introduction of new staging criteria for endometrial cancer 71.e1

From the Departments of Obstetrics and Gynecology (Drs Soucie, Chu, Ross, and Wood), Community Health Sciences (Drs Ross and Wood), and Family Medicine (Dr Ross), Faculty of Medicine, University of Calgary, and Cancer Care-Alberta Health Services (Mr Snodgrass), Calgary, Alberta, Canada. Received Jan. 28, 2012; revised March 21, 2012; accepted April 25, 2012. Supported by McClure Memorial Cancer Endowment, University of Calgary (J.E.S.). This study is based in part on data provided by Alberta Health and Wellness. The interpretation and conclusions contained herein are those of the researchers and do not necessarily represent the views of the Government of Alberta. Neither the government nor Alberta Health and Wellness expresses any opinion in relation to this study. The authors report no conflict of interest. Presented at the 40th Global Congress of Minimally Invasive Gynecology, American Association of Gynecologic Laparoscopists, Hollywood, FL, Nov. 6-10, 2011, and the 40th annual meeting, Association of Academic Professionals in Obstetrics and Gynecology of Canada, Toronto, Ontario, Canada, Dec. 2-4, 2011. Reprints not available from the authors.
0002-9378/$36.00 • © 2012 Mosby, Inc. All rights reserved. • http://dx.doi.org/10.1016/j.ajog.2012.04.026

JULY 2012 American Journal of Obstetrics & Gynecology

it was cal- www. since diagnosis with an endometrial sample may not have been required. This process did not compromise patient confidentiality as only anonymous data were received by the research team. and all identifying information was removed from the linked dataset before release for analysis.17 Alberta Health and Wellness administers a universal health care plan that covers all Albertans. The cases from the cancer registry were then linked to the Alberta Health and Wellness dataset. Bivariate analyses were performed to compare the hysteroscopy groups in regard to staging and other possible prognostic risk factors. American Journal of Obstetrics & Gynecology JULY 2012 . while 5 had staging complicated by coexistent cancer. In Alberta. The majority of cases would have also included pelvic lymph node sampling. and/or undifferentiated carcinoma.17 A thorough review of this dataset was then performed to eliminate transcription errors and to clarify staging. If peritoneal dissemination via the fallopian tubes occurs during hysteroscopy. When hysteroscopy was not performed. crossreference to other variables (ie. Staging ՆIIIa would indicate that the carcinoma had extended out of the uterus. would be needed to detect a difference in staging with a power of 80% and an alpha error of 0. Approximately 85% of these cases had complete and appropriate data on staging (350 were missing staging completely. However.05 was considered to be statistically significant. and both mean and median for continuous variables. Information on whether a diagnostic hysteroscopy was performed for each patient was abstracted. rather than the diagnostic technique used. there is a link made annually with the Canadian National Mortality database.org culated that a sample size of 387 and 581 women who have and have not undergone hysteroscopy. These numbers were easily attained from the provincial registries. Of these 1972 cases with complete staging. Data were summarized using proportions for categorical variables. Comparisons were made using Pearson ␹2 test for categorical variables. Cases were selected from the Alberta Cancer Registry based on the diagnosis of endometrial cancer as defined by a positive biopsy. any staging based on the American Joint Committee’s Cancer TNM staging manual (fifth and sixth editions) was translated to the FIGO 1989 staging criteria.17 Besides diagnosis.Research Oncology diagnoses would have been made by either office endometrial biopsy or D&C. A 99. This would represent hysteroscopy that had been performed within 1 year. Data linkage went back as far as January 1996.05. a different type of cancer. such as squamous. as each month linkage is made to Alberta Vital Statistics to identify those cancer patients who have died and the cause of death. that took place in 1989. as disease may have been more clinically apparent at presentation. P Յ .e2 R ESULTS The initial data request from the Alberta Cancer Board had provided 2331 cases that met both inclusion and exclusion criteria. this would have affected our analysis by disproportionably decreasing the survival for women who had not had hysteroscopy. Data were managed according to the Alberta Privacy Legislation. the Alberta Cancer Registry provided further information on pathology (histologic cell type and staging) and vital statistics. 672 (34. Ethical approval was obtained from the Conjoint Health Research Ethics Board at the University of Calgary (Ethics Review Board no: E-20934). There was an increase in the utilization of hysteroscopy over the study period. the Wilcoxon rank sum test was used. patients who die outside Canada could be potentially missed. For the few cases missing node sampling. The Alberta Health and Wellness dataset provided information on diagnostic hysteroscopy (specifically by fee code 80. text entered by the physician) in the wider electronic database allowed for clarification in many cases. In addition. or a benign condition). staging should indicate at least stage III. Therefore. the study hypothesis was that hysteroscopy would be associated with an increased frequency of stage III disease and endometrial cancer–related deaths. Staging was reported by the treating physician. Staging after that change included surgical observations. Review of the literature suggested that 10% of those women with endometrial cancer who undergo hysteroscopy for diagnostic purposes and 5% of those who do not undergo hysteroscopy will have stage III disease. the performance of pelvic washings alone would have dictated the classification of stage IIIa disease based on the International Federation of Gynecology and Obstetrics (FIGO) 1989 staging criteria. isolating that which was used for the diagnosis of endometrial cancer.12 From this. and through this.81) and patient characteristics (age). pelvic washings are considered the standard of care. physicians are reimbursed for all procedures performed in the province. There were 2 primary outcomes in this study: staging and overall survival. NC). to include information on cases that were pulled from the Alberta Cancer Registry for the year of 1997. papillary serous. Cases were also excluded if histology indicated a nonadenocarcinoma type of cancer. This eliminated advanced disease that was likely due to the inherent disease process of a more aggressive tumor type. Loss to follow-up within the Alberta Cancer Registry is minimal.1%) had undergone hysteroscopy. Data linkage between Alberta’s Cancer Registry and the Health and Wellness dataset was performed by Alberta Health and Wellness. otherwise. respectively. Cary. Mantel-Haenszel ␹2 test was used to identify trends in proportions.8% match rate was obtained when linkage was performed with the Alberta Health and Wellness claims data. Women with stage IV disease were excluded. As the survival in this group is also close to 0. Finally. clear cell. This code would have captured hysteroscopy performed in both the office setting and operating room. When staging information within the dataset was missing or not interpretable.AJOG. 71. A Student t test was used to compare continuous variables if they were normally distributed. Data linkage was performed using at least 2 patient-specific variables within each dataset. All statistical calculations were performed using the SAS program package (SAS Institute.

...02– 6............. 95% CI............................... Am J Obstet Gynecol 2012................................ confidence interval.........10 .........................www............................................................................................................................................................... 1............................ 1 (0....................................................................................... FIGO IIb ...........87.......5) Stage Stage ϽIII Stage III Statistical test ...... (%) 1103 (84........................................ 1...................................2%) compared to those who had not (15............................69–1................ P ϭ ................ Additionally..................................................................................................................... 95% CI..............10).............................................................................................................................................................. Oncology Research TABLE 1 Stage of disease by hysteroscopy Hysteroscopy Yes n ‫ ؍‬672 No.........................02-10..............................................38)..................2% vs 2...................87................................AJOG..........................org and in the number of cases diagnosed.................................... 0............................................. relative risk.......................25) (Table 2).... Soucie................................ JULY 2012 American Journal of Obstetrics & Gynecology 71.......8) 182 (27....................................0 (0... 0.................. 0......................... FIGO IIIb .............. RR.....2) Statistical test ........ 0............. In all.......................................... 1......................... CI.....38 RR.................. Soucie..................5) 26 (3..................................................... The mean age was 62....................... 95% CI............. Risk of hysteroscopy in endometrial cancer......3) 1 (0.................01)........8 Their group performed a multicenter.................................2) No n ‫ ؍‬1300 No.......................... nor in the proportion of women dying of female genital organ cancer between hysteroscopy groups (P ϭ .......................... ␹2 P ϭ ........................................6) FIGO Ia FIGO Ic FIGO II .........8) 89 (13........................................................................................ (%) 583 (86.................................5%.....................1) No n ‫ ؍‬1300 No....................................62 Details of FIGO stage FIGO 0 FIGO I ................ The first of the reports providing evidence against hysteroscopy was by Obermair et al........................97) and 4............................................................................................................. retrospective cohort analysis of 113 consecutive patients with endometrial cancer limited to the inner half of the myometrium..... 2..................6) 21 (3......6. 95% CI.........................2) 265 (20.......................................................... Substaging was not available..... ␹2 P ϭ ....3) 49 (7.......... International Federation of Gynecology and Obstetrics........... a ....4) CI................................ whereas 52 were diagnosed with hysteroscopy.......10.......25 RR..039............. C OMMENT Our results indicate that hysteroscopy in patients with endometrial cancer is not associated with a higher rate of subsequent stage III disease............................................ resulting in high censor rate in the analysis..2) FIGO Ib .. Previous studies have published conflicting results about the effect of hysteroscopy on peritoneal dissemination of malignant cells and upstaging of disease in women who have endometrial cancer........... FIGO IIa FIGO III ...e3 ............................. 95% confidence interval [CI].........53) (Table 3)...................2%) (relative risk............ Risk of hysteroscopy in endometrial cancer................. relative risk............................ When evaluating only those women who had died........................................................ 0..8) 197 (15........................3) 2 (0.........................................................9%).................................................4) 201 (15.................................. P ϭ ........................................................................................................................................................... 5 (0............... Am J Obstet Gynecol 2012................................... In 1997............... P ϭ ................ There was also no statistically significant difference found in death rates for those who had a hysteroscopy (13.. in 2006. The mean years of follow-up for each group were 4...............................16.........................1) 3 (0..... who underwent D&C either with or without prior diagnostic hysteroscopy............................7 years................. P ϭ .......................................................... com- Vital statistics by hysteroscopy Hysteroscopy Vital statistics Alive Dead Yes n ‫ ؍‬672 No...... (%) 621 (92..... 204 cases were diagnosed by endometrial biopsy or D&C.................................5) 85 (6......................2) 67 (10..........................................................................16.............................................9) 113 (8.........1) 116 (17........ ......... 133 (19...........2) 3 (0............................................................................................ ......0%)..04)....0) 112 (8.................................. 40 hysteroscopies were performed in 154 women who were diagnosed with endometrial cancer (26..... 0.................... Bradley et al15 reviewed 256 charts of women with endometrial cancer.9) 51 (7.......................... (%) 1215 (93....... there was no statistical difference in stage III disease between hysteroscopy groups... A nonsignificant lower proportion of patients (6.............4 (0...... They found that the only factor significantly associated with positive peritoneal cytology was a history of hysteroscopy (12... .........8) FIGO IIIa FIGO IIIc a ................67)........... Zerbe et al6 reviewed the charts of 222 patients with endometrial cancer and evaluated the peritoneal dissemination TABLE 2 of malignant cells during hysteroscopy.....2) 23 (1......... P ϭ ...........9%) had malignant or suspicious cytology in the endometrial biopsy or D&C group...........................................63.........5) 55 (4.........5) 19 (1....... 71 (10................................ They found a difference in positive peritoneal cytology in those who had hysteroscopy vs those who had not (odds ratio.............................. for women who had undergone hysteroscopy and those who had not (Wilcoxon rank sum....05)............ 95 hysteroscopies were performed in 232 women (40.......... RR.. whereas.............. ............................83–1..............62.............. a .. a ............................................................ among those who had died...................... confidence interval............................ statistically significant differences were found neither in the proportion of stage III disease (P ϭ .......................................... respectively.............0 and 60...2) 3 (0............................. respectively. FIGO.......................4) 447 (34............................................83–1....69 –1...... The frequencies of FIGO stages in the 2 groups are shown in Table 1.. Survival analysis was not possible because of the relatively fewer numbers of deaths................ The rates of stage III disease did not differ statistically between those who had and did not have hysteroscopy (relative risk.......... There was no statistical difference in death rates between hysteroscopy groups............................................................................7) 54 (4.........

...... clear cell.. and examined whether the number of hysteroscopies and the time interval between hysteroscopy and surgery had an effect on cytology............ they found suspicious or positive peritoneal cytology was present in 1. the cause of death from female genital organ Staging and cause of death by hysteroscopy among women who died Hysteroscopy Staging Stage ϽIII Stage III Yes n ‫ ؍‬89 No..........................3) 27 (13..0%)....... thus comparison could not be made.. Cause of death ......... Kudela and Pilka10 prospectively reviewed 134 women diagnosed with hysteroscopy and 61 diagnosed with D&C............................. a metaanalysis indicated that hysteroscopy is associated with a small risk of peritoneal spread.....5% (3/24) after hysteroscopy (P Ͻ ...... higher disease upstaging..............5%).......... however................................9% (2/ 104) and 7............ and not including the 2 randomized controlled trials...... Evidence in support of the use of hysteroscopy has also been published....... Sainz American Journal of Obstetrics & Gynecology JULY 2012 .......................... Peritoneal cytology was positive in 9 patients............ again 17 had abnormal peritoneal washings (9...... pared to the hysteroscopy group (13.... This difference was not statistically significant...... the small sample size only allowed for a statistical power of Ͻ20%...... with a cohort spanning over 10 years....1) 41 (46.................18 The sample sizes of the studies to date have been small to moderate with limited follow-up intervals to adequately evaluate survival differences.... However......64)..............6% (2/122) after D&C and 12................7) ␹2 P value ...07). and 39 had only hysteroscopy.....3%)........ There was no difference in peritoneal cytology between those who had hysteroscopy (5....................................... respectively (P ϭ . Risk of hysteroscopy in endometrial cancer....0) 62 (31....03)............................ Soucie........................... it suggests that hysteroscopy does not impose a significant risk of dissemination..... Most importantly..................... and 21 had microscopic intraperitoneal dissemination. Am J Obstet Gynecol 2012. Gu et al9 found that of 23 patients who were diagnosed by D&C with hysteroscopy....................... Median follow-up was 34 months........ uterine curettage (49....... .... P ϭ ......................................5%) (P ϭ ...................... and more specifically...........3) No n ‫ ؍‬197 No....008)....... Juhasz-Boss et al14 took this factor into consideration in their analysis..................................6................... Primary unknown death cause not coded 15 (7................... The rate of positive cytology was 18.......15).......16 In their review of 146 women with endometrial cancer diagnosed with either D&C or office hysteroscopy............................... However... The results indicate clearly that hysteroscopy is not associated with higher staging of endometrial cancer................... poor histologic types.......1% (5/70) for those with 1 and 2 hysteroscopies.. There were 3 patients (10%) with positive washings in the hysteroscopic group compared to 1 (5%) among the controls (P ϭ ....................... In this series.. it is evident that there is no firm conclusion as to whether hysteroscopy leads to peritoneal dissemination of malignant cells in women who have endometrial cancer...................................................... Ben-Arie et al11 reported on a cohort of 392 women diagnosed with endometrial cancer with endometrial biopsy (25... a Noncancer death cause Other cancer a 2 ................... Similarly.......... The final study providing evidence against the use of hysteroscopy was performed by Takac and Zegura.....................5) 83 (42.................... Selvaggi et al7 evaluated patients with endometrial cancer and found that 52 had a diagnosis made only by D&C...... overall survival and disease-free survival were not significantly different for the 2 groups............................ 25 (28....AJOG....5%).88 (95% CI.....................................11–13................... Patients were randomized 3:2 to have or not to have fluid hysteroscopy biopsy performed just prior to surgery.7) 19 (21................. 56 underwent D&C and then hysteroscopy....... and small cell cancer were included in the analysis....................................... and by direct extension..................... they note that greater numbers are needed to clarify the effect on prognosis................ When sentinel lymph node biopsy 71... positive cytology was not related to the time interval between preoperative hysteroscopy and definitive surgery.............. 17 had abnormal peritoneal washings (13..Research TABLE 3 Oncology www..................... There have been 2 randomized controlled trials evaluating the effects of hysteroscopy on peritoneal cytology........................org de la Cuesta et al12 examined 50 consecutive patients with endometrial cancer... Of 177 patients diagnosed by either endometrial biopsy or D&C without hysteroscopy..... neither was significantly associated with hysteroscopy (P ϭ ............. a second hysteroscopy is necessary for technetium injection......2% (4/22) in those without hysteroscopy vs 1............................. and all patients but 1 (deceased due to unrelated cause) were alive with no evidence of disease............................ From this...... Peritoneal cytology was positive in only 1 case......e4 is performed..... compared to 33.. Prior to this publication..... The rates were not different statistically.. and hysteroscopy (25..........7%) vs those who did not (8....9) 8 (9........05)..........................2%). 1...... Positive or suspect cytology in fluid from lavage was present in 30... ␹ comparing “female genital organ” cancer vs all other causes of death........ ...........9% in those who underwent a D&C...................... Both groups were comparable for stages of disease...... no statistic difference in the survival rate was found between diagnostic methods..................... including serous papillary....... However......... From the literature.... Cicinelli et al13 randomized 140 women to undergo or not undergo diagnostic fluid minihysteroscopy before surgical staging.............................8) ..3% for those with hysteroscopy................. the odds ratio for positive cytology after hysteroscopy was 3...... (%) 70 (78........ Furthermore........... The authors concluded that fluid hysteroscopy and directed biopsies may have a small risk of upstaging early endometrial cancer but does not seem to influence prognosis................................................... After a mean duration of follow-up of 62 months...........6%)..10 ..... Juhasz-Boss et al14 took a novel approach to evaluating the effects of hysteroscopy.....6) ......................... Our study provides more information as it included a large sample..............................1) 15 (16..... after controlling for stage and grade.......... there was no difference in death rates....1) 37 (18.................................................53 Female genital organ cancer ............................ (%) 170 (86..........................................................

90:143-7.33:76-8. Lewin SN. It should also be noted that FIGO did replace their staging criteria in 2009. as the information was not available in either of the electronic databases. Rulin MC. Granizo JJ. Corpus cancer staging. some degree of reporting bias may be evident. Every effort was made to ascertain missing data from the larger database when available. Revised FIGO staging system for endometrial cancer. 18. Krestan C. JAMA 2002. Song F. However. Does hysteroscopy facilitate tumor cell dissemination? Incidence of peritoneal cytology from patients with early stage endometrial carcinoma Oncology Research following dilatation and curettage (D & C) versus hysteroscopy and D & C.79:55-8. disease stage was evaluated. Thaler HT. Zegura B. Tamir S. Wren B. Gynecol Oncol 2000.28:190. Number of hysteroscopies and the time interval between hysteroscopy and surgery: influence on peritoneal cytology in patients with endometrial cancer. 16. Kurz C. 15.63:143-4. Aust N Z J Obstet Gynecol 1993. Clark TJ. et al. all staging in this cohort was based on the previous criteria. 11. Pilka R. Menopause 2010. JULY 2012 American Journal of Obstetrics & Gynecology 71. Instead. 14. 10. Gucer F.20:261-7. Hysteroscopy and cytology in endometrial cancer. Is there a real risk in patients with endometrial carcinoma undergoing diagnostic hysteroscopy (HSC)? Eur J Gynaecol Oncol 2001. et al.AJOG. Kudela M.152:220-9. Cormio G. Abdominal dissemination of malignant cells with hysteroscopy. Gynecol Oncol 1996. Guido RS. this is unlikely and thus. 7. 5. which allows for direct visualization and directed biopsy. namely reporting and selection bias. Goldrath MH. Egarter C. Voit D. 9. Int J Gynecol Cancer 2009. 3. Retrograde seeding of malignant cells during hysteroscopy in presumed early endometrial cancer. Sainz de la Cuesta R. Colafiglio G. Christopherson WA. Crespo E. Efficacy of the Pipelle endometrial biopsy in detecting endometrial cancer. et al. Rivas F. Fehm T. J Reprod Med 1995. 54:215-8. Farnsworth A. Shi W. Hysteroscopy does not increase the risk of microscopic extrauterine spread in endometrial carcinoma. Loverro G.88: 139-43. should be considered a safe diagnostic tool in women suspected of having enf dometrial cancer. 12. It would be impossible to know whether there were differences in reporting for those who had hysteroscopy vs those who had not. To retrieve this information. Webster M. and thus peritoneal cytology would have been captured by this older classification system. Montz FJ. Takac I. Zerbe MJ. Cancer 2000. Messini CI.13:223-7. however. individual patient charts at each regional health authority would have to have been reviewed. Cazzolla A. Office hysteroscopy and suction curettage: can we eliminate the hospital diagnostic dilatation and curettage? Am J Obstet Gynecol 1985. Int J Gynaecol Obstet 1989. Ben-Arie A.e5 . 288:1610-21. Barakat RR. et al. Valachis A. 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