CA Endometrial e Hiisteroscopia

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O N C O L O G Y

The risk of diagnostic hysteroscopy

in women with endometrial cancerJennifer 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

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%) hadundergone hysteroscopy. There wasno difference in stage

III disease between the hysteroscopy (7.1%) vs no hysteroscopy (6.5%)

group (P .38). There was also no difference in death rates, 13.2% vs

15.2% (P .25), or in the proportion of women dying of female genital

organ cancer, 46.1% vs 42.1% (P .53), respectively.

CONCLUSION: Hysteroscopy is not associated with a higher rate of

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.

Hysteroscopy is widely used for thediagnosis of endometrial hyper-plasia or carcinoma. The sensitivity has

been estimated to be 86.4%.1 In compar-

ison, Pipelle endometrial biopsies have

been reported to have a sensitivity of 67-

83.5%.2,3 It has also been shown that

hysteroscopically guided curettage hashigher accuracy than dilatation and cu-

rettage (D&C)alone.4However, concern

exists that the introduction of high-pres-

sure gas or fluid into the uterine cavity,

to produce distension, could facilitate

the dissemination of malignant cells in

patients with endometrial cancer. It has

been found that the distention medium

can begin draining transcervically and

transtubally when pressures reach ap-

proximately 100-150 mm Hg. Thus, in

the patient with endometrial cancer,

there is the theoretical possibility that

malignant cells might be dispersed intothe fallopian tubes and the abdominal

cavity following hysteroscopy.5 The evi-

dence associating peritoneal dissemina-

tion 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 per-

formed in patients with endometrial

cancer had an effect on subsequent sur-

gical 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 10years (1997 through 2006).

MATERIALS AND METHODS

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 In-

ternational Classification for Diseases for

Oncology. Data on women with endome-trial cancer were retrieved from the reg-

istry from Jan. 1, 1997, through Dec. 31,

2006. This start time was chosen princi-

pally because the Alberta Cancer Regis-

try had undergone a number of coding

changes prior to this time period. It was

not until 1997 that endometrioid adeno-

carcinoma 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 newstaging criteria for endometrial cancer

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 ofMedicine, 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 interpretationand conclusions contained herein are those of the researchers and do not necessarily representthe views of the Government of Alberta. Neither the government nor Alberta Health and Wellnessexpresses 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 ofGynecologic 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

Research www.AJOG.org

JULY 2012 American Journal of Obstetrics &Gynecology 71.e1
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that took place in 1989. Staging after that

change included surgical observations.17

Besides diagnosis, the Alberta Cancer

Registry provided further information

on pathology (histologic cell type and

staging) and vital statistics. Loss to fol-

low-up within the Alberta Cancer Regis-try is minimal, as each month linkage is

made to Alberta Vital Statistics to iden-

tify those cancer patients who have died

and the causeof death. In addition, there

is a link made annually with the Cana-

dian National Mortality database. How-

ever, patients who die outside Canada

could be potentially missed.

Cases were selected from the Alberta

Cancer Registry based on the diagnosis

of endometrial cancer as defined by a

positive biopsy. Staging was reported bythe treating physician. In Alberta, pelvic

washings are considered the standard of

care. The majority of cases would have

also included pelvic lymph node sam-

pling. For the few cases missing node

sampling, the performance of pelvic

washings alone would have dictated the

classification of stage IIIa disease based

on the International Federation of Gyne-

cology and Obstetrics (FIGO) 1989 stag-

ing criteria.17

A thorough review of this dataset wasthen performed to eliminate transcrip-

tion errors and to clarify staging. When

staging information within the dataset

was missing or not interpretable, cross-

reference to other variables (ie, text en-

tered by the physician) in the wider elec-

tronic database allowed for clarification

in many cases. Finally, any staging based

on the American Joint Committees

Cancer TNM staging manual (fifth and

sixth editions) was translated to the FIGO

1989 staging criteria.17

Alberta Health and Wellness adminis-

ters a universal health care plan that cov-

ers all Albertans, and through this, phy-

sicians are reimbursed for all procedures

performed in the province. The Alberta

Health and Wellness dataset provided

information on diagnostic hysteroscopy

(specifically by fee code 80.81) and patient

characteristics(age). This code would have

captured hysteroscopy performed in both

the office setting and operating room.When hysteroscopy was not performed,

diagnoses would have been made by either

office endometrial biopsy or D&C.

The cases from the cancer registry

were then linked to the Alberta Health

and Wellness dataset. Information on

whether a diagnostic hysteroscopy was

performed for each patient was ab-stracted. Data linkage went back as far as

January 1996, to include information on

cases that were pulled from the Alberta

CancerRegistry forthe year of 1997. This

would represent hysteroscopy that had

been performed within 1 year, isolating

that which was used for the diagnosis of

endometrial cancer. Data linkage was

performed using at least 2 patient-spe-

cific variables within each dataset, and allidentifying information was removed

from the linked dataset before release foranalysis.

Women with stage IV disease were ex-

cluded, since diagnosis with an endome-

trial sample may not have been required,

as disease may have been more clinically

apparent at presentation. As the survival

in this group is also close to 0,this would

have affected our analysis by dispropor-

tionably decreasing the survival for

women who had not had hysteroscopy.

Cases were also excluded if histology in-

dicated a nonadenocarcinoma type ofcancer, such as squamous, clear cell, pap-

illary serous, and/or undifferentiated car-

cinoma. This eliminated advanced dis-

ease that was likely due to the inherent

disease process of a more aggressive tu-

mor type, rather than the diagnostic

technique used.

There were 2 primary outcomes in

this study: staging and overall survival.

Staging IIIa would indicate that thecarcinoma had extended out of the

uterus. If peritoneal dissemination viathe fallopian tubes occurs during hys-

teroscopy, staging should indicate at

least stage III. Therefore, the study hy-

pothesis was that hysteroscopy would

be associated with an increased fre-

quency of stage III disease and endo-

metrial cancerrelated deaths.

Review of the literature suggested that

10% of those women with endometrial

cancerwho undergo hysteroscopyfor di-

agnostic purposes and 5% of those who

do not undergo hysteroscopy will havestage III disease.12 From this, it was cal-

culated that a sample size of 387 and 581

women who have and have not under-

gone hysteroscopy, respectively, would

be needed to detect a difference in stag-

ing with a power of 80% and an alpha

error of 0.05. These numbers were easily

attained from the provincial registries.Data were summarized using propor-

tions for categorical variables, and bothmean and median for continuous vari-

ables. Bivariate analyses were performed

to compare the hysteroscopy groups in

regard to staging and other possible

prognostic risk factors. Comparisons

were made using Pearson 2 test for cat-

egorical variables. Mantel-Haenszel 2

test was used to identify trends in pro-

portions. A Student t test was used to

compare continuous variables if theywere normally distributed; otherwise,

the Wilcoxon rank sum test was used.

P .05 was considered to be statistically

significant. All statistical calculations

were performed using the SAS program

package (SAS Institute, Cary, NC).

Data were managed according to the

Alberta Privacy Legislation. Data linkage

between Albertas Cancer Registry and

the Health and Wellness dataset was per-

formed by Alberta Health and Wellness.

Thisprocess did not compromise patientconfidentiality as only anonymous datawere received by the research team. Eth-

ical approval was obtained from the

Conjoint Health Research Ethics Board

at the University of Calgary (Ethics Re-

view Board no: E-20934).

RESULTS

The initial data request from the Alberta

Cancer Board had provided 2331 cases

that met both inclusion and exclusioncriteria. A 99.8% match rate was ob-

tained when linkage was performed with

the Alberta Health and Wellness claims

data. Approximately 85% of these cases

had complete and appropriate data on

staging (350 were missing staging com-

pletely, while 5 had staging complicated

by coexistent cancer, a different type of

cancer, or a benign condition). Of these

1972 cases with complete staging, 672

(34.1%) had undergone hysteroscopy.

There wasan increase in the utilizationof hysteroscopy over the study period,

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71.e2 American Journal of Obstetrics &Gynecology JULY 2012


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and in the number of cases diagnosed. In

1997, 40 hysteroscopies were performed

in 154 women who were diagnosed with

endometrial cancer (26.0%), whereas, in

2006, 95 hysteroscopies were performed

in 232 women (40.9%).

The mean age was 62.0 and 60.7 years,respectively, for women who had under-gone hysteroscopy and those who had

not (Wilcoxon rank sum, P .01).

The frequencies of FIGO stages in the

2 groups are shown in Table 1. The rates

of stage III disease did not differ statisti-

cally between those who had and did not

have hysteroscopy (relative risk, 1.16;

95% confidence interval [CI], 0.831.62;

P .38).

There was also no statistically signifi-

cant difference found in death rates forthose who had a hysteroscopy (13.2%)

compared to those who had not (15.2%)

(relative risk, 0.87; 95% CI, 0.691.10;

P .25) (Table 2). The mean years of

follow-up for each group were 4.0 (0.03-

9.97) and 4.4 (0.02-10.67), respectively.

Survival analysis was not possible be-

cause of the relatively fewer numbers of

deaths, resulting in high censor rate in

the analysis. When evaluating only those

women who had died, statistically signif-

icant differences were found neither inthe proportion of stage III disease (P

.10), nor in the proportion of women dy-

ing of female genital organ cancer be-

tween hysteroscopy groups (P .53)

(Table 3).

COMMENT

Our results indicate that hysteroscopy in

patients with endometrialcancer is not as-

sociated with a higher rate of subsequent

stage III disease. There was no statisticaldifference in death rates between hysteros-

copy groups. Additionally, among those

who had died, there was no statistical dif-

ference in stage III disease between hyster-

oscopy groups.

Previous studies have published con-

flicting results about the effect of hyster-

oscopy on peritoneal dissemination of

malignant cells and upstaging of disease

in women who have endometrial cancer.

The first of the reports providing evi-

dence against hysteroscopy was by Ober-mair et al.8 Their group performed a

multicenter, retrospective cohort analy-sis of 113 consecutive patients with en-

dometrialcancer limited to theinner half

of the myometrium, who underwent

D&C either with or without prior diag-

nostic hysteroscopy. They found that the

only factor significantly associated with

positive peritonealcytology was a history

of hysteroscopy (12.2% vs 2.5%, P

.04).

Zerbe et al6 reviewed the charts of 222

patients with endometrial cancer and

evaluated the peritoneal dissemination

of malignant cells during hysteroscopy.They found a difference in positive peri-

toneal cytology in those who had hyster-

oscopy vs those who had not (odds ratio,

2.6; 95% CI, 1.026.63; P .05).

Bradley et al15 reviewed 256 charts of

women with endometrial cancer. In all,

204 cases were diagnosed by endometrial

biopsy or D&C, whereas 52 were diag-

nosed withhysteroscopy. A nonsignificant

lower proportion of patients (6.9%) had

malignant orsuspicious cytology intheen-

dometrial biopsy or D&C group, com-

TABLE 1

Stage of disease by hysteroscopy

Hysteroscopy

Stage

Yesn 672

No. (%)

Non 1300

No. (%) Statistical testStageIII 621 (92.9) 1215 (93.5) 2 P .38..............................................................................................................................................................................................................................................

Stage III 51 (7.1) 85 (6.5) RR, 1.16; 95% CI, 0.831.62..............................................................................................................................................................................................................................................

Details of FIGO stage.....................................................................................................................................................................................................................................

FIGO 0 1 (0.2) 3 (0.2).....................................................................................................................................................................................................................................

FIGO Ia 67 (10.0) 112 (8.6).....................................................................................................................................................................................................................................

FIGO Ia 133 (19.8) 265 (20.4).....................................................................................................................................................................................................................................

FIGO Ib 182 (27.1) 447 (34.4).....................................................................................................................................................................................................................................

FIGO Ic 116 (17.3) 201 (15.5).....................................................................................................................................................................................................................................

FIGO IIa 2 (0.3) 19 (1.5).....................................................................................................................................................................................................................................

FIGO IIa 49 (7.3) 55 (4.2).....................................................................................................................................................................................................................................

FIGO IIb 71 (10.6) 113 (8.7).....................................................................................................................................................................................................................................

FIGO IIIa 1 (0.2) 3 (0.2).....................................................................................................................................................................................................................................

FIGO IIIa 21 (3.1) 54 (4.2).....................................................................................................................................................................................................................................

FIGO IIIb 3 (0.5) 5 (0.4).....................................................................................................................................................................................................................................

FIGO IIIc 26 (3.9) 23 (1.8)..............................................................................................................................................................................................................................................

CI, confidence interval; FIGO, International Federation of Gynecology and Obstetrics; RR, relative risk.

a Substaging was not available.

Soucie. Riskof hysteroscopy in endometrial cancer. Am J Obstet Gynecol 2012.

TABLE 2

Vital statistics by hysteroscopy

Hysteroscopy

Vital statisticsYes n 672No. (%)

No n 1300No. (%) Statistical test

Alive 583 (86.8) 1103 (84.8) 2 P .25..............................................................................................................................................................................................................................................

Dead 89 (13.2) 197 (15.2) RR, 0.87; 95% CI, 0.691.10..............................................................................................................................................................................................................................................

CI, confidence interval; RR, relative risk.


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pared to the hysteroscopy group (13.5%)(P .15). However, after controlling for

stage and grade, the odds ratio for positive

cytology after hysteroscopy was 3.88 (95%

CI, 1.1113.6; P .03).

The final study providing evidence

against the use of hysteroscopy was per-

formed by Takac and Zegura.16 In their

review of 146 women with endometrial

cancer diagnosed with either D&C or of-

fice hysteroscopy, they found suspicious

or positive peritoneal cytology was pres-

ent in 1.6% (2/122) after D&C and12.5% (3/24) after hysteroscopy (P

.05).

Evidence in support of the use of hys-

teroscopy has also been published. Gu et

al9 found that of 23 patients who were

diagnosed by D&C with hysteroscopy,

17 had abnormal peritoneal washings

(13.0%). Of 177 patients diagnosed by

either endometrial biopsy or D&C with-

out hysteroscopy, again 17 had abnor-

mal peritoneal washings (9.6%). The

rates were not different statistically.Similarly, Selvaggi et al7 evaluated pa-

tients with endometrial cancer and

found that 52 had a diagnosis made only

by D&C, 56 underwent D&C and then

hysteroscopy, and 39 had only hysteros-

copy. Peritoneal cytology was positive in

9 patients, and 21 had microscopic intra-

peritoneal dissemination; neither was

significantly associated with hysteros-

copy (P .07).

Juhasz-Boss et al14 took a novel ap-

proach to evaluating the effects of hyster-oscopy.Whensentinel lymph node biopsy

is performed, a second hysteroscopy isnecessary for technetium injection. Ju-

hasz-Boss et al14 took this factor into con-

sideration in their analysis, and examined

whetherthe number of hysteroscopiesand

the time interval between hysteroscopy

and surgery had an effect on cytology. The

rate of positive cytology was 18.2% (4/22)

in those without hysteroscopy vs 1.9% (2/

104) and 7.1% (5/70) for those with 1 and

2 hysteroscopies, respectively (P .008).

Furthermore, positive cytology was notre-

lated to the timeintervalbetween preoper-ative hysteroscopy and definitive surgery.Kudela and Pilka10 prospectively re-

viewed 134 women diagnosed with hys-

teroscopy and 61 diagnosed with D&C.

Positive or suspect cytology in fluid from

lavage was present in 30.3% for those

with hysteroscopy, compared to 33.9%

in those who underwent a D&C. Both

groups were comparable for stages of

disease.

Ben-Arie et al11 reported on a cohort of

392 women diagnosed with endometrialcancer with endometrial biopsy (25.3%),

uterine curettage (49.2%), and hysteros-

copy (25.5%). In this series, poor histo-

logic types, including serous papillary,

clear cell, and small cell cancer were in-

cluded in the analysis. Peritoneal cytol-

ogy was positivein only1 case, thus com-

parison could not be made. However, no

statistic difference in the survival rate

was found between diagnostic methods.

There have been 2 randomized con-

trolled trials evaluating the effects of hys-teroscopy on peritoneal cytology. Sainz

de la Cuesta et al12 examined 50 consec-

utive patients with endometrial cancer.

Patients were randomized 3:2 to have or

not to have fluid hysteroscopy biopsy

performed just prior to surgery. There

were 3 patients (10%) with positive

washings in the hysteroscopic groupcompared to 1 (5%) among the controls

(P .64). This difference was not statis-

tically significant; however, the small

sample size only allowed for a statistical

power of20%. Median follow-up was

34 months, and all patients but 1 (de-

ceased due to unrelated cause) were alive

with no evidence of disease. 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.Cicinelli et al13 randomized 140 women

to undergoor notundergodiagnosticfluid

minihysteroscopy before surgical staging.

There was no difference in peritoneal cy-

tology between those who had hysteros-

copy (5.7%) vs those who did not (8.5%).

After a mean duration of follow-up of 62

months, overall survival and disease-free

survival werenot significantly different for

the 2 groups.

From the literature, it is evident that

there is no firm conclusion as to whetherhysteroscopy leads to peritoneal dissem-

ination of malignant cells in women who

have endometrial cancer. Prior to this

publication, and not including the 2 ran-

domized controlled trials, a metaanalysis

indicated that hysteroscopy is associated

with a small risk of peritoneal spread, and

by direct extension, higher disease upstag-

ing. However, they note that greater num-

bers are needed to clarify the effect on

prognosis.18Thesamplesizesofthestudies

to date have been small to moderate with

limited follow-up intervals to adequately

evaluate survival differences. Our study

provides more informationas it includeda

large sample, with a cohort spanning over

10 years. The results indicate clearly that

hysteroscopy is not associated with higher

stagingof endometrialcancer.From this, it

suggests that hysteroscopy does not im-

pose a significant risk of dissemination.

Most importantly, there was no difference

in death rates, and more specifically, thecause of death from female genital organ

TABLE 3

Staging and cause of death by hysteroscopy among women who died

Hysteroscopy

StagingYes n 89No. (%)

No n 197No. (%) 2 Pvalue

StageIII 70 (78.7) 170 (86.3) .10..............................................................................................................................................................................................................................................

Stage III 19 (21.3) 27 (13.7)..............................................................................................................................................................................................................................................

Cause of death.....................................................................................................................................................................................................................................

Noncancer death cause 25 (28.1) 62 (31.5) .53a.....................................................................................................................................................................................................................................

Female genital organ cancer 41 (46.1) 83 (42.1).....................................................................................................................................................................................................................................

Other cancer 15 (16.9) 37 (18.8).....................................................................................................................................................................................................................................

Primary unknown death cause not coded 8 (9.0) 15 (7.6)..............................................................................................................................................................................................................................................a2 comparing female genital organ cancer vs all other causes of death.


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71.e4 American Journal of Obstetrics &Gynecology JULY 2012


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cancer did not differ significantly between

the groups.

There are a few limitations to this study,

the main limitation being that positive

peritoneal cytology could not be directly

evaluated, as the information was not

available in either of the electronic data-bases. To retrieve this information, indi-

vidual patient charts at each regional

health authority would have to have been

reviewed, and this was not possible. In-

stead, disease stage was evaluated, with the

hypothesisthatanyupstagingofdiseasere-

sulting from hysteroscopy should have

been evident in our analysis. It should also

be noted that FIGO did replace their stag-

ing criteria in 2009, with positive perito-

neal cytology not included as it was not

considered to have an independent effecton survival.19 Nonetheless, all staging in

this cohort was based on the previous cri-

teria, and thus peritoneal cytology would

have been captured by this older classifica-

tion system.

This study was also a retrospective co-

hort study, and therefore by design is

subject to several possible biases, namely

reporting and selection bias. It would be

ideal if all cases of endometrial cancer

were reported to the cancer registry;

however, this is unlikely and thus, somedegree of reporting bias may be evident.

It would be impossible to know whether

there were differences in reporting for

those who had hysteroscopy vs those

who had not. However, the Alberta Can-

cer Registry has an overall calculated

capture rate of 95%, and thus a differ-

ence in reporting was likely minimal.

Finally, 15% of our sample was miss-

ing staging data, and this is a common

problem with administrative databases.

Every effort was made to ascertain miss-

ing data from the larger database when

available.

Ourlarge study covering a periodof 10

years of endometrial cancer manage-

ment offers valuable evidence to guide

clinical practice. Our results clearly indi-cate that hysteroscopy, which allows for

direct visualization and directed biopsy,

should be considered a safe diagnostic

tool in women suspected of having en-

dometrial cancer. f

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CA Endometrial e Hiisteroscopia