SURGERY AND POSTOPERATIVE RADIATION THERAPY IN FIGO STAGE IIIC ENDOMETRIAL CARCINOMA
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Int. J. Radiation Oncology Biol. Phys., Vol. 50, No. 5, pp. 1154 –1160, 2001
Copyright © 2001 Elsevier Science Inc.
Printed in the USA. All rights reserved
0360-3016/01/$–see front matter
PII S0360-3016(01)01590-5
CLINICAL INVESTIGATION Endometrium
SURGERY AND POSTOPERATIVE RADIATION THERAPY IN FIGO STAGE
IIIC ENDOMETRIAL CARCINOMA
ARNO J. MUNDT, M.D.,* KEVIN T. MURPHY, M.D.,* JACOB ROTMENSCH, M.D.,*†
STEVEN E. WAGGONER, M.D.,† S. DIANE YAMADA, M.D.,† AND PHILIP P. CONNELL, M.D.*
Departments of *Radiation and Cellular Oncology and †Obstetrics and Gynecology, Section of Gynecologic Oncology,
University of Chicago Hospitals, Chicago, IL
Objective: To determine the outcome, pattern(s) of failure, and optimal treatment volume in Stage IIIC
endometrial carcinoma patients treated with surgery and postoperative radiation therapy (RT).
Methods: Between 1983 and 1998, 30 Stage IIIC endometrial carcinoma patients were treated with primary
surgery and postoperative RT at the University of Chicago. All underwent total abdominal hysterectomy,
bilateral salpingo-oophorectomy, sampling of pelvic lymph nodes (PLN), and peritoneal cytology. All were noted
to have PLN involvement. Para-aortic lymph nodes (PALN) were sampled in 26 cases, and were positive in 14
cases (54%). Twenty women received whole-pelvic RT (WPRT) and 10 (WPRT), plus paraortic RT (extended-
field RT, EFRT). One EFRT patient also underwent concomitant whole-abdominal RT (WART). Adjuvant
vaginal brachytherapy (VB) was delivered in 10, chemotherapy in 5, and hormonal therapy in 7 patients.
Results: At a median follow-up of 32 months, the actuarial 5-year disease-free and cause-specific survivals of the
entire group were 33.9% and 55.8%, respectively. Overall, 16 women (53%) relapsed. Sites of failure included
the pelvis (23%), abdomen (13%), PALN (13%), and distant (40%). Of the 7 pelvic failures, 4 were vaginal (3
vaginal only). Patients treated with VB had a trend to a lower vaginal recurrence rate (0/10 vs. 4/20, p ⴝ 0.12)
than those not receiving VB. All 4 PALN failures were in women treated with WPRT (2 negative, 1 unsampled,
and 1 positive PALN). None of the 10 EFRT patients (2 negative, 8 positive PALN) recurred in the PALN. No
patient developed an isolated abdominal recurrence. Two patients developed significant RT sequelae: chronic
diarrhea in 1 patient treated with WPRT and VB, and small bowel obstruction in 1 patient treated with EFRT.
Conclusion: FIGO Stage IIIC disease comprises a small percentage of endometrial carcinoma patients but carries
a poor prognosis. Our failure pattern suggests that the optimal adjuvant RT volume is EFRT, even in women
with negative PALN sampling. VB should also be administered to improve local control. The low rate of
abdominal recurrence does not support the routine use of WART in these women. Given the predominance of
failure in distant sites, attention should be focused on the development of systemic chemotherapy protocols.
© 2001 Elsevier Science Inc.
Endometrial cancer, Stage IIIC, Radiation therapy.
INTRODUCTION volume in these women. At some centers, these and other
patients with extrauterine disease involvement are treated
Endometrial cancer is currently the most common gyneco- with whole abdominal RT (WART) (8 –11). In fact, the
logic malignancy in the United States (1). Most patients recently completed Gynecology Oncology Group (GOG)
present with early-stage disease and have a favorable out- trial for pathologic Stage III disease included a WART arm
come following surgery and radiation therapy (RT) (2). (12). Others have limited treatment to the regional lymph
However, approximately 5–20% of patients are found to nodes and used whole-pelvic RT (WPRT) alone (5, 7,
have involvement of pelvic lymph nodes (PLN) and/or 13–15) or WPRT plus paraortic RT (PART) (extended-field
paraortic lymph nodes (PALN) (3–5) and are designated as RT, EFRT) (3, 5, 7, 15–21). Although EFRT is certainly
Stage IIIC (6). Unlike early-stage patients, these women are reasonable in women with documented PALN involvement,
at high risk for disease recurrence and death (3, 7). the choice between WPRT and EFRT in patients with
The standard approach to patients with pathologic Stage negative or unsampled PALN is unclear. In addition, the
IIIC endometrial carcinoma is postoperative RT. However, role of vaginal brachytherapy (VB) in these women remains
considerable controversy exists over the optimal treatment controversial (7).
Reprint requests to: Dr. Arno J. Mundt, Department of Radiation for Therapeutic Radiology and Oncology (ASTRO), Boston, MA,
and Cellular Oncology, University of Chicago Hospitals, MC October 22–26, 2000.
9006, 5758 S. Maryland Ave, Chicago, IL 60637. E-mail mundt@ Received Nov 21, 2000, and in revised form Mar 15, 2001.
rover.uchicago.edu Accepted for publication Mar 21, 2001.
Presented at the 42nd Annual Meeting of the American Society
1154Stage IIIC endometrial carcinoma ● A. J. MUNDT et al. 1155
To examine these treatment issues, we retrospectively Table 1. Clinicopathologic characteristics
reviewed the outcome and failure patterns in pathologic
Characteristic n %
Stage IIIC endometrial carcinoma patients who received
primary surgery and postoperative RT at our institution over No. of patients 30 100
a 15-year period. Sites of recurrence are examined and Age, years
therapeutic implications are discussed. Median 62
Range 41–82
Race
METHODS AND MATERIALS Caucasian 23 76%
African-American 7 24%
Between 1983 and 1998, 562 women with endometrial Grade
carcinoma underwent primary surgery at the University of 1 2 6%
2 14 47%
Chicago. Thirty-eight (6.8%) were found to have involve- 3 14 47%
ment of the regional lymph nodes, without evidence of Histology
extra-abdominal metastases (FIGO Stage IIIC). Excluding 8 Adenocarcinoma 26 86%
patients with multiple extrauterine sites who received adju- Papillary serous 2 7%
vant chemotherapy alone, 30 underwent postoperative RT; Clear cell 2 7%
Myometrial invasion
these patients form the basis of this report. ⬍1/2 4 14%
Patient, tumor, and treatment characteristics were ab- ⱖ1/2 26 86%
stracted from the hospital records and pathology reports. All Cervix 16 53%
patients underwent total abdominal hysterectomy and bilat- Extrauterine Sites
eral salpingo-oophorectomy (TAH-BSO) as primary ther- Adenexae 1 3%
Peritoneal cytology 5 16%
apy. None received preoperative RT and/or chemotherapy. Serosa 5 16%
At surgery, each patient underwent careful examination of LVI 10 33%
the omentum, diaphragm, and peritoneal surfaces. Involve-
ment of these sites was considered Stage IV disease. Peri- Abbreviation: LVI ⫽ lymphovascular invasion.
toneal fluid was sent for cytologic evaluation in all cases.
While PLN sampling was performed in all patients, PALN
were sampled in 26 women (86%). The decision to sample commonly used chemotherapy agents were adriamycin and
PALN was surgeon dependent. No patient underwent com- cisplatin.
plete (formal) lymphadenectomy. All cases were staged Patients were evaluated following treatment with periodic
according to the 1988 FIGO criteria (6). Clear cell and history and physical examination, blood chemistries, and
papillary serous tumors were defined as “unfavorable” his- abdominal, pelvic, and thoracic computed tomography (CT)
tologies in our analysis. scans. Other radiographic examinations, including bone
Postoperative RT was administered within 4 – 6 weeks scans, were performed only in patients with suspected met-
following surgery. Twenty women received WPRT, and 10 astatic disease. Recurrence sites were divided into pelvic,
received EFRT. The selection of the RT volume was not paraortic, abdominal, and distant. Pelvic recurrences were
standardized over the years encompassed in this report and further divided into vaginal and lateral (sidewall) pelvis.
was dependent on the treating radiation oncologist. The The treatment (simulation) films of all patients noted to
median WPRT and para-aortic doses were 50.4 Gy (range, have a pelvic recurrence were reviewed to determine
40 –50.4 Gy) and 45 Gy (range, 45–50.4 Gy), respectively. whether the failure occurred near or on the field edge
One EFRT patient also received 30 Gy to the upper abdo- (marginal miss). Actuarial curves were calculated using the
men (WART). WPRT fields included treatment to the L4 –5 method of Kaplan–Meier (22) and compared by using the
interspace using a 4-field technique. EFRT fields included log–rank test (23). Intervals were calculated from the date of
treatment from the obturator foramen to the T10 –11 in- diagnosis. Median patient follow-up was 32 months (range,
terspace using opposed anterior–posterior portals. WART 4 –158 months).
was delivered with opposed anterior–posterior fields ex-
tending from 1 to 2 cm above the diaphragm to the bottom
RESULTS
of the obturator foramen. VB was delivered with low-dose-
rate afterloading technique using standard ovoids in 10 Table 1 summarizes the characteristics of the entire
women. Doses ranged from 25 to 30 Gy prescribed to the group. Most patients had deep (⬎ 1/2) myometrial invasion
vaginal surface. Chemotherapy and hormonal therapy were (MI) (86%) and cervical involvement (CI) (53%). Grade
not standardized during the years encompassed in this report 2–3 disease was present in 94% of patients. Although most
and were administered following RT to 5 (16%) and 7 had adenocarcinoma histology, 4 (14%) had unfavorable
(23%) patients, respectively. The decision to use systemic histologies (2 papillary serous, 2 clear cell).
therapy was dependent on the treating gynecologic oncolo- All patients underwent PLN sampling and were found to
gist. Overall, 9 women (30%) received adjuvant systemic have positive PLN. The median number of sampled and
therapy (4 hormonal, 2 chemotherapy, 3 both). The most positive PLN were 5 (range, 1–30) and 2 (range, 1– 6),1156 I. J. Radiation Oncology ● Biology ● Physics Volume 50, Number 5, 2001
ment; 3 did not. Overall, a trend to a lower rate of vaginal
recurrence was seen in women treated with VB (0/10 vs.
4/20, p ⫽ 0.12), compared to those treated with WPRT or
EFRT alone (Fig. 4). Of the 4 patients who recurred in the
lateral pelvis, 3 were treated with WPRT and 1 was treated
with EFRT. None of the lateral pelvic recurrences were on
or near the borders of the treatment field.
Four patients (13%) relapsed in the PALN. Table 2 illus-
trates the relationship between the site of lymph node in-
volvement, treatment volume, and PALN recurrence. Over-
all, 0 of the 10 patients (0%) treated with EFRT recurred in
the PALN, compared to 4 of 20 (20%) treated with WPRT
Fig. 1. Disease-free survival of the entire group. (p ⫽ 0.12). Of the 10 patients treated with EFRT, 2 had
negative and 8 had positive PALN. In the 20 WPRT pa-
tients, 2 had negative, 4 had unsampled, and 6 had positive
respectively. Twenty-six patients (86%) underwent PALN PALN. Of the 4 PALN recurrent patients, 1 had an ante-
sampling. The median number of sampled and positive cedent and 1 had a concomitant pelvic recurrence. The third
PALN were 3 (range, 1– 6) and 1 (range, 1–5), respectively. patient had a concomitant abdominal recurrence. Only 1 had
Of the 26 patients who underwent PALN sampling, 14 an isolated PALN recurrence.
(54%) had positive PALN. Abdominal relapse was noted in 4 women (13%). One
Overall, 16 patients (53%) developed recurrent disease, had papillary serous histology, and 1 had multiple extra-
and 10 (33%) died of their disease. The actuarial 5-year uterine sites. PALN sampling was negative in 1, positive in
disease-free survival (DFS) and cause-specific survival 1, and not done in 2. Of note, no patient developed an
(CSS) rates of the entire group were 33.9% and 55.8%, isolated abdominal recurrence. Two recurred simulta-
respectively. These results are shown graphically in Figs. 1 neously with pelvic and distant metastases, 1 several
and 2. months following a distant recurrence and 1 following a
An analysis of clinicopathologic factors failed to identify pelvic recurrence.
any significant correlation between pathologic factors and Twelve women (40%) developed distant metastases, pri-
recurrence. Patients with positive peritoneal cytology had a marily in the lungs and bones. Two had unfavorable histol-
nonsignificant trend to a worse 5-year DFS (14.2 vs. 38.3%, ogies, and 6 had multiple extrauterine disease sites. Six
p ⫽ 0.16), compared to patients without positive cytology. patients developed distant metastases following a pelvic (3)
A worse 5-year DFS was seen in patients with Grade 3 or PALN (3) recurrence.
tumors (23.4 vs. 43.6%), compared to those with Grade 1–2 The risk of pelvic and distant recurrence was similar in
tumors; however, this difference failed to reach statistical patients treated with RT and those treated with RT and
significance (p ⫽ 0.58). The 5-year DFS of patients with systemic therapy. Of the 21 patients treated with RT alone,
positive PLN only, positive PLN and unsampled PALN, and pelvic and distant recurrence were noted in 3 (14.2%) and 8
positive PALN were 51.7%, 20%, and 33%, respectively. (38%) patients, respectively. Corresponding numbers, in the
The pattern of failure of the entire group is shown in Fig. 9 women treated with systemic therapy, were 1 (11.1%) and
3. Seven women (23%) recurred in the pelvis (3 vagina, 3 4 (44.4%). Of note, patients treated with RT alone had a
lateral pelvis, 1 both). Of the 4 patients who recurred in the higher abdominal failure (4/21 or 19%) than patients treated
vagina, none had received VB. One had cervical involve- with RT plus systemic therapy (0/9 or 0%). However, 3 of
the 4 unfavorable histology patients were in the RT alone
group.
Table 2 summarizes the risk of PALN failure based on
RT volume and systemic treatment. Clearly, the small num-
bers in each group preclude a definitive analysis. However,
several observations are noteworthy. Three of the 4 patients
who recurred in the PALN were treated with RT alone (all
WPRT). Whereas only 1 of the 6 PALN positive patients
recurred in the PALN following WPRT, 4 received adjuvant
systemic therapy.
Treatment was well tolerated, with no patients develop-
ing a significant surgical sequelae. RT was delivered with-
out treatment interruptions, and all patients received their
planned doses. Two patients (6.6%) suffered significant
Fig. 2. Cause-specific survival of the entire group. RT-related sequelae (1 chronic diarrhea, 1 SBO). The pa-Stage IIIC endometrial carcinoma ● A. J. MUNDT et al. 1157
Fig. 3. Pattern of failure.
tient with chronic diarrhea had received WPRT and VB; the 17, 18, 20, 21). Others include a mix of patients with PLN
other had received EFRT. and PALN (7, 8, 11, 16, 19) or solely PLN (13, 20) involve-
ment. Our series of 30 Stage IIIC patients represents the
largest single-institution series in the literature, and the
DISCUSSION
5-year CSS of 55.8% reported here compares favorably with
FIGO Stage IIIC endometrial carcinoma is uncommon, the published reports.
comprising only 6.7% of all endometrial carcinoma patients Most patients in our series underwent WPRT or EFRT.
treated with primary surgery at our institution during the Nonetheless, we noted a low rate of abdominal recurrence
15-year study period. At other centers, such patients repre- (13%). Moreover, no patient developed an isolated abdom-
sent 5.4 –18% of patients (3–5, 13, 17, 24). However, given inal relapse. Others have similarly noted low rates of ab-
the adoption of a surgically based staging system by FIGO dominal recurrence following WPRT or EFRT (5). Greven
in 1988 (6), the percentage of patients diagnosed with Stage et al. evaluated the sites of failure in Stage IIIC patients
IIIC disease will certainly increase in the coming years. treated with WPRT or EFRT and noted abdominal relapse
Earlier investigators have evaluated the outcome of Stage in only 7% of patients (7). In 17 Stage IIIC patients with
IIIC patients undergoing surgery and postoperative RT (Ta- disease confined to the pelvis (16 treated with WPRT),
ble 2). These series vary greatly in terms of the number of Nelson et al. reported no abdominal relapses (13). In total,
patients studied, with most including very limited numbers.
In fact, only three (all multi-institutional) consist of 25
patients or more (3, 7, 17). Moreover, these series differ in Table 2. PALN Recurrences by RT volume and site of nodal
terms of the site of nodal involvement in their patients. Most involvement
include solely patients with documented PALN (3, 5, 15, PALN recurrences
PALN status n EFRT WPRT
Negative 12 0/2 2/10
RT alone 0/1 2/8
RT ⫹ systemic* 0/1 0/2
Unsampled 4 — 1/4
RT alone — 1/4
RT ⫹ systemic — —
Positive 14 0/8 1/6
RT alone 0/6 0/2
RT ⫹ systemic† 0/2 1/4
30 0/10 4/20
(0%) (20%)
Abbreviations: PALN ⫽ paraortic lymph nodes; RT ⫽ radiation
therapy; EFRT ⫽ extended-field RT; WPRT ⫽ whole-pelvic RT.
Fig. 4. Vaginal recurrence-free survival of patients treated with (1) * 2 hormonal therapy, 1 chemotherapy.
†
and without (0) vaginal brachytherapy. 1 chemotherapy, 2 hormonal therapy, 3 both.1158 I. J. Radiation Oncology ● Biology ● Physics Volume 50, Number 5, 2001
these results fail to support the use of WART in Stage IIIC MI and CI, in Stage IIIC patients, we currently recommend
disease. Nonetheless, it is possible that WART may be VB to reduce the risk of pelvic failure.
indicated in select patients. Greven et al. (7) correlated A finding of some concern in our series was the high rate
abdominal recurrence in Stage III patients with unfavorable of nonvaginal (lateral) pelvic failure. Whereas some authors
histology and multiple extrauterine sites. Consistent with have reported excellent pelvic control rates (5, 13), others
these findings, 2 of the 4 abdominal relapses in our series have noted rates ranging from 12% to 21% (7, 15). These
were in women with such adverse factors. WART may, control rates are markedly worse than those in pathologic
thus, be an appropriate volume in these high-risk patients. Stage I–II patients (2, 26, 27). The reason for this is not
The choice between WPRT and EFRT in the low-risk entirely clear. It is possible that the density of tumor cells is
patient is less clear. A reasonable treatment volume in simply higher in Stage IIIC patients. This may also explain
women with known PALN involvement is EFRT. None of the poor pelvic control seen in node-positive cervical cancer
8 such patients relapsed in these nodes in our series. Others following adjuvant WPRT (28).
have treated PALN-positive patients similarly with EFRT To improve the pelvic control of these patients, higher
(3, 7, 15, 18, 19, 21) and noted high rates of PALN control doses may, thus, be necessary. However, doses above 45–50
(16, 18). Curiously, PALN recurrence was seen in only 1 of Gy are associated with increased toxicity (29, 30). We (31,
6 women in our series with known PALN involvement 32) and Portelance et al. (33) are currently exploring the use
treated with WPRT alone. However, given the high distant of intensity-modulated RT (IMRT) in women undergoing
metastasis rate in our series, the actual risk of failure in the WPRT and EFRT to minimize the dose to the small bowel
PALN may have been underestimated in these women. In and other normal tissues. Such an approach may allow the
the only other series to compare WPRT and EFRT in delivery of higher than conventional doses in these women.
patients with PALN involvement, Hicks et al. noted a lower Moreover, IMRT may further decrease the risk of toxicity in
rate of overall recurrence in women treated with EFRT. women undergoing WPRT or EFRT with conventional
However, no PALN recurrences were seen in either group doses.
Stage IIIC disease represents a heterogeneous group of
(5).
patients. Some have involved PLN, others PALN, or both.
In women with negative PALN sampling, the optimal
Although not statistically significant, we noted a worse
treatment volume is more controversial. Ten such patients
outcome in women with positive PALN, compared to those
were treated with WPRT in our series, and 2 recurred in the
with only positive PLN. Recently, Nelson et al. proposed
PALN. Of 13 endometrial cancer patients with positive
dividing Stage IIIC patients into 3 substages, based on the
PLN but negative PALN treated at Indiana University, 2
site of nodal involvement (13). Data from the GOG database
relapsed in the PALN following WPRT alone (13). We,
supports this division (3). Stage IIIC patients also have a
thus, currently favor the use of EFRT in these patients.
variety of adverse features, including involvement of the
PALN involvement is common in women with positive
cervix, adnexae, serosa and vagina, and LVI. Nelson et al.
PLN. In our series, 54% of patients with positive PLN who found a worse outcome in women with positive cytology
underwent PALN sampling were found to have involved and LVI (13). Others have correlated recurrence with ad-
PALN, consistent with earlier studies (3). Of note, PALN nexal involvement (15). These results are all consistent with
sampling may underestimate PALN involvement, because the findings of Greven et al., who noted a correlation
most disease involvement is microscopic and will be missed between the number of extrauterine sites and recurrence in
without formal node dissections (25). Stage III disease (14).
A similar argument exists in favor of EFRT in women A final noteworthy finding in our series is the high rate of
with positive PLN but unsampled PALN. We noted PALN failure in distant sites. Others have noted similarly high
recurrences in 1 of 4 such women following WPRT. How- rates of distant failure, particularly in women with PALN
ever, this risk may also have been underestimated given the involvement, ranging from 16% to 50% (5, 7, 11, 14). These
high rate of distant metastases in our series. We currently results provide support for the use of adjuvant systemic
feel that EFRT should be used in such patients with known therapy in these women. Unfortunately, to date, there has
high-risk factors for PALN involvement, including high- been no definitive evidence that either adjuvant chemother-
grade disease (5, 18, 24), CI (3, 24), vascular invasion (3, apy (34) or hormonal therapy (35, 36) decrease the risk of
24), and deep MI (3, 18, 24). Our results indicated that the relapse in endometrial cancer. Clearly, the small number of
use of VB in Stage IIIC patients is highly variable. We women in our study treated with systemic therapy precludes
noted a nonsignificant improvement in vaginal control in us from making any definitive statements about the utility of
women treated with VB. Others have noted conflicting systemic therapy in pathologic Stage IIIC disease. Given the
results. Greven et al. found no benefit in the use of VB in high risk of extra-abdominal relapse in these women, atten-
pathologic Stage III patients (7). However, Stage IIIC pa- tion needs to be turned to the use of EFRT in conjunction
tients were not analyzed separately. Nelson et al. noted no with novel systemic agents, including paclitaxel and her-
pelvic recurrences in their patients, although only 2 of 17 ceptin. In addition, as suggested by Corn et al. (37), many
received VB (13). Given the high rate of adverse pathologic of the patients who developed distant metastases had suf-
features correlated with vaginal recurrence, including deep fered an antecedent pelvic or PALN recurrence. ImprovedStage IIIC endometrial carcinoma ● A. J. MUNDT et al. 1159
locoregional control may thus also help reduce the risk of negative PALN sampling. VB should also be administered
extra-abdominal recurrence in these women. to improve local control. The low rate of abdominal recur-
In conclusion, FIGO Stage IIIC disease comprises a small rence does not support the routine use of WART in these
percentage of endometrial carcinoma patients, but it carries women. Given the predominance of failure in distant sites,
a poor prognosis. Our failure pattern suggests that the op- attention should be focused on the development of systemic
timal adjuvant RT volume is EFRT, even in women with chemotherapy protocols.
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