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2059
Adjuvant Small Field Pelvic Radiation for Patients
with High Risk, Stage IB Lymph Node Negative Cervix
Carcinoma after Radical Hysterectomy and Pelvic
Lymph Node Dissection
A Pilot Study
Frédéric J. Kridelka, M.B.,
Derek O. Berg2
Menahem Neuman, M.D.2
Lyndal S. Edwards2
Greg Robertson2
Peter T. Grant2
Neville F. Hacker, M.D.2
1
Ch.B.
1
Department of Gynecology, CHU Liège, Liège,
Belgium.
2
Gynaecological Cancer Centre, Royal Hospital for
Women, Randwick New South Wales, Australia.
Presented at the Australian Society of Gynecological Oncology, Bowral, Australia, May 19 –23, 1996
(awarded Keith Free Price for Best Presentation by
a Fellow in Gynecological Oncology) and at TOW
Research Price, Prince of Wales Hospital, Sydney,
Australia, October 31, 1996 (winner of the Tow
Research Price, Clinical Division).
Supported by a fellowship for overseas clinical
research from the Léon Frédérick Foundation, University of Liège, Belgium and by the Gynecologic
Oncology Fund of the Royal Hospital for Women
Foundation, Randwick, Australia.
The authors thank Mrs. T. Moryosef for data management, Mr. R. Fisher for the statistical analysis,
and Mrs. S. Rainer and M. Schneider for assisting
in radiotherapy imaging production.
Address for reprints: Prof. Neville F. Hacker,
Gynaecological Cancer Centre, Royal Hospital for
Women, Barker Street, Randwick, NSW 2031, Australia.
Received August 7, 1998; revisions received January 11, 1999 and March 18, 1999; accepted
March 18, 1999.
© 1999 American Cancer Society
BACKGROUND. After radical hysterectomy and pelvic lymph node dissection, an
identifiable subgroup of patients with International Federation of Gynecology and
Obstetrics Stage IB lymph node negative cervix carcinoma remains at high risk of
pelvic recurrence. This study attempted to determine whether postoperative small
field of pelvic radiation can improve the disease free survival (DFS) of this high risk
group of patients without producing significant morbidity.
METHODS. Between 1991 and 1995, after radical surgery, 25 patients with Stage IB
lymph node negative cervix carcinoma were considered to be at high risk of pelvic
recurrence on the basis of tumor dimension, depth of stromal invasion, and the
presence of lymph-vascular space invasion. All had a score $ 120 as determined by
the Gynecologic Oncology Group (GOG) study. These patients received 50.4 gray of
adjuvant radiation to a small central pelvic field and were followed prospectively.
A Kaplan–Meier 5-year DFS curve was generated. A log rank analysis produced an
estimated log rank P value (est P value) by comparing the 5-year DFS of the
patients in the current study with the 5-year DFS of the corresponding high risk
group of the GOG study (observation only). The morbidity of small field pelvic
radiation was recorded.
RESULTS. Among the 25 patients who received small field pelvic radiation, the
mean GOG score was 166 (range, 120 –263) and the mean follow-up was 32 months
(range, 12– 64 months). There was 1 recurrence (4%) recorded at 16 months. The
log rank analysis demonstrated a significant improvement in the 5-year DFS for the
group who received adjuvant small field pelvic radiation (est P value 5 0.005) when
compared with the DFS of the high risk GOG patients who were observed postoperatively. Four cases of minor morbidity were recorded: lymphedema (three cases)
and mild rectal incontinence (one case). No major morbidity was reported.
CONCLUSIONS. With low morbidity, adjuvant small field pelvic radiation appears to
improve significantly the 5-year DFS of patients with high risk, lymph node
negative Stage IB cervical carcinoma. However, this pilot study requires verification. Cancer 1999;86:2059 – 65. © 1999 American Cancer Society.
KEYWORDS: early cervical carcinoma, adjuvant radiation, Gynecologic Oncology
Group score, 5-year disease free survival, radiation morbidity.
T
here is no standard management of International Federation of
Gynecology and Obstetrics Stage IB cervical carcinoma.1 As a
group, most patients are treated by radical surgery, but some institutions prefer a radiotherapeutic approach. Combinations of surgery
2060
CANCER November 15, 1999 / Volume 86 / Number 10
FIGURE 1. Protocol for management of patients with carcinoma of the cervix.
GOG: Gynecolgic Oncology Group; RT: radiotherapy. Reproduced with permission from Hacker WF, Wain GV, Nicklin JL. Resection of bulky positive lymph
nodes in patients with cervical carcinoma. Int J Gynecol Cancer 1995;5:250 –7.
and radiotherapy also are used frequently, although
specific protocols vary considerably.
Our current protocol for the treatment of patients
with Stage IB cervix carcinoma has been reported
previously (Fig. 1).2 In general, all medically fit patients undergo primary radical hysterectomy with bilateral pelvic lymph node dissection regardless of the
diameter of the cervix or the patient’s age.
According to the Annual Report on Treatment for
Gynecological Cancer,3 patients with positive pelvic
lymph nodes have a 5-year survival of 59% and are at
risk of both pelvic and distant recurrences. Retrospective studies4,5 suggest that adjuvant pelvic radiation in
this setting can reduce the risk of pelvic recurrence
after radical surgery by 30 – 40%. These same studies
fail to demonstrate an impact on overall survival due
to the inability of adjuvant pelvic radiation to influence distant metastases. Improvement in survival for
this group of patients awaits the development of effective chemotherapeutic regimens.
The situation with respect to lymph node negative
patients is different. Overall 5-year survival is 89%
after radical hysterectomy and pelvic lymph node dissection.3 However, this group contributes about 50%
of the treatment failures, the majority of these which
(70%) occur in the pelvis.6 – 8 This makes it attractive
theoretically to offer adjuvant pelvic radiation to the
lymph node negative patients who are at high risk of
local recurrence, because there should be a realistic
expectation of improving overall survival by decreasing the pelvic recurrence rate.6,9,10
Two problems have to be addressed before implementing such a strategy. The first is to identify the group
of lymph node negative patients who are at high risk of
recurrence so that the others can be spared adjuvant
therapy. This was achieved in the prospective surgicalpathologic study performed by the Gynecologic Oncology Group (GOG)11 in which 645 patients with Stage IB
cervical carcinoma underwent surgery and were observed prospectively for 5 years without receiving adjuvant treatment. Of these patients, 545 had a negative
lymph node status, whereas microscopic metastatic disease in the pelvic lymph nodes was identified in the
remaining 100 patients. Patients with macroscopic involvement of the pelvic or paraaortic lymph nodes were
excluded. Three independent prognostic variables (clinical tumor size, depth of tumor penetration, and presence of lymph-vascular space invasion [LVSI]) were
identified, and the GOG developed a scoring system to
allow relative risk of recurrence to be quantified. A GOG
score $ 120 correlated with a 40% risk of recurrence,
which clearly would justify consideration of adjuvant
therapy11 (Fig. 2).
The second problem relates to the high rate (5 to
10%) of major complications associated with adjuvant
pelvic radiation after radical hysterectomy and pelvic
lymph node dissection. Radiation morbidity is correlated highly with the radiation target volume.9,12,13 A
clinical review of our own experience with Stage IB
lymph node negative cervical carcinoma showed that
87% of recurrences occurred in the central pelvis (vaginal vault or paravaginal soft tissues). Therefore, there
seemed to be little benefit in extending the upper
border of the treatment field to lumbar segments 4 –5
(L4 –L5) as in the standard field approach. By using a
smaller target volume focused on the central pelvis
(small pelvic field; Table 1, Fig. 3), we hoped to decrease the incidence of pelvic recurrence while reducing the subsequent morbidity.
After the 1990 GOG study,11 we developed a
protocol to select high risk patients with Stage IB,
lymph node negative cervix carcinoma on the basis
of a GOG score $ 120. All identified patients were
offered adjuvant external beam small field pelvic
radiation. This article reports the preliminary results
of our protocol.
MATERIALS AND METHODS
Between May, 1991 and September, 1995, 123 patients
with Stage IB carcinoma of the cervix were treated in
our institution with primary radical hysterectomy and
bilateral pelvic lymph node dissection. The procedures were performed by one of the gynecologic oncologists, either assisted by or supervising a gynecologic oncology fellow. A negative lymph node status
was confirmed in 92 cases. By using the GOG protocol
(Fig. 2),11 a GOG score was calculated for each of these
patients by multiplying the three relative risk scores
Treatment of Stage IB Cervix Carcinoma/Kridelka et al.
2061
FIGURE 2.
Disease free interval by
relative risk group for patients with
Stage IB carcinoma of the cervix. Reproduced with permission from Delgado G,
Bundy B, Zaino R, Sevin BU, Creasman
WT, Major F. Prospective surgicalpathological study of disease-free interval in patients with Stage 1IB squamous
cell carcinoma of the cervix: a Gynecologic Oncology Group study. Gynecol Oncol 1990;38:352–7.
TABLE 1
Anteroposterior and Lateral Portals of Pelvic Radiation: Standard
Field versus Small Field
Portal
Anteroposterior
Superior
Inferior
Lateral
Lateral
Anterior
Posterior
Standard field
Small field
L4–L5 junction
Inferior obturator foramen
1.5 cm lateral to pelvic
brim
S1–S2 junction
Midobturator foramen
Follows bony pelvic brim
Outer edge of pubic
symphysis
Ischial tuberosities
1 cm posterior to pubic
tubercule
Anterior sacral plane
L4–L5: lumbar spinal segments 4–5; S1–S2: sacral spinal segments 1–2.
associated with clinical tumor size, depth of tumor
penetration, and presence or absence of LVSI.
Clinical tumor size was noted preoperatively. The
depth of invasion was measured from the basement
membrane of the surface epithelium to the deepest
point of invasion. The presence of tumor cells within
endothelial-lined spaces was reported as LVSI positive. Additional information (number of lymph nodes
resected, histologic grade of differentiation) was recorded. Although this study was prospective, all 92
cases were reviewed by one pathologist (L.S.E.) to
verify the histopathologic risk factors. The pathologist
was blinded to the outcome of the patients.
Twenty-five lymph node negative patients were
considered at high risk of pelvic recurrence on the
basis of their GOG scores (.120). All received adjuvant
small field of pelvic radiation. Their mean age was 47
FIGURE 3. Anteroposterior portals for pelvic radiation: standard field versus
small field.
years (range, 33– 82 years). The histology was reported
as squamous cell carcinoma in 20 cases and adenosquamous in 5 cases. The number of lymph nodes
removed at the time of radical hysterectomy ranged
from 11 to 55, with an average count of 30.52 lymph
nodes. The tumor was moderately differentiated
(Grade 2) in 15 cases and poorly differentiated (Grade
3) in 10 cases. The mean tumor size was 32 mm (range,
20 – 60 mm), and all tumors invaded to the outer onethird of the cervical wall. LVSI was positive in all but 1
patient in whom the GOG score reached 145 on the
basis of a 4-cm tumor invading 20 mm through a
cervical stroma that measured 27-mm thick. The
2062
CANCER November 15, 1999 / Volume 86 / Number 10
FIGURE 4. Disease free interval for
high risk patients (relative risk . 120)
with Stage IB carcinoma of the cervix:
adjuvant small field pelvic radiation versus observation.
mean GOG score for the group was 166 (range, 120 –
263).
The median time from surgery to commencement
of radiation treatment was 6 weeks (range, 4 –12
weeks). The objectives and potential risks of our protocol were discussed with each patient, and all consented to receive adjuvant small field pelvic radiation.
Table 1 and Figure 3 compare the anteroposterior
and lateral portals of the small pelvic field with those
of the standard pelvic field. The total dose delivered
was 50.4 grays (Gy) in 28 fractions (1.8 Gy per fraction)
using a four-field technique.
In patients who experienced a recurrence, the site
of recurrence was noted. A 5-year disease free survival
(DFS) curve was generated by using the Kaplan–Meier
formula. In comparing the 5-year DFS curve of the
small field group with the 5-year DFS curve of the
corresponding high risk patients from the GOG study
who were observed postoperatively, we calculated an
“estimated” log-rank P value (est P value). This was
based on measuring disease free rates from an enlargement of the GOG disease free interval curve at
each of the 13 relevant distinct times for which a
censored time occurred prior to 43 months and, in our
study group, at 14 months, the time at which 1 patient
experienced a recurrence. In the GOG group, we assumed that there were no censored times prior to the
last observed recurrence. This latter assumption appears to be correct, because the actuarial disease free
rate after the last observed recurrence corresponds
closely to the crude disease free rate (83 of 141 patients; 59%). Treatment-related, long term complications of the Small Field technique were recorded.
Another group of 17 patients with Stage IB, lymph
node negative cervical carcinoma was treated in our
department between 1987 and 1990 with primary radical surgery followed by adjuvant standard field pelvic
radiation. During that period, the indication for adjuvant radiation was a combination of high risk variables
(clinical tumor size . 4 cm, presence of LVSI, deep
tumor penetration, disease free margin , 2 mm). The
mean total dose was 51 Gy (range, 45–55 Gy) delivered
in 1.8-Gy fractions using a four-field technique. The
long term morbidity experienced by the patients who
received adjuvant standard field pelvic radiation was
compared with that of the patients who received adjuvant small field pelvic radiation.
RESULTS
For the 25 patients who received adjuvant small field
pelvic radiation, the mean follow-up was 32 months
(range,12– 60 months). No patient was lost to followup. There was one recurrence (5%) at 16 months. This
patient initially suffered a poorly differentiated (Grade
3) squamous cell carcinoma of the cervix. Recurrent
disease was present within the previously irradiated
field but also outside the radiation field along the
small bowel mesentery, causing both small bowel and
bilateral ureteric obstruction. The patient died at 24
months after initial diagnosis.
Comparison of the 5-year DFS curve of the high
risk, lymph node negative patients who were treated
with adjuvant small field pelvic radiation with the
5-year DFS curve of the corresponding high risk GOG
patients who were treated with observation only after
radical surgery is shown in Figure 4. A log-rank anal-
Treatment of Stage IB Cervix Carcinoma/Kridelka et al.
TABLE 2
Long Term Radiation Morbidity: Comparison of Standard and Small
Pelvic Fields
Long term radiation
morbidity/site
Major
Bowel obstruction
Total
Minor
Leg lymphedema
Rectal incontinence
Intermittent diarrhea
Total
Standard field
(17 patients)
Small field
(25 patients)
2 (11%)
2 (11%)
0
0
2
0
1
3 (17%)
3
1
0
3 (16%)
ysis confirms a statistically significant improvement in
the DFS for the patients who were treated with small
field pelvic radiation (est P value 5 0.005).
The acute morbidity of the small field treatment
was mild, and, in all cases, radiotherapy was completed without interruption. Table 2 compares the
long term major morbidity of adjuvant small field
radiation with that of adjuvant standard field radiation
for patients at our institution.
In the small field group, four minor, long term
complications occurred. Three patients developed
mild leg lymphedema, although none of these patients
experienced recurrent local cellulitis. The fourth patient, who reported mild rectal incontinence prior to
surgery, believed that the symptoms had worsened
somewhat. No case of major morbidity was recorded.
Of the 17 Stage IB, lymph node negative patients
who received adjuvant standard field pelvic radiation
between 1987 and 1990, 2 patients (11.7%) experienced major morbidity according to the European
Organization for Research and Treatment of Cancer
(EORTC)/Radiation Therapy Oncology Group (RTOG)
criteria of radiation morbidity. Both patients developed a bowel obstruction. This required ileal resection
in one patient and ileal resection and end colostomy
in the other. An additional patient had significant
vaginal stenosis and did not resume intercourse after
treatment. Minor morbidity was experienced by three
other patients. This included two patients with mild
lymphedema and one patient with intermittent diarrhea.
DISCUSSION
Patients with Stage IB, lymph node negative cervical
carcinoma traditionally are observed without adjuvant
treatment after radical hysterectomy and pelvic lymph
node dissection. However, there is increasing evidence that a subgroup of these patients is at high risk
of recurrence9 –11 and that the recurrences occur pre-
2063
dominantly in the pelvis.6 – 8 Nevertheless, experience
with adjuvant pelvic radiation for such patients remains limited.
Fioricca et al.9 reported 33 patients who received
adjuvant standard field pelvic radiation because of the
presence of one or more of the following high risk
factors: large tumor volume, deep stromal invasion,
presence of LVSI, or extension to the lower uterine
segment. A mean total dose of 47 Gy (range, 44.8 –55
Gy) in 1.8-Gy fractions was delivered. Local control of
disease was achieved in 32 of 33 patients (96.9%), but
3 patients (9%) experienced major gastrointestinal
morbidity. Similar results were reported recently by
Takamura et al.10 in a study in which 70 patients with
lymph node negative, Stage I and II cervical carcinoma
with histologically confirmed parametrial extension
received adjuvant standard field pelvic radiation to a
total dose of 50 Gy in 2-Gy fractions. Local control was
achieved in 66 of 70 patients (94%). Twenty-eight
(40%) complications requiring medical treatment occurred (leg edema in 20 patients, bowel obstruction in
2 patients, rectal bleeding in 3 patients, and hemorragic cystitis in 3 patients). Six of the 66 patients (9%)
who were treated developed major complications requiring further surgery (bowel obstruction in 5 patients, femoral neck fracture in 1 patient).
Our experience with adjuvant standard field pelvic radiation for patients with Stage IB, lymph node
negative cervical carcinoma (1987–1990) was similar.
Pelvic disease recurred in 2 of 17patients (11.7%), and
major bowel complications occurred in 2 patients
(11.7%; EORTC/RTOG criteria for radiation morbidity). In addition, 1 patient developed severe vaginal
stenosis. It must be emphasized that the latter observations are based on limited numbers of patients (n 5
17). Therefore, suggestions regarding the relative efficacy of adjuvant standard field and small field radiation must be confirmed. The combined results of
these three studies show that pelvic disease was controlled in 92% of patients (111 of 120) but that 9.2% of
patients (11 of 120) suffered major complications.
More recently, Sedlis et al.14 presented the early
data from a GOG study that included 277 patients with
Stage IB carcinoma of the cervix and with at least two
of the following risk factors: large tumor size, deep
(greater than one-third) stromal invasion, or the presence of LVSI. After radical hysterectomy, these patients were assigned randomly to receive no further
treatment (140 patients) or to receive adjuvant standard field pelvic radiation to a dose of 50.4 Gy (137
patients). Although conclusions regarding overall patient survival await further follow-up, this preliminary
analysis showed that adjuvant standard field pelvic
radiation reduced the risk of recurrence by 44%, but it
2064
CANCER November 15, 1999 / Volume 86 / Number 10
was associated with a 5.8% incidence of severe (Grade
3 and 4) urologic and gastrointestinal morbidity. This
suggests that adjuvant pelvic radiation may have a
significant role to play in the treatment of patients
with early stage, high risk, lymph node negative cervical carcinoma if a reproducible method for identifying such patients could be developed and if radiation
morbidity (in particular, gastrointestinal morbidity)
could be reduced.
By using the score defined by Delgado et al. in the
GOG study,11 we have standardized our selection criteria. Patients with a GOG score $ 120, which carries
a 5-year recurrence risk of 40%, were offered adjuvant
pelvic radiation.
To overcome the problem of morbidity, the small
field technique was designed with the aim of reducing
the volume irradiated without jeopardizing local disease control. A comparison of the standard field and
small field anteroposterior portals (Fig. 3) confirms
that the small field technique, although it targets a
significantly smaller volume, focuses on the area at
high risk of recurrence (vault and paravaginal soft
tissues).
The small field of pelvic radiation prevented pelvic recurrence in 24 of the 25 high risk patients (96%)
who were treated in our institution since 1991. This
translates into a significant improvement in DFS (est
log-rank P value 5 0.005) compared with the outcome
of patients who were treated by observation only in
the GOG study (GOG score . 120; Fig. 4).
At the same time, the long term complication rate
after adjuvant small field pelvic radiation remained
very low. Four cases of minor morbidity were recorded, and there was no case of major morbidity.
Most important, no case of major bowel morbidity
was observed. This marks a significant improvement
compared with the morbidity experienced by our patients when they were treated with adjuvant standard
field pelvic radiation. The reduction in the volume of
small bowel irradiated when using the small field technique is shown in comparative planning abdominopelvic X-rays after a barium meal and may explain
the low gastrointestinal morbidity of the small field
technique (Fig. 5). With a median follow-up of 32
months, it also is possible that major morbidity still
may occur in the future, and these patients will remain
under careful surveillance.
Despite the relatively limited numbers of patients
analyzed, this prospective pilot study suggests that an
adjuvant small field of pelvic radiation has the potential to decrease pelvic recurrence and significantly improve DFS for high risk patients with Stage IB, lymph
node negative cervix carcinoma who are treated primarily by radical hysterectomy and pelvic lymph node
FIGURE 5. Small bowel irradiation: standard field versus small field.
dissection. Morbidity of this treatment appears to be
acceptably low and significantly less than that associated with standard field pelvic radiation. If these pilot
data can be verified in other centers, then a randomized prospective study would be justified to determine
whether or not small field adjuvant pelvic radiation
should become part of the standard approach for
these high risk patients.
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