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Cancer

Volume 94, Issue 1
Original Article
Free Access

High‐dose‐rate versus low‐dose‐rate intracavitary therapy for carcinoma of the uterine cervix

A randomized trial

Masato Hareyama M.D.

Corresponding Author

E-mail address:hareyama@sapmed.ac.jp

Department of Radiology, Sapporo Medical University, School of Medicine, Sapporo, Japan

Fax: 011‐81‐11‐613‐9920
Department of Radiology, Sapporo Medical University, School of Medicine, S1W16, Chuo‐Ku, Sapporo, 060‐8543, Japan===
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Koh‐ichi Sakata M.D.

Department of Radiology, Sapporo Medical University, School of Medicine, Sapporo, Japan

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Atushi Oouchi M.D.

Department of Radiology, Sapporo Medical University, School of Medicine, Sapporo, Japan

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Hisayasu Nagakura M.D.

Department of Radiology, Sapporo Medical University, School of Medicine, Sapporo, Japan

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Mitsuo Shido M.D.

Department of Radiology, Sapporo Medical University, School of Medicine, Sapporo, Japan

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Masanori Someya M.D.

Department of Radiology, Sapporo Medical University, School of Medicine, Sapporo, Japan

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Kazumitsu Koito M.D.

Department of Radiology, Sapporo Medical University, School of Medicine, Sapporo, Japan

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First published: 28 December 2001
https://doi.org/10.1002/cncr.10207
Cited by: 81

Abstract

BACKGROUND

This was a prospective randomized clinical trial undertaken at our institution to compare low‐dose‐rate (LDR) intracavitary radiation therapy versus high‐dose‐rate (HDR) intracavitary radiation therapy for the treatment of cervical carcinoma.

METHODS

From January 1984 to December 1997, a total of 132 patients with Stage II or IIIB of invasive carcinoma of the uterine cervix were entered into this randomized study. Treatment arm by HDR or LDR was allocated according to the month of each patient's birth. External irradiation consisted of whole pelvis irradiation and pelvic irradiation. Doses of external irradiation for both groups were identical. The authors used 0.588 as the conversion factor of total intracavitary dose from LDR to HDR.

RESULTS

The 5‐year disease specific survival rates of Stage II and III patients treated with HDR were 69% and 51% whereas those with LDR were 87% and 60%, respectively. The 5‐year pelvic recurrence free survival rates of Stage II and III patients treated with HDR were 89% and 73% whereas those with LDR were 100% and 70%, respectively. There was no significant difference in disease specific survival or pelvic recurrence free survival rates between HDR and LDR. The actuarial complication rate (Radiation Therapy Oncology Group Grade 3, 4, or 5) at 5 years was 10% in the HDR group and 13% in the LDR group, and the difference between the HDR and LDR groups was not statistically significant.

CONCLUSIONS

The pelvic control or actuarial complication rates were comparable between HDR and LDR treatment. The difference between the disease specific survival rates for HDR and LDR was not statistically significant for Stage II or III, although in Stage II, patients treated with LDR appeared to have a better survival rate than those treated with HDR. Cancer 2002;94:117–24. © 2002 American Cancer Society.

High‐dose‐rate (HDR) intracavitary radiation therapy for carcinoma of the uterine cervix has gradually found wider acceptance because of such advantages as the elimination of exposure of medical personnel to radiation, a short treatment period, and the possibility of treatment while patients are ambulatory.

There are nearly three decades of experience comparing HDR to LDR brachytherapy in the treatment of cervical carcinoma. However, controversy still persists regarding the efficacy and safety of HDR brachytherapy compared with low‐dose‐rate (LDR) brachytherapy.1 The literature supporting HDR brachytherapy in the treatment of cervical carcinoma derives primarily from retrospective series.2-8 There have been few randomized trials undertaken to compare LDR versus HDR intracavitary brachytherapy for the treatment of cervical carcinoma.

We present the results of a randomized prospective comparative study of HDR and LDR.

MATERIALS AND METHODS

From January 1984 to December 1997, a total of 151 patients with International Federation of Gynecology and Obstetrics Stage II or IIIB of invasive carcinoma of the uterine cervix were referred to the Department of Radiology, Sapporo Medical University Hospital and enrolled in this study.

The eligibility criteria were as follows: no previous operations; the external radiotherapy was performed in our institution; Stages II or IIIB, M0, and Karnofsky index greater than 50. Nineteen patients were excluded from this study because of previous surgery in 2 patients, the external radiotherapy performed in other institutions in 10 patients, and Karnofsky index less than 50 in 7 patients. Therefore, 132 of 151 patients were available for this study.

Treatment arm (HDR or LDR) was allocated according to the month of each patient's birth. Patients whose birth month was numerically odd were allocated to HDR, and those whose birth month was even to LDR. The treatment consisted of 60CO HDR for 61 patients and 137Cs LDR for 71 patients.

Patients were staged clinically on palpation, cystoscopy, and proctoscopy by both gynecologist and radiation oncologist without general anesthesia.

Distribution of patients into the stages and by median age into two groups is listed in Table 1. Treatment schedules of external and intracavitary irradiation are listed in Table 2 and Figure 1. Doses of external irradiation for both groups were identical.

Table 1. Clinical Stage According to the Classification of FIGO
Stage HDR LDR Total
II
 No. of patients 22 26 48
 Median age (range) 65 (45–81) 69 (48–84)
III
 No. of patients 39 45 84
 Median age (range) 64 (31–85) 57 (31–84)
Total 61 71 132
  • FIGO: International Federation of Gynecology and Obstetrics; HDR: high‐dose‐rate; LDR: low‐dose‐rate.
Table 2. Treatment Protocol for Cervical Carcinoma
Stage External irradiation Intracavitary irradiation
WP (Gy)a CS (Gy)a Doses to point A HDR (Gy/fraction) LDR
IIA 0 50 29/5 50/4
IIB 30 Involved side, 22 23/3 or 4 40/3
Uninvolved side, 20
III 40 Involved side, 14 17.3/2 or 3 30/3
Uninvolved side, 12
  • WP: whole‐pelvis field; Gy: gray; CS: pelvis field with central shielding; HDR: high‐dose‐rate; LDR: low‐dose‐rate.
  • a 2 Gy daily.
image
Figure 1
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Time schedule of intracavitary irradiation and external irradiation. (circles) whole pelvic irradiation; (double circles) parametrial irradiation; (stars) intracavitary irradiation. HDR: high‐dose‐rate; LDR: low‐dose‐rate.

External irradiation consisted of whole pelvis irradiation and pelvic irradiation, using a central shield during the latter half of the treatment with the anteroposterior parallel opposing technique. The external beam irradiation was performed with 2 grays (Gy) per fraction and 5 fractions per week. For external irradiation, the weight of whole‐pelvis irradiation was increased and that of intracavitary irradiation decreased for patients of a more advanced stage (Table 2). The timing of external beam radiotherapy and brachytherapy is shown in Figure 1.

External irradiation was delivered with a 10‐megavolt X‐ray except for in 2 patients who were treated with 60CO. We used 0.588 as the conversion factor of total intracavitary dose from LDR to HDR. We basically followed the system of Osaka University regarding the clinical procedures for HDR and LDR.9 The intracavitary treatment was performed with applicators of the modified Manchester system without general anesthesia. A set of Tazaki‐Arai‐Oryu applicators were used for LDR therapy. In HDR therapy, a Henschke‐type metal applicator was used. The LDR therapy was performed using a manual afterloading system. The time required for one treatment ranged from 20 to 30 hours. The HDR therapy was performed once a week during the course of external irradiation. The time required for one treatment was 15–20 minutes. The patients were treated in the supine position in LDR therapy and in the lithotomy position in HDR therapy. The geometry of two applicators of LDR and HDR was presented in the report by Shigematsu et al..9 There was no significant difference in dose distribution between LDR and HDR therapy in the cervical area.10

The severity of complication was classified according to the Radiation Therapy Oncology Group (RTOG)/European Organization for Research and Treatment of Cancer late radiation morbidity scoring scheme.11

The median follow‐up to last contact or death was 47 months, with a range of 6 to 138 months. The cutoff for analysis was August 2000. Patients alive at the cutoff date had a median follow‐up of 66 months, and all but one surviving patient had been observed for a minimum of 2 years. Two patients were lost to follow‐up, and they were considered for the statistical analysis as uncontrolled pelvic disease. Survival was calculated according to the Kaplan–Meier method,12 and statistical significance was determined by means of the generalized Wilcoxon test.

RESULTS

Disease Specific and Pelvic Recurrence Free Survivals

The disease specific survival rates for the HDR and LDR groups are shown in Figure 2. The 5‐year disease specific survival rates for the HDR group were 69% for Stage II and 51% for Stage III. The corresponding figures for the LDR group were 87% for Stage II and 60% for Stage III. The difference between the survival rates for HDR and LDR was not statistically significant for Stages II or III, although in Stage II, patients treated with LDR appeared to have a better survival rate than those treated with HDR.

image
Figure 2
Open in figure viewerPowerPoint

The disease specific survival rates of patients with carcinoma of the uterine cervix by stage and treatment group. HDR: high‐dose‐rate; LDR: low‐dose‐rate.

The pelvic recurrence free survival rates for HDR and LDR groups are shown in Figure 3. The 5‐year pelvic recurrence free survival rates for the HDR group were 89% for Stage II and 69% for Stage III. The corresponding figures for LDR groups were 100% for Stage II and 70% for Stage III. No significant differences could be found between the HDR and LDR pelvic control rates for Stages II and III.

image
Figure 3
Open in figure viewerPowerPoint

The pelvic recurrence free survival rates of patients with carcinoma of the uterine cervix by stage and treatment group. HDR: high‐dose‐rate; LDR: low‐dose‐rate.

Cause of Death and Patterns of Failure

In the HDR group, a total of 4 patients (6.6%) died from intercurrent diseases: cardiac failure (1 patient), senility (1 patient), cerebrovascular attack (1 patient), and cardiac infarction (1 patient). Twenty‐seven patients (44%) were classified as death from tumor.

In the LDR group, a total of 5 patients (7%) died from intercurrent diseases: complications of diabetes mellitus (1 patient), senility (1 patient), cerebrovascular attack (2 patients), and arterial embolism of the lower limbs (1 patient). One patient died from lung carcinoma. Twenty‐one patients (30%) were classified as death from tumor.

Patterns of failure were analyzed for 27 patients in the HDR and 21 patients in the LDR group whose sites of recurrence were evaluated at the last follow‐up (Table 3). The most common pattern of failure was distant metastasis in both groups (HDR, 25%; LDR, 24%). The next most common pattern of failure was pelvic recurrence (HDR, 18%; LDR, 13%). Paraaortic lymph node metastasis was noted in 10% in the HDR group and in 11% in the LDR group. Thus, there was no significant difference in the pattern of failure between the two groups.

Table 3. Patterns of Failure in Patients with Carcinoma of the Uterine Cervix by Stage and Treatment
Stage No. of patients Pattern of failure (%)
CR/PR PALN DM Total
HDR
 II 22 2 (9) 3 (14) 5 (23) 7 (31)
 III 39 9 (23) 3 (8) 10 (26) 20 (51)
 Total 61 11 (18) 6 (10) 15 (25) 27 (44)
LDR
 II 26 0 (0) 0 (0) 3 (12) 3 (12)
 III 45 9 (20) 8 (18) 14 (31) 18 (40)
 Total 71 9 (13) 8 (11) 17 (24) 21 (30)
  • CR: central recurrence; PR: peripheral recurrence; PALN: paraaortic lymph node metastasis; DM: distant metastasis; HDR: high‐dose‐rate; LDR: low‐dose‐rate.

Complications

The incidence of moderate to severe late complications requiring treatment (RTOG Grade 3, 4, or 5) is listed in Tables 4 and 5.

Table 4. Actuarial Complications (Grade ≥ 3) by Stage at 5 Years
HDR vs. LDR Patient no. Complications Grade ≥ 3 (%)
Overall
 HDR 61 10
 LDR 71 13
Stage II
 HDR 22 5
 LDR 26 12
Stage III
 HDR 39 7
 LDR 45 13
  • HDR: high‐dose‐rate; LDR: low‐dose‐rate.
Table 5. Actuarial Complications (Grade ≥ 3) by Organ Site at 5 Years
Rate Patient no. Overall (%) Rectum (%) Small bowel (%) Bladder (%)
HDR 61 10 3.5 2.4 4.0
LDR 71 13 8.7 1.6 7.5
  • HDR: high‐dose‐rate; LDR: low‐dose‐rate.

Table 4 indicates the complication rate by stage at 5 years in the LDR and HDR groups. The overall actuarial complication rate at 5 years was 10 % in the HDR group and 13% in the LDR group, and the difference between groups was not statistically significant. Although the actuarial complication rate of the LDR group appeared to be higher than that of the HDR group for Stages II and III, there was no statistically significant difference between them.

Five‐year complication rates in the HDR and LDR patients by organ site are shown in Table 5. Although the actuarial complication rate of the LDR group appeared to be higher than that of the HDR group for rectum and bladder, there were no statistically significant differences between HDR and LDR patients in these rates.

DISCUSSION

The use of HDR has increased rapidly for the treatment of carcinoma of the uterine cervix in Japan. Many reports already have been published about the usefulness of HDR for uterine carcinoma, and the results have been comparable with those of classic LDR.2-8, 10, 13

However, as far as we are aware, there have been only two randomized studies comparing HDR with LDR brachytherapy in the treatment of cervical carcinoma. One was the study of Osaka University.9, 10 However, in this study there was a selection bias resulting from the finding that although patients were supposed to have been allocated to a therapy arm according to their registration number from 1975, in fact, some patients assigned to the LDR arm were selected for treatment with HDR because of inadequate availability of isotope beds. There was no significant difference in 5‐year cause specific survival between those treated with the HDR versus LDR for each stage of disease in their study in their study. Patterns of failure were similar with the exception of Stage III patients who had a higher pelvic failure rate when treated with LDR compared with HDR brachytherapy (46% vs. 33%). However, moderate to severe complications were higher in the HDR group (10% vs. 4%).

The other randomized study from India reported no significant difference in 5‐year survival or pelvic control rates between the two modalities of brachytherapy.13 The significant complication rate was higher in the LDR arm (2.4% vs. 0.4%). However, the randomization process was not detailed in the report.

The remainder of the studies comparing HDR to LDR are retrospective. There may be a potential bias in their reports because older results of LDR treatment were used as historical controls whereas results of HDR were based on improvements in modern radiologic imaging (computed tomography, magnetic resonance imaging, and ultrasound) for determination of tumor volume and extent of disease, or other factors that may have contributed to an improved survival rate for their results of HDR.

Three studies have been published that have summarized the cervical HDR/LDR literature.14-16 They all suggest that HDR brachytherapy produces similar results to LDR brachytherapy. However, none of these reports is a formal meta‐analysis of the raw data, and the strengths of the conclusions are limited.17

A worldwide analysis by Orton et al. showed better clinical results for HDR than for LDR intracavitary radiation therapy. Morbidity rates were considerably lower for HDR.16 However, their report was criticized because it contained no information about the handling of patients lost to follow‐up, possible selection factor, or methods of analysis used by the individual institutions to obtain their data. Eifel commented that some of the LDR results used in the comparison are very poor, with complication rates several times higher than those described by Fletcher or Perez.1

This report demonstrated the results of a prospective randomized clinical trial undertaken at our institution to compare LDR intracavitary radiation therapy versus HDR intracavitary radiation therapy for the treatment of cervical carcinoma with Stage II or IIIB. We performed intracavitary radiation therapy to obtain the similar dose distribution between LDR and HDR therapy in the cervical area. We also made the time schedule of intracavitary irradiation and external irradiation to begin LDR or HDR intracavitary irradiation at the similar timing during or after external irradiation. However, we classified patients by clinical stage, but did not by tumor size. The correlation between size and outcome was found in patients with cervical carcinoma treated with radiotherapy.18-20 The method of randomization in our study may not be optimal because this results in an imbalance in the number of patients with more patients being assigned to the LDR group.

The disease specific survival rates and pelvic control rates after HDR or LDR in our series were comparable to or better than reports in the literature from other institutions using LDR and HDR.10, 13, 21-23 No significant differences could be found between the HDR and LDR pelvic control rates for Stages II and III in our results.

Disease specific survival rates for the HDR and LDR groups showed no significant differences either. However, in Stage II, patients treated with LDR appeared to have a better disease specific survival rate than those treated with HDR, although no conclusion could be reached because of the low number of patients. In such level as disease specific survival rates in Stage II of our results, a total of 124 patients (62 in each arm) would be required to detect a 20% difference between HDR and LDR with 0.8 power and 0.05 type error. Therefore, there might well be a significant difference, but we might be unable to detect it. The incidences of central and/or peripheral recurrence and distant and paraaortic lymph node metastasis tended to be a little higher in patients with Stage II disease treated with HDR. However, the reasons for this were unknown.

Patterns of failure for the two groups were similar. The incidence of central and/or peripheral recurrence and distant metastasis increased in accordance with the stage. Our study revealed a lower incidence of central and/or peripheral recurrence than other reports. The incidence of paraaortic lymph node metastasis and distant metastasis was comparable to that of other reports.24

We consider that the incidence of late complications requiring treatment in our series was within acceptable levels because the reported incidence of complications after LDR therapy ranged from 5% to 20%. The Patterns of Care Studies reported significant actuarial complications in approximately 10%, 15%, and 20% for Stages IB, IIB, and IIIB, respectively.22 Only 2 of the 24 series analyzed reported complication rates by the actuarial method.6, 25 The remaining series used the crude method of reporting complications, which can result in gross underestimations of the true incidence of complications.

In our series, the incidence of late complications appeared to be more frequent in the LDR group than in the HDR group although there were no significant differences between them (Tables 4 and 5). There have been many reports comparing the incidences of late complications of HDR with those of LDR; however, the results are conflicting. Some reported that the incidence was similar,3, 7, 8, 26 and others reported that LDR had a higher incidence,2, 5, 13, 16, 27, 28 and still others reported that HDR had the higher incidence.10, 29 Osaka University reported that the incidence of complications was higher for the HDR group than for the LDR group although cause specific survivals were equivalent. However, they used fewer doses of whole pelvis irradiation and more doses of intracavitary irradiation than we did. When differences in the doses of external irradiation and intracavitary irradiation such as these exist, it is difficult to compare the treatment results of different institutions.

The timing of external beam radiotherapy and brachytherapy may be also important. Petereit et al. reported that a similar outcome was observed for Stage IB and II patients treated with either HDR or LDR brachytherapy. However, poorer survival and pelvic control rates were observed for Stage IIIB patients treated with HDR brachytherapy. The first HDR implant was initiated as soon as possible whereas the first LDR brachytherapy began after external radiotherapy was given to the whole pelvis. They claimed that most external beam radiotherapy should be delivered before initiating the brachytherapy if HDR is used for Stage IIIB patients.30

High‐dose‐rate fractionation schedules reported in the literature vary markedly. Point A fraction sizes range from 2–7 and 3–14 Gy, respectively. The optimal fractionation schedule for treating cervical carcinoma by using HDR brachytherapy is still unknown. In an attempt to determine whether an optimal HDR schedule exists, Petereit and Pearcey analyzed the fractionation schedule reported to have been used in 24 studies using the linear quadratic model to determine if doses can be correlated with local control and complications rates for each stage of cervical carcinoma.17 However, they could not identify a dose–response relation between complications and Point A Gy3s. They claimed that this was because of the poor quality of the current HDR brachytherapy literature. Most of the HDR publications report inadequate details of the dose fractionation schedules and only a few publications report significant complications by using the actuarial method. The authors claimed that currently, reasonable fractionation schedules probably should be based on single‐institution experience with accurate reporting. Further studies therefore are required to elucidate the optimal HDR fractionation schedule.

In the current study, no significant differences could be found between the HDR and LDR pelvic control rates for Stages II and III in our randomized trial. The difference between the survival rates for HDR and LDR was not statistically significant for Stage II or III, although in Stage II, patients treated with LDR appeared to have a better survival rate than those treated with HDR. The overall complication rate at 5 years was 10% in the HDR group and 13% in the LDR group, and the difference between the HDR and LDR groups was not statistically significant.

Notes :

  • 1 Fax: 011‐81‐11‐613‐9920
  • FIGO: International Federation of Gynecology and Obstetrics; HDR: high‐dose‐rate; LDR: low‐dose‐rate.
  • WP: whole‐pelvis field; Gy: gray; CS: pelvis field with central shielding; HDR: high‐dose‐rate; LDR: low‐dose‐rate.
  • a 2 Gy daily.
  • CR: central recurrence; PR: peripheral recurrence; PALN: paraaortic lymph node metastasis; DM: distant metastasis; HDR: high‐dose‐rate; LDR: low‐dose‐rate.
  • HDR: high‐dose‐rate; LDR: low‐dose‐rate.
  • HDR: high‐dose‐rate; LDR: low‐dose‐rate.

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