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10.1245/ASO.2005.05.020
Annals of Surgical Oncology 12:332-337 (2005)
© 2005 Society of Surgical Oncology
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Original Article

Results of Hysterectomy in Patients With Bulky Residual Disease at the End of Chemoradiotherapy for Stage IB2/II Cervical Carcinoma

Elie Azria, MD1, Philippe Morice, MD1, Christine Haie-Meder, MD2, Anne Thoury, MD1, Patricia Pautier, MD3, Catherine Lhomme, MD3, Pierre Duvillard, MD4 and Damienne Castaigne, MD1

1 Department of Surgery, Institut Gustave Roussy, 39 Rue Camille Desmoulins, 94805 Villejuif, France
2 Department of Radiation Therapy, Institut Gustave Roussy, 39 Rue Camille Desmoulins, 94805 Villejuif, France
3 Department of Medical Oncology, Institut Gustave Roussy, 39 Rue Camille Desmoulins, 94805 Villejuif, France
4 Departments of Pathology, Institut Gustave Roussy, 39 Rue Camille Desmoulins, 94805 Villejuif, France

Correspondence: Address correspondence and reprint requests to: Philippe Morice, MD; E-mail: morice{at}igr.fr.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: We assessed the clinical outcome after hysterectomy in patients with bulky residual disease after chemoradiotherapy for stage IB2/II cervical carcinoma.

Methods: Subjects were 10 patients who had bulky (>2 cm) residual disease in the cervix after external radiotherapy (45 Gy) combined with concomitant chemotherapy (cisplatin 40 mg/m2/week) and uterovaginal brachytherapy (15 Gy).

Results: Extrafascial hysterectomy was performed in three patients, type II radical hysterectomy was performed in six patients, and pelvic exenteration was performed in one patient. Pelvic lymphadenectomy was performed in eight patients, and para-aortic lymphadenectomy was performed in eight. Five patients had nodal involvement (pelvic nodes in four and para-aortic nodes in four), and six had lymphovascular space involvement. Surgical margins were free in nine patients. Seven patients developed grade 2 (n = 3) and/or grade 3 (n = 4) complications. The median duration of follow-up after surgery was 22 months (range, 1–37 months). With follow-up available in nine patients, seven relapsed, and only two remained disease free.

Conclusions: This series confirms the high rate of nodal spread in patients with bulky residual cervical disease after chemoradiotherapy. Furthermore, patients who underwent hysterectomy had a high complication rate. Only two patients are alive and disease free. The results of surgery are disappointing; surgery does not seem to improve the survival of these patients.

Key Words: Cervical cancer • Completion surgery • Chemoradiotherapy • Morbidity


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Cervical cancer is a worldwide health problem. It is the second most common cancer among women after breast cancer1 and is a major cause of mortality worldwide, especially in the developing countries, where screening is not as effective as in developed countries. Despite the availability of cervical cytology screening in developed countries and the fact that it has greatly reduced the incidence of invasive cervical cancer, locally advanced cervical cancer remains a major problem for oncologists, who continue to search for new, more effective treatments.

The treatment of bulky cervical cancers (tumor size >4 cm) has been radically clarified during last 10 years. Two management options are proposed: chemoradiotherapy (CRT) or neoadjuvant chemotherapy (NCT). A European randomized study comparing CRT and NCT in cervical carcinoma is ongoing. Nevertheless, CRT is considered the standard treatment for bulky cervical cancer (stage IB2 or higher according to the International Federation of Gynecology and Obstetrics [FIGO] classification) by many North American and Western European teams. Radical surgery is systematically performed after neoadjuvant treatment in patients who receive NCT. In patients treated with CRT, the role of what is considered as completion surgery and which procedures ought to be used after radiotherapy remain unclear. In the literature, very few data are available about the results of completion surgery in patients who still have a bulky cervical tumor at the end of CRT. To study the results of completion surgery, we decided to conduct a retrospective analysis to evaluate patient outcomes after pelvic surgery, which, in theory, is justified in patients with bulky residual disease at the end of radiotherapy.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Data concerning 75 women treated with CRT followed by pelvic surgery for locally advanced cervical cancer between January 1999 and October 2002 were reviewed. The patients retained for this analysis had stage IB2 or II disease according to the 1995 FIGO classification and a histological subtype of squamous cell carcinoma or adenocarcinoma or an adenosquamous tumor (all slides were reviewed by the same pathologist). All patients underwent an initial chest radiograph and an abdominopelvic magnetic resonance imaging (MRI) or pelvic MRI with an abdominopelvic computed tomography (CT) scan. The tumor size was evaluated at clinical examination and on MRI. Patients had to show an absence of metastatic disease on chest radiograph or on initial abdominopelvic MRI or CT scan and an absence of radiological bulky para-aortic nodes. Treatment was based on external pelvic radiotherapy (45 Gy) combined with concomitant chemotherapy (cisplatin 40 mg/m2/week) followed by uterovaginal low-dose-rate brachytherapy. The brachytherapy dose was 15 Gy, according to the International Commission on Radiation Units recommendations,2 which take into account the initial tumor extension at the time of diagnosis and use MRI at the time of brachytherapy with the vaginal mold in place to accurately define the target to be treated, taking into account the doses to critical organs (mainly the bladder and rectum). With this technique, 30 to 40 Gy was delivered at point A. All patients underwent at least an extrafascial hysterectomy; the radicality of the parametrial dissection was classified according to the Piver classification.3 The presence at the end of radiotherapy of a macroscopic residual cervical tumor measuring at least 2 cm (evaluated within a minimum of 6 weeks after the end of brachytherapy) and confirmed during the histological analysis was also required.

Patients were excluded from this series for at least one of the following reasons: 1) other histological subtypes (small-cell carcinoma, clear-cell carcinoma, melanoma, or sarcoma); and/or the absence of an initial MRI; 2) delivery of external radiotherapy in a dose <45 Gy and/or combined with cisplatin administered at a dose exceeding or less than 40 mg/m2/week; 3) concomitant chemotherapy combining two drugs; 4) CRT delivered to the pelvic and para-aortic area; 5) the absence of pelvic surgery; 6) the absence of residual cervical disease or the presence of minimal residual disease (<1 cm) during the histological analysis or the presence of residual disease in the form of metastatic lymph node(s) without residual disease in the cervix.

Patient characteristics, complications, and recurrences were studied. Complications were classified according to the Franco-Italian glossary.4 Survival curves were determined by using the Kaplan-Meier method.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Twelve patients had bulky cervical residual disease at the end of CRT. One patient had peritoneal carcinomatosis discovered at the time of completion surgery (the hysterectomy was therefore not performed). Another patient underwent the surgical procedure outside of our institution, and complete data concerning the surgical procedure, histological results, and postoperative outcomes were unavailable. Only 10 had complete data comprising the 7 criteria described in the Patients and Methods section.

The characteristics of these 10 patients are listed in Table 1Go. The median age was 49 years (range, 28–73 years). Six of the 10 patients were postmenopausal at the time of the diagnosis. The median tumor size was 6 cm (range, 4–9 cm). The histological diagnosis was a squamous cell carcinoma in eight cases and a cervical adenocarcinoma in two cases (patients 1 and 10).


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  		TABLE 1. Characteristics of 10 patients
 
According to the FIGO classification, two patients had stage IIA and eight had stage IIB disease. The initial lymph node status was determined by pelvic and abdominal MRI or CT scan. Five patients were considered as having suspicious pelvic nodes before treatment, and two had small (<1 cm) para-aortic nodes.

Concerning CRT, the median number of fractions of external irradiation was 24, and the median total duration of external irradiation was 36 days. Two patients received a lateral pelvic radiation boost of 8 and 10 Gy because they had bulky nodes.

The surgical procedure was performed with a median interval of 49 days (range, 42–64 days) after the end of brachytherapy. Three patients underwent an extrafascial hysterectomy (patients 2, 3, and 9), six underwent a type II radical hysterectomy (patients 1, 5, 6, 7, 8, and 10), and one underwent a total pelvic exenteration (with end-to-end anastomosis; patient 4). Eight patients underwent a pelvic lymphadenectomy, and eight underwent a para-aortic lymphadenectomy according to a previously described procedure.5

All patients had a residual cervical tumor ≥2 cm after measurement on the pathology specimen. All patients but one had negative surgical margins. The patient in whom resection was incomplete underwent a type II radical hysterectomy with both a pelvic and para-aortic lymphadenectomy. The vaginal margins of resection were invaded by disease. Five patients had at least one metastatic lymph node. Four patients had pelvic lymph node involvement (among them, only one positive node was located in the external iliac group). Four patients had para-aortic lymph node involvement (among them, one had isolated involvement in this area). Two of them had small nodes in the para-aortic area on initial MRI or CT scan. Consequently, three patients had nodal involvement in pelvic and para-aortic areas. Among patients with metastatic lymph nodes, capsular rupture was found in four cases. The numbers of positive nodes in patients with para-aortic involvement were 4 of 10 removed, 24 of 31 removed, 4 of 5 removed, and 7 of 10 removed. Lymphovascular space involvement was observed in six patients. In all cases, peritoneal cytology was free of malignant cells. None of the patients with nodal involvement undergoing complete dissection of the para-aortic area underwent postoperative para-aortic radiotherapy (to decrease the risk of bowel complications), but three patients received adjuvant platinum-based chemotherapy.

A total of 13 grade 2 or 3 complications (according to the Franco-Italian glossary-4) were observed in 7 patients. We documented 4 grade 3 complications (two ureteral fistulas that necessitated permanent stenting, a severe pulmonary embolism, and a rectovaginal fistula requiring a permanent colostomy in the patient who underwent pelvic exenteration) and 9 grade 2 complications (drained lymphocysts [n = 2], iliac phlebitis [n = 1], ureteral stenosis requiring transient stenting or a surgical procedure [n = 4], bladder retention requiring catheterization [n = 1], and postural incontinence of the bladder [n = 1]).

The median duration of follow-up after surgery was 22 months (range, 1–37 months). One patient was lost to follow-up 1 month after the surgical procedure. Figure 1Go shows the survival curve. Disease recurred in seven patients, mostly at a distant site (Table 1Go). Only one patient (the only one with involved margins) had a massive pelvic recurrence that invaded the vagina, bladder, and lateral pelvic walls, 6 months after the surgical procedure. The median time to recurrence was 16 months (range, 6–32 months).



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  		FIG 1. Event-free (Kaplan-Meier) survival curve.

 
Among the four patients with a recurrence located at least in the para-aortic node group, all had a lymphadenectomy at this level. The histological examination revealed positive nodes with capsular rupture (three patients underwent chemotherapy after the surgical procedure).

Four patients died as a result of their disease. The median interval between the diagnosis of recurrence and death was 6 months (range, 2–14 months). The median progression-free survival was 18 months (range, 6–34 months). The median overall survival was 24 months (range, 9–37 months). Only two patients are alive without recurrence, 27 and 19 months after the end of treatment.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Combining concomitant chemotherapy with external radiotherapy affords a benefit of 16% for progression-free survival compared with treatment with external radiotherapy alone, particularly in patients with stage IB2 or II cervical carcinoma.6 Overall and progression-free survival are improved, with fewer local and distant recurrences.6 Radiotherapy plus cisplatin-based chemotherapy have been compared with radiotherapy alone in several recent major studies.7–9 The standard treatment for concomitant chemotherapy combined with radiotherapy is a single agent (cisplatin).10,11 Thus, external radiotherapy combined with concomitant chemotherapy (cisplatin 40 mg/m2/week) is now the standard treatment for bulky cervical cancer.

Whether performing pelvic surgery in patients treated with primary radiotherapy is justified continues to be debated. Several retrospective analyses have compared patients who underwent hysterectomy or no pelvic surgery after radiotherapy (without concomitant chemotherapy).12–20 Only one randomized trial (closed 10 years ago) comparing patients treated with initial external radiotherapy and randomly allocated to hysterectomy (completion pelvic surgery) versus no hysterectomy (whatever the presence of residual disease) has recently been published.21 This study does not seem to demonstrate a benefit for overall survival. Nevertheless, a trend toward an increase in disease-free survival was observed in patients who underwent hysterectomy (62% vs. 53% at 5 years; P = .09).21

The potential advantages of hysterectomy after external radiotherapy are 2-fold: any residual disease can be removed with the prospect of improving (ideally) event-free survival, and the nodal status can be adequately assessed, thus allowing adjuvant treatment in patients with nodal involvement. Concerning the first point (removal of potential residual disease and improved survival), three types of patients should be distinguished after CRT: patients without residual disease at the end of radiotherapy, patients with a small residuum (a tumor <1 cm or isolated groups of tumor cells in partially sterilized tissues), and patients with a bulky tumor (≥2 cm). None of the published series has evaluated the value of hysterectomy after CRT. In the randomized trial about CRT conducted by Keys et al.,9 hysterectomy was performed in both arms. The rate of residual disease after CRT was lower in patients who received CRT compared with those treated with external radiotherapy (48% vs. 59%; P = .04).9 In the case of patients without macroscopic residual disease confirmed at clinical examination and on MRI (8 weeks after the end of CRT), a randomized trial is ongoing in France to evaluate the effect of hysterectomy. Patients with a very small residuum (<1 cm) are probably in a situation similar to that of patients without residual disease; if the surgical procedure had been performed a few weeks later, this residuum would have been totally sterilized by CRT.

The outlook for patients with bulky residual disease is totally different. In theory, these patients have a poor response to CRT and surgery is the only way to increase the survival of patients by removing the residual bulky tumor that CRT did not sterilize. The number of patients in this series is small, but the study is original because, to our knowledge, there are no data in the literature on the results of pelvic surgery in patients with bulky residual disease after CRT. The small number of patients reflects the efficacy of CRT in treating cervical tumors. Indeed, of the 75 patients reviewed for this study, only 12 had bulky residual disease. Furthermore, in this series, we selected patients who received the same CRT schedule, to optimize the homogeneity of the series. Consequently, although only 10 cases are reported in this study, the population is very homogeneous. Our survival results are very disappointing, even with a short follow-up (median time, 22 months); of the nine patients followed up, only two are alive without recurrent disease. These results put into question the real benefit of completion hysterectomy in this group of patients with bulky residual disease. However, it is noteworthy that the only pelvic recurrence reported in this series was observed in the patient without free surgical margins. Furthermore, the interval between the hysterectomy and the recurrence was 16 months. Consequently, the patient did not experience unpleasant pelvic symptoms due to the local spread of the disease during this period. We know that when a pelvic tumor (recurrence) is not removed, it spreads locally, with symptoms that have disastrous effects on the patient’s quality of life (nauseating leukorrhea, rectovaginal fistula, or fistula between the bladder and the vagina). These two points could be strong arguments in favor of proposing a hysterectomy even if the effect on event-free survival is low.

Is there a subgroup of patients with bulky residual tumors in whom hysterectomy would be helpful? In this series, we observed a high rate of extracervical disease. One patient had peritoneal disease found during exploratory laparotomy, and the rate of pelvic and/or para-aortic nodal involvement was high (50%). All of these patients had a preoperative MRI, and none had bulky suspicious nodes in the para-aortic area. Several previous publications suggest that the removal of positive nodes could have therapeutic value.22–25 This is questionable because lymphadenectomy had no therapeutic value in our series of patients with bulky residual disease in the cervix: all patients with nodal spread relapsed. However, if we consider the population of patients followed up without nodal involvement and free margins (three patients), two are alive without recurrent disease. Patients without extracervical disease might therefore benefit from pelvic surgery in terms of overall survival and progression-free survival. A complete radiological work-up (abdominopelvic MRI, chest radiograph with or without CT scan, and probably positron emission tomography/CT imaging) is required to select these patients and to exclude patients with distant disease.

Evaluating the results of hysterectomy in patients with bulky results would not be complete without studying an important point: the complication rate. Weems et al.15 and Mendenhall et al.16 previously reported that surgery increases the incidence of severe complications in patients treated with initial external radiotherapy. Conversely, Gallion et al.12 and Thoms et al.13 found no significant difference in the incidence of severe complications between patients who underwent a surgical procedure and those who did not. In a previous two-center study on morbidity caused by radical hysterectomy after external radiotherapy for stage IB2 or II cervical cancer, the rate of major morbidities almost attained 25%.26 This rate was correlated with the radicality of surgery (a type III Piver dissection). Our results confirm the high rate of complications of pelvic surgery after CRT.

Our series confirms that the rate of nodal spread is high in patients with bulky residual cervical disease after CRT. Furthermore, patients had a high complication rate (70%) after pelvic surgery. Only two patients are alive and disease free. The results of surgery are disappointing and do not seem to improve patient survival. As is the case in other solid tumors, new treatment approaches need to be investigated in the near future (determination of biological or initial radiological prognostic factors of the response to treatment) for earlier identification of patients who are unlikely to respond to standard CRT. In such patients, intensification of treatment (for example, combining external radiotherapy with a new cytotoxic agent or combining external radiotherapy with local administration of chemotherapy) should then be studied.


   ACKNOWLEDGMENTS
 
The authors thank Lorna Saint Ange for editing.

Received for publication May 21, 2004. Accepted for publication November 29, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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