GYNECOLOGIC
ONCOLOGY
37, 374-377 (1990)
Reasons for Incomplete Surgical Staging in Early Ovarian Carcinoma’ J. B. TRIMBOS,*‘* J. A. SCHUELER, * M. VAN LENT,? J. HERMANS,+ AND G. J. FLEUREN§ Departments of *Gynecology, *Medical Statistics, and $Pathology, Leiden University Medical Center, Leiden, and TDepartment of Gynecology, Rotterdam Radiotherapeutic Institute, Rotterdam, The Netherlands Received July 3 1, 1989
The completeness and associated morbidity of surgical staging in 86 patients with early ovarian carcinoma were analyzed. According to strict criteria for completeness of the procedure established before the onset of the study, surgical staging after one or two laparotomies was complete in only 53% of cases. Initial staging in a peripheral hospital was complete in only 15% of patients. lntraoperative complications occurred in between 8 and 15% of patients and included injury of the vena cava (S), small bowel injury (2), myocardial infarction (l), transection of the ureter (l), and splenic rupture (1). The most frequently omitted staging steps were biopsy of the paracolic gutter, biopsy of the pelvic peritoneum, and sampling of retroperitoneal lymph nodes. Reasonsfor incomplete surgical staging were divided into factors associated with increased risk or difficulty of the procedure and lack of knowledge of the sites at risk for ovarian cancer metastases. It was found that both phenomena should be held responsible to the same extent for the large number of incomplete surgical staging procedures. The conclusion was made that either gynecologists should be better educated in the staging of ovarian cancer or a more efficient patient referral policy should be considered. 0 19!30 Academic Pm.% Inc. INTRODUCTION
In recent years, our understanding of the disseminating patterns of ovarian cancer has been greatly extended. Metastases to the periaortic lymph nodes [l] and the spread of cancer cells via the major routes of peritoneal fluid from the pelvis to the hemidiaphragms [2] form the basis of this knowledge. Together with a renewed interest in the significance of surgical staging, this has resulted in a new concept of surgical staging of ovarian cancer r31. ’ This study was supported and coordinated by The Netherlands Society of Gynecologic Oncology. * To whom all correspondence should be addressed at the Department of Gynecology and Reproduction, Leiden University Medical Center, P.O. Box 9600, 2300 RC Leiden, The Netherlands.
0090-8258/W $1.50 Copyright 0 1990by AcademicPress,Inc. All rights of reproductionin any form reserved.
It has been established by many authors that meticulous and complete surgical staging is a prerequisite to definition of the correct stage of ovarian cancer and to the planning of individual therapy [4-61. Only the most accurate determination of the extent of this disease will enable the definition of subsets of patients requiring adjuvant therapy and those in whom adjuvant treatment could be considered overkill. Despite all these considerations the feasibility of adequate surgical staging is still questionable [7], maybe because the diagnosis of early ovarian cancer confined to the internal genitalia is usually made at the time of laparotomy for other reasons and therefore unexpected [4]. This study was designed to provide more information about surgical staging practice in early ovarian cancer in The Netherlands at the moment of initial diagnosis and reasons for inadequate staging. MATERIALS
AND METHODS
This study was part of a larger multicenter trial on prpgnostic factors in early ovarian cancer supported by The Netherlands Society of Gynecologic Oncology. In this trial patients with well-differentiated early-stage (IA, IB, IC, IIA, FIG0 1976) epithelial ovarian cancer received no additional treatment after total abdominal hysterectomy (TAH), bilateral salpingo-oophorectomy (BSO), and surgical staging. In young patients with a Stage IA1 tumor wanting to retain their fertility, unilateral salpingo-oophorectomy (USO) and biopsy of the contralateral ovary were permitted [S]. Other criteria for inclusion in this follow-up study are given in Table 1. At the beginning of the study the criteria for complete staging were defined prospectively. By and large, the guidelines of Young were followed [4]. The requirements for complete surgical staging in this study are summarized in Table 2. 374
INCOMPLETE
STAGING OF OVARIAN
TABLE 1 Inclusion Criteria for Prospective Follow-up Study in Early Ovarian Cancer Epithelial ovarian cancer, stages IA, IB, IC, and IIA Well-differentiated tumor No secondary primary tumor No previous radiotherapy or chemotherapy No adjuvant treatment after surgery (TAH + BSO, USO, and surgical staging) a FIG0 1976.
For all the patients registered, clinical files, operating notes, and histology reports were studied, permitting analysis of the morbidity and extent of the staging procedure. If one of the necessary staging steps (Table 2) was omitted, the procedure was considered incomplete. Revision of the histology of the primary tumor was performed in all cases. However, revised histologic diagnosis was no reason for exclusion from this clinical study of staging performance. Pathology and outcome reports of these patients were recorded and will be reported elsewhere. RESULTS A total of 107 patients were registered from January 1, 1981 to January 1, 1988. Twenty-one patients were excluded from analysis: secondary primary tumor (n = 7), adjuvant therapy after surgery (n = 2), histology other than well-differentiated epithelial cancer (n = lo), FIG0 stage greater than IIA (n = l), laparotomy before January 1, 1980 (n = 1). The remaining 86 patients formed the study group. The mean age of these patients was 50 years (range 21-79 years). Initial staging laparotomy was performed in a gynecologic oncology center for 27 patients and in a periphTABLE 2 Criteria for Complete Surgical Staging of Early Ovarian Cancer Used in the Present Study TAH + BSO (US0 + biopsy of contralateral ovary) Peritoneal washing Careful inspection and palpation of all peritoneal surfaces Biopsy of any suspect lesion for metastasis Infracolic omentectomy Biopsy or resection of any adhesion adjacent to the primary tumor Blind biopsies of bladder peritoneum and cul-de-sac Blind biopsies of right and left paracolic gutter Blind biopsies or smear of right hemidiaphragm Lymph node sampling along common iliac arteries Lymph node sampling along the aorta and vena cava at the level between inferior mesenteric artery and left renal vein ’ In stage IA, and young patients desiring to preserve their reproductive ability.
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CANCER
era1 hospital for 59 patients. The completeness of the 59 procedures performed in peripheral hospitals is shown in Table 3, with a breakdown according to type of surgeon. Only in 5% of these procedures performed by a general gynecologist/obstetrician was surgical staging complete. Thirty-eight patients had a second laparotomy for staging purposes. After one or two laparotomies the staging procedure was considered complete in 46 of 86 patients (53%). In the remaining 40 patients one or several steps of the staging procedure had been omitted. When more than one surgical staging procedure had been done, the most extensive operation was taken into account for analysis of surgical morbidity and the reasons for incomplete staging. This was usually the operation performed last. Surgical morbidity and other characteristics of these operations are shown in Table 4. Suture repair was sufficient to treat the lesions of the vena cava wall in five patients. Bowel resection was required in the case of small bowel injury, as was splenectomy after splenic rupture and reanastomosis of the ureter after transection. In many incompletely staged patients more than one step of the surgical staging procedure was omitted (Table 5). Omission of these steps could partially be explained by the risk and difficulty of the procedure. In the remaining cases only a lack of knowledge of the correct surgical staging of ovarian cancer could be held responsible for omission of the step (Table 5). DISCUSSION The results of our study show that the percentage of complete surgical staging procedures for early ovarian cancer at the moment of initial laparotomy is very low. Evidently, in The Netherlands, the majority of patients are initially operated on by surgeons who lack not only complete knowledge but also the technical skills needed TABLE 3 Assessmentof the Surgical Staging Procedure at Initial Laparotomy in a Peripheral Hospital according to Type of Surgeon specialty Staging Procedure Surgeon General surgeon General gynecologist/ obstetrician Gynecologist with (vascular) surgeon Gynecologist with consulting gynecologic oncologist Total
Total
Complete
Percentage
1 43
2
-
13
5
38
2
2
-
59
9
15
5
376
TRIMBOS ET AL.
TABLE 4 Characteristics and Complications of Staging Laparotomy in 86 Patients with Early-Stage Ovarian Cancer
TABLE 5 Reasonsfor Incomplete Surgical Staging in Well-Differentiated Early Ovarian Carcinoma
Staging procedure
Range of operation time (min) Range of postoperative hospital stay (days) Blood loss > 1000 ml Intraoperative complications Injury of vena cava Small bowel injury Myocardial infarction Transection of ureter Splenic rupture Postoperative complications Urinary tract infection Myocardial failure Prolonged ileus Septic Peritonitis Pelvic abscess Lung atelectasis Hemorrhage requiring surgical intervention Vaginal hemorrhage Pulmonary embolism Lymphocele with compression of ureter Persistent fever and diarrhea
Complete, n = 46
Incomplete, n = 40
90-240 8-38
60-270 lo- 29
7% 15% 3 1 1 1 1 15% 3 1 1 1 1 -
13% 8% 2 1
30% 4 1 1 1
-
1 3 1
-
1
Procedures missed Procedure difficult or associated with increased morbidity Biopsy of diaphragm Sampling of retroperitoneal lymph nodes Infracolic omentectomy Easy procedure; no morbidity involved Biopsy of peritoneum of left paracolic gutter Biopsy of peritoneum of right paracolic gutter Biopsy of pelvic peritoneum (bladder, cul de sac) Biopsy or removal of adhesions adjacent to primary tumor Biopsy or removal of other pelvic adhesions (suspect lesions) Peritoneal cytologic washing
Percentage of 40 incomPercentage of total number pletely staged of 86 patients patients
40 33
85 70
8
18
42
90
40
85
39
73
9
20
6
13
5
10
peritoneal washing [ 121, infracolic omentectomy [5], removal of adhesions near the primary tumor [13], and to perform an adequate and complete surgical staging retroperitoneal lymph node sampling [ 141. Documentation of the rationale for blind peritoneal procedure. Similar conclusions have been formulated for biopsies is far less unanimous. The reasons to include the situation in the United States [4,71. In the study of McGowan et al. evaluation of the un- blind biopsies from several peritoneal locations in our dersurface of the diaphragm was the most commonly staging criteria are threefold. These sites follow the major omitted site (86%), followed by the removal of adhesions flow of potentially contaminated peritoneal fluid throughand biopsy of possible pelvic peritoneal malignant ex- out the peritoneal cavity, defining them as high-risk sites tension (65%), partial omentectomy (55%), and perito- for peritoneal tumor implants. Furthermore, biopsy of a neal washing (52%) [7]. These findings are comparable specific intraperitoneal site is the best possible guarantee that the particular location is carefully inspected, and, to those of the present study. The feasibility of preserving childbearing capacity after last but not least, the procedure is not time consuming conservative surgical treatment of early ovarian cancer and is virtually without complications. The certainty of has been demonstrated recently [9], but this approach a careful and objective examination of a high-risk site has been the subject of considerable debate. Careful ex- for tumor metastasis should be regarded as a most valamination and biopsy or wedge resection of the contra- uable tool in the evaluation of data of surgical staging lateral ovary has been emphasized since contralateral in multicenter trials. Surgical staging in our study was microscopic metastases have been described in 9 to 13% associated with appreciable intraoperative morbidity. of cases [9,10]. Most authors, however, feel that con- These staging complications, however, do not outweigh servative treatment is permitted in these cases, provided the benefits accrued by the precise definition of the disa number of prerequisites for a low-risk situation should ease. Discrimination of low-risk and high-risk patients and reliable comparative analysis of data between instibe met [ll]. The criteria for completeness of surgical staging of tutions should be mentioned in this respect. We tried to distinguish between a lack of surgical skill ovarian cancer used in the present study can be regarded and a lack of sufficient knowledge of the sites at high as very strict. There is almost general agreement on the risk for metastases as the cause of incomplete surgical necessity of a a number of staging procedures such as
INCOMPLETE
STAGING OF OVARIAN CANCER
staging. From Table 5 it can be concluded that both phenomena are involved to the same extent and that both should be held responsible for the rather disappointing results of initial staging laparotomy. In 1987, Young stated that understaging of ovarian cancer is still a significant problem and that it may lead to findings difficult to interpret at best and misleading at worst [4]. If we want to solve this problem we have to do better in educating the surgeons who perform the staging operations or we must promote a more efficient policy for referral of patients with proven or suspect early ovarian cancer. In this study we have shown that surgical staging of early ovarian cancer is associated with considerable morbidity and that lack of surgical skill as well as lack of complete knowledge of the sites at risk for tumor metastases might be held responsible for the high incidence of incomplete staging procedures at initial laparotomy. Gynecologic surgeons should be aware of these findings to improve their staging performance. Such an accomplishment will undoubtedly profit future clinical trials and, more important, benefit individual patients with early ovarian carcinoma. REFERENCES 1. Knapp, R. C., and Friedman, E. A. Aortic lymph node metastases in early ovarian cancer, Amer. J. Obstet. Gynecol. 119, 1013-1017 (1974). 2. Feldman, G. B., and Knapp, R. C. Lymphatic drainage of the peritoneal cavity and its significance in ovarian cancer, Amer. J. Obstet. Gynecol. 120, 991-994 (1974).
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