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Local Relapse in Patients Treated for Squamous Cell Vulvar Carcinoma: Incidence and Prognostic Value

From the Departments of Obstetrics and Gynecology and Pathology, Centre Hospitalier Intercommunal de Créteil, Créteil; andthe Department of Dermatology, Tarnier, Paris, France.

Address reprint requests to: Bassam Haddad, MD, Service de Gynécologieobstétrique, Centre Hospitalier Intercommunal de Créteil, 40 avenue de Verdun, 94010 Créteil Cedex, France; E-mail: bhaddad{at}chicreteil.fr.

	ABSTRACT

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OBJECTIVE: To evaluate the risk factors for local relapse in vulvar cancer patients and its impact on survival as a function of its different patterns, which include local recurrences at the primary tumor site, recurrences remote from the primary tumor, and skin bridge recurrences.

METHODS: Between January 1978 and June 1999, 215 patients were treated for vulvar squamous cell carcinoma. The median follow-up was 38 months. To evaluate the role of local relapse in survival, a Cox regression multivariable analysis was performed using local relapse as a time-dependent covariate.

RESULTS: The local relapse-free survival rate was 78.6% (± 7.1%) at 5 years. Multivariable analyses showed that the local relapse was increased by the factors margin status and depth of invasion. Pathologic nodal status, tumor size, margin status, and depth of invasion were predictors of cancer-related death in the Cox multivariable model with fixed covariates. The contribution of local relapse for disease-specific survival at the site of the primary tumor (relative risk [RR] 6.35; 95% confidence interval [CI] 2.07, 15.76) or skin bridge recurrence (RR 6.48; 95% CI 2.54, 16.49) was highly significant, whereas the contribution of local relapse at the other sites was not (RR 2.29; 95% CI 0.53, 9.91). In this model, margin status was not significant. The risk of cancer-related death after local relapse was 58.4% (± 18.3%) at 1 year and 70.9% (± 17.6%) at 3 years.

CONCLUSION: Local relapses at the site of the primary tumor or skin bridge recurrences are strong predictors for cancer-related death, but not local relapse at a distant site.

During recent decades the classic total radical vulvectomy and bilateral inguinofemoral lymphadenectomy has become a less common procedure for the treatment of squamous cell carcinoma of the vulva. Nowadays, modified radical vulvectomy is a well-established treatment for T1 lesions.¹ Encouraging results obtained in these small tumors brought clinicians to realize modified radical vulvectomy in T2 and small T3 lesions.^2–6 In a prospective study of the Gynecologic Oncology Group,⁷ local relapse was more frequent in early-stage carcinoma of the vulva treated with modified radical vulvectomy than in historic controls. The impact of local relapse on the ultimate course of vulvar cancer remains controversial. For many investigators, local relapse has no detrimental effect on the survival of patients.^1,8 Local relapse, however, may exhibit different patterns, including local recurrences on the primary tumor site, recurrences remote from the primary tumor, and skin bridge recurrences. In most of the series these different patterns have not been distinguished. The objective of this study was to evaluate further the risk factors of local relapse and its impact on survival of patients with squamous cell carcinoma of the vulva as a function of different patterns of local relapse.

	MATERIALS AND METHODS

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The records of 215 consecutive patients with squamous cell vulvar carcinoma who were treated in our department between January 1978 and June 1999 were reviewed. The review included the clinical charts, pathology and operative reports, and follow-up data. Stages were assigned according to the surgicopathologic system (International Federation of Gynecology and Obstetrics 1994).

Before 1988, all of the patients underwent total radical vulvectomy and bilateral groin dissection. After 1988, surgical treatment of the vulva was conservative (hemiradical vulvectomy or radical local excision) if possible.^2,9 The primary vulvar incisions of the total and partial radical vulvectomies were extended from the skin to the level of the urogenital diaphragm. The incision modulations were similar to those described by Burrell et al.² Three patients underwent posterior exenteration and four underwent resection of the lower urethra. Unilateral lymphadenectomy was chosen for patients with lateral vulvar lesions after 1988. Groin dissections were performed through separate incisions for all patients but six, who were operated on in the early years of the study period (en bloc butterfly technique). Groin node dissection was avoided in 15 patients because of stromal invasion no greater than 1.0 mm¹ and in 20 patients because of their poor medical status. Adjuvant radiotherapy encompassing groin, obturator, and external and internal iliac areas was given in patients with three or more micrometastases (less than 1 cm), with one macrometastasis (at least 1 cm in diameter), or with any evidence of extracapsular spread.¹⁰ None of the patients without groin dissection received inguinal radiotherapy, and no patients underwent pelvic lymph node dissection. Radiotherapy encompassing the entire vulvar and perineal area was administered in case of positive margins.

The primary end point was local relapse and the secondary end point was cancer-related death. All of the end points were calculated from the date of first treatment. We considered as local relapse any tumor recurrence involving the skin and the subcutaneous tissues located around the vulvectomy scar or involving the skin bridge between the vulvectomy and groin dissection areas. Nodal relapses were considered as regional relapses, not local relapses. Three patterns of local relapses could be distinguished: primary tumor site recurrence (up to and including 2 cm from the vulvectomy scar), recurrence at a distance from the primary tumor site (more than 2 cm from the vulvectomy scar), and skin bridge recurrence (recurrence in the dermis and the subcutaneous tissue between the groin and vulvar incision). Frequency distributions were tested using the ² test. The difference between survival distributions was determined by means of the log-rank test. Clinical, pathologic, and therapeutic factors tested included patient age, tumor size, depth of invasion, margin status, lymph node status, associated epithelial disorders, type of surgery, and time period. Margin status was assessed by the pathologist on the specimen after fixation: Margins were considered to be involved when invasive carcinoma was present at the peripheral or deep margin. Margins involved with vulvar intraepithelial neoplasia were not recorded as positive. In the univariate analysis, we separated the associated epithelial disorder (lichen sclerosis, differentiated vulvar intraepithelial neoplasia, undifferentiated vulvar intraepithelial neoplasia) according to the International Society for the Study of Vulvar Disease.^11,12 The influence of clinical, pathologic, and therapeutic factors on outcome was assessed in multivariable analysis by using the Cox proportional hazards model in a forward stepwise procedure. In these analyses, only variables with P values of less than .05 were entered in the model and their relative risk (RR) calculated. Patients with positive margins who did not receive radiotherapy and patients with a larger than 1 mm stromal invasion tumor and no lymph node excision were excluded from the multivariable analyses. For the disease-specific survival, two separate models were constructed: one without local relapse and a second including local relapse as a time-dependent covariate. In this model, we distinguished primary tumor site recurrence, recurrence at a distance from the primary tumor site, and skin bridge recurrence. The time-dependent covariate is different from the fixed covariate.¹³ For the patients without local relapse, the expected risk of cancer-related death is based on the patient and tumor characteristics (fixed covariates) noted at the time of initial treatment. The term for local relapse is introduced in the model in a manner that can change over time. In women without local relapse, or with local relapse and concomitant or previous inguinal or distant metastases, time to cancer-related death still depends on fixed covariates. In patients with local relapse as the first event, the expected risk for cancer-related death may or may not change subsequent to the evidence of local relapse. All significance tests were two tailed, and differences were considered to be statistically significant when P was less than .05. The Cox proportional hazards model was used to compute RRs and 95% confidence intervals (CIs). For these latter analyses, RRs of the variables and their 95% CIs were calculated only when the P value was less than .05. All analyses were done with the Biomedical Package (BMDP; Statistical Solutions, Cork, Ireland).

	RESULTS

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The median age of the patients was 72 years (range 28–96). Eighteen patients had stage Ia cancer, 59 stage Ib, 49 stage II, 53 stage III, and 16 stage IVa. Twenty patients could not have their cancers staged (no lymph node resection). Surgical procedures and lymph node involvement according to patient and tumor characteristic are reported in Table 1. Despite 2-cm normal skin margins around the tumor (sometimes 1 cm in case of tumor located near the urethra or the anus), 44 patients had either microscopic positive margins (n = 30) or less than 1 cm normal skin margins (n = 14). Among the 30 patients with positive margins, the deep margin was involved for 16 patients (11 T2, three T3, and two unknown bifocal lesion) and the peripheral margin was involved for 14 patients (four T2, seven T3, and three unsuspected bifocal lesion). All patients with positive margins but three had radiotherapy. Three of the 14 patients with less than 1 cm normal skin margins (close margin) also had vulvar and perineal radiotherapy. Thirty-three patients with groin metastatic lymph nodes had pelvic radiotherapy (19 patients with inguinal macrometastasis, five with at least three micrometastases, and nine with extracapsular growth of lymph node metastases).

Local relapse-free survival is represented in Figure 1. The 5-year local relapse-free survival rate was 78.6% (±7.1%). Median time to local relapse was 12 months. Thirteen relapses (39%) were primary tumor site recurrences, 13 others (39%) were recurrences at a distance from the primary tumor site, and seven (22%) were skin bridge recurrences. The mean time for local relapse was 13 months in patients with primary tumor site recurrence, 33 months in patients with recurrence at a distance from the primary tumor site, and 9 months in patients with skin bridge recurrence. Among the 13 patients with recurrence at a distance from the primary tumor site, three had close or positive margin status (three of 44 [6.8%] versus ten of 171 [5.8%], P.= 81), whereas 12 of the 20 patients with primary tumor site recurrence or skin bridge recurrence had close or positive margins (12 of 44 [27.3%] versus eight of 171 [4.7%], P < .001). Univariate analysis of various clinical and pathologic factors associated with local relapse-free survival is presented in Table 2. Tumor size, depth of invasion, lymph node status, and margin status were significantly associated with local relapse. On multivariable analysis by forward stepwise Cox model regression, margin status and depth of invasion were independent risk factors of local relapse (Table 3). We studied risk factors according to the pattern of local relapse. Univariate analysis showed that margin status (P = .001) and tumor size greater than 2 cm (P < .05) were significantly associated with occurrence of skin bridge recurrences. Age over 70 years (P = .05) and positive pathologic node status (P = .06) did not reach statistical significance. Tumor size (P = .002), depth of invasion (P< .001), and margin status (P = .002) were significantly associated with primary tumor site recurrence. Presence of adjacent dermatosis (P< .001) and time period (patients operated on during the second time period) (P = .03) could be identified as risk factors for recurrence at a distance from the primary tumor site.

View larger version (10K): [in this window] [in a new window]   Figure 1. Local relapse-free survival. Rouzier. Local Relapse in Vulvar Cancer Patients. Obstet Gynecol 2002.

View larger version (10K): [in this window] [in a new window]   Figure 2. Disease-specific survival. Rouzier. Local Relapse in Vulvar Cancer Patients. Obstet Gynecol 2002.

View larger version (9K): [in this window] [in a new window]   Figure 3. Disease-specific survival (DSS) after local relapse. Rouzier. Local Relapse in Vulvar Cancer Patients. Obstet Gynecol 2002.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

In our study, the most important predictor of primary tumor site recurrence and skin bridge recurrences was the margin status. Heaps et al¹⁶ noted that local control after radical vulvectomy was achieved in 100% of cases, provided that a 1-cm margin of normal skin was included in the surgical specimen. In contrast, a normal tissue margin of less than 8 mm was associated with a 50% local recurrence rate. Our findings partly support these observations; the RRs of local relapse were 3.35 and 2.86 in patients with a normal tissue margin of less than 1 cm and in patients with positive margins, respectively. In the multivariable analyses of disease-specific survival, margin status became nonsignificant when the interactive term for local relapse was introduced into the regression model. This demonstrates the pejorative effect of recurrence at the primary tumor site and skin bridge recurrences, and these latter may be related to close or positive margin status. The importance of margin status may lead to inclusion of patients with large and very invasive tumors into protocols of preoperative radiotherapy or chemoradiation. Boronow et al¹⁷ have shown that mega-voltage radiotherapy can cause regression of locally advanced cancer to the point where a more limited resection becomes possible with an improved resection margin. Russel et al¹⁸ have employed external beam radiation and synchronous radiopotentiating chemotherapy to treat 25 women with locoregional advanced carcinoma. For eight of them, the reason for nonsurgical management was disease extent, which was predictive of inadequate surgical margin (less than 1 cm gross margin). Twenty of the 25 patients experienced complete clinical response and were not operated on. With a median follow-up of 24 months, 16 remained alive and continuously cancer free. In contrast to these results, the poor outcome of patients with positive or close margins observed in our series point out the necessity of determining the optimal sequence of therapy for patients with large and very invasive tumors.

The margin status and the risk of vulvar relapse did not differ significantly with the modifications of radical vulvectomy. Although results may be confounded by differences in the extent of the primary tumor, other investigators have also found that modified radical vulvectomy does not increase the risk of local relapse.^2,5 The type of vulvectomy and the size of tumor were not associated with an increased risk of local relapse in the multivariable analysis (Table 3), and therefore they encourage us to perform modified radical vulvectomy, as suggested by other authors.^2–6 It is important to note that in the partial radical vulvectomy modification of the surgical resection extent applies to medial and lateral limits only. The depth of the dissection must be the same as in total radical vulvectomy and is extended from the skin to the level of the urogenital diaphragm.

The general observation is that local recurrences at a distance from the primary tumor site develop late.^1,19,20 One might hypothesize that these late local relapses may in fact represent new primary lesions arising in vulvar epithelial disorders, as opposed to true recurrences. Several arguments may favor this hypothesis. First, the only factor associated with the occurrence of local recurrence at a distance from the primary tumor site is the presence of associated epithelial disorder around the tumor. Second, local recurrences at a distance from the primary tumor site occurred more frequently in the second time period of our study (P = .03): Larger resection of skin with a precursor lesion may explain this finding. On the other hand, conservative management was not associated with decreased local control (Tables 2–5) because the radicality of partial vulvectomy prevents an increase of primary tumor site recurrence. The disease-specific survival of patients with local recurrence at a distance from the primary tumor site in our series was good (88.9% at 1 year and 66.7% at 3 years), and this is the third argument to consider recurrences remote from the primary tumor site as new primary tumors. Moreover, we demonstrate that disease-specific survival was not dependent on local recurrence remote from the initial tumor site. The consistency of all of these results indicates that local recurrences at a distance from the primary tumor site appear to have a good prognosis but underlines the need for continued follow-up in conservatively treated vulvar cancer patient.

All patients with skin bridge recurrence died of cancer in our series. The rationale to justify the use of separate incisions in vulvar carcinoma management is that the mechanism of lymphatic spread in vulvar cancer is by embolization rather than by permeation.²¹ Nevertheless, the occurrence of skin bridge recurrences shortly after surgical treatment suggests that skin bridge recurrences are the evolution of metastatic emboli arrested in their migration. The frequency of skin bridge recurrence in our study is comparable to that reported in the literature.^22,23 Only one patient with skin bridge recurrence had received radiotherapy at the time of initial treatment, although four of the seven patients had positive nodes. Indications for adjuvant radiation have been validated in patients treated with en bloc resection and have been transposed for patients treated with the three-incisions technique.¹⁰ Data confirming the adequacy of the adjuvant irradiation indications in patients operated on with the three-incisions technique are still needed. The outcome after skin bridge recurrence is particularly poor in our study. Median time from surgery to recurrence diagnosis is 5 months in the literature^22,24 and 8 months in our study. The poor prognosis is probably due to a delay in diagnosis of the recurrence in most of the cases that we have treated; recurrences were most of the time fixed to the bone or to the underlying muscle. We do not claim from our results that the triple incision technique should be given up, especially because recurrences in subcutaneous tissue of the thigh have been reported in patients treated with the en bloc butterfly technique.²⁵ Removal of underlying tissue with preservation of the skin bridge has been reported by Flannelly et al,²⁶ but the impact of this modification on recurrence rate has been poorly studied. Early detection of skin bridge recurrences is difficult: The bridges have to be carefully observed by the patient and her gynecologist in the months after surgery, and suspected nodes in this area should lead to biopsy or resection.

Some authors have demonstrated that vulvar recurrence can be treated by radiation or chemoirradiation with a high degree of success.^27,28 In our experience, as in others’,^24,29,30 only radical re-excision in the patient with limited vulvar recurrence provides satisfactory survival results. But the fact that only patients with inoperable local relapse underwent radiotherapy or chemoradiation in our series may have introduced a selection bias.

In conclusion, two patterns of vulvar relapses may be individualized: 1) recurrences at a site far from the primary tumor, which can be considered a new primary tumor as it often arises on epithelial disorders long after initial treatment, and 2) recurrences at the primary tumor site or skin metastasis, which are correlated with margin status and tumor characteristics (size and depth of invasion) more than type of surgery used. We demonstrated that occurrences of vulvar skin bridge recurrences or primary tumor site recurrences are strong predictors for cancer-related death, but not recurrences at a distance from the primary tumor site.

	Footnotes

 
PII S0029-7844(02)02501-2

Received March 19, 2002. Received in revised form May 30, 2002. Accepted September 19, 2002.

	REFERENCES

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Rouzier, R. Articles by Paniel, B.-J. Search for Related Content PubMed PubMed Citation Articles by Rouzier, R. Articles by Paniel, B.-J.