Recurrent Cancer of the Vulva: Clinicopathologic Prognostic Factors,Patterns of Recurrence,and Their Management

Abstract

Objective:

The aims of this study were to analyze the clinicopathologic parameters and patterns of recurrence in vulvar cancers at a tertiary cancer center and to evaluate their prognostic implications. Given the rarity of these tumors, the information regarding prognostic factors involving recurrent cases is limited and conflicting.

Materials and Methods:

The records of all patients with vulvar cancer who underwent primary surgery from January 2007 to December 2014 were analyzed. Information regarding each patient's demography, clinical findings, treatment given, complications, and follow-up details was collected for this retrospective study.

Results:

Seventy-eight patients were included in this analysis. Seventeen patients (21.7%) had recurrent disease after a mean interval of 15 months. Nodal status, tumor classification, depth of invasion, lymphovascular space invasion, and resection margin were statistically significant prognostic factors for disease-free and overall survivors according to a univariate analysis. On multivariate analysis, only tumor size, nodal positivity, and margin status appeared to be statistically significant.

Conclusions:

Clinicopathologic patterns could help stratify patients for adjuvant radiotherapy of the vulva. Intensified vulvoscopic follow-up is needed to prevent multiple local recurrences, especially those with high-risk prognostic factors. This study suggests the value of giving local vulvar radiation to patients in high-risk groups to prevent local recurrences. Customized and strategic management of recurrences is needed according to the pattern of recurrence. (J GYNECOL SURG 32:339)

Introduction

Cancer of the vulva is a rare neoplasm of the female genital tract, accounting for only 2%–5% of all gynecologic malignancies.¹ The age group usually affected is 50–70, with squamous-cell carcinoma being the most common histology, followed by melanoma, basal-cell carcinoma, and adenocarcinoma.¹ Surgery remains the mainstay of management, with radiation or chemoradiation reserved for locally advanced and unresectable disease. The prognosis is generally good when using this multimodality approach; however, treatments are associated with significant morbidity, and up to 40%–50% patients eventually develop recurrences.^1,2

Given the rarity of these tumors, the information regarding prognostic factors involving recurrent cases is limited and conflicting.^3–10 Most of these patients tend to be old and have comorbidities that make additional surgery and further adjuvant treatment difficult options.

The psychosexual impact that radical surgical procedures have on the well-being of a patient has been well-known for many years. This has led to changing paradigms in surgical management, from the mutilating radical en bloc procedures to triple-incision techniques,¹¹ to today's radical local excisions,^12,13 mainly to ensure the sexual identity and satisfactory body image of an affected patient. The ability to keep this fine balance of maintaining oncologic safety and yet preserving a patient's basic psychosexual quality of life is debatable and contentious even today.

There are several studies indicating that the extent of resection margins seems to be of minor importance. One study suggested that there were concerns regarding the possibility of a second primary arising after wide local excision from a possible missed abnormal vulva-in-situ.¹⁰ Some studies have shown a higher risk for disease recurrence when the pathologic tumor-free margin was <8 mm, while recent analyses failed to show any impact of the margin distance on prognosis.^13–18 Despite studies indicating diminishing importance of extent of resection margins, current guidelines recommend a surgical resection margin of at least 1 cm.

Recurrent vulvar cancer occurs in an average of 24% of cases after primary treatment comprised of surgery with or without radiation.¹⁹ Most recurrences occur locally near the original resection margins or at the ipsilateral inguinal or pelvic lymph nodes.¹⁹

The aims of this study were to analyze the clinicopathologic parameters and patterns of recurrence in vulvar cancers at a tertiary cancer center and to evaluate their prognostic implications. Management of recurrences according to their patterns and their implications for survival were also studied.

Materials and Methods

For this retrospective analysis, case records were retrieved for all patients with cancer of the vulva who were treated at the Rajiv Gandhi Cancer Institute and Research Centre, in New Delhi, India, from January 2007 to December 2014. Information regarding each patient's demography, clinical findings, treatment given, complications, and follow-up details was collected using an electronic data system (HIS VISTA). The authors have adhered strictly to ethical norms for this research.

Inclusion criteria

All patients with vulvar cancer who underwent primary surgery from January 2007 to January 2014 were eligible for study inclusion.

Institutional approach for management

The treatment approach to these cancers consisted of resection of the primary tumors and inguinofemoral lymph-node dissections (if indicated) with separate incisions. Reconstruction was performed where this was required. Adjuvant radiotherapy to the pelvis (including the groin) was administered if >1 inguinofemoral lymph node was positive for malignancy, if a single metastasis was >10 mm in diameter, or if there was extracapsular spread present in the involved lymph node.

Adjuvant radiotherapy to the vulva was administered if the surgical margin was <8 mm. After a thorough review of the literature, the following variables were tested for each recurrence: tumor size; depth of invasion; lymphovascular space invasion (LVSI); margin involvement; margin distance; grade; and lymph-node status.

Endpoints

The study endpoints were presence of recurrent disease (locoregional, groin, or distant), death, or last follow-up.

Disease-free survival (DFS) was defined as the time from the date of the last treatment (surgery or radiation) to the date of recurrence/death or last follow-up. Overall survival (OS) was defined as time from the date of the last treatment (surgery or radiation) to the date of death/last follow-up.

Statistical analysis

Statistical analysis was performed using SPSS. Descriptive statistics were used to evaluate mean, median, and standard deviation for continuous variables and proportions for categorical variables. The Kaplan–Meir method was used for DFS and OS and a log-rank test was used to find the prognostic factors for recurrence; a p-value <0.05 was considered statistically significant. All variables with a p-value <0.05 in the univariate analysis were analyzed further with multivariate Cox regression.

For conclusive statistical analysis of the invasion depths and margin distances, the cases were divided into two equal groups (invasion: ≤3 mm and >3 mm; and margin distance: <8 mm and ≥8 mm).

Results

Eighty-seven patients with primary vulvar cancer underwent surgery at the Rajiv Gandhi Cancer Institute between 2007 and 2014. Nine cases were lost to follow-up immediately after surgery and were excluded from further analysis. The median age of the remaining 78 patients was 64 years (range: 46–84 years). The median follow-up was 33 months (mean: 41 ± 23; range: 6–104 months). The demographic profiles of these patients are shown in Table 1.

Table 1.

Patients' Characteristics

Characteristics	N = 78
Age	64 years (46–84 years)
Local treatment
Radical local excision	4 (5.1%)
Modified radical vulvectomy	10 (12.8%)
Radical vulvectomy	64 (82.0%)
Reconstruction	12 (15.3%)
Inguinofemoral lymphadenectomy
Not done	4 (5.1%)
Ipsilateral	10 (12.8%)
Bilateral	64 (82.0%)
Number of lymph nodes retrieved	Mean: 11 (range: 1–32)
Radiotherapy
Pelvic	21 (26.9%)
Both pelvic and perineal	6 (7.6%)

The histology of the majority of these vulvar cancers was squamous-cell carcinomas (75 patients), while veruccous carcinoma was seen in 2 patients and basal-cell carcinoma was seen in only 1 patient (Table 2). Lichen sclerosis was observed in 12 (15.3%) patients. Vulvar intraepithelial neoplasia (VIN) was observed in 33 (25.7%) patients. In 10 patients (12.8%), both lichen sclerosis and VIN were present. Primary tumors were mainly confined to the vulva (91.3%; T1 and 2) and 94.2% of the tumors were excised with tumor-free margins. The exact margin distance was determined in a subset of 60 patients: The mean margin distance was 8 mm and ranged from 1 mm to 24 mm.

Table 2.

TNM Classification According to AJCC 2010

Histopathologic characteristics	# of patients N = 78
T (Tumor classification)	78 (100%)
1. T1A	4 (5.1%)
2. T1B	51 (65.3%)
3. T2	20 (25.6%)
4. T3	3 (3.8%)
N (Nodal classification)	78 (100%)
N0	46 (58.9%)
N1	22 (28.2%)
N2	6 (7.6%)
Nx^a	4 (5.1%)
Metastasis
M0	78 (100%)
Grade of differentiation	71 (91.0%)
G1	19 (24.3%)
G2	29 (37.1%)
G3	23 (29.4%)
Histologic differentiation	78 (100%)
Squamous-cell carcinoma	75 (96.1%)
Verrucous carcinoma	2 (2.5%)
Basal-cell carcinoma	1 (1.2%)
Depth of invasion	60 (76.9%)
≤3mm	24 (30.7%)
>3mm	36 (46.2%)
LVSI	63 (80.7%)
Present	26 (33.3%)
Absent	37 (47.4%)
Margin involvement	78 (100%)
Tumor-free	62 (79.4%)
VIN	6 (7.7%)
Positive margin	10 (12.8%)
Margin distance	60 (76.9%)
≤5mm	24 (30.7%)
>5mm	36 (46.2%)

Nx indicates that lymph nodes could not be evaluated.

TNM, tumor, node, metastasis; AJCC American Joint Committee on Cancer; LVSI, lymphovascular space invasion; VIN, vulvar intraepithelial neoplasia.

Seventy-four patients (94.8%) underwent inguinofemoral lymphadenectomy; lymph-node metastasis was diagnosed in 28 patients (37.8%). In 64 patients (82.1%), bilateral lymph-node dissection was performed, and in 10 patients (12.8%) unilateral lymph-node dissection was performed. In 4 patients (5.1%) lymph-node dissection was not performed, as their classification was T1a and lymphadenectomy was not recommended. Table 3 shows the classifications of these cancers.

Table 3.

Classification According to AJCC 2010

Variable	N	DFS p-value	DFS 2-year survival	OS p-value	OS 2-year survival%
Tumor classification	78	0.001		0.001
T1a	4		100		100
T1b	51		81.3		91.3
T2	20		67.3		76.3
T3	3		33.3		33.3
Nodal involvement	78	0.000		0.000
N0	46		100		100
N1	22		73.5		86.5
N2	6		60		74.5
Nx^a	4		100		100
Depth of invasion	60	0.006		0.001
≤3 mm	24		89.2		94.6
>3 mm	36		69.2		74.5
Lymphovascular involvement	63	0.042		0.020
Present	26		80.4		90.2
Absent	37		89.8		95.6
Grade	71	0.080		0.100
G1	19		84.5		90.2
G2	29		82.7		89.5
G3	23		78.4		85.3
Resection margin	78	0.000		0.000
Free	62		92.5		97.7
Involved	6		78.5		92.5
VIN	10		88.7		95
Margin distance	60	0.041		0.033
≤ 5mm	24		82.3		92.5
>5 mm	36		94.5		97.7

Nx indicates that lymph nodes could not be evaluated.

AJCC, American Joint Committee on Cancer; DFS, disease-free survival; OS, overall survival; VIN, vulvar intraepithelial neoplasia.

Bold signifies the statistically significant values with p < 0.05.

Of the 28 patients with positive lymph nodes at primary diagnosis, 13 (46.4%) had recurrent disease; 10 of these received radiotherapy after initial surgery and 3 did not have radiation administered despite there being indications for it. In 10 patients, only the groin and pelvis were irradiated. Recurrence affected the vulva and lymph nodes equally in each of these patients despite their primary tumors having been completely resected.

Seventeen patients (21.7%) had recurrent disease after a mean interval of 15 months (median 16 months; range: 6–19 months). Two of these patients had had stage I disease, 2 patients had Stage II disease, 11 patients had Stage III disease, and 2 patients had stage IV disease. In the majority of cases (n = 10; 59%), the recurrence was located in the vulvar region only. In 4 (23.5%) patients, recurrence was in the groin, and in 2 (11.7%) patients the recurrence was in the groin and vulva. No skin-bridge recurrences were noted. One (5.8%) patient had a recurrence in the lung. Details of these cases' characteristics are shown in Table 4. Management of these cases was as follows (Table 5):

(1) Of the 10 patients with local vulvar recurrence, 6 underwent repeat surgery, with excision of the recurrence and flaps reconstruction: transverse rectus abdominus myocutaneous (TRAM) flap (1 patient); gracilis myocutaneous flap (3 patients); and antero lateral thigh (ALT) flap (2 patients). Two patients underwent radical local excision of their tumors without the need of any flap surgery. Two patients were administered radiation, primarily to the perineum.

(2) Four patients had recurrence in the groin only. Two of these patients underwent surgery followed by radiation therapy, 1 patient received radiation only, and 1 patient underwent chemotherapy for large fixed nodes, which had already been irradiated.

(3) The 2 patients with recurrence in the groin and vulva underwent surgery followed by radiation.

(4) One patient had metastasis to the lung and was started on chemotherapy. OS was 18 months after initiation of chemotherapy.

Table 4.

Classifications of Recurrences Stage-Wise, Their Locations & Characteristics

Stage	Vulvar recurrence	Groin recurrence	Groin & vulvar recurrence	Metastasis	Prior RT to pelvis	Prior RT to pelvis & perineum	Margin positive	Tumor size >2 cm	Lymph-node positive
I	2	–	–	–	–	–	1	2	–
II	2	–	–	–	–	–	1	2	–
III	6	4	1	–	8	–	3	11	11
IV	–	–	1	1	2	–	1	2	2

RT, radiation therapy.

Table 5.

Recurrent Vulvar Cancers by Site & Mode of Primary Management of the Recurrences

Site	Surgery	Radiation	Chemotherapy	Overall survival (mean) in months
Vulvar (n = 10)	8	2	0	38
Groin (n = 4)	2	1	1	27
Groin & vulvar (n = 2)	2	0	0	25
Distant metastasis (n = 1)	0	0	1	18

Nodal status, tumor classification, depth of invasion, LVSI, and resection margin were statistically significant prognostic factors for DFS and OS by univariate analysis. After performing multivariate analysis, only tumor size, nodal positivity, and margin status appeared to be statistically significant. DFS and OS decreased with increasing tumor size and nodal positivity.

Two-year DFS was 100% in patients with no nodal involvement, 73.5% in patients with unilateral nodal disease, and 60% in patients with bilateral nodal involvement.

Discussion

In the current study, a total of 78 patients were included. The recurrence rate observed was 21.7%, which was consistent with other studies that reported recurrence rates from 15% to 35%.^20–22

The median time of recurrence was 15 months (median: 16; range: 6–24 months). Almost all the recurrences in the current study occurred within the first 2 years, which was also consistent with other studies in the literature.²³

The primary route of spread in vulvar cancer is via the lymphatics, and regional lymph-node positivity to the inguino-femoral nodes was considered prognostically significant for recurrence and survival in one study.⁷ However, the results of two studies^8,9 contradicted these results. In a study by Landrum et al.,²⁴ lymph-node status did not predict DFS or OS in patients who had vulvar cancer. This result was possibly because of the heterogeneous treatment given in different age groups in that study. The results were inconclusive because there are few studies on this rare tumor. In the current study—which is largest study on vulvar cancers in India—lymph-node status had direct relationships with DFS and OS. Patients with bilateral lymph-node positivity had the worst prognosis, and lymph-node status had a direct bearing in both univariate and multivariate analysis.

Histopathologic grade was not significant in the current series, although, this parameter has been regarded as an important prognostic factor in a few studies.^23,25,26

In the current study, nodal status, tumor size, LVSI, depth of invasion, margin status, and margin distance were statistically significant for prediction of OS and DFS in a univariate analysis. In a multivariate analysis, only tumor size (p = 0.03), nodal status (p = 0.006), and margin status (p = 0.04) were statistically significant. This was consistent with other studies.^27–29

Positive margins of central lesions do not imply bad prognoses necessarily, as these tumors do not tend to infiltrate adjacent tissues, such as urethral and anal tissues, because these tumors lack cutaneous and subcutaneous tissue and have limited lymphovascular supplies. However, margin positivity in lateral lesions is correlated with recurrences,^28,29 and, as shown in the current study, involvement of margins also correlated significantly with recurrences.

Recurrence was also seen in 3 patients who had stage I disease. One of them had stage IA disease and wide local excision with adequate margins was performed in this patient. The recurrence developed at a site different from the primary. Another patient with Stage IB had undergone a modified radical vulvectomy and developed a recurrence at a second site. This raises the possibility of a second primary affecting the vulva in the context of a probable vulva-in-situ, as has been suggested by Woolderink et al.¹⁰ In a study by Rouzier et al.,³⁰ remote recurrences occurred after 5 years, thus, suggesting a need for lifelong follow-up of these patients.

The majority (58.8%) of the recurrences occurred locally in the current study's patients. This was consistent with other studies ^3,10,20 in the literature. In addition, most of these patients had received adjuvant pelvic radiation. Recurrences occurred primarily in the vulvar region, suggesting that surgical excision with radiotherapy of the pelvic region was effective for achieving local control in the groin but not for the vulvar region. This raises further questions about recurrence patterns in patients with initial lymph-node metastasis—even in these patients, recurrence occurred predominantly in the vulvar region. Further analysis of these aggressive node-positive tumors is required to shed light on their potential for causing recurrences. In addition, the role of human papilloma virus in local, inguinal recurrences and in second primaries needs to be emphasized for understanding future screening and treatment options.

The strength of the current study would have been enhanced by multicentric studies. A shorter follow-up (median: 33 months) resulting from poor follow-up in Indian females, given their lack of education and lower socioeconomic status, also weakened the current study.

Conclusions

Like other gynecologic malignancies, clinicopathologic patterns of patients with vulvar cancer, could help stratify these patients for adjuvant radiotherapy of the vulva. Intensified vulvoscopic follow-up is needed to prevent multiple local recurrences, especially for patients with high-risk prognostic factors. The current study suggests that administering local vulvar radiation in high-risk groups of patients could help prevent local recurrences. Recurrences need to be managed strategically according to their patterns and uses of prior adjuvant therapies.

Footnotes

Acknowledgments

The authors are grateful to the Departments of Uro-Gynaecologic Oncology, Plastic Surgery, and Research of the Rajiv Gandhi Cancer Institute and Research Centre, New Delhi, India, for their constant support.

Author Disclosure Statement

The authors declare that there are no conflicts of interest in connection with this research or article.

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Stage	Vulvar recurrence	Groin recurrence	Groin & vulvar recurrence	Metastasis	Prior RT to pelvis	Prior RT to pelvis & perineum	Margin positive	Tumor size >2 cm	Lymph-node positive
I	2	–	–	–	–	–	1	2	–
II	2	–	–	–	–	–	1	2	–
III	6	4	1	–	8	–	3	11	11
IV	–	–	1	1	2	–	1	2	2

Stage	Vulvar recurrence	Groin recurrence	Groin & vulvar recurrence	Metastasis	Prior RT to pelvis	Prior RT to pelvis & perineum	Margin positive	Tumor size >2 cm	Lymph-node positive
I	2	–	–	–	–	–	1	2	–
II	2	–	–	–	–	–	1	2	–
III	6	4	1	–	8	–	3	11	11
IV	–	–	1	1	2	–	1	2	2

Stage	Vulvar recurrence	Groin recurrence	Groin & vulvar recurrence	Metastasis	Prior RT to pelvis	Prior RT to pelvis & perineum	Margin positive	Tumor size >2 cm	Lymph-node positive
I	2	–	–	–	–	–	1	2	–
II	2	–	–	–	–	–	1	2	–
III	6	4	1	–	8	–	3	11	11
IV	–	–	1	1	2	–	1	2	2