ORI GI NAL ARTI CLE COLORECTAL CANCER

Abdominoperineal Resection for Squamous Cell Anal Carcinoma:

Survival and Risk Factors for Recurrence
Jeremie H. Lefe`vre, MD
1
, Hele`ne Corte, MD
1
, Emmanuel Tiret, MD
1
, David Boccara, MD
2
, Marc Chaouat, MD
2
,
Emmanuel Touboul, MD
3
, Magali Svrcek, MD, PhD
4
, Magalie Lefrancois, MD
1
, Conor Shields, MD
1
,
and Yann Parc, MD, PhD
1
1
Department of Digestive Surgery, Hopital Saint-Antoine, AP-HP, Universite Pierre et Marie Curie, Paris, France;
2
Department of Plastic Surgery, Hopital Saint-Louis, AP-HP, Universite Diderot Paris VII, Paris, France;
3
Department of
Radiotherapy, Hopital Tenon, AP-HP, Universite Pierre et Marie Curie, Paris, France;
4
Department of pathology, Hopital
Saint-Antoine, AP-HP, Universite Pierre et Marie Curie, Paris, France
ABSTRACT
Background. Despite the results of combined chemora-
diation therapy for anal canal squamous cell carcinoma
(SCC), up to 30 % of patients will undergo abdominoper-
ineal resection (APR). The aim of this study was to
evaluate oncologic outcomes, survival, and recurrence,
following APR for anal canal SCC performed in a single
center over a 13-year period.
Methods. All patients who underwent APR for anal canal
SCC between 1996 and 2009 were retrospectively inclu-
ded. Demographic data, details on treatments, pathological
report, and follow-up were noted. Survival curves were
plotted using the KaplanMeier method and potential
prognostic factors were evaluated using Cox proportional
hazards models.
Results. A total of 105 patients (77 women) were inclu-
ded. Indications for APR included tumor persistence
(n = 42; 40 %), recurrence (n = 55; 52.4 %), or a con-
traindication to radiotherapy (n = 8; 7.6 %). Median
follow-up was 33.3 months (range, 1.5174.3 months).
Overall survival and disease-free survival were, respec-
tively, 61 and 48 % at 5 years. In multivariate analysis,
tumor stage (T3 or T4), positive margin on pathologic
examination and existence of distant metastases at the time
of the surgery were associated with a poor prognosis. The
indication for APR (persistent vs recurrent disease), gen-
der, concurrent HIV infection, or performance of a VRAM
ap did not inuence OS or DFS. Overall recurrence rate
was 42.6 % (n = 43 of 101). The type of recurrence did
not exert a signicant effect on survival (p = .4571).
Conclusion. This study describes the largest single series
of APR for anal carcinoma. Major prognostic factors for
survival and recurrence were T status and involved margin.
The 5-year overall survival was 60 %.
Since the pioneering work of Nigro et al., primary rad-
ical surgery for anal canal squamous cell carcinoma (SCC)
has been superseded by combined chemotherapy and
radiation therapy, resulting in 5-year survival rates of up to
80 % and a median overall survival of 7.6 years.
16
Despite these results of nonsurgical therapy, up to 30 % of
patients will undergo abdominoperineal resection (APR)
for persistence after radiotherapy or tumoral recur-
rence.
711
Long-term survival rates range widely from 40
to 60 %, reecting the heterogeneity in neoadjuvant ther-
apy and the individual characteristics of both patients and
tumors. The formulation of guidelines on the management
of these patients is confounded by the small size of the
published series, and the length of time over which patients
were accrued.
10,12
Some prognostic factors are well
established, including an involved margin or tumor
size.
10,13
However, other factors, such as the indication for
APR (recurrence vs persistence), are still ill dened.
10,14,15
The aim of this study was to evaluate oncologic out-
comes, survival, and recurrence, and to identify prognosis
features following APR for anal canal SCC performed in a
single center over a 13-year period.
Society of Surgical Oncology 2012
First Received: 27 June 2011;
Published Online: 24 July 2012
J. H. Lefe`vre, MD
e-mail: jeremie.lefevre@sat.aphp.fr
Ann Surg Oncol (2012) 19:41864192
DOI 10.1245/s10434-012-2485-1
METHODS AND PATIENTS
All patients who underwent APR for anal canal SCC
between January 1996 and November 2009 were included.
The diagnosis of SCCwas conrmed by biopsy and histology
in all cases. Demographic data, details on neoadjuvant
treatment, surgical procedure, signicant perioperative and
postoperative events, and histology were collated and
reviewed. Follow-up was obtained using clinic les for
patients followed in our department or with telephone inter-
views by a physician (JHLand HC) for the remaining patients
(calling family doctor/GP or patient himself/herself).
Management of anal tumor was based upon current rec-
ommendations: after a rst clinical examination, an initial
radiation dose of 4046 Gy was delivered. Patients were
then evaluated 45 weeks after with regard to response and
if a complete or nearly complete tumor ([50 %) regression
was achieved, a complementary radiotherapy to a total dose
of 6064 Gy was delivered. Conversely, if the tumor
response was questionable after 4046 Gy, or in presence of
radiation-induced morbidity (rectovaginal stula, major
fecal incontinence) the patient underwent APR. After
completion of radiotherapy, a persistent ulceration or a
re-emergence of the lesion within 6 months of radiotherapy
was classied as residual disease, while lesions appearing
after 6 months post-therapy were classied as a recurrence.
Surgical Procedure
APR was performed in a manner described previously.
14
Briey, extensive resection, when indicated, included
posterior colpectomy for women and partial prostatectomy
for men (removing a signicant portion of the gland if
needed). Primary closure with omentoplasty, pedicalized
on the left gastroepiploic vessels, was performed when
possible. When not feasible, reconstruction was performed
with a vertical rectus abdominis muscle (VRAM) ap, as
described before.
16
The original technique, which Taylor
described, has been modied to include an oblique paddle
to allow a larger area of skin to be harvested for recon-
struction. The VRAM ap has been performed since 1999
in our department. Preoperative assessment for the ap
includes ultrasound examination to verify the patency of
the inferior epigastric vessels. No coloperineal anastomosis
was performed during the study period.
Patients were followed up every 6 months during the
rst 5 years with a clinical exam, blood test (SCC Ag), and
a radiologic exam (CT scan/ultrasound alternatively).
Statistical Analysis
Results are presented as mean standard deviation and
were subjected to t test. Contingency tables were analyzed
by chi-square test. A p value of \.05 was regarded as
signicant. Survival curves were plotted using the Kaplan
Meier method.
17
Potential prognostic factors were evalu-
ated using Cox proportional hazards models.
18
For each
outcome, factors achieving a p value\.20 in the univariate
analysis were included in a multivariable model. A back-
ward stepwise variable selection procedure was used to
remove factors with p value [.05 in the multiple model.
Analyses were carried out using StatView software (Ver-
sion 5, 19921998, SAS Institute Inc., Cary, NC).
RESULTS
Patient Cohort
Between 1996 and 2009, 105 consecutive patients
underwent an APR for SCC of the anal canal. No patients
were excluded fromthe study. The clinical, pathological, and
neoadjuvant treatment data are summarized in Table 1.
There were 77 women (73.3 %). All but 8 patients received
radiotherapy or radiochemotherapy prior to surgery. Of these
8 patients, 7 had previously undergone radiotherapy [endo-
metrial cancer (n = 2), cervical cancer (n = 3), ovarian
cancer (n = 1), seminoma (n = 1)], while the last patient
was deemed unt due to systemic sclerosis. Radiotherapy
was combined with 5FU (n = 70) and/or cisplatin (n = 64).
Indications for APR included tumor persistence
(n = 42; 40 %), recurrence (n = 55; 52.4 %), or a con-
traindication to radiotherapy (n = 8; 7.6 %). Details of the
surgical procedure and histology are described in Table 2.
TABLE 1 Patient characteristics before abdominoperineal resection
for anal cancer (n = 105)
n (%)
Women 77 (73.3 %)
Body mass index (kg/m
2
) 23.9 14.9, 22.7 (1639)
HIV-infection 12 (11.2 %)
Age at the time of diagnosis 57.9 12.9, 55.5 (30.386.1)
TNM stage at the time of diagnosis 83 (79 %)
Stage I 1 (0.95 %)
Stage II 37 (44 %)
Stage IIIA 26 (35.2 %)
Stage IIIB 18 (17.1 %)
Stage IV 1 (0.95 %)
Not available 22 (20.9 %)
Neoadjuvant treatment
Radiotherapy 99 (92.5 %)
Mean dose (Gy) 56.1 18.4, 60 (072)
Concomitant chemotherapy 77 (73.3 %)
Results are expressed as the mean standard error, median (range)
for continuous variables and N (%) for categorical variables
Abdominoperineal Excision for Anal Canal Cancer 4187
The VRAM technique was mainly used in patients with T3
or T4 stage disease [35 of 51 (68.6 %) vs 16 of 51
(31.4 %); p = .005]. The incidence of involved margins on
histological examination was not statistically different
between the 2 perineal closure techniques: 23.5 % (n = 12
of 51) in the VRAM group and 13.2 % (n = 7 of 53) in the
remaining patients (p = .06). There was a trend toward a
higher rate of histological margin involvement in the T3
T4 cohort (14 of 57, 24.6 %) than in the T0T2 group (5 of
48, 10.4 %), (p = .0607).
Mortality and Morbidity
The mortality rate 2 months after surgery was 2.1 %
(n = 2). The 2 patients died at 45 and 51 days of septic
complications. Also, 35 patients had at least 1 complication
(33.3 %), resulting in 21 reoperations (20 %). Morbidity
was due to perineal wound problems in 50 % of the
patients, leading to 11 early reinterventions. Other reasons
were small bowel obstruction (n = 4) and various causes
(n = 5) (i.e., cholecystitis, wound hernia, ureteral drainage,
stoma refection, Bartholinitis).
Overall and Disease-Free Survival
Mean follow-up time, starting from the time of surgery,
was 44.3 37.2 months, with a median of 33.3 months
(range, 1.5174.3). It was comparable between patients who
had APR for recurrence and for persistence of the disease
(p = .3378). Follow-up fromthe time of diagnosis was either
comparable between the 2 indications of APR (55.6
40.3 months for patients with a persisting tumor vs 67.0
39.3 months for patients with a tumoral recurrence, p =
.1645). Overall survival (OS) and disease-free survival (DFS)
curves are shown in Fig. 1a. OS and DFS were, respectively,
85 and 84 % at 1 year, 66 and 58 % at 3 years, and 61 and
48 % at 5 years. Median OS was 77.7 months, and median
DFS was 40 months. There were 6 patients who died of
unrelated disease processes [trauma (n = 2); stroke (n = 2),
pancreatic cancer (n = 1), hepatocellular carcinoma
(n = 1)]. The 5-year cancer-specic survival was 65.8 %.
Univariate and multivariate analysis for OS and DFS are
reported in Table 3. In the multivariate analysis, tumor size
(T3 or T4), positive margin on pathologic examination and
existence of distant metastases at the time of the surgery were
associated with a poor prognosis. The impact of involved
margins on overall survival is shown on Fig. 1b. The 5-year
survival was 69 % for patients with a R0 resection, and zero
for patients with an invaded margin (p \.0001). The indi-
cation for APR (persistent vs recurrent disease), gender,
concurrent HIV infection, or performance of a VRAM ap
did not inuence OS or DFS. OS was not signicantly dif-
ferent between patient operated on for persisting tumor or a
recurrent cancer even with follow-up starting at the time of
diagnosis and not the time of surgery (Fig. 1c). However, the
8 patients operated on without chemoradiotherapy (RCT) had
a signicant worse prognosis (p = .041).
Recurrence
Overall recurrence rate (after exclusion of the 4 patients
with synchronous metastatic disease at the time of surgery)
was 42.6 % (n = 43 of 101). Recurrences were located in
local area [n = 17 (16.8 %)], inguinal nodes (n = 12;
11.9 %), or distant metastasis (n = 14; 13.9 %). The type
of recurrence did not exert a signicant effect on survival
as shown in Fig. 1d (p = .4571). Risk factor analysis for
local or distant recurrence is detailed in Table 4.
TABLE 2 Surgical procedure and histological ndings (N = 105)
Characteristics n (%)
Age at the time of surgery (years) 59.5 12.8, 57.3
(31.688)
Delay between the diagnosis and the APR
(months)
15.3 14.9, 11.6
(0.492.4)
Associated procedures
Posterior colpectomy 60/77 (77.9 %)
Partial prostatectomy 4/30 (13.3 %)
Hysterectomy 4/77 (5.2 %)
Ovariectomy 2/77 (2.6 %)
Partial resection of the coccyx 1 (1 %)
Partial resection of the bulbo-cavernous
muscle
1 (1 %)
Cystoprostatectomy 1 (1 %)
Iliac nodes resection 2 (2 %)
Hepatic metastasectomy 3 (2.8 %)
Wound healing procedures
Omentoplasty 46 (42.9 %)
VRAM 51 (48.6 %)
Cecoplasty 4 (4.2 %)
Immediate perineal closure 97 (90.6 %)
Hospital stay 26.7 14.5, 19
(8260)
Histological results
Stage 0 14 (13.3 %)
Stage I 10 (9.5 %)
Stage II 36 (34.3 %)
Stage IIIA 32 (30.5 %)
Stage IIIB 11 (10.5 %)
Stage IV 4 (3.8 %)
Resection R0 86 (81.9 %)
Resection R1 19 (18.1 %)
Results are expressed as the mean standard error, median (range)
for continuous variables and N (%) for categorical variables
VRAM vertical rectus abdominis muscle
4188 J. H. Lefe`vre et al.
DISCUSSION
In the present work, we report the oncologic results of
patients undergoing APR in a large cohort of 105 patients
over a 13-year period. This series is one of the largest ever
published on the surgical results of APR for anal canal
SCC. Overall survival was 60 % at 5 year with a major
inuence of T stage, histological margins, and presence of
distant metastases. The indication of APR (i.e., recurrence
or persisting tumor) was no longer a prognostic factor.
Recurrence rate was 40 %, and the location of the recur-
rence did not inuence survival.
SCCof the anal canal accounts for only 12 %of all lower
gastrointestinal cancers and nearly 4 % of anorectal carci-
nomas (included anal and low rectal cancer).
19
The gold
standard treatment is chemoradiotherapy, but mutilating
surgery such as abdominoperineal resection (APR) is still
required in about 30 % of patients for persistent or recurrent
disease.
7,10,20
Because of the relative infrequency of this
carcinoma, many studies examining APR for anal canal
cancer contain small numbers or include patients accrued
over a very long period of time, inducing a certain degree of
bias. Initial studies even described different conclusions
regarding the impact of the indication (i.e., recurrence or
persistence) of the APR.
14,15
We have already published on
the inuence of the VRAM ap on perineal healing after
APR.
21
The present series allowed analysis of inuencing
factors on survival and recurrence following APR.
Regarding overall survival in this study, 60 % at 5 years
compares favorably with recent studies that report a range
of 5264 % (Table 5).
10,12,15
However, in other series,
patients with rT3 or rT4 tumors comprised only between 13
and 35 %. In this series, such patients represent more than
half of the cohort (n = 57; 54.3 %) indicating favorable
survival despite the tumor size. Comparison on the basis of
histology is not easy, as in many series, the details of the
postoperative pathology are not provided.
12,15,22,23
In the present study, the main factors inuencing sur-
vival and recurrence were T status, margin status, and the
presence of metastases at the time of surgery. These factors
OS
DFS
1.00
0.75
0.50
0.25
100 0
Time (months)
a
Percent
survival
20 40 60 80
R0
R1
1.00
0.75
0.50
0.25
100 0
Follow-up (months)
b
Percent
survival
20 40 60 80
Persistance
Recurrence
No RCT
1.00
0.75
0.50
0.25
100 0
Follow-up (months)
c
Percent
survival
20 40 60 80
Inguinal
Local
Metastatic
1.00
0.75
0.50
0.25
100 0
Follow-up (months)
d
Percent
survival
20 40 60 80
FIG. 1 a Overall survival (OS)
and disease-free survival (DFS)
curves. b Impact of tumoral
margin on overall survival
(p \.0001). c Overall survival
from the time of diagnosis and
depending on the indication of
abdominoperineal resection
(p = .041). d Overall survival
depending on the site of
recurrence, log-rank test
(p = .4571)
Abdominoperineal Excision for Anal Canal Cancer 4189
are also identied in other series.
13,2325
The impact of an
involved margin is signicant with a 5-year survival of 0 %
in this study. This observation emphasizes the importance
of optimal surgical technique and the requirement for
aggressive resection (if necessary, larger tissue resection,
colpectomy, or prostatectomy). The performance of large
resections facilitated by ap reconstruction may explain the
absence of macroscopic residual tumor tissue (R2) in this
cohort with advanced tumors.
Multivariable analysis of factors inuencing tumor
recurrence revealed that resection margin (R1) and the size
of the tumor (T3 or T4) had a signicant impact. Despite
larger tumors and a greater degree of R1 margin involve-
ment in the VRAM ap cohort, overall survival did not
differ from the primary closure cohort.
With regard to the inuence of HIV infection on overall
survival and disease-free survival, we did not nd a sig-
nicant inuence, in contrast to other studies.
26
The
indication for APR (i.e., recurrence or persisting disease),
previously described as a signicant prognostic factor, was
not found in the present study to demonstrate an impact
upon survival.
14,15
This result is probably explained by the
larger number of patients included in our cohort. Indeed,
Mariani et al. included 83 patients and did not nd that the
indication for APR impacted upon survival.
10
Even with a
follow-up starting from the time of diagnosis, the survival
was similar between patients with a recurrence or a per-
sisting tumor, while one could have expected a longer
survival for patients with a recurrent tumor. In the present
series, patients with an APR without neoadjuvant radio-
chemotherapy had a signicantly worse survival than the
remaining patients. Moreover, the indication of APR had
no inuence on the localization of the recurrence.
T status and involved margins are denitively the major
prognosis factors. Accordingly, further studies are needed
to assess the role of preoperative treatment and eventually
the indications for adjuvant chemotherapy after APR if
histology reveals involved margins. To improve survival
and recurrence results for these patients, a therapeutic
option could be to improve number of R0 resection, with
enlarging resection margins (which is easier with the
ap reconstruction). Another possibility could be a better
TABLE 3 Univariate and multivariate analysis of overall and dis-
ease free survival (N = 105)
Variable Univariate
analysis
p value
Multivariate analysis
p value 95 % CI
Overall survival
Sex .65
Recurrence .3477
Age [56 .7019
VIH .9636
VRAM .5286
yp T3T4 .0005 .0056 2.76 (1.35.6)
N? .0798 NS
M1 .03 .0006 9.2 (2.632.7)
R1 \.0001 .0003 3.9 (1.98.0)
Disease-free survival
Sex .4913
Recurrence .3345
Age [56 .2754
VIH .6463
VRAM .4291
yp T3T4 .0001 .028 2.5 (1.44.6)
N? .0164 NS
M1 \.0001 \.0001 10.6 (3.531.7)
R1 \.0001 \.0001 4.1 (2.17.7)
NS not signicant, 95 % CI 95 % condence interval
TABLE 4 Multivariate analysis of risk factors of recurrences after
APR
Variable Univariate
analysis
p value
Multivariate analysis
p value 95 % CI
Local recurrence
Gender .9198
Age [56 .1683 NS
VIH .5257
No VRAM .4562
Tumoral recurrence .4994
yp T3T4 .0011 .0142 4.2 (1.413.3)
N? .0010 NS
R1 \.0001 \.0001 7.2 (2.917.9)
Metastatic recurrence
Gender .5049
Age [56 .3235
VIH NA
No VRAM .0189 NS
Tumoral recurrence .7233
yp T3-T4 .1932 NS
N? .1379 NS
R1 .2805
Inguinal recurrence
Gender .4311
Age [56 .1118 NS
VIH .4215
No VRAM .1650 NS
Tumoral recurrence .4028
yp T3T4 .0001 .0029 6.9 (1.924.4)
N? .0072 .0285 2.9 (1.17.6)
R1 .003 NS
NS not signicant, 95 % CI 95 % condence interval
4190 J. H. Lefe`vre et al.
preoperative staging, today better with the use of MRI, to
adapt preoperative treatment and extent of resection.
In conclusion, this study describes the largest single
series of APR for anal carcinoma. Major prognostic factors
for survival and recurrence were T status and involved
margin. The 5-year overall survival was 60 %. The use of a
VRAM ap was not associated with a reduction in local
recurrence, but facilitated a more extensive resection.
REFERENCES
1. Nigro ND, Vaitkevicius VK, Considine B Jr. Combined therapy
for cancer of the anal canal: a preliminary report. Dis Colon
Rectum. 1974;17:3546.
2. Epidermoid anal cancer: results from the UKCCCR randomised
trial of radiotherapy alone versus radiotherapy, 5-uorouracil,
and mitomycin. UKCCCR Anal Cancer Trial Working Party. UK
Co-ordinating Committee on Cancer Research. Lancet. 1996;
348:104954.
3. Flam M, John M, Pajak TF, Petrelli N, Myerson R, Doggett S,
et al. Role of mitomycin in combination with uorouracil and
radiotherapy, and of salvage chemoradiation in the denitive
nonsurgical treatment of epidermoid carcinoma of the anal canal:
results of a phase III randomized intergroup study. J Clin Oncol.
1996;14:252739.
4. Longo WE, Vernava AM 3rd, Wade, TP, Coplin, MA, Virgo, KS,
Johnson, FE. Recurrent squamous cell carcinoma of the anal
canal. Predictors of initial treatment failure and results of salvage
therapy. Ann Surg. 1994;220:409.
5. Bartelink H, Roelofsen F, Eschwege F, Rougier P, Bosset JF,
Gonzalez DG, et al. Concomitant radiotherapy and chemotherapy
is superior to radiotherapy alone in the treatment of locally
advanced anal cancer: results of a phase III randomized trial of
the European Organization for Research and Treatment of Cancer
Radiotherapy and Gastrointestinal Cooperative Groups. J Clin
Oncol. 1997;15:20409.
6. Northover J, Glynne-Jones R, Sebag-Monteore D, James R,
Meadows H, Wan S, et al. Chemoradiation for the treatment of
epidermoid anal cancer: 13-year follow-up of the rst randomised
UKCCCR Anal Cancer Trial (ACT I). Br J Cancer. 2010;102:
11238.
7. Peiffert D, Giovannini M, Ducreux M, Michel P, Francois E,
Lemanski C, et al. High-dose radiation therapy and neoadjuvant
plus concomitant chemotherapy with 5-uorouracil and cisplatin in
patients with locally advanced squamous-cell anal canal cancer:
nal results of a phase II study. Ann Oncol. 2001;12:397404.
8. Staib L, Gottwald T, Lehnert T, Ruf G, Sturm J, Becker HD, et al.
Sphincter-saving treatment in epidermoid anal cancer: coopera-
tive analysis of 142 patients in ve German university surgical
centers. Int J Colorectal Dis. 2000;15:28290.
9. Deniaud-Alexandre E, Touboul E, Tiret E, Sezeur A, Houry S,
Gallot D, et al. [Epidermoid carcinomas of the anal canal treated
with denitive radiation therapy in a series of 305 patients].
Cancer Radiother. 2003;7:23753.
10. Mariani P, Ghanneme A, De la Rochefordiere A, Girodet J,
Falcou MC, Salmon RJ. Abdominoperineal resection for anal
cancer. Dis Colon Rectum. 2008;51:1495501.
11. Roohipour R, Patil S, Goodman KA, Minsky BD, Wong WD,
Guillem JG, et al. Squamous-cell carcinoma of the anal canal:
predictors of treatment outcome. Dis Colon Rectum. 2008;51:
14753.
12. Mullen JT, Rodriguez-Bigas MA, Chang GJ, Barcenas CH, Crane
CH, Skibber JM, et al. Results of surgical salvage after failed
chemoradiation therapy for epidermoid carcinoma of the anal
canal. Ann Surg Oncol. 2007;14:47883.
13. Akbari RP, Paty PB, Guillem JG, Weiser MR, Temple LK,
Minsky BD, et al. Oncologic outcomes of salvage surgery for
epidermoid carcinoma of the anus initially managed with com-
bined modality therapy. Dis Colon Rectum. 2004;47:113644.
14. Pocard M, Tiret E, Nugent K, Dehni N, Parc R. Results of salvage
abdominoperineal resection for anal cancer after radiotherapy.
Dis Colon Rectum. 1998;41:148893.
15. Nilsson PJ, Svensson C, Goldman S, Glimelius B. Salvage
abdominoperineal resection in anal epidermoid cancer. Br J Surg.
2002;89:14259.
TABLE 5 Comparison of the former series on APR for anal squamous cell cancer
Study, year Period n T3T4
at initial
treatment
Median
of follow-up
(months)
Median of
5-year OS
VRAM Recurrence
rate
Ellenhorn 1994
27
19811993 38 NA 47 44 % 0 60.5 %
Pocard 1998
14
19861995 21 NA 40 33 % 0 38.1 %
Van der Wal 2001
28
19801998 17 NA 53 47 % 9 (52.9 %) NA
Nilsson 2002
15
19852000 35 37.1 % 33 52 % 0 42.8 %
Akbari 2004
13
19802001 55 NA 24.2 33 % 0 42.3 %
Ferenschild 2005
29
19852000 18 6 % 16 30 % 4 (22.2 %) 89 %
Ghouti 2005
22
19872002 36 58.3 % 67 69.4 % 10 (27.8 %) 64 %
Renehan 2005
23
19882000 70 NA 45 40 % 2 (2.8 %) NA
Mullen 2007
12
19902002 31 13 % 29 64 % 14 (45.2 %) 38.7 %
Schiller 2007
25
19882006 40 35 % 18 39 % 18 (45 %) 52 %
Vorobev 2008
30
19952007 39 NA NA 69 % 0 NA
Rouquie 2008
31
19872007 95 NA 66 53 % 2 (2.1 %) NA
Mariani 2008
10
19692003 83 35 % 104 56.5 % 0 20.7 %
Present study 19962009 105 59.2 % 33 60 % 51 (48.7 %) 40.9 %
OS overall survival, VRAM vertical rectus abdominis muscle
Abdominoperineal Excision for Anal Canal Cancer 4191
16. Bell SW, Dehni N, Chaouat M, Lifante JC, Parc R, Tiret E.
Primary rectus abdominis myocutaneous ap for repair of peri-
neal and vaginal defects after extended abdominoperineal
resection. Br J Surg. 2005;92:4826.
17. Kaplan EL, Meier P. Nonparametric estimation from incomplete
observations. J Am Stat Assoc. 1958;53:45781.
18. Cox DR. Regression models and life-tables. J R Stat Soc B.
1972;34:187220.
19. Fuchshuber PR, Rodriguez-Bigas M, Weber T, Petrelli NJ. Anal
canal and perianal epidermoid cancers. J Am Coll Surg. 1997;
185:494505.
20. Ryan DP, Compton CC, Mayer RJ. Carcinoma of the anal canal.
N Engl J Med. 2000;16:792800.
21. Lefevre JH, Parc Y, Kerneis S, Shields C, Touboul E, Chaouat M,
et al. Abdomino-perineal resection for anal cancer: impact of a
vertical rectus abdominis myocutaneous ap on survival, recur-
rence, morbidity, and wound healing. Ann Surg. 2009;250:
70711.
22. Ghouti L, Houvenaeghel G, Moutardier V, Giovannini M,
Magnin V, Lelong B, et al. Salvage abdominoperineal resection
after failure of conservative treatment in anal epidermoid cancer.
Dis Colon Rectum. 2005;48:1622.
23. Renehan AG, Saunders MP, Schoeld PF, ODwyer ST. Patterns
of local disease failure and outcome after salvage surgery in
patients with anal cancer. Br J Surg. 2005;92:60514.
24. Hill J, Meadows H, Haboubi N, Talbot IC, Northover JM.
Pathological staging of epidermoid anal carcinoma for the new
era. Colorectal Dis. 2003;5:206-13.
25. Schiller DE, Cummings BJ, Rai S, Le LW, Last L, Davey P, et al.
Outcomes of salvage surgery for squamous cell carcinoma of the
anal canal. Ann Surg Oncol. 2007;14:27809.
26. Wexler A, Berson AM, Goldstone SE, Waltzman R, Penzer J,
Maisonet OG, et al. Invasive anal squamous-cell carcinoma in the
HIV-positive patient: outcome in the era of highly active anti-
retroviral therapy. Dis Colon Rectum. 2007;51:7381.
27. Ellenhorn JD, Enker WE, Quan SH, Salvage abdominoperineal
resection following combined chemotherapy and radiotherapy for
epidermoid carcinoma of the anus. Ann Surg Oncol. 1994;1:
10510.
28. van der Wal BC, Cleffken BI, Gulec B, Kaufman HS, Choti MA.
Results of salvage abdominoperineal resection for recurrent anal
carcinoma following combined chemoradiation therapy. J Gas-
trointest Surg. 2001;5:3837.
29. Ferenschild FT, Vermaas M, Hofer SO, Verhoef C, Eggermont
AM, de Wilt JH. Salvage abdominoperineal resection and peri-
neal wound healing in local recurrent or persistent anal cancer.
World J Surg. 2005;29:14527.
30. Vorobev GI, Shelygin IuA, Nechushkin MI, Rybakov EG.
Results of surgical treatment of residual and recurrent anal
tumors. Khirurgiia (Mosk). 2008;(8):49. In Russian.
31. Rouquie D, Lasser P, Castaing M, Boige V, Goere D, Pignon JP,
et al. Complete (R0) resection is the only valid prognostic factor
in abdominoperineal resection for recurrent cancer of the anal
canal (a consecutive series of 95 patients). J Chir (Paris).
2008;145:33540 (In French).
4192 J. H. Lefe`vre et al.
Copyright of Annals of Surgical Oncology: An Oncology Journal for Surgeons is the property of Springer
Science & Business Media B.V. and its content may not be copied or emailed to multiple sites or posted to a
listserv without the copyright holder's express written permission. However, users may print, download, or
email articles for individual use.