Sphincter Saving Surgeries for Locally Advanced Low Rectal Cancer after Neoadjuvant Chemoradiation

doi:10.4236/jct.2013.47143

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Journal of Cancer Therapy, 2013, 4, 1228-1235

http://dx.doi.org/10.4236/jct.2013.47143 Published Online September 2013 (http://www.scirp.org/journal/jct)

Sphincter Saving Surgeries for Locally Advanced Low

Rectal Cancer after Neoadjuvant Chemoradiation

Mohamed A. E. Salem1*, Hamza A. Hamza2, Gamal Amira3, Abeer E. Ibrahium4, Ahmed A. S. Salem1

1Surgical Oncology Department, South Egypt Cancer Institute, Assiut University, Assiut, Egypt; 2Radiation Oncology Department,

South Egypt Cancer Institute, Assiut University, Assiut, Egypt; 3Surgical Oncology Department, National Cancer Institute, Cairo

University, Cairo, Egypt; 4Medical Oncology Department, South Egypt Cancer Institute, Assiut University, Assiut, Egypt.

Email: *[email protected]

Received May 28th, 2013; revised June 28th, 2013; accepted July 2nd, 2013

License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

Background: Rectal cancer accounts for the largest distribution within one anatomical region of the large bowel, with

approximately one third of all CRC located within the rectum. The Golden standard treatment of primary rectal cancer

is curative surgical resection; however, affine balance remains between disease cure and restoration of gastrointestinal

continuity. Combined modality has proven efficacy in many malignant tumors with advantage of organ preservation.

Methods: Forty nine (49) patients with low rectal carcinoma were included in a prospective study, between Jan 2007

and Jan 2012. Preoperative chemoradiation was administrated to all patients and subjected to different techniques of

sphincter saving surgery. Stage I and Stage IV disease at diagnosis were excluded from the study. Results: Forty nine

patients were included in the study. 27 (55%) patients were male and 22 (45%) were female; the age ranges from 23

years to 70 years with the median age 46 years. The main presenting symptoms were bleeding per rectum and tenesmus,

Stage II 18 patients (36.7%), stage III 31 patients (63.3%). Complete clinical and pathological response in 3 patients

(6%), and complete clinical response with only microscopically residual carcinoma in 20 patients (41%), partial re-

sponse in 18 patients (36.7%), and no significant response in 8 patients (16%) 7 from 8 were mucoid carcinoma. Low

anterior resection (LAR) in 22 patients (44.9%), Hartman’s procedure in 4 patients (8.1%), Coloanal pull-through (COP)

was done in 19 patients (38.9%) and perineal colostomy in 4 patients (8.1%). For patients with colo-anal pull-through

technique complete dehiscent and retraction observed in 2 cases, Major leakage in one case, stenosis in 4 cases. Con-

clusion: There is tendency of colorectal cancers to affect younger groups. Most patients presented in advanced stage.

Neadjuvant chemo radiation is an excellent tool in sphincter saving surgery. Coloanal pull-through technique is not a

widely spread technique for low rectal cancer with good oncological safety and acceptable functional outcome.

Keywords: Coloanal Pull-Through; Colo Rectal Cancer; Neoadjuvant Chemoradiation; Low Anterior Resection

1. Introduction

Rectal cancer accounts for the largest distribution within

one anatomical region of the large bowel, with approxi-

mately one third of all CRC located within the rectum.

The Golden standard treatment of primary rectal cancer

is curative surgical resection; however, a fine balance

remains between disease cure and restoration of gastro-

intestinal continuity. Combined modality has proven ef-

ficacy in many malignant tumors with advantage of or-

gan preservation.

Cancers of the distal rectum pose the double problem

of local tumor control and sphincter preservation. Ab-

dominoperineal resection (APR), long considered as the

standard treatment of tumors with a distal edge located

up to 6 cm from the anal verge, provides local control in

a substantial majority of cases, but the resulting loss of

sphincter function represents a psychological burden for

many patients [1,2]

Surgery alone has been the standard treatment for pa-

tients with adenocarcinoma of the cancer rectum. Despite

advances in surgical technique, local recurrence is still a

considerable problem [3]. At time of initial presentation,

approximately 15% of the patients diagnosed with rectal

cancer have locally advanced unresectable disease [4,5].

A more precise understanding of failure patterns,

leading to the acceptance of distal margins of less than 2

cm, and the recent progress in bowel stapling techniques

have made coloanal anastomoses feasible after low rectal

*Corresponding author.

Sphincter Saving Surgeries for Locally Advanced Low Rectal Cancer after Neoadjuvant Chemoradiation 1229

excision. This latter approach is often associated with

preoperative radiotherapy (RT), which may be consid-

ered to compensate for the limitations of the surgical

technique resulting from narrow radial and distal surgical

margins [6-8].

Primary end points of this study to:

1) Assess the pathological response after CT based de-

lineation 3DCRT concurrently with fluorouracil;

2) Feasibility of sphenteric preservation after neoad-

juvant chemoradiation;

3) Quality of life after different surgical techniques af-

ter chemoradiation to preserve anal sphincter.

Secondary end point is disease free survival and OAS.

2. Patients and Methods

From Jan 2007 to Jan 2012, 49 consecutive patients with

primary cancers involving the distal rectum (up to 6 cm

or less from the anal verge) were treated by preoperative

RT, with concomitant chemotherapy, at the South Egypt

Cancer Institute, Assiut University, Assiut, Egypt.

The aim of the preoperative chemo-radiation was es-

sentially to achieve down-staging in T2 tumors, while for

T3 tumors the aim was both improvement of local con-

trol and down-staging.

2.1. Inclusion Criteria

Patients had to present histologically confirmed adenoca-

rinoma of the rectum without evidence of distant metas-

tases, and the inferior edge of the tumor had to be located

not further than 6 cm from the anal verge. Only Interna-

tional Union Against Cancer (UICC) T2-T4, N0 or N1

tumors staged were included. The tumor should not in-

volve more than two-thirds of the rectal circumference to

be accessible to CXR therapy. Patients with a perform-

ance status ≤ 2 according to the Eastern Cooperative On-

cology Group (ECOG) system.

2.2. Exclusion Criteria

Previous pelvic irradiation therapy; Previous history of

malignant disease; Any other serious illness and/or major

organ dys-function; Pregnancy or lactation.

Pretreatment evaluation included physical examination,

proctoscopy and/or colonoscopy, abdominal/pelvic com-

puterized tomography (CT) and/or MRI, chest X-ray and

serum carcinoembryonic antigen (CEA).

The distance between anal verge and the caudal edge

of the tumor was assessed by proctoscopy and/or digital

examination.

The preoperative tumor classification was determined

using information from the digital examination (includ-

ing assessment of mobility), CT and/or MRI scan and/or

trans-rectal ultrasound, when available. Pretreatment pa-

tient characteristics are displayed in Table 1.

Table 1. pretreatment patient characteristics.

Age range (mean) 23 - 70 Ys (46 Ys)

Male/female 27/22

Distance from anal verge to the

lower tumor edge (cm)

Mean

2 - 6 cm

4 cm

Stage

Stage II (T3-T4,N0)

Stage III ( T2-T4,N1) only

18 (36.7%)

31 (63.3%)

2.3. Preoperative Therapy

On conventional simulator using prone position with full

bladder which provide maximal displacement of small

bowel out of the pelvis. We use lasyer for patient posi-

tioning and immobilization. We use CT and at the same

isocenteric position, multiple CT cuts at 0.5 cm interval

throughout the entire volume. CT data then transferred to

the computer planning system (Version Xio-Release 4.2).

At each CT slice, we delineates our target volumes

(CTV1, CTV2, CTV3, PTV) CTV1 (peri-rectal, presac-

ral, internal iliac regions) the caudal extent of this elec-

tive target volume should be a minimum of 2 cm caudal

to gross disease, including coverage of the entire meso-

rectum to the pelvic floor. Unless there is radiographic

evidence of extension into the ischiorectal fossa, exten-

sion of: CTV1 does not need to go more than a 5 milli-

meters beyond the levator muscles. For very advanced

rectal cancers, extending through the mesorectum or the

levators, we add 2 cm margin up to bone wherever the

cancer extends beyond the usual compartments.

CTV2: if there is any extension into gynecologic, geni-

tourinary structures or anal canal, the external iliac re-

gion should be added. We added 7 - 8 mm margin in soft

tissue around the external iliac vessels, but one should

consider a larger 10+ mm margin anterolaterally espe-

cially if small vessels or nodes are identified in this area.

CTV3: boost clinical target volume extend to entire

mesorectum and presacral region at involved levels, in-

cluding 2 cm cephalic and caudal in the mesorectum and

2 cm on gross tumor within the anorectum.

PTV margin of 0.7 cm around CTV, except at skin re-

sulting in PTV1, PTV2 and PTV3 around CTV1, CTV2

and CTV3 respectively.

A complete 3D plan done with tissue inhomogeneity

correction taking inconsid-eration normal tissue toller-

ance as the femoral head and neck, and intestine.

We delivered 4500 cGy in 25 fractions to PTV1 and

PTV2 then boost 540 cGy in 3 fractions to PTV3.

Chemotherapy

Laboratory studies: CBC, serum albumin, bilirubin, AST,

ALT, ALP, urea, creatinin and CEA before chemother-

apy.

Sphincter Saving Surgeries for Locally Advanced Low Rectal Cancer after Neoadjuvant Chemoradiation

1230

Chemotherapy regimen: 5-flourouracil 400 mg/m2 +

leucovorin 20 mg/m2 D1-4 of first and fifth week of ra-

diation

2.4. Surgery

Surgery was performed at a median interval of 25 days

(range 20 - 40 days) from completion of chemo radiation.

Low anterior resection was done in 22 (44.9%) patients

(9 with coloanal and 13 with colorectal anastomoses), 4

(8.1%) patients under continent perineal colostomy, 4

(8.1%) patients under Hartman’s procedures and subse-

quent continuity using surgical stapler and coloanal pull

through was done in 19 (38.9%) patients (34.7%) for

those patients where low anterior resection is not on-

cologically save and the only alternative is APR. A tem-

porary transverse colostomy was performed in 10 pa-

tients and temporary ileostomy in 5 patients.

2.4.1. Techniques of Transanal Pull-Through

The idea for transanal pull through was taken from man-

agement of Hirschsprung’s Disease. In patients undergo-

ing transanal pull through with coloanal anastomosis, the

technique was standardized according to the following

steps: The left colon with the splenic flexure was mobi-

lized after ligature and section of the inferior mesenteric

vein and artery. The mesosigmoid was then mobilized

and the plane of the mesorectum was entered in continu-

ity as the dissection proceeded distally (Figure 1). This

plane was followed down to the level of the pelvic floor

when a total mesorectal excision (TME) was performed

[9]. The dissection of the rectum and mesorectum was

performed applying slight lateral traction to open the

cleavage plane between the mesorectum and the lateral

wall of the pelvis. This allowed clear visualization and

preservation of the pelvic autonomic nerves. Transaction

of rectum at least 2 cm below tumor growth with presser-

vation of anal sphincter, Mucosectomy of any remaining

rectal mucosa, telescoping of colon (Figure 2) or ileal

loop (Figure 3) through the anus, the colo-anal anasto-

mosis was done from below between colon and the anal

canal with 2/0 absorbable sutures, the distal stump leave

to be ischemic and trimming done after 7 - 10 days post-

operative. Oral feeding started after regain bowel move-

ment.

2.4.2. Techniques of Continent Perineal Colostomy

After performing abdominoperineal resection, a 7 - 8 cm

smooth muscle colonic cuff was prepared from resected

segment of the sigmoid colon. Mesenteric fat and epip-

loic appendages were removed. The colonic tube was

then inverted and the mucosa was sharply dissected from

the sub mucosa. After a longitudinal incision along tinea

coli, a flap 3 to 4 cm wide and 7 cm long was created.

The neosphincter was created by first securing the flap to

Figure 1. Mesorectum dissection.

Figure 2. Coloanal pull through.

anti mesenteric portion of colon with interrupted 3 - 0

absorbable sutures. This was subsequently wrapped three

quarter turns through the rest 3 cm proximal to terminal

colon. The pull-through colon was matured at the skin

using interrupted 3 - 0 absorbable sutures in tension free

fashion.

3. Result

Forty nine (49) patients were included in the study. 27

(55%) patients were male and 22 (45%) were female, the

age range from 23 years to 70 years with the median age

46 years. The main presenting symptoms were bleeding

per rectum and Tenesmus. Stage II eighteen patients

(36.7%) and Stage III thirty one patients (63.3%).

All patients had a pretreatment biopsy diagnosis of

adenocarcinoma (11 well-differentiated, 18 moderately

differentiated, 7 poorly differentiated and 13 (26.5%)

mucoid carcinoma). Most cases of mucoid carcinoma (10

cases) were in young age under 40 years.

Neoadjuvant chemoradiation was administrated for all

patients. pathological evaluation of the resected specimen

show all circumferential resection margins were clear by

at least 1 cm , complete clinical and pathological response

in 3 patients (6%), and complete clinical response with

only microscopically residual carcinoma in 20 patients

(41%), partial response in 18 patients (36.7%), no sig-

nificant response in 8 patients (16%) 7 from 8 were

Sphincter Saving Surgeries for Locally Advanced Low Rectal Cancer after Neoadjuvant Chemoradiation 1231

Figure 3. Total colectomy with ileoanal pull through.

mucoid carcinoma.

Prophylactic stoma was preformed in 6 patients in

CAP and 9 patients of LAR. A closure of the diverting

stoma could be performed, on average, 18 weeks after

surgery. The closure rates were significantly lower in pa-

tients with anastomotic leakage. In one patient with clo-

sure of the colostomy and weak functional results, and in

one patient with recto-vaginal fistula, a permanent colo-

stomy was again performed after previous closure.

Major leakage occurs in 2 case of colo-anal pull through

due to ischemia of rectal stump and complete retraction

of the stump requiring refashioning in one case and re-

anastomosis in the other case and covering ileostomy.

One case of minor leakage managed conservatively.

For low anterior resection 1 case of major leakage man-

aged by covering ileostomy and 3 cases of minor leakage

managed conservatively.

Only one case with covering stoma develop minor

leakage which managed conservatively all case of conti-

nent perineal colostomy developed sever stenosis and fi-

brosis with poor continence requiring reconstruction of

terminal colostomy.

With a median follow-up of 26 months (range 4 - 72

months) from the start of RT, 10 (20.4%) patients have

died from their disease 4 in colo-anal pullthrough group

4 in low anterior resection group and 2 in continent per-

ineal colostomy. thirteen (26.5%) of 49 patients exhibited

tumor progression. Nine (18.3%) developed local recur-

rence; 4 in CAP group 4 in LAR group and 1 in CPC

group. Four patients had progress of disease without lo-

cal recurrence 2 in CAP patients 1 LAR and 1 in CPC.

Tumor progression was diagnosed at an average of 20

months (4 - 60 months).

The 4-year actuarial survival for all patients was 69%.

The 2-year actuarial locoregional control rates were

76.5% for all patients, 86% for the 14 patients with

marked pathological tumour response to chemoradiation.

No significant difference in disease-free survival was

observed between patients operated by LAR, Continent

perineal colostomy or by Trans anal pull through surgery.

The characteristics surgical types, surgical complica-

tion and functional outcome of patients (Table 2).

4. Disscussion

Historically, patients with mid to distal rectal cancers had

to undergo abdominoperineal resection to achieve ade-

quate oncological clearance. However, with better equip-

ment and improved surgical techniques, low anterior re-

section with a low colorectal or coloanal anastomosis has

become the technique of choice [10]. Two major issues

encountered in the surgical resection of low rectal can-

cers (tumor located <6 cm from anal verge) are tumor-

free surgical resection margin and adequate fields of

colo-anal pull-through anastomosis [11].

The beneficial effect of preoperative pelvic irradiation

as an adjuvant treatment has been confirmed in several

studies [12,13].

Preoperative radiochemotherapy decreases the tumor

volume, induces downstaging, and facilitates surgical re-

section. In addition, it transforms the vegetative compo-

nent of the tumor into an ulcerative scar, and this may

decrease intraoperative tumor seeding [14]. We observed

significant tumor regression 47%, This high rate of tu-

mor regression, compared with the 18% to 26% reported

after preoperative radiotherapy

alone [15,16],

is similar

to the 53% to 64% observed after preoperative radio-

therapy potentiated by che

motherapy [17-19].

Adding chemotherapy to preoperative radiotherapy

improve both local control and distal disease [14].

The

median age of our study is 46 years which younger

than age reported in other studies, where they reported

median age range from 59 - 70 years the exact cause

cannot be explained but may be due to genetic back-

ground or exposure to carcinogenic materials.

Sphincter Saving Surgeries for Locally Advanced Low Rectal Cancer after Neoadjuvant Chemoradiation

1232

Table 2. Sphincter-saving procedur e , surgical complication and functional outcome.

Colo anal pull through (COP) LAR (low anterior

resection) Continent perineal

colostomy

Gender

Male

Female

12 (63.1%)

7 (36.9%)

11 (50%)

4 (100%)

Age range

median age

23 - 62 years

42 years

31 - 70 years

48 years

35 - 55 years

43 years

Procedure Colo-anal pull through 18

Ileo-anal pull through 1

Stapler 9

Hand swing 13

Leakage

 Major

 Minor

2 (complete detachment & retracted

intra-abdominally)

Prophylactic stoma

 Colostomy

 Ileostomy

Postoperative stenosi s 5 (26%) 4 (18%) 4 (100%)

Urologic Complication 3 (15.8%) 1 (4.5%) No

Disease progression

 Local recurrence

 Distance metastasis

 Local and distance metastasis

3 (15.8%)

1 (5.3%)

2 (9%)

3 (13.6%)

1 (4.5%)

Functional outcome

 Continence for solid & liquid

stool & flatus

 Continence for solid stool & occasional

incontinence for liquid stool

 Soiling at night

 Frequent episodes of incontinence

for liquid stool

8 (42.1%)

5 (26.3%)

2 (10.6%)

15 (68.2%)

5 (22.7%)

1 (4.5%)

Most patients with rectal carcinoma can now be treat-

ed by sphincter-saving surgery, but many pay a price for

restoration of continuity. The “anterior resection syn-

drome” of faecal leakage and urgency of defaecation

may afflict up to 50 per cent of patients after low anterior

resection and is more common after very low colorectal

or coloanal anastomosis [20].

The recurrence rate in our study is 18.3% of the cura-

tively operated patients is in accordance with other studies

of this surgical procedure, where rates range from 0 to

30% [21-25].

The method of anastomosis (hand-sewn vs. stapled)

does not seem to influence recurrence rates [26].

Problems concerning the anastomosis, mostly insuffi-

ciencies, present the most common and widely discussed

complications in rectal surgery. The depth of the anas-

tomosis and the aim of a tension-free anastomosis in the

pull-through operation make high demands on the blood

supply of the colon. Most likely, the blood supply suffers

from the mobilization and the skeletonization of the

mesocolon.

Suture insufficiency plays a key role in postoperative

morbidity. The rate of this complication after CAA is

generally reported to be comparable with previous study

[21-23,27]. The correlation of this complication and neo-

adjuvant radiation (most likely by causing obliterating

endarteritis) was significant.

Stricture formation, a common problem at the site of

the anastomosis, occurred in 13 patients 26.5%, (five in

CAP and 4 of LAR and in 4 patients of CPC) in the pa-

tients in this study. This rate does not clearly differ from

the rates after deep anterior resection, although not much

Sphincter Saving Surgeries for Locally Advanced Low Rectal Cancer after Neoadjuvant Chemoradiation 1233

data exists for comparison. In general, this complication

is considered to be higher in stapled anastomosis [28].

The fistula formation was encountered in 1 (2%) pa-

tient developed rectovaginal fistula after LAR using sta-

pler techniques.

After deep anterior resection with stapled anastomosis,

the rate of fistula formation was approximately 2% [29].

In addition to rectal and gynecological surgery, radiation

and chemotherapy can typically lead to fistula formation

[30,31].

Acceptable anorectal continence after rectal resection

and hand-sewn anastomosis is widely described in the

literature [21,23,32-37].

In most of these studies the majority of patient conti-

nence was described as low grade (Grade I or II accord-

ing to Kirwan). The overall disillusioning results in this

study in comparison to other studies have to be analyzed

critically, as a uniform classification was not used in

every study, and all patients in this study had reduced

sphincter function caused by treatments prior to surgery.

Generally, a hand-sewn suture facilitates nerve growth

through the anastomosis, which is more likely to be im-

paired by stapled anastomosis, and can lead to better dis-

crimination and a better recovery of the anal inhibitory

reflex [38]. Presurgical radiotherapy of the rectum or its

neighboring organs further influences anorectal conti-

nence [27]. However the neoadjuvany therapy downstage

the locally advanced low rectal cancer and change the

decision option from abdomenoperineal to sphincter sav-

ing procedures in many cases.

5. Conclusions

There is a tendency of rectal cancers to affect younger

groups. Most patients presented advanced stage and ag-

gressive histopathology.

Using a multimodal approach, conservative treatment

was possible in patients with locally advanced carcino-

mas of the lower third of the rectum that would have re-

quired APR in most instances. Preoperative radiochemo-

therapy was associated with a low rate of complications

and induced significant down staging, Coloanal pull-

through technique is not a widely spread technique for

low rectal cancer with good oncological safety and ac-

ceptable functional outcome however large numbers of

patients have to study.

6. Acknowledgements

The authors received no financial or other support for the

research reported in manuscript.

Contributions: M.A.S. participate in collection of pa-

tient’s data, patient diagnoses and surgical evaluation and

surgical resection of patient subjected to surgery, general

coordination, drafting of manuscript and writing final

manuscript.

H.A. Carried out collection of patient’s data, patient

diagnoses, radiotherapy administration, follow up. A.I.

carried out collection of patient’s data, patient diagnoses,

chemotherapy administration and follow up. G.A. And

A.W. participate in surgical evaluation and management

of patients subjected to surgery. All authors have read

and approved manuscript.

REFERENCES

[1] R. P. Billingham, “Conservative Treatment of Rectal

Cancer. Extending the Indications,” Cancer, Vol. 70, No.

5, 1992, pp. 1355-1363.

doi:10.1002/1097-0142(19920901)70:3+<1355::AID-CN

CR2820701525>3.0.CO;2-9

[2] L. D. MacDonald, “The Health of Rectal Cancer Patients

in the Community,” European Journal of Surgical On-

cology, Vol. 11, No. 3, 1985, p. 235.

[3] A. Abdelsalem and Y. A. K. Ismail, “Preoperative Ra-

diochemotherapy in Locally Advanced Rectal Cancer,”

Journal of the Egyptian National Cancer Institute, Vol.

13, No. 2, 2008, pp. 101-108.

[4] C. V. Allen, “A Pilot Study on Preoperative Irradiation of

Rectosigmoid Carcinoma,” American Journal of Roent-

genology, Radium Therapy, and Nuclear Medicine, Vol.

114, No. 3, 1972, pp. 504-508. doi:10.2214/ajr.114.3.504

[5] J. A. Martenson Jr., et al., “Radiation Therapy Quality

Control in a Clinical Trial of Adjuvant Postoperative

Treatment for Rectal Cancer,” International Journal of

Radiation Oncology Biology Physics, Vol. 32, No. 1,

1995, pp. 51-55. doi:10.1016/0360-3016(95)00526-5

[6] J. Papillon, et al., “Role of Preoperative Radiotherapy in

Preservation of the Anal Sphincter in Cancer of the

Lower Rectum,” Bulletin du Cancer, Vol. 77, No. 1, 1990,

pp. 15-21.

[7] G. Marks, M. Mohiuddin and L. Masoni, “The Reality of

Radical Sphincter Preservation Surgery for Cancer of the

Distal 3 cm of Rectum Following High-Dose Radiation,”

International Journal of Radiation Oncology Biology

Physics, Vol. 27, No. 4, 1993, pp. 779-783.

doi:10.1016/0360-3016(93)90449-6

[8] P. Rouanet, “Sphincter Conservation and Cancer of the

Lower Rectum: Argument for a Multicenter Prospective

Study for Conservation of the Sphincter after Irradiation,”

Bulletin du Cancer, Vol. 85, No. 4, 1998, pp. 328-332.

[9] R. J. Heald, “Recurrence and Survival after Total Meso-

rectal Excision for Rectal Cancer,” Lancet Oncology, Vol.

1, No. 8496, 1986, pp. 1479-1482.

[10] W. S. Tan, et al., “Meta-Analysis of Defunctioning Stomas

in Low Anterior Resection for Rectal Cancer,” British

Journal of Surgery, Vol. 96, No. 5, 2009, pp. 462-472.

doi:10.1002/bjs.6594

[11] Y. S. Yeh, et al., “Transanal Inside-Out Rectal Resection

for Ultra-Low Rectal Cancer,” Journal of Investigative

Surgery, Vol. 25, No. 6, 2012, pp. 375-380.

doi:10.3109/08941939.2012.655369

Sphincter Saving Surgeries for Locally Advanced Low Rectal Cancer after Neoadjuvant Chemoradiation

1234

[12] O. Dahl, et al., “Low-Dose Preoperative Radiation Post-

pones Recurrences in Operable Rectal Cancer. Results of

a Randomized Multicenter Trial in Western Norway,”

Bulletin du Cancer, Vol. 66, No. 11, pp. 2286-2294.

doi:10.1002/1097-0142(19901201)66:11<2286::AID-CN

CR2820661106>3.0.CO;2-T

[13] L. Pahlman, “Pre- or Postoperative Radiotherapy in Rec-

tal and Rectosigmoid Carcinoma. Report from a Ran-

domized Multicenter Trial,” Annals of Surgical Oncology,

Vol. 211, No. 2, 1990, pp. 187-195.

doi:10.1097/00000658-199002000-00011

[14] E. Rullier, et al., “Preoperative Radiochemotherapy and

Sphincter-Saving Resection for T3 Carcinomas of the

Lower Third of the Rectum,” Annals of Surgery, Vol. 234,

No. 5, 2001, pp. 633-640.

doi:10.1097/00000658-200111000-00008

[15] C. Berger, et al., “Preoperative Radiotherapy (RT) for

Rectal Cancer: Predictive Factors of Tumor Downstaging

and Residual Tumor Cell Density (RTCD): Prognostic

Implications,” International Journal of Radiation Oncol-

ogy Biology Physics, Vol. 37, No. 3, 1997, pp. 619-627.

doi:10.1016/S0360-3016(96)00577-9

[16] M. C. Kaminsky-Forrett, et al., “Prognostic Implications

of Dowstaging Following Preoperative Radiation Ther-

apy for Operable T3-T4 Rectal Cancer,” International

Journal of Radiation Oncology Biology Physics, Vol. 42,

1998, pp. 935-941. doi:10.1016/S0360-3016(98)00345-9

[17] T. A. Rich, J. A. Ajani, et al., “Preoperative Infusional

Chemoradiation Therapy for Stage T3 Rectal Cancer,”

International Journal of Radiation Oncology Biology

Physics, Vol. 32, 1995, pp. 1025-1029.

doi:10.1016/0360-3016(95)00020-Y

[18] V. Valentini, N. Cellini, et al., “Preoperative Chemora-

diation for Extraperitoneal T3 Rectal Cancer: Acute Tox-

icity, Tumor Response, and Sphincter Preservation,” In-

ternational Journal of Radiation Oncology Biology Phys-

ics, Vol. 40, 1998, pp. 1067-1075.

[19] N. A. Janjan, J. Abbruzzese, et al., “Tumor Downstaging

and Sphincter Preservation with Preoperative Chemora-

diation in Locally Advanced Rectal Cancer: The M. D.

Anderson Cancer Center Experience,” International Jour-

nal of Radiation Oncology Biology Physics, Vol. 44, 1999,

pp. 1027-1038. doi:10.1016/S0360-3016(99)00099-1

[20] A. S. Miller, et al., “Factors That Influence Functional

Outcome after Coloanal Anastomosis for Carcinoma of

the Rectum,” British Journal of Surgery, Vol. 82, No. 10,

1995, pp. 1327-1330. doi:10.1002/bjs.1800821010

[21] D. Benchimol, et al., “Oncological and Functional Re-

sults of Direct Colo-Anal Anastomosis after Total Resec-

tion of the Rectum for Cancer,” Annales De Chirurgie,

Vol. 48, No. 7, 1994, pp. 596-603.

[22] B. Bittorf, et al., “Functional Outcome after Intersphinc-

teric Resection of the Rectum with Coloanal Anastomosis

in Low Rectal Cancer,” European Journal of Surgical

Oncology, Vol. 30, No. 3, 2004, pp. 260-265.

doi:10.1016/j.ejso.2003.11.011

[23] A. G. Parks and J. P. Percy, “Resection and Sutured Colo-

Anal Anastomosis for Rectal Carcinoma,” British Journal

of Surgery, Vol. 69, No. 6, 1982, pp. 301-304.

doi:10.1002/bjs.1800690602

[24] V. Schumpelick and J. Braun, “Intersphincteric Rectum

Resection with Radical Mesorectum Excision and Colo-

Anal Anastomosis,” Chirurg, Vol. 67, No. 2, 1996, pp.

110-120.

[25] A. Kohler, et al., “Long-Term Results of Low Anterior

Resection with Intersphincteric Anastomosis in Carci-

noma of the Lower One-Third of the Rectum: Analysis of

31 Patients,” Diseases of the Colon & Rectum, Vol. 43,

No. 6, 2000, pp. 843-850. doi:10.1007/BF02238025

[26] P. M. Sagar and J. H. Pemberton, “Surgical Management

of Locally Recurrent Rectal Cancer,” British Journal of

Surgery, Vol. 83, No. 3, 1996, pp. 293-304.

doi:10.1002/bjs.1800830305

[27] P. Luna-Perez, et al., “Anal Sphincter Preservation in

Locally Advanced Low Rectal Adenocarcinoma after Pre-

operative Chemoradiation Therapy and Coloanal Anas-

tomosis,” Journal of Surgical Oncology, Vol. 82, No. 1,

2003, pp. 3-9. doi:10.1002/jso.10185

[28] G. Eichhoff, “Short- and Long-Term Results of Hand-

Sewn Coloanal Anastomosis Performed as a Salvage Pro-

cedure after Rectal Resection,” The Internet Journal of

Surgery, Vol. 18, No. 1, 2009, pp. 1528-8242.

doi:10.1007/BF02554801

[29] H. K. Antonsen, “Early Complications after Low Anterior

Resection for Rectal Cancer Using the EEA Stapling De-

vice. A Prospective Trial,” Diseases of the Colon & Rec-

tum, Vol. 30, 1987, pp. 579-583.

[30] S. Athanasiadis, “Surgical Treatment of Radiation-In-

duced Rectovaginal Fistulas by the Continence Resection

Procedure,” Zentralblatt fur Chirurgie, Vol. 107, 1982,

pp. 1160-1168.

[31] M. P. Nowacki, “Ten Years of Experience with Parks’

Coloanal Sleeve Anastomosis for the Treatment of Post-

Irradiation Rectovaginal Fistula,” European Journal of

Surgical Oncology, Vol. 17, No. 6, 1991, pp. 563-566.

[32] R. Schiessel, et al., “Intersphincteric Resection for Low

Rectal Tumours,” British Journal of Surgery, Vol. 81, No.

9, 1994, pp. 1376-1378. doi:10.1002/bjs.1800810944

[33] E. Rullier, et al., “Laparoscopic Intersphincteric Resec-

tion with Coloplasty and Coloanal Anastomosis for Mid

and Low Rectal Cancer,” British Journal of Surgery, Vol.

90, No. 4, 2003, pp. 445-451. doi:10.1002/bjs.4052

[34] S. H. Baik, et al., “Hand-Sewn Coloanal Anastomosis for

Distal Rectal Cancer: Long-Term Clinical Outcomes,”

Journal of Gastrointestinal Surgery, Vol. 9, No. 6, 2005,

pp. 775-780. doi:10.1016/j.gassur.2005.03.003

[35] M. R. Keighley and D. Matheson, “Functional Results of

Rectal Excision and Endo-Anal Anastomosis,” British

Journal of Surgery, Vol. 67, No. 10, 1980, pp. 757-761.

doi:10.1002/bjs.1800671021

[36] P. Rouanet, et al., “Conservative Surgery for Low Rectal

Carcinoma after High-Dose Radiation. Functional and

Oncologic Results,” Annals of Surgery, Vol. 221, No. 1,

1995, pp. 67-73.

doi:10.1097/00000658-199501000-00008

[37] R. Schiessel, M. Wunderlich and R. Waneck, “Results of

Colo-Anal Anastomosis in Deep-Seated Tumors of the

Sphincter Saving Surgeries for Locally Advanced Low Rectal Cancer after Neoadjuvant Chemoradiation

1235

Rectum,” Chirurg, Vol. 57, No. 12, 1986, pp. 792-796.

[38] P. G. Horgan, et al., “Effect of Anterior Resection on

Anal Sphincter Function,” British Journal of Surgery, Vol.

76, No. 8, 1989, pp. 783-786.

doi:10.1002/bjs.1800760805