Outcomes after biological mesh reconstruction of the

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wound healing and the absence of perineal hernias dem- .... series led to chronic pain at the site of the coccygeal .... small asymptomatic parastomal hernia.

Tech Coloproctol DOI 10.1007/s10151-013-1107-7

ORIGINAL ARTICLE

Outcomes after biological mesh reconstruction of the pelvic floor following extra-levator abdominoperineal excision of rectum (APER) O. Peacock • J. A. Simpson • S. I. Tou • N. G. Hurst • W. J. Speake • G. M. Tierney J. N. Lund



Received: 24 October 2013 / Accepted: 9 December 2013 Ó Springer-Verlag Italia 2013

Abstract Background Extra-levator abdominoperineal excision of the rectum (ELAPER) for low rectal cancer is used to avoid the adverse oncological outcomes of inadvertent perforation and a positive circumferential resection margin associated with the conventional APER technique. This wider excision creates a large defect requiring pelvic floor reconstruction, and there is still controversy regarding the best method of closure. The aim of this study is to present outcomes of biological mesh pelvic floor reconstruction following ELAPER. Methods Prospective data on consecutive patients having ELAPER for low rectal cancer at a single UK institution between October 2008 and March 2013 were collected. The perineum was reconstructed using a biological mesh and the short-term outcomes were evaluated, focusing particularly on perineal wound complications and perineal hernias. Results Thirty-four patients were included [median age 62 years, range 40–72 years, 27 males (79 %)]. The median operative time was 248 min (range 120–340 min). The

An abstract of 29 patients has been submitted to the European Society of Coloproctology Conference 2013 in Belgrade and was accepted for a poster presentation. O. Peacock (&)  J. N. Lund Division of Surgery, School of Graduate Entry Medicine and Health, University of Nottingham, Royal Derby Hospital, Uttoxeter Road, Derby DE22 3DT, UK e-mail: [email protected] J. A. Simpson  S. I. Tou  N. G. Hurst  W. J. Speake  G. M. Tierney Division of Colorectal Surgery, Royal Derby Hospital, Uttoxeter Road, Derby DE22 3NE, UK

median length of hospital stay was 9 days (range 4–20 days). There were three perineal complications (9 %) requiring surgical intervention, but no meshes were removed. There were no perineal hernias. The median length of follow-up was 21 months (range 1–54 months). The overall mortality was 9 % from distant metastases. Conclusions Our series adds to the increasing evidence that good outcomes can be achieved for pelvic floor reconstruction with biological mesh following ELAPER without the additional use of myocutaneous flaps. The low serious complication rate, good outcomes in perineal wound healing and the absence of perineal hernias demonstrates that this is a safe and feasible procedure. Keywords ELAPER  Rectal cancer  Biological mesh  Perineal reconstruction

Introduction An abdominoperineal excision of the rectum (APER) maybe required for patients with a rectal cancer \6 cm from the anal verge [1]. Outcomes following the conventional APER technique have shown higher rates of inadvertent bowel perforation [2, 3] and circumferential resection margin (CRM) involvement [2, 4, 5]. This is associated with increased local recurrence rates and poorer overall survival compared to anterior resection for rectal cancer [1, 4]. The recent re-emergence of the extra-levator APER (ELAPER) technique [6, 7] increases the volume of tissue around the resected tumour, therefore, reducing intraoperative perforation and CRM involvement [8, 9]. However, this wider excision of the levators to improve oncological outcomes creates a large defect at the pelvic outlet, which requires reconstruction.

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As the levators are excised to their origins, attempts at primary closure are associated with a high incidence of wound failure due to tension and the accumulation of collections within the pelvic dead space [10]. Primary closure failure is compounded by neoadjuvant therapy, which significantly increases the risks of major wound complications [11] and impaired healing [12]. These risks may be ameliorated by importing fresh, non-irradiated tissue from neighbouring sites: various myocutaneous flap reconstructions of the pelvic cavity have been described following ELAPER [13–15]. However, the risks associated with myocutaneous flaps include wound complications at the donor site, flap necrosis and there is also an associated increase in operative costs, often including time, opportunity costs and frequently, additional input from a plastic surgeon. Recent studies have demonstrated pelvic floor reconstruction with a biological mesh to be a safe and feasible method following ELAPER [16–19]. We recently reported our early experience of pelvic floor reconstruction with a biological mesh showing significant cost-savings and comparable morbidity to myocutaneous flap reconstruction [20]. We present here outcomes of biological mesh pelvic floor reconstruction following ELAPER, in what is to the best of our knowledge the largest descriptive series thus far reported.

Materials and methods Consecutive patients with low rectal cancers (\6 cm from the anal verge, judged by the multi-disciplinary team (MDT) not to be suitable for a coloanal anastomosis) treated at the Royal Derby Hospital, UK by ELAPER between October 2008 and March 2013 were identified from a prospectively maintained database. Colonoscopy and rectal biopsies were performed to confirm the diagnosis. The patients were preoperatively staged with a chest, abdomen and pelvis computer tomography (CT) scan to assess for distant metastases and a magnetic resonance imaging (MRI) scan of the pelvis for local staging. All the cases were discussed in a MDT meeting, and the appropriate treatment plans were decided. Patients with disease extending beyond or involving the mesorectal fascia (\1 mm) received neoadjuvant therapy. This consisted of long-course chemoradiotherapy (CRT) with 45 Gy in 25 fractions with twice daily capecitabine. A further CT and MRI were performed 6 weeks following completion of CRT to define response and plan the surgical intervention with curative intent. Tumour response was defined as a decrease in the pretreatment T category and/or nodal status by at least one category. All the patients having ELAPER were reviewed by the stoma nurse prior to surgery.

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Data were collected on patient demographics, indication for referral, preoperative tumour staging, tumour distance from the anal verge, neoadjuvant and adjuvant therapies, operative details, histopathological staging, morbidity, mortality, length of hospital stay, local and distant recurrence at follow-up. As recommended by the Association of Coloproctology of Great Britain and Ireland for the management of colorectal cancer, the AJCC-TNM classification was used in the histopathological staging of the tumours [21]. The technique for insertion of the biological mesh at our institution has previously been described [20]. Rectal dissection continues distally in the total mesorectal excision (TME) until the mesorectum begins to thin, before repositioning the patient to prone jack-knife position and completing the extra-levator excision as described by Holm et al. [7]. However, the coccyx is no longer removed in our institution after excision in the first two patients of the series led to chronic pain at the site of the coccygeal division. The pelvic floor cavity is reconstructed using a 7 9 10 cm SurgisisÒ BiodesignTM (Cook Medical, Bloomington, IN, USA) 4-layer biosynthetic mesh. All operations were performed by, or supervised by, one of four consultants at our institution. The patients all followed an enhanced recovery after surgery (ERAS) protocol and receive training in stoma care. A complication was defined as early (B30 days) or late ([30 days) following surgery. A serious complication was defined as Grade III or IV of the Clavien–Dindo classification [22]. Perineal wound complications were defined as any requiring packing, antibiotic therapy, surgical intervention or vacuum-assisted therapy (VAC). Postoperative mortality was defined as a death occurring within 30 days of ELAPER. The patients are reviewed 2 weeks posthospital discharge in a colorectal nurse specialist-led clinic and are reviewed again at 8 weeks by a consultant surgeon. They are subsequently reviewed every 6 months for 2 years in the nurse specialist-led clinic, with a CT performed at year 1 and year 2 follow-up. Patients are reviewed earlier at the request of their general practitioner. A colonoscopy is also performed at year 1 and then repeated every 5 years if unremarkable. No statistical analysis was performed for this descriptive study.

Results Thirty-four consecutive patients had biological mesh pelvic floor reconstruction after ELAPER at a single UK institution between October 2008 and March 2013. No patients having ELAPER for low rectal cancer were excluded during this period. The median age for this cohort of

Tech Coloproctol Table 1 Patient demographic, preoperative and operative data

Table 2 Histopathological data of the ELAPER resection specimens

Sex

Histopathological data

Male

27 (79 %)

Female

7 (21 %)

Median age

62

Range

40–77

Primary presenting symptom/sign Rectal bleeding

19 (56 %)

COBH

9 (26 %)

Rectal mass

2 (6 %)

Positive FOBT

3 (9 %)

IDA

1 (3 %)

Preoperative staging T-stage T1

0

T2 T3

7 (21 %) 20 (58 %)

T4

7 (21 %)

Nodal status N0

9 (26 %)

N1

17 (50 %)

N2

8 (24 %)

Neoadjuvant therapy Long-course chemoradiotherapy

26 (76 %)

Long-course radiotherapy (not suitable for chemotherapy)

2 (6 %)

Not required/declined

6 (18 %)

2

pT1N1

1

pT2N0

10

pT2N1

1

pT3N0

11

pT3N1

3

pT3N2

1

pT4N0

1

pT4N2

1

Complete response (no residual tumour after CRT) Histological grading

3

Well Moderate

3 27

Poor

1

Not applicable

3

Lympho/vascular involvement Yes

8

No

23

Not applicable

3

Multivisceral resection Yes

0

No

34

CRM 30

25 (89 %) 3 (11 %)

Positive

1

Not applicable Inadvertent perforation

3

2.5 cm (0–5.5 cm)

Yes

0

No

34

Tumour location Median distance from anal verge (range)

pT1N0

Negative

Response of T category to neoadjuvant therapy Yes No

Histological staging

ASA grade 1

3 (9 %)

2

26 (76 %)

3

5 (15 %)

4

0

Median operative time

248 min

Range

120–340 min

COBH change of bowel habit, FOBT faecal occult blood test, IDA iron deficiency anaemia, ASA American Society of anesthesiologists

patients was 62 years (range 40–77 years), and the majority were male patients (29; 79 %). Patient demographics and preoperative clinical information are shown in Table 1. The median operative time was 248 min (range 120–340 min). The median length of follow-up in this study was 21 months (range 2–54 months). The CRM was positive in one patient (3 %). This patient had a T4N2 tumour on preoperative MRI with very limited

ELAPER extra-levator abdominoperineal excision of the rectum, CRT chemoradiotherapy, CRM circumferential resection margin

response to long-course CRT. After discussion with the patient and at the MDT, it was elected to perform ELAPER, but the subsequent pathological staging (pT4N2) correlated with the radiological staging. Other histopathological data are shown in Table 2. Eleven patients received adjuvant chemotherapy following postoperative MDT discussion. There was no postoperative mortality. The median length of hospital stay was 9 days (range 4–20 days). Twenty patients (59 %) did not suffer any early complications. The early complications observed in the remaining 14 patients are shown in Table 3. There were only three early complications of Clavien–Dindo Grade III or IV in this series: all three patients developing wound collections/ abscesses requiring surgical drainage and VAC therapy. None involved the mesh and no mesh was removed. Ten

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Tech Coloproctol Table 3 Early (B30 days) and late ([30 days) complications following ELAPERs, graded by the Clavien–Dindo classification [21] Type of complication

Number of patients

Clavien–Dindo classification

Early complications Perineal sinus

5

I

Acute urinary retention Superficial perineal wound infection

4 3

I II

Hospital acquired pneumonia

2

II

Urinary tract infection

1

II

Ileus

2

II

Abscess/collection

3 (VAC therapy)

III

Parastomal hernia

1

I

Erectile dysfunction

2

II

Perineal pain

2

II

Discussion

Late complications

ELAPER extra-levator abdominoperineal excision of the rectum, VAC vacuum-assisted closure

Table 4 Overall outcomes following ELAPERs Outcomes Alive

31 (91 %)

Adjuvant therapy

12 (35 %)

Local recurrence and subsequent distant metastases

1 (3 %)

Distant metastases

6 (18 %)

Palliative chemotherapy

4 (12 %)

Liver resection

2 (6 %)

Nil

1 (3 %)

Overall mortality

3 (9 %)

ELAPER extra-levator abdominoperineal excision of the rectum

patients, nine of whom had received neoadjuvant longcourse CRT, experienced minor perineal wound complications (Table 3). All perineal wound complications had healed by 6 month follow-up. There were five late postoperative complications (15 %). Two patients suffered from prolonged perineal pain for which no cause was found after extensive investigation. A further two patients developed erectile dysfunction and are currently under the care of the urologists. Finally, one patient developed a small asymptomatic parastomal hernia. There have been no perineal hernias demonstrated either on clinical examination or on follow-up CT imaging in our series. Currently, 31 patients (91 %) are alive following ELAPER (Table 4). One patient (pT3N1) developed local recurrence (3 %) and subsequently developed distant metastases. A further six patients (18 %) developed distant metastases (Table 4), with four patients receiving a

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palliative chemotherapy regime. Two patients subsequently underwent successful liver resections for metastases. One patient with distant metastases presenting in follow-up was deemed too unwell to receive any therapy. There have been three deaths (9 %) in this series, all due to metastatic disease.

The ELAPER technique is now well established for improving oncological outcomes in low rectal cancer and is increasingly adopted as the method of choice where an anastomosis is not possible [23]. However, controversy remains regarding the preferred method of closure of the large pelvic cavity created following the extended excision. Increasing use of neoadjuvant therapy for rectal cancer further confounds the issue. Radiotherapy causes capillary obliteration and fibrosis in connective tissue leading to impaired tissue oxygenation, altered cellular immune mechanisms and decreased fibroblast production of collagen [10]. This increases the risk of potential perineal wound problems; thus, careful consideration of the appropriate method for reconstruction following this technique is vital. This study demonstrates that pelvic floor reconstruction with biological mesh is quick and safe. It is technically simple and requires no additional input from other surgical specialities, nor any additional skills not already in the repertoire of all colorectal surgeons. According to a recent UK national survey, approximately 20 % of pelvic outlet closures following ELAPERs are performed by primary closure [24]. Excision of the levator muscles leaves only fatty tissue and skin, so the defect is closed under tension resulting in a high frequency of perineal wound problems [7]. Primary closure of perineal wounds is associated with high rates of wound infection and dehiscence [25]. Perineal wound complications following primary closure for conventional APER are reported between 40 and 66 % compared with flap reconstruction groups of between 22 and 52 % [26–29]. Myocutaneous flap pelvic floor reconstruction appears to mitigate the effects of radiotherapy on perineal wound healing, but is not problem-free [10]. Disadvantages include donor-site wound complications, flap necrosis, increased operative time, the need for acquisition of non-core colorectal skills and the potential requirement for a plastic surgeon, leading to opportunity costs as a result [20, 30]. The biological mesh for pelvic floor reconstruction following ELAPER in this series (SurgisisÒ BiodesignTM (Cook Medical, Bloomington, IN, USA) is used as a tension-free bridge repair, secured by a parachute inlay to the origins of the levator muscles, with the ischiorectal fat below and omental fat above. SurgisisÒ is an acellular

Tech Coloproctol

matrix biomaterial formed from porcine small intestine mucosa that promotes proliferation and formation of fibroblasts within wounds without stimulating a foreign body inflammatory response [31]. The mesh augments the body’s natural response to healing and is eventually absorbed leaving a strong vascularised tissue [32]. This potentially reduces some of the longer-term complications of perineal wounds such as fistulas and sinuses following radiotherapy and surgery [16]. Other groups have used alternative biological mesh material for pelvic floor reconstruction after ELAPER, including PermacolTM (cross-linked acellular porcine dermis; Covidien, Gosport, UK) [16–18, 33] and human acellular dermal matrix (HADM; Bio-Tissue Engineering Ltd., Beijing, China) [34, 35] with varying results. The overall perineal wound complication rate in our series was 32 %; however, only three complications (8 %) were serious and required surgical intervention and VAC therapy. In context, a recent study investigating the short-term outcome after gluteus maximus myocutaneous flap pelvic floor reconstruction following ELAPER demonstrated an overall early perineal complication rate of 42 % [15]. Our results are comparable with another study on biological mesh pelvic floor reconstruction, which reports an overall perineal wound complication rate of 53 %, with 6 (20 %) patients requiring VAC therapy [18]. In a smaller series of 11 patients, Wille-Jorgensen et al. [16] report 1 (9 %) serious perineal wound complication resulting in removal of the PermacolTM mesh due to pelvic infection. No meshes required removal in our series. In a study comparing outcomes of fasciocutaneous gluteal flaps versus PermacolTM mesh in ELAPER pelvic floor reconstruction, Christensen et al. [17] recorded only perineal wound infections requiring surgical intervention, (17 % (4/24 patients) in the mesh group). In a recent randomised controlled trial of conventional APER versus ELAPER for locally advanced rectal cancer, the overall perineal wound complication rate for the ELAPER group (HADM mesh) was 23 % [35]. However, more striking was the 14 % (5/35 patients) rate of perineal hernias following HADM mesh pelvic floor reconstruction. The authors concluded that the main reason for the high perineal hernia rate was the laxity of HADM [35], which increases with time [36]. They recommended a continued search for alternative biological materials to improve perineal outcomes [35]. Other biological mesh materials have been utilised for pelvic floor reconstruction, with two studies using PermacolTM mesh and reporting no perineal hernias with a median follow-up of 12 [16] and 20 months [17]. However, in a series, also using PermacolTM mesh, with a median follow-up of 20 months and a larger number of patients, there were three perineal hernias (10 %) reported one requiring surgical intervention [18].

Christensen et al. [17] also reported a high rate of perineal hernias (21 %) when using a fasciocutaneous gluteal flap group compared with no perineal hernias in the mesh group. They report having subsequently changed their practice to routinely using biological mesh reconstruction unless wide perineal skin resection and/or vaginal reconstruction are required, where a vertical rectus abdominis musculocutaneous (VRAM) flap is utilised [17]. However, VRAM flap pelvic reconstruction itself is not without complications: a recent study of VRAM flaps performed by a colorectal surgeon reported an overall perineal complication rate of 50 %, but no perineal hernias [13]. There were no perineal hernias on clinical examination or follow-up CT imaging in our series using SurgisisÒ with a median follow-up of 21 months (range 1–54 months). Perhaps this is in part due to SurgisisÒ having more baseline tensile strength compared with synthetic absorbable meshes, with superior collagen deposition and organisation, whilst also having increased neovascularisation compared with another biological mesh AllodermÒ (Lifecell, Branchburg, NJ, USA) [37]. Perineal pain is a reported complication of ELAPER, which is attributed mainly to the wider excision, fixation of the mesh to the pelvic fascia, neuropathy or coccygectomy. Han et al. [35] used a visual analogue score at 3 and 12 months to evaluate pain and showed that chronic perineal pain rates were common (51 %) following ELAPER. Currently there is no standardised definition of the perineal pain in the literature, only descriptive outcomes [23]. Wille-Jorgensen et al. [16] report perineal pain as a common postoperative complication (55 %), with a median duration of 5 weeks. Perineal pain in all these series was attributed mainly to the coccygectomy [16, 35]. In our series, two patients suffered from prolonged perineal pain for which no cause was found after extensive investigation. These were the first and only two patients to have coccygectomy performed as part of the procedure. Coccygectomy is no longer performed and there have been no further reports of prolonged perineal pain. A recent systematic review evaluating perineal reconstruction following ELAPER showed no significant difference in complication rates between biological mesh and myocutaneous flap repairs [30]. There are some advantages to the biological mesh for pelvic floor reconstruction over myocutaneous flaps. These include a shorter operating time, the ability to adhere to an ERAS protocol with more rapid early mobilisation and the lack of donor-site morbidity. The median operative time of 248 min in our series is comparable with other mesh pelvic floor reconstruction series [17, 35], whilst being much shorter than the operative times quoted for myocutaneous flap reconstruction

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[38]. The flap procedures also often require the presence of a plastic surgeon increasing opportunity costs. Moreover, there is a significant reduction in the length of hospital stay when biological meshes are used for perineal reconstruction [20].

Conclusions This study, to the best of our knowledge, is the largest descriptive series thus far reported and supports the use of biological mesh as the method of choice for pelvic floor reconstruction following ELAPER. A pragmatic randomised trial of biological mesh reconstruction versus myocutaneous flap reconstruction is now required to define the optimal method for pelvic floor reconstruction after ELAPER. Conflict of interest

None.

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