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The Role of the Longitudinal Muscle in the Anal Sphincter Complex: Implications for the Intersphincteric Plane in Low Rectal Cancer Surgery?

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The Role of the Longitudinal Muscle in the Anal Sphincter Complex: Implications for the Intersphincteric Plane in Low Rectal Cancer Surgery? This is a repository copy of The role of the longitudinal muscle in the anal sphincter complex: Implications for the Intersphincteric Plane in Low Rectal Cancer Surgery?. White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/149845/ Version: Accepted Version Article: Kraima, AC, West, NP orcid.org/0000-0002-0346-6709, Roberts, N et al. (6 more authors) (2020) The role of the longitudinal muscle in the anal sphincter complex: Implications for the Intersphincteric Plane in Low Rectal Cancer Surgery? Clinical Anatomy, 33 (4). pp. 567-577. ISSN 0897-3806 https://doi.org/10.1002/ca.23444 © 2019 Wiley Periodicals, Inc. This is the peer reviewed version of the following article: Kraima, A.C., West, N.P., Roberts, N., Magee, D.R., Smit, N.N., van de Velde, C.J.H., DeRuiter, M.C., Rutten, H.J. and Quirke, P. (2020), The role of the longitudinal muscle in the anal sphincter complex. Clin Anat, 33: 567-577. doi:10.1002/ca.23444, which has been published in final form at https://doi.org/10.1002/ca.23444. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions. Uploaded in accordance with the publisher's self-archiving policy. Reuse Items deposited in White Rose Research Online are protected by copyright, with all rights reserved unless indicated otherwise. They may be downloaded and/or printed for private study, or other acts as permitted by national copyright laws. The publisher or other rights holders may allow further reproduction and re-use of the full text version. This is indicated by the licence information on the White Rose Research Online record for the item. Takedown If you consider content in White Rose Research Online to be in breach of UK law, please notify us by emailing [email protected] including the URL of the record and the reason for the withdrawal request. [email protected] https://eprints.whiterose.ac.uk/ Abstract 1 Introduction 2 Intersphincteric resection (ISR) enables radical sphincter-preserving surgery in a subset of low rectal 3 tumours impinging on the anal sphincter complex (ASC). Excellent anatomical knowledge is essential 4 for optimal ISR. This study describes the role of the longitudinal muscle (LM) in the ASC and 5 implications for ISR and other low rectal and anal pathologies. 6 7 Materials and Methods 8 Six human adult en-bloc cadaveric specimens (three males, three females) were obtained from the 9 University of Leeds GIFT Research Tissue Programme. Paraffin embedded mega blocks containing 10 the ASC were produced and serially sectioned at 250 µm intervals. Whole mount microscopic sections 11 were histologically stained and digitally scanned. 12 13 Results 14 The intersphincteric plane was shown to be potentially very variable. In some places adipose tissue 15 is located between the external anal sphincter (EAS) and internal anal sphincter (IAS), whereas in 16 others the LM interdigitates to obliterate the plane. Elsewhere the LM is (partly) absent with the 17 intersphincteric plane lying on the IAS. The LM gave rise to the formation of the submucosae and 18 1 corrugator ani muscles by penetrating the IAS and EAS. In four of six specimens, striated muscle 1 fibres from the EAS curled around the distal IAS reaching the anal submucosa. 2 3 Conclusions 4 The ASC formed a complex structure, varying between individuals with an inconstant LM affecting 5 the potential location of the intersphincteric plane as well as a high degree of intermingling striated 6 and smooth muscle fibres potentially further disrupting the plane. The complexity of identifying the 7 correct pathological staging of low rectal cancer is also demonstrated. 8 9 Key words: longitudinal muscle; internal anal sphincter; external anal sphincter; anal sphincter 10 complex; rectal cancer; intersphincteric resection; sphincter-preserving surgery 11 12 13 14 15 16 17 2 Introduction 1 Low rectal cancer is a challenging disease, particularly when the tumour invades the anal sphincter 2 complex (ASC). These tumours are typically removed by an abdominoperineal excision, though 3 patients requiring this type of surgery end up with a permanent colostomy and have a poorer 4 oncological outcome compared to anterior resection (Wang et al., 2015). Damage to the anal 5 sphincters, iatrogenic tumour perforation and incomplete tumour resection are frequently 6 encountered and related to increased local recurrence and decreased survival (den Dulk et al., 7 2009). 8 For a select group of patients in whom low rectal tumours impinge on the anal canal or invade the 9 anal submucosa, a total or partial intersphincteric resection (ISR) might be a viable alternative to 10 abdominoperineal excision (APE). Theoretically, ISR is performed in combination with total 11 mesorectal excision and involves transanal division of the low rectum, removal of part or all of the 12 internal anal sphincter (IAS), and restoration of bowel continuity by means of a coloanal 13 anastomosis (Schiessel et al., 1994; Cong et al., 2014). This can be performed either from above or 14 from below by using transanal minimally invasive surgery (Fernandez-Hevia et al., 2015). 15 Although the functional outcomes may be suboptimal, long-term oncological outcomes after ISR are 16 satisfactory (Schiessel et al., 1994; Yamada et al., 2007; Martin et al., 2012; Koyama et al., 2014). 17 Historically, decision-making for sphincter-saving surgery was dependent on the tumour’s distance 18 to the anal verge. Until the 1980’s, a distal resection margin of 5 cm was required, after which a 2 19 cm distal margin was considered adequate. In the last decade, it has been shown that a distal 20 margin of less than 1 cm is oncologically safe in carefully selected patients (Ueno et al., 2004; 21 3 Rullier et al., 2005; Kiran et al., 2011). Locally advanced tumours can also be significantly 1 downsized and downstaged by pre-operative chemoradiation, after which ISR may be justified 2 (Koyama et al., 2014). Given these advances, ISR has been more widely accepted in specific cases 3 of low rectal cancer. This approach is potentially attractive in terms of achieving a balance between 4 oncological safety and preserving continence, yet there is an important risk of compromising radical 5 resections (Fernandez-Hevia et al., 2015). The key in rectal cancer surgery is the selection of 6 appropriate operative planes and achievement of a tumour-free circumferential resection margin in 7 order to reduce local recurrences (Quirke et al., 1986). 8 Hence, excellent anatomical knowledge of the ASC and the degree of variation within individuals is 9 of paramount importance to understand the planes that may be achievable to optimise results from 10 ISR. Studies reporting on the technical aspects of ISR pay little attention to the anatomy of the 11 intersphincteric plane (Schiessel et al., 1994; Akagi et al., 2014). Dissection in this plane should 12 enable separation of the IAS and external anal sphincter (EAS). The longitudinal muscle (LM) forms 13 the longitudinal layer of the smooth muscular component of the ASC and is located between the IAS 14 and EAS. As its anatomy has been mainly studied in the context of benign anal pathology and its 15 function in continence (Morgan and Thompson, 1956; Lunniss and Phillips, 1992; Macchi et al., 16 2008) potentially important details from a surgical and oncological perspective have not been 17 described. It has remained unclear how the intersphincteric plane can be precisely located during 18 surgery. Moreover, contradicting descriptions of the ASC raise the suspicion that inter-individual 19 differences are present. Although previously suggested (Rociu et al., 2000), a thorough two- 20 dimensional histological analysis of the entire ASC is needed to further examine this concept. 21 4 We studied the ASC in whole mount microscopic sections from en-bloc cadaveric specimens. In 1 particular, the anatomy of the LM and the presence of inter-individual differences were studied, and 2 implications for ISR described. 3 4 5 Materials and Methods 1 Adult cadaveric specimens 2 Six human adult specimens were obtained through the University of Leeds GIFT Research Tissue 3 Programme (www.gift.leeds.ac.uk) from consented whole-body donors. Ethical approval was 4 granted by the Northern and Yorkshire Regional Ethics Committee, Jarrow, UK (unique reference 5 number 11/H0903/6). The donor bodies belonged to three males aged 68, 89 and 99 years, and 6 three females aged 63, 64 and 74 years, respectively. All female donors had a history of childbirth. 7 All donors were free of macroscopic pelvic pathology at post mortem examination. The specimens 8 were retrieved during tissue donation autopsies performed at St. James’s University Hospital, Leeds 9 in the prone jack-knife position according to the technique of extralevator APE as described by 10 Holm et al (2007). The specimens were essentially pelvic exenterations and comprised en-bloc 11 resection of the soft-tissues in the bony pelvis with the anal canal, ASC and rectum up to the recto- 12 sigmoid junction. All specimens were processed in an identical way and fixed in 8% formaldehyde 13 solution for seven days prior to transverse sectioning at 1 cm intervals. The slices were 14 photographed and dissected to fit in Super Mega Cassettes measuring 74.8 x 52.5 x 16.5 mm 15 (CellPath, Powys, UK). The tissues underwent an extended tissue processing cycle in a Leica 16 ASP200 tissue processor as follows: 1 hour (h) in 70% ethanol, 2 h in 80% ethanol, 2 h in 90% 17 ethanol, 3 h in 95 % ethanol, 12 h in 100% ethanol (repeated three times), 12 h in xylene, 24 h in 18 xylene (repeated twice), 24 h in paraffin.
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