- Email: [email protected]
Clarifying margins in the multidisciplinary management of rectal cancer: the MERCURY experience
Clinical Radiology (2006) 61, 916e923
PICTORIAL REVIEW
Clarifying margins in the multidisciplinary management of rectal cancer: the MERCURY experience G. Salernoa, I.R. Danielsa, B.J. Morana, A. Wotherspoonb, G. Brownc,* a
Pelican Cancer Foundation, North Hampshire Hospital, Basingstoke, bDepartment of Histopathology, Royal Marsden Hospital, London, and cDepartment of Radiology, Royal Marsden Hospital, Sutton, UK
Received 3 March 2006; received in revised form 30 May 2006; accepted 5 June 2006
The Magnetic Resonance Imaging and Rectal Cancer European Equivalence Study (MERCURY) was an observational prospective study involving 11 European centres, to evaluate equivalence between magnetic resonance imaging and histopathology in measuring depth of tumour invasion beyond the bowel and involvement of the circumferential resection margin in rectal cancer specimens. ª 2006 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Background Although pathological assessment of a rectal cancer is the gold standard, preoperative staging and identification of prognostic factors allows the appropriate selection of patients for preoperative therapy or more radical surgery to reduce the incidence of positive circumferential resection margins (CRMs). Areas of rectum not surrounded by mesorectum should be classified appropriately. This is particularly important in radical surgical resections that extend into other organs. It is important to achieve complete surgical excision of the primary tumour, using total mesorectal excision (TME), as this determines the rate of local recurrence with its associated morbidity and mortality.
* Guarantor and correspondent: Gina Brown, Department of Radiology, Royal Marsden Hospital NHS Trust, Downs Road, Sutton, Surrey SM2 5PT, UK. Tel.: þ44 20 8661 3964; fax: þ44 20 8661 3506. E-mail address: [email protected] (G. Brown).
Standardization of terminology is necessary for consistent discussion and patient management within the multidisciplinary team. The term ‘‘circumferential’’ implies a margin that is fully surrounding a viscus. Whereas this does apply to rectal tumours that are wholly below the peritoneal reflection, the use of the term ‘‘circumferential resection’’ is misleading and inaccurate for tumours that straddle or are above the peritoneal reflection. The term can cause confusion because, for tumours at or above the peritoneal reflection, only the part of the circumference below the peritoneal reflection is relevant to the assessment of surgically attainable margin status. The current European practice is the selective use of neoadjuvant chemoradiotherapy to optimize delayed surgical treatment. In the UK, the National Institute for Clinical Excellence (NICE) recommends that, for patients with invasive rectal cancers for whom surgery is being considered, magnetic resonance imaging (MRI) should be performed before treatment begins to determine who might benefit from either neoadjuvant therapy or surgery alone. These cancers should be discussed
0009-9260/$ - see front matter ª 2006 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2006.06.005
Clarifying margins in the multidisciplinary management of rectal cancer
within the multidisciplinary cancer management team. Using MRI and pathological images from patients recruited during the Magnetic Resonance Imaging and Rectal Cancer European Equivalence Study (MERCURY), we aimed to highlight the potential for confusion between the members of the multidisciplinary cancer management team when discussing cases.
Introduction During analysis of the data determined in the MERCURY study, it became apparent that radiologists and pathologists alike were misclassifying CRM involvement. We have used examples encountered in that study to highlight the importance of understanding the anatomy of the surgical CRM. Quirke and colleagues have shown the importance of the radial spread of rectal cancer and its relationship to the lateral resection margin.1 Before TME surgery was widely practised, rates of lateral resection margin involvement were as high as 27% and, as a consequence, a local recurrence rate of 85% was seen in the margin-positive group but only 3% in the margin-negative group.1e3 Pathological assessment, advocated by Quirke and subsequently adapted in the National Histopathology Guidelines, uses serial transverse 5-mm sectioning of the whole tumour and surrounding mesorectum; this enables assessment of the relationship of the tumour to and its distance from the surgical resection margin. The CRM is defined as positive if this distance is less than 1 mm.4 The presence or absence of CRM involvement has emerged as one of the crucial determinants for prognosis.5 In rectal cancer surgery the CRM is formed by the mesorectal fascia, which envelops the mesorectum and constitutes the dissection plane in TME. This structure can be consistently demonstrated using high-resolution MRI and, provided the images are obtained in a plane perpendicular to the rectum and mesorectum,6 the oblique axial images obtained correspond precisely to the specimen images.7,8
917
the rectum is surrounded by the mesorectum in an eccentric way. The mesorectum contains the vascular, nervous and lymphatic supplies of the rectum, is covered by visceral fascia and is separated from the parietal pelvic fascia (which covers the other pelvic structures) by thin areolar tissue. In the upper third, the mesorectal fat is continuous with the sigmoid mesocolon and the anterior aspect of the rectum is covered by peritoneum. Below this recto-vesical peritoneal pouch, the mesorectum encompasses the rectal circumference but disappears anteriorly at approximately the point where Denonvilliers’ fascia fuses with the posterior capsule of the prostate. In the median plane, the peritoneum is attached to the uppermost part of the posterior wall of the vagina in women, forming the recto-uterine or rectovaginal pouch of Douglas. In men, the peritoneum is attached to the seminal vesicles, vas deferens and bladder, forming the recto-vesical pouch. Behind the mesorectum lies a space and, posterior to this, the anterior surface of the sacrum is covered with a presacral parietal fascia (of Waldeyer). These fascial coverings can be seen in Fig. 1. Visceral fascia surrounding the mesorectum is reflected on the parietal pelvic fascia at the level of the pelvic floor. Loose connective tissue provides an interface between the visceral and parietal fasciae, which facilitates dissection along these embryologically defined planes and, with traction and counter-traction, forms bloodless cavities filled with air. This is the surgical plane of TME, and it is important to follow this to excise the rectum with its lymphovascular supply intact. Taking into consideration this anatomy, TME surgery proceeds as follows.
Anatomy of the rectum and TME surgery In the adult, the rectum begins 15 cm from the anal orifice at the acute rectosigmoid angle, at the level of S2e3. The upper third of the rectum is located intraperitoneally, the middle third lies partly in the peritoneum and the lower third, which is the widest part of the rectum (the ampulla), lies in the extra-peritoneal plane. Most of
Figure 1 Axial MRI showing the fascial planes of the pelvis at the level of the levator origins from the pelvic sidewall.
918
The inferior mesenteric artery is divided close to the aorta, preserving the autonomic nerves, and the vein is divided close to its last tributary at the pancreas. The mesorectum is then dissected free under direct vision, using sharp dissection, in contrast to the standard technique where blunt dissection and manual extraction at the rectosacral ligament often caused disruption of the posterior mesorectum. The conventional technique identified an area of thickened fascia, which anchors the mesorectum to the lateral pelvic wall. This is the pedicle previously described as a lateral ligament. Traditionally a surgical clamp would be placed across this, as it was believed to contain the middle rectal artery. This is an artificially developed ligament formed by the medial traction of the rectum and contains the important autonomic nerve plexus, which supplies urinary continence and sexual function. If the artery is present, it is usually small and unilateral. Therefore, this structure is preserved with TME, which is performed anteriorly to this to avoid breaching the mesorectum. Denonvilliers’ fascia is eventually transected distally as it fuses with the prostatic capsule. At this point, the inferior hypogastric nerve plexus (neurovascular bundles of Walsh) taper medially
G. Salerno et al.
and must be teased off the front of the mesorectum to avoid impotence and bladder dysfunction. In a low anterior resection, an almost bare anterior aspect of the anorectal muscle is seen below the attachment of Denonvilliers’ fascia to the specimen. Posteriorly, the TME specimen is separated from the recto-sacral ligament using sharp dissection; this dissection around the mesorectal fascia produces a bilobar TME specimen. Fig. 2 shows the lines of TME surgical excision. MRI can accurately identify the relationship of the tumour to this fascial layer and can therefore stage rectal tumours into non-favourable and favourable groups. Those with involved margins can be selected for preoperative therapy. With the increasing use of preoperative staging, the terminology that the radiologist uses should be consistent with that used by the pathologist. It is also important that, when reporting the relationship between tumour and margins, distinction is made between surgical and peritoneal margins, both radiologically and pathologically.
Preparation of the TME specimen by the histopathologist The specimen is opened except for the area of the tumour, to preserve assessment of the anterior aspect where CRM or peritoneal involvement may be seen. Anterior and posterior non-peritonealized surfaces are painted with ink (Fig. 3). It should be noted that the definition of circumferential margin only applies to the inked, surgically incised mesorectal planes and not the peritonealized surfaces.
Figure 2 Sagittal MRI showing the excision planes followed in total mesorectal excision.
Figure 3 Specimen preparation. Photograph of total mesorectal excision demonstrates inking of the nonperitonealized surface in order to enable distinction between the surgical resection margin and the serosal margin.
Clarifying margins in the multidisciplinary management of rectal cancer
919
tumour. The sections should also be photographed as a valuable demonstration of the quality of the surgery (Fig. 4), which may be independently assessed by the reporting pathologist.
Understanding surgical and histological margins in upper rectal cancers Anatomy of the peritoneal reflection
Figure 4 Gross pathological assessment of the specimen from total mesorectal excision, sectioned in the axial plane. The tissue sections are laid out to enable direct visual inspection of the tumour and its relationship to the mesorectal margin. Tissue sections demonstrating close relationship between tumour and ink margins are sampled so that the appropriate glassmounted histopathological slides can be prepared.
The mesorectal surface is larger posteriorly and extends to a higher level than it does anteriorly. After the resection surfaces have been inked and the specimen fixed in formalin for a minimum of 3 days (72 h), a description of the macroscopic appearances is made and the specimen is transversely sectioned into thin (3 to 5 mm) tissue sections from 2 cm below to 2 cm above the
The CRM represents the margin that the surgeon can influence by dissection along the mesorectal plane, but not all the rectum is surrounded by the mesorectum. In mid and upper rectal tumours, there is a peritonealized anterior surface. The peritoneal reflection is said to be situated 5.5 cm above the dentate line in women (but is variable) and 7.5 cm above in men. Approximately 25% of the anatomical rectum is invested by peritoneum in women and about 16% in men, and therefore spread from an advanced upper rectal cancer might be expected to involve the pelvic peritoneum, with seeding of tumour cells into the peritoneal cavity and pelvic tissues, outside the site of resection.9 Tumour may also extend through the peritoneum into adjacent organs, particularly the bladder, uterus or small bowel, but not the prostate which lies entirely below the peritoneal reflection.
Figure 5 Axial and sagittal MRI depicting the peritoneal reflection. On the axial image, the apex of the peritoneum attaches to the anterior rectal wall in a V-shaped configuration. In men this is generally at a point just above the tip of the seminal vesicles; in women the point of attachment is rather more variable.
920
G. Salerno et al.
Figure 6 Serial axial MRI sections demonstrating fat in the anterior mesorectum from the mid to the upper rectum. The point where no anterior mesorectal fat is seen is generally the point at which the peritoneal attachment begins.
The peritoneal reflection may be identified on sagittal MRI as a low-signal linear structure that can be seen extending from the posterior aspect of the dome of the bladder to the ventral aspect of the rectum. On axial section, the point of attachment has a V-shaped configuration (Fig. 5). The
point at which the peritoneal reflection commences can also be recognized on serial axial MRI through the mesorectum, showing the anterior mesorectal fat becoming thinner and thinner in the cranial direction. The point where no anterior mesorectal fat is seen is generally where the
Figure 7 Pathology specimens demonstrating the serosal surface of the rectum in blue. This becomes progressively more wide higher up in the rectum, until almost the entire circumference of the bowel wall is peritonealized apart from a narrow posterior strip that forms the sigmoid mesentery (arrows).
Figure 8 Axial image demonstrating a T4b circumferential tumour which has perforated through the rectal wall and also through the peritoneum (arrow).
Clarifying margins in the multidisciplinary management of rectal cancer
921
peritoneum begins (Fig. 6). This bare area of rectum becomes progressively wider in the cranial direction, until almost the entire circumference of the bowel is peritonealized apart from a narrow posterior strip that forms the sigmoid mesentery (Fig. 7).
Peritoneal involvement does not equate to CRM involvement
Figure 9 Sagittal MRI demonstrating a tumour in the upper third of the rectum. Images show anterior perforation of the tumour through the peritoneal reflection and into adjacent uterus. Because of direct spread into a contiguous organ, this would be staged as T4a disease on MRI. If the surgeon resects the uterus and primary tumour en bloc, the surgical resection margins will be negative.
An anterior tumour in the upper rectum which invades the peritoneum will be classed as a T4b tumour histologically (Fig. 8). There is frequently confusion owing to discrepancy between classification by the radiologist and classification by the pathologist. These tumours should be reported on MRI and histopathology as being CRMnegative, because CRM corresponds to the cut surgical resection margin and does not cover the anterior aspect of the upper rectum. Because the surgeon cannot influence the free peritoneal surface, the surgical resection margin (SRM) will be negative as the whole rectum will be excised. A T4b tumour in this area potentially sheds cells into the rectovesical space or pouch of Douglas, there is a higher risk of pelvic recurrence and there are the limitations of MRI in detecting
Figure 10 Axial MRI and corresponding histopathology section showing tumour extending anteriorly to involve the serosal margin, as well as the mesorectal fascia. The specimen demonstrates that the surgeon has cut through tumour; thus, the circumferential resection margins are involved by tumour.
922
microscopic peritoneal invasion. Currently, the demonstration of tumour extending through the peritoneal membrane is not an indication for either preoperative or adjuvant therapy, and there is only very limited experience in the treatment of colorectal peritoneal disease.10,11 Therefore, reporting such cases on MRI or histopathology as
G. Salerno et al.
positive margins could result in potential overtreatment. Adjacent organ invasion can occur into the bladder, uterus (Fig. 9) or small bowel. If the surgeon resects these organs en bloc, the peritoneal reflection will be involved by tumour and the tumour will be staged as T4a (direct spread
Figure 11 Axial tissue sections from an anteroposterior excision specimen and the preoperative MRI of a low rectal tumour. Images demonstrate tumour infiltrating the low rectum, with extension through the full thickness of the muscularis propria. No invasion of the levator sling, puborectalis or external sphincter muscles is revealed, but the surgical margins depend on the extent of the dissection and are unpredictable. Little tissue has been removed in the area corresponding to the curved arrow or anterolaterally on the right (large arrow), but more has been removed posterolaterally on the right.
Clarifying margins in the multidisciplinary management of rectal cancer
into contiguous organ) and T4b (direct spread into the peritoneum). However, SRMs are negative unless the surgeon cuts through tumour, resulting in a positive surgical resection margin (Fig. 10).
Margins around the low rectal cancer In low rectal cancer (defined as the area below the insertion of the levator muscle, approximately below 6 cm from the anal verge), the mesorectum volume is reduced, and in ano-rectal tumours there is no mesorectal plane, as the rectal muscle tube lies against the pelvic floor before passing through the external sphincter. Thus, the mesorectal fascia tapers as it fuses to the endopelvic fascia which overlies the levator muscles and in turn fuses with muscles of the external anal sphincter. In abdomino-perineal resection there is no clearly definable or predictable surgical plane, particularly when performing the perineal dissection, and hence the final SRM is variable and not predictable radiologically (Fig. 11). The surgeon may either dissect along the muscle tube, or extend laterally along the edges of the ischiorectal fossae. Anteriorly, the posterior vaginal wall or part of the prostate may or may not be excised. The term ‘‘prediction of circumferential margin’’ is therefore also inaccurate in low tumours.
Summary The radiologist reporting the MRI should state the relationship of the tumour to the mesorectal fascia for mid and upper rectal cancers. As there is no mesorectal fascia in the lowest tumours, the radiologist should describe the anatomical compartments that might need to be removed in order to achieve clear margins. This also applies to
923
tumours above the peritoneal reflection, that are invading adjacent organs. To clarify resection margins, we propose that, instead of a report on whether CRM is involved or not by the radiologist reporting the MRI or the pathologist reporting the histology of the specimen, it should be stated whether the MRI potential surgical CRM or the surgical CRM is involved or not. In this way, the anatomical differences of the rectum and mesorectal fascia are accounted for and are related to the height of the tumour.
References 1. Quirke P, Durdey P, Dixon MF, et al. Local recurrence of rectal adenocarcinoma due to inadequate surgical resection. Histopathological study of lateral tumour spread and surgical excision. Lancet 1986;2:996e9. 2. Heald RJ, Ryall RD. Recurrence and survival after total mesorectal excision for rectal cancer. Lancet 1986;1: 1479e82. 3. Enker WE. Mesorectal excision (TME) in the operative treatment of rectal cancer. Int J Surg Investigation 1999;1:253e5. 4. Hall NR, Finan PJ, al-Jaberi T, et al. Circumferential margin involvement after mesorectal excision of rectal cancer with curative intent. Predictor of survival but not local recurrence? Dis Colon Rectum 1998;41:979e83. 5. Wibe A, Rendedal PR, Svensson E, et al. Prognostic significance of the circumferential resection margin following total mesorectal excision for rectal cancer. Br J Surg 2002;89:327e34. 6. Aeberhard P, Fasolini F, del Monte G. Anatomical basis and rationale of total mesorectal excision. Swiss Surg 1997;3:243e7. 7. Brown G, Daniels IR, Richardson C, et al. Techniques and trouble-shooting in high spatial resolution thin slice MRI for rectal cancer. Br J Radiol 2005;78:245e51. 8. Brown G, Kirkham A, Williams GT, et al. High-resolution MRI of the anatomy important in total mesorectal excision of the rectum. AJR Am J Roentgenol 2004;182:431e9. 9. Shepherd NA, Baxter KJ, Love SB. Influence of local peritoneal involvement on pelvic recurrence and prognosis in rectal cancer. J Clin Pathol 1995;48:849e55. 10. Cintron JR, Pearl RK. Colorectal cancer and peritoneal carcinomatosis. Semin Surg Oncol 1996;12:267e78. 11. Horsell KW, Merten S, Clingan P, et al. Peritonectomy and intraperitoneal chemotherapy in appendiceal and colorectal cancer. Aust N Z J Surg 1999;69:729e32.
PICTORIAL REVIEW
Clarifying margins in the multidisciplinary management of rectal cancer: the MERCURY experience G. Salernoa, I.R. Danielsa, B.J. Morana, A. Wotherspoonb, G. Brownc,* a
Pelican Cancer Foundation, North Hampshire Hospital, Basingstoke, bDepartment of Histopathology, Royal Marsden Hospital, London, and cDepartment of Radiology, Royal Marsden Hospital, Sutton, UK
Received 3 March 2006; received in revised form 30 May 2006; accepted 5 June 2006
The Magnetic Resonance Imaging and Rectal Cancer European Equivalence Study (MERCURY) was an observational prospective study involving 11 European centres, to evaluate equivalence between magnetic resonance imaging and histopathology in measuring depth of tumour invasion beyond the bowel and involvement of the circumferential resection margin in rectal cancer specimens. ª 2006 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Background Although pathological assessment of a rectal cancer is the gold standard, preoperative staging and identification of prognostic factors allows the appropriate selection of patients for preoperative therapy or more radical surgery to reduce the incidence of positive circumferential resection margins (CRMs). Areas of rectum not surrounded by mesorectum should be classified appropriately. This is particularly important in radical surgical resections that extend into other organs. It is important to achieve complete surgical excision of the primary tumour, using total mesorectal excision (TME), as this determines the rate of local recurrence with its associated morbidity and mortality.
* Guarantor and correspondent: Gina Brown, Department of Radiology, Royal Marsden Hospital NHS Trust, Downs Road, Sutton, Surrey SM2 5PT, UK. Tel.: þ44 20 8661 3964; fax: þ44 20 8661 3506. E-mail address: [email protected] (G. Brown).
Standardization of terminology is necessary for consistent discussion and patient management within the multidisciplinary team. The term ‘‘circumferential’’ implies a margin that is fully surrounding a viscus. Whereas this does apply to rectal tumours that are wholly below the peritoneal reflection, the use of the term ‘‘circumferential resection’’ is misleading and inaccurate for tumours that straddle or are above the peritoneal reflection. The term can cause confusion because, for tumours at or above the peritoneal reflection, only the part of the circumference below the peritoneal reflection is relevant to the assessment of surgically attainable margin status. The current European practice is the selective use of neoadjuvant chemoradiotherapy to optimize delayed surgical treatment. In the UK, the National Institute for Clinical Excellence (NICE) recommends that, for patients with invasive rectal cancers for whom surgery is being considered, magnetic resonance imaging (MRI) should be performed before treatment begins to determine who might benefit from either neoadjuvant therapy or surgery alone. These cancers should be discussed
0009-9260/$ - see front matter ª 2006 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2006.06.005
Clarifying margins in the multidisciplinary management of rectal cancer
within the multidisciplinary cancer management team. Using MRI and pathological images from patients recruited during the Magnetic Resonance Imaging and Rectal Cancer European Equivalence Study (MERCURY), we aimed to highlight the potential for confusion between the members of the multidisciplinary cancer management team when discussing cases.
Introduction During analysis of the data determined in the MERCURY study, it became apparent that radiologists and pathologists alike were misclassifying CRM involvement. We have used examples encountered in that study to highlight the importance of understanding the anatomy of the surgical CRM. Quirke and colleagues have shown the importance of the radial spread of rectal cancer and its relationship to the lateral resection margin.1 Before TME surgery was widely practised, rates of lateral resection margin involvement were as high as 27% and, as a consequence, a local recurrence rate of 85% was seen in the margin-positive group but only 3% in the margin-negative group.1e3 Pathological assessment, advocated by Quirke and subsequently adapted in the National Histopathology Guidelines, uses serial transverse 5-mm sectioning of the whole tumour and surrounding mesorectum; this enables assessment of the relationship of the tumour to and its distance from the surgical resection margin. The CRM is defined as positive if this distance is less than 1 mm.4 The presence or absence of CRM involvement has emerged as one of the crucial determinants for prognosis.5 In rectal cancer surgery the CRM is formed by the mesorectal fascia, which envelops the mesorectum and constitutes the dissection plane in TME. This structure can be consistently demonstrated using high-resolution MRI and, provided the images are obtained in a plane perpendicular to the rectum and mesorectum,6 the oblique axial images obtained correspond precisely to the specimen images.7,8
917
the rectum is surrounded by the mesorectum in an eccentric way. The mesorectum contains the vascular, nervous and lymphatic supplies of the rectum, is covered by visceral fascia and is separated from the parietal pelvic fascia (which covers the other pelvic structures) by thin areolar tissue. In the upper third, the mesorectal fat is continuous with the sigmoid mesocolon and the anterior aspect of the rectum is covered by peritoneum. Below this recto-vesical peritoneal pouch, the mesorectum encompasses the rectal circumference but disappears anteriorly at approximately the point where Denonvilliers’ fascia fuses with the posterior capsule of the prostate. In the median plane, the peritoneum is attached to the uppermost part of the posterior wall of the vagina in women, forming the recto-uterine or rectovaginal pouch of Douglas. In men, the peritoneum is attached to the seminal vesicles, vas deferens and bladder, forming the recto-vesical pouch. Behind the mesorectum lies a space and, posterior to this, the anterior surface of the sacrum is covered with a presacral parietal fascia (of Waldeyer). These fascial coverings can be seen in Fig. 1. Visceral fascia surrounding the mesorectum is reflected on the parietal pelvic fascia at the level of the pelvic floor. Loose connective tissue provides an interface between the visceral and parietal fasciae, which facilitates dissection along these embryologically defined planes and, with traction and counter-traction, forms bloodless cavities filled with air. This is the surgical plane of TME, and it is important to follow this to excise the rectum with its lymphovascular supply intact. Taking into consideration this anatomy, TME surgery proceeds as follows.
Anatomy of the rectum and TME surgery In the adult, the rectum begins 15 cm from the anal orifice at the acute rectosigmoid angle, at the level of S2e3. The upper third of the rectum is located intraperitoneally, the middle third lies partly in the peritoneum and the lower third, which is the widest part of the rectum (the ampulla), lies in the extra-peritoneal plane. Most of
Figure 1 Axial MRI showing the fascial planes of the pelvis at the level of the levator origins from the pelvic sidewall.
918
The inferior mesenteric artery is divided close to the aorta, preserving the autonomic nerves, and the vein is divided close to its last tributary at the pancreas. The mesorectum is then dissected free under direct vision, using sharp dissection, in contrast to the standard technique where blunt dissection and manual extraction at the rectosacral ligament often caused disruption of the posterior mesorectum. The conventional technique identified an area of thickened fascia, which anchors the mesorectum to the lateral pelvic wall. This is the pedicle previously described as a lateral ligament. Traditionally a surgical clamp would be placed across this, as it was believed to contain the middle rectal artery. This is an artificially developed ligament formed by the medial traction of the rectum and contains the important autonomic nerve plexus, which supplies urinary continence and sexual function. If the artery is present, it is usually small and unilateral. Therefore, this structure is preserved with TME, which is performed anteriorly to this to avoid breaching the mesorectum. Denonvilliers’ fascia is eventually transected distally as it fuses with the prostatic capsule. At this point, the inferior hypogastric nerve plexus (neurovascular bundles of Walsh) taper medially
G. Salerno et al.
and must be teased off the front of the mesorectum to avoid impotence and bladder dysfunction. In a low anterior resection, an almost bare anterior aspect of the anorectal muscle is seen below the attachment of Denonvilliers’ fascia to the specimen. Posteriorly, the TME specimen is separated from the recto-sacral ligament using sharp dissection; this dissection around the mesorectal fascia produces a bilobar TME specimen. Fig. 2 shows the lines of TME surgical excision. MRI can accurately identify the relationship of the tumour to this fascial layer and can therefore stage rectal tumours into non-favourable and favourable groups. Those with involved margins can be selected for preoperative therapy. With the increasing use of preoperative staging, the terminology that the radiologist uses should be consistent with that used by the pathologist. It is also important that, when reporting the relationship between tumour and margins, distinction is made between surgical and peritoneal margins, both radiologically and pathologically.
Preparation of the TME specimen by the histopathologist The specimen is opened except for the area of the tumour, to preserve assessment of the anterior aspect where CRM or peritoneal involvement may be seen. Anterior and posterior non-peritonealized surfaces are painted with ink (Fig. 3). It should be noted that the definition of circumferential margin only applies to the inked, surgically incised mesorectal planes and not the peritonealized surfaces.
Figure 2 Sagittal MRI showing the excision planes followed in total mesorectal excision.
Figure 3 Specimen preparation. Photograph of total mesorectal excision demonstrates inking of the nonperitonealized surface in order to enable distinction between the surgical resection margin and the serosal margin.
Clarifying margins in the multidisciplinary management of rectal cancer
919
tumour. The sections should also be photographed as a valuable demonstration of the quality of the surgery (Fig. 4), which may be independently assessed by the reporting pathologist.
Understanding surgical and histological margins in upper rectal cancers Anatomy of the peritoneal reflection
Figure 4 Gross pathological assessment of the specimen from total mesorectal excision, sectioned in the axial plane. The tissue sections are laid out to enable direct visual inspection of the tumour and its relationship to the mesorectal margin. Tissue sections demonstrating close relationship between tumour and ink margins are sampled so that the appropriate glassmounted histopathological slides can be prepared.
The mesorectal surface is larger posteriorly and extends to a higher level than it does anteriorly. After the resection surfaces have been inked and the specimen fixed in formalin for a minimum of 3 days (72 h), a description of the macroscopic appearances is made and the specimen is transversely sectioned into thin (3 to 5 mm) tissue sections from 2 cm below to 2 cm above the
The CRM represents the margin that the surgeon can influence by dissection along the mesorectal plane, but not all the rectum is surrounded by the mesorectum. In mid and upper rectal tumours, there is a peritonealized anterior surface. The peritoneal reflection is said to be situated 5.5 cm above the dentate line in women (but is variable) and 7.5 cm above in men. Approximately 25% of the anatomical rectum is invested by peritoneum in women and about 16% in men, and therefore spread from an advanced upper rectal cancer might be expected to involve the pelvic peritoneum, with seeding of tumour cells into the peritoneal cavity and pelvic tissues, outside the site of resection.9 Tumour may also extend through the peritoneum into adjacent organs, particularly the bladder, uterus or small bowel, but not the prostate which lies entirely below the peritoneal reflection.
Figure 5 Axial and sagittal MRI depicting the peritoneal reflection. On the axial image, the apex of the peritoneum attaches to the anterior rectal wall in a V-shaped configuration. In men this is generally at a point just above the tip of the seminal vesicles; in women the point of attachment is rather more variable.
920
G. Salerno et al.
Figure 6 Serial axial MRI sections demonstrating fat in the anterior mesorectum from the mid to the upper rectum. The point where no anterior mesorectal fat is seen is generally the point at which the peritoneal attachment begins.
The peritoneal reflection may be identified on sagittal MRI as a low-signal linear structure that can be seen extending from the posterior aspect of the dome of the bladder to the ventral aspect of the rectum. On axial section, the point of attachment has a V-shaped configuration (Fig. 5). The
point at which the peritoneal reflection commences can also be recognized on serial axial MRI through the mesorectum, showing the anterior mesorectal fat becoming thinner and thinner in the cranial direction. The point where no anterior mesorectal fat is seen is generally where the
Figure 7 Pathology specimens demonstrating the serosal surface of the rectum in blue. This becomes progressively more wide higher up in the rectum, until almost the entire circumference of the bowel wall is peritonealized apart from a narrow posterior strip that forms the sigmoid mesentery (arrows).
Figure 8 Axial image demonstrating a T4b circumferential tumour which has perforated through the rectal wall and also through the peritoneum (arrow).
Clarifying margins in the multidisciplinary management of rectal cancer
921
peritoneum begins (Fig. 6). This bare area of rectum becomes progressively wider in the cranial direction, until almost the entire circumference of the bowel is peritonealized apart from a narrow posterior strip that forms the sigmoid mesentery (Fig. 7).
Peritoneal involvement does not equate to CRM involvement
Figure 9 Sagittal MRI demonstrating a tumour in the upper third of the rectum. Images show anterior perforation of the tumour through the peritoneal reflection and into adjacent uterus. Because of direct spread into a contiguous organ, this would be staged as T4a disease on MRI. If the surgeon resects the uterus and primary tumour en bloc, the surgical resection margins will be negative.
An anterior tumour in the upper rectum which invades the peritoneum will be classed as a T4b tumour histologically (Fig. 8). There is frequently confusion owing to discrepancy between classification by the radiologist and classification by the pathologist. These tumours should be reported on MRI and histopathology as being CRMnegative, because CRM corresponds to the cut surgical resection margin and does not cover the anterior aspect of the upper rectum. Because the surgeon cannot influence the free peritoneal surface, the surgical resection margin (SRM) will be negative as the whole rectum will be excised. A T4b tumour in this area potentially sheds cells into the rectovesical space or pouch of Douglas, there is a higher risk of pelvic recurrence and there are the limitations of MRI in detecting
Figure 10 Axial MRI and corresponding histopathology section showing tumour extending anteriorly to involve the serosal margin, as well as the mesorectal fascia. The specimen demonstrates that the surgeon has cut through tumour; thus, the circumferential resection margins are involved by tumour.
922
microscopic peritoneal invasion. Currently, the demonstration of tumour extending through the peritoneal membrane is not an indication for either preoperative or adjuvant therapy, and there is only very limited experience in the treatment of colorectal peritoneal disease.10,11 Therefore, reporting such cases on MRI or histopathology as
G. Salerno et al.
positive margins could result in potential overtreatment. Adjacent organ invasion can occur into the bladder, uterus (Fig. 9) or small bowel. If the surgeon resects these organs en bloc, the peritoneal reflection will be involved by tumour and the tumour will be staged as T4a (direct spread
Figure 11 Axial tissue sections from an anteroposterior excision specimen and the preoperative MRI of a low rectal tumour. Images demonstrate tumour infiltrating the low rectum, with extension through the full thickness of the muscularis propria. No invasion of the levator sling, puborectalis or external sphincter muscles is revealed, but the surgical margins depend on the extent of the dissection and are unpredictable. Little tissue has been removed in the area corresponding to the curved arrow or anterolaterally on the right (large arrow), but more has been removed posterolaterally on the right.
Clarifying margins in the multidisciplinary management of rectal cancer
into contiguous organ) and T4b (direct spread into the peritoneum). However, SRMs are negative unless the surgeon cuts through tumour, resulting in a positive surgical resection margin (Fig. 10).
Margins around the low rectal cancer In low rectal cancer (defined as the area below the insertion of the levator muscle, approximately below 6 cm from the anal verge), the mesorectum volume is reduced, and in ano-rectal tumours there is no mesorectal plane, as the rectal muscle tube lies against the pelvic floor before passing through the external sphincter. Thus, the mesorectal fascia tapers as it fuses to the endopelvic fascia which overlies the levator muscles and in turn fuses with muscles of the external anal sphincter. In abdomino-perineal resection there is no clearly definable or predictable surgical plane, particularly when performing the perineal dissection, and hence the final SRM is variable and not predictable radiologically (Fig. 11). The surgeon may either dissect along the muscle tube, or extend laterally along the edges of the ischiorectal fossae. Anteriorly, the posterior vaginal wall or part of the prostate may or may not be excised. The term ‘‘prediction of circumferential margin’’ is therefore also inaccurate in low tumours.
Summary The radiologist reporting the MRI should state the relationship of the tumour to the mesorectal fascia for mid and upper rectal cancers. As there is no mesorectal fascia in the lowest tumours, the radiologist should describe the anatomical compartments that might need to be removed in order to achieve clear margins. This also applies to
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tumours above the peritoneal reflection, that are invading adjacent organs. To clarify resection margins, we propose that, instead of a report on whether CRM is involved or not by the radiologist reporting the MRI or the pathologist reporting the histology of the specimen, it should be stated whether the MRI potential surgical CRM or the surgical CRM is involved or not. In this way, the anatomical differences of the rectum and mesorectal fascia are accounted for and are related to the height of the tumour.
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