- Email: [email protected]
Surgical anatomy and anatomic surgery – Clinical and scientific mutualism
t h e s u r g e o n 1 1 ( 2 0 1 3 ) 1 7 7 e1 8 2
Available online at www.sciencedirect.com
The Surgeon, Journal of the Royal Colleges of Surgeons of Edinburgh and Ireland www.thesurgeon.net
Editorial
Surgical anatomy and anatomic surgery e Clinical and scientific mutualism5 Surgical anatomy and anatomic surgery The word “surgery” is derived from the Greek word “cheirourgia” (cheir refers to “hand” whilst ergos or urgos refers to “work”). Unfortunately the primary role of the surgeon is frequently obscured by myriad administrative, educational, service and research-based activities. Surgeons address diseases with specific anatomic properties. For example, in carotid artery stenosis due to atherosclerosis, the primary anatomic abnormality is a narrowing that is amenable to surgical correction. In general, the surgical approach to disease modification often involves removal or reconfiguration of an anatomic structure. Whatever the primary aim, surgery involves a restoration of anatomic conformation to as near normal as possible (in order to minimally disrupt function). Hence the central components of surgical technical practice (removal, reconfiguration, restoration) can be regarded as fundamentally anatomic-based. The importance of anatomy in surgery goes beyond this. Anatomic surgery adheres to a planar roadmap laid down during embryologic development. Planes are the interface between two contiguous structures.1 In anatomic surgery, deviation from a plane into a contiguous structure is directed and targeted such that trauma can be minimised. As a result, the fundamental principles of anatomic surgery are also those of safe and minimally traumatic surgery. It is not surprising then, historically, that surgical research was primarily anatomic in focus. The second half of the twentieth century saw a dramatic shift toward a spectrum spanning from the purely molecular to health policy implementation. Just as there was a move toward early pipeline molecular research (driven largely through the identification of the molecular basis of disease) there was a trend away from anatomic-based research. The resultant tendency has been towards acceptance of classic anatomic teaching, even in circumstances where discrepancy exists between that which we do surgically, and that which we are taught classically. A prime example of this discrepancy relates to the small intestinal and colonic mesentery (i.e. the mesocolon). Conventional teaching is the mesocolon is fragmented; the
5
Part presented in lecture format as the 35th Millin Lecture, Royal College of Surgeons in Ireland, 2012.
small intestinal mesentery, transverse and sigmoid mesocolon all “terminate” at their “insertion” into the posterior abdominal wall.2e4 However, gastrointestinal surgical practice has crucially relied on mesenteric contiguity from ileocaecal to mesorectal levels, for the past century (Fig. 1). The anatomic properties of the intestinal mesenteric attachments were established by Sir Frederick Treves in 1889 and thereafter perpetuated in almost all reference embryologic, anatomic and surgical texts.2,5e7 This remains the case to the present and is exemplified by descriptions of the small intestinal mesentery as “terminating” at its “insertion” (Fig. 2A). Such is the level of acceptance of this dogma, it surprises clinicians to hear that Carl Toldt described an alternative set of anatomic properties ten years prior to that of Treves, in 1879.8,9 Although Toldt’s findings correspond with astonishing accuracy to the anatomic principles of abdominal gastrointestinal surgery, they remain largely ignored by reference literature.2e10 In the following sections I outline recent advances in gastrointestinal anatomy and explain how these, in clarifying mesenteric structure, provide numerous opportunities across multiple scientific and clinical specialties. These advances highlight the importance of the mutualistic relationship between surgical anatomy and anatomic surgery.
Mesocolic anatomy To address the discrepancy between practice and teaching our group recently described the anatomic features of the mesocolon as they become apparent during total mesocolectomy (i.e. where the entire colon and mesocolon are mobilised and excised en-bloc).11,12 The findings contrast dramatically with those of Treves, and correspond precisely with those of Toldt (Figs. 1, 2A & B). Firstly, and perhaps most importantly, the mesocolon on the right and left persist into adulthood. Once persistence is acknowledged then it becomes apparent that the small intestinal and colonic mesenteric attachments are in fact contiguous to the level of the mesorectum. Although mesenteric contiguity was depicted in illustrations by Da Vinci, this observation, and implications thereof, have never been formally acknowledged.11,12 Next, the small intestinal and colonic mesentery do not “insert” into the posterior abdominal wall (and “terminate”) but rather become apposed to the retroperitoneum, with a
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(A)
(B)
Figure 1 e Two and a half dimension (2.5D) rendition of the colon and rectum together with associated mesenteric attachments. The small intestine and associated mesentery has been conceptually removed for the purposes of clarity. The 2.5D image is derived from a 3D model generated from a human mesocolon, in Zbrush (Pixologicª).
connective tissue layer (i.e. Toldt’s fascia) interposed between the two. In certain regions (i.e. the transverse mesocolon and the mobile component of the mesosigmoid) the mesocolon is nonapposed to the retroperitoneum and is thus mobile. When the small intestinal mesentery, right and transverse mesocolon are mobilised off the retroperitoneum, a central point of suspension becomes apparent at the origin of the superior mesenteric artery. It is from this point that the entire small intestinal and colonic mesentery fans out to adopt the adult conformation involving apposed and non-apposed regions (Fig. 1). There are several additional observations that are beyond the remit of this article (eg. the mesosigmoid is contiguous proximally with the left mesocolon and distally with the mesorectum (Figs. 1, 2 and 4)). Importantly, a compilation of these and the above observations clarifies the macroscopic structure of the mesenteric attachments of the gastrointestinal tract.
Figure 2 e (A): Zbrush-generated two and a half dimension (2.5D) rendition of the mesenteric attachment of the colon and rectum as depicted by Treves, with the colon and rectum conceptually removed for the purposes of clarity. The point of view is from the right side looking left and downward. The right and left mesocolon are “vestigial” or “absent” and the transverse mesocolon and mesosigmoid “insert” into the posterior abdominal wall along their root. (B) Zbrush-generated 2.5D rendition of the mesenteric attachment of the colon and rectum as is currently understood, with the colon and rectum conceptually removed for the purposes of clarity. The point of view is from the right side and looking left and downward. The mesocolon is contiguous throughout from ileocaecal to mesorectal levels.
This provides a standard against which abnormalities of structure (and hence of function) may be better understood.
Mesocolic histology Just as deficiencies persisted in relation to macroscopic mesocolic structure, similar deficiencies ccur regarding microscopic structure. Surprisingly, the histologic appearance of the normal mesocolon has, until recently, been ignored. Although mesocolic and mesenteric lymph nodes remain the focus of considerable oncologic and immunologic research, the surrounding structure is largely unchartered in terms of scientific endeavour. To redress this, our group conducted a
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(A)
(B)
Figure 4 e (A): Section derived from a transverse section of abdominal computerised axial tomogram (with colour inversion). The left mesocolon has been dissected off the retroperitoneum by a fluid collection contiguous with a fluid collection within the lesser sac. The patient had pancreatitis. (B) Computerised tomography of abdomen (without colour inversion) demonstrating a lymph node located within the right mesocolon. There is a lesion in the caecum. The fascia interposed between mesocolon and retroperitoneum (i.e. Toldt’s fascia) is apparent and prominent.
Figure 3 e (A): Haematoxylin and eosin stained photomicrograph of the right mesocolon progressing from the peritonealised (top) to retroperitoneal aspect (bottom). Inset is the cadaveric location from which the specimen was taken. (B) Transmission electron microscopic view of the same region (i.e. right mesocolon) progressing form the peritonealised aspect to the retroperitoneum.
formal characterisation of mesocolic histology. The mesocolon is highly organised with compartments of adipocytes of varying size and number, tightly packed between fibrous septae (Fig. 3). Septae arise from submesothelial connective tissue layers and house vessels as well as nervous structures. The outer (“superior”, or “peritoneal”, or “upper”) surface of the mesocolon is comprised of a single layer mesothelial lining as is the deeper (“retroperitoneal”, “under” or “inferior”) surface. From an anatomic perspective these findings prove the mesocolon remains extra-retroperitoneal throughout its length, in the adult human. This contradicts conventional teaching which maintains that the right and left mesocolon first become secondarily retroperitoneal (as do the right and left colon), before regressing and disappearing.
Mesocolic radiology Mesenteric attachments are a focus of abdominal radiologic imaging despite not having been formally characterised in
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detail. Though frequently mentioned in radiologic reference texts, the normal appearing mesocolon is the primary focus of two original articles only.13,14 In both, the mesocolon is identified, by proxy, using vascular markings.13,14 In neither is the mesocolon itself nor its structural relationships directly described. This is surprising as numerous intra-abdominal pathologies affect the mesocolon either directly or indirectly (for example through contiguous involvement from the gastrointestinal tract). Thus there is pressing need to determine the radiologic features of the normal appearing mesocolon, in order to better understand the implications of contiguous pathology. Our group has again commenced efforts in this regard by establishing the computerised axial tomographic (CT) appearance of the normal mesocolon. On both right and left sides of the peritoneal cavity, the mesocolon and associated fascia can be differentiated as separate from the underlying retroperitoneum (Fig. 4). Flexural confluency can be visualised between right and transverse mesocolon and also between the latter and the left mesocolon. In addition, knowledge of the normal appearing mesocolon enables a differentiation of abnormal features such as might occur in pathologic states. Dramatic mesocolic alterations can occur in severe pancreatitis, where fluid may track beneath the left mesocolon and dissect this off the retroperitoneum (Fig. 4A). Fascial oedema and mesocolic lymphadenopathy can be differentiated in cases of colonic adenocarcinoma (Fig. 4B). These findings could aid in preoperatative planning of surgical approaches as well as perioperative adjuvant treatment strategies (Fig. 4B). Recent studies highlight the importance of radiologic staging in identifying patients with colon cancer, who may be candidates for preoperative chemotherapy. In particular, patients with T3 disease beyond the musculars propria plane, appear to benefit from preoperative chemotherapy, through a reduction in apical lymph node positivity and increased downstaging.15 These are patients with radiologic evidence of contiguous spread into either the adjacent mesocolon, or into surrounding peritoneal tissue. Pilot results of the FOxTROT trial highlight the increasing clinical relevance of accurate preoperative CT radiologic staging in the management of colon cancer.15
Gastrointestinal surgery in general Most gastrointestinal tract surgery involves manipulation of the associated mesentery and mesocolon. This is crucial in safely mobilising the bowel to permit division and tensionfree anastomoses. Though not previously recorded, it is somewhat surprising how little time is spent intraoperatively on the intestinal component of a resection (i.e. dividing and re-anastomosing). This reflects the central importance of the technical approach to mesenteric/mesocolic mobilisation and division, as well as vessel skeletonisation. However, the correct three dimensional structure of the insitu mesocolon has only recently been acknowledged and as such descriptions in surgical technical literature are lacking. This is compounded by the fact that once mobilised, the mesocolon loses its in-situ shape and the resultant conformation bears little if any resemblance to that of the undisturbed structure. These factors have led to unavoidable gaps
in surgical technical literature. The classic format in which operations are generally described, centres on a collection of images depicting serial operative stages. The reader must then interpolate mesocolic shape changes between stages. For reasons outlined above, the process of interpolation has been greatly hampered in gastrointestinal surgery in general. Our group is focussing on approaches to obviating the interpolation of mesocolic shape changes and improving the educational process for gastrointestinal surgeons in training. Outwith the theatre or simulator setting, classic educational modalities have been either text or video-based. Text-based educational modalities render contiguous three dimensional shape changes by embedding appropriate graphics. Although not directly quantifiable, the requirement for interpolation between stages is considerable. Video-based modalities greatly assist in demonstrating contiguous shape changes between stages. There are limitations here too however, including poor definition and magnification, failure to provide the surgeon’s point of view, and a loss of regional anatomic orientation. Thus there is a compelling need to develop educational modalities that minimise interpolation of anatomic shapes and that enable the surgical educationalist transmit a truly anatomic understanding of mesocolic and/or mesenteric mobilisation. Our group has recently addressed this issue by applying the sculpting and animation capabilities of state-of the art digital imaging software. Using Zbrush (Pixologicª), a mesenteric and mesocolic replica was developed that could be moulded to reflect contiguous shape changes occurring during mobilisation. Anatomic regions were colour-coded and the mobilisation process animated to demonstrate contiguous anatomic alterations. This approach obviated interpolation between technical stages of mobilisation whilst simultaneously retaining regional anatomic detail (Fig. 5). Though the efficacy of this educational tool remains to be formally tested, it is likely this will greatly enhance surgical students’ understanding of what was previously regarded as a difficult area.
Mesocolic/mesenteric pathology Just as mesocolic structure is now established it is likely this will enhance our understanding of primary and secondary mesenteric pathology. To date, primary mesocolic pathology has largely been confined to concepts related to non-fixation and malrotation. Earlier interpretations indicated that the persistence of a right and left mesocolon was anomalous and contributed to pathology such as volvulus of the right or sigmoid colon. As we now acknowledge the normality of a right and left mesocolon, and of mesenteric contiguity, the primary abnormality in volvulus formation must be re-interpreted as being that of non-fixation (i.e. where these mesocolic components do not appose over a sufficient region of retroperitoneum as to prevent volvulus formation). Just as the pathogenesis of volvulus can be rationalised in these terms, so too can that of malrotation. In malrotation, the second part of the duodenum continues caudally (as opposed to transversely across the midline) into the right paracolic gutter. Given gastrointestinal and mesenteric contiguity, the right colon and mesocolon must be packaged medial to the small
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Figure 5 e (A): Two and a half dimension (2.5D) image of the mesosigmoid and mesorectum (colour-coded as follows: left mesocolon (green), apposed mesosigmoid (blue), mobile mesosigmoid (red) and mesorectum (yellow)) with the rectum and sigmoid colon conceptually removed to illustrate mesocolic contiguity. The point of view is looking down and back at the junction between the mesosigmoid and mesorectum. Partially (B), near fully (C) and fully mobilised (D) mesosigmoid respectively demonstrating contiguous shape changes during the mobilisation process. By demonstrating contiguous shape changes the surgical student is not required to interpolate topographic mesenteric changes as is currently required in standard operative texts.
intestinal mesentery, leading to a concertina-like mesenteric and gastrointestinal conformation. Once considered in terms of mesenteric topography, non-fixation and non or malrotation, are greatly simplified.16
Implications for surgical practice There are several clinical implications to the above. Recent data demonstrates that complete mesocolic excision is associated with improved oncologic outcomes. West et al. demonstrated when colectomy was performed in the “mesocolic” plane, as opposed to the “intra-mesocolic” or “muscularis propria” plane, long-term survival was improved.17 It is speculated these improvements relate to the harvest of greater numbers of lymph nodes (literature indicates that outcome is better with increasing lymph node yield). Their
findings emphasise the importance of resection of the entire mesocolon.17 The anatomic findings described in the present article relate directly to the mesocolon, and thus are likely to aid in performing a complete mesocolic resection by providing a technical roadmap for excision. In keeping with this, the concepts of mesocolic continuity, flexural contiguity and contiguity between mesosigmoid and mesorectum (as well as between small intestinal mesentery and right mesocolon), provide an anatomic platform on which surgeons may better tailor complete mesocolic resections. A second explanation of the observations of West et al., can be proffered based on our group’s histologic findings, and could have further implications for surgical practice.17 We observed that fibrous septae separate adipocyte compartments within the mesocolon and provide a scaffold for lymphatic and vascular conduits. By transgressing into the
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mesocolon, one disrupts surface mesothelium and intramesocolic fibrous channels. In so doing, it is feasible that lymphatic channels are also disrupted. These points emphasise the importance of maintaining mesocolic integrity as much as is feasible and that, where the mesocolon must be divided (e.g. dividing the mesocolon to permit segmental resection, skeletonisation of the major vessels, preparation of the colon for anastomosis) then techniques that both divide and cautery-seal might be employed. An improved appreciation of mesocolic anatomy and contiguity is also likely to facilitate high vascular tie. Debate persists as to the oncologic benefits of central/high vascular tie in colorectal resections for malignancy.18 Central or high vascular tie requires a sound understanding of mesocolic anatomy. This is particularly the case on the right side, where contiguity between the right mesocolon and small intestinal mesentery occurs. Importantly however, this contiguity has only recently been observed and documented. It follows that many so-called “high-ties” may not have been very high at all. Again, an improvement in anatomic understanding will help standardise surgical practice.18 The immediate benefits will lie in improved safety and approaches to teaching colonic/mesocolic resection. Additional benefits are also likely to occur in the context of standardisation across multi-institutional studies.
Summary An organ is defined as an anatomically and functionally distinct structure. The anatomic and histologic distinctiveness of the mesocolon and small intestinal mesentery underpin a functional distinctiveness that goes beyond acting as a simple scaffold. In keeping with this, early pipeline evidence indicates that the mesocolic and mesenteric organ is highly active at metabolic, immunologic, endocrine and many other levels. In considering the mesocolic/mesenteric organ as such, we can further systematise (and thus improve) our approach to human structure in both normality and in disease. This field of research endeavour has stemmed from the mutualistic relationship between surgical anatomy and anatomic surgery, and re-affirms the central importance of structure as a starting platform for clinico-biologic research in general.
Acknowledgements The author would like to acknowledge Dr Kevin Culligan, Dr Fabio Quondamatteo and Professor Peter Dockery.
references
1. Heald RJ. The ‘Holy Plane’ of rectal surgery. J R Soc Med 1988;81:503e8. 2. Treves F. Lectures on the anatomy of the intestinal canal and peritoneum in man. Br Med J 1885;1:580e3.
3. Ellis H. The abdomen and pelvis. In: Ellis H, editor. Clinical anatomy: applied anatomy for students and junior doctors. 12th ed. Blackwell Science; 2010. p. 86. 4. McMinn RH. The gastrointestinal tract. In: McMinn RH, editor. Last’s anatomy: regional and applied. 9th ed. London: Langman Group Ltd; 1994. p. 331e42. 5. Netter FH. Abdomen. In: Netter FH, editor. Atlas of human anatomy. Philadelphia, Pennsylvania: Saunders; 2007. p. 270e4. 6. Standring S. Large intestine. In: Standring S, editor. Gray’s anatomy: the anatomical basis of clinical practice. 40th ed. Philadelphia: Churchill Livingstone; 2008. p. 1137. 7. Adams A, McConnell T. Abnormalities of fixation of the ascending colon: the relation of symptoms to anatomical findings. Br J Surg 1923;10:532e57. 8. Toldt C. Bau und wachstumsveranterungen der gekrose des menschlischen darmkanales. Denkschrdmathnaturwissensch 1879;41:1e56. 9. Toldt C. An atlas of human anatomy for students and physicians 1919;vol.4.408. 10. Agur AMR. The abdomen. In: Agur AMR, editor. Grant’s atlas of anatomy. New York: Williams and Wilkins; 2008. p. 77e147. 11. Culligan K, Coffey JC, Kiran RP, Kalady M, Lavery IC, Remzi FH. The mesocolon: a prospective observational study. Colorectal Dis 2012;14:421e30. 12. Culligan K, Remzi FH, Soop M, Coffey JC. Review of nomenclature in colonic surgery e proposal of a standardised nomenclature based on mesocolic anatomy. Surgeon 2013;1:1e5. 13. Charnsangavej C, DuBrow RA, Varma DG, Herron DH, Robinson TJ, Whitley NO. CT of the mesocolon. Part 1. Anatomic considerations. Radiographics 1993 Sep;13(5):1035e45. 14. Charnsangavej C, Dubrow RA, Varma DG, Herron DH, Robinson TJ, Whitley NO. CT of the mesocolon. Part 2. Pathologic considerations. Radiographics 1993 Nov;13(6):1309e22. 15. Foxtrot Collaborative Group. Feasibility of preoperative chemotherapy forlocally advanced, operable colon cancer: the pilot phase of a randomisedcontrolled trial. Lancet Oncol 2012 Nov;13(11):1152e60. 16. Coffey JC. Malrotation. Chapter 4.3 in Rob and Smith operative surgery of the colon rectum and anus, in press. 17. West NP, Morris EJ, Rotimi O, Cairns A, Finan PJ, Quirke P. Pathology grading of colon cancer surgical resection and its association with survival: a retrospective observational study. Lancet Oncol 2008 Sep;9(9):857e65. 18. Hohenberger W, Weber K, Matzel K, Papadopoulos T, Merkel S. Standardized surgery for colonic cancer: complete mesocolic excision and central ligationetechnical notes and outcome. Colorectal Dis 2009 May;11(4):354e64.
J.C. Coffey Department of Surgery, 4i Centre for Interventions in Infection, Inflammation and Immunity, Graduate Entry Medical School, University of Limerick, University of Limerick, Limerick, Ireland 29 January 2013 [email protected], [email protected] Available online 15 April 2013 1479-666X/$ e see front matter ª 2013 Royal College of Surgeons of Edinburgh (Scottish charity number SC005317) and Royal College of Surgeons in Ireland. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.surge.2013.03.002
Available online at www.sciencedirect.com
The Surgeon, Journal of the Royal Colleges of Surgeons of Edinburgh and Ireland www.thesurgeon.net
Editorial
Surgical anatomy and anatomic surgery e Clinical and scientific mutualism5 Surgical anatomy and anatomic surgery The word “surgery” is derived from the Greek word “cheirourgia” (cheir refers to “hand” whilst ergos or urgos refers to “work”). Unfortunately the primary role of the surgeon is frequently obscured by myriad administrative, educational, service and research-based activities. Surgeons address diseases with specific anatomic properties. For example, in carotid artery stenosis due to atherosclerosis, the primary anatomic abnormality is a narrowing that is amenable to surgical correction. In general, the surgical approach to disease modification often involves removal or reconfiguration of an anatomic structure. Whatever the primary aim, surgery involves a restoration of anatomic conformation to as near normal as possible (in order to minimally disrupt function). Hence the central components of surgical technical practice (removal, reconfiguration, restoration) can be regarded as fundamentally anatomic-based. The importance of anatomy in surgery goes beyond this. Anatomic surgery adheres to a planar roadmap laid down during embryologic development. Planes are the interface between two contiguous structures.1 In anatomic surgery, deviation from a plane into a contiguous structure is directed and targeted such that trauma can be minimised. As a result, the fundamental principles of anatomic surgery are also those of safe and minimally traumatic surgery. It is not surprising then, historically, that surgical research was primarily anatomic in focus. The second half of the twentieth century saw a dramatic shift toward a spectrum spanning from the purely molecular to health policy implementation. Just as there was a move toward early pipeline molecular research (driven largely through the identification of the molecular basis of disease) there was a trend away from anatomic-based research. The resultant tendency has been towards acceptance of classic anatomic teaching, even in circumstances where discrepancy exists between that which we do surgically, and that which we are taught classically. A prime example of this discrepancy relates to the small intestinal and colonic mesentery (i.e. the mesocolon). Conventional teaching is the mesocolon is fragmented; the
5
Part presented in lecture format as the 35th Millin Lecture, Royal College of Surgeons in Ireland, 2012.
small intestinal mesentery, transverse and sigmoid mesocolon all “terminate” at their “insertion” into the posterior abdominal wall.2e4 However, gastrointestinal surgical practice has crucially relied on mesenteric contiguity from ileocaecal to mesorectal levels, for the past century (Fig. 1). The anatomic properties of the intestinal mesenteric attachments were established by Sir Frederick Treves in 1889 and thereafter perpetuated in almost all reference embryologic, anatomic and surgical texts.2,5e7 This remains the case to the present and is exemplified by descriptions of the small intestinal mesentery as “terminating” at its “insertion” (Fig. 2A). Such is the level of acceptance of this dogma, it surprises clinicians to hear that Carl Toldt described an alternative set of anatomic properties ten years prior to that of Treves, in 1879.8,9 Although Toldt’s findings correspond with astonishing accuracy to the anatomic principles of abdominal gastrointestinal surgery, they remain largely ignored by reference literature.2e10 In the following sections I outline recent advances in gastrointestinal anatomy and explain how these, in clarifying mesenteric structure, provide numerous opportunities across multiple scientific and clinical specialties. These advances highlight the importance of the mutualistic relationship between surgical anatomy and anatomic surgery.
Mesocolic anatomy To address the discrepancy between practice and teaching our group recently described the anatomic features of the mesocolon as they become apparent during total mesocolectomy (i.e. where the entire colon and mesocolon are mobilised and excised en-bloc).11,12 The findings contrast dramatically with those of Treves, and correspond precisely with those of Toldt (Figs. 1, 2A & B). Firstly, and perhaps most importantly, the mesocolon on the right and left persist into adulthood. Once persistence is acknowledged then it becomes apparent that the small intestinal and colonic mesenteric attachments are in fact contiguous to the level of the mesorectum. Although mesenteric contiguity was depicted in illustrations by Da Vinci, this observation, and implications thereof, have never been formally acknowledged.11,12 Next, the small intestinal and colonic mesentery do not “insert” into the posterior abdominal wall (and “terminate”) but rather become apposed to the retroperitoneum, with a
178
t h e s u r g e o n 1 1 ( 2 0 1 3 ) 1 7 7 e1 8 2
(A)
(B)
Figure 1 e Two and a half dimension (2.5D) rendition of the colon and rectum together with associated mesenteric attachments. The small intestine and associated mesentery has been conceptually removed for the purposes of clarity. The 2.5D image is derived from a 3D model generated from a human mesocolon, in Zbrush (Pixologicª).
connective tissue layer (i.e. Toldt’s fascia) interposed between the two. In certain regions (i.e. the transverse mesocolon and the mobile component of the mesosigmoid) the mesocolon is nonapposed to the retroperitoneum and is thus mobile. When the small intestinal mesentery, right and transverse mesocolon are mobilised off the retroperitoneum, a central point of suspension becomes apparent at the origin of the superior mesenteric artery. It is from this point that the entire small intestinal and colonic mesentery fans out to adopt the adult conformation involving apposed and non-apposed regions (Fig. 1). There are several additional observations that are beyond the remit of this article (eg. the mesosigmoid is contiguous proximally with the left mesocolon and distally with the mesorectum (Figs. 1, 2 and 4)). Importantly, a compilation of these and the above observations clarifies the macroscopic structure of the mesenteric attachments of the gastrointestinal tract.
Figure 2 e (A): Zbrush-generated two and a half dimension (2.5D) rendition of the mesenteric attachment of the colon and rectum as depicted by Treves, with the colon and rectum conceptually removed for the purposes of clarity. The point of view is from the right side looking left and downward. The right and left mesocolon are “vestigial” or “absent” and the transverse mesocolon and mesosigmoid “insert” into the posterior abdominal wall along their root. (B) Zbrush-generated 2.5D rendition of the mesenteric attachment of the colon and rectum as is currently understood, with the colon and rectum conceptually removed for the purposes of clarity. The point of view is from the right side and looking left and downward. The mesocolon is contiguous throughout from ileocaecal to mesorectal levels.
This provides a standard against which abnormalities of structure (and hence of function) may be better understood.
Mesocolic histology Just as deficiencies persisted in relation to macroscopic mesocolic structure, similar deficiencies ccur regarding microscopic structure. Surprisingly, the histologic appearance of the normal mesocolon has, until recently, been ignored. Although mesocolic and mesenteric lymph nodes remain the focus of considerable oncologic and immunologic research, the surrounding structure is largely unchartered in terms of scientific endeavour. To redress this, our group conducted a
t h e s u r g e o n 1 1 ( 2 0 1 3 ) 1 7 7 e1 8 2
179
(A)
(B)
Figure 4 e (A): Section derived from a transverse section of abdominal computerised axial tomogram (with colour inversion). The left mesocolon has been dissected off the retroperitoneum by a fluid collection contiguous with a fluid collection within the lesser sac. The patient had pancreatitis. (B) Computerised tomography of abdomen (without colour inversion) demonstrating a lymph node located within the right mesocolon. There is a lesion in the caecum. The fascia interposed between mesocolon and retroperitoneum (i.e. Toldt’s fascia) is apparent and prominent.
Figure 3 e (A): Haematoxylin and eosin stained photomicrograph of the right mesocolon progressing from the peritonealised (top) to retroperitoneal aspect (bottom). Inset is the cadaveric location from which the specimen was taken. (B) Transmission electron microscopic view of the same region (i.e. right mesocolon) progressing form the peritonealised aspect to the retroperitoneum.
formal characterisation of mesocolic histology. The mesocolon is highly organised with compartments of adipocytes of varying size and number, tightly packed between fibrous septae (Fig. 3). Septae arise from submesothelial connective tissue layers and house vessels as well as nervous structures. The outer (“superior”, or “peritoneal”, or “upper”) surface of the mesocolon is comprised of a single layer mesothelial lining as is the deeper (“retroperitoneal”, “under” or “inferior”) surface. From an anatomic perspective these findings prove the mesocolon remains extra-retroperitoneal throughout its length, in the adult human. This contradicts conventional teaching which maintains that the right and left mesocolon first become secondarily retroperitoneal (as do the right and left colon), before regressing and disappearing.
Mesocolic radiology Mesenteric attachments are a focus of abdominal radiologic imaging despite not having been formally characterised in
180
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detail. Though frequently mentioned in radiologic reference texts, the normal appearing mesocolon is the primary focus of two original articles only.13,14 In both, the mesocolon is identified, by proxy, using vascular markings.13,14 In neither is the mesocolon itself nor its structural relationships directly described. This is surprising as numerous intra-abdominal pathologies affect the mesocolon either directly or indirectly (for example through contiguous involvement from the gastrointestinal tract). Thus there is pressing need to determine the radiologic features of the normal appearing mesocolon, in order to better understand the implications of contiguous pathology. Our group has again commenced efforts in this regard by establishing the computerised axial tomographic (CT) appearance of the normal mesocolon. On both right and left sides of the peritoneal cavity, the mesocolon and associated fascia can be differentiated as separate from the underlying retroperitoneum (Fig. 4). Flexural confluency can be visualised between right and transverse mesocolon and also between the latter and the left mesocolon. In addition, knowledge of the normal appearing mesocolon enables a differentiation of abnormal features such as might occur in pathologic states. Dramatic mesocolic alterations can occur in severe pancreatitis, where fluid may track beneath the left mesocolon and dissect this off the retroperitoneum (Fig. 4A). Fascial oedema and mesocolic lymphadenopathy can be differentiated in cases of colonic adenocarcinoma (Fig. 4B). These findings could aid in preoperatative planning of surgical approaches as well as perioperative adjuvant treatment strategies (Fig. 4B). Recent studies highlight the importance of radiologic staging in identifying patients with colon cancer, who may be candidates for preoperative chemotherapy. In particular, patients with T3 disease beyond the musculars propria plane, appear to benefit from preoperative chemotherapy, through a reduction in apical lymph node positivity and increased downstaging.15 These are patients with radiologic evidence of contiguous spread into either the adjacent mesocolon, or into surrounding peritoneal tissue. Pilot results of the FOxTROT trial highlight the increasing clinical relevance of accurate preoperative CT radiologic staging in the management of colon cancer.15
Gastrointestinal surgery in general Most gastrointestinal tract surgery involves manipulation of the associated mesentery and mesocolon. This is crucial in safely mobilising the bowel to permit division and tensionfree anastomoses. Though not previously recorded, it is somewhat surprising how little time is spent intraoperatively on the intestinal component of a resection (i.e. dividing and re-anastomosing). This reflects the central importance of the technical approach to mesenteric/mesocolic mobilisation and division, as well as vessel skeletonisation. However, the correct three dimensional structure of the insitu mesocolon has only recently been acknowledged and as such descriptions in surgical technical literature are lacking. This is compounded by the fact that once mobilised, the mesocolon loses its in-situ shape and the resultant conformation bears little if any resemblance to that of the undisturbed structure. These factors have led to unavoidable gaps
in surgical technical literature. The classic format in which operations are generally described, centres on a collection of images depicting serial operative stages. The reader must then interpolate mesocolic shape changes between stages. For reasons outlined above, the process of interpolation has been greatly hampered in gastrointestinal surgery in general. Our group is focussing on approaches to obviating the interpolation of mesocolic shape changes and improving the educational process for gastrointestinal surgeons in training. Outwith the theatre or simulator setting, classic educational modalities have been either text or video-based. Text-based educational modalities render contiguous three dimensional shape changes by embedding appropriate graphics. Although not directly quantifiable, the requirement for interpolation between stages is considerable. Video-based modalities greatly assist in demonstrating contiguous shape changes between stages. There are limitations here too however, including poor definition and magnification, failure to provide the surgeon’s point of view, and a loss of regional anatomic orientation. Thus there is a compelling need to develop educational modalities that minimise interpolation of anatomic shapes and that enable the surgical educationalist transmit a truly anatomic understanding of mesocolic and/or mesenteric mobilisation. Our group has recently addressed this issue by applying the sculpting and animation capabilities of state-of the art digital imaging software. Using Zbrush (Pixologicª), a mesenteric and mesocolic replica was developed that could be moulded to reflect contiguous shape changes occurring during mobilisation. Anatomic regions were colour-coded and the mobilisation process animated to demonstrate contiguous anatomic alterations. This approach obviated interpolation between technical stages of mobilisation whilst simultaneously retaining regional anatomic detail (Fig. 5). Though the efficacy of this educational tool remains to be formally tested, it is likely this will greatly enhance surgical students’ understanding of what was previously regarded as a difficult area.
Mesocolic/mesenteric pathology Just as mesocolic structure is now established it is likely this will enhance our understanding of primary and secondary mesenteric pathology. To date, primary mesocolic pathology has largely been confined to concepts related to non-fixation and malrotation. Earlier interpretations indicated that the persistence of a right and left mesocolon was anomalous and contributed to pathology such as volvulus of the right or sigmoid colon. As we now acknowledge the normality of a right and left mesocolon, and of mesenteric contiguity, the primary abnormality in volvulus formation must be re-interpreted as being that of non-fixation (i.e. where these mesocolic components do not appose over a sufficient region of retroperitoneum as to prevent volvulus formation). Just as the pathogenesis of volvulus can be rationalised in these terms, so too can that of malrotation. In malrotation, the second part of the duodenum continues caudally (as opposed to transversely across the midline) into the right paracolic gutter. Given gastrointestinal and mesenteric contiguity, the right colon and mesocolon must be packaged medial to the small
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Figure 5 e (A): Two and a half dimension (2.5D) image of the mesosigmoid and mesorectum (colour-coded as follows: left mesocolon (green), apposed mesosigmoid (blue), mobile mesosigmoid (red) and mesorectum (yellow)) with the rectum and sigmoid colon conceptually removed to illustrate mesocolic contiguity. The point of view is looking down and back at the junction between the mesosigmoid and mesorectum. Partially (B), near fully (C) and fully mobilised (D) mesosigmoid respectively demonstrating contiguous shape changes during the mobilisation process. By demonstrating contiguous shape changes the surgical student is not required to interpolate topographic mesenteric changes as is currently required in standard operative texts.
intestinal mesentery, leading to a concertina-like mesenteric and gastrointestinal conformation. Once considered in terms of mesenteric topography, non-fixation and non or malrotation, are greatly simplified.16
Implications for surgical practice There are several clinical implications to the above. Recent data demonstrates that complete mesocolic excision is associated with improved oncologic outcomes. West et al. demonstrated when colectomy was performed in the “mesocolic” plane, as opposed to the “intra-mesocolic” or “muscularis propria” plane, long-term survival was improved.17 It is speculated these improvements relate to the harvest of greater numbers of lymph nodes (literature indicates that outcome is better with increasing lymph node yield). Their
findings emphasise the importance of resection of the entire mesocolon.17 The anatomic findings described in the present article relate directly to the mesocolon, and thus are likely to aid in performing a complete mesocolic resection by providing a technical roadmap for excision. In keeping with this, the concepts of mesocolic continuity, flexural contiguity and contiguity between mesosigmoid and mesorectum (as well as between small intestinal mesentery and right mesocolon), provide an anatomic platform on which surgeons may better tailor complete mesocolic resections. A second explanation of the observations of West et al., can be proffered based on our group’s histologic findings, and could have further implications for surgical practice.17 We observed that fibrous septae separate adipocyte compartments within the mesocolon and provide a scaffold for lymphatic and vascular conduits. By transgressing into the
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mesocolon, one disrupts surface mesothelium and intramesocolic fibrous channels. In so doing, it is feasible that lymphatic channels are also disrupted. These points emphasise the importance of maintaining mesocolic integrity as much as is feasible and that, where the mesocolon must be divided (e.g. dividing the mesocolon to permit segmental resection, skeletonisation of the major vessels, preparation of the colon for anastomosis) then techniques that both divide and cautery-seal might be employed. An improved appreciation of mesocolic anatomy and contiguity is also likely to facilitate high vascular tie. Debate persists as to the oncologic benefits of central/high vascular tie in colorectal resections for malignancy.18 Central or high vascular tie requires a sound understanding of mesocolic anatomy. This is particularly the case on the right side, where contiguity between the right mesocolon and small intestinal mesentery occurs. Importantly however, this contiguity has only recently been observed and documented. It follows that many so-called “high-ties” may not have been very high at all. Again, an improvement in anatomic understanding will help standardise surgical practice.18 The immediate benefits will lie in improved safety and approaches to teaching colonic/mesocolic resection. Additional benefits are also likely to occur in the context of standardisation across multi-institutional studies.
Summary An organ is defined as an anatomically and functionally distinct structure. The anatomic and histologic distinctiveness of the mesocolon and small intestinal mesentery underpin a functional distinctiveness that goes beyond acting as a simple scaffold. In keeping with this, early pipeline evidence indicates that the mesocolic and mesenteric organ is highly active at metabolic, immunologic, endocrine and many other levels. In considering the mesocolic/mesenteric organ as such, we can further systematise (and thus improve) our approach to human structure in both normality and in disease. This field of research endeavour has stemmed from the mutualistic relationship between surgical anatomy and anatomic surgery, and re-affirms the central importance of structure as a starting platform for clinico-biologic research in general.
Acknowledgements The author would like to acknowledge Dr Kevin Culligan, Dr Fabio Quondamatteo and Professor Peter Dockery.
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J.C. Coffey Department of Surgery, 4i Centre for Interventions in Infection, Inflammation and Immunity, Graduate Entry Medical School, University of Limerick, University of Limerick, Limerick, Ireland 29 January 2013 [email protected], [email protected] Available online 15 April 2013 1479-666X/$ e see front matter ª 2013 Royal College of Surgeons of Edinburgh (Scottish charity number SC005317) and Royal College of Surgeons in Ireland. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.surge.2013.03.002