MMCTS
(June 3, 2009). doi:10.1510/mmcts.2007.002956
Copyright © 2009 European Association for Cardio-thoracic Surgery
Procedure
Colon interposition for oesophageal replacement
Pascal A. Thomas*,
Adrian Gilardoni,
Delphine Trousse,
Xavier B. D'Journo,
Jean-Philippe Avaro,
Christophe Doddoli,
Roger Giudicelli and
Pierre Fuentes
Department of Thoracic Surgery and Diseases of the Oesophagus, Sainte Marguerite Hospital, University of the Mediterranean, Assistance Publique and Hôpitaux de Marseille, 270 bvd Sainte Marguerite, 13274 Marseille, France
* Corresponding author: Tel.: +33-491-744 680; fax: +33-491-744 590. pathomas{at}ap-hm.fr
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Summary
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The choice of the colon as an oesophageal substitute results primarily from the unavailability of the stomach. However, given its durability and function, colon interposition keeps elective indications in patients with benign or malignant oesophageal disease who are potential candidates for long survival. The choice of the colonic portion used for oesophageal reconstruction depends on the required length of the graft, and the encountered colonic vascular anatomy, the last being characterised by the near-invariability of the left colonic vessels, in contrast to the vascular pattern of the right side of the colon. Accordingly, the transverse colon with all or part of the ascending colon is the substitute of choice, positioned in the isoperistaltic direction, and supplied either from the left colic vessels for long grafts or middle colic vessels for shorter grafts. Technical key points are: full mobilisation of the entire colon, identification of the main colonic vessels and collaterals, and a prolonged clamping test to ensure the permeability of the chosen nourishing pedicle. Transposition through the posterior mediastinum in the oesophageal bed is the shortest one and thereby offers the best functional results. When the oesophageal bed is not available, the retrosternal route is the preferred alternative option. The food bolus travelling mainly by gravity makes straightness of the conduit of paramount importance. The proximal anastomosis is a single-layer hand-fashioned end-to-end anastomosis to prevent narrowing. When the stomach is available, the distal anastomosis is best performed at the posterior part of the antrum for the reasons of pedicle positioning and reflux prevention, and a gastric drainage procedure is added when the oesophagus and vagus nerves have been removed. In the other cases, a Roux-en-Y jejunal loop is preferable to prevent bile reflux into the colon. Additional procedures include re-establishment of the colonic continuity, a careful closure of the mesentery to avoid a further internal hernia, and routine appendectomy. When applying these technical aids, the chances of achieving a viable and well-functioning colon graft are excellent.
Key Words: Colon graft interposition Oesophageal surgery
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Introduction
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Even if gastric tubulisation has received wide acceptance by most teams involved in oesophageal surgery, the use of the colon as an oesophageal substitute plays a key role in the field of oesophageal reconstruction, especially, when the stomach is no more available. Hence, coloplasty may be the only option in various situations: when a previous gastric surgery precludes the use of the stomach, when a total gastrectomy is required in combination with the oesophagectomy, or as a salvage procedure when a previous gastroplasty failed. Besides these by default indications, coloplasty keeps elective indications in those situations typified by the young age of the patient and the need for oesophagectomy for a benign disorder [1]. Indeed, the preservation of the stomach as a pouch is an important aspect to be considered as far as quality of life is concerned. The use of the stomach leads to a significant loss of capacity of the gastric reservoir leading to the fractionation of food intake during the first month after the operation and long-term gastroesophageal reflux with its attendant pulmonary complications and possible recurrent peptic stricture. In the spectrum of cancer operations, colon interposition is also used selectively for reconstruction of the alimentary tract after the resection of tumours located at the vicinity of the pharynx because of transplant length (Photo 1). Nowadays, by-pass oesophagocoloplasty has become a very uncommon operation performed in highly selected patients. Nevertheless, it can be particularly helpful after failure or complications of endoscopic procedures attempted to palliate dysphagia.

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Photo 1 (A) Total oeso-pharyngo-laryngectomy for cancer (operative specimen); (B) pharyngo-colic anastomosis (the pharynx is identified by the asterisk).
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As a result of its technical complexity, postoperative morbidity associated with coloplasty remains a matter of serious concern. The present chapter focuses on technical points that can prevent devastating complications because, as often in surgery, the devil lies in details. Indeed, seemingly minor judgmental or technical errors can have disastrous consequences on the initial viability or long-term function of the graft.
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Vascular anatomy
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In the healthy state, the colon derives its blood supply from branches of the superior mesenteric artery (SMA) and the inferior mesenteric artery (IMA) (Schematic 1). By convention, a colonic graft that is partly or mainly constituted of right anatomical colon but for which the nourishing pedicle is issuing from the inferior mesenteric system is termed left colonic graft. Conversely, a colonic graft that is branched on the superior mesenteric vasculature is named right colonic graft.

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Schematic 1 Vasculature of the colon.
1 and 2, right colic arteries; 3 and 4, ileocolic arteries; 5, superior mesenteric artery; 6, marginal artery; 7, inferior mesenteric artery; 8, sigmoid arteries; 9, left colic artery. (Reproduced from Thomas P, D'Journo XB. Ceroplastics. In: Triboulet JP, editor. Chirurgie du tube digestif. Paris: Masson, 2008:92, with permission from Masson.)
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The colonic vascular anatomy is characterised by the near-invariability of the left colonic vessels, in contrast to the vascular pattern of the right side of the colon. These features have been extensively addressed in a recent comprehensive review [2]. The right colon – that is, the cecum, ascending colon, hepatic flexure, and proximal half or two-thirds of the transverse colon – is supplied by branches of the SMA: the middle colic, the right colic, and the ileocolic arteries. Of these, the ileocolic artery is the most constant, as the right colic and the middle colic arteries could be absent. The middle colic artery primarily supplies the transverse colon. Anatomic variations of the middle colic artery include complete absence in up to 25% of individuals, presence of an accessory or double middle colic artery in 10%. The middle colic artery is divided into a right and a left branch, approximately at the centre of the transverse mesocolon. The left branch of the middle colic artery supplies a part of the colon also supplied by the left colic artery through the collateral channel of the marginal artery. The right colic artery, together with the ileocecal artery, supplies the ascending colon. Of surgical importance is the fact that the right colic artery has the greatest variations among colic arteries. It may be absent in about 20% of subjects, in whom the ascending colon is supplied by the middle colic and ileocolic arteries. It divides into an ascending and descending branch that communicates with the right branch of the middle colic artery and the ileocolic artery, respectively. Anastomosis between the right colic and ileocolic arteries is absent in 5% of subjects, creating a weak point at this level when a long isoperistaltic colonic graft is performed, leading to segmental ischaemia, anastomotic breakdown, and sepsis. The ileocolic artery is the terminal branch of the SMA and, therefore, is the most constant tributary leaving the SMA. It supplies the terminal ileum, cecum, and first half of the right colon.
The arterial supply to the left colon is from the IMA by means of its left colic and sigmoid branches. The left colic artery is the highest branch of the IMA. Typically, the ascending branch of the left colic artery supplies the distal third of the transverse colon and the splenic flexure, by joining the left branch of the middle colic artery. In the absence of a prominent left colic artery, branches of the colosigmoid artery and the paracolic artery may form an anastomotic arcade supplying collateral to the splenic flexure.
A rich collateral circulation supports this complex vascular network. The marginal artery of Drummond is the major collateral arcade between the two mesenteric vessels. It consists usually of a continuous artery that runs parallel to the colon. The marginal artery is better developed in the left colon and can be inconsistent in the right colon in 25–75% of individuals, and even interrupted in 5% at the level of the splenic flexure. However, it can enlarge markedly when the IMA is occluded to provide blood supply to the entire left colon. Indeed, in patients with severe atherosclerotic disease or abdominal aortic aneurysm, IMA may be occluded (or ligated), and yet the sigmoid vessels fill satisfactorily, through the superior mesenteric/middle colic, and marginal arteries, thus providing an adequate blood flow to the left colon in the vast majority of cases. Likely, misleading arterial beatings may be palpated by the surgeon at the level of the left colic artery, even in the presence of an IMA occlusion, with disastrous consequences when a left colonic graft is performed.
The veins of the colon closely go along with the corresponding arteries and the venous blood flow reaches the portal vein by superior or inferior mesenteric tributaries. However, there are considerable variations in number and size. Therefore, the surgeon should always remember that ischaemia is not always the result of an arterial failure, but may also originate from venous blood flow impairment due to an injury or a skewing of the corresponding veins.
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Surgical technique
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Preoperative evaluation of the colon
Preoperative evaluation of the colon is necessary when the patient is at risk for associated colonic pathology such as chronic ischaemia, cancer, or diverticulosis. Colonoscopy allows for the evaluation of mucosal trophicity in patients with atherosclerosis, and the opportunity to biopsy and treat unsuspected lesions. The role of preoperative mesenteric arteriography is controversial. The routine use of this invasive technique seems somewhat excessive, because anatomic variations in the colonic vasculature rarely modify the planned operative procedure in the healthy state dramatically. However, elective indications remain when the patient complains of lower extremity claudication or presents with an aortic aneurysm. Another indication is a history of a previous abdominal operation during which major colonic vessels or the marginal artery may have been injured or ligated [1]. This information is of paramount importance in patients in whom a long conduit and anastomosis at the neck are required.
Bowel preparation
In patients in whom oral feeding is still possible, bowel preparation consists of five days of an appropriate diet, followed by oral cathartics and retrograde tap water enemas the day before operation. Patients who receive total parenteral nutrition undergo solely repeated water enemas, the number of which is adapted to the aspect of the washing.
Surgical approach
A midline laparotomy is usually performed unless the oesophagocolic anastomosis is to be made below the aortic arch. In this case, a left posterolateral thoracoabdominal incision is typically used, and the diaphragm is incised peripherally to allow access into the abdomen for preparation of the colon graft. In fact, even long segment coloplasty can be equally well-performed through a left thoraco-abdominal approach. Depending on the level of the proposed proximal oeso-colic anastomosis, a right thoracotomy, or a left pre-sternomastoid cervical approach could be appropriate.
The longest grafts are usually performed for oncological reasons with a proximal anastomosis in the neck after a transthoracic or a transhiatal oesophagectomy. Shorter grafts are usually dedicated to non-tumoral stenosis with a normal oesophageal motricity and involve an intrathoracic anastomosis.
Choice of the colonic graft
The choice of the colonic portion used for oesophageal reconstruction depends on the required length of the graft, and the encountered colonic vascular anatomy. For obvious functional reasons, an isoperistaltic coloplasty should be preferred whenever possible. In most cases the transverse colon with all or part of the ascending colon is chosen, positioned in the isoperistaltic direction, and based either on the left colic vessels for long grafts or the middle colic vessels for shorter grafts. For the aforementioned reasons, these grafts are the safest ones in terms of blood supply. Their main disadvantage lies in the great diameter of the viscera at the level of the oeso-colonic anastomosis with the inherent incongruence. Another long isoperistaltic graft could be provided by the ascending colon and the terminal ileum, branched on the middle or right colic vessels. It mirrors the characteristics of the preceding grafts since the size of the ileum matches well with that of the oesophagus, while its blood supply may be threatened by frequent anatomical variations.
When the left colic artery is occluded, an option is an anisoperistaltic transverse colon interposition with its blood supplied by the middle or the right colic artery. The diameter of the descending colon fits well with the cervical oesophagus for the proximal anastomosis. However, it has to be regarded as a salvage procedure because it exposes to pulmonary aspirations in the early postoperative course, and poor long-term functional results with disabling regurgitations.
The common first surgical step is to mobilise the entire colon from the cecum to the pelvic brim. The omentum is dissected off the transverse mesocolon (Photo 2, Video 1), the splenic (Photo 3, Video 2) and hepatic (Photo 4, Video 3) flexures are taken down, and the ascending colon (Video 4) is fully mobilised to the midline so that the whole colon from the sigmoid to the cecum is free on its mesentery until the aorta.
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Video 1 Division of the omentum. The head of the patient is on the right side of the screen.
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Video 2 Freeing of the splenic flexure. The head of the patient is on the left side of the screen. Marginal arcade of Drummond shown at the end of the video strip.
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Video 3 Freeing of the hepatic flexure. The head of the patient is on the left side of the screen.
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Video 4 Mobilisation of the right colon.
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Usually, identification of the pedicles and collateral arcades supplying the colon is feasible through the mesocolon using transillumination (Photo 5).

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Photo 5 Transillumination of the mesentery allowing the identification of the left colic vessels (*) and the marginal arcade of Drummond (#).
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The ascending branch of the left colic artery can be clearly identified when the mesentery is stretched in a cephalad direction by its tendency to form a natural pedicle ascending in the direction of the splenic flexure adjacent to the ligament of Treitz. Similarly, the arterial arcades can be seen when the mesentery is stretched transversely. Dissection of the right colic vessels and the middle colic vessels nearby the superior mesenteric vessels is the key point of the procedure. It could be difficult in obese patients with a fatty mesentery. In this situation, dissection of the right and middle colic arteries should be done as close as possible to their origin from the superior mesenteric vessels to identify and, if necessary, to preserve early branching vessels (Photos 6 and 7).
The base of the mesocolon is incised from this point to the left, as far as the inferior mesenteric vein. Once these main vascular pedicles are clearly identified, the mesentery is excised in between (Photo 8, Video 5).
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Video 5 Creation of the mesocolic windows. The marginal arcade of Drummond then the mid-colic artery is pointed out at the beginning of the strip.
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Clamping test and section of the colon
The preferred colon graft is an isoperistaltic conduit supplied by the left colic vessels. Adequacy of the blood supply from the left colic artery is tested before ligation and division with non-traumatic vascular bulldog clamps occluding temporarily the right and middle colic arteries as well as the colic arcade at both ends of the foreseen colonic graft, by palpating a pulse along the marginal vessels until its proximal end (Photo 9, Video 6).

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Photo 9 (A) Colic graft supplied by the left colic vessels (*); a bulldog clamp is occluding the marginal arcade at the level of the planned distal colic division. (B) Bulldog clamps are occluding the right colic vessels (1), the mid-colic artery (2): hidden by the left-hand of the surgeon), and the marginal arcade at the level of the planned proximal division (3).
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Video 6 Vascular clamping test.
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This procedure, especially in patients with atheroma, could detect thrombosis of the IMA. Similarly, venous outflow is tested by observing that the veins do not become overly distended, indicating venous congestion. After this clamping test, the optimal length of the colonic graft and therefore the limit for the colic section on the right colon are determined. A tape is placed along the colon from its antimesenteric border directly opposite the tethering artery to ensure the adequacy of the available graft and the measured distance to reach the level of the planned proximal anastomosis (Video 7).
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Video 7 Measurement of the planned colon interposition. The measurement of the coloplasty is based on the length of vascular arcades rather than on the length of the colon itself.
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The marginal artery and vein are ligated at the proximal end of the foreseen colon graft, whereas the arcade is preserved at its distal part where only the colon is transected without dividing the mesentery other than few centimetres along its mesenteric border (Video 8). This trick preserves additional arterial supply and venous drainage both to the colon graft and the colo-colic anastomosis. It may be useful to excise few centimetres of colon immediately, distal to the graft while preserving the marginal vessel and augmenting perfusion. Tethering of the pedicle by the descending branches of the left colic artery and descending colon is thereby eliminated [3]. The midcolic artery and vein are ligated proximal to their right and left branches for long grafts, whereas only the left branch is ligated for short grafts. Proximal ligation of the midcolic artery and vein preserving early branching (Photo 10), and sometimes of the right colic (Photo 11) and ileocolic arteries and veins (Video 9), is done for very long grafts (Photo 12) because of the poorly developed peripheral arcade between the right and left branches. The availability of the vasculature is checked at the proximal edge of the graft (Video 10).
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Video 8 Colic division. The right side of the colon is divided first. The marginal artery and vein are not divided on the left side.
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Video 9 Ligation of the right colic vessels.
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Video 10 Vessels beating at the proximal edge of the graft.
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Route of the colon interposition
The route for the graft depends mainly on whether or not an oesophagectomy (transthoracic or transhiatal) is required and performed during the same session. Transposition through the posterior mediastinum in the oesophageal bed is the shortest one and thereby offers the best functional results. It should be used predominantly. In that case, it is recommended to anchor the colon graft in as straight a line as possible to the diaphragm. This avoids redundancy and upper movement of the colon into the chest.
When the oesophageal bed is not available, there are three options. The intrapleural route offers many disadvantages. The inferior inlet requires an anterior or a lateralised phrenotomy, which may cause redundancy. The colon graft is either transposed anteriorly or posteriorly to the pulmonary hilum, which creates also favourable conditions for the development of angulations and subsequent swelling. Finally, when a proximal anastomosis to the neck is required, the superior inlet is demanding to create because of its narrowness and vascular connections.
A retrosternal transposition is preferred when the oesophageal bed is not available: when the oesophagus is left in place (bypass), or when the oesophagectomy has been performed during an earlier intervention. This route is also helpful when a macroscopically incomplete tumoral resection has been performed with a predictable early local recurrence, and/or when a high-dose mediastinal radiotherapy is required. Care should be paid to avoid the opening of both pleural spaces into which the pulled-up graft could possibly glide and develop a subsequent kinking. Its main difficulty is at the level of the upper thoracic inlet. It is necessary to obtain a large channel, usually measured with four crossing fingers behind the manubrium in order to prevent compression. Graft compression in this location could result in vascular impairment, of the veins more often than arteries, and ischaemia. Some authors proposed the resection of the left side of the manubrium with the head of the clavicle in order to enlarge the space [4], but with the associated risk of osteitis. If there is a very large left lateral segment of the liver, it may be necessary to remove it to prevent interference with the lie of the graft as it joins the stomach.
The subcutaneous route, in front of the sternum, is exceptionally used for obvious cosmetic reasons, but is still an alternative when no other route is available, especially when the retrosternal route is obliterated by the fibrous sequels of a previous sternotomy. However, the scarring associated with a previous midline skin incision may also preclude the creation of an adequate subcutaneous tunnel. A tight tunnel may easily impede venous drainage and threaten the viability of the graft. Tissue expanders have been used successfully to palliate this problem [5].
Whatever the route, the colonic graft is pulled-up cautiously and put snugly in a straight position (Video 11). Indeed, the food bolus travels mainly by gravity, making straightness of the conduit of paramount importance. The position of the nourishing pedicle should be checked continuously, and any kind of tension at its level is prohibited. As well, the surgeon should make sure that the position of the mesocolon avoids any twisting with its related vascular compromise.
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Video 11 Colon graft pull-up (retrosternal route).
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Proximal and distal anastomoses
The length of the transplant is evaluated and possibly trimmed away when there is an exceeding part of the graft. This manoeuvre helps to ensure the quality of the transplant vascularisation at the cutting edge. The proximal anastomosis in the neck uses a hand-sewn single-layer end-to-end technique with 3-0 absorb able sutures. The large calibre of the colon is well-suited when a pharyngo-colic anastomosis is required (Photo 13), but is not convenient for an oesocolic one. In that case, it could be done end-to-side at the non-mesenteric aspect of the colon, very close to the proximal closed edge of the graft (Photo 14).

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Photo 13 Hand-fashioned single-layer end-to-end pharyngo-colic anastomosis. The pharynx is labelled with *.
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As expected, the proximal anastomosis is congruent between the ileum and the proximal oesophagus in case of a right ileo-coloplasty. Running sutures are expeditive and safe (Video 12), but non-congruent calibres are preferably handled with interrupted stitches (Photo 15).
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Video 12 End-to-end pharyngo-colic anastomosis.
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Photo 15 Short colic interposition: intrathoracic end-to-end oeso-colic anastomosis with interrupted stitches. The oesophagus is labelled with *.
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Accordingly, the musculomucosal layer of the esophagus and the seromuscular layer of the colon are approximated to correct problems associated with discrepancy in lumen size (Video 13).
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Video 13 Proximal anastomosis between the cervical oesophagus and colon via left cervical incision.
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Circular stapling devices may be used. A pursestring suture is made before transecting the proximal oesophagus. The anvil is then inserted into the lumen of proximal oesophagus, and the pursestring suture is tied. The shaft of the device is introduced inside the colonic graft through its proximal edge and angled to puncture the trocar of the stapler through the non-mesenteric side of the colon. The shaft of the device and the anvil are then locked, and the adjusting knob is turned clockwise to prepare the anastomosis. After firing the instrument, the proximal colon is closed with a linear stapler to terminalise the anastomosis.
The distal anastomosis stays in the abdomen. The distal cutting of the graft is done nearby the supplying vessel in order to prevent the further constitution of a siphon at the level of the distal colovisceral anastomosis. The colon graft is joined to the stomach or the jejunum. Whenever possible, the anastomosis is best performed at the posterior part of the antrum for the reasons of pedicle positioning and reflux prevention (Photo 16, Video 14).
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Video 14 Distal colo-gastric anastomosis at the posterior aspect of the antrum.
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A gastric drainage procedure, i.e. a Mikulicz pyloromyotomy, is performed when the oesophagus and vagus nerves have been removed (Photo 17).
In case of an oesophagectomy and subtotal gastrectomy, the distal anastomosis is feasible at the antrum or at the duodenum. However, it is not recommended because of the related massive bile reflux into the colonic graft. A Roux-en-Y jejunal loop is preferable (Video 15).
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Video 15 Side-to-side colo-jejunal anastomosis in a patient in whom total gastrectomy was performed. Distal anastomosis between the coloplasty and the efferent loop of the Roux-en-Y jejunum construction.
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The length of this jejunal loop has to be sufficient (50 cm at least) in order to prevent bile reflux into the colon (Video 16).
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Video 16 End-to-side jejuno-jejunal anastomosis.
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Colonic continuity is re-established by bringing the remaining previously mobilised right ileo-colon over to the distal end of the divided colon graft and performing an end-to-end single-layer anastomosis with running 3-0 absorbable sutures (Photo 18). Special attention should be paid to the closure of the mesentery to avoid a further internal hernia by suturing the mesentery of the right colon to the mesentery of the descending colon. Appendectomy is routinely performed.
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Results, technical failures and complications
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The colon has a number of characteristics that make it an excellent option for oesophageal replacement. Advantages include long length, acid resistance, and typically excellent blood supply. However, coloplasty remains a demanding and time-consuming operation, especially for long-segment interposition. The added time is in part related to the need to mobilise the colon, and the fact that rather than the one anastomosis required with a gastric pull-up there are at least three required when using the colon.
Operative mortality still ranges from 5 to 10% [1, 4, 6, 7, 8, 9, 10, 11, 12, 13, 14], the most serious complications being leaks and conduit necrosis (Table 1). Survivors of colon graft necrosis are often left with a loss of intestinal continuity after total or partial removal of the conduit, and may require delayed complex procedures with composite transplants to re-establish a swallowing function (Photo 19).

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Photo 19 Composite graft reconstruction with a retrosternal gastric tube (*) and a free jejunal graft proximally anastomosed to the pharynx (#), and branched on the jugulo-carotidian vessels (vascular anastomoses hidden by the fatty mesentery), following colon graft necrosis after oeso-pharyngo-laryngectomy.
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On the other hand, some patients will develop insidious swallowing dysfunction with time [1, 4, 6, 8, 10, 11, 12, 13, 14, 15] that often can be attributed to a specific anatomical etiology such as intractable anastomotic narrowing, mainly at the level of the proximal anastomosis, and conduit redundancies (Table 2). Complex revisional operative techniques may be necessary [16] in as high as 10–20% of the patients to re-establish swallowing function and preserve the conduit, such as resection of the redundant portion of the colon graft with re-anastomosis of the colon end-to-end, stricturoplasty of the narrowed anastomosis, or segmental resection followed by a free jejunal graft or skin tube interposition (Photo 20).

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Photo 20 Segmental resection of a narrowed oeso-colic anastomosis followed by a free skin tube (#) based on the radial vessels (+) branched on the jugulo-carotidian vessels, interposed between the colon and the pharynx (*).
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References
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