0361803X/07/189130 American Roentgen Ray Society Li et al. Nonanastomotic Strictures After Colonic Interposition Gas t roi nt es t i nal I magi ng Cl i ni cal Obs er vat i ons Nonanastomotic Strictures After Colonic Interposition Diane X. Li 1 Marc S. Levine Stephen E. Rubesin Igor Laufer Li DX, Levine MS, Rubesin SE, Laufer I Keywords: colonic interposition, esophageal atresia, esophageal cancer, esophageal replacement surgery, gastrointestinal radiology, ischemia, swallowing disorders DOI:10.2214/AJR.06.1217 Received September 13, 2006; accepted after revision December 6, 2006. M. S. Levine and S. E. Rubesin are consultants for E-Z-EM. 1 All authors: Department of Radiology, Hospital of the University of Pennsylvania, 3400 Spruce St., Philadelphia, PA 19104. Address correspondence to M. S. Levine (marc.levine@uphs.upenn.edu). OBJECTIVE. The purpose of this study was to describe the clinical and radiographic find- ings in a series of patients with nonanastomotic strictures after colonic interposition. CONCLUSION. Nonanastomotic strictures usually appear on upper gastrointestinal tract ra- diography as relatively long segments of smooth, tapered narrowing involving the interposed colon, most likely resulting from chronic ischemia. Unlike strictures at the esophagocolic or cologastric anastomosis, these long nonanastomotic strictures generally have a poor response to endoscopic di- latation procedures and are more likely to necessitate surgical revision of the colonic interposition. olonic interposition is a form of esophageal replacement surgery performed for severe caustic stric- tures and other debilitating dis- eases affecting the esophagus, such as acha- lasia and esophageal atresia [15]. This procedure may also be performed on patients with malignant esophageal tumors in whom an esophagogastrectomy is not feasible because of previous gastric surgery. Although colonic interposition can have excellent long-term re- sults [2, 6], it is a major surgical procedure as- sociated with a substantial morbidity and mor- tality related to a variety of complications, including anastomotic leaks, wound infec- tions, aspiration pneumonia, and ischemic ne- crosis of the interposed colon [710]. Anasto- motic strictures are the most common late complication of colonic interposition, with a reported prevalence ranging from 17% to 59% [3, 4, 7, 1113]. These strictures are sometimes thought to occur as the sequela of healed anas- tomotic leaks with subsequent scarring [11]. Anastomotic strictures may cause severe dys- phagia, but they often respond to one or more endoscopic dilatation procedures without need for additional surgery [11, 13, 14]. Although anastomotic strictures are a well- recognized complication of colonic interposi- tion, we have encountered a number of patients who developed nonanastomotic strictures of the interposed colon. To our knowledge, this finding has been described only anecdotally in the radiology literature [11, 15]. We there- fore report a series of patients with nonanas- tomotic strictures after colonic interposition and present the clinical and radiographic find- ings in these patients. Materials and Methods A computerized search of the radiology depart- ments database at our university hospital revealed 16 patients with colonic interposition who under- went upper gastrointestinal tract radiography dur- ing an 8-year period from January 1998 to Decem- ber 2005. A subsequent review of the radiology reports showed that eight (50%) of these 16 patients developed nonanastomotic strictures in the inter- posed colon. Medical records were available for seven of the eight patients. These seven patients constituted our study group. The mean age of the seven patients was 47 years (range, 2379 years). Six patients were men and one was a woman. The seven patients in our study group underwent a total of 14 upper gastrointestinal radiographic ex- aminations during the study period; four patients had multiple studies (mean, 2.8 studies; range, 24 studies). When multiple studies were performed, the first study in which a nonanastomotic stricture was detected was designated as the index study. Three of the four patients with multiple radio- graphic studies had one or more follow-up exami- nations, and one patient had undergone a previous examination before the index study. The mean du- ration from surgery to the time of the index study was 8.5 years (range, 7 days28 years). Four of the 14 radiographic examinations were performed with a 250% weight/volume (w/v) barium suspension (E-Z-HD, E-Z-EM), two with a 100% w/v barium suspension (Solopaque, Lafayette Pharmaceutical), and eight with a water-soluble contrast agent (dia- trizoate meglumine and diatrizoate sodium [Gas- C D o w n l o a d e d
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Nonanastomotic Strictures After Colonic Interposition AJR:189, July 2007 31 troview, Mallinckrodt]) followed by barium if there was no evidence of a leak. All the studies were performed with digital flu- oroscopy equipment (Diagnost 76, Philips Medical Systems; or Sireskop SD, Siemens Medical Solu- tions) using a combination of spot images, rapid se- quence imaging, and video and DVD recordings. Swallowing function was evaluated initially with the patient in the upright frontal and lateral posi- tions; for subsequent evaluations of the interposed colon, proximal and distal anastomoses, and stom- ach, the patient underwent imaging in the upright and in various recumbent positions. The images from the index examinations were re- viewed retrospectively by consensus of two authors, both of whom are experienced gastrointestinal radi- ologists, to determine the morphologic features of these nonanastomotic strictures, including their length and width (accounting for magnification), contour (smooth vs irregular), and proximal and dis- tal margins (tapered vs abrupt). The strictures were also assessed for the presence of obstructive features, including proximal dilatation and delayed emptying. The anastomoses and interposed colon were evalu- ated for the presence of anastomotic leaks or fistulas, ulceration, spasm, thickened or effaced haustral folds, and other abnormalities. Finally, the studies and study reports were evaluated for the presence of gastrocolic reflux, aspiration, or other types of swal- lowing dysfunction. Medical, endoscopic, surgical, and pathologic records were reviewed to determine the indications for colonic interposition; type of colonic interposi- tion performed (including the portion of colon used for the conduit, the orientation of the interposed co- lon, and whether the interposed colon was clamped at surgery); nature and duration of symptoms after colonic interposition; subsequent treatment (in- cluding endoscopic dilatation procedures or addi- tional surgery); histopathologic findings (if a por- tion of the interposed colon was resected); and patient course. The mean duration of clinical fol- low-up from the time of the index examination was 1.2 years (range, 12 days5.2 years). When two or more radiographic examinations were performed, serial examinations were reviewed to determine the course of the strictures over time. Our institutional review board approved all as- pects of this retrospective study and did not re- quire informed consent from the patients included in our study. Results Indications and Technique for Colonic Interposition The indications for colonic interposition included esophageal carcinoma in four pa- tients, caustic injuries to the esophagus in two, and congenital esophageal stenosis sec- ondary to VATER (vertebral defects, imperfo- rate anus, tracheoesophageal fistula, and ra- dial and renal dysplasia) syndrome in one. Three of the four patients with esophageal carcinoma had recurrent tumor after an esophagogastrectomy and one had a new esophageal tumor. Both patients with caustic injuries had undergone previous surgery (failed colonic interposition in one and cervi- cal esophagostomy in the other) for treatment of intractable lye strictures. The left colon was used as the neoesoph- ageal conduit in three patients and the right colon in three. We were unable to determine which portion of the colon was used as the conduit in the remaining patient. The inter- posed colon had an isoperistaltic orientation in three patients, an antiperistaltic orientation in two, and an unknown orientation in two. The interposed colon was not clamped at sur- gery in any of the seven patients. Clinical Findings Four (57%) of the seven patients with co- lonic interposition had dysphagia as the major presenting symptom at the time of the index radiographic studies. Two patients had dys- phagia for solids only, and two had dysphagia for solids and liquids. The mean duration of dysphagia was 6.6 years (range, 3 days14 years). The remaining three patients (43%) with colonic interposition had clinical signs and symptoms (fever, leukocytosis, and in- creased wound drainage) of anastomotic leaks at the time of the index radiographic studies, which were performed much earlier in the postoperative course; the mean duration from colonic interposition to the index studies was only 3 months (range, 7 days8 months) for this group versus 16.7 years (range, 2 months28 years) for the group with dysph- agia. Subsequently, all three patients in the group with clinically suspected leaks also de- veloped dysphagia. Two patients (29%) had clinical signs of as- piration, and one (14%) had a wound infection. Radiographic Findings Index examinationThe mean length of the nonanastomotic strictures in the seven pa- tients with colonic interpositions was 8 cm (range, 3.514 cm), and the mean width was 0.9 cm (range, 0.31.8 cm). These strictures therefore were relatively long segments of narrowing involving the interposed colon (Figs. 13). The strictures had a smooth con- tour in six patients and an irregular contour in one. The proximal margins of the strictures were tapered in all seven patients, and the distal margins were tapered in six and abrupt in one. Haustral folds in the interposed colon were ef- faced in six patients and were thickened in one. The strictures caused partial obstruction in two patients, with proximal dilatation and delayed emptying of contrast material into the stomach in both. One of the patients with delayed emp- tying had a food impaction above the proximal end of the stricture. Two patients also had small sealed-off leaks from the esophagocolic anastomosis into the adjacent mediastinum. Three patients had tra- cheobronchial aspiration, and one had divertic- ulosis of the interposed colon. No patients had evidence of gastrocolic reflux at fluoroscopy. Serial examinationsIn two of the four patients with nonanastomotic strictures in the interposed colon who had multiple studies, we observed progressive shortening and nar- rowing of the strictures, which decreased in both length and width on follow-up examina- tions. One of these patients also had a sealed- off leak from the esophagocolic anastomosis that subsequently progressed to a colocutane- ous fistula on later examinations. In contrast, the third patient with multiple studies had a stricture that increased in length and width on follow-up examinations. The final patient with multiple studies had an earlier radio- graphic examination showing no evidence of a nonanastomotic stricture in the interposed colon 3 months before the index study re- vealed a stricture (Fig. 1B). Treatment Six (86%) of the seven patients with co- lonic interpositions underwent a total of 27 endoscopic dilatation procedures (mean num- ber of dilatations, 5; range, 111). Four pa- tients (57%) ultimately required surgical revi- sion of the colonic interposition (with resection of a portion of the interposed colon in three) because of intractable dysphagia. Pathologic examination of the resected speci- mens revealed extensive submucosal fibrosis in two patients and erosion of the mucosa with hemosiderin-laden macrophages in one. When surgery was repeated, the mean dura- tion from the time of the original colonic in- terposition to the time of the first surgical re- vision was 5.7 years (range, 4 days15 years). Discussion Anastomotic strictures are a well-known complication of colonic interposition second- ary to postsurgical scarring at the esophago- D o w n l o a d e d
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Li et al. 32 AJR:189, July 2007 colic or cologastric anastomosis [3, 4, 7, 1113]. These strictures usually appear as rel- atively short segments of narrowing that are confined to the region of the affected anasto- mosis [11, 12]. In contrast, the radiology lit- erature contains only anecdotal descriptions of nonanastomotic strictures developing after colonic interposition [11, 15]. Such strictures have manifested on barium studies as seg- mental or diffuse colonic narrowing and are postulated to be caused by ischemia of the surgically mobilized colon [11, 15]. In our study, however, seven (44%) of the 16 pa- tients with colonic interpositions who under- went postoperative upper gastrointestinal tract radiographic examinations had nonanas- tomotic strictures of the interposed colon. These nonanastomotic strictures after co- lonic interposition had characteristic findings on upper gastrointestinal radiographic stud- ies: The nonanastomotic strictures appeared as relatively long segments of narrowing in- volving the interposed colon (Figs. 13). The strictures almost always had smooth con- tours, tapered margins, and effaced haustral folds. The location, length, and appearance of nonanastomotic strictures after colonic inter- position therefore enable differentiation from anastomotic strictures on upper gastrointesti- nal radiography in almost all cases. All seven patients with nonanastomotic strictures after colonic interposition presented with dysphagia at the time of the index exami- nation (n = 4) or developed dysphagia after the index examination (n = 3). When dysphagia was present at the index examination, it usually occurred months to years after colonic interpo- sition, and the strictures responded poorly to treatment, frequently necessitating multiple endoscopic dilatation procedures or even sur- gical revision of the interposed colon. In con- trast, anastomotic strictures that develop after colonic interposition are often amenable to en- doscopic dilatation without the need for multi- ple dilatation procedures or repeat surgery [11, 13, 14]. The development of nonanastomotic strictures in the interposed colon therefore has important implications for the long-term man- agement of these patients. Although the cause of nonanastomotic strictures after colonic interposition is uncer- tain, the frequent effacement or obliteration of haustral folds and the relatively long length of the narrowed colonic segment in our pa- tients are characteristic of ischemic strictures involving the colon elsewhere [16]. In two cases, pathologic examination of the resected portion of the interposed colon revealed ex- tensive submucosal fibrosis. Although none of the patients in our series had radiographic A B Fig. 155-year-old man with nonanastomotic stricture after colonic interposition for esophageal carcinoma. A, Frontal spot image from single-contrast upper gastrointestinal tract examination shows long segment of narrowing (white arrows) involving proximal two thirds of interposed colon. Note relatively smooth contour and tapered margins (long black arrows) of stricture. Esophagocolic anastomosis (short black arrow) is located proximally in upper chest just above aortic arch. B, Frontal spot image from upper gastrointestinal tract examination with water-soluble contrast material 3 months before A shows relatively normal distention of proximal portion of interposed colon with effacement of haustral folds. Nodular indentations (white arrows) along left lateral wall of colon could be secondary to bowel wall edema or weak colonic contractions. Note esophagocolic anastomosis (black arrow) in upper chest below medial end of left clavicle. D o w n l o a d e d
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Nonanastomotic Strictures After Colonic Interposition AJR:189, July 2007 33 findings of acute colonic ischemia, other au- thors have described edema, spasm, ulcer- ation, and thumbprinting as radiographic signs of acute ischemia in the interposed co- lon and actual perforation as a sign of is- chemic necrosis of the interposed colon [11, 12]. The surgical literature also contains sev- eral reports of patients who developed dys- phagia as a result of long nonanastomotic strictures after colonic interposition [1719]. One patient had an acute hypotensive episode after surgery [17]; in another patient, a post- operative angiogram showed abnormal vas- cularization of the interposed colon [18]. We therefore believe these nonanastomotic stric- tures most likely develop as a result of chronic ischemia from inadequate perfusion of the surgically mobilized colon. Nonanastomotic strictures after colonic in- terposition could also result from postopera- tive leaks with associated scarring and fibrosis, but most leaks involve the esophagocolic or cologastric anastomosis, so developing stric- tures are usually located at or near these anas- tomoses [2, 7, 11, 13]. Although two of our pa- Fig. 227-year-old man with nonanastomotic stricture after colonic interposition for chronic lye stricture. Double-contrast upper gastrointestinal tract examination shows moderately long stricture (white arrows) in lower one third of interposed colon. Note smooth contour and tapered margins (black arrows) of stricture. Fig. 325-year-old man with nonanastomotic stricture after colonic interposition for VATER (vertebral defects, imperforate anus, tracheoesophageal fistula, and radial and renal dysplasia) syndrome with congenital esophageal stenosis. Single-contrast upper gastrointestinal tract examination shows 3.5-cm-long stricture (white arrows) in midportion of interposed colon. This tight stricture is causing partial obstruction with proximal colonic dilatation. Note smooth contour and tapered margins of stricture. Also note proximal esophagocolic anastomosis (black arrow) and Harrington rod in thoracic spine. tients did have small sealed-off anastomotic leaks, we doubt that these leaks were an impor- tant contributing factor because of the long length of the strictures in our patients and be- cause of the location of these stricturesthat is, at a discrete distance from the proximal and distal anastomoses. Reflux of acid from the stomach via the cologastric anastomosis could also account for the development of nonanas- tomotic strictures in the interposed colon, but such reflux was not observed at fluoroscopy in any of our patients. Furthermore, one would expect reflux-induced strictures in the inter- posed colon to be located distally at or near the cologastric anastomosis, whereas all of the strictures in our patients were located well above the distal anastomosis. Our investigation has the inherent limita- tions of a retrospective study. Selection bias may also have increased the prevalence of nonanastomotic strictures in our series be- cause many patients were referred to our in- stitution as a result of preexisting complica- tions from failed colonic interpositions. The limited duration of follow-up for several pa- tients also limits our ability to draw firm con- clusions in all cases. In summary, nonanastomotic strictures after colonic interposition have characteris- tic features on radiographic examinations of the upper gastrointestinal tract, appearing as relatively long segments of smooth, tapered narrowing involving the interposed colon that are separate from the proximal esoph- agocolic and distal cologastric anasto- moses. These strictures most likely develop as a result of chronic ischemia of the surgi- cally mobilized colon. Unlike strictures at the esophagocolic or cologastric anastomo- sis, nonanastomotic strictures after colonic interposition have a poor response to endo- scopic dilatation procedures and are more likely to necessitate surgical revision of the colonic interposition. References 1. Orringer MB, Kirsh MM, Sloan H. New trends in esophageal replacement for benign disease. Ann Thorac Surg 1977; 23:409416 2. Postlethwait RW. Colonic interposition for esophageal substitution. Surg Gynecol Obstet 1983; 156:377383 3. Kelly JP, Shackelford GD, Roper CL. Esophageal replacement with colon in children: functional re- sults and long-term growth. Ann Thorac Surg 1983; 36:634641 4. Ahmad SA, Sylvester KG, Hebra A, et al. Esoph- ageal replacement using the colon: is it a good choice? J Pediatr Surg 1996; 31:10261031 5. Hsu H, Wang C, Hsieh C, Huang M. Short-segment colon interposition for end-stage achalasia. Ann Thorac Surg 2003; 76:17061710 6. Mansour KA, Bryan FC, Carlson GW. Bowel in- terposition for esophageal replacement: twenty- five-year experience. Ann Thorac Surg 1997; D o w n l o a d e d
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