Abdom Imaging 28:624 – 630 (2003) DOI: 10.1007/s00261-002-0070-y

Abdominal Imaging © Springer-Verlag New York Inc. 2003

Afferent loop obstruction after gastric cancer surgery: helical CT findings H.-C. Kim,1 J. K. Han,1 K. W. Kim,1 Y. H. Kim,2 H.-K. Yang,3 S. H. Kim,1 H. J. Won,1 K. H. Lee,1 B. I. Choi1 1

Department of Radiology, Institute of Radiation Medicine, and Clinical Research Institute, Seoul National University Hospital, 28 Yongon-dong, Chongno-gu, Seoul, 110-744, Korea 2 Department of Radiology, Inje University Sanggyepaik Hospital, Seoul, Korea 3 Department of Surgery, Seoul National University College of Medicine, Seoul, Korea Received: 23 July 2002/Revision accepted: 11 September 2002

Abstract Background: We reviewed the computed tomographic (CT) findings of afferent loop obstruction and assessed the value of helical CT in determining the underlying cause. Methods: Helical CT scans of 18 patients (12 men and six women; age range ⫽ 35– 67, mean age ⫽ 50 years) with afferent loop obstruction were reviewed. All patients had gastric cancer. Ten patients had undergone radical subtotal gastrectomy with Billroth II gastrojejunostomy, and eight had undergone total gastrectomy with Roux-en-Y esophagojejunostomy. CT images were analyzed retrospectively, and the presumed cause of obstruction on CT was compared with surgical findings (n ⫽ 8) and clinical courses (n ⫽ 10). Results: Local recurrence (n ⫽ 15), peritoneal seeding (n ⫽ 1), internal hernia (n ⫽ 1), and adhesion (n ⫽ 1) were the presumed causes of obstruction on CT. In all eight patients who underwent a second operation, the cause of afferent loop obstruction was correctly suggested on CT (local recurrence in six patients and adhesion and internal hernia in one patient). In 10 patients who were not re-explored, the clinical findings or biopsy indicated recurrent tumor as suggested on CT. Conclusion: Recurrent tumors and other potential causes of afferent loop obstruction can be correctly predicted with CT in most cases. Key words: Stomach, neoplasms—Stomach, surgery— Bowel obstruction—Computed tomography. Afferent loop syndrome is an uncommon complication that occurs in 0.3% of patients after subtotal gastrectomy

Correspondence to: J. K. Han

and Billroth II gastrojejunostomy. Clinical findings are relatively nonspecific and include abdominal pain, nausea, vomiting, postprandial fullness, and, rarely, obstructive jaundice. Reported causes of the syndrome include internal hernia, kinking at the anastomosis, adhesions, stomal stenosis, and recurrent malignancy [1, 2]. Barium studies may suggest the diagnosis if there is nonfilling of the afferent loop secondary to mechanical obstruction or preferential filling of a dilated afferent loop [3]. Ultrasound and computed tomography (CT) are useful in establishing the diagnosis of afferent loop syndrome [4, 5]. The fluid-filled, dilated afferent portion of jejunum can be easily identified by both imaging modalities. However, most of the articles on the radiologic features of afferent loop obstruction were published decades ago [1–9], and only a small number of cases diagnosed with CT has been reported [5–14]. Moreover, the recent advance of medical and endoscopic therapies in patients with peptic ulcer disease has greatly diminished the need for anti-ulcer surgery [15], which could alter the cause of afferent loop obstruction. At our institution, more than 500 gastric cancer patients are surgically treated each year [16]. Helical CT play a crucial role in preoperative staging and evaluation of postoperative complications of these patients. We reviewed the helical CT features of afferent loop obstruction and assessed the value of CT in determining the cause.

Materials and methods A computerized search of the medical records at our institution showed 20 patients who had developed afferent loop obstruction after gastric surgery between July

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Fig. 1. Local tumor recurrence with afferent loop obstruction in a 50-year-old woman after subtotal gastrectomy and retrocolic gastrojejunostomy for treatment of gastric carcinoma. A CT shows the remnant stomach (S), an efferent loop (E), and the colon (C). B CT 14 mm caudal to the view shown in A shows wall thickening and stenosis of the afferent loop (arrow) indicating recurrent tumor. The afferent and efferent (E) loops are behind the colon (C) due to retrocolic gastrojejunostomy. C CT 56 mm caudal to the view shown in A shows a dilated afferent loop (A). D Barium study shows a markedly dilated afferent loop (A) and severe stenosis at the anastomosis (arrow). The second operation confirmed recurrent tumor at the anastomosis.

1997 and June 2001. In this group were 18 patients who had undergone contrast-enhanced abdominal helical CT. There were 12 men and six women (age range ⫽ 35– 67 years, mean age ⫽ 50 years). Ten patients had undergone radical subtotal gastrectomy with Billroth II gastrojejunostomy for advanced gastric cancer (n ⫽ 9) or early gastric cancer (n ⫽ 1). Eight had undergone total gastrectomy with Roux-en-Y esophagojejunostomy for advanced gastric cancer. Gastrojejunostomy and esophagojejunostomy were performed in an antecolic (n ⫽ 10) or retrocolic (n ⫽ 8) manner. None of our patients had received abdominal radiation therapy, but 13 patients had received adjuvant chemotherapy after surgery. The interval between initial gastric operation and presentation of afferent loop obstruction was 3–75 months

(mean ⫽ 20 months). Clinical manifestation included epigastric pain (n ⫽ 15), vomiting (n ⫽ 12), fever (n ⫽ 4), and jaundice (n ⫽ 4). One patient presented with a palpable abdominal mass that was shown to be a dilated afferent loop on CT. Patients were managed by second operation (n ⫽ 7), percutaneous tube enterostomy (n ⫽ 6), second operation after percutaneous tube enterostomy (n ⫽ 1), percutaneous transhepatic biliary drainage (n ⫽ 1), or conservative management (n ⫽ 3). In 10 patients, the recurrent tumor was diagnosed pathologically by a second operation (n ⫽ 6), endoscopic biopsy (n ⫽ 3), or cytology of ascites (n ⫽ 1). In six patients, the recurrent tumor was diagnosed by radiologic findings and clinical course [17, 18]. In the remaining two patients, there was mechanical obstruction but no evidence of tumor recurrence.

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Fig. 2. Local tumor recurrence with afferent loop obstruction in a 63-year-old woman after subtotal gastrectomy and antecolic gastrojejunostomy for treatment of gastric carcinoma. A CT shows local tumor recurrence involving the gastrojejunal anastomosis (arrows). The remnant stomach (S) and a dilated second portion of the duodenum (D) are

noted. B CT 21 mm caudal to the view shown in A shows a dilated afferent loop (A), a prominent distal common bile duct (arrow), and an air-filled efferent loop (E). The distal afferent loop is in front of the colon due to antecolic gastrojejunostomy. The second operation confirmed recurrent tumor at the anastomosis.

CT was performed with a Somatom Plus 4 scanner (Siemens Medical Systems, Erlangen, Germany) or a HiSpeed Advantage scanner (GE Medical Systems, Milwaukee, WI, USA). Four patients were asked to drink 200 –300 mL of 2.5% Gastrografin (Schering, Berlin, Germany) before CT scanning. Fourteen patients did not take oral contrast. Each patient received 120 mL of non-ionic contrast material (Ultravist 370 [iopromide]; Schering Korea, Seoul, Korea) through an 18-gauge catheter inserted into a forearm vein by using a Mark V dedicated CT injector (Medrad, Pittsburgh, PA, USA) at a rate of 3 mL/s. Spiral CT was done from the diaphragm to the lower pelvic cavity, with parameters of 7-mm collimation, a 1:1 table pitch, and 7-mm reconstruction intervals. The delay between contrast administration and scanning was 60 s. CT images were evaluated for the following: the presence of bowel wall thickening at the anastomosis site and in the afferent or efferent loop, length of involved bowel, maximal diameter of the afferent loop (measured from outer wall to outer wall), the presence of keyboard sign, ascites, peritoneal enhancement, lymph node enlargement, biliary and/or pancreatic duct dilation, and concurrent metastatic lesion involving other sites. Jejunal wall thickening was diagnosed if the bowel wall was at least 4 mm thick in an area where the bowel was adequately distended [19]. The keyboard sign consisted of small linear densities projecting from the wall into the fluid-filled bowel in the area of the transverse portion of the duodenum caused by the valvulae conniventes. The amount of ascites was defined as minimal if fluid was confined to the pelvic cavity or localized within the peritoneal cavity and had less than 2 cm of its maximal depth, marked if fluid overflowed into the peritoneal cavity from the pelvic cavity and had more than 6 cm of

its maximal depth, and moderate if fluid did not fit the other two definitions. Regional lymph nodes were considered metastatic if the short-axis diameter was larger than 10 mm [20]. Common bile duct dilation was diagnosed when its maximal diameter was larger than 8 mm [21]. Pancreatic duct dilation was diagnosed if the greatest internal duct diameter was larger than 5 mm in the head and 2 mm in the body and tail [22]. The presumed causes of afferent loop obstruction were classified as local recurrence, peritoneal seeding, adhesion, or internal hernia. Local recurrence was defined as a tumor in the surrounding tissues of the resected stomach or lymphadenopathy along the celiac axis [17]. Local recurrence was suspected as a cause when CT showed abrupt or gradual change of the lumenal caliber at the anastomotic site or an afferent loop with evident wall thickening. Huge lymphadenopathy around the celiac axis encasing the afferent loop was also categorized as local recurrence. Peritoneal seeding was suspected as a cause when ascites and peritoneal enhancement were present and bowel wall thickening around the level of the obstruction was absent. Internal hernia was diagnosed when crowding, stretching, and crossover of mesenteric vessels and the whirl sign [23] were seen on CT. When a point of transition from a dilated bowel to a normal-caliber loop without a mass or other apparent cause was identified, adhesions were presumed to be the cause of obstruction [24]. In eight patients who had undergone a second operation, surgical findings were compared with the presumed cause of obstruction on CT. In 10 patients who had conservative management, the cause of afferent loop obstruction was determined by endoscopic biopsy and clinical course.

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Fig. 3. Local tumor recurrence with afferent loop obstruction in a 35-year-old woman after total gastrectomy and antecolic esophagojejunostomy for treatment of gastric carcinoma. A CT shows a dilated distal afferent loop (A) and focal wall thickening at the anastomosis (solid arrow), suggesting local recurrence. Dilated intrahepatic bile (open

arrow) and pancreatic (arrowheads) ducts are noted. B CT 63 mm caudal to the view shown in A shows a markedly dilated afferent loop (A) and a distal common bile duct (arrow). The second operation confirmed the local, recurrent mass lesion.

Fig. 4. Local tumor recurrence with afferent loop obstruction in a 67-yearold man after subtotal gastrectomy and retrocolic gastrojejunostomy for treatment of gastric carcinoma. CT shows local tumor recurrence (long solid arrows) involving the third portion of the duodenum, which causes dilation of the proximal duodenal segment (afferent loop). Note the afferent loop (A), gallbladder (G), superior mesenteric artery (small solid arrow), the superior mesenteric vein (open arrow), and ascites.

Results Bowel wall thickening was evident in 14 patients (Figs. 1–3) and localized to the anastomosis in eight. In four patients, segmental wall thickening (7–20 cm long) from the afferent to the efferent loop was noted. In two patients, the distal duodenal wall (afferent loop) was thickened and the gastrojejunal anastomosis was normal (Fig. 4). Lymphadenopathy was present in four patients. In one patient, it was enough to cause bowel obstruction without tumors at other sites on CT (Fig. 5). The maximal diam-

eter of the afferent loop ranged from 36 to 82 mm. Ascites was present in 12 patients (minimal in nine, moderate in one, and marked in two), and peritoneal enhancement was evident in six of 12 patients. The presence of the keyboard sign (n ⫽ 15), common bile duct dilation (n ⫽ 9), pancreatic duct dilation (n ⫽ 2), and metastasis to the incision site (n ⫽ 1) were noted. The presumed causes of obstruction included local recurrence (n ⫽ 15), peritoneal seeding (n ⫽ 1), adhesion (n ⫽ 1), and internal hernia (n ⫽ 1; Fig. 6). Of eight patients who had a second operation, the presumed causes of afferent loop obstruction were local recurrence (n ⫽ 6), adhesion (n ⫽ 1), and internal hernia (n ⫽ 1), which were confirmed at surgery. Local recurrence and peritoneal seeding were demonstrated on CT in two patients and the second operation confirmed the CT diagnosis. In 10 patients who were not reoperated, the presumed causes of afferent loop obstruction were local recurrence (n ⫽ 9) and peritoneal seeding (n ⫽ 1). Three patients had local recurrence and peritoneal seeding on CT, and local recurrence was supposed to have caused the obstruction in these patients. The recurrent tumor was diagnosed by endoscopic biopsy (n ⫽ 3) and clinical criteria (n ⫽ 6), and peritoneal seeding was confirmed by positive a result for cytology of ascites (n ⫽ 1). Therefore, in all 10 patients who did not have a second operation, the causes were associated with malignancy, as suggested on CT.

Discussion Acute afferent loop syndrome usually develops within the first week after surgery and results from complete

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Fig. 5. Lymphadenopathy with afferent loop obstruction in a 39-yearold man after total gastrectomy and antecolic esophagojejunostomy for treatment of gastric carcinoma. A CT shows conglomerated lymphadenopathy (L) abutting the superior mesenteric artery. The dilated proximal afferent loop (A) and common bile duct (arrow) are noted. This

lymphadenopathy had been detected 10 months before and kept growing. B CT 77 mm caudal to the view shown in A shows the dilated transverse portion of the afferent loop (A) with effacement of valvulae conniventes.

Fig. 6. Internal hernia with afferent loop obstruction in a 64-year-old man after total gastrectomy and antecolic esophagojejunostomy for treatment of gastric carcinoma. A CT shows a dilated afferent loop (A) with the keyboard sign. Crowded vessels and mesentery (arrow) are arranged vertically. B CT 14 mm caudal to the view shown in A shows

horizontally arranged vessels (thin arrow) and a whirl sign (open arrow) suggesting internal hernia. A second operation confirmed transmesenteric internal hernia and twisting mesentery with no evidence of recurrent tumor.

obstruction of the afferent limb secondary to a kink, herniation, or volvulus. Improved surgical techniques incorporating a short afferent loop and closure of the retroanastomotic space have markedly reduced the incidence of this form [2]. The classic presentation of chronic afferent loop syndrome has been described as bilious vomiting with relief of the abdominal pain [1]. This is due to chronic partial obstruction of the afferent loop and the intermittent release of its content into the stomach. In the chronic form, anastomotic stricture, adhesion, and stomal ulceration may be responsible [1]. Recurrent tumor had been reported to be an uncommon cause of afferent loop obstruction [1–3].

The improvement in medical therapy for peptic ulcer disease has greatly lessened the need for elective gastric surgery in benign disease. However, gastric cancer is common in Korea and the developing countries [16]. Therefore, most gastrectomies are done in patients with gastric malignancy as evident from the high incidence of afferent loop obstruction in our series compared with previous reports [1–3]. Recurrence at the gastric stump or anastomosis is seen as an area of localized bowel wall thickening on CT [17]. In our series, 14 patients had bowel wall thickening at or near the anastomosis, and local recurrence was the main cause of afferent loop obstruction. Although the detection

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of thickened bowel walls is an important sign of recurrent tumor, the potential source of erroneous interpretation may be inadequately distended bowel loops, surgical plication, bowel adhesion, and thickened fold secondary to hypertrophic gastritis [17]. Peritoneal seeding usually causes multiple sites of incomplete obstruction combined with a motility disorder, probably resulting from obstruction of venous and lymphatic channels in the mesentery [25]. Therefore, we suspected local recurrence as the main cause of obstruction in five patients who had typical findings of local recurrence and peritoneal seeding on CT, which was confirmed at surgery in two patients. Sonography and CT may demonstrate the keyboard sign emanating from the valvulae conniventes. The most convincing feature may be seen in the transverse portion of the duodenum. In our series, 15 patients had the keyboard sign, which led us to diagnose afferent loop obstruction at a glance. When the keyboard sign is absent due to effacement of the valvulae conniventes, a Ushaped fluid-filled tubular structure crossing the midline between the abdominal aorta and the superior mesenteric artery is a characteristic CT feature of a dilated afferent loop. Obstruction of the afferent loop with continuous accumulation of biliary, pancreatic, and intestinal secretions can result in marked distention of its lumen, dilatation of the bile ducts and the gallbladder, and acute pancreatitis. In our series, four patients had obstructive jaundice or cholangitis and three had elevated serum amylase. These symptoms can be managed with percutaneous tube enterostomy or percutaneous biliary drainage. Conservative therapy is often elected in patients with advanced carcinoma who would be poor candidates for a second surgery because of their debilitating state, associated peritoneal adhesion, or disseminated tumor. It is the role of radiologists to differentiate benign, curable causes such as adhesion or internal hernia from recurrent malignancy. Surgical treatment is strongly recommended in benign afferent loop obstruction, whereas more conservative or interventional management might be more suitable for malignant afferent loop obstruction. The inherent limitation of this study was the lack of pathologic correlation in many cases. Surgical proof of the exact cause of afferent loop obstruction could not be obtained in 10 patients because percutaneous tube enterostomy or conservative management negated the need for surgery. Further, because metastatic carcinoma usually preserves the mucosa, the positive yield from endoscopic biopsy is low [18]. Cancer history, clinical presentation, CT findings, and clinical course, however, strengthened the presumed cause of afferent loop obstruction. Another limitation is the selection of patients. All cases were selected from the medical records made by

clinicians. Therefore, clinicians might have diagnosed patients whose afferent loop obstruction was recognized on CT. Moreover, all patients who had undergone gastrectomy did not have postoperative CT. Therefore, the actual incidence of afferent loop syndrome or the diagnostic accuracy of CT in its detection could not be ascertained. Acknowledgment. This study was supported in part by 2001 BK21 Project for Medicine, Dentistry, and Pharmacy.

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