Effects of Inferior Mesenteric Vein Flow in Patients With Cirrhosis
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1 CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2013;11: Effects of Inferior Mesenteric Vein Flow in Patients With Cirrhosis HITOSHI MARUYAMA, HIDEHIRO KAMEZAKI, TAKAYUKI KONDO, TADASHI SEKIMOTO, TARO SHIMADA, MASANORI TAKAHASHI, HIDEHIRO OKUGAWA, and OSAMU YOKOSUKA Department of Gastroenterology and Hepatology, Chiba University Graduate School of Medicine, Inohana, Chuou-ku, Chiba, Japan BACKGROUND & AIMS: METHODS: RESULTS: CONCLUSIONS: The inferior mesenteric vein (IMV) is detected in more than 90% of computed tomography images. Little is known about the hemodynamic features of IMV as a collateral vessel in portal hypertension, or its effects in clinical presentation and outcome. We investigated the roles of the IMV in portal hemodynamics, clinical presentation, and outcomes of patients with cirrhosis. We performed a prospective study of 467 patients with cirrhosis (274 men; age, y). We assessed hemodynamics in the IMV using Doppler sonography and compared these data with patients clinical presentation and patient outcome. IMV was detected in 94 patients (20.1%); 51 patients had hepatopetal flow, 33 patients had hepatofugal flow, and 10 patients had to-and-fro flow. Those with hepatofugal flow had a significantly greater number of ascites than those with hepatopetal flow, higher Child classification (P [.004), and a higher incidence of decompensated liver (51.5% vs 27.5%; P [.015) and rectal varices (56.3% vs 13.3%; P [.013). The incidence of gastroesophageal varices was lower among those with hepatofugal flow (51.5%; P [.005) or to-and-fro flow (40%; P [.008) than those with hepatopetal flow (80.4%). IMV had similar effects after adjustment for liver function. There were no differences in the cumulative rates of survival during the median 17.2 months of follow-up evaluation, when the patients with and without IMV were stratified by Child classification. In patients with cirrhosis, hepatofugal flow of the IMV appears to increase the risk of ascites and liver decompensation but reduce the risk for gastroesophageal varices. Although IMV is associated with reduced liver function, it does not affect survival. Keywords: Hepatic Encephalopathy; Prognostic Factor; Marker; Imaging. Portal hypertension is characterized by a combination of increased outflow resistance in the liver and increased portal inflow from the splenic and splanchnic circulation. The development of portal-collateral pathways is one of the hemodynamic features of portal hypertension. Collateral circulation develops along with increased portal pressure, and the hepatic venous pressure gradient threshold for the development of portosystemic collaterals and esophageal varices may be as low as 10 mm Hg. 1,2 The severity of portal hypertension may affect the liver function reserve and the prognosis of cirrhosis patients. 3,4 The inferior mesenteric vein (IMV) is the vessel that carries blood derived from the embryologic hindgut, which extends from the distal transverse colon to the proximal rectum. 5 It originates anterior to the sacrum and runs toward the upper abdomen, passing posterior to the distal duodenum and anterior to the left renal vein and the superior mesenteric artery before communicating with the portal system. The main drainage route of the IMV is the splenic vein, followed by the superior mesenteric vein or the splenomesenteric confluence. The IMV also has been a target of surgical treatment for portal decompression. 6 Previous studies have reported that the IMV is a common vessel that is detected in more than 90% of computed tomography images. 7,8 The incidence and diameter of the IMV were similar between the control and cirrhosis groups. 9 However, reversed flow in the IMV is considered rare, 10 and little is known about the hemodynamic features of IMV as a collateral vessel involved with portal hypertension. Furthermore, the vessel s influence on clinical presentations and long-term outcomes has not been fully discussed. The purpose of this study was to investigate the significance of IMV to portal hemodynamics, clinical presentations, and prognosis in cirrhosis patients. Patients and Methods Study Design This prospective study was performed between April 2007 and March 2012, and it was approved by the ethical committee at our hospital. Informed written consent was obtained from all subjects. Consecutive patients in our Gastroenterology Department who met the following conditions were Abbreviations used in this paper: IMV, inferior mesenteric vein; MELD, model for end-stage liver disease by the AGA Institute /$
2 December 2013 INFERIOR MESENTERIC VEIN IN CIRRHOSIS 1649 potential candidates for the study: (1) cirrhosis patients with signs of portal hypertension, such as gastroesophageal varices diagnosed via routine endoscopy or bleeding/bleeding history, ascites detected via routine ultrasonography, and overt hepatic encephalopathy; and (2) patients who received Doppler ultrasonography for a detailed evaluation of portal hemodynamics. This examination was conducted for patients with compensated cirrhosis, such as those with varices without bleeding history and decompensated cirrhosis. The study also had the following exclusion criteria: (1) patients with hepatocellular carcinoma that was not controllable with nonsurgical treatment; (2) patients with a history of abdominal surgery; (3) patients who underwent partial splenic embolism or splenectomy; (4) patients who received antiviral treatment during the follow-up period; and (5) patients who received vasoactive medication, such as a b-blockers. Cirrhosis was diagnosed based on both biochemical findings and 2 different imaging findings (ultrasound and computed tomography/magnetic resonance imaging). A portal vein thrombus was defined as an echogenic area in the portal trunk, a main intrahepatic branch of the portal vein, the splenic vein, or the superior mesenteric vein detected with ultrasonography. Hepatic encephalopathy was graded according to the West Haven criteria, 11 and grades of II or higher were categorized as overt hepatic encephalopathy. Decompensated cirrhosis was defined by the detection of at least one of the following presentations: variceal bleeding, uncontrolled ascites, overt hepatic encephalopathy, spontaneous bacterial peritonitis, or jaundice (total bilirubin level, >3.0 mg/dl). The grade of ascites was defined according to the clinical and ultrasound findings: mild (þ) for ascites only detectable by ultrasound examination and moderate to severe (þþ) for ascites causing abdominal distension. Ultrasound An SSA-770A or 790A ultrasound system (Toshiba, Tokyo, Japan) with a 3.75-MHz convex probe was used in this study. All examinations were performed with the patient in the supine position after fasting for 4 hours or longer. The portal trunk was detected with a longitudinal or oblique scan of the upper abdomen. The IMV was detected on a long-axis view with the oblique scan slightly toward the left lower quadrant in the upper to middle abdomen. 5 The diameter of, and blood flow in, the portal trunk and the IMV were measured with the sampling width corresponding to the diameter of the vessel and at an angle less than 60 between the ultrasound beam and the vessel. The average value of measurements taken 2 or more times was calculated and used for analysis. All of the ultrasound examinations were performed by H.M. or M.T., each of whom had more than 8 years of experience. Endoscopy Routine or screening endoscopy was performed using GIF Q240 or Q260 endoscopes for upper gastrointestinal endoscopy and CF-H260AI or PCF-Q260AI endoscopes for colonoscopy (Olympus, Tokyo, Japan). We followed the Japan Research Society for Portal Hypertension s General Rules for Recording Endoscopic Findings for grading the endoscopic findings of gastroesophageal or rectal varices, as follows: F1 (small), F2 (medium), and F3 (large). 12 All endoscopic procedures were performed by H.M., H.O., M.T., T.S., T.S., or T.K. The study used endoscopic data that were obtained within 6 months before/after Doppler examination. Statistical Analysis All of the data were expressed as medians or means with the SD or as percentages. Continuous variables were compared using the Student t test, the Mann Whitney U test, or the Fisher protected least-significant-difference test. Categoric variables were compared using the chi-squared test. The patients survival times were based on the date of death, liver transplantation, or the final date during the study period on which the patient was confirmed to be alive. The Kaplan Meier method was used to calculate survival probabilities, and the difference was compared with the log-rank test. The primary comparison of the study was a comparison of patients with and without a detected IMV, and the secondary comparison was among 3 groups according to the flow direction in the IMV on Doppler sonogram (hepatopetal, to and fro, and hepatofugal) among patients with a detectable IMV. Statistical significance was defined as a P value of less than.05; however, the Bonferroni correction was used for multiple comparisons (3 groups), and a P value of less than.0166 was considered significant. Statistical analyses were performed using the SPSS software package (version 17.0; SPSS, Inc, Chicago, IL). Results Patients and Portal Hemodynamics The study consisted of 467 cirrhotic patients (Figure 1, Table 1). The IMV was detected in 20.1% (94 of 467) of the patients and had a mean diameter of mm (range, ). The flow direction was hepatopetal in 51 patients, hepatofugal in 33 patients, and to and fro in 10 patients. The IMVs with a hepatofugal flow direction had a mean diameter of mm (median, 6.6 mm; range, ), a flow velocity of cm/s (median, 10.9 cm/s; range, ), and a flow volume of ml/min (median, 230 ml/min; range, ). There was no difference in the diameter, velocity, and flow volume in the portal vein of patients with and without IMV. Reversed flow direction in the portal trunk was detected in 3 patients who had IMVs with a hepatofugal flow direction (hepatofugal IMV) and a flow volume higher than the median value of 230 ml/min. In addition, the diameter and flow volume in the portal trunk were lower in patients with a hepatofugal IMV greater than 230 ml/min (mean SD, mm; ml/min) than those with a hepatofugal IMV of 230 ml/min or less (mean SD, mm, P ¼.006; mean SD, ml/min, P ¼.02). The median follow-up period for all of the subjects was 17.2 months. Clinical Presentations There were significant differences in the clinical presentations depending on the flow direction in the IMV (Table 2). The patients with hepatofugal IMV showed more severe ascites (P ¼.006), a more severe Child classification (P ¼.004), a higher incidence of decompensated condition of the liver (17 of 33,
3 1650 MARUYAMA ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No. 12 Figure 1. Diagram for patient enrollment. According to the inclusion and exclusion criteria, there were 467 subjects in this study. 51.5%; vs 14 of 51, 27.5%; P ¼.015), and more frequent rectal varices (9 of 16, 56.3% vs 2 of 15, 13.3%; P ¼.013) compared with patients with IMVs with a hepatopetal flow direction (hepatopetal IMV). None of the patients presented with bleeding from rectal varices (median follow-up period, 17.5 mo). The incidence of gastroesophageal varices was lower in patients with hepatofugal IMV (17 of 33, 51.5%; P ¼.005) or to and fro IMV (4 of 10, 40%; P ¼.008) than in those with hepatopetal IMV (41 of 51, 80.4%). The clinical presentations were compared after the adjustment of liver function severity based on the model for end-stage liver disease (MELD) score (Table 3). The incidence of rectal varices was higher and the grade of ascites was worse in patients with hepatofugal/to-and-fro IMV than in those with hepatopetal IMV among the patients with a MELD score less than 10, or greater than 10 and less than 20. The incidence of gastroesophageal varices was lower in patients with hepatofugal IMV than in those with hepatofugal/to-and-fro IMV among the patients with a MELD score less than 10, or greater than 10 and less than 20. Overt hepatic encephalopathy was more frequent among patients with hepatofugal IMV greater than 230 ml/min (4 of 17; 23.5%) than those with hepatofugal IMV of 230 ml/min or less (0 of 16; P ¼.04; Table 4). The 4 patients with hepatofugal IMV greater than 230 ml/min developed overt hepatic encephalopathy despite taking oral medications that consisted of both nonabsorbable disaccharides and kanamycin monosulfate during the median observation period of 15.2 months (mean SD; ; range, 5 days to 60.4 mo). Neither the incidence of portal vein thrombosis nor bleeding/ treatment history of varices showed a significant relationship between the presence and absence of IMV or its flow direction (Tables 1 and 2). Prognosis Cumulative survival rates were compared in terms of the presence of IMV by stratifying the cohorts according to their Child classification (A, B, and C) because of the differences in the liver function reserve at baseline (Table 2). There were no significant differences in the cumulative survival rates of patients with hepatopetal IMV and hepatofugal/to-and-fro IMV in the cohorts classified as Child A (72.8% at 1 y, 59.1% at 3 y, and 59.1% at 5 y in patients with hepatopetal IMV; 83.3% at 1 y, 55.6% at 3 y, and 55.6% at 5 y in patients with hepatofugal/toand-fro IMV; P ¼.73), Child B (67.4% at 1 y and 19.6% at 3 y in patients with hepatopetal IMV; 65.23% at 1 y and 46.7% at 3 y in patients with hepatofugal/to-and-fro IMV; P ¼.62), or Child C (19.4% at 1 y in patients with hepatopetal IMV; 80% at 1 y in patients with hepatofugal/to-and-fro IMV; P ¼.34). There was also no significant difference in the ratio for concomitant hepatocellular carcinoma between the 2 groups (P ¼.51). Discussion We report the clinical significance of the IMV in patients with cirrhosis. As previously reported, the IMV may be a common vessel that is similar in healthy subjects and patients with cirrhosis because it reflects normal embryologic and anatomic development. 7 9 However, our study focused on the IMV as a collateral route in portal hypertension. The incidence of IMV based on Doppler sonography was 20.1% in cirrhosis showing various flow directions, and the mean diameter of the IMVs with a hepatofugal flow direction was 7.7 mm. One study reported that the IMV diameter was less than 6 mm on computed tomography images in normal subjects. Considering the presence of a hyperdynamic state in cirrhosis, the mean diameter of IMV in our study may be reasonable. 13 Meanwhile, the incidence of IMV may be much lower than that in previous reports. 7,8 The
4 December 2013 INFERIOR MESENTERIC VEIN IN CIRRHOSIS 1651 Table 1. Baseline Characteristics of the Patients IMV Absence Presence P value N Age, y Sex, male/female 219/154 55/39.97 Etiology C/A/NBNC/PBC/B/AIH/NASH/PSC/C 167/63/48/28/27/16/ 47/27/8/4/6/1/1/.26 þa/bþc/bþa/aihþa/pbcþaih 13/3/2/2/2/1/1 0/0/0/0/0/0 Platelet count, 10 4 /mm Child class, A/B/C 130/166/77 35/42/17.83 Child Pugh score Total bilirubin level, mg/dl Albumin level, g/dl Prothrombin time, % NH3, mg/ml NH3 in patients with Tx NH3 in patients without Tx MELD score Varices Gastroesophageal, -/þ 81/292 30/ Rectal, -/þ 101/27 22/12.09 Bleeding history from varices Prior treatment for varices Portal vein Diameter, mm Velocity, cm/s Volume, ml/min Portal vein thrombosis Spleen size, mm Ascites, -/þ/þþ 242/72/59 31/35/28 <.0001 HE, -/þ 348/25 85/9.34 Hepatic venous pressure gradient, mm H 2 O HE in patients with Tx, -/þ 103/16 8/9.35 Hepatocellular carcinoma, -/þ 238/135 60/34.99 Decompensated cirrhosis, -/þ 281/92 51/43 <.0001 NOTE. A comparison was made between patients with and without detected inferior mesenteric vein. -, absence; þ, presence. Grade of ascites: þ, ascites only detectable by ultrasound examination; þþ, ascites causing abdominal distension. A, alcohol; AIH, autoimmune hepatitis; B, hepatitis B virus; C, hepatitis C virus; HE, hepatic encephalopathy by West Haven criteria (overt hepatic encephalopathy for grade II or more); NASH, nonalcoholic steatohepatitis; NBNC, non-b non-c; PBC, primary biliary cirrhosis; PSC, primary sclerosing cholangitis; Tx, oral medication with nonabsorbable disaccharides and/or kanamycin monosulfate. presence of ascites and/or intestinal bloating caused by cirrhosis in some of the patients might have affected the detection of the vessel and flow signals by ultrasound. Nonetheless, there is a possibility of a false-negative result for IMV detection. Considering the recent improvement of detectability of color signals by ultrasonography, however, the influence of IMV on portal hemodynamics might be weak in patients without detection of IMV in our study. Collateral vessel formation may be linked closely to clinical presentation. First, our study examined the incidence and types of varices as IMV-related presentations. As expected, rectal varices were seen significantly more often in more than onethird of the patients with IMV and more than half of the patients with hepatofugal IMV. Next, the effect of IMV on the development of gastroesophageal varices was evaluated. A previous study based on a radionuclide examination via the rectum reported that an IMV-related portosystemic shunt did not prevent the formation of large varices and that the magnitude of blood flow through peripheral collaterals might reflect the risk of a variceal hemorrhage. 14 The results may be inconsistent with our data, which showed a significantly lower incidence of gastroesophageal varices in patients with IMV than in those without. The discrepancy may be explained by the different methods used; the data based on radionuclide behavior might have been influenced by the systemic circulation, whereas our study was based on the direct measurement of IMV. According to our data, because hemodynamics in the portal trunk are influenced by the hepatofugal flow in the IMV, the presence of IMV may offer some effects that suppress the development of gastroesophageal varices. Hepatic encephalopathy is a significant complication of chronic liver dysfunction and is related closely to the serum ammonia level. The key sources of circulating ammonia depend on the metabolism in the intestine, kidney, and striated muscle. 15 In particularly, urease-containing gut flora, such as Klebsiella and Proteus species in the intestine, are important sources of ammonia, and the blood in the mesenteric vein is rich in ammonia. Nevertheless, our study found no difference in the
5 1652 MARUYAMA ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No. 12 Table 2. Comparison of Baseline Characteristics in Patients With IMV IMV Hepatopetal To and fro Hepatofugal N Age, y Sex, male/female 30/21 4/6 21/12.84 Platelet count, 10 4 /mm Child, A/B/C 27/19/5 a 2/5/3 b 6/18/9 c.011 Child Pugh score MELD score Varices Gastroesophageal, -/þ 10/41 d 6/4 e 16/17 f.045 Rectal, -/þ 13/2 g 2/1 h 7/9 i.044 Bleeding history from varices Prior treatment for varices Portal vein Diameter, mm Velocity, cm/s Volume, ml/min Portal vein thrombosis Spleen size, mm Ascites, -/þ/þþ 33/13/5 j 5/4/1 k 10/14/9 l.03 HE, -/þ 46/5 10/0 29/4.52 Hepatic venous pressure gradient, mm H 2 O HE in patients with Tx, -/þ 20/5 7/0 11/4.33 Hepatocellular carcinoma, -/þ 30/21 7/3 23/10.55 Decompensated cirrhosis, -/þ 37/14 o 8/2 m 16/17 n.03 NOTE. A comparison was made among 3 groups according to the flow direction in the inferior mesenteric vein on Doppler sonogram (hepatopetal, to and fro, and hepatofugal) among patients with a detectable inferior mesenteric vein. -, absence; þ, presence. Grade of ascites: þ, ascites only detectable by ultrasound examination; þþ, ascites causing abdominal distension. Child: a vs b, P ¼.09; a vs c, P ¼.004; b vs c, P ¼.97. Gastroesophageal varices: d vs e, P ¼.008; d vs f, P ¼.005; e vs f, P ¼.52. Rectal varices: g vs h, P ¼.4; g vs i, P ¼.013; h vs i, P ¼.47. Ascites: j vs k, P ¼.63; j vs l, P ¼.006; k vs l, P ¼.4. Decompensated cirrhosis: o vs m, P ¼.71; o vs n, P ¼.015; m vs n, P ¼.79. A, alcohol; AIH, autoimmune hepatitis; B, hepatitis B virus; C, hepatitis C virus; HE, hepatic encephalopathy by West Haven criteria (overt hepatic encephalopathy for grade II or more); NASH, nonalcoholic steatohepatitis; NBNC, non-b non-c; PBC, primary biliary cirrhosis; PSC, primary sclerosing cholangitis; Tx, oral medication with nonabsorbable disaccharides and/or kanamycin monosulfate. P value Table 3. Comparison of Clinical Presentations Based on the Adjustment of Liver Function (MELD Score) MELD clinical presentation Hepatopetal (n ¼ 51) To and fro (n ¼ 10) Hepatofugal (n ¼ 33) P value 10 (n ¼ 31) Gastroesophageal varices, -/þ 1/16 a 1/1 b 6/6 c.02 Rectal varices, -/þ 6/0 d 1/0 e 2/4 f.034 Ascites, -/þ/þþ 15/2/0 g 0/2/0 h 2/6/4 i.0004 Hepatic encephalopathy, -/þ 17/0 2/0 12/0 - >10 to 20 (n ¼ 47) Gastroesophageal varices, -/þ 6/20 j 4/1 k 10/6 l.009 Rectal varices, -/þ 6/1 m 0/1 n 1/5 o.027 Ascites, -/þ/þþ 18/7/1 p 0/1/4 q 4/6/6 r.0006 Hepatic encephalopathy, -/þ 25/1 5/0 15/1.82 >20 (n ¼ 16) Gastroesophageal varices, -/þ 3/5 1/2 0/5.29 Rectal varices, -/þ 1/1 1/0 4/0.23 Ascites, -/þ/þþ 6/1/1 s 0/1/2 t 0/1/4 u.038 Hepatic encephalopathy, -/þ 4/4 3/0 2/3.22 NOTE. A comparison was made among 3 groups according to the flow direction in the inferior mesenteric vein on Doppler sonogram (hepatopetal, to and fro, and hepatofugal) among patients with a detectable inferior mesenteric vein. -, absence; þ, presence. Grade of ascites: þ, ascites only detectable by ultrasound examination; þþ, ascites causing abdominal distension. Gastroesophageal varices: a vs b, P ¼.055; a vs c, P ¼.006; b vs c, P ¼ NS; j vs k, P ¼.013; j vs l, P ¼.011; k vs l, P ¼.47. Rectal varices: d vs e, P ¼ NS; d vs f, P ¼.014; e vs f, P ¼.21; m vs n, P ¼.06; m vs o, P ¼.013; n vs o, P ¼.66. Ascites: g vs h, P ¼ NS; g vs i, P ¼.0004; h vs i, P ¼.42; p vs q, P <.0001; p vs r, P ¼.0045; q vs r, P ¼.22; s vs t, P ¼.08; s vs u, P ¼.023; t vs u, P ¼ NS.
6 December 2013 INFERIOR MESENTERIC VEIN IN CIRRHOSIS 1653 Table 4. Comparison of Clinical Data in Patients With IMV Showing Hepatofugal Flow Direction IMV 230 ml/min a >230 ml/min a P value N Age, y Sex, male/female 10/6 9/8.58 Platelet count, 10 4 /mm Child score Total bilirubin, mg/dl Albumin, g/dl Prothrombin time, % NH3, mg/dl MELD score Varices Gastroesophageal, -/þ 6/10 11/6.12 Rectal, b -/þ 5/3 2/5.19 Spleen size, mm Portal trunk F/to-and-fro/R 15/1/0 13/1/3.21 Diameter, mm Velocity, cm/s Volume, ml/min Ascites, -/þ/þþ 2/14 7/10.06 HE, 0 I/IIwV 16/0 13/4.04 NOTE. Grade of ascites: þ, ascites only detectable by ultrasound examination; þþ, ascites causing abdominal distension. F, forward; HE, hepatic encephalopathy by West Haven criteria (overt hepatic encephalopathy for grade II or more); MELD, model for end-stage liver disease; R, reverse. a A rate of 230 ml/min is the median flow volume in the IMV with hepatofugal flow direction. b Rectal varices were evaluated in patients who received a colonoscopy within 6 months before/after Doppler study. risk of developing overt hepatic encephalopathy with respect to the presence/absence of IMV. However, overt hepatic encephalopathy was significantly more common in patients with advanced IMV (flow volume >230 ml/min) than in other patients, probably because of the carrier effect of blood flow with a high level of ammonia entering into the systemic circulation without passing though the liver. All 4 of these patients suffered from treatment-resistive presentations, suggesting the need for interventional control of the blood flow in the IMV. Decompensated conditions in the liver and severe ascites were significantly more common in patients with IMV than in those without IMV and in patients with hepatofugal IMV than in those with hepatopetal IMV. One possibility for these results is the inefficient use of blood flow from the intestine; that is, the IMV acts as a bypass for intestinal blood flow with a high nutritional content, which intrinsically should be carried into the liver, and it also acts as a route to release harmful components, such as endotoxin, into the systemic circulation. 16,17 Such disadvantageous behaviors of intestinal blood may account for the close relationship between IMV and poor liver function. Portal vein thrombosis represents considerable complication in cirrhosis. Our study did not find a significant relationship between development of IMV and incidence of portal vein thrombosis at baseline. However, presence of IMV might affect the cumulative occurrence rate of portal vein thrombosis in long-term observation due to the potential poor liver function in patients with IMV. Also, it should be examined whether IMV may have some effects on anticoagulation for portal vein thrombosis, which is an emerging trend in the literature. 19,20 There were some limitations to our study. First, this study did not take into account the outflow route of IMV because it is hard for Doppler ultrasonography to detect the outflow vessel. IMV flow drains into the internal iliac vein, gonadal vein, or directly to the inferior vena cava, 10,18 and these different types of shunt formations might represent different clinical presentations. Second, data for rectal varices were not acquired from all subjects, in some cases because colonoscopy is not a routine examination for patients with cirrhosis and in other cases because the patient declined the procedure. Furthermore, some data were not used because of the maximum elapsed time we permitted between the Doppler study and colonoscopy. Thus, the incidence of rectal varices and its relationship with IMV hemodynamics needs to be validated in future studies with a large patient population. In conclusion, the IMV has 2 opposing effects as a collateral vessel in cirrhosis: it promotes the development of rectal varices and hepatic encephalopathy, and it reduces the patient s chance of developing gastroesophageal varices. Although the presence of IMV was associated closely with poor liver function, it did not appear to have a significant influence on the prognosis in cirrhosis patients. It remains to be determined whether therapeutic radiologic intervention for IMV may have a positive effect on patients. References 1. Groszmann RJ, Garcia-Tsao G, Bosch J, et al. Beta-blockers to prevent gastroesophageal varices in patients with cirrhosis. N Engl J Med 2005;353: Garcia-Tsao G, Groszmann RJ, Fisher RL, et al. Portal pressure, presence of gastroesophageal varices and variceal bleeding. Hepatology 1985;5: Ripoll C, Groszmann R, Garcia-Tsao G, et al. Hepatic venous pressure gradient predicts clinical decompensation in patients with compensated cirrhosis. Gastroenterology 2007;133: Abraldes JG, Villanueva C, Banares R, et al. Hepatic venous pressure gradient and prognosis in patients with acute variceal bleeding treated with pharmacologic and endoscopic therapy. J Hepatol 2008;48: Wachsberg RH. Inferior mesenteric vein: gray-scale and Doppler sonographic findings in normal subjects and in patients with portal hypertension. AJR Am J Roentgenol 2005;184: Warren WD, Milliken WJ, Henderson JM, et al. Ten years of portal hypertensive surgery at Emory: results and new perspective. Ann Surg 1982;195: Graf O, Boland GW, Kaufman JA, et al. Anatomic variants of mesenteric veins: depiction with helical CT venography. AJR Am J Roentgenol 1997;168: Sakaguchi T, Suzuki S, Morita Y, et al. Analysis of anatomic variants of mesenteric veins by 3-dimensional portography using multidetectorrow computed tomography. Am J Surg 2010;200: Ito K, Blasbalg R, Hussain SM, et al. Portal vein and its tributaries: evaluation with thin-section three-dimensional contrast-enhanced dynamic fat-suppressed MR imaging. Radiology 2000;215: Akpinar E, Turkbey B, Karcaaltincaba M, et al. MDCT of inferior mesenteric vein: normal anatomy and pathology. Clin Radiol 2008; 63: Ferenci P, Lockwood A, Mullen K, et al. Hepatic encephalopathydefinition, nomenclature, and quantification: final report of the working party at the 11th World Congress of Gastroenterology, Vienna, Hepatology 2002;35:
7 1654 MARUYAMA ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 11, No Tajiri T, Yoshida H, Obara K, et al. General rules for recording endoscopic findings of esophagogastric varices. Dig Endosc 2010;22: Shapir J, Rubin J. CT appearance of the inferior mesenteric vein. J Comput Assist Tomogr 1984;8: Hartleb M, Boldys H, Rudzki K, et al. Portal shunting in inferior mesenteric vein in cirrhosis: correlation with hemorrhage from esophageal varices. Am J Gastroenterol 1994;89: Olde Damink SW, Deutz NE, Dejong CH, et al. Interorgan ammonia metabolism in liver failure. Neurochem Int 2002;41: Wiest R, Garcia-Tsao G. Bacterial translocation (BT) in cirrhosis. Hepatology 2005;41: Bellot P, Frances R, Such J. Pathological bacterial translocation in cirrhosis: pathophysiology, diagnosis and clinical implications. Liver Int 2013;33: Matsumoto S, Mori H, Sagara Y, et al. Inferior mesenteric veno-caval shunt: imaging features and interventional treatment. Clin Radiol 2007;62: Amitrano L, Guardascione MA, Menchise A, et al. Safety and efficacy of anticoagulation therapy with low molecular weight heparin for portal vein thrombosis in patients with liver cirrhosis. J Clin Gastroenterol 2010;44: Delgado MG, Seijo S, Yepes I, et al. Efficacy and safety of anticoagulation on patients with cirrhosis and portal vein thrombosis. Clin Gastroenterol Hepatol 2012;10: Reprint requests Address requests for reprints to: Hitoshi Maruyama, MD, PhD, Department of Gastroenterology and Hepatology, Chiba University Graduate School of Medicine, 1-8-1, Inohana, Chuou-ku, Chiba, , Japan. maru-cib@umin.ac.jp; fax: (81) Conflicts of interest The authors disclose no conflicts.
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