Hemoperitoneum in cirrhotic patients without abdominal trauma or tumor

Yuan-Ji Ma, En-Qiang Chen, Jia-Jie Lu, Ming-Zhen Tan and Hong Tang

Chengdu, China

Hemoperitoneum in cirrhotic patients without abdominal trauma or tumor

Yuan-Ji Ma, En-Qiang Chen, Jia-Jie Lu, Ming-Zhen Tan and Hong Tang

Chengdu, China

BACKGROUND:Hemoperitoneum is associated with several emergency conditions and is especially evident when it occurs in patients with liver cirrhosis. This study aimed to assess the clinical characteristics of cirrhotic patients who did not have abdominal trauma or tumor but who developed hemoperitoneum.

METHODS:We reviewed the clinical records of 1276 consecutive cirrhotic patients with hemoperitoneum at our center between January 2007 and December 2009. Hemoperitoneum was confirmed by abdominal paracentesis.

RESULTS:Of the 1276 cirrhotic patients, 19 were found to have hemoperitoneum, but only 6 did not have abdominal trauma or tumor. The occurrence of spontaneous hemoperitoneum in the cirrhotic patients was therefore 0.5%. Hemoperitoneum can occur spontaneously in severely decompensated cirrhotic patients with intra-abdominal collateral vessels and high scores on the model for end-stage liver disease and Child-Pugh-Turcotte test. Most patients presented with abdominal distension, abdominal pain, increased abdominal girth and hemodynamic instability with a significant drop in the hemoglobin level. Three patients died of hemorrhagic shock within 24 hours, and the other 3 died of hepatic encephalopathy or spontaneous bacterial peritonitis after 5 to 10 days because of further decompensation of the liver.

CONCLUSIONS:Hemoperitoneum can occur in cirrhotic patients who do not have abdominal trauma or tumor. It mainly occurs in severely decompensated end-stage cirrhotic patients. Cirrhotic patients with hemoperitoneum have a poor prognosis.

(Hepatobiliary Pancreat Dis Int 2011; 10: 644-648)

liver cirrhosis; portal pressure; hemoperitoneum; abdominal paracentesis

Introduction

Ascitic fluid is considered to be hemorrhagic when its erythrocyte count is more than 50 000/mL or when a hematocrit value is approximately 0.5%. In patients with massive hemoperitoneum, ascitic fluid becomes grossly hemorrhagic and can have a hematocrit value close to 40%, often exceeding that of the peripheral blood.[1,2]Ascites may occur with gynecological diseases, abdominal traumas, tumors, inflammatory disorders, vascular disorders, ruptured viscera and abnormal hemostasis.[1]Hemorrhagic ascites is encountered in 5% of patients with cirrhosis[3]and is often associated with various conditions. Hepatocellular carcinoma, ruptured varices or lymphatic channels, blunt abdominal trauma, and postprocedural complications are classic causes of hemoperitoneum in patients with hepatic cirrhosis.[1]Spontaneous hemoperitoneum in cirrhotic patients may be a poor prognostic sign because it is associated with an increased risk for hepatorenal syndrome and encephalopathy and with a high mortality rate.[3,4]

This study describes the clinical features of hemoperitoneum in 6 cirrhotic patients without abdominal trauma or tumor. The causes and management of hemoperitoneum in these patients are also discussed.

Methods

In this study we reviewed 1276 consecutive cirrhotic patients who had been hospitalized in our center between January 1, 2007 and December 31, 2009. Patients with hemoperitoneum were identified from medical records with terms "cirrhosis", "hemoperitoneum" or "intra-abdominal hemorrhage". Patients with abdominal trauma, tumor and gynecological conditions were excluded from the study because hemoperitoneum can often occur as a complication of these disorders.

The diagnosis of liver cirrhosis was dependent on the history of chronic liver disease, physical examination, laboratory studies and imaging examinations.[5]The diagnosis of hemoperitoneum was confirmed by theaspiration of grossly and uniformly bloody fluid via abdominal paracentesis performed in the left lower quadrant, 2-3 cm lateral to the anterior rectus muscle border. If there was a contraindication such as severe bowel distension, an ultrasound-guided paracentesis was considered. In case of grossly hemorrhagic ascites, paracentesis was repeated immediately at a distant site to exclude the possibility that a dilated peritoneal vessel was punctured at the first tap.[1]

Clinical manifestations, laboratory studies, imaging examinations, management and prognoses of the patients were analysed retrospectively. The results of laboratory studies included coagulation parameters, liver function, renal function and alpha-fetoprotein. Imaging examinations included color Doppler ultrasonography, contrast-enhanced computed tomography and upper gastrointestinal endoscopy. The severity of cirrhosis was rated with the Child-Pugh-Turcotte (CPT) method[6]and the model for end-stage liver disease (MELD) as reported by Kamath et al.[7]The creatinine clearance rate was estimated with the Cockcroft-Gault formula.[8]The data were presented as mean±SD.

Results

In a 3-year period, 1276 consecutive patients with liver cirrhosis were admitted to our center. Hemoperitoneum was identified in 19 of these patients, but only 6 patients were found to have no abdominal trauma, tumor or gynecological conditions. Hence the frequency of hemoperitoneum was 0.5% in cirrhotic patients without abdominal trauma or tumor. The remaining 13 patients received abdominal paracentesis and the final procedure was performed between 1 and 5 days prior to the appearance of hemoperitoneum. Although clear ascites was found in the last abdominal paracentesis before the appearance of hemoperitoneum, bleeding may still be related to the abdominal paracentesis.

Five of the 6 patients were male. Their average age was 44±10 years, and all were infected with hepatitis B virus. Three patients had alcoholism. Two patients had a history of alimentary tract hemorrhage, and one had undergone an endoscopic oesophageal variceal ligation 5 weeks before hemoperitoneum was diagnosed.

Hemoperitoneum may present with a variety of symptoms, but most of our patients had abdominal distension, abdominal pain, and increased abdominal girth. Two patients presented with hemodynamic instability and another one showed signs of hemodynamic instability later. Four patients experienced cough, vomiting or constipation as a precipitating factor. The patients showed a significant drop in the hemoglobin level (an average from 117±18 g/L to 91±24 g/L).

Hemoperitoneum occurred in hospitalized patients with decompensated end-stage liver disease. Color Doppler ultrasonography and contrast-enhanced computed tomography before the appearance of hemoperitoneum showed that all of the patients had a nodular contour of the liver, a small liver with hypertrophy of the left lobe, splenomegaly, intra-abdominal collateral vessels and ascites. The average size of the oblique diameter of the right liver in these patients was 11.5± 0.7 cm, the average diameter of the portal vein was 1.5± 0.1 cm, the average diameter of the splenic vein was 0.5±0.1 cm and the average spleen thickness was 4.7± 0.5 cm. None of the patients had tumor-like masses or dilated intra- and extra-hepatic biliary tracts. Two patients underwent ultrasonography 2-3 days after the diagnosis of hemoperitoneum and one underwent computed tomography 5 days after the diagnosis of hemoperitoneum (Fig.). None of these procedures identified the source of the hemoperitoneum. The other patients were too ill to undergo imaging examination. Screening with upper gastrointestinal endoscopy 6 to 35 days before the appearance of hemoperitoneum revealed varying degrees of varix involving the lower oesophagus in 5 patients.

The MELD scores of these patients were 28±3 and the CPT scores were 11±1; the level of total bilirubin was elevated to 405.0±43.8 μmol/L and the level of albumin was as low as 27.7±3.5 g/L. Coagulation parameters were apparently abnormal with a lower platelet count of 66±28×109/L and an elevated international normalized ratio (INR) of 2.8±0.8. Renal function was assessed in all patients. The creatinine clearance rate was 94.0±23.9 mL/min and the serum urea level was elevated to 3.9±0.6 mmol/L. The alpha-fetoprotein level was also elevated to 41.65±44.09 ng/mL. Artificial liver support was performed 5 times in 3 patients with 2950 to 3050 mLof plasma per exchange; the last plasma exchange was performed between 2 and 11 days before the diagnosis of hemoperitoneum.

Fig. Portal venous phase image. The source of hemoperitoneum was not found in this 36-year-old patient with severe cirrhosis, even after contrast-enhanced computed tomography scanning was performed 5 days after hemoperitoneum.

All patients with hemoperitoneum were managed conservatively after the administration of adequate fluid resuscitation, blood products (fresh frozen plasma and red cell suspension) and appropriate medication (somatostatin, hemostatics and dopamine). None of the patients underwent surgery because of their severe end-stage liver disease. Despite control of hemorrhage, all patients died during the period of the hospital stay. Among them 3 patients died of hemorrhagic shock within 24 hours and the rest 3 died of hepatic encephalopathy or spontaneous bacterial peritonitis 5 to 10 days after the development of hemoperitoneum because of further decompensation of the liver.

Discussion

Although hemoperitoneum is a rare complication in patients with liver cirrhosis, it is also seen in decompensated end-stage cirrhotic patients who do not have either abdominal trauma or tumor. Some patients, like the three in this study, die of hemorrhagic shock; other patients, even in the presence of hemodynamic stability, have a poor prognosis. Although the incidence of hemoperitoneum in cirrhotic patients without abdominal trauma or tumor was 0.5% in this study, physicians should be aware of this lethal complication in decompensated end-stage cirrhotic patients.

The initial clinical manifestations of hemoperitoneum include abdominal pain and distension, increased abdominal girth, dizziness or syncope.[1,4,9-12]Hypotension either at presentation or shortly thereafter is almost universal.[1,4,11]In this study, clinical manifestations included all of the signs and symptoms listed above. A previous study[13]showed that Cullen's and Turner's signs can appear several days after the occurrence of intra-abdominal hemorrhage in patients with portal hypertension. However, blood is a minor peritoneal irritant, and the intensity of abdominal pain is related to the rapidity and volume of extravasation; peritoneal signs may not be present.[1]A characteristic clinical feature of intra-abdominal hemorrhage is the rapid enlargement of abdominal girth and rapid increase of ascites; this is in contrast to the relatively slow accumulation of non-hemorrhagic ascites.[1,9]The levels of hemoglobin and hematocrit also decrease in case of intra-abdominal hemorrhage.[3,10,12]In this study, the mean hemoglobin level decreased from 117 g/L to 91 g/L. However, the hemoglobin level as measured in a serum sample obtained at initial presentation may not reflect the extent of a hemorrhage; this was true for one of the patients in our study, whose hemoglobin level changed by less than 10 g/L. In our opinion, when cirrhotic patients present with rapid abdominal distension, increased abdominal girth and hypotension without evidence of alimentary tract hemorrhage, hemoperitoneum should be considered and abdominal paracentesis should be performed to confirm the diagnosis as soon as possible.

In this study, the diagnosis of hemoperitoneum was confirmed by the aspiration of gross and uniform bloody fluid via abdominal paracentesis. In cirrhotic patients, a sudden onset of abdominal pain in combination with hypotension and a falling hematocrit level in the absence of external blood loss indicate a need for an abdominal ultrasound.[14]Although the source of hemoperitoneum was not identified in the 3 patients who underwent ultrasonography or computed tomography in this study, other studies showed that computed tomography and nuclear magnetic resonance imaging do play an important role in the diagnosis, detection and source localization of acute intra-abdominal hemorrhage.[14,15]In patients for whom computed tomography is negative for localized hematoma or hepatocellular carcinoma, hemoperitoneum is most likely caused by a ruptured abdominal varices.[1]

In this study, the 6 patients showed evidence of decompensated end-stage liver cirrhosis with intraabdominal collateral vessels and liver insufficiency but without abdominal trauma or tumor. Several mechanisms have been proposed to explain the hemorrhagic complication.

First, the spontaneous rupture of ectopic varices in the peritoneum can lead to hemoperitoneum. Ectopic varices are natural portosystemic shunts occurring anywhere in the abdomen except in the cardioesophageal region. Ectopic varices are an unusual cause of hemorrhage that account for between 1% and 5% of all variceal bleeding.[9]A review of 169 cases of bleeding ectopic varices found that 17% occur in the duodenum, 17% in the jejunum or ileum, 14% in the colon, 8% in the rectum, and 9% in the peritoneum.[9]The tension in the varix wall is proportional to portal pressure and the vessel size of ectopic varices.[16]When liver cirrhosis is aggravated, portal pressure and vessel size increase; spontaneous rupture of intraperitoneal or retroperitoneal varices and hemoperitoneum may then occur. Two studies demonstrate that increasing intraabdominal pressure markedly increases the volume, pressure, and wall tension of the varices.[17,18]Therefore, increasing intra-abdominal pressure can increase the risk for variceal rupture in cirrhotic patients withcollateral circulation. Some precipitating factors, such as coughing, vomiting, dysuria, constipation, lifting heavy objects, and tense ascites can increase intraabdominal pressure and may induce variceal rupture and spontaneous hemoperitoneum in these patients. In this study, 4 patients had these precipitating factors.

Second, clotting factor deficiency due to the progressive loss of hepatic parenchymal cells and a low platelet count caused by portal hypertension and hypersplenism leads to hemoperitoneum. The coagulation parameters of patients in this study were abnormal; the average platelet count was 66±28×109/L, and the average INR was 2.8±0.8. Alhough these patients were at risk for spontaneous and procedure-related bleeding, no definitive evidence was found to suggest that individual clotting factor levels are more predictive of bleeding.[19]The large retrospective study of 4729 paracentesis procedures confirmed that hemorrhagic complications do not necessarily occur in the context of severe thrombocytopenia and/or a prolonged coagulation time.[10]In that study, only 2 of 9 patients who bled presented platelet levels under 50×109/L or an INR of more than 2.

The management of hemoperitoneum involves monitoring, volume resuscitation and hemostasis based on pathogenesis. Blood pressure, heart rate, urine output, hemoglobin level and renal function are the basic parameters that are monitored dynamically. In order to achieve hemodynamic stabilization, volume resuscitation must be put into practice immediately; this includes adequate fluid resuscitation, blood products (fresh frozen plasma and red cell suspension) and vasopressor drugs (amines) if necessary. Hemostasis can be accomplished with a variety of treatments depending on the pathogenesis of the bleeding: appropriate medication (somatostatin, terlipressin, hemostatics and recombinant activated factor VII),[20]a transjugular intrahepatic approach to the portal system for angiographic embolization, a transjugular intrahepatic portosystemic stent shunt and surgery for ligating the bleeding varices.[1,9,12,21-23]In this study, none of the patients underwent embolization, transjugular intrahepatic portosystemic stent shunt or surgery because of their severe liver disease. In the end, all 6 died of hemorrhagic shock or further decompensation of the liver. Because of this high mortality rate, orthotopic liver transplantation should be considered.

In conclusion, hemoperitoneum in cirrhotic patients without abdominal trauma or tumor is rare (0.5%). It may occur spontaneously in patients who have decompensated cirrhosis with intra-abdominal collateral vessels and liver insufficiency. Abdominal pain and distension, increased abdominal girth, dizziness or syncope, hypotension, and a significant drop in the hemoglobin level are common clinical manifestations. When hemoperitoneum is confirmed by a repeated paracentesis, imaging examinations may detect and localise its source. Angiographic embolization, transjugular intrahepatic portosystemic stent shunt or surgery should be considered cautiously when hemodynamic instability persists despite adequate volume resuscitation and medications. Orthotopic liver transplantation may be the best therapeutic option in this rare, high-risk situation that carries such a poor prognosis.

Funding:None.

Ethical approval:Not needed.

Contributors:TH proposed the study. MYJ and CEQ wrote the first draft and analyzed the data. All authors contributed to the interpretation of the study and to further drafts. TH is the guarantor.

Competing interest:No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

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Received September 30, 2010

Accepted after revision February 8, 2011

Knowledge is pleasure as well as power.

—William Hazlitt

Author Affiliations: Center of Infectious Diseases, West China Hospital, Sichuan University, Chengdu 610041, China (Ma YJ, Chen EQ, Lu JJ, Tan MZ and Tang H)

Hong Tang, MD, Center of Infectious Diseases, West China Hospital, Sichuan University, Chengdu 610041, China (Tel: 86-28-85422650; Fax: 86-28-85423052; Email: htang6198@hotmail.com) © 2011, Hepatobiliary Pancreat Dis Int. All rights reserved.

10.1016/S1499-3872(11)60109-4