Abstract
Objectives
This study aimed to explore the incidence and causes of intra-abdominal haemorrhage after hepatectomy, indications for re-exploration, and factors affecting occurrence.
Methods
Clinical data for 77 patients (0.2% of 32 856 hepatectomy patients) submitted to re-exploration for haemorrhage following hepatectomy for primary liver cancer (PLC) from 2001 to 2010 were retrospectively reviewed and analysed for postoperative complications, potential site and cause of bleeding.
Results
The median interval between hepatectomy and re-exploration was 23 h in the 77 patients (range: 1 h to 11 days). Re-exploration occurred within 24 h after hepatectomy in 64 patients (83.1%), and within 8 h in 37 patients (48.1%). The most common anatomic site of intra-abdominal haemorrhage was the cut surface of the liver (n = 51, 66.2%), followed by the perihepatic ligaments (n = 19, 24.7%), the splenic fossa (n = 7, 9.1%), the diaphragm (n = 6, 7.8%), the retroperitonium (n = 6, 7.8%), the right adrenal gland (n = 3, 3.9%), and the gallbladder bed (n = 2, 2.6%). The most common form of bleeding was oozing. Early haemorrhage (at ≤ 24 h) was most likely to occur in the form of venous bleeding or oozing from the cut surface of the liver. Rates of 5-year overall and disease-free survival in the 77 patients were 22.1% and 3.9%, respectively.
Conclusions
Re-exploration for haemorrhage following hepatectomy for PLC is a rare event. Haemorrhage occurs predominantly at the cut parenchymal surface. Early return to the operating room is vital and perioperative survival is common in this high-risk group.
Introduction
Primary liver cancer (PLC) is one of the most common cancers worldwide, especially in China. Hepatic resection remains the best therapeutic strategy for PLC at present and can significantly improve both overall survival (OS) and disease-free survival (DFS) in these patients. However, incidences of post-hepatectomy complications range from 10% to as high as 50%,1–4 and incidences of postoperative intra-abdominal haemorrhage range between 1% and 5%.4–8 Haemorrhage is one of the leading causes of morbidity and mortality after hepatectomy. Few studies have investigated the outcomes of post-hepatectomy haemorrhage.
During a recent 10-year period, over 30 000 hepatectomies for PLC were performed at the present institution. This report examines patients submitted to a second laparotomy for haemorrhage following hepatectomy at the study institution. Risk factors for post-hepatectomy complications, the management of postoperative complications, and survival data were reviewed and analysed.
Materials and methods
Patients and preoperative management
A total of 32 856 hepatectomies for PLC were performed between January 2001 and December 2010 at the Eastern Hepatobiliary Surgery Hospital in Shanghai, China. Among the patients represented by these hepatectomies, 77 (0.2%) required re-laparotomy for postoperative intra-abdominal haemorrhage. Clinical data were collected on age, gender, liver and kidney function tests, coagulation function, alpha-fetoprotein (AFP), hepatitis, reoperation time, type of hepatectomy, operative data, postoperative complications, and length of postoperative hospital stay. All of the 77 patients were assessed by B-ultrasound, computed tomography or magnetic resonance imaging prior to hepatectomy. Liver function was evaluated according to serum bilirubin, Child–Pugh class9 and coagulation function. Hepatectomies involving more than two Couinaud segments were designated as major hepatectomies and all other resections were considered minor hepatectomies.10
Surgical procedures
An intermittent Pringle manoeuvre was used at the time of liver transection with a modified total hepatic vascular exclusion (THVE) procedure if necessary.11 Hepatectomy was performed using the Kelly clamp-crush method and the finger-fracture technique. A venovenous bypass was not used in any case. Any bleeding or open bile ducts on the remaining side of the parenchyma were directly sutured. The cut surface was managed at the discretion of the operating surgeon with full-thickness compression sutures, a pedicle of the greater omentum and/or fibrin glue.12 Before the abdomen was closed, a drain was routinely placed below the right diaphragm and continuous low suction was applied postoperatively. The total bilirubin level in the drainage fluid was measured postoperatively and bile leakage was diagnosed when the bilirubin level in drainage fluid exceeded 30 μmol/l and persisted for > 7 days. The tubes were removed when the amount of discharge decreased to < 10 ml per day. Postoperative haemorrhage was considered when bleeding from the drainage tubes exceeded 100 ml/h.
Laparotomic exploration procedures (second surgery)
Laparotomy was performed through the original incision and blood clots were evacuated. For haemorrhage involving the cut surface of the liver, compression sutures of the residual liver were opened to identify the source of bleeding. For oozing sites, absorbable haemostatic gauze was applied. A drain was placed below the right diaphragm again. All patients were admitted to the intensive care unit and were observed continuously for changes in the abdominal drain and/or vital signs.
Postoperative assessment
Surgical postoperative complications in patients who were returned to the operating room (OR) included ascites, pleural effusions, hyperbilirubinaemia, bile leakage, abdominal abscesses, renal failure and wound infections. The presence of hyperbilirubinaemia referred to a maximum postoperative serum total bilirubin of > 100 μmol/l,13,14 for which aggressive steroid hormone therapy, liver protection drugs and fresh plasma replacement therapy were administered. Shock was defined as a mean arterial pressure (MAP) of < 60 mmHg. Patients with postoperative ascites or pleural effusion were defined as requiring diuretic agents or paracentesis/pleuracentesis. Death within 90 days after hepatectomy was defined as death from postoperative complications.15
Statistical methods
Statistical analysis was performed using spss Version 13.0 (SPSS, Inc., Chicago, IL, USA). Continuous variables were expressed as the median and range, and comparative variables were compared using the Mann–Whitney U-test. Differences were considered significant at a P-value of < 0.05. Overall and disease-free survival were evaluated using the Kaplan–Meier method.
Results
Patient data
Preoperative data are shown in Table 1.
Table 1.
Characteristics of patients requiring a return to the operating room after hepatectomy as a result of haemorrhage
| Patients | Variable data |
|---|---|
| Gender (female/male), n | 11/66 |
| Age, years, median (range) | 52 (16–79) |
| Underlying liver, n (%) | |
| Normal | 12 (15.6%) |
| Fibrosis | 24 (31.2%) |
| Cirrhosis | 41 (53.2%) |
| Child–Pugh class, A/B/C, n | 48/29/0 |
| Preoperative laboratory results, median (range) | |
| ALT, IU/l, median (range) | 45.3 (17.2–249.3) |
| AST, IU/l, median (range) | 59.4 (22.6–275.6) |
| Total bilirubin, μmol/l, median (range) | 16.8 (6.6–37.6) |
| Albumin, g/l, median (range) | 39.7 (29.5–52.8) |
| Prothrombin time, s, median (range) | 12.6 (9.6–19.2) |
| Haemoglobin, g/l, median (range) | 136 (79–180) |
| Platelet count, ×109/l, median (range) | 133 (68–397) |
| AFP, ng/l, (0–40/40–400/> 400 ng/l), n | 29/16/32 |
| HBsAg, (positive/negative), n | 62/15 |
| HCV, (positive/negative), n | 1/76 |
| Liver tumour, n | |
| Tumour differentiation (good/moderate) | 17/60 |
| Tumour size (< 10 cm/≥ 10 cm) | 44/33 |
| Tumour capsule (−/+) | 47/30 |
| Tumour number (single/multiple) | 72/5 |
| Satellite tumours (−/+) | 67/10 |
| Macrovascular invasion (−/+) | 67/10 |
| Microvascular invasion (−/+) | 50/27 |
ALT, alanine aminotransferase (normal range: 11–50 IU/l); AST, aspartate aminotransferase (normal range: 14–50 IU/l); total bilirubin (normal range: 2–17 μmol/l); albumin (normal range: 35–50 g/l); prothrombin time (normal range: 10–14 s); AFP, alpha-fetoprotein; HBsAg, hepatitis B virus surface antigen; HCV, hepatitis C virus.
Of the 32 856 patients examined, 77 (0.2%) patients required to be returned to the OR for haemorrhage. This group included 11 female and 66 male patients with a median age of 52 years (range: 16–79 years). Of the 77 patients, 62 (80.5%) showed positive findings for HBsAg [hepatitis B virus (HBV) surface antigen], 41 (53.2%) were positive for HBV DNA, and one (1.3%) was positive for hepatitis C virus (HCV). Primary liver cancer in these patients was classified as hepatocellular carcinoma in 69 (89.6%) patients, cholangiocarcinoma in five (6.5%) patients, hepatic sarcoma in two (2.6%) patients, and clear cell carcinoma of the liver in one (1.3%) patient.
Hepatectomy outcomes
The median operative time for the original hepatectomy, including in the 11 patients in whom inflow occlusion was not used and the 66 in whom inflow occlusion (Pringle technique) was applied, was 190 min (range: 95–226 min). The median occlusion time was 19 min (range: 5–58 min). Single occlusions were required in 47 patients and two occlusions were required in 19, including six patients in whom both a Pringle occlusion and THVE were used. Median intraoperative blood loss was 600 ml (range: 50–5600 ml); there was no significant difference in mean ± standard deviation (SD) intraoperative blood loss between patients with and without cirrhosis (1025 ± 1138 ml and 811 ± 870 ml, respectively; P = 0.409). Intraoperative transfusions were administered in 53 (68.8%) patients. Thirty-five patients received transfusions of red blood cells (RBC) (median: 695 ml, range: 400–5000 ml) and 36 received transfusions of fresh frozen plasma (FFP) (median: 400 ml, range: 200–1800 ml). Minor hepatectomies were performed in 40 (51.9%) patients and major hepatectomies were performed in 37 (48.1%) patients (Table 2); there were no significant differences between patients undergoing major and minor hepatectomy, respectively.
Table 2.
Types of liver resection in patients with primary liver cancer who required a return to the operating room as a result of haemorrhagea
| Type of resection | Patients, n (%) |
|---|---|
| Major hepatectomy | 37 (48.1%) |
| Extended right hemi-hepatectomy | 9 (11.7%) |
| Extended left hemi-hepatectomy | 1 (1.3%) |
| Right hemi-hepatectomy | 15 (19.5%) |
| Left hemi-hepatectomy | 6 (7.8%) |
| Media trisegmentectomy | 6 (7.8%) |
| Minor hepatectomy | 40 (51.9%) |
| Left lateral sectionectomy (segments II, III) | 4 (5.2%) |
| Right bisegmentectomy | 14 (18.2%) |
| Left segmentectomy | 2 (2.6%) |
| Right segmentectomy | 18 (23.4%) |
| Atypical resection | 2 (2.6%) |
| Associated resections | 37 (48.1%) |
| Cholecystectomy | 25 (32.5%) |
| Splenectomy | 10 (13.0%) |
| Portal vein embolectomy | 5 (6.59%) |
| Choledochojejunostomy | 1 (1.3%) |
37 patients underwent associated surgeries including: cholecystectomy (n = 21); splenectomy (n = 8); portal vein embolectomy (n = 4); cholecystectomy and splenectomy (n = 2); portal vein embolectomy and cholecystectomy (n = 1), and choledochojejunostomy and cholecystectomy (n = 1).
Patients with large tumours (diameter > 10 cm) were more likely to develop intraoperative haemorrhage than those with smaller tumours (mean ± SD: 1469 ± 1252 ml and 586 ± 651 ml, respectively; P < 0.01), and required greater intraoperative transfusion volumes (mean ± SD: 1261 ± 1500 ml and 322 ± 632 ml, respectively; P < 0.01), and longer Pringle occlusion time (mean ± SD: 29.5 ± 19.1 min and 11.7 ± 12.1 min, respectively; P < 0.01).
Outcomes of the return to the OR
A total of 77 patients were returned to the OR for suspected bleeding. The median interval between the initial hepatectomy and return to the OR was 23 h (range: 1 h to 11 days). Return occurred within 24 h after hepatectomy in 64 (83.1%) patients and within 8 h after hepatectomy in 37 (48.1%) patients. The most common clinical presentations were haemorrhage into the drain (67.5%), shock (37.7%), and a declining haemoglobin (Hb) level (48.1%). Drain output exceeded 100 ml/h in 52 patients. Signs of shock (MAP of < 60 mmHg) were not significantly improved by increasing fluid replacement and led to re-exploration in 29 patients. The median decline in Hb after hepatectomy was 30 g/l (range: 1–74 g/l) in 37 patients and 60 g/l in six patients.
At the time of re-exploration, median occlusion time was 12 min (range: 6–25 min) in four patients in whom a Pringle occlusion technique was used. Median blood loss at re-exploration (excluding evacuated clots) was 245 ml (range: 10–6000 ml). Transfusions were required in 73 (94.8%) of the 77 patients, and included RBC (median: 1800 ml, range: 400–5700 ml) and FFP (median: 800 ml, range: 200–2500 ml).
Arterial haemorrhage, haemorrhage from portal branches, haemorrhage from hepatic veins or branches of the inferior vena cava, and oozing of blood were observed during surgery in 14 (18.2%), eight (10.4%), nine (11.7%) and 46 (59.7%) [including 37 (48.1%) patients in whom blood oozing occurred on the cut surface of the liver] patients, respectively. The most common site of intra-abdominal haemorrhage was the cut surface of the liver (n = 51, 66.2%), followed by the perihepatic ligaments (n = 19, 24.7%), the splenic fossa (n = 7, 9.1%), the diaphragm (n = 6, 7.8%), the retroperitonium (n = 6, 7.8%), the right adrenal gland (n = 3, 3.9%) and the gallbladder bed (n = 2, 2.6%) (Table 3). Hepatic outflow obstruction occurred in two of the 77 patients, presenting as liver swelling and congestion, and was relieved by the undoing of full-thickness compression sutures. Early haemorrhage (< 24 h) was most likely to occur in the form of venous bleeding or oozing from the cut surface of the liver (Tables 3,4; Fig. 1). However, there were no significant differences between patients experiencing early and late haemorrhage, respectively, in preoperative Child–Pugh class, postoperative international normalized ratio (INR) or time for Pringle procedure.
Table 3.
Sites of intra-abdominal haemorrhage
| Artery, n | Portal vein, n | Hepatic vein, n | Oozing, n | P-value | ||
|---|---|---|---|---|---|---|
| Liver remnant facet | + | 4 | 6 | 4 | 37 | 0.002 |
| − | 10 | 2 | 5 | 9 | ||
| Diaphragm | + | 0 | 0 | 2 | 4 | 0.211 |
| − | 14 | 8 | 7 | 42 | ||
| Perihepatic ligamenta | + | 7 | 1 | 2 | 9 | 0.105 |
| − | 7 | 7 | 7 | 37 | ||
| Gallbladder bed | + | 0 | 0 | 0 | 2 | 0.709 |
| − | 14 | 8 | 9 | 44 | ||
| Splenic fossa | + | 1 | 1 | 0 | 5 | 0.740 |
| − | 13 | 7 | 9 | 41 | ||
| Retroperitoneum | + | 1 | 0 | 1 | 4 | 0.832 |
| − | 13 | 8 | 8 | 42 | ||
| Right adrenal gland | + | 2 | 0 | 1 | 0 | 0.058 |
| − | 12 | 8 | 8 | 46 |
The perihepatic ligament category includes the falciform ligament, left and right triangular ligament, hepatogastric ligament and coronary ligament.
Table 4.
Relationship between postoperative intra-abdominal haemorrhage and sites of haemorrhage following hepatectomy
| Early haemorrhage | P-value | |||
|---|---|---|---|---|
| > 24 h | ≤ 24 h | |||
| Sites of haemorrhage | Patients, n | Patients, n | ||
| Liver remnant facet | − | 8 | 18 | 0.027 |
| + | 5 | 46 | ||
| Diaphragm | − | 11 | 60 | 0.226 |
| + | 2 | 4 | ||
| Ligament | − | 7 | 51 | 0.075 |
| + | 6 | 13 | ||
| Retroperitonium | − | 13 | 58 | 0.582 |
| + | 0 | 6 | ||
| Gallbladder bed | − | 12 | 63 | 0.311 |
| + | 1 | 1 | ||
| Splenic fossa | − | 10 | 60 | 0.089 |
| + | 3 | 4 | ||
| Right adrenal gland | − | 13 | 61 | 0.570 |
| + | 0 | 3 | ||
| Nature of haemorrhage | ||||
| Artery | 6 | 8 | 0.018 | |
| Portal vein | 2 | 6 | ||
| Hepatic vein | 0 | 9 | ||
| Oozing | 5 | 41 | ||
Figure 1.
Time between the initial hepatectomy and return to the operating room
Other postoperative complications
Of the 77 patients submitted to re-exploration, 42 (54.5%) developed other postoperative complications and seven (9.1%) died of postoperative complications. The most common postoperative complications were ascites (n = 30), hyperbilirubinaemia (n = 11), pleural effusion (n = 10), and intra-abdominal infection (n = 4). Two patients died during the hospital stay of liver dysfunction and septicaemia, respectively. No patient required to be returned to the OR a third time. Rates of 5-year OS and DFS in the 77 patients were 22.1% and 3.9%, respectively (Fig. 2).
Figure 2.
Kaplan–Meier survival curves for overall survival and disease-free survival in 77 patients with primary liver cancer submitted to laparotomy haemostasis after hepatectomy
Discussion
As a result of technical advances in surgery, anaesthesia and perioperative management, the incidence of mortality in patients submitted to hepatectomy has decreased from 20% to < 5% over the past 30 years.16 However, post-hepatectomy complication rates remain between 38% and 47%.3,4,17 The most common postoperative complications following hepatectomy include pneumonia, ascites, hepatic dysfunction, intra-abdominal haematoceles, and abscesses. Some researchers17,18 have concluded that the occurrence of post-hepatectomy complications is related to Child–Pugh class, time of portal occlusion, duration of operation and extent of hepatectomy. Other authors3 believe the occurrence of post-hepatectomy complications to be related to the preoperative platelet count, a surrogate for portal pressure and/or intraoperative transfusion requirements. It is felt the immunosuppressive effects of transfusion may yield increased complications19 and these effects have been shown to impact overall survival.20,21 Kusano et al.22 reported that Child–Pugh class B status and intraoperative blood loss of > 1200 ml are independent predictive factors of post-hepatectomy complications. Although a recent report6 suggested that post-hepatectomy intra-abdominal haemorrhage should be classified for the purpose of statistical analysis, few studies have focused on its causes, and the subject of return to the OR is rarely addressed in the literature.
In the present series, the most common clinical signs of haemorrhage in patients who were returned to the OR after hepatectomy were blood in the drain, postoperative shock and a decrease in serum haemoglobin. Although drainage rates exceeded 100 ml/h during the early period after hepatectomy in some patients, laparotomy was not performed for the reasons of intra-abdominal effusion, a progressive decrease in drainage rate or a gradual lightening in the colour of the drainage fluid. In patients in whom drainage rates do not decrease but instead increase, Hb in the abdominal fluid should be measured and the Hb ratio in the abdominal fluid and blood should be compared. Immediate laparotomy is necessary in patients in whom the abdominal fluid : blood Hb ratio is > 0.5.
Drain output is not the only indicator of postoperative haemorrhage. In the event that postoperative drainage is small, but the patient is hypotensive and/or tachycardic, follow-up Hb and bedside B-ultrasound are necessary.
The timing of return to the OR must be based on the clinical judgement of the surgeon. The results of the present study showed that postoperative haemorrhage often occurred within 24 h after hepatectomy. However, the timing of reoperation should be considered in the context of a comprehensive assessment of the actual clinical situation, including the rate and colour of drain output, the abdominal fluid : blood Hb ratio, and vital signs. Haemoglobin fluctuation is an important factor in decision making in the post-hepatectomy patient. In the occasional patient in whom re-laparotomy does not yield significant haemorrhage, a second laparotomy is recommended as long as the patient’s condition permits this in order to avoid the occurrence of more severe complications. Early haemorrhage (at < 24 h) is more likely to occur as venous bleeding or oozing from facets of the liver remnant, which suggests that early postoperative haemorrhage is related to inappropriate intraoperative haemostasis and/or poor postoperative coagulation. Timely clotting factor replacement, and the meticulous observation of vital signs, drain output and Hb changes in the drainage fluid are important in the management of postoperative haemorrhage.
In addition to careful intraoperative manipulation, the mode of remnant liver management is also important for the prevention of postoperative intra-abdominal haemorrhage. As the liver is cirrhotic in most liver cancer patients, blood oozing is likely to occur in the liver remnant and excessive sutures cannot prevent this from happening. Haemostatic agents and clotting factors, or local packing with gauze, can potentially assist in these cases.
Intraoperative blood loss and transfusion have proved to have significant impact on short- and longterm postoperative survival in hepatectomy patients. The control of intraoperative haemorrhage has long been a major concern.23,24 Massive perioperative blood loss may adversely affect longterm postoperative OS and DFS, both of which may be shortened by intraoperative blood loss of > 1200 ml.22 Intraoperative hepatic outflow occlusion and half-hepatic inflow occlusion can improve intraoperative haemorrhage markedly,11 but are not effective for controlling retroperitoneal haemorrhage.
In the present series, hepatic outflow occlusion led to clinical symptoms of intra-abdominal haemorrhage in two patients, presenting as hypovolaemia, persistent postoperative hypotension and increased abdominal drainage, but Hb was not significantly decreased in these patients in comparison with that in patients in whom intra-abdominal haemorrhage occurred after other types of hepatectomy.
In summary, haemorrhage that requires the patient to be returned to the OR is most likely to occur within 24 h after hepatectomy. The best time for a return to the OR is within 4 h following hepatectomy because an early return implies fewer postoperative complications and improved survival. Drain output, haemodynamics and serum haemoglobin can serve as valuable cues to guide a prompt return to the OR.
Acknowledgments
The authors thank Associate Professor T. Clark Gamblin, Department of Surgery, Medical College of Wisconsin, Milwaukee, WI, USA, for editing the English-language version of this article, and Professor Michael G. Sarrh, Department of Surgery, Mayo Clinic, Rochester, MN, USA, for the provision of much help and guidance on this paper.
Conflicts of interest
None declared.
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