Introduction
The liver is the most frequently injured abdominal organ, despite its relatively protected location [
1,
2]. The management of hepatic trauma has undergone a paradigm shift over the past several decades with significant improvement in outcomes, shifting from mandatory operation to selective nonoperative treatment, and, presently, to nonoperative treatment with selective operation [
3]. The present review considers the consensus of emergency strategies and trends regarding trauma of the liver.
The literature works cited were mainly reviewed if the work discussed is an original research or highly cited article, if it reports research finding based on the systematic collection of data, if it uses statistical methods for data analysis, and if it was published within the last five years. The following keywords were used to search the PubMed: “liver trauma and resuscitation,” “liver trauma and sonography,” “liver trauma and computed tomography,” “liver trauma and angiography,” “liver trauma and nonoperative treatment,” “liver trauma and packing,” “liver trauma and Pringle maneuver,” “liver trauma and damage control,” limited to “Humans,” “English,” and “All Adult.” The broad consensus regarding most aspects of liver trauma management is based on available published prospective, observational, retrospective data and expert opinions because of the limited number of published prospective randomized trials.
Mechanisms of liver injury
A better understanding of the mechanisms aids in the initial assessment and establishment of a management strategy. Road traffic accidents and violent behavior account for the majority of liver injuries. Farming and industrial accidents also account for a significant number [
4]. The liver consists of a fragile parenchyma within the thin Glisson’s capsule, which makes the liver very susceptible to blunt or penetrating trauma. The vasculature consists of wide-bore, thin-walled vessels with a high blood flow, and injury usually causes significant blood loss. Liver trauma should be suspected in all patients with penetrating or blunt thoracoabdominal trauma, particularly in shocked patients with penetrating or blunt trauma on the right side [
4].
Penetrating injuries are usually associated with a significant vascular injury. A stab injury may cause major bleeding from the portal vein, hepatic artery, hepatic vein, or vena cava [
5]. Gunshots may similarly disrupt these major vessels, and are probably much more marked than stab wounds due to their cavitation effect [
6]. Blunt trauma more usually affects the right hepatic lobe, particularly the posterior sector, while the caudate lobe is rarely affected. Blunt trauma in a road traffic accident or fall from a height may result in a deceleration injury, which leads to tears at sites of the liver fixed to the diaphragm and abdominal wall. This type of injury usually involves a fracture between the posterior sector and the anterior sector of the right lobe, which may be associated with a significant vascular injury of the right hepatic vein. In contrast, a direct blow (from a fist or weapon) to the abdomen may produce a central crush injury, which may cause an extensive laceration involving segments IV, V, and VIII. This type of injury may lead to major vascular injury, such as damage to the hepatic arteries, portal veins, or hepatic veins [
4].
Grade of liver injury
The severity of liver injuries ranges from minor capsular tear to extensive disruption of both lobes with associated portal vein, hepatic vein, or vena caval injury. Among the various classification systems of liver injury, that of the American Association for the Surgery of Trauma is probably the most widely used (Table 1) [
7]. According to the system, grade I or II injuries are generally considered as minor injuries, while injuries of grades III to V are usually considered as severe injuries. Significant vascular injuries usually occur with major parenchymal laceration (grades IV and V). High-grade hepatic injuries are associated with a higher surgical intervention rate and a poorer prognosis.
Initial assessment
Initial resuscitation and examination
The initial resuscitation of liver trauma should follow the Advanced Trauma Life Support principles of aggressive fluid resuscitation, guided by the monitoring of central venous pressure and urinary output [
8]. Special attention should be paid to the patient’s abdominal examination, vital signs, and response to resuscitation (Fig. 1). Peritonitis remains the indication for exploration after abdominal trauma. In addition, emergency management should also be directed toward the avoidance of the sinister triad of hypothermia, coagulopathy, and acidosis, all of which significantly increase mortality. Managements to avoid hypothermia are now commonly used in major emergency centers and include rewarming blankets and heat exchanger pumps for rapid infusion of resuscitation fluid and blood. The early use of a massive transfusion protocol, rather than the excessive use of crystalloids, is encouraged for patients with ongoing transfusion needs and has been shown to avoid coagulopathy and to reduce mortality [
9,
10]. Data from recent study also support the early use of plasma to red blood cells at a ratio approaching 1:1, which improves outcomes in massively transfused civilian trauma patients [
11]. Meanwhile, patients receiving massive transfusion are also at risk for hypocalcemia, which results from the binding of calcium by citrate found in stored blood, particularly in patients with impaired hepatic function [
12].
Focused abdominal sonography for trauma
The traditionally accepted definition of hemodynamic instability is a systolic pressure of≤90βmmHg, although a truly well accepted definition has not yet been achieved [
13]. Hemodynamically unstable patients should undergo a focused abdominal sonography for trauma (FAST), as shown in Fig. 1 [
14]. A positive FAST examination in hemodynamically unstable patient is an indication for operation. The delay in surgery and control of bleeding in unstable patient must be very strongly emphasized as bleeding is associated with significantly higher mortality [
15]. If patients with persistent hemodynamic instability have a negative FAST, extraabdominal injuries contributing to shock should be suspected [
16]. Extraabdominal sources of hemorrhagic shock usually include massive hemothorax, severe pelvic fracture, or multiple long bone fractures; nonhemorrhagic shock from cardiogenic (tension pneumothorax, cardiac tamponade, and myocardial contusion or infarct) or neurogenic (spinal shock) causes may also be present. If extraabdominal sources of exsanguinating hemorrhage are not present or if hemoperitoneum remains a concern in a hemodynamically unstable patient with a negative FAST, a diagnostic peritoneal aspirate should be considered (Fig. 1). A positive diagnostic aspirate greater than 10 ml of gross blood is an indicator for operative exploration in unstable patients [
17]. For hemodynamically stable patients, however, surgery is not the immediate priority. Appropriate further investigation may ultimately lead to nonoperative management. The main investigative and therapeutic strategy includes ultrasonography, computed tomography (CT), and interventional vascular radiological techniques.
CT and angiography
Ultrasound scan is very accurate for penetrating and blunt abdominal injuries, with specificity reported from 95% to 100% and sensitivity from 63% to 100% [
4]. FAST has largely replaced the diagnostic peritoneal lavage in the initial assessment of blunt truncal injuries [
18]. However, FAST is highly operator-dependent. Therefore, it must be emphasized that a negative FAST scan does not safely rule out injury [
19]. The exclusion of liver injury in the event of significant blunt trauma should be based on the combination of a negative ultrasound scan and normal clinical examination and observation [
20]. Additionally, ultrasound cannot accurately calculate the extent of hepatic parenchymal or vascular injury and cannot take the place of CT scan. CT scan has become the standard examination for stable patients with an abdominal injury (Fig. 1) [
21]. The decreased mortality associated with nonoperative management can be attributed to the use of CT to aid in the diagnosis of hepatic trauma [
22]. CT has particularly high sensitivity and specificity for detecting liver injuries (Fig. 2). The type and extent of liver injury can be precisely identified by CT; such injuries may include subcapsular and intraparenchymal hematomas, lacerations, and vascular injuries. CT could also detect active ongoing hemorrhage, which is visible as an extravasation of contrast material and is a strong predictor of failure in nonoperative treatment [
23]. The presence of ongoing hemorrhage on CT has been considered to be an indicator for intervention [
24]. The use of CT usually requires resuscitation facilities being moved away from the patient to get into the X-ray department; therefore, CT examination is recommended for hemodynamically stable patients. Interventional radiological techniques provide a new dimension to the treatment of complex hepatic injuries and push the boundaries of nonoperative management of liver trauma. Angiography allows the intervention at difficult-to-access locations, which is important in both pre- and post-operative stages of treatment [
25]. Arterial embolization is an important element in modern management of high-grade liver injuries (Fig. 1). There are two principal indications in the acute post-injury phase: (1) primary hemostatic control in hemodynamically stable or stabilized patients with radiologic computed tomography evidence of active arterial bleeding and (2) adjunctive hemostatic control in patients with uncontrolled suspected arterial bleeding despite emergency laparotomy [
26].
Nonoperative management
Hogarth Pringle first described the operative management of liver trauma in 1908. However, all patients who underwent operations died and Pringle recommended conservative nonoperative management in patients of liver trauma. Nonoperative management was first reported in 1972; it is considered one of the most significant changes in the treatment of liver injuries over the past two decades [
27]. The paradigm shift from operative management to nonoperative management is ascribed to several factors: (1) the observation that 50% to 80% of all liver injuries stop bleeding spontaneously, (2) the success of nonoperative management in children, and (3) the significant development of CT techniques to provide precise diagnosis of liver trauma. A recent review of the National Trauma Data Base in America showed that 86.3% of all hepatic injuries are now managed without operative intervention and that although organ specific operative rates are associated with increasing grade, grade alone does not accurately predict the need for operation [
28]. Nonoperative management has been popular for high-grade injuries (grades III to V) [
29].
Indications of nonoperative management
In the appropriate environment, selective nonoperative management of penetrating abdominal solid organ injuries has high success and low complication rates [
30]. Nonoperative management is usually recommended for stable patients with stab injuries. There is also increasing evidence to support the use of nonoperative management in gunshot liver injuries [
6,
31]. The traditional fears in nonoperative management of liver trauma, such as increased sepsis rates due to infection of bile and blood collections, have been shown to be inaccurate [
32]. The rate of resorting to open surgery in patients with nonoperative managements is significantly higher in severe grade injuries (grades IV and V); however, the open surgery is rarely due to liver-related complications [
33]. The most common reason for surgical intervention in patients with initial nonoperative management is coexisting abdominal injury, such as delayed bleeding from the kidney or spleen [
34]. The failure of nonoperative management due to delayed liver bleeding is rare (0–3.5%) [
34]. There has always been a debate on the selection criteria of nonoperative management for liver trauma, but it is generally accepted that the key assessment criteria for nonoperative management should include: (1) hemodynamic stability, (2) absence of other visceral or retroperitoneal injuries that need surgery, and (3) the availability of an effective multidisciplinary team, which could provide good-quality CT imaging, intensive care facilities, and experienced surgeons.
Complications of nonoperative management
Not surprisingly, as more nonoperative management is pursued, more liver-related complications are being diagnosed. The role of repeat CT scans is limited in nonoperative management of liver trauma. Follow-up CT was not helpful in clinically stable patients [
35]. An 8-year retrospective review showed that no patients developed hepatic complications in a no follow-up abdominal CT group (40%), and only 3% patients received later operation based on repeat CT scans, all of which were prompted by a change in clinical status [
36]. Hemodynamic instability during nonoperative management of liver trauma may be an indication for surgery irrespective of CT findings. Although routine follow-up CT scans are not necessary, an evaluation by CT scan should be prompted in the situation of persistent systemic inflammatory response syndrome, abdominal pain, jaundice, or an unexplained drop in hemoglobin. Complications of nonoperative management are primarily related to the grade of liver injury and the need for transfusion [
37]. The management of hepatic complications is a multimodality treatment strategy that includes endoscopic retrograde cholangiographic embolization, stenting, transhepatic angioembolization, and image guided percutaneous drainage techniques. Operative intervention also plays an important role in the successful management of complications. Complications that require operative intervention usually include bleeding, abdominal compartment syndrome, and failure of percutaneous drainage techniques. Delayed hemorrhage from blunt hepatic injuries usually occurs within the first 72 h post-injury. The incidence of hepatic or perihepatic abscess is low and could be managed by percutaneous catheter drainage. Biliary complications usually include biloma, bile leak, biliary fistula, and bile peritonitis [
38], and commonly present in a delayed fashion in patients with grade IV injuries. When bile leaks into the hepatic parenchyma with necrosis led by the increasing pressure, a biloma is formed. The common management of biloma is percutaneous catheter drainage, although asymptomatic bilomas do not require management. Bile peritonitis typically presents several days after injury [
39]. Laparotomy is an option, but drainage can also be safely and effectively performed by laparoscopy [
38,
40]. A missed bowel injury may be suspected with the signs of peritonitis, but the incidence is very low even in high-grade injuries. Continued high output biliary drainage may need adjunctive endoscopic retrograde cholangiopancreatography (ERCP) to aid in healing [
41]. A nonoperative-treated patient should stay at the hospital for at least two weeks because of complications of nonoperative management.
Operative management
Packing and resuscitation
When nonoperative management is unfeasible, or fails, the surgeon must be prepared to conduct a resuscitative laparotomy. Minor liver bleeding is usually present in liver injuries of grades I and II and can usually be managed by packing alone. If needed, simple techniques, such as electrocautery, argon beam coagulation, or topical hemostatic agents, can be used (Fig. 3). Balloon catheter tamponade can be used in multiple anatomic regions and for variable patterns of injury to arrest ongoing hemorrhage. Placement for central hepatic gunshot wounds is particularly useful [
42]. The first step in the management of patients with major hepatic hemorrhage is manual compression followed by perihepatic packing. The surgeon compresses the injured parenchyma between two hands and places laparotomy pads around the liver to compress the injury and accelerate hemostasis. Perihepatic packing will control profuse hemorrhaging in most patients undergoing laparotomy when done correctly and expeditiously [
43]. Packing is also extremely useful for the general surgeon in a district hospital, as it can be life-saving during transfer to a major trauma center to undergo further surgery; otherwise, the patients may possibly lose the chance to survive.
The measures to rapidly control bleeding are vital and should be maintained to help the anaesthetist achieve restoration of the blood volume and effective intraoperative resuscitation. The patient should undergo intraoperative resuscitation with blood component therapy as discussed above. A massive transfusion protocol should be strongly considered, as early massive transfusion has been proven to reduce mortality [
10]. Attempts to identify and repair hepatic vascular injuries before effective resuscitation should be avoided as they always lead to further hemorrhage, hypotension, acidosis, and coagulopathy, which increase mortality. Rapid and systematic abdominal exploration should be performed to identify the sources of nonhepatic hemorrhage and areas of contamination. If the bleeding is under control, temporary abdominal closure is performed. The patient is then transported to the intensive care unit (ICU) for resuscitation, as shown in Fig. 3.
Leaving packs around the liver is known to cause significant cardiopulmonary compromise and increase the risk of abdominal compartment syndrome [
44]. Liver packs should be removed as soon as the patient is stable and coagulopathy, hypothermia, and acidosis have been corrected [
45]. However, the cardiopulmonary benefits of pack removal should be weighed against the risk of re-bleeding requiring repeat liver packing. Re-bleeding from the liver has been demonstrated to be greater when liver packs were removed within 36 h [
46]. A retrospective review of 534 liver injuries showed that the first relook laparotomy following packing should be performed after 48 h and when hypotension, hypothermia, coagulopathy, and acidosis have been corrected. An early relook at 24 h is associated with re-bleeding and may not lead to the successful removal of liver packs [
47].
Damage control surgery
The concept of damage control was introduced by Stone
et al. in the 1980s [48] and promulgated by Burch
et al. in 1992 [
49]. The term “damage control” was popularized by the group at the University of Pennsylvania in 1993 [
50]. The concept of damage control surgery includes three principle phases. Phase 1 involves the initial control of hemorrhage and contamination followed by packing and rapid wound closure, without immediate concern for restoration of anatomical integrity. Phase 2 involves further resuscitation and stabilization in the intensive care unit for 24 h to 48 h period until normal physiologic parameters have been restored. Phase 3 involves re-exploration and definitive operation [
51]. The sinister triad that interact to produce a deteriorating metabolic situation are hypothermia, coagulopathy, and acidosis. Patients in this condition are at the limit of their physiological reserves, while prolonged and complex surgical repair attempts may cause exceptionally high mortality [
52]. Early recognition of hypothermia, coagulopathy, and acidosis is essential in the damage control approach.
The damage control concept is quite appropriate for the treatment of major liver injuries, as described by Halsted in 1908 for the control of liver bleeding by packing. The concept was re-popularized in the early 1980s, and was more widely adopted throughout the next two decades. The common criteria to use damage control surgery in patients with liver trauma should include: (1) blunt abdominal trauma of high energy, multiple abdominal penetrating trauma, hemodynamic instability, (2) major vessel injury of abdomen or thorax, multiple visceral injury, and severe craniocerebral injury, (3) severe metabolic acidosis (pH≤7.30), hypothermia (temperature≤35°C), resuscitation, and operation time>90 min, coagulopathy, and massive transfusion (>10 U), (4) continuous bleeding from wound surface after resectional debridement, hepatectomy, and vessel ligation, (5) extensive parenchymal laceration or extensive subcapsular hematoma expending, and (6) intraoperative uncontrolled hemorrhage and intrahepatic/extrahepatic major vessel injury [
53].
Pringle maneuver
If the bleeding cannot be controlled by packing alone, complex hepatic injury must be suspected. Pringle maneuver should be performed immediately, with the placement of a vascular clamp on the porta hepatis to control portal vein and hepatic artery bleeding (Fig. 3). Additionally, the mobilization of the liver with the takedown of the falciform, coronary, and triangular ligaments can be used to optimize exposure. Hepatotomy is performed under Pringle control and involves finger fracture to allow ligation of the bleeding vessels. Despite the risk of tissue necrosis or injury to intact vessels and bile ducts, deep parenchymal sutures is still an option for hemostasis. However, in major hepatic venous injuries, severe hemorrhage may occur while extending a deep liver laceration, which cannot be controlled by a Pringle clamp and may increase morbidity. In such cases, hepatotomy should be abandoned and an alternative, such as total vascular exclusion or definitive packing, should be adopted. For hepatic parenchymal devascularization or destruction, resectional debridement should be performed. Resectional debridement refers to the removal of inviable parenchyma using the line of injury as the boundary of the resection rather than standard anatomical planes [
54]. The patient should be hemodynamically stable and not have a coagulopathy. The principle of resectional debridement is to minimize the extent of parenchymal dissection so that operating time is short and tissue with further potential for bleeding is not created. Anatomical resection is now rarely performed, especially at the time of initial surgery.
The Pringle maneuver was initially introduced to reduce hepatic hemorrhage after abdominal trauma at the beginning of the 20th century. However, the maximal ischemic time tolerated by the liver is still controversial. At the beginning of the 1960s, experimental studies showed that the human liver was thought to tolerate no longer than 20 min of continuous ischemia. The time limit was subsequently extended to over an hour [
55]. Intermittent Pringle maneuver gradually replaced the continuous maneuver to improve liver tolerance to ischemia. There is enough evidence to show that intermittent maneuver allows the liver to better tolerate ischemia for prolonged duration and reduces both the risk of massive bleeding and postoperative liver failure [
56]. However, no consensus regarding the time limits of intermittent maneuver has been reached. According to the study of Man
et al. [
57], 120 min was the safer upper limit for intermittent maneuver. Meanwhile, Ishizaki
et al. [
58] showed how the limit could be extended to 325 min in a normal liver without major complications. A recent study showed that hepatectomies done with intermittent clamping exceeding 120 min are as safe as those performed with shorter times [
59].
If the bleeding persists after a Pringle maneuver, the existence of juxtahepatic venous injury must be suspected (Fig. 3). Packing is the best choice to control bleeding because there is a strong argument against any type of direct repair, which may increase mortality [
60]. Dismal results from direct repair alone may lead to the introduction of vascular isolation with shunting. Atriocaval shunts have largely been abandoned because of their poor survival figures. Venovenous bypass can be a useful adjunct if performed prior to significant shock, hypothermia, and coagulopathy [
2]. This procedure entails vascular isolation along with establishment of femoral to axillary or jugular veno-veno bypass.
Delayed laparotomy
After the patient has been adequately resuscitated, including correction of hypothermia, acidosis, and coagulopathy, delayed laparotomy may be performed (Fig. 3). Packs are removed and ongoing bleeding, biliary leak, and associated nonhepatic injuries are assessed. If nonviable parenchyma is found, resectional debridement is frequently all that is required. There is no evidence to support routine drainage for elective uncomplicated liver resection [
61]. A closed suction drain should be considered when obvious bile leak is identified at the time of trauma laparotomy. Liver transplantation for trauma is a rare condition, with only 19 cases described in the literature. Emergent liver transplantation after liver trauma is a last-resort option and is only suggested when all other means fail [
62].
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