Non-operative management and immune function after splenic injury

Authors

  • J. Skattum,

    1. Department of Traumatology, Division of Emergency and Critical Care, Oslo University Hospital, N-0407, Oslo, Norway
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  • P. A. Naess,

    1. Department of Traumatology, Division of Emergency and Critical Care, Oslo University Hospital, N-0407, Oslo, Norway
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  • C. Gaarder

    Corresponding author
    1. Department of Traumatology, Division of Emergency and Critical Care, Oslo University Hospital, N-0407, Oslo, Norway
    • Department of Traumatology, Division of Emergency and Critical Care, Oslo University Hospital, N-0407, Oslo, Norway
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Abstract

Background:

There is still considerable controversy about the importance and method of preserving splenic function after trauma. Recognition of the immune function of the spleen and the risk of overwhelming postsplenectomy infection led to the development of spleen-preserving surgery and non-operative management. More recently angiographic embolization has been used to try to reduce failure of conservative management and preserve splenic function.

Methods:

A literature review was performed of the changing treatment of splenic injury over the last century, focusing on whether and how to maintain splenic immune function.

Results:

Non-operative management continues to be reported as a successful approach in haemodynamically stable patients without other indications for laparotomy, achieving high success rates in both children and adults. Except for haemodynamic instability, reported predictors of failure of conservative treatment should not be seen as absolute contraindications to this approach. Angiographic embolization is generally reported to increase success rates of non-operative management, currently approaching 95 per cent. However, the optimal use of angioembolization is still debated. Splenic immunocompetence after angioembolization remains questionable, although existing studies seem to indicate preserved splenic function.

Conclusion:

Non-operative management has become the treatment of choice to preserve splenic immune function. Current knowledge suggests that immunization is unnecessary after angiographic embolization for splenic injury. Identifying a diagnostic test of splenic function will be important for future studies. Most importantly, in efforts to preserve splenic function, care must be taken not to jeopardize patients at risk of bleeding who require early surgery and splenectomy. Copyright © 2011 British Journal of Surgery Society Ltd. Published by John Wiley & Sons, Ltd.

Introduction

The spleen is the most commonly injured organ after blunt abdominal trauma and its management has been a topic for discussion over the past decade. There is still considerable controversy about the importance and method of preserving splenic function after trauma. The discovery of the immunological function of the spleen1 and recognition of the risk of overwhelming postsplenectomy infection (OPSI) led to the development of spleen-preserving strategies. Given the morbidity associated with unnecessary laparotomy2, 3, non-operative management of blunt splenic injury has become the treatment of choice in haemodynamically stable patients with no other indication for laparotomy.

Currently, non-operative treatment is attempted in 60–90 per cent of patients with splenic injuries. The success of conservative strategies has been facilitated by access to modalities such as computed tomography (CT), and angiographic embolization for haemorrhage control and treatment of splenic artery pseudoaneurysms. Angioembolization is generally reported to increase the success rate of non-operative management, currently approaching 95 per cent4–11. Splenic immunocompetence after angiographic embolization remains questionable, although existing studies seem to suggest that splenic function is preserved. However, in efforts to preserve splenic function and improve the success rates of non-operative treatment, care must be taken to avoid jeopardizing a group of patients at risk of bleeding. The shocked patient with splenic injury still needs a laparotomy, with splenectomy as the most likely outcome. This article reviews the treatment of splenic injury over recent decades, focusing on whether and how to maintain splenic immune function after trauma.

Overwhelming postsplenectomy infection

Based on the assumptions that the spleen had no function and no ability to heal, splenectomy was performed for most splenic injuries up to the 1950s. The mortality rate associated with non-operative strategies for splenic trauma was believed to be 90–100 per cent, whereas the corresponding operative mortality rate was low12. During this period, the increased risk of infection and sepsis in asplenic and hyposplenic individuals was probably masked by the overall high incidence of infection in the preantibiotic era13. In the 1950s the use of antibiotics changed the landscape. King and Shumacker1 described OPSI in 1952, correlating the asplenic state with this aggressive and rapidly fatal illness.

The true incidence of OPSI remains unknown, but estimates range from 0·1 to 9 per cent14–18. Although the risk of OPSI is lifelong, most episodes occur within the first 2 years after splenectomy, with incidence depending on age, previous exposure to infection and underlying disease. The condition is reported to be fatal in 35–80 per cent1, 14–18. Encapsulated bacteria such as Haemophilus influenzae, meniningococci and pneumococci are the major pathogens causing OPSI, with pneumococci accounting for more than 50 per cent of cases18. Asplenic individuals should be immunized with pneumococcal, H. influenzae and meningococcal vaccines according to existing protocols and follow recommendations to contact a physician about the need for antibiotic prophylaxis in the event of high fever19. However, guidelines are based on low-grade evidence, tend to vary, and patient education and adherence is often poor19, 20.

Splenic function

The spleen has a well described haemofiltration function, contributing to haematopoiesis, phagocytosis, and the destruction of defective erythrocytes, platelets and leucocytes. The spleen also plays a role in immunological host defence mechanisms20. Macrophages and antigen-presenting cells line the sinusoids in the red pulp, and lymphocytes responsible for immunological activation are adjacent in the white pulp. The spleen also produces opsonins such as tuftsin, properdin and fibronectin, facilitating phagocytosis and complement activation13, 21. Although the exact mechanism remains unclear, awareness about the role of the spleen in immunoprotection led to changes in the management of splenic injury in the 1960s22–24.

Spleen-preserving surgical strategies

In 1902, Berger25 reported 14 patients treated by suture of splenic lacerations. Perisplenic packing to prevent bleeding from splenic injury was described the following year26. However, it was not until the importance of splenic immune function became apparent in the 1960s that spleen-preserving surgery gained popularity. Several surgical repair techniques evolved in order to preserve splenic tissue and as much function as possible27, 28. Splenorrhaphy, partial splenectomy, splenic artery ligation and autotransplantation of splenic tissue were performed increasingly29, 30. Several advances in surgical technology have since facilitated spleen preservation, including staplers, advanced coagulators, haemostatic wraps and local haemostatic agents. With increasing use of conservative strategies, these spleen-preserving surgical techniques are now performed less frequently, as most patients who need an operation are haemodynamically unstable and splenectomy is the most appropriate procedure for unstable patients31.

Rationale for non-operative management

Non-operative management of haemodynamically stable patients with splenic trauma became an option in 1948 after an incidental perioperative finding of two separate viable splenic halves in a child with intestinal obstruction and a history of blunt abdominal trauma23. The bleeding had obviously stopped spontaneously in this patient, and a strategy for conservative treatment of haemodynamically stable children with isolated blunt splenic injuries was developed32, 33. A group of surgeons disagreed with this approach and continued to perform splenectomy. This led to the first case–control study on operative versus non-operative management by Upadhyaya and Simpson34 in 1968, which suggested that isolated splenic injuries could safely be treated without surgery in children. Paediatric surgeons led the way during the following decades, and non-operative management is now reported to be successful in more than 90 per cent of children with isolated blunt splenic injuries22, 35, 36.

Inspired by the success of conservative treatment in children, combined with the introduction of CT in the early 1980s enabling more accurate diagnosis, the promulgation of non-operative management in haemodynamically stable adults with splenic injury was made possible (Fig.1)37, 38. The results of a 5-year study of 23 532 patients with blunt splenic injury from the National Trauma Data Bank provide justification for this approach: the success rate was 87 per cent among 90 per cent of patients in whom conservative treatment was attempted39.

Figure 1.

Computed tomogram showing splenic injury (Organ Injury Scale grade 4) with contrast extravasation (white arrow)

Failure of non-operative management

During the past two decades, factors affecting selection for conservative treatment and failure rates have been debated24. In 2000, Peitzman and colleagues40 reported a non-operative management rate of 61·5 per cent in 1488 adults from 27 trauma centres within the USA. The failure rate was 10·8 per cent, with most failures occurring within 24 h and 90 per cent within 72 h. Failure of this strategy was associated with compromised vital signs on admission, increased injury severity including splenic Organ Injury Scale (OIS) grade, and larger volume of blood in the peritoneal cavity40. In a subsequent study of the subgroup with unsuccessful non-operative management, 30–40 per cent of the failures were found to be due to underestimation of haemodynamic instability or misinterpretation of diagnostic images, emphasizing the importance of clinical judgement41. Smith and co-workers39 reported that 95 per cent of conservative treatment failures among 21 166 patients occurred within 72 h. In their study, failure was associated with higher injury severity and lower American College of Surgeons' trauma centre designation.

Several studies have confirmed these predictors and identified other risk factors associated with failure of non-operative management, such as contrast extravasation, arteriovenous fistula, pseudoaneurysm, age over 55 years and multiple injuries3, 5, 6, 11, 42–44. Although these represent risk factors for failure, they are not considered to be absolute contraindications to a conservative approach. The reported rates of success of non-operative treatment of severe splenic injuries (OIS grade 3–5) are high in haemodynamically stable injured adults in spite of the correlation between failure and injury grade4–6, 10, 31, 39, 40, 43, 44.

Age over 55 years has been suggested as a predictor of failure of non-operative management. In studies addressing this patient group specifically, in which conservative treatment is attempted in around 60 per cent, success rates range from 76 to 90 per cent43, 45–47. However, it is important to emphasize that morbidity and mortality rates in older patients are high compared with those in younger patients in all treatment categories. Other studies have reported no difference in failure rates in older and younger patients47, 48.

The variation in success rate reported between different levels of trauma centre can probably be explained by different resource availability, and institutional protocols should probably reflect these differences.

The risk of missing a hollow viscus injury is a concern in non-operative treatment of blunt abdominal trauma. In a study of 190 consecutive patients with splenic injury, Pachter and colleagues38 found no missed hollow viscus injuries in patients managed conservatively. An analysis of 275 557 trauma admissions found hollow viscus injuries in association with only 0·3 per cent of blunt injuries, supporting the practice of non-operative management49. Studies have confirmed long-term preserved immunocompetence after conservative treatment of high-grade splenic injury, and preservation should therefore be considered when resources allow adequate follow-up, albeit with the risk of failure in mind50, 51.

Angiographic embolization as an adjunct to non-operative management

Following the identification of contrast extravasation, arteriovenous fistula and pseudoaneurysm as predictors of failure of conservative treatment, angioembolization was introduced as an adjunct to non-operative management to improve splenic tissue preservation and outcome4–6, 10. In angiographic embolization, coils or pledgets are used to reduce splenic haemorrhage, by occlusion either of the proximal splenic artery or of more distal branches (Fig.2a,b). Proximal splenic artery embolization is thought to reduce the perfusion pressure in the spleen, thereby stopping bleeding and the risk of delayed rupture or rebleeding. Peripheral embolization stops bleeding more selectively and occludes pseudoaneurysms or arteriovenous fistulas7, 52.

Figure 2.

Angiography a with signs of ongoing bleeding before embolization and b after distal and proximal embolization

Liberal use of angioembolization has been reported to improve non-operative management rates and decrease failure rates3, 4, 43, 53. Recent studies including angiographic embolization have reported conservative treatment rates of 56–89 per cent, with success rates of 94–98 per cent, depending on the population4, 6–10. Wei and co-workers9 registered significantly fewer abdominal complications in patients who had angioembolization compared with those who had surgery (6 versus 36 per cent). In contrast to these reports, Harbrecht and colleagues54 compared two groups of conservatively treated patients, but failed to demonstrate improved success rates with the use of angioembolization. Duchesne et al.44 registered an increased incidence of acute respiratory distress syndrome in a group of patients managed by angiographic embolization compared with those treated by splenectomy, but the mortality rate was not significantly different. Some authors have been tempted to include haemodynamically less stable patients in the angioembolization protocols to increase the splenic salvage rate. Hagiwara and colleagues55 demonstrated that this could be done with the appropriate resources, but with a limited number of patients this remains a feasibility study that should be interpreted with caution.

The angioembolization procedure has inherent complications, such as risk of splenic infarction, splenic abscess, contrast-induced renal insufficiency, splenic bleeding, coil migration, fever and pleural effusion56. However, the risk of procedure-related complications should be weighed against complications associated with avoidable laparotomies9, 57.

Ultimately, the aim of angiographic embolization should be to optimize non-operative management rates safely, without increasing failure or complication rates, minimizing laparotomy rates while preserving splenic function. The overall level of evidence is low; most published studies are retrospective, with differences in protocols and clinical practice. Aggressive non-operative management protocols with liberal use of angioembolization are resource intensive but seem to be associated with high success rates. However, the optimal use of angioembolization has yet to be identified by a prospective randomized study and will always depend on the resources available at individual institutions.

Angioembolization and splenic immune function

Whether or not angioembolization impairs splenic function remains unknown. To date no specific marker of splenic immune function has been identified, and immune function is assessed by means of indirect tests of the spleen's viability, haemofiltrative and immunological functions58–63. Patients treated with splenic artery ligation, a technique comparable in effect to proximal splenic artery embolization, have been reported to have normal immunological outcome64. Bessoud and colleagues58 examined 24 patients after proximal angioembolization, reporting normal-sized and well perfused spleens with Howell–Jolly (HJ) bodies present in only two patients, and a sufficient immunoglobulin response to H. influenzae and pneumococci. Nakae and co-workers59 found no immunological advantage in patients undergoing angioembolization as part of non-operative management compared with those who had a splenectomy, in terms of levels of immunoglobulin (Ig)M, IgG and pneumococcus-serospecific IgM and IgG, complement factors and B cell subsets. However, significant differences in platelet count, HJ bodies, white blood cells, lymphocytes, total B and T cell counts, and serum IgG levels were noted. Tominaga et al.60 detected no significant immunological differences between 17 patients who had undergone angioembolization, nine splenectomy and ten healthy controls, except for higher cytotoxic T cell levels in those who had been splenectomized. Malhotra and co-workers61 reported that T cell subgroups after angioembolization in eight patients were similar to those in healthy controls. In a recent study from the authors' institution, there were no differences in lymphocyte subsets, total and pneumococcus-specific immunoglobulin counts, and HJ bodies between 15 patients who had undergone angioembolization and their matched healthy controls63. Ultrasound examination detected normal-sized and well perfused spleens after angioembolization (Fig. S1, supporting information)63, 64.

Existing studies on immune function after angioembolization are not sufficient for any firm conclusions to be drawn about preservation of splenic immunocompetence, but current knowledge seems to support the view that vaccination is unnecessary after embolization in most patients. Identifying a specific test of splenic function will be important for further studies. Patients undergoing splenectomy should be educated, vaccinated and receive prophylaxis according to existing protocols with the necessary follow-up20.

Disclosure

The authors declare no conflict of interest.

Supporting information

Additional supporting information may be found in the online version of this article:

Fig. S1 Contrast-enhanced ultrasound examination performed 2 months after embolization showing contrast defect as a sign of scarring in an otherwise perfused spleen (Word document)

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