Intraperitoneal cytokine response after major surgery: higher postoperative intraperitoneal versus systemic cytokine levels suggest the gastrointestinal tract as the major source of the postoperative inflammatory reaction

doi:10.1016/j.amjsurg.2003.12.019

The American Journal of Surgery

Volume 187, Issue 3, March 2004, Pages 372-377

https://doi.org/10.1016/j.amjsurg.2003.12.019 Get rights and content

Abstract

Background

Cytokine response is an important factor in the development of shock and organ failure. The aim of this study was to investigate intraperitoneal (peritoneal) and venous (systemic) postoperative cytokine release after major surgery.

Methods

Major abdominal surgery was performed in 19 patients. Preoperative systemic measurements and postoperative systemic and peritoneal measurements of C-reactive protein (CRP) and the cytokines tumor necrosis factor-alpha (TNF-α), interleukin (IL-6), and IL-10 were performed.

Results

Significantly higher TNF-α, IL-6, and IL-10 peritoneal values were recorded compared with systemic values, whereas peritoneal CRP was significantly decreased. CRP increased significantly over time, whereas postoperative values of IL-6, IL-10, and peritoneal TNF-α decreased. Systemic TNF-α was constant over time, but values after emergent abdominal surgery showed a more extensive response. An additional effect of surgery and emergent abdominal disease was seen in increased TNF-α and IL-10 levels.

Conclusions

Compared with systemic cytokines, peritoneal cytokines respond extensively after major surgery, indicating that measurement of peritoneal cytokines is a more sensible method to determine postoperative inflammatory reaction. A normal postoperative course is characterized by decreasing levels of peritoneal cytokines.

Section snippets

Methods

Nineteen patients were included, 17 men and two women, age 20 to 83 years (median 73). Because of the different surgeries performed, we divided the patients three groups. Group A was composed of a homogenous group of patients who underwent elective cancer recti surgery; group B included patients who underwent emergency surgery; and group C was a heterogeneous group of patients who underwent different types of surgery. In group A, nine patients underwent elective rectal resection for treatment

Results

Peritoneal TNF-α, IL-6, and IL-10 values were greater (P < 0.001) and peritoneal CRP values were lower (P < 0.001) compared with their systemic counterparts. There were significant correlations (P < 0.001) both systemically and peritoneally between TNF-α, IL-6, and IL-10 (Table 1, Table 2) (Pearson's correlation coefficient).

CRP

After surgery, systemic CRP (Fig. 1A through C and Table 3) increased for 30 hours and was then constant. Peritoneal values were lower and increased until 45 hours. The increases were significant (P < 0.001). The interaction effect over time between systemic and peritoneal curves was also significant (P = 0.002).

TNF-α

Systemic TNF-α level (Fig. 1D through F and Table 3) was normal in groups A and C, whereas it increased in group B (P = 0.04). Systemic TNF-α was unchanged over time compared with peritoneal TNF-α, which—except for a small increase to postoperative hour 9 in group B–decreased continuously until 45 hours. The interaction effect over time between systemic and peritoneal values was significant (P < 0.001). Peritoneal TNF-α was numerically slightly higher in group A compared with group C.

IL-6

Groups A and C both showed systemic IL-6 values (Fig. 1G through I and Table 3) within the normal range before surgery. Highest values, both systemic and peritoneal, were seen between 3 and 9 hours after surgery. Peritoneal sampling showed IL-6 values that where 100-fold higher than systemic values. In group B, the first sampling after three postoperative hours was two to three times higher than in groups A and C. Peritoneal as well as systemic IL-6 values decreased significantly over time (P <

IL-10

Both peritoneal and systemic IL-10 values (Fig. 1J though L and Table 3) decreased significantly over time (P < 0.001). Systemic IL-10 showed the same pattern in groups A and C, with a fourfold increase from before surgery until nine hours after surgery. Peritoneal values in group B started were increased before surgery compared with groups A and C and decreased during 33 hours. Values in groups A and C increased initially and then decreased subsequently as they did group B. The interaction

Clinical outcome

Sixteen patients had an uneventful postoperative course, and 3 patients suffered postoperative complications. One patient in group B developed shock and multiorgan failure and died 42 hours after surgery. One patient in group A underwent a second surgery on postoperative day 10 to treat an anastomotic leakage, and one patient in group C underwent a second surgery to treat an abdominal abscess. Neither of these two patients with late complications showed a cytokine response differing from the

Comments

Previous studies have found correlations between the severity of septicemia [15], peritonitis [16], [17], [18], [19], [20], and systemic proinflammatory cytokines and IL-10. A correlation also exists between levels of proinflammatory cytokines and length of surgery [21], [22], blood loss, and bacterial count [23]. Furthermore, an correlation has been shown between IL-6, IL-10, and postsurgical complications [24]. The severity of the disease correlates with IL-10, and it has been described that

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Scientific paperIntraperitoneal cytokine response after major surgery: higher postoperative intraperitoneal versus systemic cytokine levels suggest the gastrointestinal tract as the major source of the postoperative inflammatory reaction

Abstract

Background

Methods

Results

Conclusions

Section snippets

Methods

Results

CRP

TNF-α

IL-6

IL-10

Clinical outcome

Comments

J Surg Res

J Gastrointest Surg

Am J Surg

Am J Surg

Gastroenterology

Splanchnic ischaemia and its role in multiple organ failure

Acta Anaesthesiol Scand

Gut ischemia and mesenteric synthesis of inflammatory cytokines after hemorrhagic or endotoxic shock

Am J Physiol

The relationship between visceral ischemia, proinflammatory cytokines, and organ injury in patients undergoing thoracoabdominal aortic aneurysm repair

Crit Care Med

Cytokines as mediators in the pathogenesis of septic shock

Curr Top Microbiol Immunol

The inflammatory basis of trauma/shock-associated multiple organ failure

Inflamm Res

Interleukin-6 mediates host defense responses induced by abdominal surgery

Surgery

Role of the gut in multiple organ failurebacterial translocation and permeability changes

World J Surg

Interleukin 10 reduces mortality from severe peritonitis in mice

Antimicrob Agents Chemother

Scientific paper
Intraperitoneal cytokine response after major surgery: higher postoperative intraperitoneal versus systemic cytokine levels suggest the gastrointestinal tract as the major source of the postoperative inflammatory reaction