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Ann Thorac Surg 2000;70:639-643
© 2000 The Society of Thoracic Surgeons

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Original articles: cardiovascular

Do peritoneal catheters remove pro-inflammatory cytokines after cardiopulmonary bypass in neonates?

^a Departments of Cardiothoracic Anesthesia, The Cleveland Clinic Foundation, Cleveland, Ohio, USA
^b Pediatric Critical Care, The Cleveland Clinic Foundation, Cleveland, Ohio, USA
^c Congenital Heart Surgery, The Cleveland Clinic Foundation, Cleveland, Ohio, USA

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
Background. Cardiopulmonary bypass (CPB) in neonates induces a cytokine-mediated capillary leak syndrome that can cause organ dysfunction. Removing harmful cytokines after CPB may attenuate this response. This study measured the concentrations of serum and peritoneal fluid (PF) cytokines after CPB to determine if harmful cytokines can be removed with peritoneal catheters.

Methods. Neonates (n = 18) had cardiac surgery using CPB with circulatory arrest. Peritoneal catheters were placed at the end of surgery to drain excess fluid. Serum samples were obtained before and after CPB, and PF after CPB. Cytokines were measured by enzyme-linked immunosorbent assay.

Results. Tumor necrosis factor- and interleukin-1ß (IL-1ß) were not detected in any serum or PF sample. Serum concentrations of IL-6, IL-8, and IL-10 increased significantly after CPB. PF concentrations of IL-6 and IL-8 exceeded serum concentrations, whereas IL-10 concentrations were higher in the serum. There was a significant negative correlation between serum and PF concentrations of IL-6 after CPB (r = -0.63; p < 0.05).

Conclusions. PF has very high concentrations of the proinflammatory cytokines, IL-6 and IL-8, after CPB but not the antiinflammatory cytokine IL-10. The PF may be a depot for the harmful inflammatory cytokines after CPB, and removing the PF could lower serum concentrations.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
Cardiopulmonary bypass (CPB) induces an acute systemic inflammatory response characterized by complement activation, adhesion molecule up-regulation, neutrophil activation, and release of the proinflammatory cytokines [1]. This post-CPB inflammatory response, also called "post-pump syndrome" or "capillary leak syndrome," is associated with pulmonary and myocardial dysfunction, renal failure, pancreatitis, and neurologic injury [2–5]. The inflammatory response, and associated organ dysfunction becomes clinically apparent approximately 3 to 6 hours after CPB. Neonates and infants may be particularly vulnerable to organ dysfunction from CPB because of their propensity for capillary leaking, particularly into the peritoneal cavity [6].

Efforts to diminish the circulating inflammatory mediators from CPB include preemptive therapies to diminish the inflammatory response and removal strategies to eliminate the inflammatory mediators once they are expressed. Corticosteroids, biocompatible coatings for the extracorporeal circuit, and monoclonal antibodies to specific cytokines, adhesion molecules, and complement factors have been used to attenuate the inflammatory response [7–9]. However, these preemptive strategies have not shown improved outcome, or are too expensive, unavailable, or too specific to inhibit the entire inflammatory cascade. Furthermore, complete suppression of the immune response is not desirable after open-heart surgery. Removal strategies such as leukocyte-depletion and ultrafiltration may be effective during bypass but cannot be used in the postoperative period when reperfusion injury processes are greatest [10].

We routinely place acute Tenckhoff catheters in the peritoneal cavity during cardiac surgery in neonates and infants to remove excess fluid. Removing excess fluid improves ventilation and renal and cardiac functions in the postoperative period [11–13]. Neonates typically accumulate fluid in the peritoneal cavity after CPB. We postulated that this fluid might contain cytokines as a result of the inflammatory response and subsequent capillary leakage. Furthermore, we hypothesized that the clinical improvement in organ function that we observed postoperatively is not only a result of the removal of excessive fluid, but perhaps the removal of the harmful cytokines. In this study, we report our analysis of cytokines in the peritoneal fluid and propose a novel technique to remove these proinflammatory mediators after cardiac surgery.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
The Institutional Review Board of the Cleveland Clinic Foundation approved this work and written consent was obtained from the parents of the patients. We studied 18 neonates undergoing open-heart surgery for hypoplastic left heart syndrome (n = 16) or interrupted aortic arch (n = 2). Anesthesia was induced with intravenous fentanyl (20 µg/kg), midazolam (0.125 mg/kg), and pancuronium (0.15 mg/kg) and was maintained with nitrous oxide and isoflurane before CPB and additional doses of fentanyl and midazolam during the operation. Isoflurane was also used while on CPB. Percutaneous arterial and central venous catheters were placed in all patients after induction of anesthesia. An infusion of morphine sulfate, 40 µg/kg/min, was given throughout the operation and postoperatively until extubation. All patients were given methylprednisolone, 20 mg/kg, and phenoxybenzamine, 0.25 mg/kg, before CPB.

Deep hypothermic CPB was used with nonpulsatile flow (Stockert-Shiley, Munich, Germany) at 150 to 220 ml/kg/min. At a nasopharyngeal temperature of 18°C, hypothermic circulatory arrest was used. A Cobe VPCML (Cobe Cardiovascular, Inc, Arvada, CO) membrane oxygenator was used in all patients. The pump circuit is primed in all neonates with fresh (< 24-hour-old) heparinized (2,500 U) whole blood, adjusted with Plasma-lyte 148 (Travenol Labs, Deerfield, IL) to achieve a mixture of the patient’s and prime hemoglobin of 9 g/dl; 10 mmol/liter of sodium bicarbonate; 50 ml D5W. Perfusion pressure was maintained at 35 to 40 mmHG while on CPB and hematocrit of 25% to 27%. Anticoagulation was achieved with heparin, 3 mg/kg, and was reversed with protamine, 3 to 4 mg/kg, after terminating CPB. The myocardium was protected with intermittent cold blood cardioplegia composed of oxygenated crystalloid cardioplegic solution containing 6 g% albumin. Conventional ultrafiltration was used in all patients with an ultrafiltrator (Hemocor Plus; Minitech Corp, Minneapolis, MN) placed in the bypass circuit. Ultrafiltration was started during the rewarming phase of CPB and terminated at the end of bypass. The volume of ultrafiltrate removed was equal to the volume of crystalloid added to the prime from the infused cardioplegia solution. The blood remaining in the circuit after termination of CPB was washed and centrifuged with a cell separator (Fresenius, Bad Hamburg, Germany) and transfused back into the patient as needed to achieve a hematocrit of 40 g%. All patients were weaned from CPB with dopamine at 5 µg/kg/min.

Acute Tenckoff catheters (41 cm; Sherwood Medical, Inc, Markham, Canada) were placed in the peritoneal cavity after terminating CPB, before closing the chest, and connected sterilely to a drainage bag.

Blood samples, 1 ml, were obtained from the internal jugular vein at the following times: postinduction before steroids, on CPB at the end of rewarming, post-CPB before protamine, and 1, 3, 6, 24, and 48 hours after CPB. Blood samples were collected in sterile vacutainer tubes with SST gel and clot activator (Becton Dickinson, Franklin Lakes, NJ) and were immediately centrifuged at 7,000 rpm for 10 minutes. Aliquots of serum were stored at -80°C until assayed. Peritoneal fluid samples (2 ml) were obtained at 1, 3, 6, 24, and 48 hours after CPB, centrifuged, and immediately frozen at -80°C. In 6 patients, urine samples were obtained at 6 and 24 hours after CPB and frozen at -80°C. In 3 patients, serum samples were obtained from the pump suckers at the end of CPB and the washed cell saver blood.

Tumor necrosis factor- (Tnf-), interleukin-(IL-)1ß, IL-6, IL-8, and IL-10 were determined in serum and PF using a specific biotinylated monoclonal antibody enzyme-linked immunosorbent assay (ELISA) according to the manufacturer’s directions (Endogen, Inc, Woburn, MA). According to the manufacturer, this assay detects the unbound, whole cytokine and not fragments. The sensitivity of this assay was less than 5 pg/ml for TNF- and IL-1ß, less than 3 pg/ml for IL-10, less than 2 pg/ml for IL-8, and less than 1 pg/ml for IL-6. Tnf- soluble receptor-I (SR) was similarly measured in the serum and peritoneal fluid of 10 patients only (R & D Systems, Minneapolis MN; sensitivity less than 1.5 pg/ml).

Outcome parameters, including time (hours) to extubation and discharge from the intensive care unit, were recorded in all patients. Time off inotropic support, defined as less than or equal to 2.0 µg/kg/min of dopamine or dubutamine and any dose of epinephrine or milrinone, were also recorded in all patients. The total peritoneal fluid drainage at 24 and 48 hours postoperatively was recorded for both groups.

Data is presented as mean ± standard error of mean. Because there are genetic variations to cytokine expression, the nonparametric Mann-Whitney rank sum test was used to compare variables between the groups. Analysis of variance (Sigma Stat; San Rafael, CA) was used to compare time points between groups. The Spearman rank correlation coefficient was assessed for correlation of independent parameters. A probability of less than 0.05 was considered statistically significant.

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
All patients were similar in weight and age. The demographic data is presented in Table 1. Three patients died (2 hypoplasts and 1 interrupted arch).

Most patients had serum concentrations less than 100 pg/ml of IL-6, 8, and 10 prior to surgery that, in all patients, increased significantly (p < 0.001) while on CPB and in the postoperative period. Serum concentrations of IL-10 were highest 1 hour after CPB, whereas IL-6 and IL-8 peaked 3 to 6 hours after CPB (Figs 1–3). All serum concentrations approached baseline by 48 hours. Samples obtained from the pump suckers also contained low levels of cytokines, IL-6 = 17 ± 6.2 pg/ml. Neither the ultrafiltrate nor the washed cell saver blood samples contained cytokines greater than 20 pg/ml.

View larger version (28K): [in this window] [in a new window]   Fig 1. Box plot of IL-6 concentrations in serum and peritoneal fluid (PF). Serum concentrations of IL-6 at 3 and 6 hours post-CPB were significantly higher ( p < 0.05; n = 18) than before CPB (Pre). All PF concentrations of IL-6 were significantly higher (*p < 0.001) than serum concentrations of IL-6 after CPB. (CPB = cardiopulmonary bypass.)

View larger version (32K): [in this window] [in a new window]   Fig 2. Box plot of IL-8 concentrations in serum and peritoneal fluid (PF). Serum concentrations of IL-8 were significantly higher ( p < 0.05; n = 18) at 3 and 6 hours post-CPB than before CPB (Pre). All PF concentrations of IL-8 were significantly greater than serum concentrations after CPB (*p < 0.05). (CPB = cardiopulmonary bypass.)

View larger version (18K): [in this window] [in a new window]   Fig 3. Box plot of IL-10 concentrations in serum and peritoneal fluid (PF). Serum IL-10 concentrations were significantly higher ( p < 0.01; n = 18) at 1, 3, and 6 hours after CPB compared to preoperative concentrations (Pre). PF concentrations of IL-10 were not significantly different from each other post-CPB. (CPB = cardiopulmonary bypass.)

The 3 patients who died had elevated serum concentrations of IL-6 before surgery: 99.5 ± 20.9 pg/ml versus 38.6 ± 7.2 pg/ml in the surviving patients. Elevated serum concentrations of IL-6 preoperatively, on CPB and 1 hour after CPB correlated with death (p < 0.01). None of the peritoneal fluid concentrations of cytokines correlated with survival or time to extubation, off inotropic support, or discharge from the intensive care unit (data not shown). Peritoneal and serum concentrations of IL-6 showed a negative correlation (-0.62, p < 0.05) indicating that peritoneal concentrations increased at 3 and 6 hours post-CPB as serum concentrations decreased (Fig 4). Serum IL-6 concentrations after CPB also correlated directly with the volume of PF collected in 24 hours (r = 0.54; p = 0.04).

View larger version (17K): [in this window] [in a new window]   Fig 4. Correlation of serum and peritoneal fluid (PF) concentrations of IL-6 at 6 hours post-CPB. Serum concentration of IL-6 decreases as PF concentration increases (r = -0.62; p = 0.04). (IL = interleukin.)

	Comment

Top Abstract Introduction Patients and methods Results Comment References

Our serum cytokine results are consistent with other reports of significantly elevated serum concentrations of IL-6 and IL-8 after CPB in neonates, infants, and children [9, 14, 15]. Also, our results are similar to other reports with respect to serum IL-10 reaching peak concentration 1 hour post-CPB [16]. Pretreatment with corticosteroids markedly enhances the early release of IL-10.

There are conflicting reports in the literature on Tnf- release after CPB. Adult patients are reported to have significant Tnf- release with CPB that is attenuated, but still measurable, with corticosteroid pretreatment [16, 17]. Another study in 21 infants (average age 17 months) found only traces of Tnf- in 2 patients [9]. Seghaye and colleagues reported concentrations of Tnf- at 30 pg/ml in 24 neonates prior to CPB that increased significantly to 60 pg/ml by 4 hours post-CPB [4]. All of their patients underwent the arterial switch operation using deep hypothermic circulatory arrest for TGA. In the present study, we did not detect Tnf- at any time in either serum or PF. Both Seghaye and coworkers’ study and the present study were in neonates having circulatory arrest, and both study groups received corticosteroids and prostaglandin E₁ before CPB. Both studies used similar assay techniques to measure Tnf-. The only obvious difference between these studies was the cohort of patients, hypoplasts versus transposition of the great arteries. It is possible that the ELISA technique used by Seghaye and colleagues detected fragments or bound Tnf- as well as the intact Tnf- protein. According to our sources at Endogen, Inc, the ELISA method used in our study measures only the unbound, intact cytokine and not fragments.

Although we did not measure any Tnf- in any of our samples, we did measure Tnf-SRI in both serum and PF. Tnf- needs to bind to its receptors in order to be effective. Mammalian cells can proteolytically cleave the Tnf- receptor from the cell membrane and they exist in the circulation as soluble receptors. Although the exact biologic role of the soluble receptors for Tnf- is not clear, they may serve as buffers that are capable of rapidly neutralizing the highly cytotoxic effects of Tnf- [18]. However, in the long-term, elevated levels of these receptors may be harmful by stabilizing Tnf- and slowly releasing it into the circulation. Elevated levels of Tnf- soluble receptors have been shown to correlate with adverse clinical outcome in heart failure patients [19]. The elevated serum and peritoneal concentrations (> 6,000 pg/ml) of Tnf-SRI in the 2 patients who died suggests that they had increased expression of Tnf- that was bound by the soluble receptors.

The inflammatory response usually follows a cascade of events beginning with the release of Tnf- and IL-1 that stimulate the release of the secondary mediators IL-6, IL-8, and IL-10 [20]. Unlike infectious triggers of inflammation, that usually include endotoxin, our results indicate that dramatic increases in IL-6 and IL-8 occur following heart surgery in neonates without detectable elevation of the early mediators.

Trauma or infection in the peritoneal cavity causes a local acute-phase reaction involving the release of cytokines that are synthesized by peritoneal mesothelial cells and macrophages [21]. The peritoneal inflammatory cascade is similar to the better-described systemic response. Peritonitis results in the local release of TNF- and IL-1, which stimulate the release of secondary mediators, IL-6, IL-8, and IL-10 [21]. Although it is tempting to attribute the elevated concentrations of IL-6 and IL-8 in peritoneal fluid as a response to the Tenkhoff catheter, this seems unlikely in that TNF- and IL-1 were not present in these samples, and IL-10 was present at low concentrations (1 to 3 hours post-CPB) when compared to the serum concentrations. Finally, the peritoneal concentrations increased and declined over time as did the serum samples. If the Tenckhoff catheter was responsible for the cytokine response, it seems unlikely that the concentration of IL-6 would decrease at 24 to 48 hours. Instead, our data suggests that the peritoneal cavity serves as a depot for the proinflammatory cytokines. Serum concentrations of IL-6 decrease as the PF concentrations increase (Fig 4).

The marked differences between the plasma and peritoneal concentrations of cytokines suggest that plasma cytokines do not equilibrate readily between the peritoneal space and blood, and that peritoneal cytokines do not diffuse easily into the systemic circulation. Alternatively, the peritoneal clearance of cytokines may be less effective than systemic clearance, and the elevated peritoneal concentrations of cytokines after CPB may represent a systemic spillover. Finally, since the molecular weight of the cytokines are similar (20 kDaltons for IL-10 and 26 kDaltons for IL-6), the peritoneum appears to be selectively permeable to the proinflammatory cytokines [20, 22].

This study is limited because there is no control group; that is, all patients have peritoneal catheters placed at the end of surgery to drain fluid. A control group without peritoneal catheters to compare serum cytokine concentrations under the same surgical conditions would be useful. However, our standard of care for this operation is to always place peritoneal catheters because of the other benefits already described [11–13].

We can only speculate about the significance of the results of this study and their practical implications. CPB is an abnormal circulation. Blood flow to the brain, gut, and kidneys decline significantly with hypothermic CPB. Diminished perfusion activates endothelial cells and neutrophils that decrease further the blood flow in the microcirculation and cause capillary leakage. Neonates are at particularly high risk for the development of edema and ascites as a result of microvascular protein leakage during CPB. The high peritoneal fluid volumes and cytokine concentrations in neonates with hypoplastic left heart syndrome may be a result of diminished splanchnic perfusion as a result of the shunt.

If cytokines are advantageous to the normal immune response, then the concept of "don’t block local cytokines," but rather remove excess cytokines from the systemic circulation may be true [23]. Under certain circumstances, however, cytokines probably cause persistent end-organ damage. The elimination of excessive amounts of intraperitoneal cytokines may be beneficial and is supported by decreased mortality of patients who were treated by staged abdominal repair, an operative strategy in which the abdominal cavity is purged every 24 hours [24]. Further outcome studies are needed to determine if removal of peritoneal fluid and cytokines by peritoneal dialysis improve organ function after CPB in neonates.

	Footnotes

 
This article has been selected for the open discussion forum on the STS Web site: http://www.sts.org/section/atsdiscussion/

	References

Top Abstract Introduction Patients and methods Results Comment References

 

1. Miller N.E., Levy J.H. The inflammatory response to cardiopulmonary bypass. J Cardiothorac Vasc Anesth 1997;11:355-366.[Medline]
2. Seghaye M.-C., Duchateau J., Grabitz R.G., et al. Complement activation during cardiopulmonary bypass in infants and children. J Thorac Cardiovasc Surg 1993;106:978-987.[Abstract]
3. Moat N.E., Shore D.F., Evans T.W. Organ dysfunction and cardiopulmonary bypass. Eur J Cardiothorac Surg 1993;7:563-573.[Abstract]
4. Seghaye M.-C., Grabitz R.G., Duchateau J., et al. Inflammatory reaction and capillary leak syndrome related to cardiopulmonary bypass in neonates undergoing cardiac operations. J Thorac Cardiovasc Surg 1996;112:687-697.[Abstract/Free Full Text]
5. Menasche P. The inflammatory response to cardiopulmonary bypass and its impact on postoperative myocardial function. Curr Opin Cardiol 1996;10:497-604.
6. Simpson J., Stephenson T. Regulation of extracellular fluid volume in neonates. Early Hum Dev 1993;34:926-931.
7. Butler J., Rocker G.M., Westaby S. Inflammatory response to cardiopulmonary bypass. Ann Thorac Surg 1993;55:552-559.[Abstract]
8. Hickey P.R., McGowan F.X. Adhesion molecules and inflammation. Anesth Analg 1995;81:1123-1124.[Medline]
9. Ashraf S., Tian Y., Cowan D., Entress A., Martin P.G., Watterson K.G. Release of proinflammatory cytokines during pediatric cardiopulmonary bypass. Ann Thorac Surg 1997;64:1790-1794.[Abstract/Free Full Text]
10. Elliot M.J. Ultrafiltration and modified ultrafiltration in pediatric open heart operations [Review]. Ann Thorac Surg 1993;56:1518-1522.[Abstract]
11. Stromberg D., Fraser C.D., Sorof J.M., Drescher K., Feltes T.F. Peritoneal dialysis. An adjunct to pediatric postcardiotomy fluid management. Tex Heart Inst J 1997;24:269-277.[Medline]
12. Dittrich S., Daehnert I., Vogel M., et al. Peritoneal dialysis after infant open heart surgery. Ann Thorac Surg 1999;68:160-163.[Abstract/Free Full Text]
13. Baden H.P., Morray J.P. Drainage of tense ascites in children after cardiac surgery. J Cardiothorac Vasc Anesth 1995;9:720-721.[Medline]
14. Khabar K.S., El Barbary M.A., Khouqeer F., Devol E., Al-Gain S., Al-Halees Z. Circulating endotoxin and cytokines after cardiopulmonary bypass. Clin Immunol Immunopathol 1997;85:97-103.[Medline]
15. Tarnok A., Hambsch J., Emmrich F., et al. Complement activation, cytokines, and adhesion molecules in children undergoing cardiac surgery with or without cardiopulmonary bypass. Pediatr Cardiol 1999;20:113-125.[Medline]
16. Tabardel Y., Duchateau J., Schmartz D., et al. Corticosteroids increase blood interleukin-10 levels during cardiopulmonary bypass in men. Surgery 1996;119:76-80.[Medline]
17. Jansen N.J.G., van Oeveren W., Broek L.V.D., et al. Inhibition by dexamethasone of the reperfusion phenomena in cardiopulmonary bypass. J Thorac Cardiovasc Surg 1991;102:515-525.[Abstract]
18. Kapadia S., Dibbs A., Kurrelmeyer K., et al. The role of cytokines in the failing human heart. Cardiol Clin 1998;16:645-656.[Medline]
19. Ferrari R., Bachetti T., Confortini R. Tumor necrosis factor soluble receptors in patients with various degrees of congestive failure. Circulation 1995;92:1479-1486.[Abstract/Free Full Text]
20. Abbas AK, Lichtman AH, Pober JS. Cytokines in cellular and molecular immunology, 2nd ed. Philadelphia: WB Saunders, 1994.
21. Tsukada K., Katoh H., Shiojima M., et al. Concentrations of cytokines in peritoneal fluid after abdominal surgery. Eur J Surg 1993;159:475-479.[Medline]
22. Moore K.W., O’Garra A., Mosmann T.R., et al. Interleukin-10. Annu Rev Immunol 1993;11:165-190.[Medline]
23. Natanson C., Hoffman W.D., Suffredini A.F., Eichacker P.Q., Lanner R.L. Selected treatment strategies for septic shock based on proposed mechanisms of pathogenesis. Ann Intern Med 1994;120:771-783.[Abstract/Free Full Text]
24. Wittmann D.H., Aprahamian C., Bergstein J.M., Bansal N., Wallace J.R., Wittmann M.M. Staged abdominal repair compares favorably to conventional operative therapy for intra-abdominal infections when adjusting for prognostic factors with a logistic model. Theor Surg 1994;25:273-284.

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This Article Abstract Full Text (PDF) Online Discussion Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Jonathan J. Drummond-Webb Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Bokesch, P. M. Articles by Mee, R. B.B. Search for Related Content PubMed PubMed Citation Articles by Bokesch, P. M. Articles by Mee, R. B.B.