ATS
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Eugene A. Grossi
Miguel G. Aguinaga
Bryan M. Steinberg
Michael Artman
Aubrey C. Galloway
Stephen B. Colvin
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Grossi, E. A.
Right arrow Articles by Colvin, S. B.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Grossi, E. A.
Right arrow Articles by Colvin, S. B.

Ann Thorac Surg 2000;70:191-196
© 2000 The Society of Thoracic Surgeons

Original articles: Cardiovascular

Impact of heparin bonding on pediatric cardiopulmonary bypass: a prospective randomized study

Eugene A. Grossi, MDa, Klaus Kallenbach, MDa, Sophie Chau, MDa, Christopher C. Derivaux, MDa, Miguel G. Aguinaga, MDa, Bryan M. Steinberg, MDa, David Kim, BAa, Shilesh Iyer, BAa, Majid Tayyarah, BAa, Michael Artman, MDb, Aubrey C. Galloway, MDa, Stephen B. Colvin, MDa

a Division of Cardiothoracic Surgery, Tisch Hospital, New York University School of Medicine, New York, New York, USA
b Division of Pediatric Cardiology, Tisch Hospital, New York University School of Medicine, New York, New York, USA

Address reprint requests to Dr Grossi, Department of Surgery, New York University Medical Center, 530 First Ave, Suite 9V, New York, NY 10016
e-mail: grossi{at}cv.med.nyu.edu


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Heparin-coated circuits reduce the inflammatory response to cardiopulmonary bypass in adult patients; however, little is known about its effects in the pediatric population. Two studies were performed to assess this technology’s impact on inflammation and clinical outcomes.

Methods. In a pilot study, complement and interleukins were measured in 19 patients who had either uncoated cardiopulmonary bypass circuits or heparin-bonded circuits. Subsequently, 23 additional patients were studied in a randomized fashion. Respiratory function and blood product utilization were recorded.

Results. In the pilot study, heparin-bonded circuit patients had less complement 3a (p < 0.001) and interleukin-8 (p < 0.05) compared with uncoated cardiopulmonary bypass circuit patients. The randomized study revealed that the heparin-bonded circuit was associated with reduced complement 3a (p = 0.02). Multiple variable analysis revealed that the following postoperative variables were increased with bypass time (p = 0.01) and diminished with heparin-bonded circuits: interleukins (p = 0.01), peak airway pressures (p = 0.05), and prothrombin time (p = 0.03).

Conclusions. Heparin-bonded circuits significantly reduce cytokines and complement during cardiopulmonary bypass and lower interleukin levels postbypass; they were also associated with improved pulmonary and coagulation function. Heparin-bonded circuits ameliorate the systemic inflammatory response in pediatric patients from cardiopulmonary bypass.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Although cardiopulmonary bypass (CPB) has been in use for more than 40 years, significant morbidity continues to be associated with the contact of blood with the artificial surfaces of the bypass circuit. An increasing body of evidence suggests that these adverse responses are similar to the systemic inflammatory response syndrome evoked by sepsis or trauma [1], which is characterized by hypotension, coagulopathy, adult respiratory distress syndrome, and multiple system organ failure [2]. The common mechanism appears to involve the activation of a number of biological pathways, including the complement, coagulation, and fibrinolytic system cascades, as well as platelet activation [3]. Several studies have reported that the mediators of these pathways are elevated during CPB [4–6], most likely because of contact activation of the blood elements with the bypass circuit. Pediatric patients are at particular risk for the development of systemic inflammatory response syndrome and multiple system organ failure after CPB [4, 5, 7, 8] with an observed incidence of 3.5% and an associated 44% mortality [7]. Studies have demonstrated that interleukin (IL)-8 is significantly elevated in pediatric CPB and may also be responsible for capillary leak. This elevation of IL-8 correlates with length of time on bypass [9].

In adults the use of a heparin-bonded bypass circuit diminishes activation because of blood contact with the artificial surface resulting in the reduction of both complement activation [10] and cytokine release [11–14]. Because pediatric patients have a greater bypass circuit surface area to blood volume ratio than adult patients, we proposed that heparin coating of pediatric bypass circuits might provide even greater benefit than that appreciated in adults. In nonblinded, randomized studies, interleukins, postoperative body temperature, soluble E-selectin, and ß-thromboglobulin have been shown to be improved with heparin-bonded oxygenators in a pediatric population [15, 16]. Because little information is available on clinical outcomes, however, we undertook a surgeon-blinded, randomized study to investigate the impact of heparin-bonded bypass circuits in pediatric patients.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Pilot nonrandomized study
Nineteen pediatric patients (median age, 6.6 months) underwent heart operations requiring CPB at Tisch Hospital, NYU School of Medicine. The patients were divided into two groups without any selection criteria other than the availability of the heparin-bonded pump circuits (Table 1). As a result, standard extracorporeal circulation was performed in 7 patients using a conventional membrane oxygenator, pump pack, and centrifugal pump (uncoated cardiopulmonary bypass circuit group). Twelve patients were perfused with a circuit that was identical except for covalent heparin bonding of the tubing, pump, oxygenator, and cannulas (Medtronic, Minneapolis, MN) (HBCPB group). All patients had standard systemic heparinization (4 mg/kg) with activated clotting times being maintained at greater than 450 seconds during CPB.


View this table:
[in this window]
[in a new window]
  		Table 1. Diagnoses of Patients in Studies Undergoing Repair Using Cardiopulmonary Bypass With or Without a Covalently Bonded Heparin-Coated Bypass Circuit

 
Subsequent randomized, blinded study
Subsequently, 23 additional patients (median age, 13.3 months) undergoing heart operations requiring CPB were studied in our institution. Informed consent for the randomization process was obtained from guardians. Just before operating room setup, the randomization process was performed based on a random number sequence generator. The perfusionists were informed as to which equipment to use; the surgeon was never informed. Both studies were performed with the approval of the Institutional Review Board. In neither study did patients receive aprotinin or steroids. Where blood cardioplegia was used, the cardioplegia mixing device was not heparin coated. Cardiopulmonary bypass was conducted typically at 22°C; core body temperature was lowered to 17°C for patients undergoing circulatory arrest.

Blood collection and processing
Blood samples were obtained after the induction of anesthesia, at 30-minute intervals during CPB, and at 1 and 24 hours after completion of CPB. Serum was separated, preserved with aprotinin, and stored at -70°C. Serum cytokine levels of IL-1ß0, IL-6, and IL-8 and serum complement levels C3a and C5a were later batch-analyzed using enzyme-linked immunosorbent assay (cytokines: R&D Systems, Minneapolis, MN; complement: Quidel, San Diego, CA). Each assay was performed in duplicate with the mean result being used for statistical analysis. The postoperative pulmonary function was studied in the recovery room in the randomized group of patients.

Pulmonary function analysis
All patients had arterial and venous blood gas analysis along with static airway compliance measured upon admission to the recovery room; no children were extubated in the operating room. Ventilatory management was performed with pressure control ventilators. Patients with residual shunts were excluded from A-a gradient calculations.

Statistical analysis
Data were tabulated and analyzed on a computer using SPSS for Windows (SPSS, Inc, Chicago, IL). Demographic data were analyzed with the nonpaired Student’s t test for continuous variables. Repeated measures analysis of variance was used to analyze serologic data from samples obtained after 60 minutes of CPB with significance being accepted at a level of 0.05 or less. Samples obtained at intervals beyond 60 minutes of bypass were not included in the repeated measures analysis because of an insufficient number of specimens in this time range. For comparisons of clinical indicators the nonpaired Student’s t test was performed on continuous variables, and {chi}2 testing was performed for ordinal variables. A nonparametric test (Mann-Whitney) was also used for analysis when the normal distribution assumption was violated. General linear modeling (SPSS) was used for analysis of variance, covariance, and regression for multiple variable analysis and repeated measures analysis of variance.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Initial, nonrandomized study
Nineteen patients underwent CPB for the diagnoses listed in Table 1. There was no statistical difference between the treatment groups with respect to age, aortic cross-clamp time, or length of CPB (Table 2). There was a greater (but nonsignificant) proportion of female patients in the HBCPB group.


View this table:
[in this window]
[in a new window]
  		Table 2. Patient Demographics (Mean ± SD)

 
Serologic results are presented in Table 3. Serum C3a levels increased during CPB in the uncoated cardiopulmonary bypass circuit group and returned toward baseline 24 hours after bypass. However, patients in the HBCPB group did not have a significant increase in C3a levels (p < 0.05) (Fig 1). In contrast, serum C5a did not increase over baseline levels in either group (Table 3). Serum IL-8 levels increased in both groups during CPB (Fig 2). The patients with HBCPB were noted to have significantly lower production of IL-8 compared to the uncoated cardiopulmonary bypass circuit patients (p < 0.01), with 51% lower serum levels measured at 60 minutes. There was a significant elevation in serum IL-6 levels in both groups over time (p < 0.01), but no difference was observed between treatment groups. Serum IL-1 levels did not increase in either patient group during or after CPB (Table 3).


View this table:
[in this window]
[in a new window]
  		Table 3. Serum Complement and Cytokine Levels Before, During, and After Cardiopulmonary Bypass in Pilot Study Group

 


View larger version (24K):
[in this window]
[in a new window]
  		Fig 1. Serum complement C3a level in the standard bypass circuit groups increased significantly over baseline as compared to the heparin-bonded cardiopulmonary bypass group (p < 0.05), reaching a maximum value at 90 minutes after the institution of cardiopulmonary bypass and returning to baseline at 24 hours.

 


View larger version (25K):
[in this window]
[in a new window]
  		Fig 2. Serum IL-8 levels increased in both groups but to a significantly lesser degree in the heparin-bonded cardiopulmonary bypass group (p < 0.05).

 
Subsequent randomized, blinded study
Twelve patients were randomized to the uncoated cardiopulmonary bypass circuit treatment and 11 patients to HBCPB; the diagnoses are listed in Table 1. CPB time was significantly longer (28 minutes) in the HBCPB patients (p = 0.01); this variable was introduced into further multiple variable analyses. Group demographics are listed in Table 2. Serologic analysis revealed a significant reduction during bypass in the C3a, IL-6, and IL-8 levels associated with the treatment (Table 4). In addition to the effect of circuit coating, the duration of CPB was associated with significantly higher interleukin levels (p < 0.001 for IL-6 and IL-8). This effect of duration of bypass time was not noted for C3a levels.


View this table:
[in this window]
[in a new window]
  		Table 4. Serum Complement and Cytokine Levels Before, During, and After Cardiopulmonary Bypass in the Randomized Study Group

 
There was one death in each treatment group and, therefore, these patients could not be included in some of these analyses. Blood usage was similar in the two treatment groups as listed in Table 5. Nonparametric and multiple variable analysis did not reveal a significant difference associated with heparin coating. Multiple variable analysis revealed that 24-hour postoperative prothrombin time was significantly elevated by the use of uncoated cardiopulmonary bypass circuits (15.7 versus 13.3 seconds; p = 0.04, estimated at a covariate bypass time of 100.0 minutes).


View this table:
[in this window]
[in a new window]
  		Table 5. Univariate and Multiple Variable Analysis of Intraoperative and Postoperative Blood and Blood Product Usage and Hematologic Profile in the Randomized Study Groups

 
Univariate analysis of initial postoperative static airway compliance, peak airway pressure, alveolar–arterial gradient, and time-to-extubation are listed in Table 6. Two patients in the nonheparin-coated group required nitric oxide therapy, which was started intraoperatively; nitric oxide was not required in any of the HBCPB patients. Multiple variable analysis of recovery room peak airway pressures revealed an increase associated with longer bypass times (ß = 0.131; p = 0.01) and a decrease of 5.0 cm H20 associated with HBCPB (mean covariate bypass time of 100 minutes; p = 0.05).


View this table:
[in this window]
[in a new window]
  		Table 6. Univariate and Multiple Variable Analysis of Postoperative Pulmonary Function in the Randomized Study Groupsa

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
Although CPB is routinely performed without significant clinical sequelae, a small percentage of patients go on to develop a generalized systemic inflammatory response that is clinically similar to the systemic inflammatory response syndrome seen in sepsis and trauma [1, 17]. The pathogenesis of this process is multifactorial and involves the activation of the coagulation, fibrinolytic, complement, and contact system cascades. This activation results in the release of cytokines, chemoattraction of neutrophils, and expression of vascular adhesion molecules [18, 19]. Subsequently, leukocytes and platelets are recruited and activated and adhere to the microvasculature. Oxygen-free radicals are generated and endothelial injury results [17].

Pediatric patients are particularly susceptible to such damaging effects of extracorporeal circulation. The pediatric patient’s smaller blood volume has a relatively greater percentage of contact with the bypass circuit surfaces than in the adult patient; this increased exposure may cause greater activation of the inflammatory cascades. The immaturity of pediatric organ systems may also play a role. Pediatric patients have an increased propensity to develop capillary leakage and postoperative edema [20], especially those patients with prolonged bypass times [15, 19]. Neonatal patients also have abnormal activity of the complement cascade [7] and an immature immune response system, both of which may increase the risk of cellular injury associated with CPB. Therefore, increasing the "biocompatibility" of the bypass circuit for pediatric patients could theoretically blunt the activation of the systemic inflammatory response and reduce postoperative morbidity.

The results of this study showed a significant increase in C3a levels in the standard bypass circuit group as compared to the heparin-coated circuit during bypass. A similar effect of HBCPB has been reported in adults [13, 14]. The exact mechanism for the inhibition of C3a activation is unknown, but inhibition may occur through the classic pathway or the alternative pathway [12]. This inhibition of complement production can have important implications as C3a is a potent stimulus for the release of IL-6 and IL-1 and causes neutrophil degranulation [21]. Furthermore, C3a is an anaphylatoxin and can lead to cardiac dysfunction [22]. We failed to observe increased C5a levels during bypass in our first study. Seghaye and colleagues [5] reported increased C5a levels at the end of bypass, but did not include any baseline values for comparison. In addition, C5a is avidly bound by neutrophils, and its production at low concentrations may be masked by this effect [11].

Proinflammatory cytokines are elevated in adult [11, 23] and pediatric patients [9] after CPB. IL-8 is a powerful chemoattractant, which induces pulmonary sequestration of neutrophils as seen in acute respiratory distress syndrome [9]. IL-8 is released in response to injury and is elevated in pediatric patients after CPB. Our results demonstrate that IL-8 production during CPB can be markedly reduced with HBCPB. IL-6 is a marker of inflammation and has prognostic value in septic shock patients [24]. IL-6 is induced by complement, with the serum concentration lagging 2 to 3 hours behind the complement peak. In this study the IL-6 levels increased in both groups and remained elevated 24 hours later. Thus, use of HBCPB did not affect IL-6 production in these patients. IL-1 is an endogenous pyrogen, which results in the production of adhesion molecules [25] and increases the synthesis of other inflammatory mediators. Serum IL-1 was not elevated in either patient group during or after CPB. This result is consistent with previous findings in adult patients [11, 23, 26]. However, elevated IL-1 levels have been found in monocytes with a peak at 24 hours after CPB [27], and IL-1 may still prove to play a significant role in the systemic inflammatory response after CPB.

Our randomized study revealed significant differences in the postoperative clinical outcomes associated with the use of heparin-coated bypass circuits. These differences included improvement of recovery room respiratory function and postoperative coagulation status. The difference in postoperative respiratory function confirms a clinical pulmonary advantage previously described by Ashraf and associates [15], who demonstrated that the use of heparin-coated oxygenators was significantly associated with decreased ventilator time. These findings are not sufficiently detailed to allow calculation of a cost-to-benefit ratio of the heparin coating. This heparin coating technology, however, has demonstrated a clinical advantage in the care of pediatric bypass patients.

The limitations of this study were the relatively small number of patients in each group. However, the number of patients used in this study was chosen based on our experience in adults [28] to have sufficient power to delineate differences in complement activation and cytokine production. The pilot study we performed was designed to determine the validity of the concept and the feasibility of demonstrating such serologic differences. The second study was performed in a surgeon-blinded, randomized fashion to confirm the results of the first study. Although we did not detect trends or differences in transfusion requirements between the treatment groups in the second study, it is possible that the power of the test was insufficient given the diversity of our patient population. Whereas a much larger randomized study would be necessary to demonstrate all possible clinical benefits of heparin coating of bypass circuits for pediatric patients, it is questionable whether such a study could now be ethically performed.

In conclusion, these results demonstrate that a covalently bonded coating of heparin on CPB circuits can reduce the release of several mediators and markers of inflammation in pediatric patients. Use of HBCPB prevented complement activation and blunted production of inflammatory cytokines. The use of heparin-bonded circuits during CPB in pediatric patients has the potential to decrease postoperative complications which are associated with a bypass-related systemic inflammatory response, such as bleeding and pulmonary dysfunction. Therefore, this technology has the potential to lower the risks of cardiac operations in infants and children.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. Butler J., Rocker G.M., Westaby S. Inflammatory response to cardiopulmonary bypass. Ann Thorac Surg 1993;55:552-559.[Abstract]
  2. Moore FA ME. Evolving concepts in the pathogenesis of postinjury multiple organ failure. Surg Clin North Am 1995; 75:257–77.
  3. Balk R.A., Bone R.C. The septic syndrome. Definition and clinical implications. Crit Care Clin 1989;5:1-8.[Medline]
  4. Seghaye M.C., Engelhardt W., Grabitz R.G., et al. Multiple system organ failure after open heart surgery in infants and children. Thorac Cardiovasc Surg 1993;41:49-53.[Medline]
  5. Seghaye M.C., Duchateau J., Grabitz R.G., et al. Complement, leukocytes, and leukocyte elastase in full-term neonates undergoing cardiac operation. J Thorac Cardiovasc Surg 1994;108:29-36.[Abstract/Free Full Text]
  6. Korn R.L., Fisher C.A., Livingston E.R., et al. The effects of Carmeda Bioactive Surface on human blood components during simulated extracorporeal circulation. J Thorac Cardiovasc Surg 1996;111:1073-1084.[Abstract/Free Full Text]
  7. Seghaye M.C., Duchateau J., Grabitz R.G., et al. Complement activation during cardiopulmonary bypass in infants and children. Relation to postoperative multiple system organ failure. J Thorac Cardiovasc Surg 1993;106:978-987.[Abstract]
  8. Rinder C.S., Bonan J.L., Rinder H.M., Mathew J., Hines R., Smith B.R. Cardiopulmonary bypass induces leukocyte-platelet adhesion. Blood 1992;79:1201-1205.[Abstract/Free Full Text]
  9. Finn A., Naik S., Klein N., Levinsky R.J., Strobel S., Elliott M. Interleukin-8 release and neutrophil degranulation after pediatric cardiopulmonary bypass. J Thorac Cardiovasc Surg 1993;105:234-241.[Abstract]
  10. Videm V., Svennevig J.L., Fosse E., Semb G., Osterud A., Mollnes T.E. Reduced complement activation with heparin-coated oxygenator and tubings in coronary bypass operations. J Thorac Cardiovasc Surg 1992;103:806-813.[Abstract]
  11. Steinberg J.B., Kapelanski D.P., Olson J.D., Weiler J.M. Cytokine and complement levels in patients undergoing cardiopulmonary bypass. J Thorac Cardiovasc Surg 1993;106:1008-1016.[Abstract]
  12. Gu Y.J., van Oeveren W., Akkerman C., Boonstra P.W., Huyzen R.J., Wildevuur C.R. Heparin-coated circuits reduce the inflammatory response to cardiopulmonary bypass. Ann Thorac Surg 1993;55:917-922.[Abstract]
  13. Pekna M., Hagman L., Halden E., Nilsson U.R., Nilsson B., Thelin S. Complement activation during cardiopulmonary bypass. Ann Thorac Surg 1994;58:421-424.[Abstract]
  14. Fosse E., Moen O., Johnson E., et al. Reduced complement and granulocyte activation with heparin-coated cardiopulmonary bypass. Ann Thorac Surg 1994;58:472-477.[Abstract]
  15. 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]
  16. Schreurs H.H., Wijers M.J., Gu Y.J., et al. Heparin-coated bypass circuits. effects on inflammatory response in pediatric cardiac operations. Ann Thorac Surg 1998;66:166-171.[Abstract/Free Full Text]
  17. Casey L.C. Role of cytokines in the pathogenesis of cardiopulmonary-induced multisystem organ failure. Ann Thorac Surg 1993;56:S92-S96.
  18. Kilbridge P.M., Mayer J.E., Newburger J.W., Hickey P.R., Walsh A.Z., Neufeld E.J. Induction of intercellular adhesion molecule-1 and E-selectin mRNA in heart and skeletal muscle of pediatric patients undergoing cardiopulmonary bypass. J Thorac Cardiovasc Surg 1994;107:1183-1192.[Abstract/Free Full Text]
  19. Moat N.E., Rebuck N., Shore D.F., Evans T.W., Finn A.H. Humoral and cellular activation in a simulated extracorporeal circuit. Ann Thorac Surg 1993;56:1509-1514.[Abstract]
  20. 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]
  21. Haeffner-Cavaillon N., Kazatchkine M.D. Induction of interleukin-1 synthesis. A new criterion of biocompatibility of extracorporeal circuits. Presse Med 1991;20:797-801.
  22. Downing S.W., Edmunds L.H., Jr Release of vasoactive substances during cardiopulmonary bypass. Ann Thorac Surg 1992;54:1236-1243.[Abstract]
  23. Kalfin R.E., Engelman R.M., Rousou J.A., et al. Induction of interleukin-8 expression during cardiopulmonary bypass. Circulation 1993;88:II401-II406.
  24. Damas P., Ledoux D., Nys M., et al. Cytokine serum level during severe sepsis in human IL-6 as a marker of severity. Ann Surg 1992;215:356-362.[Medline]
  25. Hailer N.P., Blaheta R.A., Harder S., Scholz M., Encke A., Markus B.H. Modulation of adhesion molecule expression on endothelial cells by verapamil and other Ca++ channel blockers. Immunobiology 1994;191:38-51.[Medline]
  26. Hennein H.A., Ebba H., Rodriguez J.L., et al. Relationship of the proinflammatory cytokines to myocardial ischemia and dysfunction after uncomplicated coronary revascularization. J Thorac Cardiovasc Surg 1994;108:626-635.[Abstract/Free Full Text]
  27. Haeffner-Cavaillon N., Roussellier N., Ponzio O., et al. Induction of interleukin-1 production in patients undergoing cardiopulmonary bypass. J Thorac Cardiovasc Surg 1989;98:1100-1106.[Abstract]
  28. Steinberg B.M., Grossi E.A., Schwartz D.S., et al. Heparin bonding of bypass circuits reduces cytokine release during cardiopulmonary bypass. Ann Thorac Surg 1995;60:525-529.[Abstract/Free Full Text]
Accepted for publication December 30, 1999.




This article has been cited by other articles:


Home page
 Asian Cardiovasc. Thorac. Ann.Home page
G. Furlanetto, C. H Passerino, R. Siegel, D. T Chueng, S. Levitsky, and I. S J Casagrande
Biointegration and Growth of Porcine Valved Pulmonary Conduits in a Sheep Model
Asian Cardiovasc Thorac Ann, August 1, 2009; 17(4): 350 - 356.
[Abstract] [Full Text] [PDF]

Home page
 Anesth. Analg.Home page
G. S. Murphy, E. A. Hessel II, and R. C. Groom
Optimal Perfusion During Cardiopulmonary Bypass: An Evidence-Based Approach
Anesth. Analg., May 1, 2009; 108(5): 1394 - 1417.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Thorac. Surg.Home page
R. Eggum, T. Ueland, T. E. Mollnes, V. Videm, P. Aukrust, A. E. Fiane, and H. L. Lindberg
Effect of Perfusion Temperature on the Inflammatory Response During Pediatric Cardiac Surgery
Ann. Thorac. Surg., February 1, 2008; 85(2): 611 - 617.
[Abstract] [Full Text] [PDF]

Home page
 Eur. J. Cardiothorac. Surg.Home page
O. Mangoush, S. Purkayastha, S. Haj-Yahia, J. Kinross, M. Hayward, F. Bartolozzi, A. Darzi, and T. Athanasiou
Heparin-bonded circuits versus nonheparin-bonded circuits: an evaluation of their effect on clinical outcomes
Eur. J. Cardiothorac. Surg., June 1, 2007; 31(6): 1058 - 1069.
[Abstract] [Full Text] [PDF]

Home page
 Anesth. Analg.Home page
M. E. Jessen
Pro: Heparin-Coated Circuits Should be Used for Cardiopulmonary Bypass
Anesth. Analg., December 1, 2006; 103(6): 1365 - 1369.
[Full Text] [PDF]

Home page
 Anesth. Analg.Home page
R. Taneja and D. C. Cheng
Con: Heparin-Bonded Cardiopulmonary Bypass Circuits Should Be Routine for All Cardiac Surgical Procedures
Anesth. Analg., December 1, 2006; 103(6): 1370 - 1372.
[Full Text] [PDF]

Home page
 PerfusionHome page
S W Sutton, A N Patel, V A Chase, L A Schmidt, E K Hunley, L W Yancey, R F Hebeler, E H Cheung, A C Henry III, T P Meyers, et al.
Clinical benefits of continuous leukocyte filtration during cardiopulmonary bypass in patients undergoing valvular repair or replacement
Perfusion, January 1, 2005; 20(1): 21 - 29.
[Abstract] [PDF]

Home page
 PerfusionHome page
M. J. Scallan
Cerebral injury during paediatric heart surgery: perfusion issues
Perfusion, July 1, 2004; 19(4): 221 - 228.
[Abstract] [PDF]

Home page
 J. Thorac. Cardiovasc. Surg.Home page
A. Boning, J. Scheewe, T. Ivers, C. Friedrich, J. Stieh, S. Freitag, and J. T. Cremer
Phosphorylcholine or heparin coating for pediatric extracorporeal circulation causes similar biologic effects in neonates and infants
J. Thorac. Cardiovasc. Surg., May 1, 2004; 127(5): 1458 - 1465.
[Abstract] [Full Text] [PDF]

Home page
 Anesth. Analg.Home page
M. J. Eisses, K. Seidel, G. S. Aldea, and W. L. Chandler
Reducing Hemostatic Activation During Cardiopulmonary Bypass: A Combined Approach
Anesth. Analg., May 1, 2004; 98(5): 1208 - 1216.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Thorac. Surg.Home page
E. Jensen, S. Andreasson, A. Bengtsson, H. Berggren, R. Ekroth, L. E. Larsson, and J. Ouchterlony
Changes in hemostasis during pediatric heart surgery: impact of a biocompatible heparin-coated perfusion system
Ann. Thorac. Surg., March 1, 2004; 77(3): 962 - 967.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Thorac. Surg.Home page
E. Jensen, S. Andreasson, A. Bengtsson, H. Berggren, R. Ekroth, L. Lindholm, and J. Ouchterlony
Influence of two different perfusion systems on inflammatory response in pediatric heart surgery
Ann. Thorac. Surg., March 1, 2003; 75(3): 919 - 925.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Thorac. Surg.Home page
E. R. Stephenson Jr and J. L. Myers
Pediatric cardiopulmonary bypass
Ann. Thorac. Surg., December 1, 2001; 72(6): 2176 - 2177.
[Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Eugene A. Grossi
Miguel G. Aguinaga
Bryan M. Steinberg
Michael Artman
Aubrey C. Galloway
Stephen B. Colvin
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Grossi, E. A.
Right arrow Articles by Colvin, S. B.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Grossi, E. A.
Right arrow Articles by Colvin, S. B.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
ANN THORAC SURG ASIAN CARDIOVASC THORAC ANN EUR J CARDIOTHORAC SURG
J THORAC CARDIOVASC SURG ICVTS ALL CTSNet JOURNALS