Risk factors of sepsis after open congenital cardiac surgery in infants: a pilot study

Dicky Fakhri, Pribadi W. Busro, Budi Rahmat, Salomo Purba, Aryo A.P. Mukti, Michael Caesario, Kelly Christy, Anwar Santoso, Samsuridjal Djauzi

DOI: https://doi.org/10.13181/mji.v25i3.1450


Background: Postsurgical sepsis is one of the main causes of the high mortality and morbidity after open congenital heart surgery in infants.  This study aimed to evaluate the role of cardiopulmonary bypass duration, thymectomy, surgical complexity, and nutritional status on postsurgical sepsis after open congenital cardiac surgery in infants.

Methods: A total of 40 patients <1 year of age with congenital heart disease, Aristotle Basic Score (ABS) ≥6 were followed for clinical and laboratory data before and after surgery until the occurrence of signs or symptoms of sepsis or until a maximum of 7 days after surgery. Bivariate analyses were performed. Variables with p≤0.200 were then included for logistic regression.

Results: Duration of cardiopulmonary bypass ≥90 minutes was associated with 5.538 increased risk of postsurgical sepsis in comparison to those ≤90 minutes (80% vs 25%, RR=5.538, p=0.006). No association was observed between the incidence of postsurgical sepsis with poor nutritional status (86% vs 84%, RR=1.059, p=1.000), thymectomy (and 50% vs 76%, RR=0.481, p=0.157), and Aristotle Basic Score (p=0.870).

Conclusion: Cardiopulmonary bypass time influences the incidence of sepsis infants undergoing open congenital cardiac surgery. Further studies are needed to elaborate a number of risk factors associated with the incidence of sepsis in this population.


aortic cross-clamp; Aristotle Basic Score; cardiopulmonary bypass; congenital heart disease; nutritional status; sepsis

Full Text:



  1. Allen HD, Driscoll DJ, Shaddy RE, Feltes TF. Moss and Adams' heart disease in infants, children, and adolescents including the fetus and young adult. Philadelphia: Lippincott Williams & Wilkins; 2008. p. 597–639.
  2. David WB, David RF. Congenital Heart Disease in Children And Adolescents. In: Richard AW, Robert AH, Valentin F, editors. Hurst's the heart. 13th ed. United States: The McGraw-Hill Companies Inc; 2011.
  3. Daniel B. Epidemiology and genetic basic of congenital heart disease. In: Kliegman R, Behrman R, Jenson H, editors. Nelson Textbook of Pediatrics. 19th ed. Philadelphia: Saunders Elsevier. 2011.
  4. Mills JL, Troendle J, Conley MR, Carter T, Druschel CM. Maternal Obesity and Congenital Heart defect: a Population –based Study. Am J Clin Nutr. 2010;91:1543–9. http://dx.doi.org/10.3945/ajcn.2009.28865
  5. Rahayuningsih SE. Detection of NKX2.5, TBX5, GATA4, and MYH6 Gene Mutations in Finding an Association with Sporadic Secundum Atrial Septal Defect. Majalah Kedokteran Indonesia. 2009;59:315–21.
  6. Wallace MC, Jaggers J, Li JS, Jacobs ML, Jacobs JP, Benjamin DK, et al. Center variation in patient age and weight at Fontan operation and impact on postoperative outcomes. Ann Thorac Surg. 2011;91(5):1445–52. http://dx.doi.org/10.1016/j.athoracsur.2010.11.064
  7. Lee AH, Borek BT, Gallagher PJ, Saunders R, Lamb RK, Livesey SA, et al. Prospective study of the value of necropsy examination in early death after cardiac surgery. Heart. 1997;78:34–8. http://dx.doi.org/10.1136/hrt.78.1.34
  8. Aylin P, Bottle A, Jarman B, Elliott P. Paediatric cardiac surgical mortality in England after Bristol: descriptive analysis of hospital episode statistics 1991-2002. BMJ. 2004;329(7470):825. http://dx.doi.org/10.1136/bmj.329.7470.825
  9. Limperopoulos C, Majnemer A, Shevell MI, Rosenblatt B, Rohlicek C, Tchervenkov C, et al. Functional limitations in young children with congenital heart defects after cardiac surgery. Pediatrics. 2001;108(6):1325–31. http://dx.doi.org/10.1542/peds.108.6.1325
  10. Catre D, Lopes MF, Madrigal A, Oliveiros B, Viana JS, Cabrita AS. Early mortality after neonatal surgery: analysis of risk factors in an optimized health care system for the surgical newborn. Rev Bras Epidemiol. 2013;16(4):943–52. http://dx.doi.org/10.1590/S1415-790X2013000400014
  11. Oppido G, Pace Napoleone C, Formigari R, Gabbieri D, Pacini D, Frascaroli G, et al. Outcome of cardiac surgery in low birth weight and premature infants. Eur J Cardiothorac Surg. 2004;26(1):44–53. http://dx.doi.org/10.1016/j.ejcts.2004.04.004
  12. Kochilas LK, Vinocur JM, Menk JS. Age-dependent sex effects on outcomes after pediatric cardiac surgery. J Am Heart Assoc. 2014:3(1)-e000608. http://dx.doi.org/10.1161/JAHA.113.000608
  13. Barker GM, O'Brien SM, Welke KF, Jacobs ML, Jacobs JP, Benjamin DK Jr, et al. Major infection after pediatric cardiac surgery: a risk estimation model. Ann Thorac Surg. 2010;89(3):843–50. http://dx.doi.org/10.1016/j.athoracsur.2009.11.048
  14. Shane AL, Stoll BJ. Neonatal sepsis: progress towards improved outcomes. J Infect. 2014;68(Suppl1):S24–32. http://dx.doi.org/10.1016/j.jinf.2013.09.011
  15. Valera M, Scolfaro C, Cappello N, Gramaglia E, Grassitelli S, Abbate MT, et al. Nosocomial infection in pediatric cardiac surgery, Italy. Infect Control Hosp Epidemiol. 2001;22(12):771–5. http://dx.doi.org/10.1086/501861
  16. Franke A, Lante W, Fackeldey V, Becker HP, Thode C, Kuhlmann WD, et al. Proinflamatory and antiinflamatory cytokines after cardiac operation: different cellular sources at different times. Ann Thorac Surg. 2002;74(2):363–70. http://dx.doi.org/10.1016/S0003-4975(02)03658-5
  17. Wynn J, Cornell TT, Wong HR, Shanley TP, Wheeler DS. The host response to sepsis and developmental impact. Pediatrics. 2010;125(5):1031–41. http://dx.doi.org/10.1542/peds.2009-3301
  18. Larmann J, Theilmeier G. Response to cardiac surgery: cardiopulmonary bypass versus non-cardiopulmonary bypass surgery. Best Prac Res Cl Anaesth. 2004;18(3):425–38. http://dx.doi.org/10.1016/j.bpa.2003.12.004
  19. Paparella D, Yau TM, Young E. Cardiopulmonary bypass induced inflammation: pathophysiology and treatment. An Update. Eur J Cardiothoracic Surg. 2002;21:232–44. http://dx.doi.org/10.1016/S1010-7940(01)01099-5
  20. Kapoor MC, Ramachandran TR. Inflammatory response to cardiac surery and strategies to overcome it. Ann Card Anaesth. 2004;7(2):113–28. http://dx.doi.org/10.1155/2014/905238
  21. Wan S, LeClerc JL, Vincent JL. Inflammatory response to cardiopulmonary bypass: mechanisms involved and possible therapeutic strategies. Chest. 1997;112(3):676–92. http://dx.doi.org/10.1378/chest.112.3.676
  22. Salis S, Mazzani VV, Merli G, Salvi L, Tedesco CC, Veglia F, et al. Cardiopulmonary bypass duration is an independent predictor of morbidity and mortality after cardiac surgery. J Cardiothorac Vasc Anesth. 2008;20(6):814–22. http://dx.doi.org/10.1053/j.jvca.2008.08.004
  23. Chai PJ, Williamson JA, Lodge AJ, Daggett CW, Scarborough JE, Meliones JN, et al. Effect of ischemia on pulmonary dysfunction after cardiopulmonary bypass. Ann Thorac Surg. 1999;67(3):731–5. http://dx.doi.org/10.1016/S0003-4975(99)00096-X
  24. Tsuchida M, Watanabe H, Watanabe T, Hirahara H, Haga M, Ohzeki H, et al. effect of cardiopulmonary bypass on cytokine release and adhesion molecule expression in alveolar macrophage. Preliminary report in six cases. Am J Respir Crit Care Med. 1997;156(3 Pt 1):932–8. http://dx.doi.org/10.1164/ajrccm.156.3.9611055
  25. Gormley SM, McBride WT, Armstrong MA, Young IS, McClean E, MacGowan SW, et al. Plasma and urinary cytokinie homeostasis and renal dysfunction during cardiac surgery. Anesthesiology. 2000;93(5):1210–6. http://dx.doi.org/10.1097/00000542-200011000-00013
  26. Brown WR, Moody DM, Challa VR, Stump DA, Hammon JW. Longer duration of cardiopulmonary bypass is associated with greater number of cerebral microemboli. Stroke. 2000;31(3):707–13. http://dx.doi.org/10.1161/01.STR.31.3.707
  27. Dong GH, Wang CT, Li Y, Xu B, Qian JJ, Wu HW, et al. Cardiopulmonary bypass induced microcirculatory injury of the small bowel in rats. World J Gastroenterol. 2009;15(25):3166–72. http://dx.doi.org/10.3748/wjg.15.3166
  28. Jonas RA, Wypij D, Roth SJ, Bellinger DC, Visconti KJ, du Plessis AJ, et al. The influence of hemodilution on outcome after hypothermic cardiopulmonary bypass: result of a randomized trial in infants. J Thorac Cardiovasc Surg. 2003;126(6):1765–74. http://dx.doi.org/10.1016/j.jtcvs.2003.04.003
  29. Siddiqui MMA, Paras I, Jalal A. Risk factors of prolonged mechanical ventilation following open heart surgery: what has changed over the last decade? Cardiovasc Diagn Ther. 2012;2(3):192–9. http://dx.doi.org/10.3978/j.issn.2223-3652.2012.06.05.
  30. Klein DJ, Briet F, Nisenbaum R, Romaschin AD, Mazer CD. Endotoxemia related to cardiopulmonary bypass is associated with increased risk of infection after cardiac surgery: a prospective observational study. Crit Care. 2011;15(1);1–6. http://dx.doi.org/10.1186/cc10051
  31. McElhinney DB, Hendrick HL, Bush DM, Pereira GR, Stafford PW, Gaynor JW, et al. Necrotizing enterocolitis in neonates with congenital heart disease: risk factors and outcomes. Pediatrics. 2000;106(5):1080–7. http://dx.doi.org/10.1542/peds.106.5.1080
  32. Mancebo E, Clemente J, Sanchez J, Ruiz-Contreras J, De Pablos P, Cortezon S, et al. Longitudinal analysis of immune function in the first 3 years of life in thymectomized neonates during cardiac surgery. Clin Exp Immunol. 2008;154(3):375–83. http://dx.doi.org/10.1111/j.1365-2249.2008.03771.x
  33. Bayer A, Doğan OF, Ersoy F, Ersoy U. The effect of open heart surgery on circulatin lymphocytes and lymphocyte subsets in pediatrics patients. Turk J Thorac Cardiovasc Surg. 2009:17(1):13–17.
  34. Eysteindottir JH, Freysdottir J, Haraldsson A, Stefansdottir J, Skaftadottir R, Helgason H, et al. The influence of partial or total thymectomy during open heart surgery in infants on the immune function later in life. Clin Exp Immunol. 2004;136(2):349–55. http://dx.doi.org/10.1111/j.1365-2249.2004.02437.x
  35. Madhok AB, Chandrasekran A, Parnell V, Gandhi M, Chowdhury D, Pahwa S. Level of recent thymic emigrant cells decrease in children undergoing partial thymectomy during cardiac surgery. 2005;12(5):563–5. http://dx.doi.org/10.1128/CDLI.12.5.563-565.2005
  36. Cameron JW, Rosenthal A, Olson AD. Malnutrition in hospitalized children with congenital heart disease. Arch Pediatr Adolesc Med. 1995;149(10):1098–102. http://dx.doi.org/10.1001/archpedi.1995.02170230052007
  37. Katona P, Katona-Apte J. The interaction between nutrition and infection. Clin Infect Dis. 2008;46(10):1582–8. http://dx.doi.org/10.1086/587658
  38. Calder PC, Jackson AA. Undernutrition, infection and immune function. Nutr Res Rev. 2000;13(1):3–29. http://dx.doi.org/10.1079/095442200108728981
  39. Raqib R, Alam DS, Sarker P, Ahmad SM, Ara G, Yunus M, et al. Low birth weight is associated with altered immune function in rural banglades children: a birth cohort study. Am J Clin Nutr. 2007;85(3):845–52.
  40. Hassen TA, Pearson S, Cowled PA, Fritdge RA. Preoperative nutritional status predict the severity of the systemic inflammatory response syndrome (sirs) following major vascular surgery. Eur J Vasc Endovasc Surg. 2007;33:696–702. http://dx.doi.org/10.1016/j.ejvs.2006.12.006
  41. Wallace MC, Jaggers J, Li JS, Jacobs ML, Jacobs JP, Benjamin DK, et al. Center variation in patient age and weight at Fontan operation and impact on post-operative outcomes. Ann Thorac Surg. 2011;91(5):1145–52. http://dx.doi.org/10.1016/j.athoracsur.2010.11.064
  42. Anderson JB, Beekman RH, Border WL, Kalkwarf HJ, Khoury PR, Uzark K, et al. Lower weight-for-age z score adversely affects hospital length of stay after the bidirectional Glenn procedure in 100 infants with a single ventricle. J Thorac Cardiovasc Surg. 2009;138(2):397–404. http://dx.doi.org/10.1016/j.jtcvs.2009.02.033
  43. Leite HP, Fisberg M, de Carvalho WB, de Camargo Carvalho AC. Serum albumin and clinical outcome in pediatric cardiac surgery. Nutrition. 2005;21(5):553–8. http://dx.doi.org/10.1016/j.nut.2004.08.026
  44. Azakie A, Johnson NC, Anagnostopoulos PV, Egrie GD, Lavrsen MJ, Sapru A. Cardiac surgery in low birth weight infants: current outcomes. J Cardiovasc Thorac Surg. 2012;12(3):409–14. http://dx.doi.org/10.1510/icvts.2010.253823
  45. Lacour-Gayet F, Clarke DR, Aristotle Committee. The Aristotle method: a new concept to evaluate quality of care based on complexity. Curr Opin Pediatr. 2005;17(3):412–7. http://dx.doi.org/10.1097/01.mop.0000165361.05587.b9
  46. Lacour-Gayet F, Clarke D, Jacobs J, Comas J, Daebritz S, Daenen W, et al. The Aristotle score: a complexity-adjusted method to evaluate surgical result. Eur J Cardiothorac Surg. 2004;25(6):911–24. http://dx.doi.org/10.1016/j.ejcts.2004.03.027
  47. Kansy A, Maruszewski B, Jacobs J, Maruszewski P. Application of four complexity stratification tools (Aristotle Basic Score, RACHS-1, STAT Mortality Scorem and STAT Mortality Categories) to evaluate early congenital heart surgery outcomes over 16 years at a single institution. Kardiochir Thorakochir Polsk. 2013;10(2):115–9. http://dx.doi.org/10.5114/kitp.2013.36129

Copyright (c) 2016 Dicky Fakhri, Pribadi W. Busro, Budi Rahmat, Salomo Purba, Aryo A.P. Mukti, Michael Caesario, Kelly Christy, Anwar Santoso, Samsuridjal Djauzi

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

All articles and issues in Medical Journal of Indonesia have unique DOI number registered in Crossref.