Acute gastrointestinal injury after pediatric cardiac surgery with cardiopulmonary bypass: A prospective observational study_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

WANG Shouping ¹ ,  DENG Lijing ¹ , LUO Shuhua ² , ZENG Jiarong ¹

1. Department of Critical Care Medicine, West China Hospital, Sichuan University, Chengdu, 610041, P. R. China;
2. Department of cardiovascular surgery, West China Hospital, Sichuan University, Chengdu, 610041, P. R. China;

Corresponding author：

DENG Lijing, Email: deng_lijng@163.com

Keywords：

Cardiopulmonary bypass; congenital heart disease; acute gastrointestinal injury; overall adverse outcomes

DOI：

10.7507/1007-4848.202311020

Video：

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Objective To analyze the occurrence of acute gastrointestinal injury (AGI) after pediatric cardiac surgery with cardiopulmonary bypass (CPB) and its impact on prognosis, and to explore the risk factors and early warning indicators for AGI, in order to identify and diagnose AGI at an early stage. Methods This is a prospective observational study. The patients under 14 years with congenital heart disease receiving surgeries with CPB who were admitted to the pediatric ICU of West China Hospital, Sichuan University from December 2020 to December 2021 were included. The general information, perioperative gastrointestinal symptoms and intra-abdominal pressure, surgery-related information, postoperative organ function and prognosis of the children were collected. The patients were divided into an AGI group and a non-AGI group according to the 2012 European Society of Critical Care Medicine AGI diagnostic criteria. Results A total of 137 patients were enrolled, including 68 males and 69 females with a median age of 20.0 (6.0, 43.0) months. There were 60 patients in the AGI group and 77 patients in the non-AGI group, with an AGI incidence of 43.80%. The incidences of overall adverse outcomes, low cardiac output syndrome, and infectious complications were higher in the AGI group, and the vasoactive-inotropic score (VIS), mechanical ventilation time, ICU stay, and hospital stay were higher or longer in the AGI group, the differences were statistically significant (P<0.001). AGI was an independent risk factor for the overall adverse outcomes (OR=3.191, 95%CI 1.187 to 8.579, P=0.021). Univariate and multivariate logistic regression analyses indicated that weight, male, CPB time and intraoperative VIS were independent predictors for AGI after pediatric cardiac surgery. The receiver operating characteristic curve indicated that the patients with an intraoperative VIS>10.5 points and CPB time>96.5 min might have a higher possibility of postoperative AGI. Conclusion The incidence of AGI in pediatric cardiac surgery with CPB is high, and it is an independent risk factor for overall adverse outcomes. Weight, male, CPB time , and intraoperative VIS are independent risk factors for AGI.

1.	Dolk H, Loane M, Garne E, et al. Congenital heart defects in Europe: Prevalence and perinatal mortality, 2000 to 2005. Circulation, 2011, 123(8): 841-849.
2.	van der Linde D, Konings EE, Slager MA, et al. Birth prevalence of congenital heart disease worldwide: A systematic review and meta-analysis. J Am Coll Cardiol, 2011, 58(21): 2241-2247.
3.	Mason CA, Kirby RS, Sever LE, et al. Prevalence is the preferred measure of frequency of birth defects. Birth Defects Res A Clin Mol Teratol, 2005, 73(10): 690-692.
4.	Bernier PL, Stefanescu A, Samoukovic G, et al. The challenge of congenital heart disease worldwide: Epidemiologic and demographic facts. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu, 2010, 13(1): 26-34.
5.	汤楚中, 赵鸿, 髙文根, 等. 中国先天性心脏病外科治疗现状. 中国循证心血管医学杂志, 2009, 1(1): 68-69.
6.	Ohri SK, Velissaris T. Gastrointestinal dysfunction following cardiac surgery. Perfusion, 2006, 21(4): 215-223.
7.	Viana FF, Chen Y, Almeida AA, et al. Gastrointestinal complications after cardiac surgery: 10-year experience of a single Australian centre. ANZ J Surg, 2013, 83(9): 651-656.
8.	Pathan N, Burmester M, Adamovic T, et al. Intestinal injury and endotoxemia in children undergoing surgery for congenital heart disease. Am J Respir Crit Care Med, 2011, 184(11): 1261-1269.
9.	Typpo KV, Larmonier CB, Deschenes J, et al. Clinical characteristics associated with postoperative intestinal epithelial barrier dysfunction in children with congenital heart disease. Pediatr Crit Care Med, 2015, 16(1): 37-44.
10.	Sinclair DG, Haslam PL, Quinlan GJ, et al. The effect of cardiopulmonary bypass on intestinal and pulmonary endothelial permeability. Chest, 1995, 108(3): 718-724.
11.	Meng M, Klingensmith NJ, Coopersmith CM. New insights into the gut as the driver of critical illness and organ failure. Curr Opin Crit Care, 2017, 23(2): 143-148.
12.	Carrico CJ, Meakins JL, Marshall JC, et al. Multiple-organ-failure syndrome. Arch Surg, 1986, 121(2): 196-208.
13.	Reintam Blaser A, Malbrain ML, Starkopf J, et al. Gastrointestinal function in intensive care patients: Terminology, definitions and management. Recommendations of the ESICM Working Group on Abdominal Problems. Intensive Care Med, 2012, 38(3): 384-394.
14.	Butts RJ, Scheurer MA, Zyblewski SC, et al. A composite outcome for neonatal cardiac surgery research. J Thorac Cardiovasc Surg, 2014, 147(1): 428-433.
15.	Gaies MG, Gurney JG, Yen AH, et al. Vasoactive-inotropic score as a predictor of morbidity and mortality in infants after cardiopulmonary bypass. Pediatr Crit Care Med, 2010, 11(2): 234-238.
16.	中国医师协会心脏重症专家委员会. 低心排血量综合征中国专家共识. 解放军医学杂志, 2017, 42(11): 933-944.
17.	Goldstein B, Giroir B, Randolph A, et al. International pediatric sepsis consensus conference: Definitions for sepsis and organ dysfunction in pediatrics. Pediatr Crit Care Med, 2005, 6(1): 2-8.
18.	Jenkins KJ. Risk adjustment for congenital heart surgery: The RACHS-1 method. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu, 2004, 7: 180-4.7-180.
19.	李土凤, 黄宇戈, 钟娩玲, 等. PICU儿童急性胃肠损伤的分级、预后及原因探讨. 中国小儿急救医学, 2019, 26(9): 676-680.
20.	范晓蕾, 李海英, 陈晓昕, 等. 肠脂肪酸结合蛋白在肺炎合并胃肠功能损伤患儿血清中的变化及意义. 中国当代儿科杂志, 2016, 18(7): 603-606.
21.	张妮, 朱炜, 朱家睿, 等. 瓜氨酸、肠型脂肪酸结合蛋白、肠三叶因子联合检测对儿童危重症急性胃肠损伤的诊断价值. 临床儿科杂志, 2015, 33(7): 650-654.
22.	Rodriguez R, Robich MP, Plate JF, et al. Gastrointestinal complications following cardiac surgery: A comprehensive review. J Card Surg, 2010, 25(2): 188-197.
23.	Chaudhry R, Zaki J, Wegner R, et al. Gastrointestinal complications after cardiac surgery: A nationwide population-based analysis of morbidity and mortality predictors. J Cardiothorac Vasc Anesth, 2017, 31(4): 1268-1274.
24.	Chor CYT, Mahmood S, Khan IH, et al. Gastrointestinal complications following cardiac surgery. Asian Cardiovasc Thorac Ann, 2020, 28(9): 621-632.
25.	Haywood N, Mehaffey JH, Hawkins RB, et al. Gastrointestinal complications after cardiac surgery: Highly morbid but improving over time. J Surg Res, 2020, 254: 306-313.
26.	Dong G, Liu C, Xu B, et al. Postoperative abdominal complications after cardiopulmonary bypass. J Cardiothorac Surg, 2012, 7: 108.
27.	Croome KP, Kiaii B, Fox S, et al. Comparison of gastrointestinal complications in on-pump versus off-pump coronary artery bypass grafting. Can J Surg, 2009, 52: 125-128.
28.	Seilitz J, Edström M, Sköldberg M, et al. Early onset of postoperative gastrointestinal dysfunction is associated with unfavorable outcome in cardiac surgery: A prospective observational study. J Intensive Care Med, 2021, 36(11): 1264-1271.
29.	Bronicki RA, Hall M. Cardiopulmonary bypass-induced inflammatory response: Pathophysiology and treatment. Pediatr Crit Care Med, 2016, 17(8 Suppl 1): S272-S278.
30.	Piton G, Capellier G. Biomarkers of gut barrier failure in the ICU. Curr Opin Crit Care, 2016, 22(2): 152-160.
31.	Memet O, Zhang L, Shen J. Serological biomarkers for acute mesenteric ischemia. Ann Transl Med, 2019, 7(16): 394.
32.	Peoc'h K, Corcos O. Biomarkers for acute mesenteric ischemia diagnosis: State of the art and perspectives. Ann Biol Clin (Paris), 2019, 77(4): 415-421.
33.	Nuzzo A, Guedj K, Curac S, et al. Accuracy of citrulline, I-FABP and D-lactate in the diagnosis of acute mesenteric ischemia. Sci Rep, 2021, 11(1): 18929.
34.	Peoc'h K, Nuzzo A, Guedj K, et al. Diagnosis biomarkers in acute intestinal ischemic injury: So close, yet so far. Clin Chem Lab Med, 2018, 56(3): 373-385.
35.	Otani S, Chihade DB, Coopersmith CM. Critical illness and the role of the microbiome. Acute Med Surg, 2018, 6(2): 91-94.
36.	Zaher S. Nutrition and the gut microbiome during critical illness: A new insight of nutritional therapy. Saudi J Gastroenterol, 2020, 26(6): 290-298.
37.	Ho SW, Chang SC, Chen LW. Urinary intestine fatty acid binding protein is associated with poor outcome of pneumonia patients in intensive care unit. Clin Lab, 2016, 62(11): 2219-2226.
38.	Zou L, Song X, Hong L, et al. Intestinal fatty acid-binding protein as a predictor of prognosis in postoperative cardiac surgery patients. Medicine (Baltimore), 2018, 97(33): e11782.
39.	Kitai T, Kim YH, Kiefer K, et al. Circulating intestinal fatty acid-binding protein (I-FABP) levels in acute decompensated heart failure. Clin Biochem, 2017, 50(9): 491-495.
40.	Ho KM, Kalgudi S, Corbett JM, et al. Gut microbiota in surgical and critically ill patients. Anaesth Intensive Care, 2020, 48(3): 179-195.
41.	Lederer AK, Pisarski P, Kousoulas L, et al. Postoperative changes of the microbiome: Are surgical complications related to the gut flora? A systematic review. BMC Surg, 2017, 17(1): 125.
42.	Maekawa M, Yoshitani K, Yahagi M, et al. Association between postoperative changes in the gut microbiota and pseudopsia after cardiac surgery: Prospective observational study. BMC Surg, 2020, 20(1): 247.

1. Dolk H, Loane M, Garne E, et al. Congenital heart defects in Europe: Prevalence and perinatal mortality, 2000 to 2005. Circulation, 2011, 123(8): 841-849.
2. van der Linde D, Konings EE, Slager MA, et al. Birth prevalence of congenital heart disease worldwide: A systematic review and meta-analysis. J Am Coll Cardiol, 2011, 58(21): 2241-2247.
3. Mason CA, Kirby RS, Sever LE, et al. Prevalence is the preferred measure of frequency of birth defects. Birth Defects Res A Clin Mol Teratol, 2005, 73(10): 690-692.
4. Bernier PL, Stefanescu A, Samoukovic G, et al. The challenge of congenital heart disease worldwide: Epidemiologic and demographic facts. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu, 2010, 13(1): 26-34.
5. 汤楚中, 赵鸿, 髙文根, 等. 中国先天性心脏病外科治疗现状. 中国循证心血管医学杂志, 2009, 1(1): 68-69.
6. Ohri SK, Velissaris T. Gastrointestinal dysfunction following cardiac surgery. Perfusion, 2006, 21(4): 215-223.
7. Viana FF, Chen Y, Almeida AA, et al. Gastrointestinal complications after cardiac surgery: 10-year experience of a single Australian centre. ANZ J Surg, 2013, 83(9): 651-656.
8. Pathan N, Burmester M, Adamovic T, et al. Intestinal injury and endotoxemia in children undergoing surgery for congenital heart disease. Am J Respir Crit Care Med, 2011, 184(11): 1261-1269.
9. Typpo KV, Larmonier CB, Deschenes J, et al. Clinical characteristics associated with postoperative intestinal epithelial barrier dysfunction in children with congenital heart disease. Pediatr Crit Care Med, 2015, 16(1): 37-44.
10. Sinclair DG, Haslam PL, Quinlan GJ, et al. The effect of cardiopulmonary bypass on intestinal and pulmonary endothelial permeability. Chest, 1995, 108(3): 718-724.
11. Meng M, Klingensmith NJ, Coopersmith CM. New insights into the gut as the driver of critical illness and organ failure. Curr Opin Crit Care, 2017, 23(2): 143-148.
12. Carrico CJ, Meakins JL, Marshall JC, et al. Multiple-organ-failure syndrome. Arch Surg, 1986, 121(2): 196-208.
13. Reintam Blaser A, Malbrain ML, Starkopf J, et al. Gastrointestinal function in intensive care patients: Terminology, definitions and management. Recommendations of the ESICM Working Group on Abdominal Problems. Intensive Care Med, 2012, 38(3): 384-394.
14. Butts RJ, Scheurer MA, Zyblewski SC, et al. A composite outcome for neonatal cardiac surgery research. J Thorac Cardiovasc Surg, 2014, 147(1): 428-433.
15. Gaies MG, Gurney JG, Yen AH, et al. Vasoactive-inotropic score as a predictor of morbidity and mortality in infants after cardiopulmonary bypass. Pediatr Crit Care Med, 2010, 11(2): 234-238.
16. 中国医师协会心脏重症专家委员会. 低心排血量综合征中国专家共识. 解放军医学杂志, 2017, 42(11): 933-944.
17. Goldstein B, Giroir B, Randolph A, et al. International pediatric sepsis consensus conference: Definitions for sepsis and organ dysfunction in pediatrics. Pediatr Crit Care Med, 2005, 6(1): 2-8.
18. Jenkins KJ. Risk adjustment for congenital heart surgery: The RACHS-1 method. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu, 2004, 7: 180-4.7-180.
19. 李土凤, 黄宇戈, 钟娩玲, 等. PICU儿童急性胃肠损伤的分级、预后及原因探讨. 中国小儿急救医学, 2019, 26(9): 676-680.
20. 范晓蕾, 李海英, 陈晓昕, 等. 肠脂肪酸结合蛋白在肺炎合并胃肠功能损伤患儿血清中的变化及意义. 中国当代儿科杂志, 2016, 18(7): 603-606.
21. 张妮, 朱炜, 朱家睿, 等. 瓜氨酸、肠型脂肪酸结合蛋白、肠三叶因子联合检测对儿童危重症急性胃肠损伤的诊断价值. 临床儿科杂志, 2015, 33(7): 650-654.
22. Rodriguez R, Robich MP, Plate JF, et al. Gastrointestinal complications following cardiac surgery: A comprehensive review. J Card Surg, 2010, 25(2): 188-197.
23. Chaudhry R, Zaki J, Wegner R, et al. Gastrointestinal complications after cardiac surgery: A nationwide population-based analysis of morbidity and mortality predictors. J Cardiothorac Vasc Anesth, 2017, 31(4): 1268-1274.
24. Chor CYT, Mahmood S, Khan IH, et al. Gastrointestinal complications following cardiac surgery. Asian Cardiovasc Thorac Ann, 2020, 28(9): 621-632.
25. Haywood N, Mehaffey JH, Hawkins RB, et al. Gastrointestinal complications after cardiac surgery: Highly morbid but improving over time. J Surg Res, 2020, 254: 306-313.
26. Dong G, Liu C, Xu B, et al. Postoperative abdominal complications after cardiopulmonary bypass. J Cardiothorac Surg, 2012, 7: 108.
27. Croome KP, Kiaii B, Fox S, et al. Comparison of gastrointestinal complications in on-pump versus off-pump coronary artery bypass grafting. Can J Surg, 2009, 52: 125-128.
28. Seilitz J, Edström M, Sköldberg M, et al. Early onset of postoperative gastrointestinal dysfunction is associated with unfavorable outcome in cardiac surgery: A prospective observational study. J Intensive Care Med, 2021, 36(11): 1264-1271.
29. Bronicki RA, Hall M. Cardiopulmonary bypass-induced inflammatory response: Pathophysiology and treatment. Pediatr Crit Care Med, 2016, 17(8 Suppl 1): S272-S278.
30. Piton G, Capellier G. Biomarkers of gut barrier failure in the ICU. Curr Opin Crit Care, 2016, 22(2): 152-160.
31. Memet O, Zhang L, Shen J. Serological biomarkers for acute mesenteric ischemia. Ann Transl Med, 2019, 7(16): 394.
32. Peoc'h K, Corcos O. Biomarkers for acute mesenteric ischemia diagnosis: State of the art and perspectives. Ann Biol Clin (Paris), 2019, 77(4): 415-421.
33. Nuzzo A, Guedj K, Curac S, et al. Accuracy of citrulline, I-FABP and D-lactate in the diagnosis of acute mesenteric ischemia. Sci Rep, 2021, 11(1): 18929.
34. Peoc'h K, Nuzzo A, Guedj K, et al. Diagnosis biomarkers in acute intestinal ischemic injury: So close, yet so far. Clin Chem Lab Med, 2018, 56(3): 373-385.
35. Otani S, Chihade DB, Coopersmith CM. Critical illness and the role of the microbiome. Acute Med Surg, 2018, 6(2): 91-94.
36. Zaher S. Nutrition and the gut microbiome during critical illness: A new insight of nutritional therapy. Saudi J Gastroenterol, 2020, 26(6): 290-298.
37. Ho SW, Chang SC, Chen LW. Urinary intestine fatty acid binding protein is associated with poor outcome of pneumonia patients in intensive care unit. Clin Lab, 2016, 62(11): 2219-2226.
38. Zou L, Song X, Hong L, et al. Intestinal fatty acid-binding protein as a predictor of prognosis in postoperative cardiac surgery patients. Medicine (Baltimore), 2018, 97(33): e11782.
39. Kitai T, Kim YH, Kiefer K, et al. Circulating intestinal fatty acid-binding protein (I-FABP) levels in acute decompensated heart failure. Clin Biochem, 2017, 50(9): 491-495.
40. Ho KM, Kalgudi S, Corbett JM, et al. Gut microbiota in surgical and critically ill patients. Anaesth Intensive Care, 2020, 48(3): 179-195.
41. Lederer AK, Pisarski P, Kousoulas L, et al. Postoperative changes of the microbiome: Are surgical complications related to the gut flora? A systematic review. BMC Surg, 2017, 17(1): 125.
42. Maekawa M, Yoshitani K, Yahagi M, et al. Association between postoperative changes in the gut microbiota and pseudopsia after cardiac surgery: Prospective observational study. BMC Surg, 2020, 20(1): 247.

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