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Necrotizing Enterocolitis in Infants with Hypoplastic Left Heart Syndrome Following Stage 1 Palliation or Heart Transplant

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Abstract

Previous studies of necrotizing enterocolitis (NEC) among infants with hypoplastic left heart syndrome (HLHS) were conducted in single centers or had small sample sizes. This study aimed to determine the mortality rate and the risk factors for NEC among infants with HLHS who were discharged over a 10-year period (2004–2013) from 41 Pediatric Health Information System affiliated children’s hospitals. Either stage 1 palliation and/or heart transplant were completed prior to patient’s death or hospital discharge. We compared the characteristics of infants with HLHS who did not develop NEC and those who developed medical or surgical NEC and of patients who had medical vs. surgical NEC. The primary outcome was mortality over time and by birth weight category (low birth weight [LBW], birth weight < 2500 vs. ≥ 2500 g). Multivariable analyses were performed to identify the risk factors for developing NEC and for mortality among infants with HLHS. The study evaluated 5720 infants with HLHS including 349 patients (6.1%) with medical or surgical NEC. Fifty-two patients (0.9%) required laparotomy or percutaneous abdominal drainage. On univariable analysis, the overall mortality rate for infants who developed NEC was significantly higher than infants who did not develop NEC (23.5 vs. 13.9%, P < 0.001). On multivariable analysis, neither medical nor surgical NEC was a significant predictor of mortality in the study population. LBW infants were at higher risk for mortality in both the univariable and the multivariable models. Nevertheless, LBW did not significantly predispose infants with HLHS to develop NEC. Our results provide a national benchmark incidence of NEC, its risk factors, and outcomes among a large cohort of infants with HLHS and establish that NEC is not a significant risk factor for mortality in this population.

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Abbreviations

CPB:

Cardiopulmonary bypass

CPR:

Cardiac pulmonary resuscitation

CHCA:

Child Health Corporation of America

CHD:

Congenital heart disease

CI:

Confidence interval

CPT:

Current Procedural Terminology

CTC:

Clinical Transaction Classification™

ECMO:

Extracorporeal membrane oxygenation

GT:

Gastrostomy tube

HLHS:

Hypoplastic left heart syndrome

ICD-9:

International Classification of Diseases, Ninth Revision

LBW:

Low birth weight

NEC:

Necrotizing enterocolitis

PHIS:

Pediatric Health Information System

SGA:

Small for gestational age

RR:

Relative risk

VLBW:

Very low birth weight

References

  1. McElhinney DB, Hedrick HL, Bush DM et al (2000) Necrotizing enterocolitis in neonates with congenital heart disease: risk factors and outcomes. Pediatrics 106:1080–1087

    Article  CAS  PubMed  Google Scholar 

  2. Stoll BJ, Kanto WP, Glass RI, Nahmias AJ, Brann AW (1980) Epidemiology of necrotizing enterocolitis: a case control study. J Pediatr 96:447–451

    Article  CAS  PubMed  Google Scholar 

  3. Cozzi C, Aldrink J, Nicol K, Nicholson L, Cua C (2013) Intestinal location of necrotizing enterocolitis among infants with congenital heart disease. J Perinatol 33:783–785

    Article  CAS  PubMed  Google Scholar 

  4. Pickard SS, Feinstein JA, Popat RA, Huang L, Dutta S (2009) Short- and long-term outcomes of necrotizing enterocolitis in infants with congenital heart disease. Pediatrics 123:e901–e906

    Article  PubMed  Google Scholar 

  5. Luce WA, Schwartz RM, Beauseau W et al (2011) Necrotizing enterocolitis in neonates undergoing the hybrid approach to complex congenital heart disease. Pediatr Crit Care Med 12:46–51

    Article  PubMed  Google Scholar 

  6. Motta C, Scott W, Mahony L et al (2015) The association of congenital heart disease with necrotizing enterocolitis in preterm infants: a birth cohort study. J Perinatol 35:949–953

    Article  CAS  PubMed  Google Scholar 

  7. Fisher JG, Bairdain S, Sparks EA et al (2015) Serious congenital heart disease and necrotizing enterocolitis in very low birth weight neonates. J Am Coll Surg 220:1018–1026.e14

    Article  PubMed  Google Scholar 

  8. Cheng W, Leung MP, Tam PK (1999) Surgical intervention in necrotizing enterocolitis in neonates with symptomatic congenital heart disease. Pediatr Surg Int 15:492–495

    Article  CAS  PubMed  Google Scholar 

  9. Dominguez KM, Moss RL (2012) Necrotizing enterocolitis. Clin Perinatol 39:387–401

    Article  PubMed  Google Scholar 

  10. Llanos AR, Moss ME, Pinzon MC, Dye T, Sinkin RA, Kendig JW (2002) Epidemiology of neonatal necrotising enterocolitis: a population-based study. Paediatr Perinatal Epidemiol 16:342–349

    Article  Google Scholar 

  11. Holman RC, Stehr-Green JK, Zelasky MT (1989) Necrotizing enterocolitis mortality in the United States, 1979-85. Am J Public Health 79:987–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hirsch JC, Gurney JG, Donohue JE, Gebremariam A, Bove EL, Ohye RG (2008) Hospital mortality for Norwood and arterial switch operations as a function of institutional volume. Pediatr Cardiol 29:713–717

    Article  PubMed  Google Scholar 

  13. Kalfa D, Krishnamurthy G, Levasseur S et al (2015) Norwood stage I palliation in patients less than or equal to 2.5 kg: outcomes and risk analysis. Ann Thorac Surg 100:167–173

    Article  PubMed  Google Scholar 

  14. Dees E, Lin H, Cotton RB, Graham TP, Dodd DA (2000) Outcome of preterm infants with congenital heart disease. J Pediatr 137:653–659

    Article  CAS  PubMed  Google Scholar 

  15. Fletcher DM (2004) Achieving data quality. How data from a pediatric health information system earns the trust of its users. J AHIMA 75:22–26

    PubMed  Google Scholar 

  16. Abdullah F, Zhang Y, Camp M et al (2010) Necrotizing enterocolitis in 20,822 infants: analysis of medical and surgical treatments. Clin Pediatr 49:166–171

    Article  Google Scholar 

  17. Spong CY (2013) Defining “term” pregnancy: recommendations from the defining “Term” pregnancy workgroup. JAMA 309:2445–2446

    Article  CAS  PubMed  Google Scholar 

  18. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  19. Miller TA, Minich LL, Lambert LM, Joss-Moore L, Puchalski MD (2014) Abnormal abdominal aorta hemodynamics are associated with necrotizing enterocolitis in infants with hypoplastic left heart syndrome. Pediatr Cardiol 35:616–621

    Article  PubMed  Google Scholar 

  20. Hebra A, Brown MF, Hirschl RB et al (1993) Mesenteric ischemia in hypoplastic left heart syndrome. J Pediatr Surg 28:606–611

    Article  CAS  PubMed  Google Scholar 

  21. Giannone PJ, Luce WA, Nankervis CA, Hoffman TM, Wold LE (2008) Necrotizing enterocolitis in neonates with congenital heart disease. Life Sci 82:341–347

    Article  CAS  PubMed  Google Scholar 

  22. Malagon I, Onkenhout W, Klok M, van der Poel PF, Bovill JG, Hazekamp MG (2005) Gut permeability in neonates after a stage 1 Norwood procedure. Pediatr Crit Care Med 6:547–549

    Article  PubMed  Google Scholar 

  23. Torres A (2011) Classic Norwood versus Sano modification versus hybrid approach: necrotizing enterocolitis or no necrotizing enterocolitis? Pediatr Crit Care Med 12:109–110

    Article  PubMed  Google Scholar 

  24. Maayan-Metzger A, Itzchak A, Mazkereth R, Kuint J (2004) Necrotizing enterocolitis in full-term infants: case-control study and review of the literature. J Perinatol 24:494–499

    Article  PubMed  Google Scholar 

  25. Dean PJ, McHugh KE, Conaway MR, Hillman DG, Gutgesell HP (2013) Effects of race, ethnicity, and gender on surgical mortality in hypoplastic left heart syndrome. Pediatr Cardiol 34:1829–1836

    Article  PubMed  PubMed Central  Google Scholar 

  26. Czosek RJ, Anderson JB, Heaton PC et al (2013) Staged palliation of hypoplastic left heart syndrome: trends in mortality, cost, and length of stay using a national database from 2000 through 2009. Am J Cardiol 111:1792–1799

    Article  PubMed  Google Scholar 

  27. Hornik CP, He X, Jacobs JP et al (2012) Relative impact of surgeon and center volume on early mortality after the Norwood operation. Ann Thorac Surg 93:1992–1997

    Article  PubMed  PubMed Central  Google Scholar 

  28. Karamlou T, Overman D, Hill KD et al (2015) Stage 1 hybrid palliation for hypoplastic left heart syndrome-assessment of contemporary patterns of use: an analysis of the Society of Thoracic Surgeons Congenital Heart Surgery Databse. J Thorac Cardiovasc Surg 149:195–202

    Article  PubMed  Google Scholar 

  29. Patole SK, de Klerk N (2005) Impact of standardised feeding regimens on incidence of neonatal necrotising enterocolitis: a systematic review and meta-analysis of observational studies. Arch Dis Child Fetal Neonatal Ed 90:F147–F151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. McCallie KR, Lee HC, Mayer O, Cohen RS, Hintz SR, Rhine WD (2011) Improved outcomes with a standardized feeding protocol for very low birth weight infants. J Perinatol 31(Suppl 1):S61–S67

    Article  CAS  PubMed  Google Scholar 

  31. Toms R, Jackson KW, Dabal RJ, Reebals CH, Alten JA (2015) Preoperative trophic feeds in neonates with hypoplastic left heart syndrome. Congenit Heart Dis 10:36–42

    Article  PubMed  Google Scholar 

  32. del Castillo SL, McCulley ME, Khemani RG et al (2010) Reducing the incidence of necrotizing enterocolitis in neonates with hypoplastic left heart syndrome with the introduction of an enteral feed protocol. Pediatr Crit Care Med 11:373–377

    PubMed  Google Scholar 

  33. Schwalbe-Terilli CR, Hartman DH, Nagle ML et al (2009) Enteral feeding and caloric intake in neonates after cardiac surgery. Am J Crit Care 18:52–57

    Article  PubMed  Google Scholar 

  34. Hamilton S, McAleer DM, Ariagno K et al (2014) A stepwise enteral nutrition algorithm for critically ill children helps achieve nutrient delivery goals. Pediatr Crit Care Med 15:583–589

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Pediatrics (Neonatology), University of Arkansas for Medical Sciences, Arkansas Children’s Hospital, 1 Children’s Way, Little Rock, AR, 72202, USA

    Nahed O. ElHassan, Ashley Ross & Sashi K. Kona

  2. Department of Pediatrics (Biostatistics), University of Arkansas for Medical Sciences, Arkansas Children’s Hospital, 1 Children’s Way, Little Rock, AR, 72202, USA

    Xinyu Tang

  3. Department of Pediatrics (Biostatistics & Cardiology), University of Arkansas for Medical Sciences, Arkansas Children’s Hospital, 1 Children’s Way, Little Rock, AR, 72202, USA

    Jeffrey Gossett

  4. Departments of Pediatrics (Cardiology), University of Arkansas for Medical Sciences, Arkansas Children’s Hospital, 1 Children’s Way, Little Rock, AR, 72202, USA

    Dala Zakaria

  5. Department of Pediatrics (Cardiology and Pediatric Intensive Care), University of Arkansas for Medical Sciences, Arkansas Children’s Hospital, 1 Children’s Way, Little Rock, AR, 72202, USA

    Parthak Prodhan

Authors
  1. Nahed O. ElHassan
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  2. Xinyu Tang
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Correspondence to Nahed O. ElHassan.

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The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed Consent

This study received the University of Arkansas for Medical Sciences Institutional Board Review approval and individual consent was waived.

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ElHassan, N.O., Tang, X., Gossett, J. et al. Necrotizing Enterocolitis in Infants with Hypoplastic Left Heart Syndrome Following Stage 1 Palliation or Heart Transplant. Pediatr Cardiol 39, 774–785 (2018). https://doi.org/10.1007/s00246-018-1820-0

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  • DOI: https://doi.org/10.1007/s00246-018-1820-0

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