Pediatric Cardiology

, Volume 35, Issue 4, pp 616–621 | Cite as

Abnormal Abdominal Aorta Hemodynamics Are Associated With Necrotizing Enterocolitis in Infants With Hypoplastic Left Heart Syndrome

  • Thomas A. Miller
  • L. LuAnn Minich
  • Linda M. Lambert
  • Lisa Joss-Moore
  • Michael D. Puchalski
Original Article


The risk of necrotizing enterocolitis (NEC) in association with congenital heart disease is highest in patients with hypoplastic left heart syndrome (HLHS). Within the HLHS population, however, risk factors for NEC remain debated. We hypothesized that some infants with HLHS have vascular changes that contribute to gut hypoperfusion independent of diastolic runoff and low cardiac output. We analyzed the abdominal aorta pulsatility index and right-ventricular function on routine preoperative and postoperative echocardiograms for all infants who underwent stage I palliation for HLHS from January 2007 to January 2012. The echocardiography findings and clinical course were compared between those with and those without an episode of NEC. Of the 61 cases reviewed, 11 (18 %) developed NEC during a mean follow-up of 3.8 ± 1.3 years. Those with NEC had a lower abdominal aorta pulsatility index compared with those without NEC both on stage I preoperative (3.38 ± 0.15 vs. 3.89 ± 0.09, p < 0.05) and postoperative echocardiograms (2.21 ± 0.28 vs. 3.05 ± 0.78, p = 0.01) despite similar ventricular function and operative risk. Abdominal aorta Doppler pulsations are lower in patients with HLHS whose clinical course is complicated by NEC. This finding suggests that the systemic vasculature in a subset of neonates with HLHS may be inherently abnormal. Further investigation is warranted to determine if this is secondary to structural changes in the mesenteric and/or systemic vasculature.


Congenital heart disease Hypoplastic left heart syndrome Necrotizing enterocolitis 



The authors thank research coordinators Mason Heywood and Anna Jolley for their assistance with data collection and organization. Study data were collected and managed using REDCap [8] electronic data capture tools hosted at University of Utah Center for Clinical and Transitional Sciences. The Center is supported by National Institutes of Health (NIH) funding (Grant No. CTSA 5UL1RR025764-02). Dr. Miller is supported by NIH training grant NHLBI T32 5T32HL007576-27.


  1. 1.
    Akira M, Yoshiyuki S (2006) Placental circulation, fetal growth, and stiffness of the abdominal aorta in newborn infants. J Pediatr 148:49–53CrossRefPubMedGoogle Scholar
  2. 2.
    Cozzi C, Stines J, Luce WA, Hayes J, Cheatham JP, Galantowicz M, Cua CL (2013) Diastolic flow parameters are not sensitive in predicting necrotizing enterocolitis in patients undergoing hybrid procedure. Congenit Heart Dis 8:234–239CrossRefPubMedGoogle Scholar
  3. 3.
    Davis EF, Lazdam M, Lewandowski AJ, Worton SA, Kelly B, Kenworthy Y et al (2012) Cardiovascular risk factors in children and young adults born to preeclamptic pregnancies: a systematic review. Pediatrics 129:e1552–e1561CrossRefPubMedGoogle Scholar
  4. 4.
    del Castillo SL, Moromisato DY, Dorey F, Ludwick J, Starnes VA, Wells WJ et al (2006) Mesenteric blood flow velocities in the newborn with single-ventricle physiology: modified Blalock-Taussig shunt versus right ventricle-pulmonary artery conduit. Pediatr Crit Care Med 7:132–137CrossRefPubMedGoogle Scholar
  5. 5.
    Downard CD, Grant SN, Matheson PJ, Guillaume AW, Debski R, Fallat ME et al (2011) Altered intestinal microcirculation is the critical event in the development of necrotizing enterocolitis. J Pediatr Surg 46:1023–1028CrossRefPubMedGoogle Scholar
  6. 6.
    Frommelt PC, Gerstenberger E, Baffa J, Border WL, Bradley TJ, Colan S et al (2013) Doppler flow patterns in the right ventricle-to-pulmonary artery shunt and neo-aorta in infants with single right ventricle anomalies: Impact on outcome after initial staged palliations. J Am Soc Echocardiogr 26:521–529PubMedCentralCrossRefPubMedGoogle Scholar
  7. 7.
    Golbus JR, Wojcik BM, Charpie JR, Hirsch JC (2011) Feeding complications in hypoplastic left heart syndrome after the Norwood procedure: a systematic review of the literature. Pediatr Cardiol 32:539–552CrossRefPubMedGoogle Scholar
  8. 8.
    Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG (2009) Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform 42:377–381PubMedCentralCrossRefPubMedGoogle Scholar
  9. 9.
    Iannucci GJ, Oster ME, Mahle WT (2013) Necrotising enterocolitis in infants with congenital heart disease: the role of enteral feeds. Cardiol Young 23:553–559CrossRefPubMedGoogle Scholar
  10. 10.
    Jeffries HE, Wells WJ, Starnes VA, Wetzel RC, Moromisato DY (2006) Gastrointestinal morbidity after Norwood palliation for hypoplastic left heart syndrome. Ann Thorac Surg 81:982–987CrossRefPubMedGoogle Scholar
  11. 11.
    Johnson JN, Ansong AK, Li JS, Xu M, Gorentz J, Hehir DA et al (2011) Celiac artery flow pattern in infants with single right ventricle following the Norwood procedure with a modified Blalock-Taussig or right ventricle to pulmonary artery shunt. Pediatr Cardiol 32:479–486PubMedCentralCrossRefPubMedGoogle Scholar
  12. 12.
    McElhinney DB, Hedrick HL, Bush DM, Pereira GR, Stafford PW, Gaynor JW et al (2000) Necrotizing enterocolitis in neonates with congenital heart disease: risk factors and outcomes. Pediatrics 106:1080–1087CrossRefPubMedGoogle Scholar
  13. 13.
    McElhinney DB, Benson CB, Brown DW, Wilkins-Haug LE, Marshall AC, Zaccagnini L et al (2010) Cerebral blood flow characteristics and biometry in fetuses undergoing prenatal intervention for aortic stenosis with evolving hypoplastic left heart syndrome. Ultrasound Med Biol 36:29–37PubMedCentralCrossRefPubMedGoogle Scholar
  14. 14.
    Neu J (1996) Necrotizing enterocolitis: the search for a unifying pathogenic theory leading to prevention. Pediatr Clin North Am 43:409–432CrossRefPubMedGoogle Scholar
  15. 15.
    Olsen IE, Groveman SA, Lawson ML, Clark RH, Zemel BS (2010) New intrauterine growth curves based on United States data. Pediatrics 125:e214–e224CrossRefPubMedGoogle Scholar
  16. 16.
    Payne JA, Alexander BT, Khalil RA (2003) Reduced endothelial vascular relaxation in growth-restricted offspring of pregnant rats with reduced uterine perfusion. Hypertension 42:768–774CrossRefPubMedGoogle Scholar
  17. 17.
    Silvilairat S, Cetta F, Biliciler-Denktas G, Ammash NM, Cabalka AK, Hagler DJ et al (2008) Abdominal aortic pulsed wave Doppler patterns reliably reflect clinical severity in patients with coarctation of the aorta. Congenit Heart Dis 3:422–430CrossRefPubMedGoogle Scholar
  18. 18.
    Szwast A, Tian Z, McCann M, Soffer D, Rychik J (2012) Comparative analysis of cerebrovascular resistance in fetuses with single-ventricle congenital heart disease. Ultrasound Obstet Gynecol 40:62–67CrossRefPubMedGoogle Scholar
  19. 19.
    Verburg BO, Jaddoe VW, Wladimiroff JW, Hofman A, Witteman JC, Steegers EA (2008) Fetal hemodynamic adaptive changes related to intrauterine growth: the Generation R Study. Circulation 117:649–659CrossRefPubMedGoogle Scholar
  20. 20.
    Yamamoto Y, Khoo NS, Brooks PA, Savard W, Hirose A, Hornberger LK (2013) Severe left heart obstruction with retrograde arch flow importantly influences fetal cerebral and placental blood flow. Ultrasound Obstet Gynecol. doi: 10.1002/uog.12448 Google Scholar
  21. 21.
    Zani A, Eaton S, Leon FF, Malerba A, Hall NJ, De Coppi P et al (2008) Captopril reduces the severity of bowel damage in a neonatal rat model of necrotizing enterocolitis. J Pediatr Surg 43:308–314CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Thomas A. Miller
    • 1
  • L. LuAnn Minich
    • 1
  • Linda M. Lambert
    • 2
  • Lisa Joss-Moore
    • 3
  • Michael D. Puchalski
    • 1
  1. 1.Division of Pediatric Cardiology, Department of PediatricsUniversity of UtahSalt Lake CityUSA
  2. 2.Division of Cardiothoracic Surgery, Department of SurgeryUniversity of UtahSalt Lake CityUSA
  3. 3.Division of Neonatology, Department of PediatricsUniversity of UtahSalt Lake CityUSA

Personalised recommendations