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Am J Perinatol 2017; 34(07): 676-683
DOI: 10.1055/s-0036-1597326
Original Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Necrotizing Enterocolitis and Growth in Preterm Infants Fed Predominantly Maternal Milk, Pasteurized Donor Milk, or Preterm Formula: A Retrospective Study

Paula M. Sisk
1   Department of Pediatrics, Wake Forest School of Medicine, Novant Health Forsyth Medical Center, Winston-Salem, North Carolina
,
Tinisha M. Lambeth
1   Department of Pediatrics, Wake Forest School of Medicine, Novant Health Forsyth Medical Center, Winston-Salem, North Carolina
,
Mario A. Rojas
2   Department of Pediatrics, Industrial University of Santander, Bucaramanga, Santander, Colombia
,
Teisha Lightbourne
3   Department of Clinical Nutrition, Children's National Medical Center, Washington, District of Columbia
,
Maria Barahona
1   Department of Pediatrics, Wake Forest School of Medicine, Novant Health Forsyth Medical Center, Winston-Salem, North Carolina
,
Evelyn Anthony
4   Department of Radiology, Brenner Children's Hospital, Wake Forest Baptist Medical Center, Wake Forest School of Medicine, Winston-Salem, North Carolina
,
Sam T. Auringer
5   Department of Radiology, Novant Health Forsyth Medical Center, Winston-Salem, North Carolina
› Author Affiliations
Further Information

Publication History

21 June 2016

03 November 2016

Publication Date:
09 December 2016 (online)

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Abstract

Objective To evaluate the association between necrotizing enterocolitis (NEC), growth, and feeding.

Methods This is a retrospective study of 551 infants (birth weight ≤ 1,500 g, ≤32 weeks' gestation). NEC, Bell's stage ≥ 2, was confirmed by independent review of sentinel radiographs. Feeding type was defined as ≥ 50% maternal milk (MM), pasteurized donor human milk (PDHM), or preterm formula (PF). Demographic and clinical characteristics including growth were compared between the three groups. Multivariable regression analysis was performed to control variables that differed in bivariate analysis.

Results PDHM and PF mothers were more likely to be African-American, be enrolled in Medicaid, and have chorioamnionitis. PF mothers received antenatal steroids less frequently. NEC rates were different by feeding group (MM: 5.3%; PHDM: 4.3%; PF: 11.4%; p = 0.04). Adjusting for group differences, lower gestational age (adjusted odds ratio [aOR]: 0.85; 95% confidence interval [CI]: 0.74–0.97; p = 0.02], and PF (aOR: 2.53; 95% CI: 1.15–5.53; p = 0.02] were associated with NEC. There were no differences in other health outcomes or growth at hospital discharge.

Conclusion MM and PDHM feedings, given until 34 weeks postmenstrual age, were associated with lower rates of NEC in very low birth weight infants without interfering with growth.

Keywords

necrotizing enterocolitis - preterm infant - growth - feeding - preterm formula - maternal milk - pasteurized human donor milk - very low birth weight
 

  • References

  • 1 Stoll BJ, Hansen NI, Bell EF , et al; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network. Trends in care practices, morbidity, and mortality of extremely preterm neonates, 1993–2012. JAMA 2015; 314 (10) 1039-1051
    CrossrefPubMedGoogle Scholar
  • 2 Shah TA, Meinzen-Derr J, Gratton T , et al. Hospital and neurodevelopmental outcomes of extremely low-birth-weight infants with necrotizing enterocolitis and spontaneous intestinal perforation. J Perinatol 2012; 32 (7) 552-558
    CrossrefPubMedGoogle Scholar
  • 3 Yee WH, Soraisham AS, Shah VS, Aziz K, Yoon W, Lee SK ; Canadian Neonatal Network. Incidence and timing of presentation of necrotizing enterocolitis in preterm infants. Pediatrics 2012; 129 (2) e298-e304
    CrossrefPubMedGoogle Scholar
  • 4 Luig M, Lui K ; NSW & ACT NICUS Group. Epidemiology of necrotizing enterocolitis--part II: risks and susceptibility of premature infants during the surfactant era: a regional study. J Paediatr Child Health 2005; 41 (4) 174-179
    CrossrefPubMedGoogle Scholar
  • 5 Ganapathy V, Hay JW, Kim JH. Costs of necrotizing enterocolitis and cost-effectiveness of exclusively human milk-based products in feeding extremely premature infants. Breastfeed Med 2012; 7 (1) 29-37
    CrossrefPubMedGoogle Scholar
  • 6 Sharma R, Hudak ML. A clinical perspective of necrotizing enterocolitis: past, present, and future. Clin Perinatol 2013; 40 (1) 27-51
    CrossrefPubMedGoogle Scholar
  • 7 Stey A, Barnert ES, Tseng CH , et al. Outcomes and costs of surgical treatments of necrotizing enterocolitis. Pediatrics 2015; 135 (5) e1190-e1197
    CrossrefPubMedGoogle Scholar
  • 8 Lucas A, Cole TJ. Breast milk and neonatal necrotising enterocolitis. Lancet 1990; 336 (8730): 1519-1523
    Google Scholar
  • 9 Schanler RJ, Shulman RJ, Lau C. Feeding strategies for premature infants: beneficial outcomes of feeding fortified human milk versus preterm formula. Pediatrics 1999; 103 (6 Pt 1): 1150-1157
    CrossrefPubMedGoogle Scholar
  • 10 Sisk PM, Lovelady CA, Dillard RG, Gruber KJ, O'Shea TM. Early human milk feeding is associated with a lower risk of necrotizing enterocolitis in very low birth weight infants. J Perinatol 2007; 27 (7) 428-433
    CrossrefPubMedGoogle Scholar
  • 11 Meinzen-Derr J, Poindexter B, Wrage L, Morrow AL, Stoll B, Donovan EF. Role of human milk in extremely low birth weight infants' risk of necrotizing enterocolitis or death. J Perinatol 2009; 29 (1) 57-62
    CrossrefPubMedGoogle Scholar
  • 12 Dvorak B, Halpern MD, Holubec H , et al. Maternal milk reduces severity of necrotizing enterocolitis and increases intestinal IL-10 in a neonatal rat model. Pediatr Res 2003; 53 (3) 426-433
    CrossrefPubMedGoogle Scholar
  • 13 Abdelhamid AE, Chuang S-L, Hayes P, Fell JME. In vitro cow's milk protein-specific inflammatory and regulatory cytokine responses in preterm infants with necrotizing enterocolitis and sepsis. Pediatr Res 2011; 69 (2) 165-169
    CrossrefPubMedGoogle Scholar
  • 14 Willems R, Krych L, Rybicki V , et al. Introducing enteral feeding induces intestinal subclinical inflammation and respective chromatin changes in preterm pigs. Epigenomics 2015; 7 (4) 553-565
    CrossrefPubMedGoogle Scholar
  • 15 Taylor SN, Basile LA, Ebeling M, Wagner CL. Intestinal permeability in preterm infants by feeding type: mother's milk versus formula. Breastfeed Med 2009; 4 (1) 11-15
    CrossrefPubMedGoogle Scholar
  • 16 Perrine CG, Scanlon KS. Prevalence of use of human milk in US advanced care neonatal units. Pediatrics 2013; 131 (6) 1066-1071
    CrossrefPubMedGoogle Scholar
  • 17 Colaizy TT. Donor human milk for very low birth weights: patterns of usage, outcomes, and unanswered questions. Curr Opin Pediatr 2015; 27 (2) 172-176
    Google Scholar
  • 18 Quigley M, McGuire W. Formula versus donor breast milk for feeding preterm or low birth weight infants. Cochrane Database Syst Rev 2014; 4 (4) CD002971 . Doi: 10.1002/14651858.CD002971.pub3
    PubMedGoogle Scholar
  • 19 Agostoni C, Buonocore G, Carnielli VP , et al; ESPGHAN Committee on Nutrition. Enteral nutrient supply for preterm infants: commentary from the European Society of Paediatric Gastroenterology, Hepatology and Nutrition Committee on Nutrition. J Pediatr Gastroenterol Nutr 2010; 50 (1) 85-91
    CrossrefPubMedGoogle Scholar
  • 20 Section on Breastfeeding. Breastfeeding and the use of human milk. Pediatrics 2012; 129 (3) e827-e841
    CrossrefPubMedGoogle Scholar
  • 21 Adamkin DH, Radmacher PG. Fortification of human milk in very low birth weight infants (VLBW <1500.  g birth weight). Clin Perinatol 2014; 41 (2) 405-421
    CrossrefPubMedGoogle Scholar
  • 22 Sullivan S, Schanler RJ, Kim JH , et al. An exclusively human milk-based diet is associated with a lower rate of necrotizing enterocolitis than a diet of human milk and bovine milk-based products. J Pediatr 2010; 156 (4) 562-567.e1
    CrossrefPubMedGoogle Scholar
  • 23 Bell MJ, Ternberg JL, Feigin RD , et al. Neonatal necrotizing enterocolitis. Therapeutic decisions based upon clinical staging. Ann Surg 1978; 187 (1) 1-7
    CrossrefPubMedGoogle Scholar
  • 24 Patel AL, Engstrom JL, Meier PP, Jegier BJ, Kimura RE. Calculating postnatal growth velocity in very low birth weight (VLBW) premature infants. J Perinatol 2009; 29 (9) 618-622
    CrossrefPubMedGoogle Scholar
  • 25 Jones F. Best Practice for Expressing, Storing and Handling Human Milk in Hospitals, Homes, and Child Care Settings. 3rd ed. Fort Worth, TX: Human Milk Banking Association of North America; 2011
    Google Scholar
  • 26 Human Milk Banking Association of North America. Guidelines for the Establishment and Operation of a Donor Human Milk Bank. Fort Worth, TX: Human Milk Banking Association of North America; 2015
    Google Scholar
  • 27 Sisk PM, Lovelady CA, Dillard RG, Gruber KJ, O'Shea TM. Maternal and infant characteristics associated with human milk feeding in very low birth weight infants. J Hum Lact 2009; 25 (4) 412-419
    CrossrefPubMedGoogle Scholar
  • 28 García-Muñoz Rodrigo F, Galán Henríquez G, Figueras Aloy J, García-Alix Pérez A. Outcomes of very-low-birth-weight infants exposed to maternal clinical chorioamnionitis: a multicentre study. Neonatology 2014; 106 (3) 229-234
    CrossrefPubMedGoogle Scholar
  • 29 Cristofalo EA, Schanler RJ, Blanco CL , et al. Randomized trial of exclusive human milk versus preterm formula diets in extremely premature infants. J Pediatr 2013; 163 (6) 1592-1595.e1
    Google Scholar
  • 30 Koivusalo A, Kauppinen H, Anttila A , et al. Intraluminal casein model of necrotizing enterocolitis for assessment of mucosal destruction, bacterial translocation, and the effects of allopurinol and N-acetylcysteine. Pediatr Surg Int 2002; 18 (8) 712-717
    CrossrefPubMedGoogle Scholar
  • 31 Thymann T, Møller HK, Stoll B , et al. Carbohydrate maldigestion induces necrotizing enterocolitis in preterm pigs. Am J Physiol Gastrointest Liver Physiol 2009; 297 (6) G1115-G1125
    CrossrefPubMedGoogle Scholar
  • 32 Chowning R, Radmacher P, Lewis S, Serke L, Pettit N, Adamkin DH. A retrospective analysis of the effect of human milk on prevention of necrotizing enterocolitis and postnatal growth. J Perinatol 2016; 36 (3) 221-224
    CrossrefPubMedGoogle Scholar
  • 33 Schanler RJ, Lau C, Hurst NM, Smith EO. Randomized trial of donor human milk versus preterm formula as substitutes for mothers' own milk in the feeding of extremely premature infants. Pediatrics 2005; 116 (2) 400-406
    CrossrefPubMedGoogle Scholar
  • 34 Colaizy TT, Carlson S, Saftlas AF, Morriss Jr FH. Growth in VLBW infants fed predominantly fortified maternal and donor human milk diets: a retrospective cohort study. BMC Pediatr 2012; 12: 124-133
    CrossrefPubMedGoogle Scholar
  • 35 Hair AB, Hawthorne KM, Chetta KE, Abrams SA. Human milk feeding supports adequate growth in infants ≤ 1250 grams birth weight. BMC Res Notes 2013; 6 (1) 459-467
    Google Scholar
  • 36 Corpeleijn WE, de Waard M, Christmann V , et al. Effect of donor milk on severe infections and mortality in very low-birth-weight infants: the early nutrition study randomized clinical trial. JAMA Pediatr 2016; 170 (7) 654-661
    CrossrefPubMedGoogle Scholar
  • 37 Ewaschuk JB, Unger S, Harvey S, O'Connor DL, Field CJ. Effect of pasteurization on immune components of milk: implications for feeding preterm infants. Appl Physiol Nutr Metab 2011; 36 (2) 175-182
    CrossrefPubMedGoogle Scholar
  • 38 Sharma D, Shastri S. Lactoferrin and neonatology - role in neonatal sepsis and necrotizing enterocolitis: present, past and future. J Matern Fetal Neonatal Med 2016; 29 (5) 763-770
    CrossrefPubMedGoogle Scholar
  • 39 Maheshwari A, Kelly DR, Nicola T , et al. TGF-β2 suppresses macrophage cytokine production and mucosal inflammatory responses in the developing intestine. Gastroenterology 2011; 140 (1) 242-253
    CrossrefPubMedGoogle Scholar
  • 40 Goelz R, Hihn E, Hamprecht K , et al. Effects of different CMV-heat-inactivation-methods on growth factors in human breast milk. Pediatr Res 2009; 65 (4) 458-461
    CrossrefPubMedGoogle Scholar
  • 41 Groer M, Duffy A, Morse S , et al. Cytokines, chemokines, and growth factors in banked human donor milk for preterm infants. J Hum Lact 2014; 30 (3) 317-323
    CrossrefPubMedGoogle Scholar
  • 42 Coscia A, Peila C, Bertino E , et al. Effect of holder pasteurisation on human milk glycosaminoglycans. J Pediatr Gastroenterol Nutr 2015; 60 (1) 127-130
    CrossrefPubMedGoogle Scholar
  • 43 Untalan PB, Keeney SE, Palkowetz KH, Rivera A, Goldman AS. Heat susceptibility of interleukin-10 and other cytokines in donor human milk. Breastfeed Med 2009; 4 (3) 137-144
    CrossrefPubMedGoogle Scholar
  • 44 Silvestre D, Ruiz P, Martínez-Costa C, Plaza A, López MC. Effect of pasteurization on the bactericidal capacity of human milk. J Hum Lact 2008; 24 (4) 371-376
    CrossrefPubMedGoogle Scholar
  • 45 Bertino E, Coppa GV, Giuliani F , et al. Effects of Holder pasteurization on human milk oligosaccharides. Int J Immunopathol Pharmacol 2008; 21 (2) 381-385
    CrossrefPubMedGoogle Scholar
  • 46 Ward TL, Hosid S, Ioshikhes I, Altosaar I. Human milk metagenome: a functional capacity analysis. BMC Microbiol 2013; 13: 116 . Doi: 10.1186/1471-2180-13-116
    CrossrefPubMedGoogle Scholar