Maternal Antenatal Treatments Influence Initial Oral Microbial Acquisition in Preterm Infants

Abstract

Objective The purpose of this study was to analyze the association of maternal antenatal therapy on initial preterm infant oral microbial acquisition of gut metabolically important bacteria: Firmicutes, Bacteroidetes, Lactobacillus, Bifidobacterium, and Bacteroides species.

Study Design Infant oral samples were collected prefeeding at 24 hours and analyzed using group-specific primers by real-time 16S rRNA quantitative polymerase chain reaction with analysis of variance and logistic regression to evaluate effect of antenatal exposure.

Results Sixty-five infants <34 weeks' gestational age (GA) were evaluated; mean GA was 28.6 ± 2.6 (standard deviation) weeks. Infants unexposed to antenatal treatment (n = 5) acquired <1% Firmicutes, which was composed of 100% Lactobacillus species with no detectable Bifidobacterium, Bacteroidetes, or Bacteroides species. Infants exposed to antibiotics (n = 7), acquired fivefold less total bacterial density (TBD) with 45% Firmicutes 1.3% Lactobacillus species, 23.5% Bacteroidetes and rare Bacteroides. Compared with unexposed infants, steroids (n = 26) or steroid and antibiotics (n = 27) exposure led to an eightfold increase in TBD with <1% Lactobacillus species and Bacteroides species 100% and 30%, respectively (p < 0.04). Bifidobacterium was undetectable in all groups.

Conclusion Preterm infant exposure to routine maternal antenatal treatments influence early oral microbial acquisition during the primary hours related to establishment of gut commensal bacteria.

Keywords

antenatal therapy - preterm infant - oral microbiota - Lactobacillus

• References

• 1 Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol 2007; 5: e177
• 2 Mackie RI, Sghir A, Gaskins HR. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 1999; 69: 1035S-1045S
• 3 Fanaro S, Chierici R, Guerrini P, Vigi V. Intestinal microflora in early infancy: composition and development. Acta Paediatr Suppl 2003; 91: 48-55
• 4 Alexander VN, Northrup V, Bizzarro MJ. Antibiotic exposure in the newborn intensive care unit and the risk of necrotizing enterocolitis. J Pediatr 2011; 159: 392-397
• 5 Grönlund MM, Lehtonen OP, Eerola E, Kero P. Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J Pediatr Gastroenterol Nutr 1999; 28: 19-25
• 6 Li Y, Caufield PW, Dasanayake AP, Wiener HW, Vermund SH. Mode of delivery and other maternal factors influence the acquisition of Streptococcus mutans in infants. J Dent Res 2005; 84: 806-811
• 7 Kalliomäki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol 2001; 107: 129-134
• 8 Roberts D, Dalziel S. Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth (review). Coch Collab 2006; (4) 1-141
• 9 Ward RM. Pharmacologic enhancement of fetal lung maturation. Clin Perinatol 1994; 21: 523-542
• 10 Lee BH, Stoll BJ, McDonald SA, Higgins RD. National Institute of Child Health and Human Development Neonatal Research Network. Adverse neonatal outcomes associated with antenatal dexamethasone versus antenatal betamethasone. Pediatrics 2006; 117: 1503-1510
• 11 American College of Obstetricians and Gynecologists Committee on Obstetric Practice. ACOG Committee Opinion No. 402: Antenatal corticosteroid therapy for fetal maturation. Obstet Gynecol 2008; 111: 805-807
• 12 Guo X, Xia X, Tang R, Zhou J, Zhao H, Wang K. Development of a real-time PCR method for Firmicutes and Bacteroidetes in faeces and its application to quantify intestinal population of obese and lean pigs. Lett Appl Microbiol 2008; 47: 367-373
• 13 Fierer N, Jackson JA, Vilgalys R, Jackson RB. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 2005; 71: 4117-4120
• 14 Armougom F, Henry M, Vialettes B, Raccah D, Raoult D. Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and Methanogens in anorexic patients. PLoS ONE 2009; 4: e7125
• 15 Matsuki T, Watanabe K, Fujimoto J , et al. Quantitative PCR with 16S rRNA-gene-targeted species-specific primers for analysis of human intestinal bifidobacteria. Appl Environ Microbiol 2004; 70: 167-173
• 16 Guo X, Xia X, Tang R, Wang K. Real-time PCR quantification of the predominant bacterial divisions in the distal gut of Meishan and Landrace pigs. Anaerobe 2008; 14: 224-228
• 17 Rook GA, Stanford JL. Give us this day our daily germs. Immunol Today 1998; 19: 113-116
• 18 Stappenbeck TS, Hooper LV, Gordon JI. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci U S A 2002; 99: 15451-15455
• 19 Thompson FM, Catto-Smith AG, Moore D, Davidson G, Cummins AG. Epithelial growth of the small intestine in human infants. J Pediatr Gastroenterol Nutr 1998; 26: 506-512
• 20 Xu J, Gordon JI. Honor thy symbionts. Proc Natl Acad Sci U S A 2003; 100: 10452-10459
• 21 Lin HC, Su BH, Chen AC , et al. Oral probiotics reduce the incidence and severity of necrotizing enterocolitis in very low birth weight infants. Pediatrics 2005; 115: 1-4
• 22 Kalliomäki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 2001; 357: 1076-1079
• 23 Dotterud CK, Storrø O, Johnsen R, Øien T. Probiotics in pregnant women to prevent allergic disease: a randomized, double-blind trial. Br J Dermatol 2010; 163: 616-623
• 24 Liggins GC, Howie RN. A controlled trial of antepartum glucocorticoid treatment for prevention of the respiratory distress syndrome in premature infants. Pediatrics 1972; 50: 515-525
• 25 Crowley P, Chalmers I, Keirse MJ. The effects of corticosteroid administration before preterm delivery: an overview of the evidence from controlled trials. Br J Obstet Gynaecol 1990; 97: 11-25
• 26 Bauer CR, Morrison JC, Poole WK , et al. A decreased incidence of necrotizing enterocolitis after prenatal glucocorticoid therapy. Pediatrics 1984; 73: 682-688
• 27 Jauréguy F, Carton M, Panel P, Foucaud P, Butel M-J, Doucet-Populaire F. Effects of intrapartum penicillin prophylaxis on intestinal bacterial colonization in infants. J Clin Microbiol 2004; 42: 5184-5188
• 28 Sullivan A, Edlund C, Nord CE. Effect of antimicrobial agents on the ecological balance of human microflora. Lancet Infect Dis 2001; 1: 101-114
• 29 Jernberg C, Löfmark S, Edlund C, Jansson JK. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J 2007; 1: 56-66