Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-22T06:20:20.212Z Has data issue: false hasContentIssue false

Maternal group B Streptococcus and the infant gut microbiota

Published online by Cambridge University Press:  12 August 2015

A. E. Cassidy-Bushrow*
Affiliation:
Department of Public Health Sciences, Henry Ford Hospital, One Ford Place, Detroit, MI, USA Center for Allergy, Asthma and Immunology Research, Henry Ford Hospital, Detroit, MI, USA
A. Sitarik
Affiliation:
Department of Public Health Sciences, Henry Ford Hospital, One Ford Place, Detroit, MI, USA Center for Allergy, Asthma and Immunology Research, Henry Ford Hospital, Detroit, MI, USA
A. M. Levin
Affiliation:
Department of Public Health Sciences, Henry Ford Hospital, One Ford Place, Detroit, MI, USA Center for Allergy, Asthma and Immunology Research, Henry Ford Hospital, Detroit, MI, USA
S. V. Lynch
Affiliation:
Department of Medicine, University of California, San Francisco, CA, USA
S. Havstad
Affiliation:
Department of Public Health Sciences, Henry Ford Hospital, One Ford Place, Detroit, MI, USA Center for Allergy, Asthma and Immunology Research, Henry Ford Hospital, Detroit, MI, USA
D. R. Ownby
Affiliation:
Center for Allergy, Asthma and Immunology Research, Henry Ford Hospital, Detroit, MI, USA Department of Pediatrics, Division of Allergy and Clinical Immunology, Georgia Regents University, Augusta, GA, USA
C. C. Johnson
Affiliation:
Department of Public Health Sciences, Henry Ford Hospital, One Ford Place, Detroit, MI, USA Center for Allergy, Asthma and Immunology Research, Henry Ford Hospital, Detroit, MI, USA
G. Wegienka
Affiliation:
Department of Public Health Sciences, Henry Ford Hospital, One Ford Place, Detroit, MI, USA Center for Allergy, Asthma and Immunology Research, Henry Ford Hospital, Detroit, MI, USA
*
*Address for Correspondence: A. E. Cassidy-Bushrow, PhD, MPH, Department of Public Health Sciences, Henry Ford Hospital, 1 Ford Place, 5C, Detroit, MI 48202, USA. (Email [email protected])

Abstract

Early patterns of gut colonization may predispose children to adult disease. Exposures in utero and during delivery are associated with the infant gut microbiome. Although ~35% of women carry group B strep (GBS; Streptococcus agalactiae) during pregnancy, it is unknown if GBS presence influences the infant gut microbiome. As part of a population-based, general risk birth cohort, stool specimens were collected from infant’s diapers at research visits conducted at ~1 and 6 months of age. Using the Illumina MiSeq (San Diego, CA) platform, the V4 region of the bacterial 16S rRNA gene was sequenced. Infant gut bacterial community compositional differences by maternal GBS status were evaluated using permutational multivariate analysis of variance. Individual operational taxonomic units (OTUs) were tested using a zero-inflated negative binomial model. Data on maternal GBS and infant gut microbiota from either 1 (n=112) or 6-month-old stool (n=150) specimens was available on 262 maternal-child pairs. Eighty women (30.5%) were GBS+, of who 58 (72.5%) were given intrapartum antibiotics. After adjusting for maternal race, prenatal antifungal use and intrapartum antibiotics, maternal GBS status was statistically significantly associated with gut bacterial composition in the 6 month visit specimen (Canberra R2=0.008, P=0.008; Unweighted UniFrac R2=0.010, P=0.011). Individual OTU tests revealed that infants of GBS+ mothers were significantly enriched for specific members of the Clostridiaceae, Ruminococcoceae, and Enterococcaceae in the 6 month specimens compared with infants of GBS- mothers. Whether these taxonomic differences in infant gut microbiota at 6 months lead to differential predisposition for adult disease requires additional study.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Penders, J, Stobberingh, EE, van den Brandt, PA, Thijs, C. The role of the intestinal microbiota in the development of atopic disorders. Allergy. 2007; 62, 12231236.Google Scholar
2. Saavedra, JM, Dattilo, AM. Early development of intestinal microbiota: implications for future health. Gastroenterol Clin North Am. 2012; 41, 717731.CrossRefGoogle ScholarPubMed
3. Palmer, C, Bik, EM, DiGiulio, DB, Relman, DA, Brown, PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007; 5, e177.CrossRefGoogle ScholarPubMed
4. Koenig, JE, Spor, A, Scalfone, N, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA. 2011; 108(Suppl. 1), 45784585.CrossRefGoogle ScholarPubMed
5. Dominguez-Bello, MG, Blaser, MJ, Ley, RE, Knight, R. Development of the human gastrointestinal microbiota and insights from high-throughput sequencing. Gastroenterology. 2011; 140, 17131719.CrossRefGoogle ScholarPubMed
6. Adlerberth, I. Factors influencing the establishment of the intestinal microbiota in infancy. Nestle Nutr Workshop Ser Pediatr Program. 2008; 62, 1329.CrossRefGoogle ScholarPubMed
7. Penders, J, Thijs, C, Vink, C, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006; 118, 511521.Google Scholar
8. Azad, MB, Konya, T, Maughan, H, et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013; 185, 385394.CrossRefGoogle ScholarPubMed
9. Dillon, HC Jr., Gray, E, Pass, MA, Gray, BM. Anorectal and vaginal carriage of group B streptococci during pregnancy. J Infect Dis. 1982; 145, 794799.Google Scholar
10. ACOG Committee Opinion: number 279, December 2002. Prevention of early-onset group B streptococcal disease in newborns. Obstet Gynecol. 2002; 100, 14051412.Google Scholar
11. ACOG Committee Opinion No. 485. Prevention of early-onset group B streptococcal disease in newborns. Obstet Gynecol. 2011; 117, 10191027.CrossRefGoogle Scholar
12. Sheehy, A, Davis, D, Homer, CS. Assisting women to make informed choices about screening for Group B Streptococcus in pregnancy: a critical review of the evidence. Women Birth. 2013; 26, 152157.Google Scholar
13. Bedford Russell, AR, Murch, SH. Could peripartum antibiotics have delayed health consequences for the infant? BJOG. 2006; 113, 758765.CrossRefGoogle ScholarPubMed
14. Kubota, T, Nojima, M, Itoh, S. Vaginal bacterial flora of pregnant women colonized with group B streptococcus. J Infect Chemother. 2002; 8, 326330.Google Scholar
15. Bayo, M, Berlanga, M, Agut, M. Vaginal microbiota in healthy pregnant women and prenatal screening of group B streptococci (GBS). Int Microbiol. 2002; 5, 8790.CrossRefGoogle ScholarPubMed
16. Brzychczy-Wloch, M, Pabian, W, Majewska, E, et al. Dynamics of colonization with group B streptococci in relation to normal flora in women during subsequent trimesters of pregnancy. New Microbiol. 2014; 37, 307319.Google Scholar
17. Aloisio, I, Mazzola, G, Corvaglia, LT, et al. Influence of intrapartum antibiotic prophylaxis against group B Streptococcus on the early newborn gut composition and evaluation of the anti-Streptococcus activity of Bifidobacterium strains. Appl Microbiol Biotechnol. 2014; 98, 60516060.Google ScholarPubMed
18. Havstad, S, Wegienka, G, Zoratti, EM, et al. Effect of prenatal indoor pet exposure on the trajectory of total IgE levels in early childhood. J Allergy Clin Immunol. 2011; 128, 880885.CrossRefGoogle ScholarPubMed
19. Wegienka, G, Havstad, S, Joseph, CL, et al. Racial disparities in allergic outcomes in African Americans emerge as early as age 2 years. Clinical & Experimental Allergy. 2012; 42, 909917.CrossRefGoogle Scholar
20. Caporaso, JG, Kuczynski, J, Stombaugh, J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010; 7, 335336.Google Scholar
21. Wegienka, G, Havstad, S, Zoratti, EM, et al. Combined effects of prenatal medication use and delivery type are associated with eczema at age 2 years. Clin Exp Allergy. 2015; 45, 660668.Google Scholar
22. Oken, E, Kleinman, KP, Rich-Edwards, J, Gillman, MW. A nearly continuous measure of birth weight for gestational age using a United States national reference. BMC Pediatr. 2003; 3, 6.Google Scholar
23. Oksanen, J, Guillaume Blanchet, F, Kindt, R. et al. Vegan: community ecology package. R package version 2.0-9. 2013.Google Scholar
24. Chen, J. GUniFrac: Generalized UniFrac distances, 2012. Retrieved 30 January 2015 from http://cran.r-project.org/package=GUniFrac Google Scholar
25. Lozupone, C, Knight, R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005; 71, 82288235.Google Scholar
26. Chen, J, Bittinger, K, Charlson, ES, et al. Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics. 2012; 28, 21062113.Google Scholar
27. Storey, JD, Tibshirani, R. Statistical significance for genomewide studies. Proc Natl Acad Sci USA. 2003; 100, 94409445.CrossRefGoogle ScholarPubMed
28. Olivares, M, Neef, A, Castillejo, G, et al. The HLA-DQ2 genotype selects for early intestinal microbiota composition in infants at high risk of developing coeliac disease. Gut. 2015; 64, 406417.Google Scholar
29. Ling, Z, Li, Z, Liu, X, et al. Altered fecal microbiota composition associated with food allergy in infants. Appl Environ Microbiol. 2014; 80, 25462554.Google Scholar
30. Bryant, AS, Cheng, YW, Caughey, AB. Equality in obstetrical care: racial/ethnic variation in group B streptococcus screening. Matern Child Health J. 2011; 15, 11601165.CrossRefGoogle ScholarPubMed
31. Winn, HN. Group B streptococcus infection in pregnancy. Clinics Perinatol. 2007; 34, 387392.Google Scholar
32. Berardi, A, Rossi, C, Creti, R, et al. Group B streptococcal colonization in 160 mother-baby pairs: a prospective cohort study. J Pediatr. 2013; 163, 10991104 e1091.Google Scholar
33. Van Dyke, MK, Phares, CR, Lynfield, R, et al. Evaluation of universal antenatal screening for group B streptococcus. N Engl J Med. 2009; 360, 26262636.CrossRefGoogle ScholarPubMed
34. Schrag, SJ, Verani, JR. Intrapartum antibiotic prophylaxis for the prevention of perinatal group B streptococcal disease: experience in the United States and implications for a potential group B streptococcal vaccine. Vaccine. 2013; 31(Suppl. 4), D20D26.Google Scholar
35. Jaureguy, F, Carton, M, Panel, P, et al. Effects of intrapartum penicillin prophylaxis on intestinal bacterial colonization in infants. J Clin Microbiol. 2004; 42, 51845188.Google Scholar
36. Arboleya, S, Sanchez, B, Milani, C, et al. Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics. J Pediatr. 2015; 166, 538544.Google Scholar
37. Berardi, A, Rossi, C, Lugli, L, et al. Group B streptococcus late-onset disease: 2003-2010. Pediatrics. 2013; 131, e361e368.Google Scholar
38. Hickman, ME, Rench, MA, Ferrieri, P, Baker, CJ. Changing epidemiology of group B streptococcal colonization. Pediatrics. 1999; 104, 203209.Google Scholar
39. Dominguez-Bello, MG, Costello, EK, Contreras, M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA. 2010; 107, 1197111975.Google Scholar
40. Towers, CV, Rumney, PJ, Asrat, T, et al. The accuracy of late third-trimester antenatal screening for group B streptococcus in predicting colonization at delivery. Am J Perinatol. 2010; 27, 785790.Google Scholar
41. Illuzzi, JL, Bracken, MB. Duration of intrapartum prophylaxis for neonatal group B streptococcal disease: a systematic review. Obstet Gynecol. 2006; 108, 12541265.Google Scholar
42. Berardi, A, Rossi, C, Guidotti, I, et al. Factors associated with intrapartum transmission of group B streptococcus. Pediatr Infect Dis J. 2014; 33, 12111215.Google Scholar
Supplementary material: File

Cassidy-Bushrow supplementary material

Table S1

Download Cassidy-Bushrow supplementary material(File)
File 26.5 KB
Supplementary material: File

Cassidy-Bushrow supplementary material

Table S2

Download Cassidy-Bushrow supplementary material(File)
File 34.7 KB