Prenatal exposure to Hurricane Maria is associated with an altered infant nasal microbiome

Abstract

Background: Prenatal adverse exposures have been associated with increased risks of development of respiratory diseases in children. The infant nasal microbiome is an important mechanism and indicator.

Objective: Our aim was to characterize and compare the nasal microbiome of infants who were in utero and exposed to Hurricane Maria in Puerto Rico during 2017 with that of infants who were conceived at least 5 months after the hurricane as controls.

Methods: We recruited 63 vaginally born infants, 29 of whom were in the exposure group and 34 of whom were in the control group. Nasal swab samples were collected and analyzed by using 16S ribosomal RNA gene sequencing at the community and taxon levels, respectively.

Results: Infants in the exposure group were more likely to harbor a Staphylococcus-Streptococcus-dominant microbial community in their nose. The richness and diversity of the microbiome was significantly higher in the exposure group than in the control group. In the exposure group, the bacterial genera Rhodocista, Azospirillum, Massilia, Herbaspirillum, Aquabacterium, and Pseudomonas were enriched, whereas Corynebacterium and Ralstonia were depleted. Food insecurity due to Hurricane Maria was associated with an increase in Pseudomonas in the infant nasal microbiome.

Conclusion: Infants who were exposed to Hurricane Maria during gestation had an altered nasal microbiome, with a higher prevalence of environmental bacteria. More research is needed to evaluate the long-term impacts of extreme weather events occurring in the prenatal stage on a child's nasal microbiome and respiratory health.

Keywords: Prenatal maternal; asthma; disaster; extreme weather event; hurricane; in utero; infant nasal microbiome; nasal swab; respiratory infection; upper airway bacteria.

Fig 1

Location of the study area and municipalities in Puerto Rico in which the study participants resided.

Fig 2

Characterization of the infant nasal microbiome by community type. A, Stacked plots showing the average relative abundances of the top 10 bacterial genera detected in each nasal swab sample grouped by the community types. Community type A is codominated by Corynebacterium and Dolosigranulum, community type B is codominated by Staphylococcus and Streptococcus, community type C is dominated by Corynebacterium, and community type D is dominated by Moraxella. B, The relative abundance of dominated genera in each community type. C, α-Diversity analyses (observed number of taxa and Shannon index value) by community type. D, PCoA plot based on the weighted UniFrac distance matrix and unweighted UniFrac distance, (analysis of similarities; P = .001). Statistical significance in (B) and (C) was determined by using the pairwise Wilcoxon rank sum test; P values were adjusted by using the Benjamini and Hochberg method. Statistical significance in (D) was determined by using the analysis of similarities test. PC, Principal coordinate.

Fig 3

Evaluation of the infant nasal microbiome at the community level by exposure status. A, α-Diversity analyses (observed number of taxa and Shannon index value) between the exposure and control groups. B, α-Diversity of the infant nasal microbiome for each phylum by exposure status. C, PCoA plot by exposure status based on the weighted UniFrac distances or unweighted UniFrac distances. Statistical significance in (A) and (B) was determined by using the Wilcoxon rank sum test. Statistical significance in (C) was determined by using the analysis of similarities test. PC, Principal coordinate.

Fig 4

Subgroup analyses of the infant nasal microbiome at the community level. A, α-Diversity (observed number of taxa and Shannon index value) in subgroup analyses between the exposure and control groups. B, PCoA plots in subgroup analyses between the exposure and control groups. Statistical significance in (A) was determined by using the Wilcoxon rank sum test. Statistical significance in (B) was determined by using the analysis of similarities test. PC, Principal coordinate.

Fig 5

Differentially abundant bacterial genera identified in the nasal microbiome between infants who were exposed to Hurricane Maria in utero with those who were not. A, Volcano plot showing the fold change (FC) and P values of all of the genera using the DESeq2 algorithm. The dots in red or blue represent significant genera identified after adjustment for multiple comparisons using the Benjamini and Hochberg methods. B, Bar plot showing the FC and SE of the significantly different genera. C, The relative abundance of Pseudomonas by maternal prenatal food access in the exposure group (n = 29).