Improved feeding tolerance and growth are linked to increased gut microbial community diversity in very-low-birth-weight infants fed mother's own milk compared with donor breast milk

Study information

Reviewed Marked as Reviewed by Peace Sandy on 2024-2-21

study design

prospective cohort

Citation

PMID PubMed identifier for scientific articles.

30982856

DOI Digital object identifier for electronic documents.

10.1093/ajcn/nqz006

URI

https://pubmed.ncbi.nlm.nih.gov/30982856/

Authors

Ford SL, Lohmann P, Preidis GA, Gordon PS, O'Donnell A, Hagan J, Venkatachalam A, Balderas M, Luna RA, Hair AB

Journal

The American journal of clinical nutrition

Year

2019

Keywords:

breast milk, donor milk, feeding intolerance, growth, microbiota, neonate, premature infant, very low birth weight

BACKGROUND: Mother's own milk (MOM) is protective against gut microbiota alterations associated with necrotizing enterocolitis (NEC) and feeding intolerance among preterm infants. It is unclear whether this benefit is preserved with donor milk (DM) feeding. OBJECTIVE: We aimed to compare microbiota development, growth, and feeding tolerance in very-low-birth-weight (VLBW) infants fed an exclusively human milk diet of primarily MOM or DM. METHODS: One hundred and twenty-five VLBW infants born at Texas Children's Hospital were enrolled and grouped into cohorts based on percentage of MOM and DM in enteral feeds. Feeds were fortified with DM-derived fortifier per unit protocol. Weekly stool samples were collected for 6 wk for microbiota analysis [16S ribosomal RNA (rRNA) sequencing]. A research nurse obtained weekly anthropometrics. Clinical outcomes were compared via Wilcoxon's rank-sum test and Fisher's exact test, as well as multivariate analysis. RESULTS: The DM cohort (n = 43) received on average 14% mothers' milk compared with 91% for the MOM cohort (n = 74). Diversity of gut microbiota across all time points (n = 546) combined was increased in MOM infants (P < 0.001). By 4 and 6 wk of life, microbiota in MOM infants contained increased abundance of Bifidobacterium (P = 0.02) and Bacteroides (P = 0.04), whereas DM-fed infants had increased abundance of Staphylococcus (P = 0.02). MOM-fed infants experienced a 60% reduction in feeding intolerance (P = 0.03 by multivariate analysis) compared with DM-fed infants. MOM-fed infants had greater weight gain than DM-fed infants. CONCLUSIONS: Compared with DM-fed infants, MOM-fed infants have increased gut microbial community diversity at the phylum and genus levels by 4 and 6 wk of life, as well as better feeding tolerance. MOM-fed infants had superior growth. The incidence of NEC and other gastrointestinal morbidity is low among VLBW infants fed an exclusively human milk diet including DM-derived fortifier. This trial was registered at clinicaltrials.gov as NCT02573779.

Experiment 1

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-21

Curated date: 2022/06/29

Curator: Uyokeeswaran

Revision editor(s): Uyokeeswaran, Aiyshaaaa, Atrayees

Subjects

Location of subjects: United States of America

Host species Species from which microbiome was sampled. Contact us to have more species added.: Homo sapiens

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology: Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces,feces

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology: Maternal milk mother's own milk,breast milk,Maternal milk,maternal milk

Group 0 name Corresponds to the control (unexposed) group for case-control studies: DM (Donor's Milk)

Group 1 name Corresponds to the case (exposed) group for case-control studies: MOM (Mother's own milk)

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group: Mother's own milk group consists of infants who drank at least >50% of mother's own milk. Any less and they were placed in the other cohort.

Group 0 sample size Number of subjects in the control (unexposed) group: 43

Group 1 sample size Number of subjects in the case (exposed) group: 74

Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any): No antibiotic exclusions were listed as infants were at a vulnerable stage in their lives.

Lab analysis

Sequencing type: 16S

16S variable region One or more hypervariable region(s) of the bacterial 16S gene: V4

Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance: Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).: relative abundances

Statistical test: Logistic Regression

Significance threshold p-value or FDR threshold used for differential abundance testing (if any): 0.05

MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?: No

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness: unchanged

Richness Number of species: increased

Signature 1

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-21

Curated date: 2022/06/29

Curator: Uyokeeswaran

Revision editor(s): Uyokeeswaran, Peace Sandy

Source: FIGURE 2C and FIGURE 2 D

Description: (C) When comparing longitudinal changes across samples from all study subjects, increasing relative abundance of Proteobacteria was observed. There were no significant differences observed at the phylum level during the first 2 wk of life. By week 4, microbiota from the MOM cohort had significantly higher abundance of Actinobacteria (P = 0.032) and decreased abundance of Firmicutes (P = 0.011). (D) By week 4, microbiota from the MOM cohort had significantly increased abundance of Bacteroides (P = 0.046), Bifidobacterium (P = 0.026), and Enterococcus (P < 0.001) in comparison to the DM cohort. DM infants had significantly higher abundance of Staphylococcus (P = 0.014). DM, donor human milk; MOM, mother's own milk; PCoA, principal coordinates analysis.

Abundance in Group 1: increased abundance in MOM (Mother's own milk)

NCBI	Quality Control	Links
Actinomycetota
Bacteroides
Bifidobacterium
Enterococcus

Revision editor(s): Uyokeeswaran, Peace Sandy

Signature 2

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Curated date: 2022/06/29

Curator: Uyokeeswaran

Revision editor(s): Uyokeeswaran, Peace Sandy

Source: Figure 2C and Figure 2D

Description: (C) When comparing longitudinal changes across samples from all study subjects, increasing relative abundance of Proteobacteria was observed. There were no significant differences observed at the phylum level during the first 2 wk of life. By week 4, microbiota from the MOM cohort had significantly higher abundance of Actinobacteria (P = 0.032) and decreased abundance of Firmicutes (P = 0.011). (D) By week 4, microbiota from the MOM cohort had significantly increased abundance of Bacteroides (P = 0.046), Bifidobacterium (P = 0.026), and Enterococcus (P < 0.001) in comparison to the DM cohort. DM infants had significantly higher abundance of Staphylococcus (P = 0.014). DM, donor human milk; MOM, mother's own milk; PCoA, principal coordinates analysis.

Abundance in Group 1: decreased abundance in MOM (Mother's own milk)

NCBI	Quality Control	Links
Bacillota
Staphylococcus

Revision editor(s): Uyokeeswaran, Peace Sandy