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Research Paper

Effects of breastfeeding on children’s gut colonization with multidrug-resistant Enterobacterales in peri-urban Lima, Peru

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Article: 2309681 | Received 24 Jul 2023, Accepted 19 Jan 2024, Published online: 01 Feb 2024
 

ABSTRACT

Children living in low-resource settings are frequently gut-colonized with multidrug-resistant bacteria. We explored whether breastfeeding may protect against children’s incident gut colonization with extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-Ec) and Klebsiella, Enterobacter, or Citrobacter spp. (ESBL-KEC). We screened 937 monthly stool samples collected from 112 children aged 1–16 months during a 2016–19 prospective cohort study of enteric infections in peri-urban Lima. We used 52,816 daily surveys to examine how exposures to breastfeeding in the 30 days prior to a stool sample were associated with children’s risks of incident gut-colonization, controlling for antibiotic use and other covariates. We sequenced 78 ESBL-Ec from 47 children to explore their diversity. Gut-colonization with ESBL-Ec was increasingly prevalent as children aged, approaching 75% by 16 months, while ESBL-KEC prevalence fluctuated between 18% and 36%. Through 6 months of age, exclusively providing human milk in the 30 days prior to a stool sample did not reduce children’s risk of incident gut-colonization with ESBL-Ec or ESBL-KEC. From 6 to 16 months of age, every 3 additional days of breastfeeding in the prior 30 days was associated with 6% lower risk of incident ESBL-Ec gut-colonization (95% CI: 0.90, 0.98, p = .003). No effects were observed on incident ESBL-KEC colonization. We detected highly diverse ESBL-Ec among children and few differences between children who were predominantly breastfed (mean age: 4.1 months) versus older children (10.8 months). Continued breastfeeding after 6 months conferred protection against children’s incident gut colonization with ESBL-Ec in this setting. Policies supporting continued breastfeeding should be considered in efforts to combat antibiotic resistance.

Acknowledgments

We thank all field workers and the community of Villa El Salvador for their collaboration. We thank Lucero Arias and Mayra Ochoa for their assistance in the lab, David Snydman and Laura McDermott for their technical support, Ashlee Earl for input on study design, and Paola Sebastiani for input on statistical methods.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Authors’ contributions

MLN, MJP, SC, AJP, and RHG conceptualized the study. MJP, MC, and MLN supervised and LRS and JMS performed laboratory analyses. MLN, MJP, and AJP contributed to statistical analyses. MJP, MS, RHG, and LZC oversaw field activities in the original trial. MLN wrote the first draft of the manuscript. All authors edited the final manuscript.

Availability of data and materials

Short-read data are available in NCBI’s Sequence Read Archive (https://www.ncbi.nlm.nih.gov/sra) under BioProject number PRJNA821865. Other datasets analyzed here are available from the corresponding author upon reasonable request.

Ethics approval and consent to participate

The cohort study was approved by the Institutional Review Boards of Asociación Benefica PRISMA, Universidad Peruana Cayetano Heredia, and Johns Hopkins University. Written informed consent was obtained from caretakers of the infants for both study participation and the use of collected specimens for subsequent research. The analysis of stool specimens for this substudy was approved by the Institutional Review Boards of Asociación Benefica PRISMA and Universidad Peruana Cayetano Heredia (no. 201592). The analysis of de-identified participant data linked to stool specimen results was determined to be not human subjects research by the Health Sciences Institutional Review Board of Tufts University.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/19490976.2024.2309681

Additional information

Funding

This work was supported by NIH R01AI108695-01A1, NIH award KL2TR002545, and a Tufts Springboard award. MLN’s contributions were supported by the Stuart B. Levy Center for Integrated Management of Antimicrobial Resistance at Tufts (Levy CIMAR), a collaboration of Tufts Medical Center and the Tufts University Office of the Vice Provost for Research (OVPR) Research and Scholarship Strategic Plan (RSSP).