Disinfection of Maternal Environments Is Associated with Piglet Microbiome Composition from Birth to Weaning

Law, Kayla; Lozinski, Brigit; Torres, Ivanellis; Davison, Samuel; Hilbrands, A. M.; Nelson, Emma; Parra, Jorge Eduardo Duque; Johnston, Lee J; Gómez, Andrés

doi:10.1128/msphere.00663-21

Cited by 20 publications

(26 citation statements)

References 76 publications

(93 reference statements)

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“…The relative contribution of the milk and breast skin microbiota to the piglets was lower than that of other sow sources of transmission, which was not consistent with previous reports on the sources of gut microbiota in breastfed infants ( Pannaraj et al, 2017 ). This finding may be due to the previous study sequencing only communities from milk and areolar skin while ignoring other maternal or environmental sources, which may have influenced the results of the source-tracking estimates ( Knights et al, 2011 ; Chen et al, 2018 ; Law et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

“…Another reason might be the major differences in how piglets and human infants are raised. Other studies with pigs have also shown that milk has limited effects on the colonization of the piglet gut microbiota ( Chen et al, 2018 ; Law et al, 2021 ). Overall, our results reinforce the importance of this vertical sow-to-piglet microbial transmission from multiple sources, and further studies are needed to elucidate the mechanism of microbial vertical transmission.…”

Section: Discussionmentioning

confidence: 99%

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Selective Maternal Seeding and Rearing Environment From Birth to Weaning Shape the Developing Piglet Gut Microbiome

Chen

Jiang

et al. 2022

Front. Microbiol.

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The acquisition and development of the mammalian microbiome early in life are critical to establish a healthy host-microbiome symbiosis. Despite recent advances in understanding microbial sources in infants, the relative contribution of various microbial sources to the colonization of the gut microbiota in pigs remains unclear. Here, we longitudinally sampled the microbiota of 20 sow-piglet pairs (three piglets per sow) reared under identical conditions from multiple body sites and the surrounding weaning environment from birth to 28 days postpartum (1,119 samples in total). Source-tracking analysis revealed that the contribution of various microbial sources to the piglet gut microbiome gradually changed over time. The neonatal microbiota was initially sparsely populated, and the predominant contribution was from the maternal vaginal microbiota that increased gradually from 69.0% at day 0 to 89.3% at day 3 and dropped to 0.28% at day 28. As the piglets aged, the major microbial community patterns were most strongly associated with the sow feces and slatted floor, with contributions increasing from 0.52 and 9.6% at day 0 to 62.1 and 33.8% at day 28, respectively. The intestinal microbial diversity, composition, and function significantly changed as the piglets aged, and 30 age-discriminatory bacterial taxa were identified with distinctive time-dependent shifts in their relative abundance, which likely reflected the effect of the maternal and environmental microbial sources on the selection and adaptation of the piglet gut microbiota. Overall, these data demonstrate that the vaginal microbiota is the primary source of the gut microbiota in piglets within 3 days after birth and are gradually replaced by the sow fecal and slatted floor microbiota over time. These findings may offer novel strategies to promote the establishment of exogenous symbiotic microbes to improve piglet gut health.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Selective Maternal Seeding and Rearing Environment From Birth to Weaning Shape the Developing Piglet Gut Microbiome

Chen

Jiang

et al. 2022

Front. Microbiol.

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“…Livestock is usually managed in intensive farming conditions under the so-called all-in/all-out system, in which facilities are emptied and cleaned between batches. Considering the potential effect of the environment on the establishment of the microbiota after weaning ( 8 ) and the lack of specific studies addressing it in piglets at weaning, we decided to evaluate the extent to which the cleaning protocol influenced the reshaping of the pigs’ microbiota a week after weaning. Analyses of the factors influencing microbiota ordination clearly reflected, regardless of the cleaning protocol applied or the trial, that the in-feed treatment (ZnO, apramycin, or control diet) was the factor shaping the gut microbiota.…”

Section: Discussionmentioning

confidence: 99%

“…Indeed, early establishment of a desirable microbiota after weaning can promote intestinal health and prevent enteric diseases ( 3 , 7 ). The postweaning microbiota is influenced by factors such as the mother’s microbiota, the environment and cleaning protocols used ( 8 ), and in particular, diet ( 9 ). Despite this generally accepted view, the importance of each individual factor is still not well understood.…”

Section: Introductionmentioning

confidence: 99%

Using Shotgun Sequencing to Describe the Changes Induced by In-Feed Zinc Oxide and Apramycin in the Microbiomes of Pigs One Week Postweaning

et al. 2022

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Weaning is a critical period for piglets, during which potentially harmful bacteria such as Escherichia coli can increase in abundance in the intestine, creating digestive problems and diarrhea. In-feed antibiotics, the most frequent administration route for antibiotics in livestock, and therapeutic doses of zinc oxide (ZnO) help to control diarrhea but prompt secondary problems such as antimicrobial resistance and soil pollution from heavy metals.

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“…This may be due to both sampler bias (a single person collected all samples in each country) and farm environment, practices, and regulations that vary by country. The piglet microbiota may for instance be influenced by factors such as cleaning, feed composition, temperature, and antimicrobial treatment [34][35][36][37][38][39][40][41]. However, the microbiota composition was not more similar on farms with comparable management practices.…”

Section: Discussionmentioning

confidence: 99%

Streptococcus suis infection on European farms is associated with an altered tonsil microbiome and resistome

Fredriksen

Neila‐Ibáñez

Hennig-Pauka

et al. 2022

Preprint

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Introduction Streptoccocus suis is a Gram-positive opportunistic pathogen causing systemic disease in piglets around weaning age. Outbreaks of S. suis disease are controlled by metaphylactic use of antibiotics, leading to high levels of antimicrobial resistance in S. suis isolates. This is an issue for both animal and human health due to the zoonotic disease potential of S. suis. The mechanisms facilitating invasive disease are not known but may involve host and environmental factors. The palatine tonsils are considered a portal of entry for pathogenic strains to cause systemic disease. We hypothesised that tonsil colonization by pathogenic and commensal bacteria may impact on disease risk via colonization resistance and co-infections. We conducted a case-control study on 9 European farms, comparing the tonsil microbiome of piglets with S. suis systemic disease with asymptomatic controls. We also compared these to piglets on control farms and piglets reared naturally in a forest. Results We found a small but significant difference in the tonsil microbiota composition of case and control piglets. Case-control associations varied between amplicon sequence variants (ASVs) and metagenome assembled genomes (MAGs) within the same species. Variants of putatively commensal taxa including Rothia nasimurium were reduced in abundance in case piglets compared to asymptomatic controls. Case piglets had higher relative abundance of Fusobacterium gastrosuis, Bacteroides heparinolyticus, and uncultured Prevotella and Alloprevotella species. There was, however, no higher abundance of S. suis itself at the species-level or of clinical strain marker genes in case piglets. Piglets sampled prospectively weeks prior to developing clinical signs had reduced microbiota alpha diversity. Despite case-control pairs receiving equal antimicrobial treatment, case piglets had higher abundance of antimicrobial resistance genes (ARGs) conferring resistance to antimicrobial classes used to treat S. suis. Conclusions The tonsillar microbiota of S. suis case piglets had increased abundance of taxa not previously linked to S. suis disease. This coincided with increased ARG abundance in case piglets, possibly due to adaptation of the disease-associated microbiota to frequent antimicrobial treatment.

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Disinfection of Maternal Environments Is Associated with Piglet Microbiome Composition from Birth to Weaning

Cited by 20 publications

References 76 publications

Selective Maternal Seeding and Rearing Environment From Birth to Weaning Shape the Developing Piglet Gut Microbiome

Selective Maternal Seeding and Rearing Environment From Birth to Weaning Shape the Developing Piglet Gut Microbiome

Using Shotgun Sequencing to Describe the Changes Induced by In-Feed Zinc Oxide and Apramycin in the Microbiomes of Pigs One Week Postweaning

Streptococcus suis infection on European farms is associated with an altered tonsil microbiome and resistome

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