Effects of parity, blood progesterone, and non-steroidal anti-inflammatory treatment on the dynamics of the uterine microbiota of healthy postpartum dairy cows

Pascottini, Osvaldo Bogado; Sprícigo, J. F. W.; Schyndel, Sabrina J. Van; Mion, B.; Rousseau, Joyce D.; Weese, J. Scott; LeBlanc, S.J.

doi:10.1101/2020.05.18.101766

Cited by 7 publications

(5 citation statements)

References 23 publications

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“…For the present study, 21 cows were retrospectively and deliberately selected to balance as nearly as possible for meloxicam treatment (n = 9 were treated with meloxicam and n = 12 were non-treated control), parity, and uterine health status (described below). Meloxicam treatment did not affect the uterine inflammatory status 19 nor the uterine microbiome composition 20 . This lack of effect allowed us to study the associations between reproductive tract inflammatory disease and the uterine microbiome in the postpartum period.…”

Section: Methodsmentioning

confidence: 86%

Dynamics of uterine microbiota in postpartum dairy cows with clinical or subclinical endometritis

Pascottini

Schyndel

Sprícigo

et al. 2020

Sci Rep

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our objectives were to describe and compare the uterine bacterial composition of postpartum Holstein cows diagnosed as healthy (n = 8), subclinical endometritis (SCE; n = 8), or clinical endometritis (CE; n = 5) in the fifth week postpartum. We did metagenomic analyses of 16S rRNA gene sequences from endometrial cytobrush samples at 10, 21, and 35 days in milk (DIM), and endometrial bacterial culture at 35 DIM. Uterine bacterial composition in healthy, SCE, and CE was stable at 10, 21, and 35 DIM. Alpha and beta diversities showed a different uterine microbiome from CE compared to healthy or SCE, but no differences were found between healthy and SCE cows. At the phylum level, the relative abundance of Bacteroidetes and Fusobacteria, and at genera level, of Trueperella was greater in ce than healthy or Sce cows. Trueperella pyogenes was the predominant bacteria cultured in cows with ce, and a wide variety of bacterial growth was found in healthy and Sce cows. Bacteria that grew in culture were represented within the most abundant bacterial genera based on metagenomic sequencing. the uterine microbiota was similar between Sce and healthy, but the microbiome in cows with ce had a loss of bacterial diversity. Multiple potential mechanisms that drive reproductive tract inflammatory disease in dairy cattle have been discovered 1,2 , but questions remain about the nature and causes of the different manifestations of reproductive tract infection and inflammation. Remarkable changes in the composition of the microbiome occur in postpartum cows that develop uterine disease 3,4 , but few papers have described the dynamics of the uterine microflora in healthy postpartum cows 5,6. A robust but well-regulated postpartum uterine inflammatory response is necessary to avoid disease 7. However, in early lactation, cows experience a state of immune dysfunction concurrent with changes in metabolism associated with physiologic adaptations to support milk production. Although certain phyla and genera of bacteria are reasonably consistently associated with some forms of uterine disease, the changes of the microbiome and the host interaction with it in the progression or avoidance of disease are only partially understood. Metritis (overt systemic illness due to uterine infection, characterized by fetid vaginal discharge) and purulent vaginal discharge (PVD) without systemic signs have commonly been associated with Trueperella pyogenes using culture-dependent methods 8,9,10. Clinical endometritis (CE) is PVD with concurrent endometritis based on > 5% polymorphonuclear (PMN) neutrophils 7,11. However, with the advent of cultureindependent methods using metagenomic sequencing, it has been shown that loss of diversity and increase in abundance of Bacteroides, Porphyromonas, and Fusobacterium were associated with metritis and PVD in postpartum cows 3,4,12. Numerous studies attempted to associate the presence of bacteria with subclinical endometritis (SCE; absence of PVD and > 5% endometrial PMN), but the role of pathogenic bacteria in SCE re...

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Section: Methodsmentioning

confidence: 86%

Dynamics of uterine microbiota in postpartum dairy cows with clinical or subclinical endometritis

Pascottini

Schyndel

Sprícigo

et al. 2020

Sci Rep

Self Cite

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“…Recent studies suggest that microbiome-mediated maternal effects are indeed possible. In several mammals, maternal traits, such as parity (i.e., the number of times a mother has given birth), have been associated with differences in the composition of both maternal [39,60] and offspring microbial communities [10,39]. In nonhuman primates (vervet monkeys: Chlorocebus pygerythrus), infants born to low-parity mothers harbored reduced microbial diversity and a greater abundance of Bacteroides fragilis [10], a bacterium derived from the milk microbiota that is specialized in digesting milk glycans [61,62].…”

Section: Introductionmentioning

confidence: 99%

Maternal effects on early-life gut microbiome maturation in a wild nonhuman primate

Baniel

Petrullo

Mercer

et al. 2021

Preprint

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Early-life gut microbial colonization is an important process shaping host physiology, immunity and long-term health outcomes in humans and other animals. However, our understanding of this dynamic process remains poorly investigated in wild animals, where developmental mechanisms can be better understood within ecological and evolutionary relevant contexts. Using 16s rRNA amplicon sequencing on 525 fecal samples from a large cohort of infant and juvenile geladas (Theropithecus gelada), we characterized gut microbiome maturation during the first three years of life and assessed the role of maternal effects in shaping offspring microbiome assembly. Microbial diversity increased rapidly in the first months of life, followed by more gradual changes until weaning. As expected, changes in gut microbiome composition and function with increasing age reflected progressive dietary transitions: in early infancy when infants rely heavily on their mother’s milk, microbes that facilitate milk glycans and lactose utilization dominated, while later in development as graminoids are progressively introduced into the diet, microbes that metabolize plant complex polysaccharides became dominant. Furthermore, the microbial community of nursing infants born to first-time (primiparous) mothers was more “milk-oriented” compared to similarly-aged infants born to experienced (multiparous) mothers. Comparisons of matched mother-offspring fecal samples to random dyads did not support vertical transmission as a conduit for these maternal effects, which instead could be explained by slower phenotypic development (and associated slower gut microbiome maturation) in infants born to first-time mothers. Together, our findings highlight the dynamic nature of gut colonization in early life and the role of maternal effects in modulating this trajectory in a wild primate.

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“…Since both the maternal gut microbiome and parity have been identified as key determinants of gestational health, it is important to understand whether parity influences the microbiome during pregnancy. Previous studies in dairy cows have shown that animals pregnant for the first time (nulliparous) have different uterine and rumen microbiome compositions than do animals with only a single prior pregnancy (primiparous) or two or more previous pregnancies (multiparous)[13, 14]. However, it is as yet unclear if parity impacts either the maternal gut microbiome during pregnancy or the microbiome of the developing offspring.…”

Section: Introductionmentioning

confidence: 99%

Remodeling of the maternal gut microbiome during pregnancy is shaped by parity

Berry

Pierdon

Misic

et al. 2020

Preprint

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BackgroundThe maternal microbiome has emerged as an important factor in gestational health and outcome and is associated with risk of preterm birth and offspring morbidity. Epidemiological evidence also points to successive pregnancies – referred to as maternal parity – as a risk factor for preterm birth, infant mortality, and impaired neonatal growth. Despite the fact that both the maternal microbiome and parity are linked to maternal-infant health, the impact of parity on the microbiome remains largely unexplored, in part due to the challenges of studying parity in humans.ResultsUsing synchronized pregnancies and dense longitudinal monitoring of the microbiome in pigs, we describe a microbiome trajectory during pregnancy and determine the extent to which parity modulates this trajectory. We show that the microbiome changes reproducibly during gestation and that this remodeling occurs more rapidly as parity increases. At the time of parturition, parity was linked to the relative abundance of several bacterial species, including Treponema bryantii, Lactobacillus amylovorus, and Lactobacillus reuteri. Strain tracking carried out in 18 maternal-offspring ‘quadrads’ – each consisting of one mother sow and three piglets – linked maternal parity to altered levels of Akkermansia muciniphila, Prevotella stercorea, and Campylobacter coli in the infant gut 10 days after birth.ConclusionsCollectively, these results identify parity as an important environmental factor that modulates the gut microbiome during pregnancy and highlight the utility of a swine model for investigating the microbiome in maternal-infant health. In addition, our data show that the impact of parity extends beyond the mother and is associated with alterations in the community of bacteria that colonize the offspring gut early in life. The bacterial species we identified as parity-associated in the mother and offspring have been shown to influence host metabolism in other systems, raising the possibility that such changes may influence host nutrient acquisition or utilization. These findings, taken together with our observation that even subtle differences in parity are associated with microbiome changes, underscore the importance of considering parity in the design and analysis of human microbiome studies during pregnancy and in infants.

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Effects of parity, blood progesterone, and non-steroidal anti-inflammatory treatment on the dynamics of the uterine microbiota of healthy postpartum dairy cows

Cited by 7 publications

References 23 publications

Dynamics of uterine microbiota in postpartum dairy cows with clinical or subclinical endometritis

Dynamics of uterine microbiota in postpartum dairy cows with clinical or subclinical endometritis

Maternal effects on early-life gut microbiome maturation in a wild nonhuman primate

Remodeling of the maternal gut microbiome during pregnancy is shaped by parity

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