Productivity of the sow herd is traditionally measured by the number of pigs weaned1 or kilograms of piglets weaned per sow per year.2 Longevity is another factor that can impact herd productivity and is directly affected by disease.3 Antimicrobials are used in all production phases of pig production; and with respect to the sow, they are more frequently used during the lactation phase.4 Reproductive failures and diseases frequently associated with polymicrobial organisms are traditionally controlled with use of in-feed, broad-spectrum antimicrobials.5,6 It is estimated that a sow will be treated with at least one active antimicrobial ingredient for an average 3.2 days/year,7 however this is often underestimated in treatment records.8 The category of antibiotics used in sows varies greatly between herds, but it was reported that 26% of all herds use antibiotics to treat sows.9 Rosengren et al10 reported an incidence of 7.84 sows treated with antibiotics per 1000 sows/day, while Sjölund et al11 reported an incidence of 42 sows treated with antibiotics per 1000 sows/day. In some herds, all sows were routinely injected with an antimicrobial agent after farrowing.10 The majority of antimicrobials used in swine herds are classified as critically important or highly important by the World Health Organization.12 Rosengren et al10 reported that some herds routinely use ceftiofur for treating sows. The use of third-generation cephalosporins has increased since 2001 and an increase in bacterial isolates from healthy swine showing extended-spectrum, beta-lactamases was observed in the same period.13 Ceftiofur is restricted to use in animals but is similar to ceftriaxone, which is widely used in human medicine. Therefore, ceftiofur should not be used as a first-choice antimicrobial for sows.12 The use of antimicrobials in animal production is a public health matter, as it engenders selection pressure for resistance to antimicrobials. Of all swine, sows are the pigs least treated with antimicrobials.9,11 Attention should be paid to antimicrobial administration to sows as they can act as a reservoir for transferal of resistant bacteria to their offspring.4 Due to recent concerns about antimicrobial resistance and the subsequent restrictions on the use of antimicrobials in animal production, researchers are looking for new alternatives to prevent and treat disease. One possible alternative relies on unveiling the mechanisms by which the microbiome interacts with the host and its relationship with health and productivity.14-16
The microbiome is defined as a characteristic microbial community occupying a well-defined habitat which has distinct physio-chemical properties and includes the whole spectrum of molecules produced by the microorganisms, their structural elements, metabolites, and molecules produced by the host and are influenced by the surrounding environmental conditions. The microbiome is prone to change in time and scale and is essential for multicellular organism health.17,18
Studies associating the microbiome with disease have been carried out in various species, including humans.16,19-23 Alterations in vaginal and intestinal microbiomes can reduce urinary tract infections and gut infections in humans.19,24,25 This new knowledge opens possibilities for new studies to provide a better understanding about microbiome relationships with diseases and reproductive performance. In sows, several factors may alter the microbiome composition. It was reported that antimicrobials used,26 reproductive stage,27 genetic line,28 feed additives, probiotic and prebiotic supplementation,29 pathogen exposure, vaccines to prevent disease,23 and stressful conditions30 can affect the microbiome. Some of these factors are being studied to increase sow productivity by microbiome modulation14,15,28 alongside studies investigating the possibility of modulating the offspring microbiome through sow microbiome modulation.29,31,32 These factors are presented in Figure 1.
In pigs, microbiome modulation can prevent disease and reduce the use of antimicrobials.33 Pathogen exposures can cause dysbiosis,23 which can result in an unstable microbiome and increase susceptibility to diseases caused by opportunistic organisms.34 Both factors contribute to development of disease in sows and impair productivity. Development of a stable microbiome by administration of Lactobacillus to newborn piglets has been shown to reduce diarrhea and improve weaning weight.35,36 Similarly, probiotic supplementation to weaned piglets had a positive effect on average daily gain and reduced diarrhea37-39 and Salmonella shedding.37 Other studies in swine indicate interaction between the microbiome and other areas of the body. It was observed that Enterococcus faecalis EC-12 increased the response of ex vivo tissue to immuno-stimulants such as porcine reproductive and respiratory syndrome virus (PRRSV) modified live virus vaccine.40 A fecal microbiota transplant (FMT) had beneficial effects in pigs challenged against Mycoplasma hyopneumoniae, reducing gross lung pathology.41
In sows, there is evidence that changes in the local microbiome (eg, intestinal and vaginal microbiome) may have led to effects in different systems and, consequently, several biomarkers for productivity and optimal health were found.14,15,30 It was observed that symbiotic supplementation in sows improved their litter performance.42 It is possible to modulate the sow’s microbiome through microbiome transplantation, altering endometrial glands, circulating hormones, and improving reproductive efficiency.28,43 Research to date has focused mainly on piglet microbiomes, so there is a lack of information regarding the use of probiotics to prevent vaginal discharge, cystitis, mastitis, and diseases that have a great economic impact in sow herds.
For decades, microbiology research has focused on culture methods or detection of individual microbial species or polycultures that may not represent the full bacterial population and diversity since most microorganisms could not be grown by traditional culture methods.44 The seminal work of Woese and Fox45 in the 1970s using ribosomal RNA (rRNA) as a bacterial evolutionary marker, mainly with the 16S rRNA gene, revolutionized microbiology research. This and the development of new generation sequencing (NGS) methods have made it possible to characterize the bacterial community in all its richness, diversity, and relative abundance, even in tissues believed to be sterile.46 Recently, technological advances have allowed a drastic reduction in sequencing costs, mainly due to the emergence of commercial high-throughput sequencing platforms,47 and research involving the assessment of the microbiome in swine has gained importance.
Despite the increase of microbiome analysis research, there is a lack of studies correlating the microbiome with its impact on sow productivity. Furthermore, studies that perform organism-based metabolic analysis, identify microbe-microbe interactions, and identify microbe-host interactions are even more scarce. The microbiome is complex, and studies focused on system-based approaches would probably provide more valuable information.48,49 Thus, this review aims to compile information related to modifications or alterations in the microbiome to improve reproductive performance, as well as to point out topics that require further investigation.
The reproductive tract microbiome
The number of studies analyzing the vaginal microbiome of sows has increased, especially in the last four years.14,15,50-54 Studies have focused on identifying possible biomarkers related to increased productivity,14 infectious diseases in target sites, ie, endometritis,16 and immune responses against systemic diseases, such as PRRS. The vaginal microbiome was also studied to identify possible biomarkers for diseases that have an ill-defined biological factor, such as prolapses.51
Endometritis has a major impact on the reproductive efficiency of sows55-58 and its main cause is bacterial infection.59,60 Common clinical manifestations include purulent vulvar secretion, reproductive failure, abortion, anestrus, reduced farrowing rates, inappetence, and poor body condition which often leads to sow culling.60,61 This condition could also predispose the sow to other diseases such as postpartum dysgalactia syndrome (PDS) and cystitis.62,63 Vaginal discharge is the reported reason for 20.5% of culled sows, and endometritis was the most common postmortem lesion (14.5%) in sows culled due to anestrus and repeated breeding.61
The application of culture methods associated with biomolecular techniques, notably polymerase chain reaction (PCR), has identified several organisms in purulent vaginal discharge, such as Escherichia coli, Staphylococcus, Streptococcus, Trueperella pyogenes,60,63 Arcobacter,64 Chlamydia,65 Proteus, Pseudomonas, and Corynebacterium.63,66 The most common organism found was E coli, which was isolated in more than 30% of endometritis cases.60 Despite the great potential of extraintestinal pathogenic E coli to cause metritis, it can also be part of the vaginal microbiome in samples from healthy sows.16,52-54 The NGS-based studies have corroborated the importance of some of these organisms previously identified by traditional methods, such as E coli, Staphylococcus, and Streptococcus.16,52 However, NGS metagenomic techniques allow the identification of microbes at a whole community level, in addition to allowing the comparison of relative abundances of each microbe type. This allows for greater resolution to identify organisms which are difficult to identify with traditional methods and may be important in dysbiosis such as low-abundance or fastidious microbes (eg, Bacteroides, Clostridium, and Fusobacterium) recently identified in metagenomic approaches as important pathogenic causes of endometritis.16,52,53
Previous studies demonstrated that the vaginal microbiome may act as biological barrier by secreting antimicrobial components such as lactic acid, bacteriocin, and hydrogen peroxide to maintain the health of the reproductive tract.67,68 Therefore, a sow’s vaginal microbiome is complex and even potentially pathogenic bacteria can be part of the community, suggesting that urogenital diseases may arise from dysbiosis.
Wang et al16 analyzed sow vaginal samples classified as either affected or not affected by endometritis. The Firmicutes phylum was the most abundant (40%-60%) in the vaginal microbiome followed by Proteobacteria (20%-32%) and Bacteroidetes (9%-13%). However, the Firmicutes phylum had the greatest relative abundance in healthy sows, while Proteobacteria and Bacteroidetes were more abundant in samples of sows affected by endometritis. At the genus level, Wang et al16 found that Bacillus and Paenibacillus were relatively more abundant in the healthy sows, while Escherichia-Shigella and Bacteroides were relatively more abundant in sows affected by endometritis. Wang et al16 observed that one sow with endometritis had a great abundance of Staphylococcus during the metagenomic analysis, although the microbial species within the Staphylococcus genus was not classified. Experimental inoculation with Staphylococcus hyicus caused endometritis in sows in a previous study, as did E coli.59
Similarly to Wang et al16, Zhang et al52 found that sows with endometritis had a higher relative abundance of Porphyromonas, Clostridium sensu stricto 1, Streptococcus, Fusobacterium, Actinobacillus, and Bacteroides in the birth canal. Escherichia-Shigella and Bacteroides were higher in the intestines of sows suffering from endometritis, suggesting a link between the onset of endometritis and the increase of these organisms in intestinal microbiota. Xu et al53 also found the phyla Proteobacteria, Firmicutes, and Bacteroidetes among the most abundant in sow vaginal samples; at the genus level, the most abundant were Escherichia, Streptococcus, Enterococcus, Bacillus, Clostridium sensu stricto 1, Staphylococcus, Acinetobacter, Lactobacillus, and Proteus. Although Escherichia-Shigella, Clostridium sensu stricto 1, and Streptococcus relative abundance were related to endometritis in the other studies,16,52 no sow had endometritis in the Xu et al53 study. However, the small number of females evaluated in these two studies (n = 8) precludes stronger conclusions.
Furthermore, Xu et al53 showed that the addition of lysozyme, an antimicrobial enzyme that occurs naturally in the mucosal barrier of mammals, to the diet of sows affected the vaginal bacterial community by decreasing the relative abundance of Escherichia-Shigella and increasing Lactobacillus. Members of the Lactobacillaceae family are most abundant in the birth canal of healthy women and are considered protective against infection by other organisms and probiotic candidates.69 The metagenomic studies related to the vaginal microbiome did not observe a higher prevalence of Lactobacillus in healthy sows16,52 and that even healthy sows carried a higher prevalence of potential pathogenic or opportunistic organisms.16,52 These results indicate that the sow vaginal microbiome is more complex than what is observed in humans, which contributes to the difficulty of describing a core vaginal microbiome in sows since even discrete changes can impair sow health. Therefore, these authors suggested lysozyme as a candidate for the maintenance of a beneficial vaginal microbiome and consequently reduce the necessity of antimicrobial use to prevent or treat vaginal discharge in the sow herd. Further studies should elucidate the ability of lysozyme to modulate the sow vaginal microbiome for only beneficial microbes.
Sanglard et al14 evaluated the vaginal microbiome of sows with low and high reproductive performance after PRRSV vaccination. Sows with low reproductive performance had a higher abundance of noxious bacteria such as Phascolarctobacterium, Filifactor, Treponema, and Bacteroides compared to sows with high reproductive performance. Phascolarctobacterium was negatively correlated with litter weight at day 21 of lactation27 and Filifactor has been associated with metritis in dairy cows.70 In addition, discriminant linear analysis using the specific genera Campylobacter, Bacteroides, Porphyromonas, unclassified Lachnospiraceae, Prevotella, and Phascolarctobacterium was able to differentiate animals with high and low farrowing performance, indicating that these could serve as potential biomarkers.14 Understanding the vaginal microbiome and potential biomarkers of high reproductive performance may guide improvements in genetic selection at an early age, even prior to breeding. Sanglard et al14 verified that this method is minimally invasive and can be performed at early ages, such as 4 and 52 days after PRRSV vaccination (132 ± 12 days of age).
Another study50 investigated the relationship between the vaginal microbiome and sow genetics and the impact on immune response and farrowing traits in commercial gilts. It was found that the genotype was able to explain up to 33% of the immune response variation to vaccination and 14% of the total microbial variation of the vaginal microbiome. The results indicated that the microbiome can be modulated by genetic selection for beneficial microbes, which may indirectly improve reproductive performance, and the possibility to genetically select sows for a better immune response.50
The diversity of the vaginal microbiome has been discussed in recent years. Laguardia-Nascimento et al71 found great variability in the vaginal microbiome of cows, which contradicted previous studies that used culture methods. Sanglard et al14 found that the microbiome of sows with low reproductive performance had greater vaginal microbial diversity compared to sows with high reproductive performance.
Another factor that contributes to impaired herd productivity is pelvic organ prolapse. Prolapses are more prevalent during late gestation and early lactation and contributes to approximately 21% of sow mortalities annually.51,72 Sow mortality during the peripartum period is economically critical because it increases nonproductive days and impairs neonatal nutrition. Despite the great impact of prolapses, prevention is in part neglected due to an ill-defined biological factor. Kiefer et al51 observed that alpha diversity revealed no significant differences between samples for species richness, community evenness, and diversity. But when analyzed with linear discriminant analysis, there was abundant differences in 89 total operational taxonomic units between sows with high and low prolapse risk. A higher abundance of Prevotellaceae, Treponema, and Streptococcus dysgalactiae was observed in high prolapse risk sows. However, principal coordinate analyses revealed no distinct clustering of sows with high or low prolapse risk and the putative markers identified in this work will require determination of causality.49 While the Sanglard et al,14,50 Wang et al,16 Kiefer et al,51 Zhang et al,52 and Xu et al53 studies were not designed to describe a core vaginal microbiome community associated with better reproductive outcomes in sows, they do show that some changes in bacterial composition may influence a sow’s disease response and reproductive performance. Further studies focusing on system-based approaches are required to understand the role of the microbiome in reproductive performance.
The urinary tract microbiome
Urinary tract infections (UTIs) have great prevalence in swine herds and cause economic losses due to reproductive failures, increased sow culling, and mortality.73,74 It was reported that more than 90% of sows with some reproductive disorder also were diagnosed with a UTI.75 Additionally, UTIs during gestation are reported to reduce litter size by 0.6 piglets/litter.76 Sows diagnosed with a UTI had 3.5 times higher risk of developing endometritis compared with healthy animals.63 Furthermore, UTIs are associated with other diseases, such as mastitis metritis agalactia.77-79
The UTI etiology is complex, polymicrobial, and may feature rotation or changes in etiological pathogens. Among the possible organisms, E coli was the predominant microbiological organisms isolated in single (71%) and mixed (85%) UTIs in sows.80 For a long period, the urine within the urinary tract was generally considered sterile.81,82 This was due to insensitive identification for most bacterial species using traditional microbiological cultures.83-87 However, a growing list of studies using DNA methods (PCR, NGS, and genome sequencing) detected a wide range of microbiological species in urine samples from diseased and healthy humans and animals.22,84 Furthermore, it was observed that not only was DNA present, but that the bacterial strains were viable.86 Therefore, the urinary bladder has an active and functional microbiome and may affect the onset of a UTI. The microbiome role in UTIs was demonstrated by a study in humans that administered Lactobacillus crispatus in vaginal suppositories after completion of a full course of antibiotic therapy, which reduced the recurrence of UTIs by 50% in UTI-prone women.19 This is of particular importance in pigs because UTIs are prevalent in swine herds, and are usually treated with in-feed, broad-spectrum antimicrobials.88,89 Another alternative for reducing the prevalence of UTIs, and consequently antibiotic use, is the use of urine acidifiers in the diet. The use of acidifiers affects the acid-base balance of the sow diet and is correlated with urinary pH and reduced total bacteria colony- forming units in the urine.90 Similar results were found in a mouse model with the reduction of uropathogenic E coli.91 Kluge et al92 showed that supplementation with 1% benzoic acid in the diet reduced the urinary pH of sows by up to one unit when compared to the nonsupplemented group.
Few studies in animal science have analyzed the urinary tract microbiome. One study using dogs as a model identified a urinary tract microbiome in these animals.22 There seems to be a relationship between vaginal and urinary tract microbiomes in animals and humans.19,22 Similarly, a positive correlation between UTI and endometritis was observed in pigs.63,75 Overlap between vaginal and urinary microbiota exists in dogs and humans, but more research is needed to determine if this overlap also exists in sows.19,22
However, there are no studies to our knowledge that have evaluated the urinary tract microbiome in sows and its relationship with the use of nutritional management strategies (eg, probiotics and acidifiers). Nevertheless, Xu et al53 observed that lysozyme administration in sow feed altered vaginal microbiota. Other literature indicates that nutritional changes led to a reduction in urinary pH and a reduction in some potential pathogens in sow urine.90,92 If gut microbiome can be modulated to prevent dysbiosis, perhaps similar strategies can be used to prevent or even treat UTIs and consequently reduce the use of antibiotics. However, further investigation is necessary to understand the microbiome role in the sow bladder during cystitis and to develop new technologies and strategies to modulate the microbiome, minimizing dysbiosis and diseases.
Colostrum and milk microbiomes
Besides their nutritional value, colostrum and milk are essential to stimulate immune system development of piglets.32,93-95 Postpartum dysgalactia syndrome is commonly associated with infectious pathogens and is classified as having a multifactorial etiology. Postpartum dysgalactia syndrome compromises milk production and is triggered by associations between risk factors such as management, feeding, and hygiene.77-79
It was observed that a lack of sufficient milk production resulted in an increase in piglet preweaning mortality, especially during the first week of age where mortality can be up to 38.6%.79,96 The infection of mammary glands may lead to their lack of function and impairment of pregnancy rate.79 Mastitis has a complex treatment and, consequently, it was observed that a high percentage (23%-33%) of antimicrobials used were classified as highest priority or critically important for human medicine by the World Health Organization.12,97 Moreover, Jenny et al97 showed that for antibiotic treatment of sow mastitis, duration was shorter and dosage was lower than recommended in 54% and 19%, respectively, which can influence antibiotic resistance selection.96 Based on the negative impact of PDS on reproductive performance and antimicrobial resistance, alternative tools are essential to reduce the occurrence of this syndrome.
The origin of colostrum and milk microbiomes is complex and not fully elucidated.98 The high percentage of anaerobic intestinal microorganisms in milk samples indicates that part of the milk bacterial community originates from the maternal gastrointestinal tract through the bacterial entero-mammary pathway99 or ascending colonization of the udder via the teat canal (galactogenic route).77,78,100 Other studies indicate that the skin may also be a source for the colostrum and milk microbiome.101,102 Bacteriological analysis of colostrum and samples from mammary gland skin from healthy sows showed that all skin samples were bacteriologically positive with Staphylococcaceae as the most frequently isolated (96.9%) followed by Streptococcaceae (63.5%). In addition, 66.7% of all skin samples had species from the Enterobacteriaceae family, with E coli the dominant species. Similarly, 79.2% of colostrum samples were bacteriologically positive with Staphylococcaceae as the most frequently isolated (54.1%) followed by Streptococcaceae (30.3%) and Enterobacteriaceae (3.9%). Again, E coli was the dominant species among the Enterobacteriaceae family.102
Despite not fully understanding the makeup of the mammary gland microbiome, it was observed that sow milk contained Enterobacteriaceae102 and anaerobic gut-associated genera such as Bacteroides, Blautia, Ruminococcus, and Bifidobacterium indicating that the gut has an essential role in the mammary microbiome composition.95 Gerjets et al103 studied the virulence genes most frequently detected in milk samples from healthy sows and sows with coliform mastitis. Although sows with coliform mastitis had significantly more specific virulence genes in their samples, healthy sows showed frequencies close to and even higher of some virulence coding genes.103 Furthermore, no pattern was found in the virulence profile comparing sick and healthy animals.103 These findings raise the question whether the presence of virulence genes alone is sufficient for bacteria to cause disease. There is no doubt that virulence genes are determinant for bacteria to attach, invade, and colonize the host resulting in illness.104 However, it also indicates that there is a complex interaction among pathogenic and opportunistic organisms, the environment, and animal genetics. The disruption of one of these factors by stressful handling, mixing of animals from different origins, or the entry of a new infectious pathogen in the naive herd can affect the microbiome allowing the multiplication of pathogenic bacteria causing dysbiosis and disease.
Chen et al95 analyzed the bacterial 16S rRNA gene sequences from sow colostrum and milk, and the predominant phyla were Firmicutes and Proteobacteria with a counter-balanced relationship between them. The relative abundance of these two phyla significantly fluctuated throughout lactation, while total proportions between them remained at a certain level (75.9%-80.9%).95 The predominant genera observed during a microbiome assay was different between sow colostrum and milk. The most predominant genus in the colostrum was Streptococcus, while transitional and mature milk samples were dominated by unclassified Ruminococcaceae, Bifidobacterium, Staphylococcus, and Acinetobacter, which are lactose-utilizing genera.95 The six most predominant genera in sows’ milk were Ruminococcaceae, Streptococcus, unclassified Clostridiales, Lactobacillus, Corynebacterium, and unclassified Lachnospiraceae.95 Analysis from bacteriological isolation102 and 16S rRNA sequences95 indicates that Staphylococcus and Streptococcus are generally the predominant genera in sow colostrum and milk. Moreover, it was reported that microbiome changes in the mammary gland can be the cause for some nutritional alterations from colostrum to transitional and mature milk.95
It was observed that microbiome in the gut is related to diseases in other organs41,53 and a probiotic/prebiotic or symbiotic supplementation may reduce the shedding of potential opportunistic organisms.37,53 The bacterial entero-mammary pathway is being established99 and this interconnection indicates that gut microbiome modulation may affect colostrum and milk microbiome composition. In this context, lysozyme feed supplementation altered fecal microbiome and decreased some proinflammatory and increased anti-inflammatory cytokines. These inflammatory cytokines may play a role in PDS development.105 Based on this, the mammary gland microbiome and its interaction with the gastrointestinal microbiome would constitute an alternative strategy to prevent mammary disorders through gut microbiome modulation and consequently reduce the use of antimicrobials to treat mastitis. Another possibility to reduce the occurrence of mastitis is the development of probiotics for topical application to the sow udder to exclude opportunistic organisms from colonizing the mammary gland. Similar strategies using probiotics in the form of biofilm, spray, or intramammary inoculation to prevent mastitis have been developed and have shown promising results in vitro106 and in dairy cows.107,108 Furthermore, formulations to be applied in sows should also be beneficial to piglet gut health.
Finally, the sow colostrum and milk microbiome can also influence piglet gut development and innate immune response. The maternal milk microbiome is primarily responsible for the colonization of the piglet gut contributing approximately 90% of the bacteria throughout the first 35 days of life.32 Lactobacillus reuteri, Lactobacillus mucosae, and Akkermansia muciniphila are present in sow milk and can act as potential probiotic bacteria.109,110 An increase of these organisms in the milk was observed during the lactation period.95 Conversely, potentially pathogenic bacteria such as Staphylococcus epidermidis, Helcococcus, Corynebacterium, Actinobacillus, and Haemophilus are also present in sow milk, but these organisms generally decreased during lactation in healthy sows.95,111,112 The Helcococcus genus was negatively correlated with the abundance of the most bacteria genera in sow milk95 and its increase in the milk may affect sow and piglet health.
Further studies exploring the sow milk microbiome are necessary to determine a microbial core. More research is also needed to evaluate the influence of environmental characteristics and the gut microbiome on the colostrum and milk microbiome and the subsequent impacts on the offspring.
Fecal microbiome and reproduction
The increased number of piglets born with lower birth weights and the greater within-litter weight variation leads to concerns about the ability of the sow to satisfactorily raise the piglets until weaning. In recent years, numerous studies were developed to understand the impact of the sow gut microbiome and the effects of microbiome modulation on offspring performance. Moreover, the gut microbiome has being studied to find possible biomarkers for productivity, and studies related to FMT were conducted to observe the impact of microbiome of different genetic lines on productivity.
The colonization of the piglet gut is initiated during the farrowing process and immediately after birth. This early colonization plays a crucial role in intestinal maturation. The developmental process of the intestinal microbiome is similar for humans and most animals.113 The earliest colonizers in the gut are facultative anaerobes, which are responsible for the creation of a favorable environment for anaerobe establishment.114,115 Chen et al115 demonstrated that the core microbiome of piglet feces in the first days post partum is determined by surrounding environmental factors such as floor microorganisms and the microbiomes of the sow’s vagina, teats, mammary secretions (colostrum and milk), and feces. Also, several studies demonstrated that the process of immune maturation is influenced by the microbiome that colonizes the gut during the early stage of life.116,117 The piglet gut microbiome is influenced by milk oligosaccharides (MOS). The MOS decrease intestinal pH and increase cecal and colonic butyrate in the piglet gut and have prebiotic activity, anti-adhesion effects, and anti-inflammatory properties. These characteristics stimulate the growth of beneficial microbes and inhibit possible pathogens.118,119 It was observed that sows fed with chitooligosaccharide supplement had altered MOS with increasing trisaccharide and tetrasaccharide, but the impact on the piglet gut microbiome was not evaluated.119 Although a plethora of preweaning and postweaning factors (eg, tail docking, teeth clipping, antibiotic treatment, weaning- associated stressors, and diet composition) may affect the gut microbiome of piglets, a maternal influence on the piglet microbiome was observed for up to 63 days of age.120
Dysbiosis in the intestinal microbiome may increase gut permeability and plasma endotoxin concentrations leading to sow metabolic disorders and exacerbated inflammatory status during early lactation.121 Wang et al27 found that differences in the intestinal microbiome of sows resulted from oxidative stress during the peripartum period. The authors observed that the relative abundance of Bacteroides was correlated to a reduced dam oxidative stress status and higher litter weight on day 21 of lactation. In contrast, Phascolarctobacterium and Streptococcus were associated with increased oxidative stress and lower litter weight at 21 days post partum.27
In highly productive sows, the gut microbiome at 3 days before farrowing was mainly enriched in genera belonging to the Prevotellaceae and Ruminococcaceae families and a relative abundance of gram-negative bacteria in comparison to sows classified with low productivity.4 Sows classified as high performing during gestation15,122 and lactation27 had lower microbiome diversity. Uryu et al15 also identified that sows with high reproductive performance had an increase in the relative abundances of 43 bacterial genera, markedly the short-chain fatty acid (SCFA)-producing bacteria.
One important factor to evaluate during gut microbiome manipulation is SCFA production. The SCFAs play a role in sow metabolism, immune regulation, and gut homeostasis31,122-124 and act as precursor of colostrum and milk fat.125 Moreover, the SCFA-producing bacteria were negatively correlated with porcine epidemic diarrhea virus infection23 and heat stress.30 Brutsaert126 indicates that feeding the sow with a nutritional additive (phenolic compound, slow release C12, target release butyrate, medium-chain fatty acids, and organic acids) has the potential to stabilize the sow gut microbiome during parturition, increase feed intake, and increase the proportion of females that produce heavier piglets at weaning.
The fermentation of dietary fiber, notably soluble fiber, by the hindgut microbiome leads to high production of SCFA124 and improves piglet development,127 reduces pathogenic bacteria in the gut,123,124 reduces digesta transit time, and may prevent colonization by opportunistic organisms and lipopolysaccharide absorption.128 According to Jiang et al,43 sows that received a diet with 7.5% crude fiber throughout the reproductive cycle, as compared to sows that received 2.5%, had an increased litter size (3.57 piglets/litter), increased proportion of genera considered beneficial to the intestinal microbiome (Ruminococcus, Butyrivibrio, Lactobacillus, and Fibrobacter), and decreased potentially pathogenic genera such as Clostridium, Streptococcus, Bacteroides, and Escherichia-Shigella. When the level of dietary fiber was the same, a higher soluble fiber vs insoluble fiber inclusion improved enzymes with antioxidant capacity and decreased proinflammatory factors in the sows and their offspring.129 The authors also reported that soluble fiber in sow diets increased the proportion of Romboutsia, Sediminibacterium, Bifidobacterium, unidentified Lachnospiraceae, unidentified Ruminococcaceae, Subdoligranulum, Bacillus, Blautia, Bacteroides, and Parabacteroides and reduced the proportion of Acinetobacter, Vagococcus, and Streptococcus in sow feces and piglet colons.129 The microbial organisms reduced in the piglet colon were already characterized as opportunistic organisms.130-132 Similarly, Cheng et al133 observed that increasing soluble fiber to 2% in the sow gestation diet resulted in piglets with greater growth rate and lower diarrhea rate during the lactation period. Furthermore, the inclusion of dietary fiber in sow diets may contribute to maintenance of proper satiety throughout gestation,134 reduced constipation,128 decreased farrowing duration,127 and reduced stillbirth rate.125
Supplementing the diet with functional foods capable of altering the intestinal microbiome has also been an area of research in recent years. Hasan et al29 showed that the supplementation of yeast hydrolysate in sow diets changed the composition of the fecal microbiome of pregnant sows at the phylum level, reduced farrowing duration, and increased colostrum production, which resulted in a 13% increase in colostrum consumption by piglets. In addition, a lower relative abundance of the phylum Proteobacteria was observed in the supplemented group, which can be considered beneficial since the increased prevalence of this phylum is a marker of dysbiosis associated with intestinal diseases and inflammation.
It is well established that nutrition during the rearing period may affect the performance of future gilts135 but there is a lack of information regarding the gut microbiome role in this aspect. Emerging evidence in rats suggests that the gut microbiome may affect reproductive function since estrogens interact with the commensal microbiome through the estrogen-gut microbiome axis.136,137 Wang et al138 observed that the gut of gilts showing failure to enter estrus before 210 days of age was enriched with Ruminococcacea, Lachnospiraceae, Ruminococcus, Coprococcus, and Oscillospira. In contrast, gilts showing a normal heat cycle had higher abundance of Prevotella, Treponema, Faecalibacterium, Oribacterium, Succinivibrio, and Anaerovibrio. In the same study, the authors found that the abundance of both Sphaerochaeta and Treponema was associated with specific periods of the estrus cycle in which estrogen is high (estrus and proestrous).
Some studies showed that most of the afore mentioned genera may be increased in the gut microbiome of sows and gilts by including fiber in the diet.123,133 The high inclusion of fiber, predominantly soluble (50% beet pulp), between the 1st and 19th day of the 3rd post-puberty estrous cycle resulted in improved oocyte quality and embryo development in vitro and in vivo.139,140 Also, the inclusion of 350 g/kg of lupine (rich in insoluble fiber and a moderate amount of soluble fiber) in the diet of prepubertal gilts improved oocyte quality and embryonic survival at 28 days of age. Moreover, a recent study showed that highly prolific Meishan sows have increased fecal microbiome diversity and levels of fecal steroid hormones (estradiol and progesterone) than less prolific sows, which may contribute to the improvement of sow reproductive performance.29 Xu et al141 observed that the gut of sows with a short wean-to-estrus interval had lower Prevotella and Bacteroides at the genus level, whereas Firmicutes and Lentisphaerae are greater at the phylum level.
The uterus of Meishan gilts secrete more endometrial proteins than the uterus of white crossbred gilts and that the secretion of endometrial proteins is positively correlated with endometrial gland development before 60 days of age. Xu et al28 designed a study to evaluate the role of the gut microbiome on endometrial gland development through an FMT from Meishan to Landrace × Yorkshire gilts from 90 days of age until puberty. Fecal microbiome transplantation explained 60.49% of the variation in gut microbiome and increased concentrations of SCFAs, endometrial gland area, insulin-like growth factor 1 (IGF-1) concentration in plasma and uterine tissue, and mRNA expression level of estrogen receptor 1 gene in ovary tissue. The authors also observed that Lentisphaerae, Bifidobacterium, and Fibrobacter were positively correlated with endometrial gland area; Bacteroidetes was negatively correlated with estradiol and IGF-1 concentration; Firmicutes and Fibrobacter were positively correlated with estradiol concentration; and Bacteroidetes was positively correlated with progesterone concentration while Fibrobacteres, Firmicutes, Bifidobacterium, and Fibrobacter were negatively correlated.
Conclusion and future approaches
The microbiome composition is very sensitive and influenced by diverse environmental, management, and nutritional events. Recent studies indicate that in some cases correlations are insufficient to understand the microbiome complexity. The productivity of offspring may also be affected by sow microbiome modulation. Sow microbiome modulation with probiotics, prebiotics, symbiotics, or other feed additives or nutritional management may constitute a new tool to increase productivity and reduce disease in swine herds and consequently reduce antimicrobial use. Some biomarkers for productivity and disease have been identified, but further investigation using different herds are necessary to determine causality and repeatability of these findings. Future studies should focus on system biology approaches to understand the microbial-microbial and microbial-sow interactions as well as the effect of microbial metabolic production on reproductive outcomes and disease. Randomized blinded clinical trials are necessary to determine if it is possible to increase or decrease target microbial genera previously identified as biomarkers in metagenomics studies and their impact on reproductive outcomes and disease. The decrease in cost per base sequenced over the past few years is encouraging further research in this area. With an increase in metagenomics studies, future research may be aimed at the development of more specific and useful commercial products and to guide future genetic selections.
Acknowledgments
This study was financed in part by the Coordination of Improvement of Higher Education Personnel - Brazil (CAPES) - Finance Code 001. Dr Monteiro is the recipient of FAPESP fellowship (2019/17683-0). Dr Poor is the recipient of FAPESP fellowship (2017/09515-4 and 2019/01192-7). Dr Muro is the recipient of FAPESP fellowship (2020/02731–6). Dr Carnevale is recipient of FAPESP fellowship (2019/23320–7). Dr Moreno is a CNPq fellow (310736/2018-8). Dr Garbossa is a FAPESP fellow (2020/11016-9).
Conflict of interest
None reported.
Disclaimer
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References
1. Koketsu Y, Tani S, Iida R. Factors for improving reproductive performance of sows and herd productivity in commercial breeding herds. Porcine Health Manag. 2017;3(1):1. https://doi.org/10.1186/s40813-016-0049-7
2. Pierozan CR, Callegari MA, Dias CP, de Souza KL, Gasa J, da Silva CA. Herd-level factors associated with piglet weight at weaning, kilograms of piglets weaned per sow per year and sow feed conversion. Animal. 2020;14(6):1283-1292. https://doi.org/10.1017/S175173111900346X
3. Niemi JK, Bergman P, Ovaska S, Sevón-Aimonen M-L, Heinonen M. Modeling the costs of postpartum dysgalactia syndrome and locomotory disorders on sow productivity and replacement. Front Vet Sci. 2017;4:181. https://doi.org/10.3389/fvets.2017.00181
4. Callens B, Faes C, Maes D, Catry B, Boyen F, Francoys D, de Jong E, Haesebrouck F, Dewulf J. Presence of antimicrobial resistance and antimicrobial use in sows are risk factors for antimicrobial resistance in their offspring. Microb Drug Resist. 2015;21(1):50-58. https://doi.org/10.1089/mdr.2014.0037
5. Alexopoulos C, Fthenakis GC, Burriel A, Bourtzi-Hatzopoulou E, Kritas SK, Sbiraki A, Kyriakis SC. The effects of the periodical use of in-feed chlortetracycline on the reproductive performance of gilts and sows of a commercial pig farm with a history of clinical and subclinical viral and bacterial infections. Reprod Domest Anim. 2003;38(3):187-192. https://doi.org/10.1046/j.1439-0531.2003.00415.x
6. Cromwell GL. Why and how antibiotics are used in swine production. Anim Biotechnol. 2002;13(1):7-27. https://doi.org/10.1081/ABIO-120005767
7. Hemme M, Ruddat I, Hartmann M, Werner N, van Rennings L, Käsbohrer A, Kreienbrock L. Antibiotic use on German pig farms - A longitudinal analysis for 2011, 2013 and 2014. PLoS One. 2018;13(7):e0199592. https://doi.org/10.1371/journal.pone.0199592
8. Dunlop R, McEwen S, Meek A, Black W, Clarke R, Friendship R. Individual and group antimicrobial usage rates on 34 farrow-to-finish swine farms in Ontario, Canada. Prev Vet Med. 1998;34(4):247-264. https://doi.org/10.1016/S0167-5877(97)00093-7
9. Jensen VF, Emborg H-D, Aarestrup FM. Indications and patterns of therapeutic use of antimicrobial agents in the Danish pig production from 2002 to 2008. J Vet Pharmacol Ther. 2012;35(1):33-46. https://doi.org/10.1111/j.1365-2885.2011.01291.x
10. Rosengren LB, Waldner CL, Reid- Smith RJ, Harding JCS, Gow SP, Wilkins WL. Antimicrobial use through feed, water, and injection in 20 swine farms in Alberta and Saskatchewan. Can J Vet Res. 2008;72(2):143-150.
11. Sjölund M, Postma M, Collineau L, Lösken S, Backhans A, Belloc C, Emanuelson U, Beilage EG, Stärk K, Dewulf J, MINAPIG consortium. Quantitative and qualitative antimicrobial usage patterns in farrow-to-finish pig herds in Belgium, France, Germany and Sweden. Prev Vet Med. 2016;130:41-50. https://doi.org/10.1016/j.prevetmed.2016.06.003
*12. World Health Organization. Critically important antimicrobials for human medicine. World Health Organization; 2019. Accessed March 22, 2022. http://apps.who.int/iris/bitstream/handle/10665/312266/9789241515528-eng.pdf?sequence=1&isAllowed=y
*13. Danish Integrated Antimicrobial Resistance Monitoring and Research Programme. DANMAP 2010 - Use of antimicrobial agents and occurrence of anti-microbial resistance in bacteria from food animals, foods and humans in Denmark. Published August 2011. Accessed August 16, 2021. https://www.danmap.org/-/media/sites/danmap/downloads/reports/1996-2010/danmap_2010.pdf?la=da&hash=3E3551E8120146791F9761CAB399FAEAC1CA16AC
14. Sanglard LP, Schmitz-Esser S, Gray KA, Linhares DCL, Yeoman CJ, Dekkers JCM, Niederwerder MC, Serão NVL. Vaginal microbiota diverges in sows with low and high reproductive performance after porcine reproductive and respiratory syndrome vaccination. Sci Rep. 2020;20:3046. https://doi.org/10.1038/s41598-020-59955-8
15. Uryu H, Tsukahara T, Ishikawa H, Oi M, Otake S, Yamane I, Inoue R. Comparison of productivity and fecal microbiotas of sows in commercial farms. Microorganisms. 2020;8(10):1469. https://doi.org/10.3390/microorganisms8101469
16. Wang J, Li C, Nesengani LT, Gong Y, Zhang S, Lu W. Characterization of vaginal microbiota of endometritis and healthy sows using high-throughput pyrosequencing of 16S rRNA gene. Microb Pathog. 2017;111:325-330. https://doi.org/10.1016/j.micpath.2017.08.030
17. Berg G, Rybakova D, Fischer D, Cernava T, Champomier Vergès M-C, Charles T, Chen X, Cocolin L, Eversole K, Herrero Corral G, Kazou M, Kinkel L, Lange L, Lima N, Loy A, Macklin JA, Maguin E, Mauchline T, McClure R, Mitter B, Ryan M, Sarand I, Smidt H, Schelkle B, Roume H, Kiran GS, Selvin J, Correa de Souza RS, van Overbeek L, Singh BK, Wagner M, Walsh A, Sessitsch A, Schloter M. Microbiome definition re-visited: Old concepts and new challenges. Microbiome. 2020;8(1):103. https://doi.org/10.1186/s40168-020-00875-0
18. Whipps J, Lewis K, Cooke R. Mycoparasitism and plant disease control. In: Burge M, ed. Fungi in Biological Control Systems. Manchester University Press; 1988:162-167.
19. Stapleton AE, Au-Yeung M, Hooton TM, Fredricks DN, Roberts PL, Czaja CA, Yarova-Yarovaya Y, Fiedler T, Cox M, Stamm WE. Randomized, placebo-controlled phase 2 trial of a Lactobacillus crispatus probiotic given intravaginally for prevention of recurrent urinary tract infection. Clin Infect Dis. 2011;52(10):1212-1217. https://doi.org/10.1093/cid/cir183
20. Cho I, Blaser MJ. The human microbiome: At the interface of health and disease. Nat Rev Genet. 2012;13:260-270. https://doi.org/10.1038/nrg3182
21. Thomas-White KJ, Kliethermes S, Rickey L, Lukacz ES, Richter HE, Moalli P, Zimmern P, Norton P, Kusek JW, Wolfe AJ, Brubaker L. Evaluation of the urinary microbiota of women with uncomplicated stress urinary incontinence. Am J Obstet Gynecol. 2017;216(1):55.e1-55.e16. https://doi.org/10.1016/j.ajog.2016.07.049
22. Burton EN, Cohn LA, Reinero CN, Rindt H, Moore SG, Ericsson AC. Characterization of the urinary microbiome in healthy dogs. PLoS One. 2017;12(5):e0177783. https://doi.org/10.1371/journal.pone.0177783
23. Song D, Peng Q, Chen Y, Zhou X, Zhang F, Li A, Huang D, Wu Q, Ye Y, He H, Wang L, Tang Y. Altered gut microbiota profiles in sows and neonatal piglets associated with porcine epidemic diarrhea virus infection. Sci Rep. 2017;7(1):17439. https://doi.org/10.1038/s41598-017-17830-z
24. Bakken JS. Fecal bacteriotherapy for recurrent Clostridium difficile infection. Anaerobe. 2009;15(6):285-289. https://doi.org/10.1016/j.anaerobe.2009.09.007
25. Rubin TA, Gessert CE, Aas J, Bakken JS. Fecal microbiome transplantation for recurrent Clostridium difficile infection: Report on a case series. Anaerobe. 2013;19:22-26. https://doi.org/10.1016/j.anaerobe.2012.11.004
26. McCormack UM, Curião T, Wilkinson T, Metzler-Zebeli BU, Reyer H, Ryan T, Calderon-Diaz JA, Crispie F, Cotter PD, Creevey CJ, Gardiner GE, Lawlor PG. Fecal microbiota transplantation in gestating sows and neonatal offspring alters lifetime intestinal microbiota and growth in offspring. mSystems. 2018;3(3):e00134-17. https://doi.org/10.1128/mSystems.00134-17
27. Wang H, Ji Y, Yin C, Deng M, Tang T, Deng B, Ren W, Deng J, Yin Y, Tan C. Differential analysis of gut microbiota correlated with oxidative stress in sows with high or low litter performance during lactation. Front Microbiol. 2018;9:1665. https://doi.org/10.3389/fmicb.2018.01665
28. Xu B, Qin W, Yan Y, Tang Y, Zhou S, Huang J, Xie C, Ma L, Yan X. Gut microbiota contributes to the development of endometrial glands in gilts during the ovary-dependent period. J Anim Sci Biotechnol. 2021;12(1):57. https://doi.org/10.1186/s40104-021-00578-y
29. Hasan S, Junnikkala S, Peltoniemi O, Paulin L, Lyyski A, Vuorenmaa J, Oliviero C. Dietary supplementation with yeast hydrolysate in pregnancy influences colostrum yield and gut microbiota of sows and piglets after birth. PLoS One. 2018;13(5):e0197586. https://doi.org/10.1371/journal.pone.0197586
30. He J, Guo H, Zheng W, Xue Y, Zhao R, Yao W. Heat stress affects fecal microbial and metabolic alterations of primiparous sows during late gestation. J Anim Sci Biotechnol. 2019;10(1):84. https://doi.org/10.1186/s40104-019-0391-0
31. Li Y, Liu H, Zhang L, Yang Y, Lin Y, Zhuo Y, Fang Z, Che L, Feng B, Xu S, Li J, Wu D. Maternal dietary fiber composition during gestation induces changes in offspring antioxidative capacity, inflammatory response, and gut microbiota in a sow model. Int J Mol Sci. 2019;21(1):31. https://doi.org/10.3390/ijms21010031
32. Liu H, Zeng X, Zhang G, Hou C, Li N, Yu H, Shang L, Zhang X, Trevisi P, Yang F, Liu Z, Qiao S. Maternal milk and fecal microbes guide the spatiotemporal development of mucosa-associated microbiota and barrier function in the porcine neonatal gut. BMC Biol. 2019;17(1):106. https://doi.org/10.1186/s12915-019-0729-2
33. Roselli M, Pieper R, Rogel-Gaillard C, de Vries H, Bailey M, Smidt H, Lauridsen C. Immunomodulating effects of probiotics for microbiota modulation, gut health and disease resistance in pigs. Anim Feed Sci Technol. 2017;233:104-119. https://doi.org/10.1016/j.anifeedsci.2017.07.011
34. Jo HE, Kwon M-S, Whon TW, Kim DW, Yun M, Lee J, Shin M-Y, Kim S-H, Choi H-J. Alteration of gut microbiota after antibiotic exposure in finishing swine. Front Microbiol. 2021;12:596002. https://doi.org/10.3389/fmicb.2021.596002
35. Abe F, Ishibashi N, Shimamura S. Effect of administration of bifidobacteria and lactic acid bacteria to newborn calves and piglets. J Dairy Sci. 1995;78(12):2838-2846. https://doi.org/10.3168/jds.S0022-0302(95)76914-4
36. Liu H, Zhang J, Zhang S, Yang F, Thacker PA, Zhang G, Qiao S, Ma X. Oral administration of Lactobacillus fermentum I5007 favors intestinal development and alters the intestinal microbiota in formula-fed piglets. J Agric Food Chem. 2014;62(4):860-866. https://doi.org/10.1021/jf403288r
37. Gebru E, Lee JS, Son JC, Yang SY, Shin SA, Kim B, Kim MK, Park SC. Effect of probiotic-, bacteriophage-, or organic acid-supplemented feeds or fermented soybean meal on the growth performance, acute-phase response, and bacterial shedding of grower pigs challenged with Salmonella enterica serotype Typhimurium. J Anim Sci. 2010;88(12):3880-3886. https://doi.org/10.2527/jas.2010-2939
38. Suo C, Yin Y, Wang X, Lou X, Song D, Wang X, Gu Q. Effects of Lactobacillus plantarum ZJ316 on pig growth and pork quality. BMC Vet Res. 2012;8(1):89. https://doi.org/10.1186/1746-6148-8-89
39. Suda Y, Villena J, Takahashi Y, Hosoya S, Tomosada Y, Tsukida K, Shimazu T, Aso H, Tohno M, Ishida M, Makino S, Ikegami S, Kitazawa H. Immunobiotic Lactobacillus jensenii as immune-health promoting factor to improve growth performance and productivity in post-weaning pigs. BMC Immunol. 2014;15(1):24. https://doi.org/10.1186/1471-2172-15-24
40. Tsuruta T, Inoue R, Tsushima T, Watanabe T, Tsukahara T, Ushida K. Oral administration of EC-12 increases the baseline gene expression of antiviral cytokine genes, IFN-γ and TNF-α, in splenocytes and mesenteric lymph node cells of weaning piglets. Biosci Microbiota Food Health. 2013;32(4):123-128. https://doi.org/10.12938/bmfh.32.123
41. Schachtschneider KM, Yeoman CJ, Isaacson RE, White BA, Schook LB, Pieters M. Modulation of systemic immune responses through commensal gastrointestinal microbiota. PLoS One. 2013;8(1):e53969. https://doi.org/10.1371/journal.pone.0053969
42. Ma C, Zhang W, Gao Q, Zhu Q, Song M, Ding H, Yin Y, Kong X. Dietary synbiotic alters plasma biochemical parameters and fecal microbiota and metabolites in sows. J Funct Foods. 2020;75:104221. https://doi.org/10.1016/j.jff.2020.104221
43. Jiang X, Lu N, Xue Y, Liu S, Lei H, Tu W, Lu Y, Xia D. Crude fiber modulates the fecal microbiome and steroid hormones in pregnant Meishan sows. Gen Comp Endocrinol. 2019;277:141-147. https://doi.org/10.1016/j.ygcen.2019.04.006
44. Hugenholtz P, Tyson GW. Metagenomics. Nature. 2008;455:481-483. https://doi.org/10.1038/455481a
45. Woese CR, Fox GE. Phylogenetic structure of the prokaryotic domain: The primary kingdoms. Proc Natl Acad Sci USA. 1977;74(11):5088-5090. https://doi.org/10.1073/pnas.74.11.5088
46. Moreno I, Franasiak JM. Endometrial microbiota-new player in town. Fertil Steril. 2017;108(1):32-39. https://doi.org/10.1016/j.fertnstert.2017.05.034
47. Knight DR, Squire MM, Collins DA, Riley TV. Genome analysis of Clostridium difficile PCR ribotype 014 lineage in Australian pigs and humans reveals a diverse genetic repertoire and signatures of long-range interspecies transmission. Front Microbiol. 2017;7:2138. https://doi.org/10.3389/fmicb.2016.02138
48. Aluthge ND, Van Sambeek DM, Carney-Hinkle EE, Li YS, Fernando SC, Burkey TE. The pig microbiota and the potential for harnessing the power of the microbiome to improve growth and health. J Anim Sci. 2019;97(9):3741-3757. https://doi.org/10.1093/jas/skz208
49. Waldor MK, Tyson G, Borenstein E, Ochman H, Moeller A, Finlay BB, Kong HH, Gordon JI, Nelson KE, Dabbagh K, Smith H. Where next for microbiome research? PLoS Biol. 2015;13(1):e1002050. https://doi.org/10.1371/journal.pbio.1002050
50. Sanglard LP, Schmitz-Esser S, Gray KA, Linhares DCL, Yeoman CJ, Dekkers JCM, Niederwerder MC, Serão NVL. Investigating the relationship between vaginal microbiota and host genetics and their impact on immune response and farrowing traits in commercial gilts. J Anim Breed Genet. 2020;137(1):84-102. https://doi.org/10.1111/jbg.12456
51. Kiefer ZE, Koester LR, Showman L, Studer JM, Chipman AL, Keating AF, Schmitz-Esser S, Ross JW. Vaginal microbiome and serum metabolite differences in late gestation commercial sows at risk for pelvic organ prolapse. Sci Rep. 2021;11(1):6189. https://doi.org/10.1038/s41598-021-85367-3
52. Zhang L, Wang L, Dai Y, Tao T, Wang J , Wu Y, Zeng X, Zhang J. Effect of sow intestinal flora on the formation of endometritis. Front Vet Sci. 2021;8:663956. https://doi.org/10.3389/fvets.2021.663956
53. Xu S, Dong Y, Shi J, Li Z, Che L, Lin Y, Li J, Feng B, Fang Z, Yong Z, Wang J, Wu D. Responses of vaginal microbiota to dietary supplementation with lysozyme and its relationship with rectal microbiota and sow performance from late gestation to early lactation. Animals. 2021;11(3):593. https://doi.org/10.3390/ani11030593
54. Torres Luque A, Fontana C, Pasteris SE, Bassi D, Cocconcelli PS, Otero MC. Vaginal bacterial diversity from healthy gilts and pregnant sows subjected to natural mating or artificial insemination. Res Vet Sci. 2021;140:26-37. https://doi.org/10.1016/j.rvsc.2021.07.023
55. Scofield AM, Clegg FG, Lamming GE. Embryonic mortality and uterine infection in the pig. J Reprod Fertil. 1974;36(2):353-361. https://doi.org/10.1530/jrf.0.0360353
56. de Winter PJJ, Verdonck M, de Kruif A, Devriese LA, Haesebrouck F. Endometritis and vaginal discharge in the sow. Anim Reprod Sci. 1992;28(1):51-58. https://doi.org/10.1016/0378-4320(92)90091-Q
57. Marcus S, Menda A, Shore L, Cohen G, Atweh E, Friedman N, Karpas Z. A novel method for the diagnosis of bacterial contamination in the anterior vagina of sows based on measurement of biogenic amines by ion mobility spectrometry: A field trial. Theriogenology. 2012;78(4):753-758. https://doi.org/10.1016/j.theriogenology.2012.03.022
58. de Jong E, Appeltant R, Cools A, Beek J, Boyen F, Chiers K, Maes D. Slaughterhouse examination of culled sows in commercial pig herds. Livest Sci. 2014;167:362-369. https://doi.org/10.1016/j.livsci.2014.07.001
59. de Winter PJJ, Verdonck M, de Kruif A, Devriese LA, Haesebrouck F. Bacterial endometritis and vaginal discharge in the sow: Prevalence of different bacterial species and experimental reproduction of the syndrome. Anim Reprod Sci. 1995;37(3-4):325-335. https://doi.org/10.1016/0378-4320(94)01342-J
60. Tummaruk P, Kesdangsakonwut S, Prapasarakul N, Kaeoket K. Endometritis in gilts: Reproductive data, bacterial culture, histopathology, and infiltration of immune cells in the endometrium. Comp Clin Path. 2010;19:575-584. https://doi.org/10.1007/s00580-009-0929-1
61. Tummaruk P, Kesdangsakonwut S, Kunavongkrit A. Relationships among specific reasons for culling, reproductive data, and gross morphology of the genital tracts in gilts culled due to reproductive failure in Thailand. Theriogenology. 2009;71(2):369-375. https://doi.org/10.1016/j.theriogenology.2008.08.003
62. Waller CM, Bilkei G, Cameron RDA. Effect of periparturient diseases accompanied by excessive vulval discharge and weaning to mating interval on sow reproductive performance. Aust Vet J. 2002;80(9):545-549. https://doi.org/10.1111/j.1751-0813.2002.tb11033.x
63. Biksi I, Takács N, Vetési F, Fodor L, Szenci O, Fenyö E. Association between endometritis and urocystitis in culled sows. Acta Vet Hung. 2002;50(4):413-423. https://doi.org/10.1556/avet.50.2002.4.4
64. de Oliveira SJ, Baetz AL, Wesley IV, Harmon KM. Classification of Arcobacter species isolated from aborted pig fetuses and sows with reproductive problems in Brazil. Vet Microbiol. 1997;57(4):347-354. https://doi.org/10.1016/S0378-1135(97)00106-5
65. Hoelzle LE, Steinhausen G, Wittenbrink MM. PCR-based detection of chlamydial infection in swine and subsequent PCR-coupled genotyping of chlamydial omp1-gene amplicons by DNA-hybridization, RFLP-analysis, and nucleotide sequence analysis. Epidemiol Infect. 2000;125(2):427-439. https://doi.org/10.1017/S0950268899004446
66. Poor AP, Moreno LZ, Matajira CEC, Parra BM, Gomes VTM, Silva APS, Dutra MC, Christ APG, Barbosa MRF, Sato MIZ, Moreno AM. Characterization of Corynebacterium diphtheriae, C confusum and C amycolatum isolated from sows with genitourinary infection. Vet Microbiol. 2017;207:149-152. https://doi.org/10.1016/j.vetmic.2017.06.008
67. Oakley BB, Fiedler TL, Marrazzo JM, Fredricks DN. Diversity of human vaginal bacterial communities and associations with clinically defined bacterial vaginosis. Appl Environ Microbiol. 2008;74(15):4898-4909. https://doi.org/10.1128/AEM.02884-07
68. Lamont RF, Sobel JD, Akins RA, Hassan SS, Chaiworapongsa T, Kusanovic JP, Romero R. The vaginal microbiome: New information about genital tract flora using molecular based techniques. BJOG: 2011;118(5):533-549. https://doi.org/10.1111/j.1471-0528.2010.02840.x
69. Pino A, Rapisarda AMC, Vitale SG, Cianci S, Caggia C, Randazzo CL, Cianci A. A clinical pilot study on the effect of the probiotic Lacticaseibacillus rhamnosus TOM 22.8 strain in women with vaginal dysbiosis. Sci Rep. 2021;11(1):2592. https://doi.org/10.1038/s41598-021-81931-z
70. Jeon SJ, Vieira-Neto A, Gobikrushanth M, Daetz R, Mingoti RD, Parize ACB, de Freitas SL, Lima da Costa AN, Bicalho RC, Lima S, Jeong KC, Galvão KN. Uterine microbiota progression from calving until establishment of metritis in dairy cows. Appl Environ Microbiol. 2015;81(18):6324-6332. https://doi.org/10.1128/AEM.01753-15
71. Laguardia-Nascimento M, Branco KMGR, Gasparini MR, Giannattasio-Ferraz S, Leite LR, Araujo FMG, de Matos Salim AC, Nicoli JR, de Oliveira GC, Barbosa-Stancioli EF. Vaginal microbiome characterization of Nellore cattle using metagenomic analysis. PLoS One. 2015;10(11):e0143294. https://doi.org/10.1371/journal.pone.0143294
72. Supakorn C, Stock JD, Hostetler C, Stalder KJ. Prolapse incidence in swine breeding herds is a cause for concern. Open J Vet Med. 2017;7:85-97. https://doi.org/10.4236/ojvm.2017.78009
73. D’Allaire S, Drolet R, Chagnon M. The causes of sow mortality: A retrospective study. Can Vet J. 1991;32(4):241-243.
74. Vearick G, Mellagi APG, Bortolozzo FP, Wentz I, Bernardi ML. Causes of mortality in swine female. Article in Portuguese. Arch Vet Sci. 2008;13(2):126-132. https://doi.org/10.5380/avs.v13i2.12893
75. Menin A, Reck C, Capelli JC, Ferraz SM, Vaz EK. Diagnosis of urinary tract infection in productive sows in commercial farms in southern Brazil. Article in Portuguese. Ciência Anim Braz. 2008;9(1):197-206.
76. Amaral AL, Morés N, Barioni Jr W, Wentz I, Bortolozzo FP, Sobestiansky J, Dalla Costa OA. Risk factors associated with the reproductive performance in sows. Article in Portuguese. Arq Bras Med Vet Zootec. 2000;52(5):479-486. https://doi.org/10.1590/S0102-09352000000500013
77. Bertschinger HU, Pohlenz J, Hemlep I. Studies on the mastitis-metritis-agalactia syndrome (milk fever) in sows. II. Bacteriological findings in spontaneous cases. Article in German. Schweiz Arch Tierheilkd. 1977;119(6):223-233.
78. Bertschinger HU, Bürgi E, Eng V, Wegmann P. Lowering of the incidence of puerperal mastitis in the sow by protection of the mammae from contamination. Article in German. Schweiz Arch Tierheilkd. 1990;132(10):557-566.
79. Gerjets I, Kemper N. Coliform mastitis in sows: A review. J Swine Health Prod. 2009;17(2):97-105.
80. Moreno LZ, Matajira CEC, Poor AP, Mesquita RE, Gomes VTM, Silva APS, Amigo CR, Christ APG, Barbosa MRF, Sato MIZ, Moreno AM. Identification through MALDI-TOF mass spectrometry and antimicrobial susceptibility profiling of bacterial pathogens isolated from sow urinary tract infection. Vet Q. 2018;38(1):1-8. https://doi.org/10.1080/01652176.2017.1397302
81. Dukes CE. Urine examination and clinical interpretation. South Med J. 1940; 28-78. https://doi.org/10.1097/00007611-194009000-00042
82. Frimodt-Møller N. The urine microbiome - Contamination or a novel paradigm? EBioMedicine. 2019;44:20-21. https://doi.org/10.1016/j.ebiom.2019.05.016
83. Imirzalioglu C, Hain T, Chakraborty T, Domann E. Hidden pathogens uncovered: Metagenomic analysis of urinary tract infections. Andrologia. 2008;40(2):66-71. https://doi.org/10.1111/j.1439-0272.2007.00830.x
84. Siddiqui H, Nederbragt AJ, Lagesen K, Jeansson SL, Jakobsen KS. Assessing diversity of the female urine microbiota by high throughput sequencing of 16S rDNA amplicons. BMC Microbiol. 2011;11:244. https://doi.org/10.1186/1471-2180-11-244
85. Wolfe AJ, Toh E, Shibata N, Rong R, Kenton K, FitzGerald MP, Mueller ER, Schreckenberger P, Dong Q, Nelson DE, Brubaker L. Evidence of uncultivated bacteria in the adult female bladder. J Clin Microbiol. 2012;50(4):1376-1383. https://doi.org/10.1128/JCM.05852-11
86. Hilt EE, McKinley K, Pearce MM, Rosenfeld AB, Zilliox MJ, Mueller ER, Brubaker L, Gai X, Wolfe AJ, Schreckenberger P. Urine is not sterile: Use of enhanced urine culture techniques to detect resident bacterial flora in the adult female bladder. J Clin Micro-biol. 2014;52(3):871-876. https://doi.org/10.1128/JCM.02876-13
87. Salipante SJ, Sengupta DJ, Rosenthal C, Costa G, Spangler J, Sims EH, Jacobs MA, Miller SI, Hoogestraat DR, Cookson BT, McCoy C, Matsen FA, Shendure J, Lee CC, Harkins TT, Hoffman NG. Rapid 16s rRNA next-generation sequencing of polymicrobial clinical samples for diagnosis of complex bacterial infections. PLoS One. 2013;8(5):e65226. https://doi.org/10.1371/journal.pone.0065226
88. de Moura R, Caldara FR, Foppa L, Machado SP, de Alencar Nääs I, Garcia RG, Gonçalves LMP. Correlation between urinary tract infection and reproductive performance of sows. R Braz Zootec. 2018;47. https://doi.org/10.1590/rbz4720180073
89. Bach MJ, Donin DG, Fernandes SR, Martins GB, Alberton GC. Rational use of antibiotics for treatment of urinary infection in sows. Ciênc Anim Bras. 2021;22. https://doi.org/10.1590/1809-6891v22e-68919
90. DeRouchey JM, Hancock JD, Hines RH, Cummings KR, Lee DJ, Maloney CA, Dean DW, Park JS, Cao H. Effects of dietary electrolyte balance on the chemistry of blood and urine in lactating sows and sow litter performance. J Anim Sci. 2003;81(12):3067-3074. https://doi.org/10.2527/2003.81123067x
91. Jensen HD, Struve C, Christensen SB, Krogfelt KA. Cranberry juice and combinations of its organic acids are effective against experimental urinary tract infection. Front Microbiol. 2017;8:542. https://doi.org/10.3389/fmicb.2017.00542
92. Kluge H, Broz J, Eder K. Effects of dietary benzoic acid on urinary pH and nutrient digestibility in lactating sows. Livest Sci. 2010;134(1-3):119-121. https://doi.org/10.1016/j.livsci.2010.06.116
93. Díaz-Ropero MP, Martín R, Sierra S, Lara-Villoslada F, Rodríguez JM, Xaus J, Olivares M. Two Lactobacillus strains, isolated from breast milk, differently modulate the immune response. J Appl Microbiol. 2007;102(2):337-343. https://doi.org/10.1111/j.1365-2672.2006.03102.x
94. Walker A. Breast milk as the gold standard for protective nutrients. J Pediatr. 2010;156(suppl 2):S3-7. https://doi.org/10.1016/j.jpeds.2009.11.021
95. Chen W, Mi J, Lv N, Gao J, Cheng J, Wu R, Ma J, Lan T, Liao X. Lactation stage-dependency of the sow milk microbiota. Front Microbiol. 2018;9:945. https://doi.org/10.3389/fmicb.2018.00945
96. Kemper N. Update on postpartum dysgalactia syndrome in sows. J Anim Sci. 2020;98(suppl 1):S117-S125. https://doi.org/10.1093/jas/skaa135
97. Jenny B, Vidondo B, Pendl W, Kummerlen D, Sidler X. Evaluation of risk factors for mastitis-metritis-agalactia in pig farms in Switzerland. Article in German. Schweiz Arch Tierheilkd. 2015;157(12):689-696. https://doi.org/10.17236/sat00047
98. McGuire MK, McGuire MA. Got bacteria? The astounding, yet not-so-surprising, microbiome of human milk. Curr Opin Biotechnol. 2017;44:63-68. https://doi.org/10.1016/j.copbio.2016.11.013
99. Rodríguez JM. The origin of human milk bacteria: Is there a bacterial entero-mammary pathway during late pregnancy and lactation? Adv Nutr. 2014;5(6):779-784. https://doi.org/10.3945/an.114.007229
100. Kaipainen T, Pohjanvirta T, Shpigel NY, Shwimmer A, Pyörälä S, Pelkonen S. Virulence factors of Escherichia coli isolated from bovine clinical mastitis. Vet Microbiol. 2002;85(1):37-46. https://doi.org/10.1016/S0378-1135(01)00483-7
101. Urbaniak C, Angelini M, Gloor GB, Reid G. Human milk microbiota profiles in relation to birthing method, gestation and infant gender. Microbiome. 2016;4:1. https://doi.org/10.1186/s40168-015-0145-y
102. Kemper N, Preissler R. Bacterial flora on the mammary gland skin of sows and in their colostrum. J Swine Health Prod. 2011;19(2):112-118.
103. Gerjets I, Traulsen I, Reiners K, Kemper N. Comparison of virulence gene profiles of Escherichia coli isolates from sows with coliform mastitis and healthy sows. Vet Microbiol. 2011;152(3-4):361-367. https://doi.org/10.1016/j.vetmic.2011.05.002
104. Dobrindt U. (Patho-)genomics of Escherichia coli. Int J Med Microbiol. 2005;295(6-7):357-371. https://doi.org/10.1016/j.ijmm.2005.07.009
105. Martineau G-P, Treut YL, Guillou D, Waret-Szkuta A. Postpartum dysgalactia syndrome: A simple change in homeorhesis? J Swine Health Prod. 2013;21(2):85-93.
106. Wallis JK, Krömker V, Paduch J-H. Biofilm formation and adhesion to bovine udder epithelium of potentially probiotic lactic acid bacteria. AIMS Microbiol. 2018;4(2):209-224. https://doi.org/10.3934/microbiol.2018.2.209
107. Alawneh JI, James AS, Phillips N, Fraser B, Jury K, Soust M, Olchowy TWJ. Efficacy of a Lactobacillus-based teat spray on udder health in lactating dairy cows. Front Vet Sci. 2020;7:584436. https://doi.org/10.3389/fvets.2020.584436
108. Frola ID, Pellegrino MS, Espeche MC, Giraudo JA, Nader-Macias ME, Bogni CI. Effects of intramammary inoculation of Lactobacillus perolens CRL1724 in lactating cows’ udders. J Dairy Res. 2012;79(1):84-92. https://doi.org/10.1017/S0022029911000835
109. Urbańska M, Szajewska H. The efficacy of Lactobacillus reuteri DSM 17938 in infants and children: A review of the current evidence. Eur J Pediatr. 2014;173(10):1327-1337. https://doi.org/10.1007/s00431-014-2328-0
110. Chelakkot C, Choi Y, Kim D-K, Park HT, Ghim J, Kwon Y, Jeon J, Kim M-S, Jee YK, Gho YS, Park H-S, Kim Y-K, Ryu SH. Akkermansia muciniphila-derived extracellular vesicles influence gut permeability through the regulation of tight junctions. Exp Mol Med. 2018;50:e450. https://doi.org/10.1038/emm.2017.282
111. MacInnes JI, Desrosiers R. Agents of the “suis-ide diseases” of swine: Actinobacillus suis, Haemophilus parasuis, and Streptococcus suis. Can J Vet Res. 1999;63(2):83-89.
112. Brescó MS, Harris LG, Thompson K, Stanic B, Morgenstern M, O’Mahony L, Richards RG, Moriarty TF. Pathogenic mechanisms and host interactions in Staphylococcus epidermidis device-related infection. Front Microbiol. 2017;8:1401. https://doi.org/10.3389/fmicb.2017.01401
113. Mackie RI, Sghir A, Gaskins HR. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr. 1999;69(5):1035S-1045S. https://doi.org/10.1093/ajcn/69.5.1035s
114. Adlerberth I, Lindberg E, Åberg N, Hesselmar B, Saalman R, Strannegård I-L, Wold AE. Reduced enterobacterial and increased staphylococcal colonization of the infantile bowel: An effect of hygienic lifestyle? Pediatr Res. 2006;59(1):96-101. https://doi.org/10.1203/01.pdr.0000191137.12774.b2
115. Chen X, Xu J, Ren E, Su Y, Zhu W. Co-occurrence of early gut colonization in neonatal piglets with microbiota in the maternal and surrounding delivery environments. Anaerobe. 2018;49:30-40. https://doi.org/10.1016/j.anaerobe.2017.12.002
116. Lewis MC, Inman CF, Patel D, Schmidt B, Mulder I, Miller B, Gill BP, Pluske J, Kelly D, Stokes CR, Bailey M. Direct experimental evidence that early-life farm environment influences regulation of immune responses. Pediatr Allergy Immunol. 2012;23(3):265-269. https://doi.org/10.1111/j.1399-3038.2011.01258.x
117. Schokker D, Zhang J, Zhang L, Vastenhouw SA, Heilig HGHJ, Smidt H, Rebel JMJ, Smits MA. Early-life environmental variation affects intestinal microbiota and immune development in new-born piglets. PLoS One. 2014;9(6):e100040. https://doi.org/10.1371/journal.pone.0100040
118. Salcedo J, Frese SA, Mills DA, Barile D. Characterization of porcine milk oligosaccharides during early lactation and their relation to the fecal microbiome. J Dairy Sci. 2016;99(10):7733-7743. https://doi.org/10.3168/jds.2016-10966
119. Cheng LK, Wang LX, Xu QS, Huang LJ, Zhou DS, Li Z, Li SG, Du YG, Yin H. Chitooligosaccharide supplementation improves the reproductive performance and milk composition of sows. Livest Sci. 2015;174:74-81. https://doi.org/10.1016/j.livsci.2015.02.003
120. Han GG, Lee J-Y, Jin G-D, Park J, Choi YH, Kang S-K, Chae BJ, Kim EB, Choi YJ. Tracing of the fecal microbiota of commercial pigs at five growth stages from birth to shipment. Sci Rep. 2018;8(1):6012. https://doi.org/10.1038/s41598-018-24508-7
121. Cheng C, Wei H, Yu H, Xu C, Jiang S, Peng J. Metabolic Syndrome During Perinatal Period in Sows and the Link With Gut Microbiota and Metabolites. Front Microbiol. 2018;9:1989. https://doi.org/10.3389/fmicb.2018.01989
122. Shao Y, Zhou J, Xiong X, Zou L, Kong X, Tan B, Yin Y. Differences in gut microbial and serum biochemical indices between sows with different productive capacities during perinatal period. Front Microbiol. 2019;10:3047. https://doi.org/10.3389/fmicb.2019.03047
123. Xu C, Cheng C, Zhang X, Peng J. Inclusion of soluble fiber in the gestation diet changes the gut microbiota, affects plasma propionate and odd-chain fatty acids levels, and improves insulin sensitivity in sows. Int J Mol Sci. 2020;21(2):635. https://doi.org/10.3390/ijms21020635
124. Wu J, Xiong Y, Zhong M, Li Y, Wan H, Wu D, Liu Q. Effects of purified fibre-mixture supplementation of gestation diet on gut microbiota, immunity and reproductive performance of sows. J Anim Physiol Anim Nutr. 2020;104(4):1144-1154. https://doi.org/10.1111/jpn.13287
125. Feyera T, Zhou P, Nuntapaitoon M, Sørensen KU, Krogh U, Bruun TS, Purup S, Jorgensen H, Poulsen HD, Theil PK. Mammary metabolism and colostrogenesis in sows during late gestation and the colostral period. J Anim Sci. 2019;97(1):231-245. https://doi.org/10.1093/jas/sky395
*126. Brutsaert B. Healthy sow gut - higher litter weight. Pig Progress. June 24, 2014. Accessed July 15, 2021. https://www.pigprogress.net/pigs/healthy-sow-gut-higher-litter-weight/
127. Oliviero C, Kokkonen T, Heino-nen M, Sankari S, Peltoniemi O. Feeding sows with high fiber diet around farrowing and early lactation: Impact on intestinal activity, energy balance related parameters and litter performance. Res Vet Sci. 2009;86(2):314-319. https://doi.org/10.1016/j.rvsc.2008.07.007
128. Agyekum AK, Nyachoti CM. Nutritional and metabolic consequences of feeding high-fiber diets to swine: A review. Engineering. 2017;3(5):716-725. https://doi.org/10.1016/J.ENG.2017.03.010
129. Li Q, Peng X, Burrough ER, Sahin O, Gould SA, Gabler NK, Loving CL, Dorman KS, Patience JF. Dietary soluble and insoluble fiber with or without enzymes altered the intestinal microbiota in weaned pigs challenged with enterotoxigenic E coli F18. Front Microbiol. 2020;11:1110. https://doi.org/10.3389/fmicb.2020.01110
130. Matajita CEC, Poor AP, Moreno LZ, Monteiro MS, Dalmutt AC, Gomes VTM, Dutra MC, Barbosa MRF, Sato MIZ, Moreno AM. Vagococcus sp. a porcine pathogen: Molecular and phenotypic characterization of strains isolated from diseased pigs in Brazil. J Infect Dev Ctries. 2020;14(11):1314-1319. https://doi.org/10.3855/jidc.12081
131. Vötsch D, Willenborg M, Weldearegay YB, Valentin-Weigand P. Streptococcus suis - the “two faces” of a pathobiont in the porcine respiratory tract. Front Microbiol. 2018;9:480. https://doi.org/10.3389/fmicb.2018.00480
132. Wareth G, Neubauer H, Sprague LD. Acinetobacter baumannii - a neglected pathogen in veterinary and environmental health in Germany. Vet Res Commun. 2019;43(1):1-6. https://doi.org/10.1007/s11259-018-9742-0
133. Cheng C, Wei H, Xu C, Xie X, Jiang S, Peng J. Maternal soluble fiber diet during pregnancy changes the intestinal microbiota, improves growth performance, and reduces intestinal permeability in piglets. Appl Environ Microbiol. 2018;84(17):e01047-18. https://doi.org/10.1128/AEM.01047-18
134. Sapkota A, Marchant-Forde JN, Richert BT, Lay DC. Including dietary fiber and resistant starch to increase satiety and reduce aggression in gestating sows. J Anim Sci. 2016;94(5):2117-2127. https://doi.org/10.2527/jas.2015-0013
135. Tummaruk P, Tantasuparuk W, Techakumphu M, Kunavongkrit A. Age, body weight and backfat thickness at first observed oestrus in crossbred Landrace × Yorkshire gilts, seasonal variations and their influence on subsequence reproductive performance. Anim Reprod Sci. 2007;99(1-2):167-181. https://doi.org/10.1016/j.anireprosci.2006.05.004
136. Baker JM, Al-Nakkash L, Herbst-Kralovetz MM. Estrogen-gut microbiome axis: Physiological and clinical implications. Maturitas. 2017;103:45-53. https://doi.org/10.1016/j.maturitas.2017.06.025
137. Park S, Kim DS, Kang ES, Kim DB, Kang S. Low-dose brain estrogen prevents menopausal syndrome while maintaining the diversity of the gut microbiomes in estrogen-deficient rats. Am J Physiol Endocrinol Metab. 2018;315(1):E99-E109. https://doi.org/10.1152/ajpendo.00005.2018
138. Wang Z, Fu H, Zhou Y, Yan M, Chen D, Yang M, Xiao S, Chen C, Huang L. Identification of the gut microbiota biomarkers associated with heat cycle and failure to enter oestrus in gilts. Microb Biotechnol. 2020;14:1316-1330. https://doi.org/10.1111/1751-7915.13695
139. Ferguson EM, Slevin J, Edwards SA, Hunter MG, Ashworth CJ. Effect of alterations in the quantity and composition of the pre-mating diet on embryo survival and foetal growth in the pig. Anim Reprod Sci. 2006;96(1-2):89-103. https://doi.org/10.1016/j.anireprosci.2005.11.007
140. Ferguson EM, Slevin J, Hunter MG, Edwards SA, Ashworth CJ. Beneficial effects of a high fibre diet on oocyte maturity and embryo survival in gilts. Reproduction. 2007;133(2):433-439. https://doi.org/10.1530/REP-06-0018
141. Xu K, Bai M, Liu H, Duan Y, Zhou X, Wu X, Liao P, Li T, Yin Y. Gut microbiota and blood metabolomics in weaning multiparous sows: Associations with oestrous. J Anim Physiol Anim Nutr. 2020;104(4):1155-1168. https://doi.org/10.1111/jpn.13296
* Non-refereed references.
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