1. Introduction
Gut microbiota can be shaped by dietary probiotics, thereby improving nutrient utilization, and exerting immunomodulatory effects [
1]. Probiotic supplementation is able to modify the fecal microbiota of sows and further affect the gut microbiota in their offspring [
2,
3]. Probiotics in combination with antibiotic supplementation in the diet of sows and piglets improve growth performance and reduce diarrhea incidence of piglets during the nursery phase [
2]. The combined use of
Bacillus licheniformis and
Bacillus subtilis in the diet of sows increases feed intake and decreases weight loss during the suckling period [
4]. Furthermore,
Bacillus species-based probiotic supplementation in the diet of sows reduces the diarrhea score and pre-weaning mortality of piglets, leading to an increased number of weaned piglets per litter and body weight at weaning [
4]. The fat and protein content in the milk of sows 14 h postpartum is higher in
Bacillus species-based probiotics-treated group compared with the control group [
4].
Postpartum dysgalactia syndrome (PDS) is a multifactor disease in sows with recently reported prevalence varying from 6.0 to 48.2% [
5,
6]. Sows with PDS exhibit clinical signs of mastitis, dysgalactia, and a fever above 39.5 °C within 12 to 48 h postpartum. In addition to sows, the increased mortality rate and growth retardation are also observed in her offspring due to dysgalactia [
7]. PDS leads to enormous economic losses in the swine industry worldwide [
8]. Pathogens can invade the mammary gland of sows and cause a local inflammation via the endogenous or the galactogenous route, thereby inducing PDS [
7]. Therefore, alteration of gut microbiota of sows may prevent PDS by inhibiting pathogen growth and protecting the mammary glands against fecal contamination.
B. licheniformis, an endospore-forming probiotic strain exhibits antibacterial activity in vitro through the producing antibacterial cyclic lipopeptide [
9,
10]. The surfactin is a
B. licheniformis-derived antibacterial cyclic lipopeptide [
11].
B. licheniformis-fermented products (BLFP) containing
B. licheniformis and surfactin prevent disease and improve growth performance in broilers [
12,
13]. Recently, it has been demonstrated that BLFP has beneficial effects on the alteration of gut bacterial community and prevention of post-weaning diarrhea in piglets [
14,
15]. However, to the best of our knowledge, little is known about whether BLFP has a beneficial effect on the sows with PDS and whether this effect can further affect her offspring.
In practice, PDS is treated generally with anti-inflammatory drugs, hormones, or antibiotics. An alternative strategy for PDS control is still rarely investigated. There is an urgent need to demonstrate the positive effects of BLFP for the prevention of PDS in sows before practical application. Therefore, this study aimed to evaluate the effect of BLFP, PDS, and interaction on litter performance traits, milk composition, and fecal microbiota in sows. The results provide a theoretical basis for the use of B. licheniformis-fermented products in sows for improving productivity.
4. Discussion
Here, we demonstrated for the first time that BLFP supplementation in the diet of sows improved the piglet body weight at weaning. We confirmed that BLFP supplementation in the diet of sows decreased the milk fat content of prepartum sows and PDS increased the milk solid content of postpartum sows. Principal component analysis, principal coordinates analysis, and a species abundance heat map in the feces of sows revealed distinct bacterial clusters between the groups. The abundance of the family Prevotellaceae was lower in the feces in sows with PDS. The abundance of the genus (Eubacterium) coprostanoligenes group was higher in the feces in the group treated with BLFP.
Previous studies have demonstrated that the use of probiotics in the diet of sows can improve the litter performance and milk yield [
4,
17,
18]. Dietary
B. subtilis supplementation in the diet of sows has been shown to increase the piglet body weight at birth per litter and piglet body weight at weaning [
19,
20]. However, a recent study has shown that dietary supplementation of
B. subtilis in the diet of sows and their neonates did not improve the performance [
21]. The administration of
B. mesentericus in combination with
Clostridium butyricum and
Enterococcus faecalis in the diet of sows and their neonates can reduce post-weaning diarrhea and improve growth performance [
22]. The combined use of
B. subtilis and
B. licheniformis in sows decreases the pre-weaning mortality per litter and increases the number of weaned piglets per litter and piglet body weight at weaning [
4]. In addition to probiotic supplementation, the beneficial effects of fermented feed on the reproductive and lactation performance of sows and the growth performance of piglets has been observed [
23,
24]. Our previous studies have confirmed that BLFP exhibits antibacterial activity and prevents post-weaning diarrhea in weaning piglets [
10,
14,
15]. Here, we further demonstrated that dietary supplementation of BLFP in the diet of sows during gestation and lactation can improve the piglet body weight at weaning. The milk fat content in prepartum (5.9% for health and 7.28% for PDS) or postpartum (6.44% for health and 7.73% for PDS) sows of the control group was higher than prepartum (4.66% for health and 4.07% for PDS) or postpartum (5.18% for health and 6.38% for PDS) sows of the BLFP-treated group. The result indicates that BLFP supplementation negatively affects the milk fat content of sows. Although it did not reach statistical significance, the average milk protein content (18.46%) of prepartum BLFP-fed healthy sows was higher than in other groups. However, the average milk protein content (11.23%) of postpartum BLFP-fed healthy sows was not the highest among the groups. Based on current findings, it is hard to conclude that milk composition plays a role in improving the piglet body weight at weaning in the BLFP-treated group. According to a previous study [
24], the fermented feed can increase milk yield and milk immunoglobulin Acontent of sows, leading to the improved growth performance of piglets. Whether supplementing sow diets with BLFP can increase milk yield and milk immunoglobulin A content needs to be elucidated in the future. Collectedly, the findings indicate that dietary supplementation of BLFP in the diet of sows has beneficial effects on the piglet body weight at weaning. The detailed mechanisms of BLFP in improving litter performance of sows remain to be investigated.
It has been reported that probiotic supplementation is able to modify the fecal microbiota of sows and further shape the gut microbiota in their offspring [
2,
3]. Dietary
B. subtilis supplementation can elevate the abundance of the
Lactobacillus species in the colon of sows and reduce the abundance of
Clostridium perfringens and
Escherichia coli [
3,
19]. In contrast, the fecal microbial population of sows is not changed in response to administration of
B. mesentericus in combination with
Clostridium butyricum and
Enterococcus faecalis, whereas the abundance of genus
Bifidobacterium in the ileum of their offspring is increased [
22]. Dietary supplementation of
B. subtilis in the diet of sows increases the abundance of
Bacillus species in the feces [
21]. Previous studies have mainly used traditional methods for investigating the effects of probiotic supplementation on the microbiota of sows and their offspring. Here, we found that BLFP-fed sows tended to have increased bacterial species evenness in the feces and modified bacterial composition. Dietary supplementation of BLFP in the diet of sows also increased the genus
(Eubacterium) coprostanoligenes group abundances in the feces. The genus
(Eubacterium) coprostanoligenes group, a cholesterol-reducing anaerobe, catalyzes the conversion of cholesterol to coprostanol [
25]. It has been reported that dietary
B. subtilis supplementation increases the genus
(Eubacterium) coprostanoligenes group abundances in the feces of weaning piglets [
26]. The abundance of the genus
(Eubacterium) coprostanoligenes group in the feces is negatively correlated with the diarrhea incidence of piglets [
27]. Taken together, supplementation of BLFP in the diet of sows can modify the gut microbiota and probably increase the beneficial bacterial population, thereby reducing the load of pathogens in the environment. Whether feeding the BLFP to sows also has an impact on the gut microbiota of their offspring still needs to be investigated.
PDS is a major disease occurring in sows and many pathogens can be isolated from the milk and feces of sows with PDS [
7]. The coliform bacteria, such as genus
Escherichia,
Citrobacter,
Enterobacter, and
Klebsiella, are frequently found in sows with PDS [
7]. It has been reported that dietary fermented feed supplementation can reduce the pathogen challenge of the neonatal environment [
23]. In the present study, we found that sows with PDS tended to have increased abundance of the genus
Escherichia-Shigella and decreased abundance of the genera
Prevotella 9 and
Ruminococcaceae UCG-005 in the feces. The genera
Escherichia-Shigella and
Prevotella 9 are classified as pathogenic bacteria and beneficial bacteria in pigs, respectively [
14,
15,
27]. Furthermore, postpartum sows with PDS had increased solid content compared with healthy sows. However, PDS did not have an impact on the piglet body weight at weaning. A previous study has shown that the combined use of
B. subtilis and
B. licheniformis in sows tends to reduce the incidence of PDS and the return to oestrus interval [
4]. In the present study, no significant interaction between BLFP and PDS on the improvement in litter performance traits, milk composition, and fecal microbiota was found. These observations suggest that sows with PDS can cause gut microbiota imbalance. Whether these changes of fecal microbiota have a direct effect on the incidence of PDS in sows remains to be confirmed.
Since the farm had a previous history of pre-weaning diarrhea syndrome caused by PEDV, the PEDV may be a major reason for the increased pre-weaning mortality in the present study. However, the PEDV infection rate, recovery rate, and died from porcine epidemic diarrhea rate in piglets is unclear. Based on the current findings, the average pre-weaning mortality per litter of the control group was 38.37% in this PEDV-positive farm. In the BLFP group, the average pre-weaning mortality per litter was not improved (40.68%). This result implies that PEDV may be prevalent and has a similar infection rate in these two groups. Further, BLFP supplementation in the diet of sows cannot alleviate the pre-weaning mortality per litter. Whether there is any interaction between BLPF, PDS, and PEDV on litter performance traits still needs to be investigated.