
==== Front
Poult Sci
Poult Sci
Poultry Science
0032-5791
1525-3171
Elsevier

S0032-5791(24)00766-1
10.1016/j.psj.2024.104187
104187
IMMUNOLOGY, HEALTH AND DISEASE
Yeast cell wall supplementation affects the Salmonella enteretidis load in the ceca and ovaries of layer pullets
Hofacre Charles L. ⁎
Baxter Jennie ⁎
Berghaus Roy †‡
Bonato Melina Aparecida melina.bonato@iccbrazil.com.br
§1
de Souza Fernando Augusto §
⁎ Southern Poultry Research Group, INC., Watkinsville, GA 30677
† Department of Population Health, The University of Georgia, Athens, GA 30607
‡ Department of Population Health, Food Animal Health and Management, Poultry Diagnostic and Research Center, Southeastern Cooperative Wildlife Disease Study, The University of Georgia, Athens, GA 30607
§ R&D Department, ICC Ind. Com. Imp. Exp. Sao Paulo, SA, 01451-909, Brazil
1 Corresponding author: melina.bonato@iccbrazil.com.br
08 8 2024
11 2024
08 8 2024
103 11 10418727 5 2024
3 8 2024
© 2024 The Authors
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Salmonella enteretidis (SE) has a great propensity to translocate from the cecum into internal organs such as the spleen and liver. However, a major concern is the ability of SE to colonize the ovaries. This study aimed to evaluate the efficacy of cell walls from Saccharomyces cerevisiae to control the Salmonella load in the ceca and ovaries of commercial layer pullets. Ten-week-old layer pullets were divided into 2 groups: one group was fed a control diet with commercial feed without additives, and another group was fed the same diet supplemented with 0.5 kg/metric ton of yeast cell walls (YCWs). At 16 wk of age, the birds in both groups were challenged with 3.0 × 109 CFU/mL SE by oral gavage. The birds were euthanized on d 7 and 14 postchallenge to collect the ceca and ovaries for Salmonella load determination. The results demonstrated that there were no statistical differences in ovary SE infection rates. The trend in the prevalence of SE positivity in the ovaries was similar at 14 d, with 2.1% (YCW pullets) to 4.2% positive for the ovaries of the nontreated pullets. There was also no significant difference in the SE log10 MPN/gram between the YCW and the control groups. In the ceca, the high level of SE (3.0 × 109 cfu/pullet), which results in ovarian transmission, causes high intestinal tract inflammation. There was a significant difference in the prevalence of SE in the ceca at 7 d postchallenge but not at 14 d postchallenge. In conclusion, the reduction in Salmonella load observed in the ceca on d 7 in this study shows the potential of YCW supplementation for reducing Salmonella colonization in poultry.

Key words

Salmonella enteretidis
Saccharomyces cerevisiae
cecal contamination
oral gavage
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pmcINTRODUCTION

Salmonellosis in humans is a disease transmitted mainly by contaminated food, including eggs (Chousalkar et al., 2018). An egg can be contaminated with Salmonella during its formation in the reproductive tract of an infected hen (vertical transmission), or it can be contaminated horizontally (after the shell has formed either during oviposition or following oviposition), depending upon the nature of the pathogen and the architecture of the eggshell (Samiullah et al., 2013). Salmonella enteretidis (SE) primarily follows the vertical transmission route (Keller et al., 1997).

SE is likely to translocate from the ceca into internal organs such as the spleen and liver. However, a major concern is the ability of SE to colonize the ovaries (Gast et al., 2019) and, consequently, to contaminate the eggs. Invasion of the ovaries and oviducts may contaminate the edible interior contents of forming eggs before they are surrounded by shells and laid (De Buck et al., 2004; Gantois et al., 2009).

Some feed additives, such as prebiotics and probiotics, have been shown to effectively reduce the load of Salmonella in the gastrointestinal tracts of animals (Van Immerseel et al., 2002; Bielecka et al., 2010; Micciche et al., 2018; Kim et al., 2019). The yeast cell walls (YCW) of Saccharomyces cerevisiae are a prebiotic feed additive that can reduce Salmonella load through an agglutination mechanism (Mirelman et al., 1980; Borowsky et al., 2009). Attachment is often mediated through the binding of bacterial lectins to receptors containing D-mannose (Eshdat et al., 1978), and it is possible to block lectin binding with mannose or similar sugars, such as the mannan oligosaccharides (MOS) present in the YCW, and inhibit bacterial attachment (Spring et al., 2000).

A reduction in the SE load in the gastrointestinal tract can also lower the chances of Salmonella infection and colonization in the ovary and oviduct, which potentially contaminates eggs and thereby contributes to human outbreaks of salmonellosis (De Buck et al., 2004; Gantois et al., 2009).

Research on the preventive efficacy of yeast-derived components such as mannan-oligosaccharides (MOS), beta-glucans, and cell wall polysaccharides against Salmonella infection in chickens has shown promising results. Studies by Baurhoo et al. (2007) and Spring et al. (2000) demonstrated that dietary MOS supplementation at levels of 0.2 to 0.5% reduced Salmonella colonization in the ceca and improved growth performance. Lowry et al. (2005) and Chen et al. (2008) found that yeast beta-glucan supplementation (0.05–0.1%) enhanced immune responses and reduced Salmonella colonization in the ceca. Furthermore, Gómez-Verduzco et al. (2009) and Shanmugasundaram et al. (2013) showed that yeast cell wall polysaccharides (0.1–0.2%) improved immune responses, reduced Salmonella shedding in feces, and enhanced growth performance. The preventive efficacy is typically observed when these components are supplemented at levels ranging from 0.05 to 0.5% in the diet.

The mechanisms of action include binding to Salmonella to prevent its attachment to the intestinal epithelium, modulating gut microbiota, and stimulating both innate and adaptive immune responses (Spring et al, 2000). These findings suggest that yeast-derived supplements could serve as effective natural alternatives to antibiotics for controlling Salmonella infections in poultry.

The objective of this study was to evaluate the ability of Yeast Cell Wall (YCW) supplementation to reduce the SE load in the gastrointestinal and reproductive tracts of layer pullets.

MATERIALS AND METHODS

Birds and Housing

A total of 192 pullets (HyLine W36, Aviagen Dallas Center, Iowa) of 10 wk of age were housed in individual cages, composing groups of 48 cages per battery and 2 groups per treatment (96 birds per treatment). Each cage was considered a replicate. These birds had not previously received any Salmonella vaccine. Ambient humidity and controlled lighting were applied to induce egg production at the appropriate age.

Diet

Upon arrival, all birds were fed a nonmedicated commercial layer diet with formulations typically used for birds of a similar age. The diets were fed in mash form, and the formulations were based on corn and soybean meal (Table 1). The calculated analyses met or exceeded the NRC standards (National Research Council, 1994). Antibiotics were not added to any feed. Feed and water were provided ad libitum.Table 1 Diet ingredients and formulation.

Table 1Ingredient	%	
Corn	69,12	
Soybean meal	17,43	
Corn DDGS	10,00	
Dicalcium phosphate	1,566	
Calcium carbonate	1,362	
Salt (NaCl)	0,323	
Trace Mineral	0,075	
Vitam premix	0,065	
Fat (vegetable)	0,050	
Methionine MHA	0,008	
Total	100,0	

The YCWs used in this test (IMW50, ICC Animal Nutrition, Brazil) were originally from S. cerevisiae, which was used in sugar-cane fermentation processes to produce ethanol. The guaranteed beta-glucan level was 35%, and that of mannan oligosaccharides was 20%. The nutritional levels of the diets were the same; the difference between the treatments was the inclusion of 0.5 kg/MT of YCW on top. This dosage is a minimum described to obtain beneficial effects and have a good relationship with the costs.

Challenge Protocol

At 12 wk of age, the day length of the pullet was increased to 16 h to stimulate ovarian development. At 16 wk of age, each bird was orally challenged with 1 mL of a nalidixic acid-resistant strain of SE at 3.0 × 109 CFU/mL, according to Hofacre et al. (2018). One week postchallenge (17 wk of age), 48 pullets per treatment group were necropsied to obtain ceca and ovarian samples. At 14 d postchallenge (18 wk of age), the remaining 48 birds per treatment group were necropsied and cultured. Environmental contamination was measured by boot sock swabs of feces below the pullet cages and was negative for SE twice before challenge initiation. One week postchallenge, all the environmental boot sock swabs were SE-positive.

Sample Collection

At 7 and 14 d postchallenge, pullets were euthanized by cervical dislocation. The ceca and ovaries were aseptically removed, weighed, and placed into sterile plastic sampling bags (Fisher Scientific, Suwanee, GA) for Salmonella isolation. Each ovary clutch was placed in one bag, mashed, and cultured.

Salmonella Isolation and Identification

Individual samples were placed in a 125 mL sterile container, 100 mL of Buffer Peptone Water (BPW) was added, and the samples were serially diluted and spread-plated onto an XLT-4 plate (Difco). After incubation (24 h at 37°C), black colonies were counted. Selective enrichment was used to detect the presence of Salmonella when the direct plating method was negative. The remaining 9 mL of BPW was incubated (24 h at 37°C). A 1 mL aliquot was enriched in 9 mL of tetrathionate broth (Difco) and incubated (24 h at 42°C). A loopful of incubated media was streaked onto xylose Lysine tergitol-4 (XLT-4) plates containing 25 μg of nalidixic acid/mL to facilitate the selection of antimicrobial-resistant challenge organisms for selective differentiation by incubation (24 h at 37°C). Suspect Salmonella identification was confirmed, and serogroup identification was performed using poly-O Salmonella-specific antiserum (MiraVista, Indianapolis, IN). Ten milliliters of BPW were added to each ceca plastic bag and homogenized for 1 min. Serial dilution by MPN was performed.

Salmonella Enumeration Procedure

Salmonella in all ceca samples was enumerated using the MPN method. A 1 mL sample of supplemented peptone broth was transferred to 3 adjacent wells in the first row of a 2 mL-deep 96-well block. A 0.1 mL aliquot was transferred to 0.9 mL of tetrothionate broth in the second row. This process was repeated for the remaining rows, producing 5 tenfold dilutions. The blocks were incubated (24 h at 42°C). One microliter from each well was transferred onto XLT-4 agar containing nalidixic acid with a sterile multichannel pipette or a pin-tool replicator, and the plates were incubated for 24 h at 37°C. The final dilution of each sample was recorded, and the sample was entered into the MPN calculator (U.S. Environmental Protection Agency, 2013) to determine the sample MPN. Suspect Salmonella isolates were confirmed by poly(O) antisera.

Monitoring of Health and Mortality

All birds were monitored for general flock conditions, temperature, lighting, water, feed, litter culture, and unanticipated house conditions/events. No concomitant drug therapy was used during the study. The birds were checked daily for mortality. Birds were culled only to relieve suffering. When a bird was culled (or found dead), the date was recorded, and gross necropsy was performed to determine the probable cause of death.

Statistical Analysis

The prevalence of Salmonella in the ovarian and ceca samples was compared between treatment groups by using Fisher's exact test. Salmonella MPNs were compared between treatment groups using the nonparametric Mann‒Whitney test. To compare Salmonella MPNs, samples with a negative culture result by the MPN method but a positive culture result by primary or secondary enrichment were arbitrarily assigned an MPN value equal to one-half the minimum detection limit of the MPN assay. MPN values were log-transformed before statistical analysis. All statistical tests assumed a 2-sided alternative hypothesis, and P < 0.05 was considered to indicate statistical significance. Analyses were performed using commercially available statistical software (Stata version 14.1, StataCorp LP, College Station, TX).

RESULTS

Cecal and Ovarian Contamination

The SE challenge applied in this experiment was proposed to involve intestinal ovarian transmission, which could be observed through the identification and bacterial count of SE in the cecum and ovaries (Tables 2 and 4).Table 2 Summary of log10 Salmonella MPN per gram in culture-positive cecal samples from each of the 2 treatment groups by day postchallenge.

Table 2Day postchallenge	Treatment	n	Mean (SD)	Median	1P value	
7	None	47	2.91 (1.35)	2.70 a	0.016	
YCW	45	2.30 (1.46)	2.23 b	
14	None	25	0.40 (0.77)	0.07	0.563	
YCW	23	0.30 (0.61)	0.07	
1 Mann‒Whitney test. Within days, medians with a superscript in common do not differ with a level of significance of 5%.

Table 2 summarizes the Salmonella counts by MPN for the culture-positive cecal samples. On d7, the MPNs of the YCW group were significantly lower than those of the untreated group (P = 0.016), while they did not differ significantly between the groups on d 14 (P = 0.563).

The prevalence of cecal Salmonella in the 2 treatment groups is summarized by day post-challenge in Table 3. There was no significant difference between the groups with respect to Salmonella prevalence in the ceca on either d 7 (P = 0.617) or D 14 (P = 0.683). All Salmonella isolates from the cecal samples were identified as serogroup D.Table 3 Cecal Salmonella prevalence in birds from each treatment group by day postchallenge.

Table 3Day postchallenge	Treatment	n	No. positive (%)	1P	
7	None	48	47 (97.9)	0.617	
YCW	48	45 (93.8)	
14	None	47	25 (53.2)	0.683	
YCW	48	23 (47.9)	
1 Mann‒Whitney test. Within days, medians with a superscript in common do not differ with a level of significance of 5%.

Table 4 summarizes the Salmonella MPNs in the culture-positive ovary samples on d 7 postchallenge. The MPNs did not differ significantly between the groups (P = 0.464). MPN assays were not performed for ovarian samples collected 14 d postchallenge.Table 4 Summary of log10 Salmonella MPN per gram in culture-positive ovary samples from the 2 treatment groups on d 7 postchallenge.

Table 4Day postchallenge	Treatment	n	Mean (SD)	Median	1P	
7	None	20	0.07 (0.35)	−0.01	0.464	
YCW	16	0.24 (0.59)	−0.02	
1 Mann‒Whitney test. Medians with a superscript in common do not differ at the 5% level of significance.

There were no significant differences in SE prevalence between the treatment groups on either d 7 (P = 0.527) or d 14 (P = 1.00) (Table 5). All Salmonella isolates were identified as serogroup D, consistent with the SE challenge strain.Table 5 The prevalence of ovarian Salmonella in birds from each treatment group by day postchallenge.

Table 5Day postchallenge	Treatment	N	No. positive (%)	1P	
7	None	48	20 (41.7)	0.527	
YCW	48	16 (33.3)	
14	None	48	2 (4.2)	1.00	
YCW	48	1 (2.1)	
1 Fisher's exact test. Within days, percentages with a superscript in common do not differ at a level of significance of 5%.

DISCUSSION

In this study, administering a high dose (3.0 × 109 CFU/mL) of SE intended to induce ovarian SE colonization resulted in a major challenge to the intestinal tract (Table 3). Studies have shown that SE challenge doses used in experiments with broilers and chickens can range from 105 to 109 CFU per bird, depending on the age of the birds, the purpose of the study, and the challenge model used (Borsoi et al., 2011; Ricke et al., 2013; Kilroy et al., 2015; Pande et al., 2016; Adhikari et al., 2020).

According to Gast et al. (2007), lower dosages are generally used in studies with older birds or in studies aiming to assess the prevalence of Salmonella, while higher dosages are generally used in studies with young birds or in studies aiming to assess the pathogenicity of the bacteria or translocation of the bacteria, as well as the effectiveness of vaccines, additives, or antibiotics.

In this study, YCW supplementation in pullet feed at an inclusion rate of 0.5 kg/MT did not affect the number of Salmonella-positive ovarian samples. Although there was a significant reduction in Salmonella numbers in the ceca on d 7, this change did not translate to a reduction in Salmonella numbers in the ovaries of the pullets. It is possible that the dose and/or duration of YCW supplementation were insufficient to significantly impact ovarian colonization in this high-dose challenge model.

There was a reduction in the log of SE in ceca at d 7 (Table 2) in YCW treatment, but on the 14th occurred a natural reduction in both treatments. Compared with ovaries, the contamination was lower than ceca, but the effect was similar: positivity for SE at d 7 and a natural reduction at d 14 (Table 5). Previous studies have demonstrated the ability of MOS present in YCWs to reduce Salmonella colonization in the gastrointestinal tracts of poultry (Spring et al., 2000; Fernandez et al., 2002). MOS can bind to Salmonella type 1 fimbriae, preventing their adhesion to the intestinal epithelium (Firon et al., 1983). However, the efficacy of YCW in reducing Salmonella infection in poultry may vary depending on factors such as the dose and duration of supplementation, as well as the strain and dose of the challenge (Pourabedin and Zhao, 2015).

The dose used in this study, 0.5 kg/MT YCW, represents 100 g of MOS per ton of feed or 0.01% of MOS. A feed intake of 100 g/bird is equivalent to an average intake of 10 g MOS/bird/d. The dosage in this study was sufficient to reduce the bacterial count on the 7th d in the cecum, but it could not be reduced in the ovaries (Table 4). It's an important point to be considered is the effect of bacterial agglutination on the surface of the MOS; there must be direct contact between the bacteria and the receptors containing D-mannose present in the YCW (Eshdat et al., 1978). Therefore, the concentration and constant presence of MOS in the intestine are important for promoting the elimination of these pathogens from the intestine and, consequently, preventing infection of other organs, such as the ovaries.

Several studies evaluated the dosages of MOS supplementation in laying hens and broilers, ranging from 500 g/MT to 5 kg/MT. Agunos et al. (2007) used 1 kg D-mannose in the diets of broiler chickens orally challenged with 2 × 107 cfu SE/mL and observed a reduction in SE colonization in the ceca and livers. Baurhoo et al. (2009) supplemented the diets of chickens with 2 kg/MT and 5 kg/MT YCW in a study without challenge and with good sanitary conditions and reported a reduction in the cecal populations of E. coli and improvements in intestinal morphology in the birds. Chee et al. (2010) added 2 kg/MT of YCW to the diets of laying hens and observed a positive effect on S. enteritidis agglutination and the immune response. Gómez-Verduzco et al. (2009) supplemented chickens' diets with 500 g/MT of YCW and reported a positive impact on broilers' humoral immune responses and antibody production against the Newcastle vaccine. Lourenço et al. (2015) added 1 kg/MT and 2 kgMT of MOS to the diets of chickens and observed a positive effect on the intestinal morphology, cecal microbiota, and performance of broilers challenged with S. enteritidis. These results suggest that a minimum of 1 kg/MT of MOS supplementation may be a promising nutritional strategy for improving gut health, immune response, and performance in poultry, and it may aid in controlling pathogenic bacteria such as Salmonella and E. coli.

It was observed that even in the case of Saccharomyces cerevisiae, the source of the yeast cell wall, the method of extraction of MOS and Beta-glucans, the degree of purity, and their origin could directly influence the efficacy of the final product (Liu et al., 2021). Yeasts from the sugarcane ethanol fermentation process have a thicker cell wall than yeasts used in bakeries and breweries, mainly altering beta-glucan concentrations (Basílio et al., 2008). The type of processing and extraction of digestible compounds from the cell wall also modifies its effectiveness; that is, the functional effect of yeast is inversely proportional to its digestibility (Basílio et al., 2008).

In this study, a YCW from the ethanol fermentation process was used, which contains a composition of 20% of MOS and 35% of Beta-glucans. Due to the link with beta-glucan, the digestibility of YCW is lower than that of a bakery or brewery. The cell wall structure is merely determined by cross-linking between cell wall polymers, which points out the role of b-1,6-glucan in this process (Aguilar-Uscanga and Francois, 2003). When linked with beta-glucan, MOS efficacy promotes agglutination's effect on bacteria, and it is eliminated with feces.

Interestingly, after 14 d, both treatments reduced the total bacterial load (Tables 3 and 5), which was also observed by Kogut et al. (2005). According to Gast et al. (2005), birds' immune systems and defense mechanisms continuously work to eliminate Salmonella from the body, either through the action of macrophages and heterophils, through phagocytosis and destruction of bacteria, or through fecal elimination to reduce the bacterial load over time.

YCW is a source of beta-glucans (35%), and although immune system parameters were not measured in this study, beta-glucans are recognized by receptors present in macrophages, neutrophils, and dendritic cells (Brown and Gordon, 2003). They stimulate the immune system and increase the production of proinflammatory cytokines and microbicidal activity (Estrada et al., 1997; Vetvicka and Yvin, 2004).

CONCLUSIONS

In conclusion, the use of YCW promoted a reduction in cecal Salmonella load on d 7 postinfection and demonstrated the potential of MOS supplementation for reducing Salmonella cecal colonization in layer pullets. However, the dosage of YCW used in this study did not influence the colonization in ovaries. A significant impact on ovarian colonization highlights the need for further research to determine the optimal dose and duration of YCW supplementation, particularly in high-dose challenge models.

DISCLOSURES

The authors declare no conflicts of interest.

Declaration of Generative AI and AI-Assisted Technologies in the Writing Process: During the preparation of this work the author(s) do not used AI services.

ACKNOWLEDGMENTS

ICC Animal Nutrition has funded the research.

Ethical Approval: This study was approved by the SPRG IACUC (number ICSE122015-52G ).
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