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. 2023 Jun 7;101:skad191. doi: 10.1093/jas/skad191

Effects of a Saccharomyces cerevisiae fermentation product on fecal characteristics, metabolite concentrations, and microbiota populations of dogs undergoing transport stress

Patrícia M Oba 1,✉, Meredith Q Carroll 2, Kelly M Sieja 3, Xiaojing Yang 4, Tammi Y Epp 5, Christine M Warzecha 6, Jessica L Varney 7, Jason W Fowler 8, Craig N Coon 9, Kelly S Swanson 10,11,12
PMCID: PMC10284041  PMID: 37283549

Abstract

Previously, a Saccharomyces cerevisiae fermentation product (SCFP) positively altered fecal microbiota, fecal metabolites, and immune cell function of adult dogs. Our objective was to determine the fecal characteristics, microbiota, and metabolites of SCFP-supplemented dogs subjected to transport stress. All procedures were approved by the Four Rivers Kennel IACUC prior to experimentation. Thirty-six adult dogs (18 male, 18 female; age: 7.1 ± 0.77 yr; body weight: 28.97 ± 3.67 kg) were randomly assigned to be controls or receive SCFP supplementation (250 mg/dog/d) (N = 18/group) for 11 wk. At that time, fresh fecal samples were collected before and after transport in a hunting dog trailer with individual kennels. The trailer was driven 40 miles round trip for about 45 min. Fecal microbiota data were evaluated using Quantitative Insights Into Microbial Ecology 2, while all other data were analyzed using the Mixed Models procedure of Statistical Analysis System. Effects of treatment, transport, and treatment × transport were tested, with P < 0.05 being considered significant. Transport stress increased fecal indole concentrations and relative abundances of fecal Actinobacteria, Collinsella, Slackia, Ruminococcus, and Eubacterium. In contrast, relative abundances of fecal Fusobacteria, Streptococcus, and Fusobacterium were reduced by transport. Fecal characteristics, metabolites, and bacterial alpha and beta diversity measures were not affected by diet alone. Several diet × transport interactions were significant, however. Following transport, relative abundance of fecal Turicibacter increased in SCFP-supplemented dogs, but decreased in controls. Following transport, relative abundances of fecal Proteobacteria, Bacteroidetes, Prevotella, and Sutterella increased in controls, but not in SCFP-supplemented dogs. In contrast, relative abundances of fecal Firmicutes, Clostridium, Faecalibacterium, and Allobaculum increased and fecal Parabacteroides and Phascolarctobacterium decreased after transport stress in SCFP-supplemented dogs, but not in controls. Our data demonstrate that both transport stress and SCFP alter fecal microbiota in dogs, with transport being the primary cause for shifts. SCFP supplementation may provide benefits to dogs undergoing transport stress, but more research is necessary to determine proper dosages. More research is also necessary to determine if and how transport stress impacts gastrointestinal microbiota and other indicators of health.

Keywords: 16S rRNA sequencing, canine microbiota, yeast product

A study was conducted to determine the fecal characteristics, microbiota, and metabolites of dogs supplemented with a Saccharomyces cerevisiae fermentation product (SCFP) and subjected to transport stress. Our data demonstrate that both transport stress and SCFP alter fecal microbiota in dogs, but that greater changes were due to transport.

Introduction

In biology, stress refers to an organism’s inability to respond adequately to a physical challenge (Selye, 1936). The physiological changes that result from environmental disturbances are not inherently negative; instead, they play a crucial role in assisting an organism in adapting to a shifting environment. Response mechanisms include cortisol, the autonomic nervous system, metabolic hormones, and immune system mediators that aid in adaptation to stressors (McEwen, 1998). In situations that animals find unpleasant, they display behavioral and physiological signs of stress. Transport stress is classified as acute stress because it is a brief stressor lasting only a few minutes or hours, and a physical stressor, resulting in a change in the animal’s environment. Noise, movement, and immobilization during transportation have been shown to elicit responses in behavioral, cardiovascular, endocrine, renal, gastrointestinal, and hematological parameters (Beerda et al., 1997).

Experiments conducted over the years, utilizing germ-free animals or by inducing gut microbiota shifts in conventional animals with antibiotics, probiotics, or prebiotics, have provided evidence that the gut microbiota has an impact on the brain and behavior, thereby confirming the existence of a gut-microbiome-brain axis (Cryan and Dinan, 2012). In mice, stress-induced gut dysbiosis has been shown to have negative health consequences such as disruption of the intestinal barrier and increased inflammation (Chassaing et al., 2015). Stress-induced pathogenic bacteria overgrowth has also been shown to disrupt the gut microbiota and immune system, resulting in intestinal inflammation, depression, and cognitive impairment in mice (Jang et al., 2018; Kim et al., 2020). Changes in the composition of the murine gut microbiota may be to blame for stress-related gastrointestinal symptoms (Bharwani et al., 2016; Kuti et al., 2020). Furthermore, the gut microbiome produces numerous metabolites, such as short-chain fatty acids (SCFA), that play an important role in colon health by lowering colonic pH (Scott et al., 2013; Louis and Flint, 2017). Stress has been shown to lower SCFA concentrations in the colon of mice and alter the abundance of SCFA-producing bacteria (Maltz et al., 2019). Increasing SCFA concentrations has been shown to help alleviate stress-induced changes in the gut-brain axis of mice (van de Wouw et al., 2018). Therefore, the gut microbiota and its metabolites play an important role in maintaining host immune function and intestinal homeostasis (Takakuwa et al., 2019).

SCFP is a dried substance that contains residual yeast cells, fragments of yeast cell walls, metabolites produced during fermentation, and the media used in the process. SCFP is considered a functional ingredient with the potential to reduce oxidative stress and inflammation during periods of acute stress. Previous studies have demonstrated that it can positively impact immune function, gastrointestinal health outcomes, and oxidative stress markers in adult dogs (Lin et al., 2019; Varney et al., 2021; Wilson et al. 2022, 2023; Oba et al., 2023). Supplementing SCFP during transport stress may also suppress activation of innate immune cells, providing additional benefits to dogs (Wilson et al., 2023). Mannanoligosaccharides and β-glucans, which are components of yeast cell walls, have been shown to have a positive impacts on intestinal health and barrier function. Specifically, they can enhance beneficial microbial populations, reduce the expression of inflammatory mediators, and improve the expression of tight junction proteins that are linked to lower intestinal permeability (Swanson et al., 2002; Grieshop et al., 2004; Han et al., 2017; Theodoro et al., 2019; de Oliveira Matheus et al., 2021).

Dogs are frequently exposed to a range of stress-inducing situations as a result of their interactions with humans. One of the most common stressors for most domestic animals relates to travel or transportation. Having a better understanding of the impact that travel-induced stress has on fecal characteristics, metabolite concentrations, and microbiota populations, and how dietary supplementation influences these responses, may facilitate more effective stress management. Therefore, the current study aimed to investigate the fecal characteristics, microbiota populations, and metabolite concentrations of SCFP-supplemented dogs subjected to transport stress. We hypothesized that SCFP would beneficially shift and maintain the stability of the fecal microbiota and metabolites, and avoid poor fecal scores, following transport stress.

Materials and Methods

The animal study was conducted at Four Rivers Kennel, LLC. (Walker, MO). All experimental procedures were approved by the Four Rivers Kennel, LLC. IACUC (FRK-20) prior to experimentation, with all procedures being performed in accordance with the U. S. Public Health Service Policy on Humane Care and Use of Laboratory Animals.

Animals and housing

Thirty-six healthy and working Labrador Retrievers [18 intact males and 18 intact females; mean age: 7.19 ± 0.77 yr, mean body weight (BW): 28.97 ± 3.67 kg, mean body condition score (BCS): 4.83 ± 0.97] were utilized for this completely randomized design study. All dogs were housed in individual kennels overnight and during inclement weather. Each kennel measured 1.22 m × 1.83 m × 1.83 m. Each kennel had a metal nipple drinker available for access to water ad libitum. All dogs were fed in their individual kennels each morning (0900 hours). The temperature of the kennel was controlled with the use of heated floors, tunnel ventilation, ceiling fans, and HVAC units. All dogs were placed in social groups in outside airing yards each day, weather permitting, which contain shade/shelter and automatic waters.

Diets and experimental timeline

All dogs consumed the same diet (Gold-N-Pro, MFA Inc., Columbia, MO) throughout the study to maintain BW and BCS. This diet is the standard kennel diet and is fed to all dogs beginning from 1 yr of age. The analyzed chemical and ingredient composition of this diet is presented in Supplementary Table 1. Dogs were randomly divided into two groups, blocked on the basis of age, sex, BW, BCS, and body composition data (via dual-energy x-ray absorptiometry scans). Dogs were either fed the standard kennel diet only (control) or were fed the standard kennel diet + a SCFP tablet containing TruMune (Diamond V Mills Inc., Cedar Rapids, IA) for 11 wk (N = 18 per group). The 0.5 g tablet contained 0.25 g of active ingredients and 0.25 g of inactive ingredients (dicalcium phosphate, powdered cellulose, magnesium stearate). The dosage was based on the results of a previous study (Lin et al., 2019).

After 11 wk of feeding, dogs were subjected to transport stress. Fresh fecal samples were collected before (morning before transport) and after (morning on the day after transport). The transport stress was induced by transporting dogs for 40 miles round-trip using a hunting dog trailer towed by a standard pick-up truck. The stressor lasted 45 min, from the time the trailer departed the kennel to its return. The trailer held a capacity of six dogs, requiring six individual trips that followed the same route at the same speed. Each dog was confined to an individual kennel space in the trailer but could see and hear the dogs kenneled next to them.

Fecal sample collection

Fresh fecal samples (within 15 min of defecation) were collected before (morning before transport) and after (morning of 1 d after transport) transport for the measurement of fecal characteristics (fecal scores; pH; dry matter percentage), microbiota populations, and metabolites. At each time point, fecal samples were scored according to the following scale: 1 = hard, dry pellets, small hard mass; 2 = hard, formed, dry stool; remains firm and soft; 3 = soft, formed, and moist stool, retains shape; 4 = soft, unformed stool, assumes shape of container; and 5 = watery, liquid that can be poured.

Fecal pH was measured immediately using a pH meter (Denver Instrument, Bohemia, NY) equipped with an electrode (Beckman Instruments Inc., Fullerton, CA) and then samples were divided into several aliquots. Aliquots for analysis of phenols and indoles were frozen at −20 °C immediately after collection. One aliquot was collected and placed in 2 N hydrochloric acid and then −20 °C for ammonia, SCFA, and branched-chain fatty acid (BCFA) analyses. One aliquot was immediately transferred to four sterile cryogenic vials (Nalgene, Rochester, NY) and placed on dry ice until being transferred to a −80 °C freezer and stored until microbial analyses. A final aliquot was collected for measurement of dry matter (105 °C in oven for 2 d).

Fecal metabolite concentrations

Fecal SCFA and BCFA concentrations were determined by gas chromatography according to Erwin et al. (1961) using a gas chromatograph (Hewlett-Packard 5890A series II, Palo Alto, CA) and a glass column (180 cm × 4 mm i.d.) packed with 10% SP-1200/1% H3PO4 on 80/100+ mesh Chromosorb WAW (Supelco Inc., Bellefonte, PA). Nitrogen was the carrier with a flow rate of 75 mL/min. Oven, detector, and injector temperatures were 125, 175, and 180 °C, respectively. Fecal ammonia concentrations were determined according to the method of Chaney and Marbach (1962). Fecal phenol and indole concentrations were determined using gas chromatography according to the methods described by Flickinger et al. (2003).

Fecal DNA extraction and MiSeq Illumina sequencing of 16S rRNA gene amplicons

Total DNA from fecal samples were extracted using Mo-Bio PowerSoil kits (MO BIO Laboratories Inc., Carlsbad, CA). Concentrations of extracted DNA were quantified using a Qubit 3.0 Fluorometer (Life Technologies, Grand Island, NY). 16S rRNA gene amplicons were generated using a Fluidigm Access Array (Fluidigm Corporation, South San Francisco, CA) in combination with Roche High Fidelity Fast Start Kit (Roche, Indianapolis, IN). The primers 515F (5ʹ-GTGCCAGCMGCCGCGGTAA-3ʹ) and 806R (5ʹ-GGACTACHVGGGTWTCTAAT-3ʹ) that target a 252 bp-fragment of the V4 region of the 16S rRNA gene were used for amplification (primers synthesized by IDT Corp., Coralville, IA; Caporaso et al., 2012). CS1 forward tag and CS2 reverse tag were added according to the Fluidigm protocol. Quality of the amplicons were assessed using a Fragment Analyzer (Advanced Analytics, Ames, IA) to confirm amplicon regions and sizes. A DNA pool were generated by combining equimolar amounts of the amplicons from each sample. The pooled samples will then be size selected on a 2% agarose E-gel (Life Technologies, Grand Island, NY) and extracted using a Qiagen gel purification kit (Qiagen, Valencia, CA). Cleaned size-selected pooled products were run on an Agilent Bioanalyzer to confirm appropriate profile and average size. Illumina sequencing was performed on a MiSeq using v3 reagents (Illumina Inc., San Diego, CA) at the Roy J. Carver Biotechnology Center at the University of Illinois.

16S rRNA microbial data analysis

Illumina 16S rRNA gene amplicon sequencing produced a total of 3,266,364 sequences, with an average of 45,366 sequences per sample. Forward reads were trimmed using the FASTX-Toolkit (version 0.0.13) and QIIME 2 (version 2019.4; Caporaso et al., 2011) were used to process the resulting sequence data. Raw sequenced amplicons were imported into the QIIME2 package and analyzed by the DADA2 pipeline for quality control (QC value ≥ 20), after removal of chimeric sequences. On average, 72.64% of features and 100% of the samples were retained after QC. Samples were then rarefied to 24,844 reads and subsequently assigned to taxonomic groups with the Greengenes database (Greengenes 13_8 99%, with the qiime2 classifier trained on the 515F/806R V4 region of 16S; Bokulich et al., 2018; Robeson et al., 2021).

Quantitative polymerase chain reaction (qPCR) and dysbiosis index (DI)

qPCR was performed according to previous methods (Panasevich et al., 2015). Briefly, primers targeting specific bacterial genera (Faecalibacterium, Turicibacter, Streptococcus, Escherichia coli, Blautia, Fusobacterium, Clostridium hiranonis, Bifidobacterium, Lactobacillus, Enterococcus) were used. qPCR data were expressed as the log amount of DNA (fg) for each particular bacterial group/10 ng of isolated total DNA according to Suchodolski et al. (2012). DI, which is based on the abundances of Faecalibacterium, Turicibacter, Streptococcus, E. coli, Blautia, Fusobacterium, C. hiranonis, was calculated according to Alshawaqfeh et al. (2017).

Statistical analyses

All data were analyzed using the Mixed Models procedure of SAS (version 9.4; SAS Institute, Cary, NC). Treatments and transport stress challenge were considered to be fixed effects and dogs were considered to be a random effect. The effects of treatment, transport stress, and treatment × transport stress interactions were tested. Data normality was checked using the univariate procedure and Shapiro–Wilk statistic, with log transformation being used when normal distribution was lacking. If after the logarithmic transformation of the data, the data did not reach normality, the data were analyzed using the npar1way procedure and Wilcoxon statistic. The Tukey’s multiple comparison analysis was used to compare LS means and control for experiment-wise error. Data were reported as means. Differences were considered significant when P < 0.05 and trends when P < 0.10.

Results

Transport stress challenge increased (P ≤ 0.05) fecal indole and total phenol and indole concentrations, with both being greater after transport stress (Table 1). However, fecal scores, pH, and dry matter content, and other fermentative metabolite concentrations were unaffected by transport stress. SCFP supplementation did not affect fecal characteristics and metabolite concentrations.

Table 1.

Fecal characteristics and metabolite concentrations of dogs before and after transport stress

Item Control SCFP1 SEM P-value
Before After Before After Treatment1 Transport Treatment × Transport
Fecal score2 3.28 3.19 3.25 3.17 0.10 0.8025 0.3570 1.0000
pH 6.32 6.22 6.43 6.24 0.11 0.5527 0.1679 0.6424
Dry matter (%) 31.08 31.57 31.32 32.03 0.93 0.7058 0.5200 0.9020
µmol/g dry matter basis
Ammonia 163.27 162.43 162.39 163.14 9.31 0.9187 0.9573 0.7925
Phenols and indoles
 Phenol 0.19 0.21 0.08 0.13 0.11 0.8513 0.1225 0.8725
 Indole 0.28 1.00 0.29 1.16 0.16 0.6521 <0.0001 0.5364
 Total phenols/indoles 0.47 1.21 0.37 1.28 0.23 0.9700 <0.0001 0.5039
SCFA
 Acetate 401.8 391.37 390.91 402.39 19.78 0.9979 0.9754 0.5230
 Propionate 202.76 196.59 202.69 206.13 10.35 0.6883 0.8780 0.5892
 Butyrate 58.54 56.53 57.96 65.04 4.69 0.4972 0.4444 0.1743
 Total SCFA 663.11 644.5 651.55 673.56 32.63 0.8138 0.9515 0.4693
BCFA
 Isobutyrate 6.29 6.42 7.03 6.37 0.40 0.4807 0.3531 0.1729
 Isovalerate 8.94 9.7 10.4 9.42 0.77 0.4269 0.9634 0.1607
 Valerate 3.81 3.26 1.99 2.14 0.73 0.2956 0.3987 0.3351
 Total BCFA 19.04 19.37 19.42 17.94 1.36 0.7626 0.4833 0.2736
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1SCFP = 1 tablet/d, 250mg.

2Fecal samples were scored according to the following scale: 1 = hard, dry pellets, small hard mass; 2 = hard, formed, dry stool; remains firm and soft; 3 = soft, formed, and moist stool, retains shape; 4 = soft, unformed stool, assumes shape of container; and 5 = watery, liquid that can be poured.

Transport stress or SCFP supplementation did not affect fecal bacterial alpha diversity (species richness; Figure 1). Bacterial beta diversity, as presented by an unweighted and weighted principal coordinates analysis (PCoA) plots, was not affected by SCFP treatment in dogs before or after transport stress challenge (Figure 2). When transport stress was analyzed on its own, the weighted PCoA plot showed a tendency (P = 0.093) for clustering of dogs before and after transport stress (Figure 3).

Figure 1.

Figure 1.

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Bacterial alpha diversity measures of fecal samples collected from dogs before and after transport stress.

Figure 2.

Figure 2.

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Bacterial beta diversity of fecal samples collected from control or SCFP-supplemented dogs before and after transport stress. The PCoA plot of weighted (a) and unweighted (b) UniFrac distances of fecal microbial communities were not different.

Figure 3.

Figure 3.

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Bacterial beta diversity of fecal samples collected from dogs before and after transport stress. The PCoA plot of unweighted (b) UniFrac distances of fecal microbial communities were not different. However, weighted (a) UniFrac distances of fecal microbial communities tended (P = 0.093) to cluster before and after transport stress.

Based on sequence data, transport stress challenge had significant (P < 0.05) effects on several fecal bacterial phyla and genera of dogs (Table 2). After transport stress, the relative abundances of fecal Actinobacteria, Collinsella, Slackia, Ruminococcus, and Eubacterium were higher (P < 0.05), while the relative abundances of fecal Fusobacteria, Streptococcus, and Fusobacterium were lower (P < 0.05) than baseline (before transport). The relative abundance of fecal Lactobacillus was affected by SCFP, being higher (P = 0.05) in SCFP-supplemented dogs than controls. Several treatment × transport interactions (P < 0.05) were identified. Following transport, fecal Turicibacter increased in SCFP-supplemented dogs, but decreased in controls. Following transport, fecal Proteobacteria, Bacteroidetes, Prevotella, and Sutterella increased in controls, but not in SCFP-supplemented dogs. Fecal Firmicutes, Clostridium, Faecalibacterium, and Allobaculum increased and fecal Parabacteroides and Phascolarctobacterium decreased after transport stress in SCFP-supplemented dogs, but not in controls.

Table 2.

Fecal bacteria (% of sequences) of dogs before and after transport stress

Phyla Genus Control SCFP1 SEM P-value
Before After Before After Treatment Transport Treatment × Transport
Actinobacteria 1.01 1.20 0.85 1.25 0.159 0.8983 0.0138 0.2922
Collinsella 0.83 0.99 0.65 1.01 0.140 0.9601 0.0092 0.1883
Slackia 0.15 0.17 0.12 0.18 0.021 0.9955 0.0150 0.1392
Bacteroidetes 16.98b 20.31a 18.92a,b 15.41a,b 1.872 0.5438 0.9306 0.0034
Parabacteroides 0.28a,b 0.35a,b 0.46a 0.23b 0.081 0.9356 0.3150 0.0099
Prevotellaceae Prevotella 4.72b 6.68a 5.66a,b 4.16a,b 0.930 0.5125 0.6797 0.0036
Paraprevotellaceae Prevotella 2.2 2.72 2.53 2.19 0.381 0.8130 0.7568 0.0902
Lactobacillus 5.33 3.77 10.46 8.42 1.970 0.0507 0.3557 0.8912
Firmicutes 59.32a,b 58.26a,b 57.66b 66.18a 2.751 0.3515 0.0773 0.0253
Streptococcus 0.95 0.59 1.17 0.98 0.320 0.9309 0.0100 0.8292
Turicibacter 1.24a,b 0.72b 0.82a,b 1.18a 0.376 0.1143 0.3658 0.0313
Clostridium 14.42a,b 13.88a,b 11.23b 14.51a 1.148 0.4622 0.0661 0.0138
Ruminococcus 1.92 2.27 1.74 2.31 0.183 0.9616 0.0058 0.2269
Butyricicoccus 0.27 0.29 0.31 0.34 0.121 0.0671 0.2448 0.7679
Faecalibacterium 6.33a,b 6.35a,b 5.47b 8.20a 0.023 0.5685 0.0034 0.0037
Phascolarctobacterium 1.14a,b 1.39a,b 1.38a 1.06b 0.104 0.7166 0.6871 0.0010
Allobaculum 1.50a,b 1.28a,b 1.09b 1.46a 0.166 0.4712 0.8490 0.0148
Clostridium 0.93 0.74 0.73 0.91 0.127 0.7378 0.7247 0.0670
Eubacterium 2.38 3.03 2.24 3.18 0.372 0.7543 0.0003 0.1360
Fusobacteria 19.02 15.37 17.84 13.29 1.161 0.2016 0.0005 0.6697
Fusobacterium 6.85 5.78 6.59 4.59 0.814 0.5104 0.0206 0.3194
Proteobacteria 3.62b 4.79a 4.67a,b 3.82a,b 0.542 0.8998 0.3155 0.0053
Sutterella 2.72b 3.65a 3.28a,b 2.81a,b 0.449 0.8111 0.3815 0.0125
Anaerobiospirillum 0.61 0.78 1.10 0.63 0.199 0.4079 0.5933 0.0577
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1SCFP = 1 tablet/d, 250mg.

a-bMeans with different superscripts within a row differ (P < 0.05).

Based on qPCR data, transport stress challenge affected (P < 0.05) several fecal bacterial genera, bacterial species, and DI (Table 3). DI and abundance of fecal E. coli, Fusobacterium, Bifidobacterium, and Enterococcus were lower (P < 0.05) after transport stress challenge. In contrast, abundance of fecal Faecalibacterium tended to be greater (P < 0.10), while abundance of fecal Streptococcus tended to be lower (P < 0.10) after transport stress. Supplementation of SCFP affected two bacterial genera, with the abundance of fecal Lactobacillus being greater (P < 0.05) and the abundance of fecal Turicibacter tending to be greater (P < 0.10) in dogs fed with SCFP.

Table 3.

Fecal bacteria (log DNA/gram of feces) and DI of dogs before and after transport stress

Control SCFP 1 SEM P-value
Before After Before After Treatment Transport Treatment× Transport
DI −2.59 −2.87 −2.11 −2.75 0.349 0.5202 0.0204 0.3472
Total bacteria (universal) 11.50 11.49 11.53 11.50 0.031 0.3135 0.8393 0.5185
Faecalibacterium 7.92 7.94 7.88 8.03 0.050 0.6245 0.0927 0.2145
Turicibacter 7.47 7.27 7.56 7.61 0.103 0.0938 0.3069 0.1174
Streptococcus 6.79 6.59 6.98 6.67 0.217 0.6245 0.0614 0.6565
E. coli 5.08 4.62 5.34 5.03 0.334 0.4546 0.0143 0.6446
Blautia 10.88 10.82 10.81 10.87 0.050 0.8329 0.9752 0.1500
Fusobacterium 9.70 9.55 9.70 9.44 0.058 0.3626 0.0003 0.2577
C. hiranonis 7.02 6.98 6.85 7.03 0.082 0.5506 0.3001 0.1146
Bifidobacterium 3.68 3.55 4.00 3.73 0.176 0.3061 0.0472 0.5916
Lactobacillus 7.25 6.99 7.61 7.43 0.239 0.0426 0.3889 0.8203
Enterococcus 4.27 3.90 4.43 4.28 0.139 0.1226 0.0094 0.2563
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1SCFP = 1 tablet/d, 250mg.

Discussion

Stress responses in dogs can be classified as behavioral, physiological, or immunological, with each highlighting a different way by which stress manifests itself. Noise, imbalance, ­immobilization, novelty, and transportation have all been linked to changes in behavioral, cardiovascular, endocrine, renal, gastrointestinal, and hematological parameters (Beerda et al., 1997; Farca et al., 2006; Gandia Estellés and Mills, 2006; Cannas et al., 2010). Transportation stress is commonly associated with vocalizations, restlessness, panting, trembling, salivation, and vomiting in dogs (Beerda et al., 1997; Farca et al., 2006; Gandia Estellés and Mills, 2006; Cannas et al., 2010), with 44% of dogs being reported to have travel-related issues (Cannas et al., 2010). While some studies have investigated the impact of transportation stress on canine behavior and identified physiological markers of acute stress during transportation, there is a lack of comprehensive research on how transportation stress affects companion animal fecal characteristics and microbiota (Venable et al., 2016; Perry et al., 2017; Wilson et al., 2023). Furthermore, there are limited solutions available for preventing or mitigating the negative effects of transportation without resorting to sedation or medication.

Regarding the impact of transportation stress on stool quality, one study reported that transporting dogs results in softer stools (Venable et al., 2016), while another study reported that transportation stress had no effect on canine fecal characteristics (Wilson et al., 2023). In the current study, transportation stress did not have an impact on fecal pH, dry matter percentage, or scores. One study tested the effects of transportation stress on the fecal microbiota composition of working dogs subjected to air travel (2.5 h). In that study, weighted UniFrac distances that take into account the relative abundances of taxa shared between samples, and unweighted UniFrac PCoA that takes in account the presence/absence of taxa shared between samples, revealed that animals undergoing transport stress had bacterial communities that were distinct from controls dogs not traveling (Venable et al., 2016). Additionally, relative abundances of fecal Clostridia and Bacteroidaceae were higher in dogs after transport stress than controls. Additionally, the relative abundances of fecal Bifidobacteriaceae, Blautia, and Bifidobacterium increased and relative abundance of fecal Clostridium tended to decrease after transport stress. A similar study testing working dogs subjected to helicopter travel (30 min) reported that transport stress had no effect on alpha and beta diversity measures of fecal microbiota and had no effect on fecal microbiota stability (Perry et al., 2017).

Puppies have been reported to have altered fecal bacterial alpha diversity and microbiota profiles when exposed to environmental stress (Yang et al., 2022). In that study, puppies had higher fecal Anaerobiospirillum, Erysipelatoclostridium, Escherichia-Shigella, Dermatophilaceae, Fournierella, Nesterenkonia, and Streptococcus, and lower Allobaculum following transportation. After removal of the environmental stressor, fecal Faecalibacterium, Fournierella, Prevotella, and Parasutterella increased (Yang et al., 2022). In the current study, alpha diversity measures were not affected by transport stress or SCFP supplementation, and weighted UniFrac distances of fecal microbial communities tended to cluster before and after transport stress. Moreover, transport stress led to a decrease in fecal Bifidobacterium and Streptococcus, while Clostridium, Faecalibacterium, Turicibacter, and Allobaculum increased only in animals supplemented with SCFP after transport stress. In contrast, Prevotella increased only in control animals following transport stress. Streptococcus is a pathogenic bacterium that can cause diarrhea and inflammatory cytokine secretion when overgrown (Walker et al., 2014). On the other hand, Allobaculum and Faecalibaculum have been positively associated with butyrate production (Yang et al., 2022), while Bifidobacterium, Prevotella, Faecalibacterium, Turicibacter, and Parasutterella are well-known SCFA-producing bacteria (AlShawaqfeh et al., 2017; Christensen et al., 2019; Deleu et al., 2021; Nakashima et al., 2021). The observed increases in Faecalibacterium, Turicibacter, and Allobaculum in animals supplemented with SCFP after experiencing transportation stress suggest a potential protective effect of SCFP supplementation.

The gut microbiota and its metabolites play and important role in maintaining host immune function and intestinal homeostasis (Takakuwa et al., 2019). In mice, stress was shown to reduce colonic SCFA concentrations and alter the prevalence of SCFA-producing bacteria (Maltz et al., 2019). Identifying ways to increase SCFA concentrations may help mitigate the effects of stress on the gut-brain axis (van de Wouw et al., 2018). In the canine study published by Yang et al. (2022), removal of environmental stress did not greatly impact SCFA, but increased fecal BCFA concentrations, with noticeable increases in isobutyrate and isovalerate. In the present study, transport stress did not impact fecal SCFA or BCFA concentrations, but led to increased fecal indole concentrations. Greater chronic indole production by the gut microbiota have been reported to make mice more vulnerable to negative effects of chronic mild stress on emotional behavior (Mir et al., 2020). The intestinal microbiota are known to primarily metabolize tryptophan into indole, which is then further metabolized into various oxidized and conjugated derivatives (Lee et al., 2015). Among these derivatives, oxindole and isatin have been identified as ­having neurodepressant effects. Both oxindole and isatin can decrease locomotor activity in rats. Oxindole has also been observed to induce hypotension and a loss of the righting reflex, while isatin has been found to promote anxiety and depression-like behaviors, including feelings of helplessness (Bhattacharya and Acharya, 1993; Carpenedo et al., 2002; Medvedev et al., 2005). Collectively, these findings suggest that transport stress can influence fecal indole concentrations, a compound associated with various stress-related side effects.

Given the results of recent studies in dogs, it was thought that SCFP supplementation may attenuate the side effects associated with transportation stress. Earlier research indicated that SCFP led to a reduction in fecal phenol, an increase in the proportion of Bifidobacterium, and a decrease in Fusobacterium (Lin et al., 2019). Additionally, long-term (11 wk) consumption of SCFP (0.13% of active ingredient in diet; average intake = 30 mg SCPF/kg BW) tended to minimize changes to fecal dry matter percentage during transport stress (Wilson et al., 2023). Those results suggested that SCFP may help minimize loose stools or diarrhea during transportation stress. In another recent study, we reported the effects of SCFP supplementation (250 mg/d) on the fecal characteristics, microbiota, and metabolite concentration of dogs subjected to exercise challenge in untrained and trained states (Oba et al., 2023). In that study, SCFP supplementation did not impact fecal scores, pH, dry matter percentage, or metabolite concentrations. The combination of SCFP supplementation and exercise challenge stress did not affect alpha or beta diversity measures in untrained dogs, but SCFP-fed dogs had a lower relative abundance of fecal Clostridium and higher relative abundances of fecal Turicibacter and Lactobacillus than control dogs over time. Similarly, data from the present study showed that while transport stress and SCFP supplementation did not affect fecal characteristics or microbiota diversity, dogs fed with SCFP tended to have greater relative abundances of Turicibacter, Butyricicoccus, and Lactobacillus than controls. Butyricicoccus and Turicibacter are recognized for their ability to produce SCFA, while numerous Lactobacillus strains are used as probiotics because of their lactate production and benefits to colon health (AlShawaqfeh et al., 2017; Christensen et al., 2019; Moens et al., 2019; Deleu et al., 2021; Nakashima et al., 2021). Lactate in the gastrointestinal tract acts as a growth stimulant for lactate-consuming bacteria, resulting in an increase in SCFA production, particularly butyrate (Moens et al., 2019).

In conclusion, our findings indicate that transport stress and SCFP supplementation have mild impacts on the fecal microbiota populations and activity in dogs. The major factor shifting the fecal microbiota was transport stress. However, transport stress did not result in dysbiosis. Although dramatic SCFP-induced changes were not observed, increases in fecal Faecalibacterium, Allobaculum, Lactobacillus, and Turicibacter suggest that it may provide benefits to dogs undergoing transport stress. Further studies using higher SCFP doses, which may result in greater changes, should be explored in future studies. Additionally, more research is necessary to determine the effects of different transport types on gastrointestinal microbiota and other health indicators.

Supplementary Material

skad191_suppl_Supplementary_Table_S1
Click here for additional data file. (19.9KB, docx)

Acknowledgment

The funding for this study was provided by Diamond V. Mills Inc.

Glossary

Abbreviations:

BCFA

branched-chain fatty acids

BCS

body condition score

BW

body weight

DI

dysbiosis index

OTU

operational taxonomic unit

PCoA

principal coordinates analysis

qPCR

quantitative polymerase chain reaction

SCFA

short-chain fatty acids

SCFP

Saccharomyces cerevisiae fermentation product

Contributor Information

Patrícia M Oba, Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.

Meredith Q Carroll, Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.

Kelly M Sieja, Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.

Xiaojing Yang, Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.

Tammi Y Epp, Cargill Incorporated, Wayzata, MN 55391, USA.

Christine M Warzecha, Cargill Incorporated, Wayzata, MN 55391, USA.

Jessica L Varney, Four Rivers Kennel, LLC, Walker, MO 64790, USA.

Jason W Fowler, Four Rivers Kennel, LLC, Walker, MO 64790, USA.

Craig N Coon, Four Rivers Kennel, LLC, Walker, MO 64790, USA.

Kelly S Swanson, Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA; Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA; Division of Nutritional Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.

Conflict of Interest

T.Y.E. and C.M.W. were employed by Cargill Inc. at the time the study was conducted. All other authors have no conflicts of interest.

Literature Cited

  1. AlShawaqfeh, M. K., Wajid B., Minamoto Y., Markel M., Lidbury J. A., Steiner J. M., Serpedin E., and Suchodolski J. S.. . 2017. A dysbiosis index to assess microbial changes in fecal samples of dogs with chronic inflammatory enteropathy. FEMS Microbiol. Ecol. 93:1–8. doi: 10.1093/femsec/fix136 [DOI] [PubMed] [Google Scholar]
  2. Beerda, B., Schilder M. B. H., van Hooff J. A. R. A. M., and de Vries H. W.. . 1997. Manifestations of chronic and acute stress in dogs. Appl. Anim. Behav. Sci. 52:307–319. doi: 10.1016/S0168-1591(96)01131-8 [DOI] [Google Scholar]
  3. Bharwani, A., Mian M. F., Foster J. A., Surette M. G., Bienenstock J., and Forsythe P.. . 2016. Structural & functional consequences of chronic psychosocial stress on the microbiome & host. Psychoneuroendocrinol 63:217–227. doi: 10.1016/j.psyneuen.2015.10.001 [DOI] [PubMed] [Google Scholar]
  4. Bhattacharya, S. K., and Acharya S. B.. . 1993. Further investigations on the anxiogenic action of isatin. Biog. Amin. 9:453–463. [Google Scholar]
  5. Bokulich, N. A., Kaehler B. D., Rideout J. R., Dillon M., Bolyen E., Knight R., Huttley G. A., and Caporaso J. G.. . 2018. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6:90. doi: 10.1186/s40168-018-0470-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cannas, S., Evangelista M., Accorsi P. A., and Michelazzi M.. . 2010. An epidemiology study on travel anxiety and motion sickness. J. Vet. Behav. 5:25–26. doi: 10.1016/j.jveb.2009.10.037 [DOI] [Google Scholar]
  7. Caporaso, J. G., Lauber C. L., Costello E. K., Berg-Lyons D., Gonzalez A., Stombaugh J., Knights D., Gajer P., Ravel J., Fierer N., . et al. 2011. Moving pictures of the human microbiome. Genome Biol. 12:R50. doi: 10.1186/gb-2011-12-5-r50 [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Caporaso, J. G., Lauber C. L., Walters W. A., Berg-Lyons D., J. Huntley, N. Fierer, S. M. Owens, J. Betley, L. Fraser, M. Bauer, et al. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6:1621–1624. doi: 10.1038/ismej.2012.8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Carpenedo, R., Mannaioni G., and Moroni F.. . 2002. Oxindole, a sedative tryptophan metabolite, accumulates in blood and brain of rats with acute hepatic failure. J. Neurochem. 70:1998–2003. doi: 10.1046/j.1471-4159.1998.70051998.x [DOI] [PubMed] [Google Scholar]
  10. Chaney, A. L., and Marbach E. P.. 1962. Modified reagents for determination of urea and ammonia. Clin. Chem. 8:130–132. doi: 10.1093/clinchem/8.2.130 [DOI] [PubMed] [Google Scholar]
  11. Chassaing, B., Koren O., Goodrich J. K., Poole A. C., Srinivasan S., Ley R. E., and Gewirtz A. T.. . 2015. Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 519:92–96. doi: 10.1038/nature14232 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Christensen, L., Vuholm S., Roager H. M., Nielsen D. S., Krych L., Kristensen M., Astrup A., and Hjorth M. F.. . 2019. Prevotella abundance predicts weight loss success in healthy, overweight adults consuming a whole-grain diet ad libitum: a post hoc analysis of a 6-wk randomized controlled trial. J. Nutr. 149:2174–2181. doi: 10.1093/jn/nxz198 [DOI] [PubMed] [Google Scholar]
  13. Cryan, J. F., and Dinan T. G.. . 2012. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13:701–712. doi: 10.1038/nrn3346 [DOI] [PubMed] [Google Scholar]
  14. Deleu, S., Machiels K., Raes J., Verbeke K., and Vermeire S.. . 2021. Short chain fatty acids and its producing organisms: an overlooked therapy for IBD? EBioMedicine 66:103293. doi: 10.1016/j.ebiom.2021.103293 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Erwin, E. S. S., Marco G. J. J., and Emery E. M. M.. 1961. Volatile fatty acid analyses of blood and rumen fluid by gas chromatography. J. Dairy Sci. 44:1768–1771. doi: 10.3168/jds.S0022-0302(61)89956-6 [DOI] [Google Scholar]
  16. Farca, A. M., Cavana P., Badino P., Barbero R., Odore R., and Pollicino P.. . 2006. Measurement of faecal corticoid metabolites in domestic dogs. Schweiz. Arch. Tierheilkd 148:649–655. doi: 10.1024/0036-7281.148.12.649 [DOI] [PubMed] [Google Scholar]
  17. Flickinger, E. A., Schreijen E. M. W. C., Patil A. R., H. S. Hussein, C. M. Grieshop, Merchen N. R., and Fahey G. C.. 2003. Nutrient digestibilities, microbial populations, and protein catabolites as affected by fructan supplementation of dog diets. J. Anim. Sci. 81:2008– 2018. doi: 10.2527/2003.8182008x [DOI] [PubMed] [Google Scholar]
  18. Gandia Estellés, M., and Mills D. S.. . 2006. Signs of travel-related problems in dogs and their response to treatment with dog appeasing pheromone. Vet. Rec. 159:143–148. doi: 10.1136/vr.159.5.143 [DOI] [PubMed] [Google Scholar]
  19. Grieshop, C. M., Flickinger E. A., Bruce K. J., Patil A. R., Czarnecki-Maulden G. L., and Fahey G. C.. . 2004. Gastrointestinal and immunological responses of senior dogs to chicory and mannan-oligosaccharides. Arch. Anim. Nutr. 58:483–493. doi: 10.1080/00039420400019977 [DOI] [PubMed] [Google Scholar]
  20. Han, F., Fan H., Yao M., Yang S., and Han J.. . 2017. Oral administration of yeast β-glucan ameliorates inflammation and intestinal barrier in dextran sodium sulfate-induced acute colitis. J. Funct. Foods 35:115–126. doi: 10.1016/j.jff.2017.05.036 [DOI] [Google Scholar]
  21. Jang, H. -M., Lee K. -E., Lee H. -J., and Kim D. -H.. . 2018. Immobilization stress-induced Escherichia coli causes anxiety by inducing NF-κB activation through gut microbiota disturbance. Sci. Rep. 8:13897. doi: 10.1038/s41598-018-31764-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kim, J. -K., Lee K. -E., Lee S. -A., Jang H. -M., and Kim D. -H.. . 2020. Interplay between human gut bacteria Escherichia coli and Lactobacillus mucosae in the occurrence of neuropsychiatric disorders in mice. Front. Immunol. 11:273. doi: 10.3389/fimmu.2020.00273 [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kuti, D., Winkler Z., Horváth K., Juhász B., Paholcsek M., Stágel A., Gulyás G., Czeglédi L., Ferenczi S., and Kovács K. J.. . 2020. Gastrointestinal (non-systemic) antibiotic rifaximin differentially affects chronic stress-induced changes in colon microbiome and gut permeability without effect on behavior. Brain Behav. Immun. 84:218–228. doi: 10.1016/j.bbi.2019.12.004 [DOI] [PubMed] [Google Scholar]
  24. Lee, J. -H., Wood T. K., and Lee J.. . 2015. Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol. 23:707–718. doi: 10.1016/j.tim.2015.08.001 [DOI] [PubMed] [Google Scholar]
  25. Lin, C. -Y., Alexander C., Steelman A. J., Warzecha C. M., de Godoy M. R. C., and Swanson K. S.. . 2019. Effects of a Saccharomyces cerevisiae fermentation product on fecal characteristics, nutrient digestibility, fecal fermentative end-products, fecal microbial populations, immune function, and diet palatability in adult dogs1. J. Anim. Sci. 97:1586–1599. doi: 10.1093/jas/skz064 [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Louis, P., and Flint H. J.. . 2017. Formation of propionate and butyrate by the human colonic microbiota. Environ. Microbiol. 19:29–41. doi: 10.1111/1462-2920.13589 [DOI] [PubMed] [Google Scholar]
  27. Maltz, R. M., Keirsey J., Kim S. C., Mackos A. R., Gharaibeh R. Z., Moore C. C., Xu J., Somogyi A., and Bailey M. T.. . 2019. Social stress affects colonic inflammation, the gut microbiome, and short-chain fatty acid levels and receptors. J. Pediatr. Gastroenterol. Nutr. 68:533–540. doi: 10.1097/MPG.0000000000002226 [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. McEwen, B. S. 1998. Protective and damaging effects of stress mediators. N. Engl. J. Med. 338:171–179. doi: 10.1056/nejm199801153380307 [DOI] [PubMed] [Google Scholar]
  29. Medvedev, A., Igosheva N., Crumeyrolle-Arias M., and Glover V.. . 2005. Isatin: role in stress and anxiety. Stress 8:175–183. doi: 10.1080/10253890500342321 [DOI] [PubMed] [Google Scholar]
  30. Mir, H. -D., Milman A., Monnoye M., Douard V., Philippe C., Aubert A., Castanon N., Vancassel S., Guérineau N. C., Naudon L., . et al. 2020. The gut microbiota metabolite indole increases emotional responses and adrenal medulla activity in chronically stressed male mice. Psychoneuroendocrinol 119:104750. doi: 10.1016/j.psyneuen.2020.104750 [DOI] [PubMed] [Google Scholar]
  31. Moens, F., Abbeele P. V., Basit A. W., Dodoo C., Chatterjee R., Smith B., and Gaisford S.. . 2019. A four-strain probiotic exerts positive immunomodulatory effects by enhancing colonic butyrate production in vitro. Int. J. Pharm. 555:1–10. doi: 10.1016/j.ijpharm.2018.11.020 [DOI] [PubMed] [Google Scholar]
  32. Nakashima, A., Sasaki K., Sasaki D., Yasuda K., Suzuki K., and Kondo A.. . 2021. The alga Euglena gracilis stimulates Faecalibacterium in the gut and contributes to increased defecation. Sci. Rep. 11:1074. doi: 10.1038/s41598-020-80306-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Oba, P. M., Carroll M. Q., Sieja K. M., de Souza Nogueira J. P., Yang X., Epp T. Y., Warzecha C. M., Varney J. L., Fowler J. W., Coon C. N., . et al. 2023. Effects of a Saccharomyces cerevisiae fermentation product on fecal characteristics, metabolite concentrations, and microbiota populations of dogs subjected to exercise challenge. J. Anim. Sci. 101:1–13. doi: 10.1093/jas/skac424 [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. de Oliveira Matheus, L. F., Risolia L. W., Ernandes M. C., de Souza J. M., Oba P. M., Vendramini T. H. A., Pedrinelli V., Henríquez L. B. F., de Oliveira Massoco C., Pontieri C. F. F., . et al. 2021. Effects of Saccharomyces cerevisiae cell wall addition on feed digestibility, fecal fermentation and microbiota and immunological parameters in adult cats. BMC Vet. Res. 17:351. doi: 10.1186/s12917-021-03049-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Panasevich, M. R., Kerr K. R., Dilger R. N., Fahey G. C., Guérin-Deremaux L., Lynch G. L., Wils D., Suchodolski J. S., Steer J. M., Dowd S. E., . et al. 2015. Modulation of the faecal microbiome of healthy adult dogs by inclusion of potato fibre in the diet. Br. J. Nutr. 113:125–133. doi: 10.1017/S0007114514003274 [DOI] [PubMed] [Google Scholar]
  36. Perry, E., Gulson N., Liu Cross T. -W., and Swanson K. S.. . 2017. Physiological effects of stress related to helicopter travel in Federal Emergency Management Agency search-and-rescue canines. J. Nutr. Sci. 6:e28. doi: 10.1017/jns.2017.25 [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Robeson, M. S.II, O’Rourke D. R., Kaehler B. D., Ziemski M., Dillon M. R., Foster J. T., and Bokulich N. A.. . 2021. RESCRIPt: Reproducible sequence taxonomy reference database management. PLoS Comput. Biol. 17:e1009581. doi: 10.1371/journal.pcbi.1009581 [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Scott, K. P., Gratz S. W., Sheridan P. O., Flint H. J., and Duncan S. H.. . 2013. The influence of diet on the gut microbiota. Pharmacol. Res. 69:52–60. doi: 10.1016/j.phrs.2012.10.020 [DOI] [PubMed] [Google Scholar]
  39. Selye, H. 1936. A syndrome produced by diverse nocuous agents. Nature 138:32–32. doi: 10.1038/138032a0 [DOI] [PubMed] [Google Scholar]
  40. Suchodolski, J. S., Markel M. E., Garcia-Mazcorro J. F., S. Unterer, Heilmann R. M., S. E. Dowd, P. Kachroo, I. Ivanov, Y. Minamoto, E. M. Dillman, et al. 2012. The fecal microbiome in dogs with acute diarrhea and idiopathic inflammatory bowel disease. PLoS One 7:e51907. doi: 10.1371/journal.pone.0051907 [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Swanson, K. S., Grieshop C. M., Flickinger E. A., Bauer L. L., Healy H. -P. P., Dawson K. A., Merchen N. R., and Fahey G. C.. . 2002. Supplemental fructooligosaccharides and mannanoligosaccharides influence immune function, ileal and total tract nutrient digestibilities, microbial populations and concentrations of protein catabolites in the large bowel of dogs. J. Nutr. 132:980–989. doi: 10.1093/jn/132.5.980 [DOI] [PubMed] [Google Scholar]
  42. Takakuwa, A., Nakamura K., Kikuchi M., Sugimoto R., Ohira S., Yokoi Y., and Ayabe T.. . 2019. Butyric acid and leucine induce α-defensin secretion from small intestinal paneth cells. Nutrients 11:2817. doi: 10.3390/nu11112817 [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Theodoro, S. S., Putarov T. C., Tiemi C., Volpe L. M., de Oliveira C. A. F., Glória M. B. A., and Carciofi A. C.. . 2019. Effects of the solubility of yeast cell wall preparations on their potential prebiotic properties in dogs. PLoS One 14:e0225659. doi: 10.1371/journal.pone.0225659 [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Varney, J. L., Coon C. N., and Norton S. A.. . 2021. PSV-B-20 effects of Saccharomyces cerevisiae fermentation product (SCFP) postbiotic in labrador retrievers during exercise and transport stress. J. Anim. Sci. 99:332–333. doi: 10.1093/jas/skab235.611 [DOI] [Google Scholar]
  45. Venable, E. B., Bland S. D., Holscher H. D., and Swanson K. S. . . 2016. Effects of air travel stress on the canine microbiome: a pilot study. Int. J. Vet. Health Sci. Res. 4:132–139. doi: 10.19070/2332-2748-1600028 [DOI] [Google Scholar]
  46. Walker, M. J., Barnett T. C., McArthur J. D., Cole J. N., Gillen C. M., Henningham A., Sriprakash K. S., Sanderson-Smith M. L., and Nizet V.. . 2014. Disease manifestations and pathogenic mechanisms of group A Streptococcus. Clin. Microbiol. Rev. 27:264–301. doi: 10.1128/CMR.00101-13 [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Wilson, S. M., Oba P. M., Koziol S. A., Applegate C. C., Soto-Diaz K., Steelman A. J., Panasevich M. R., Norton S. A., and Swanson K. S.. . 2022. Effects of a Saccharomyces cerevisiae fermentation product-supplemented diet on circulating immune cells and oxidative stress markers of dogs. J. Anim. Sci. 100:1–11. doi: 10.1093/jas/skac245 [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wilson, S. M., Oba P. M., Applegate C. C., Koziol S. A., Panasevich M. R., Norton S. A., and Swanson K. S.. . 2023. Effects of a Saccharomyces cerevisiae fermentation product-supplemented diet on fecal characteristics, oxidative stress, and blood gene expression of adult dogs undergoing transport stress. J. Anim. Sci. 101:1–9. doi: 10.1093/jas/skac378 [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. van de Wouw, M., Boehme M., Lyte J. M., Wiley N., Strain C., O’Sullivan O., Clarke G., Stanton C., Dinan T. G., and Cryan J. F.. . 2018. Short-chain fatty acids: microbial metabolites that alleviate stress-induced brain-gut axis alterations. J. Physiol. 596:4923–4944. doi: 10.1113/JP276431 [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Yang, K., Jian S., Wen C., Guo D., Liao P., Wen J., Kuang T., Han S., Liu Q., and Deng B.. . 2022. Gallnut tannic acid exerts anti-stress effects on stress-induced inflammatory response, dysbiotic gut microbiota, and alterations of serum metabolic profile in beagle dogs. Front. Nutr. 9:847966. doi: 10.3389/fnut.2022.847966 [DOI] [PMC free article] [PubMed] [Google Scholar]

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Supplementary Materials

skad191_suppl_Supplementary_Table_S1
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