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Meta-analysis of responses of broiler chickens to Bacillus supplementation: Intestinal histomorphometry and blood immunoglobulin

  • Ifeanyi Princewill Ogbuewu EMAIL logo and Christian Anayo Mbajiorgu
Published/Copyright: June 22, 2022
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Open Agriculture
From the journal Open Agriculture Volume 7 Issue 1

Abstract

The broiler chicken industry needs effective probiotics to boost productivity and health. However, published data on the impact of in-feed Bacillus supplementation on physiological parameters in healthy broiler chickens are often conflicting and inconclusive. As a result, this meta-analysis aimed to assess the influence of Bacillus on intestinal histomorphometry (villus height [VH], crypt depth [CD], and VH:CD) and blood immunoglobulin (A, G, and M) levels in healthy broiler chickens. Results were pooled using a random-effects model and presented as Hedges d (d) at 95% confidence intervals (CIs). The results indicate that Bacillus improves gut histomorphometric variables in broilers with the exception of duodenal and ileal CD, which had comparable values with the controls. Likewise, broiler chickens fed Bacillus had increased blood immunoglobulin (Ig) levels compared to controls (IgA: d = 2.29 mg/mL, 95% CI: 1.54–3.04; IgG: d = 2.17 mg/mL, 95% CI: 1.36–2.98; IgM: d = 1.00 mg/mL, 95% CI: 0.54–1.46) taking cognizance of heterogeneity (I 2 = 96–98%). Subgroup analysis showed that studied moderators (Bacillus species, broiler strain, and dosage and duration of supplementation) influenced the results of the meta-analysis. In conclusion, our results suggested that the inclusion of Bacillus at 0.1–6.0 × 106 colony-forming unit/g in broiler chicken feed enhanced the absorptive capacity of the small intestine and blood immunoglobulin levels of broiler chickens. The findings of this study avail important suggestions on policy advancements and sustainable usage of Bacillus in broiler chicken industry.

Keywords: probiotics; broiler chickens; intestinal histomorphometry; immunity; meta-analysis

1 Introduction

High productivity and efficient feed conversion is the bane of the modern broiler chicken industry, which to a reasonable extent can be accomplished by the use of probiotics. Probiotics are live microbial supplements that enhance intestinal microecosystem for the benefit of the host when taken in an adequate amount [1,2]. Probiotics have excellent features, such as being non-toxic, environmentally friendly, and leaving no residue in animal products, and may be a good alternative to in-feed antibiotics [3]. They also inhibit the activity of pathogens such as Clostridium spp., Salmonella spp., and Escherichia coli [4,5] that cause morbidity and mortality in farm animals. Probiotics also increase the population of beneficial microbes like yeast which enhance digestion and absorptive capacity of the small intestine [6], leading to improve growth performance in farm animals [6,7,8].

Bacillus is a thermophilic spore-forming gram-positive aerobic bacteria that produce digestive enzymes and vitamins, which may improve feed conversion and weight gain in poultry. Its spore is resistant to heat during pelleting conditions and tolerant to bile salts, gastric acids, and intestinal juice [9]. It also maintains gut function by lowering intestinal oxygen concentrations, thus facilitating the growth and maintenance of useful anaerobic bacteria including yeast and Bifidobacterium [10]. Guo et al. [11] have shown that Bacillus increases the population of beneficial intestinal microbes and the diversity of microbial ecology of the caeca in layers. In addition, Bacillus produces antimicrobial factors (surfactins, amicoumacins, and bacillomycin D) that limit the growth of destructive microbes in the intestine [9]. Different researchers have investigated the effect of Bacillus on intestinal histomorphometry and immune system of broiler chicken [10,12,13,14], but there are still several research gaps regarding the impact of Bacillus on broiler chicken performance because published data are often contradictory. The use of meta-analysis to pool studies with conflicting results to reach new conclusions has been demonstrated [8].

Meta-analysis is a statistical tool that combines the results of individual published studies addressing the same research objectives, by increasing sample size and revealing variations that individual study could not detect. The objective of this meta-analysis was to evaluate the effect of dietary Bacillus on physiological parameters such as intestinal histomorphometry and blood immunoglobulin concentrations in healthy broiler chickens.

2 Materials and methods

2.1 Article selection

Peer-reviewed studies on the impact of diets with and without Bacillus on intestinal histomorphometry and blood immunoglobulin concentrations in broiler chickens were retrieved from a methodical search conducted in PubMed, Google Scholar, and Scopus databases. This study adopted the Preferred Reporting Items for Systematic Review and Meta-analyses guidelines [15]. The search was performed using the following keywords: Bacillus*, broiler chickens*, intestinal histomorphometry*, gut histomorphometry*, “blood immunoglobulin,” IgA*, IgM*, and IgG*. The search was not restricted by language and publication dates. Additional studies were identified by screening the reference list of retrieved studies. Articles included in the analysis fulfilled the following criteria: (1) used clinically healthy broiler chickens, (2) fed Bacillus-based diets, (3) had control group without Bacillus, and (4) reported at least one of the variables of interest (intestinal histomorphometry or blood immunoglobulin) and their associated measures of variance. Two hundred published articles were identified, of which 15 fulfilled the selection criteria (Figure 1).

Figure 1 Flow diagram of the paper selection process used for the analysis.
Figure 1

Flow diagram of the paper selection process used for the analysis.

  1. Ethical approval: The conducted research is not related to either human or animal use.

2.2 Data extraction and management

Authors’ name, publication year, study country, moderators (Bacillus species, broiler strains, duration and dosage), mean values of the variables of interest (gut histomorphometry and blood immunoglobulin), standard deviation, and number of broilers included in control (without Bacillus) and treatment (with Bacillus) groups for each included study were extracted. We used standard deviation (SD) as a measure of variance, and studies that reported standard error rather than SD were converted to SD using a standard formula [16]. When multiple Bacillus spp. or different dose levels of the same Bacillus were used in the trial, results were compared using a standard method [17]. Stratification analysis was disaggregated based on the following moderators that may have an impact on the magnitude of the treatment: (1) Bacillus spp. (B. subtilis, B. coagulans, and B. amyloliquefaciens), (2) the dose level of Bacillus spp. (0.1–0.5, 0.6–1.0, and 1.1–6.0 × 106  colony-forming unit [cfu]/g), (3) duration of supplementation (1–21, 1–35, and 1–42 days), and (4) broiler chicken strain (Arian, Hubbard, Ross, Cobb, and Arbor acres).

2.3 Data analysis

Statistical analyses were performed in Open Meta-analyst for Ecology and Evolution software [18], whereas a study location map was done in Tableau. Effect size (ES) was quantified using standardized mean difference also referred to as d. The overall ES was aggregated using a random-effects model at 95% CIs. The pooled ES is said to be significant when the CI did not include zero [19]. ES is categorized into low (0.2), moderate (0.5), and substantial (0.8). Heterogeneity was assessed with I 2 statistics [20]. Analysis of subgroup was used to explore the sources of heterogeneity and was performed only when there are ≥3 datasets.

3 Results

3.1 Study characteristics

The details of the 15 studies used for the analysis are presented in Table 1. Two hundred published articles were obtained and 15 met the inclusion criteria as shown in Figure 1. These articles were published between 2012 and 2020. Out of the 15 studies, 6 were published before 2015 and the remaining were published after 2015. The studies included in the meta-analysis cut across nine study locations (Figure 2) with most of the research performed in China (n = 5) and Korea (n = 3). Arbor acres strain was the most frequent strain followed by Ross and Cobb. Most of the papers included in the study used B. subtilis, while B. amyloliquefaciens and B. coagulans were the least used species of Bacillus. Dosage and duration of supplementation were ranged between 0.1–6.0 × 106 cfu/g and 1–42 days, respectively.

Table 1

Features of the articles included in the meta-analysis

Authors Location Explanatory moderator variables Outcomes
Bacillus species Dose (×106 cfu/g) DOS (d) Broiler strain
[10] China B. subtilis 0, 1 1–42 Ross Duodenum VH, CH, VH:CD; Jejunum VH, CD, VH:CD; Ileum VH, CH, VH:CD, IgA, IgG, IgM
[21] Germany B. subtilis 0, 0.8 1–42 Cobb Duodenum VH, CH, VH:CD; Jejunum VH, CD, VH:CD; Ileum VH, CH, VH:CD
[22] Korea B. amyloliquefaciens 0, 0.1, 0.5,1.0, 2.0 1–35 Ross IgA, IgG, IgM
[14] China B. coagulans/subtilis 0, 1 1–42 Arbor acres Duodenum VH, CH, VH:CD; Jejunum VH, CD, VH:CD; Ileum VH, CH, VH:CD
[23] Poland B. subtilis 0, 2.5 1–42 Ross Jejunum VH, CD
[24] USA B. subtilis 0, 3 1–28 Cobb Duodenum VH, CH, VH:CD; Ileum VH, CH, VH:CD
[25] Jordan B. subtilis 0, 1 1–35 Hubbard Duodenum CH; Ileum VH, CH
[26] China B. subtilis 0, 0.2, 0.3, 0.4, 0.5 1–42 Arbor acres IgA, IgG, IgM
[27] Korea B. subtilis 0, 0.1 1–35 Arbor acres IgG
[28] Iran B. subtilis 0, 0.5 1–42 Arian Jejunum VH, CD, VH:CD
[29] Australia B. coagulans 0, 0.1, 0.2, 0.25 1–42 Arbor acres Duodenum VH, CH, VH:CD; Jejunum VH, CD; VH:CD
[30] Korea B. subtilis 0, 0.15, 0.3, 0.45 1–35 Ross Duodenum VH, CH, VH:CD, Ileum VH, CH, VH:CD
[13] China B. subtilis 0, 0.2, 0.3, 0.4, 0.5 1–21 Arbor acres Jejunum VH, CD, VH:CD; Ileum VH, CH, VH:CD
[31] India B. subtilis 0, 0.4 1–35 Cobb Duodenum VH, CH, VH:CD, Jejunum VH, CD, VH:CD
[12] China B. amyloliquefaciens 0, 3, 6 1–21/1–42 Arbor acres Duodenum VH, CH, VH:CD; Jejunum VH, CD, VH:CD; Ileum VH, CH, VH:CD IgA, IgG, IgM

cfu – colony-forming unit; d – day, g – grams; DOS – duration of supplementation.

Figure 2 Locations and the frequency of the 15 studies included in the meta-analysis.
Figure 2

Locations and the frequency of the 15 studies included in the meta-analysis.

3.2 Intestinal histomorphometry

The number of articles, datasets, and broiler chickens included in the meta-analysis is presented in Table 2. Pooled results as shown in Table 3 indicated that Bacillus supplementation had a positive and significant effect on aspects of the intestinal villus histomorphometry (villus height [VH] and VH:CD) in the duodenum and ileum region of the small intestine of broiler chickens compared to controls. In contrast, there are no significant differences in the duodenal and ileal crypt depth [CD] between broiler chickens fed Bacillus and control diets. Bacillus supplementation improved histomorphometry of the jejunum region compared to the controls.

Table 2

Datasets and number of broiler chickens included in the meta-analysis

Outcome measures n t Datasets n a n b Total
Duodenum VH 9 18 967 1,823 2,790
CD 9 18 967 1,823 2,790
VH:CD 8 17 867 1,723 2,590
Jejunum VH 9 19 953 1,829 2,782
CD 9 19 953 1,829 2,782
VH:CD 8 18 813 1,689 2,502
Ileum VH 7 18 847 1,643 2,490
CD 8 18 847 1,643 2,490
VH:CD 7 17 747 1,543 2,290
Immunoglobulin IgA 4 13 470 1,010 1,480
IgG 5 14 590 1,130 1,720
IgM 4 13 470 1,010 1,480

VH – villi height; CD – crypt depth; IgA – immunoglobulin A; IgG – immunoglobulin G; IgM – immunoglobulin M; n t – number of trials used for the analysis; n a – number of broilers included in the control group; n b – number of broilers included in the treatment group.

Table 3

Histomorphometric changes in the intestine of broiler chickens fed Bacillus-supplemented diets

Response variables Duodenum Jejunum Ileum
d 95% CI d 95% CI d 95% CI
VH (μm) 0.94 0.48–1.40 1.85 1.37–2.34 0.96 0.44–1.49
CD (μm) –0.38 –0.83–0.06 0.76 0.12–1.34 0.20 –0.40–0.80
VH:CD 0.99 0.42–1.57 1.33 0.80–1.86 1.28 0.78–1.77

d – Hedge’s d; CI – confidence interval; VH – villi height; CD – crypt depth.

3.3 Blood immunoglobulin

The meta-analysis suggested that birds fed dietary Bacillus had significantly increased blood IgA in comparison with controls (d = 2.29 mg/mL; 95% CI: 1.54–3.04; Figure 3a). In addition, broiler chickens fed Bacillus-supplemented diets had significantly increased blood IgG level compared to control d of 2.17 mg/mL (95% CI: 1.36–2.98; Figure 3b) and heterogeneity (I 2) of 98% between studies (Figure 3b). Broiler chickens on Bacillus intervention recorded higher blood IgM concentration in comparison with controls d of 1.00 mg/mL (95% CI: 0.54–1.46; Figure 3c).

Figure 3 Forest plots of the effect of diets with or without Bacillus supplement on blood (a) IgA; (b) IgG and (c) IgM in broiler chickens. The x-axis shows the difference between diets with or without Bacillus supplements. The points to the left of the line represent a reduction in the trait, while the points to the right of the line indicate an increase. Each square represents the size of the mean effect of that study, and the size of the square reflects the relative weight of the study of the overall estimate of effect size with the larger squares representing a larger weight. The upper and lower bound of the squared line represents the upper and lower confidence intervals (CIs) of 95% for the size of the effect. The diamond at the bottom represents the 95% CI for the global estimate, and the vertical line of points represents the mean difference of zero or no effect.
Figure 3

Forest plots of the effect of diets with or without Bacillus supplement on blood (a) IgA; (b) IgG and (c) IgM in broiler chickens. The x-axis shows the difference between diets with or without Bacillus supplements. The points to the left of the line represent a reduction in the trait, while the points to the right of the line indicate an increase. Each square represents the size of the mean effect of that study, and the size of the square reflects the relative weight of the study of the overall estimate of effect size with the larger squares representing a larger weight. The upper and lower bound of the squared line represents the upper and lower confidence intervals (CIs) of 95% for the size of the effect. The diamond at the bottom represents the 95% CI for the global estimate, and the vertical line of points represents the mean difference of zero or no effect.

3.4 Subgroup analysis

Table 4 shows the results of the subgroup analysis of the effect of studied moderators on VH, CH, and VH:CH in the duodenal region of broiler chickens. Results of sub-analysis revealed that Cobb and Arbor acres broilers on Bacillus supplementation had significantly higher duodenal VH compared to controls. There were no differences in duodenal VH between Ross broilers fed diet with and without Bacillus supplementation. Broiler chickens on B. subtilis and B. amyloliquefaciens supplementation had significantly higher duodenal VH than controls. In contrast, there was no significant difference in duodenal VH of broiler chickens fed B. coagulans and control diets. Broiler chickens that received Bacillus at 0.1–0.5, 0.6–1.0, and 1.1–6.0 × 106 cfu/g for 1–35 and 1–42 days had significantly higher duodenal VH than broiler chickens fed control diets. Table 5 presents the results of the subgroup analysis of the effect of moderators on VH, CD, and VH:CD in the jejunum region of broiler chickens. Bacillus spp. (B. subtilis, B. amyloliquefaciens, and B. coagulans) inclusion at 0.1–0.5 and 1.1–6.0 × 106 cfu/g for 1–21 and 1–42 days improved the VH of the jejunum relative to the controls. Furthermore, the incorporation of B. subtilis and B. amyloliquefaciens in broiler diets at 0.10.5 × 106 cfu/g for 1–21 days increased jejunal CD when compared to the controls. Broiler chickens offered B. coagulans had significantly lower jejunal CD than controls. In comparison with the controls, birds that received Bacillus spp. (B. subtilis, B. amyloliquefaciens, and B. coagulans) at 0.1–0.5 × 106 cfu/g for 1–42 days had significantly higher jejunal VH:CD. There were no significant changes in VH:CD between broilers fed Bacillus at 1.1–6.0 × 106 cfu/g for 1–21 days and the control broilers.

Table 4

Impact of moderators on duodenal histomorphometry of broilers fed Bacillus-supplemented diets

Moderators Model results Heterogeneity
d (95% CI) SE P-value I 2 (%) P-value
Duodenum VH
Broiler strain
Cobb 1.78 (0.04–3.52) 0.89 0.045 99 <0.001
Ross 0.52 (–0.17–1.21) 0.35 0.141 95 <0.001
Arbor acres 0.80 (0.22–1.38) 0.30 0.007 97 <0.001
Bacillus spp.
 B. subtilis 0.82 (0.14–1.50) 0.35 0.018 98 <0.001
 B. amyloliquefaciens 1.86 (0.89–2.84) 0.50 <0.01 96 <0.001
 B. coagulans 0.34 (–0.13–0.81) 0.24 0.153 92 <0.001
Dosage (×106 cfu/g)
0.1–0.5 0.52 (–0.03–1.07) 0.28 0.063 97 <0.001
0.6–1.0 0.18 (0.01–0.36) 0.09 0.044 0 0.985
1.1–6.0 1.86 (0.89–2.84) 0.50 <0.001 96 <0.001
DOS (days)
1–35 0.82 (0.10–1.55) 0.37 0.027 96 <0.001
1–42 0.46 (0.04–0.89) 0.22 0.032 96 <0.001
Duodenum CD
Broiler strain
Cobb –0.74 (–2.36–0.89) 0.83 0.374 99 <0.001
Ross –0.40 (–0.93–0.13) 0.27 0.141 92 <0.001
Arbor acres –0.27 (–0.92–0.38) 0.33 0.416 98 <0.001
Bacillus spp.
 B. subtilis –0.66 (–1.17–0.15) 0.26 0.011 97 <0.001
 B. amyloliquefaciens 0.70 (–0.24–1.64) 0.48 0.142 97 <0.001
 B. coagulans –0.76 (–1.65–0.14) 0.46 0.096 98 <0.001
Dosage (×106 cfu/g)
0.1–0.5 –0.59 (–1.20–0.03) 0.31 0.061 97 <0.001
0.6–1.0 –0.15 (–0.32–0.03) 0.09 0.112 0 0.932
1.1–6.0 0.70 (–0.24–1.64) 0.48 0.142 97 <0.001
VH/CD ratio
Broiler strain
Cobb 2.40 (0.49–4.31) 0.98 0.014 99 <0.001
Ross 0.88 (–0.22–1.98) 0.56 0.117 98 <0.001
Arbor acres 0.62 (0.01–1.23) 0.31 0.046 98 <0.001
Bacillus spp.
 B. subtilis 1.05 (0.02–2.08) 0.53 0.047 99 <0.001
 B. amyloliquefaciens 1.13 (0.95–1.30) 0.09 <0.001 0 0.511
 B. coagulans 0.73 (–0.21–1.67) 0.48 0.126 98 <0.001
Dosage (×106 cfu/g)
0.1–0.5 0.34 (–0.42–1.09) 0.39 0.381 98 <0.001
0.6–1.0 0.31 (0.13–0.49) 0.09 <0.001 0 0.917
1.1–6.0 1.13 (0.95–1.30) 0.09 <0.001 0 0.511
DOS (days)
1–35 0.38 (0.21–0.56) 0.09 <0.001 12 0.331
1–42 0.88 (0.12–1.65) 0.39 0.023 99 <0.001

cfu – colony-forming unit; DOS – duration of supplementation; d – Hedge’s d; CI – confidence interval; SE – standard error; I 2 – inconsistency index; VH – villi height; CD – crypt depth.

Table 5

Impact of moderators on jejunal histomorphometric traits in broiler fed Bacillus-supplemented diets

Moderators Model results Heterogeneity
d (95% CI) SE P-value I 2-test (%) P-value
VH
Bacillus spp.
 B. subtilis 2.22 (1.57–2.87) 0.33 <0.001 98 <0.001
 B. amyloliquefaciens 1.50 (0.53–2.47) 0.49 0.002 96 <0.001
 B. coagulans 1.22 (0.09–2.36) 0.58 0.035 92 <0.001
Dosage (×106 cfu/g)
0.1–0.5 2.09 (1.43–2.74) 0.33 <0.001 98 <0.001
1.1–6.0 1.50 (0.53–2.47) 0.49 0.002 96 <0.001
DOS (days)
1–21 2.65 (2.16–3.14) 0.25 <0.001 84 <0.001
1–42 1.33 (0.79–1.87) 0.28 <0.001 98 <0.001
CD
Bacillus spp.
 B. subtilis 1.52 (0.52–2.51) 0.51 0.003 97 <0.001
 B. amyloliquefaciens 0.43 (–0.17–1.03) 0.31 <0.001 97 <0.001
 B. coagulans –0.95 (–1.25–0.66) 0.15 <0.001 98 <0.001
Dosage (×106 cfu/g)
0.1–0.5 1.01 (0.06–1.94) 0.48 0.037 99 <0.001
1.1–6.0 0.43 (–0.17–1.03) 0.31 0.162 92 <0.001
DOS (days)
1–21 2.48 (1.42–3.54) 0.54 <0.001 97 <0.001
1–42 –0.09 (–0.76–0.58) 0.34 0.785 99 <0.001
VH/CD ratio
Bacillus spp.
 B. subtilis 1.05 (0.25–1.85) 0.41 0.011 98 <0.001
 B. amyloliquefaciens 1.13 (0.63–1.63) 0.26 <0.001 87 <0.001
 B. coagulans 2.21 (1.32–3.10) 0.45 <0.001 97 <0.001
Dosage (×106 cfu/g)
0.1–0.5 1.39 (0.59–2.19) 0.41 0.037 99 <0.001
1.1–6.0 1.13 (0.63–1.63) 0.26 0.162 87 <0.001
DOS (days)
1–21 0.30 (–0.44–1.04) 0.38 0.426 96 <0.001
1–42 1.78 (1.17–2.39) 0.31 <0.001 98 <0.001

cfu – colony-forming unit; DOS – duration of supplementation; d – Hedge’s d; CI – confidence interval; SE – standard error; I 2 – inconsistency index; VH – villi height; CD – crypt depth.

The subgroup analyses of the impact of moderators on intestinal villus histomorphometry of the duodenum of broiler chickens are described in Table 6. Arbor acres and Ross stains from studies that fed B. subtilis and B. amyloliquefaciens at 0.1–0.5, 0.6–1.0, and 1.1–6.0 × 106 cfu/g for 1–21 days had significantly longer ileum VH than controls. However, birds fed Bacillus for 1–35 and 1–42 days had similar ileum VH with the controls. Arbor acres offered Bacillus-based diets had significantly increased ileum CD compared to the Ross. Bacillus supplementation at 0.6–1.0 × 106 cfu/g improved the ileum CD in Arbor acres aged 1–21 days when compared to controls. Similarly, broiler chickens fed diets supplemented with B. subtilis and B. amyloliquefaciens at 0.1–0.5, 0.6–1.0, and 1.1–6.0 × 106 cfu/g for 1–21, 1–35, and 1–42 days had significantly better ileum VH:CD than controls. In contrast, Ross from studies that received B. subtilis and B. amyloliquefaciens at 0.1–0.5 and 1.1–6.0 × cfu/g for 1–35 and 1–42 days had similar ileum CD with the controls.

Table 6

Effect of modifiers on ileal histomorphometric variable in broilers fed Bacillus-supplemented diets

Moderators Model results Heterogeneity
d (95% CI) Standard error P-value I 2 (%) P-value
VH
Broiler strain
Ross 0.43 (0.22–0.63) 0.11 <0.001 50 0.114
Arbor acres 8.60 (7.11–10.09) 0.76 <0.001 99 <0.001
Bacillus spp.
 B. subtilis 5.50 (4.43–6.56) 0.54 <0.001 99 <0.001
 B. amyloliquefaciens 2.063 (1.43–2.70) 0.32 <0.001 90 <0.001
Dosage (×106 cfu/g)
0.1–0.5 12.60 (10.54–14.66) 1.05 <0.001 99 <0.001
0.6–1.0 0.32 (0.13–0.50) 0.09 <0.001 0 <0.001
1.1–6.0 2.06 (1.43–2.70) 0.32 <0.001 90 <0.001
DOS (days)
1–21 21.08 (16.02–26.15) 2.58 <0.001 99 <0.001
1–35 0.80 (–0.10–1.70) 0.46 0.080 97 <0.001
1–42 0.50 (–0.12–1.12) 0.32 0.117 97 <0.001
CD
Broiler strain
Ross –0.50 (–1.07–0.07) 0.290 0.083 93 <0.001
Arbor acres 0.92 (0.14–1.70) 0.397 0.020 98 <0.001
Bacillus spp.
 B. subtilis 0.23 (–0.50–0.96) 0.37 0.540 99 <0.001
 B. amyloliquefaciens 0.58 (–0.31–1.46) 0.45 0.200 96 <0.001
Dosage (×106 cfu/g)
0.1–0.5 0.83 (–0.27–1.93) 0.56 0.139 99 <0.001
0.6–1.0 –0.24 (–0.44–0.03) 0.11 0.023 24 0.270
1.1–6.0 0.58 (–0.31–1.46) 0.45 0.200 96 <0.001
DOS (days)
1–21 1.93 (1.44–2.42) 0.25 <0.001 88 <0.001
1–35 –0.48 (–0.98–0.02) 0.26 0.060 90 <0.001
1–42 –0.59 (–1.28–0.10) 0.35 0.096 98 <0.001
VH/CD
Broiler strain
Ross 0.68 (0.29–1.071) 0.20 <0.001 85 <0.001
Arbor acres 1.32 (0.71–1.93) 0.31 <0.001 97 <0.001
Bacillus spp.
 B. subtilis 1.13 (0.52–1.74) 0.31 <0.001 98 <0.001
 B. amyloliquefaciens 1.33 (1.15–1.51) 0.09 <0.001 0 0.486
Dosage (×106 cfu/g)
0.1–0.5 1.13 (0.33–1.93) 0.41 0.006 98 <0.001
0.6–1.0 0.89 (0.36–1.42) 0.27 0.001 86 <0.001
1.1–6.0 1.40 (1.19–1.62) 0.11 <0.001 0 0.731
DOS (days)
1–21 1.51 (1.29–1.74) 0.12 <0.001 49 0.082
1–35 0.50 (0.29–0.71) 0.11 <0.001 27 0.253
1–42 1.02 (0.26–1.78) 0.39 0.009 98 <0.001

cfu – colony-forming unit; DOS – duration of supplementation; d – Hedge’s d; CI – confidence interval; SE – standard error; I 2 – inconsistency index; VH – villi height; CD – crypt depth.

4 Discussion

The current meta-analysis discusses the effect of dietary Bacillus supplementation on blood immunoglobulin and intestinal histomorphometry of broiler chickens. The integrity and proper function of the intestinal epithelium are entirely dependent on the rapid regeneration of epithelial cells, which leads to the proliferation and differentiation of the crypts. The crypt is where enterocytes proliferate and differentiate, allowing them to migrate and promote villus growth [32]. On the same hand, shallower CD boosts rapid epithelial turnover in response to inflammation from pathogenic bacteria [25]. Our results suggested that incorporation of Bacillus in broiler chicken feed elicited a positive impact on the histomorphological indices of the three anatomical segments (duodenum, jejunum, and ileum) of the small intestine in broiler chickens. This could be the plausible explanation for the improved growth performance in broilers fed Bacillus-based diets [13,22]. Our results are in agreement with Dong et al. [10], who found an improvement on duodenal and jejunal VH and VH:CD of Ross 308 broilers fed B. subtilis at 1.0 × 106 cfu/g for 5 weeks.

4.1 Blood immunoglobulin

Immunoglobulin, also known as antibodies, plays a vital role in immune response of chicken by binding to specific antigens such as bacteria or viruses assisting in their destruction. The IgA plays a key role in the immune function of mucous membrane, whereas IgM serves as the first line of defense against infection [33]. The IgY antibody is one of the most important antibodies produced by chicken, and it serves a similar function to mammalian IgGs [34]. In the current meta-analysis, the addition of Bacillus to broiler diets remarkably increased the content of IgA, IgM, and IgG in the sera, indicating that Bacillus treatment improves the immune resistance of broiler chickens. This observation is consistent with Zhang et al. [35], who demonstrated improved content of immunoglobulin in the sera of 6-week old broiler chickens fed 5 × 106 cfu/g B. coagulans. Similarly, Dong et al. [10] found 32 and 31% increases in IgG and IgM levels in the sera of broilers fed 1.0 × 106 cfu/g B. subtilis for 5 weeks relative to the control group. Studies in animals other than broiler chickens showed that probiotics improve blood IgG [36]. Similarly, combinations of different strains of Lactobacillus improved IgG and IgM levels in the sera of chickens [37].

4.2 Analysis of moderators

4.2.1 Broiler strains

Our analysis indicated that Cobb and Arbor acres on Bacillus intervention had significantly better duodenal VH and VH:CD in comparison with controls, which implies that Bacillus enhances the absorptive capacity of the duodenum [38]. The comparable duodenal VH and VH:CD values of Ross on Bacillus treatments and controls imply a similar nutrient absorption rate. However, our analysis demonstrated that broiler strain did not influence duodenal CD in broilers fed diets treated with Bacillus. Ross and Arbor acres from studies that offered dietary Bacillus had better ileal function than the controls. However, Arbor acres had a larger effect estimate than Ross, indicating a stronger relationship between Arbor acres and Bacillus. Improved intestinal histomorphometry due to Bacillus treatment could be the reason for the improved performance witnessed in broiler chickens fed Bacillus-supplemented diets [10,13,22].

4.2.2 Bacillus species

Our results revealed that broiler chickens on B. subtilis interventions had improved duodenal function than those that received control diets. The improvement on histomorphological variables of the duodenum in the present meta-analysis is in harmony with the results of Jayaraman et al. [31], who reported significantly increased villus histomorphometry of the duodenum and jejunum in VenCobb 400 broiler chicks fed 5 × 106 cfu/g B. subtilis PB6 for 35 days. This is also in agreement with Dong et al. [10], who found enhanced histomorphometry of the duodenum and jejunum in broiler chickens fed 1.0 × 106 cfu/g B. subtilis BYS2 for 42 days. Chickens on B. subtilis and B. amyloliquefaciens intervention had better ileal VH and VH:CD. Similarly, broilers from studies that fed B. amyloliquefaciens had better duodenal function than controls. In contrast, birds fed B. coagulans experienced similar VH, CD, and VH:CD with the controls, showing that B. coagulans did not affect the histomorphological indices of the duodenum. Bacillus spp. (B. coagulans, B. subtilis, and B. amyloliquefaciens) had a positive influence on histomorphological indices of the jejunum except for birds from studies that fed B. coagulans that did not experience improved jejunal CD. The significantly lower jejunal CD in broiler chickens fed B. coagulans as recorded in the current study agreed with Zhen et al. [39], who recorded lower CD in Salmonella enteritidis challenged Cobb broiler chicks fed 1.0 × 106 cfu/g B. coagulans for 42 days. It was also observed that Bacillus (B. subtilis and B. amyloliquefaciens) had no adverse influence on ileal CD.

4.2.3 Dosage

Interestingly, broilers fed Bacillus at 0.6–1.0 and 1.1–6.0 × 106 cfu/g experienced better duodenal VH and VH:CD than controls. However, there is no significant effect of dosage on duodenal CD. In the present meta-analysis, broiler chickens fed Bacillus at 0.1–0.5 and 1.1–6.0 × 106 cfu/g had enhanced jejunal VH, while those fed 0.1–0.5 × 106 cfu/g had significantly increased jejunal CD and VH:CD. Our result also revealed that supplementation with Bacillus at 0.1–0.5, 0.6–1.0, and 1.1–6.0 × 106 cfu/g improved ileal VH, CD, and VH:CD. There are negative associations between dosage (0.6–1.0 × 106 cfu/g) and ileal CD. In contrast, dosage at 0.1–0.5 and 1.1–6.0 × 106 cfu/g had no impact on ileal CD in broiler chickens.

4.2.4 Duration of supplementation

Intestinal histomorphology characteristics are vital indices of gut health and function in poultry. In the current meta-analysis, subgroup analysis restricted to duration of supplementation demonstrated that broiler chickens from studies that fed Bacillus for 1–35 and 1–42 days had better duodenal VH and VH:CD in comparison with controls. Likewise, broilers fed Bacillus for 1–21 and 1–42 days had significantly higher jejunal VH than controls. Also, broilers offered Bacillus for 1–21 and 1–42 days had improved jejunal variables (CD and VH:CD, respectively) than controls. Similarly, broilers from trials that received Bacillus for 1–21 and 1–35 days had better ileal VH:CD than those from studies that fed Bacillus for 1–42 days. In addition, broiler chickens from studies that received probiotic-Bacillus for 1–21 days and had improved ileal VH and CD than those from studies that fed Bacillus for 1–35 and 1–42 days. This indicates that feeding Bacillus for more than 1–21 days has no effect on ileal VH and CD in broiler chickens.

5 Conclusion

From the present meta-analysis, it is evident that probiotic-Bacillus intervention at 0.1–6.0 × 106 cfu/g positively impacted villi histomorphometry. However, the mechanisms of action of Bacillus on villi histomorphometry of broiler chickens need to be studied further. In addition, Bacillus supplementation at 0.1–6.0 × 106 cfu/g improves the blood immunoglobulin levels in broiler chickens. Considering the complexity of immunity, the specific mechanism by which Bacillus can enhance blood immunoglobulin concentrations in broilers needs to be explored further.

Acknowledgments

The authors thank the Agriculture for Food Security (AgriFoSe2030) for the training fellowship on Introduction to Meta-analysis provided to the first author.

  1. Funding information: The authors state no funding involved.

  2. Author contributions: The authors participated in study conception and design. Material preparation, data collection, and analysis were performed by all the authors. The first draft of the manuscript was written by IPO, and CAM reviewed the draft. All authors read and approved the final draft.

  3. Conflict of interest: The authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2022-03-03
Revised: 2022-04-01
Accepted: 2022-05-20
Published Online: 2022-06-22

© 2022 Ifeanyi Princewill Ogbuewu and Christian Anayo Mbajiorgu, published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/opag-2022-0110
Keywords for this article
probiotics; broiler chickens; intestinal histomorphometry; immunity; meta-analysis
Creative Commons
BY 4.0

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  25. The supply chain and its development concept of fresh mulberry fruit in Thailand: Observations in Nan Province, the largest production area
  26. Toward achieving sustainable development agenda: Nexus between agriculture, trade openness, and oil rents in Nigeria
  27. Phenotyping cowpea accessions at the seedling stage for drought tolerance in controlled environments
  28. Apparent nutrient utilization and metabolic growth rate of Nile tilapia, Oreochromis niloticus, cultured in recirculating aquaculture and biofloc systems
  29. Influence of season and rangeland-type on serum biochemistry of indigenous Zulu sheep
  30. Meta-analysis of responses of broiler chickens to Bacillus supplementation: Intestinal histomorphometry and blood immunoglobulin
  31. Weed composition and maize yield in a former tin-mining area: A case study in Malim Nawar, Malaysia
  32. Strategies for overcoming farmers’ lives in volcano-prone areas: A case study in Mount Semeru, Indonesia
  33. Principal component and cluster analyses based characterization of maize fields in southern central Rift Valley of Ethiopia
  34. Profitability and financial performance of European Union farms: An analysis at both regional and national levels
  35. Analysis of trends and variability of climatic parameters in Teff growing belts of Ethiopia
  36. Farmers’ food security in the volcanic area: A case in Mount Merapi, Indonesia
  37. Strategy to improve the sustainability of “porang” (Amorphophallus muelleri Blume) farming in support of the triple export movement policy in Indonesia
  38. Agrarian contracts, relations between agents, and perception on energy crops in the sugarcane supply chain: The Peruvian case
  39. Factors influencing the adoption of conservation agriculture by smallholder farmers in KwaZulu-Natal, South Africa
  40. Meta-analysis of zinc feed additive on enhancement of semen quality, fertility and hatchability performance in breeder chickens
  41. Meta-analysis of the potential of dietary Bacillus spp. in improving growth performance traits in broiler chickens
  42. Biocomposites from agricultural wastes and mycelia of a local mushroom, Lentinus squarrosulus (Mont.) Singer
  43. Cross transferability of barley nuclear SSRs to pearl millet genome provides new molecular tools for genetic analyses and marker assisted selection
  44. Detection of encapsulant addition in butterfly-pea (Clitoria ternatea L.) extract powder using visible–near-infrared spectroscopy and chemometrics analysis
  45. The willingness of farmers to preserve sustainable food agricultural land in Yogyakarta, Indonesia
  46. Transparent conductive far-infrared radiative film based on polyvinyl alcohol with carbon fiber apply in agriculture greenhouse
  47. Grain yield stability of black soybean lines across three agroecosystems in West Java, Indonesia
  48. Forms of land access in the sugarcane agroindustry: A comparison of Brazilian and Peruvian cases
  49. Assessment of the factors contributing to the lack of agricultural mechanization in Jiroft, Iran
  50. Do poor farmers have entrepreneurship skill, intention, and competence? Lessons from transmigration program in rural Gorontalo Province, Indonesia
  51. Communication networks used by smallholder livestock farmers during disease outbreaks: Case study in the Free State, South Africa
  52. Sustainability of Arabica coffee business in West Java, Indonesia: A multidimensional scaling approach
  53. Farmers’ perspectives on the adoption of smart farming technology to support food farming in Aceh Province, Indonesia
  54. Rice yield grown in different fertilizer combination and planting methods: Case study in Buru Island, Indonesia
  55. Paclobutrazol and benzylaminopurine improve potato yield grown under high temperatures in lowland and medium land
  56. Agricultural sciences publication activity in Russia and the impact of the national project “Science.” A bibliometric analysis
  57. Storage conditions and postharvest practices lead to aflatoxin contamination in maize in two counties (Makueni and Baringo) in Kenya
  58. Relationship of potato yield and factors of influence on the background of herbological protection
  59. Biology and life cycle Of Diatraea busckella (Lepidoptera: Crambidae) under simulated altitudinal profile in controlled conditions
  60. Evaluation of combustion characteristics performances and emissions of a diesel engine using diesel and biodiesel fuel blends containing graphene oxide nanoparticles
  61. Effect of various varieties and dosage of potassium fertilizer on growth, yield, and quality of red chili (Capsicum annuum L.)
  62. Review Articles
  63. Germination ecology of three Asteraceae annuals Arctotis hirsuta, Oncosiphon suffruticosum, and Cotula duckittiae in the winter-rainfall region of South Africa: A review
  64. Animal waste antibiotic residues and resistance genes: A review
  65. A brief and comprehensive history of the development and use of feed analysis: A review
  66. The evolving state of food security in Nigeria amidst the COVID-19 pandemic – A review
  67. Short Communication
  68. Response of cannabidiol hemp (Cannabis sativa L.) varieties grown in the southeastern United States to nitrogen fertilization
  69. Special Issue on the International Conference on Multidisciplinary Research – Agrarian Sciences
  70. Special issue on the International Conference on Multidisciplinary Research – Agrarian Sciences: Message from the editor
  71. Maritime pine land use environmental impact evolution in the context of life cycle assessment
  72. Influence of different parameters on the characteristics of hazelnut (var. Grada de Viseu) grown in Portugal
  73. Organic food consumption and eating habit in Morocco, Algeria, and Tunisia during the COVID-19 pandemic lockdown
  74. Customer knowledge and behavior on the use of food refrigerated display cabinets: A Portuguese case
  75. Perceptions and knowledge regarding quality and safety of plastic materials used for food packaging
  76. Understanding the role of media and food labels to disseminate food related information in Lebanon
  77. Liquefaction and chemical composition of walnut shells
  78. Validation of an analytical methodology to determine humic substances using low-volume toxic reagents
  79. Special Issue on the International Conference on Agribusiness and Rural Development – IConARD 2020
  80. Behavioral response of breeder toward development program of Ongole crossbred cattle in Yogyakarta Special Region, Indonesia
  81. Special Issue on the 2nd ICSARD 2020
  82. Perceived attributes driving the adoption of system of rice intensification: The Indonesian farmers’ view
  83. Value-added analysis of Lactobacillus acidophilus cell encapsulation using Eucheuma cottonii by freeze-drying and spray-drying
  84. Investigating the elicited emotion of single-origin chocolate towards sustainable chocolate production in Indonesia
  85. Temperature and duration of vernalization effect on the vegetative growth of garlic (Allium sativum L.) clones in Indonesia
  86. Special Issue on Agriculture, Climate Change, Information Technology, Food and Animal (ACIFAS 2020)
  87. Prediction model for agro-tourism development using adaptive neuro-fuzzy inference system method
  88. Special Issue of International Web Conference on Food Choice and Eating Motivation
  89. Can ingredients and information interventions affect the hedonic level and (emo-sensory) perceptions of the milk chocolate and cocoa drink’s consumers?
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