Effects of encapsulated butyric acid on general performance, intestinal health, and colonization in organs of poultry infected with <i>Salmonella</i> Enteritidis

This experiment was carried out to evaluate the effects of organic acids on the intestinal integrity and productive performance of broiler chickens experimentally inoculated with Salmonella Enteritidis. Additionally, Salmonella colonization levels in internal organs were evaluated. The study included 576 one-day-old Cobb^TM male broilers, distributed into eight treatment groups and six replicates. A completely randomized experimental design (encapsulated butyric acid × inoculation by Salmonella Enteritidis) was used. Poultry was orally inoculated with Salmonella Enteritidis in the first day (0 or 2.0 × 10⁶ CFU/mL) and after 22 days of age (0 or 1.0 × 10⁹ CFU/ mL). The butyric acid was added to the feed in different concentration (treatments 0.03, 0.075, and 0.15%), and the chickens were raised up to 42 days old. Encapsulated butyric acid at 0.03% increased the body weight gain and the average weight of the chickens up to 21 days old. After 14 days old, the butyric acid had a positive effect on jejunum villus. Encapsulated butyric acid at 0.03% in feed improves the performance and intestinal integrity of chickens.

Keywords
additives; chicks; histomorphometry; organic acids; salmonellosis

Authorship

Angélica Ribeiro Araújo Leonídio

Conceptualization

Data curation

Formal analysis

Funding acquisition

Investigation

Methodology

Resources

Software

Supervision

Validation

Visualization

Writing – original draft

Writing – review & editing

Instituto Federal de Educação, Ciência e Tecnologia Goiano, Urutaí, GO, Brasil.Instituto Federal de Educação, Ciência e Tecnologia GoianoBrasilUrutaí, GO, Brasil Instituto Federal de Educação, Ciência e Tecnologia Goiano, Urutaí, GO, Brasil.

http://orcid.org/0000-0002-6466-4856

Cíntia Minafra

Data curation

Methodology

Visualization

Universidade Federal de Goiás, Escola de Veterinária e Zootecnia, Goiânia, GO, Brasil.Universidade Federal de GoiásBrasilGoiânia, GO, Brasil Universidade Federal de Goiás, Escola de Veterinária e Zootecnia, Goiânia, GO, Brasil.

http://orcid.org/0000-0002-0727-5651

Maria Auxiliadora Andrade

Conceptualization

Methodology

Project administration

Resources

Supervision

Validation

Writing – original draft

http://orcid.org/0000-0002-8373-1671

Eduardo de Paula Nascente

Visualization

Writing – review & editing

http://orcid.org/0000-0002-9862-9127

Gisele Mendanha Nascimento

Funding acquisition

Investigation

Instituto Federal de Educação, Ciência e Tecnologia do Tocantins, Lagoa da Confusão, TO, Brasil.Instituto Federal de Educação, Ciência e Tecnologia do TocantinsBrasilLagoa da Confusão, TO, Brasil Instituto Federal de Educação, Ciência e Tecnologia do Tocantins, Lagoa da Confusão, TO, Brasil.

http://orcid.org/0000-0002-6826-1325

Jardel Barbosa dos Santos

Formal analysis

Software

http://orcid.org/0000-0003-2504-8783

José Henrique Stringhini

Data curation

Supervision

Validation

http://orcid.org/0000-0002-3710-6963

Ana Maria de Souza Almeida ^**Corresponding author:ana_almeida@ufg.br

Project administration

Validation

Visualization

Writing – review & editing

http://orcid.org/0000-0002-5699-2569

*Corresponding author:ana_almeida@ufg.br

Editors: Mateus Pies Gionbelli. Kyung-Woo Lee

Conflict of Interest

The authors declare no conflict of interest.

SCIMAGO INSTITUTIONS RANKINGS

Figures | Tables | Formulas

Figures (1)
Tables (7)
Formulas (1)

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Figure 1
Histomorphometry of villi height and crypt depth in the jejunum of 14- and 42-day-old chicks non-inoculated and inoculated with Salmonella Enteritidis, fed diet supplemented with different levels of encapsulated butyric acid (EBA).

HE, 4x.

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Table 1
Percentage composition of the experimental diets offered to the birds during the experimental period (1 to 42 days old)

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Table 2
Performance of 14-day-old broilers inoculated with Salmonella Enteritidis (SE) and treated with doses of butyric acid

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Table 3
Performance of 21-day-old broilers inoculated with Salmonella Enteritidis (SE) and treated with doses of butyric acid

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Table 4
Performance of 42-day-old broilers inoculated with Salmonella Enteritidis (SE) and treated with doses of butyric acid

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Table 5
Intestinal histomorphometry, average of villus height (VH), crypt depth (CD), and villi to crypt ratio (V:C) of the duodenum of 14- and 42-day-old chickens inoculated with Salmonella Enteritidis (SE) and treated with doses of encapsulated butyric acid (EBA)

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Table 6
Intestinal histomorphometry, average of villus height (VH), crypt depth (CD), and villi to crypt ratio (V:C) of the jejunum of 14- and 42-day-old chickens inoculated with Salmonella Enteritidis (SE) and treated with doses of encapsulated butyric acid (EBA)

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Table 7
Frequency of Salmonella Enteritidis isolation in organs and cloacal swabs of inoculated chicks treated with doses of encapsulated butyric acid

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Figure 1 Histomorphometry of villi height and crypt depth in the jejunum of 14- and 42-day-old chicks non-inoculated and inoculated with Salmonella Enteritidis, fed diet supplemented with different levels of encapsulated butyric acid (EBA).
HE, 4x.

Table 1 Percentage composition of the experimental diets offered to the birds during the experimental period (1 to 42 days old)

Ingredient	Diet (g kg⁻¹ as fed)
Ingredient	Pre-starter (1-7 d)	Starter (8-21 d)	Grower (22-35 d)	Finisher (36-42 d)
Corn grain	600.0	641.01	725.0	773.0
Soybean meal (45%)	333.0	265.0	175.0	136.0
Soybean oil	15.0	-	-	-
Meat and bone meal (45%)	-	45.0	45.0	35.0
Offal meal	-	15.2	15.2	15.0
Poultry fat	-	10.5	10.0	10.0
Limestone	8.1	4.5	3.1	3.8
Dicalcium phosphate	19.5	-	-	-
Salt	4.5	3.4	3.2	3.3
L-threonine	3.6	1.6	7.3	6.9
L-lysine HCL	4.9	4.3	5.9	6.4
DL-methionine	4.1	3.3	3.6	3.5
Vitamin premix¹	1.0	1.0	1.0	1.0
Mineral premix²	0.5	0.5	0.5	0.5
Inert/EBA³	5.0	5.0	5.0	5.0
Total	1,000.00	1,000.00	1,000.00	1,000.00
Nutrient (on dry matter)
Metabolizable energy (kcal kg⁻¹)	2,960	3,050	3,150	3,200
Crude protein	22.40	21.20	19.80	18.40
Calcium (%)	0.92	0.841	0.75	0.66
Available phosphorus (%)	0.47	0.40	0.38	0.32
Sodium (%)	0.22	0.21	0.20	0.19
Lysine (%)	1.34	1.21	0.82	1.06
Methionine + cysteine (%)	0.96	0.87	0.82	0.77
Methionine (%)	0.68	0.60	0.59	0.56

¹ Vitamin supplement (levels guaranteed per kg of product): vitamin A, 1,680,000 IU; vitamin D3, 400,000 IU; vitamin E, 3500 mg; vitamin K, 360 mg; vitamin B1, 436.50 mg; vitamin B2, 1200 mg; vitamin B6, 624 mg; vitamin B12, 2400 mcg; folic acid, 200 mg; pantothenic acid, 3120 mg; niacin, 8400 mg; biotin, 10,000 mcg.
² Mineral supplements (levels guaranteed per kg of product): zinc, 17,500 ppm; iron, 12,500 ppm; copper, 2,000 ppm; iodine, 187.50 ppm; selenium, 75 ppm.
³ Digestible minimum concentration of calcium butyrate in the microcapsules: 45%. Encapsulated butyric acid was added to the feed instead of the inert material (starch) at 0.03, 0.075, and 0.15%.

Table 2 Performance of 14-day-old broilers inoculated with Salmonella Enteritidis (SE) and treated with doses of butyric acid

EBA level	1 to 14 days
EBA level	AW (g)	WG (g)	FI (g)	FC (g/g)
Placebo	462.78	417.80	536.26	1.29b
0.03%	460.43	415.49	542.49	1.30b
0.075%	459.36	414.47	541.26	1.31ab
0.15%	456.56	411.59	550.08	1.36a
Regression	NS	NS	NS	NS
Contamination with SE
Non-inoculated	475.90a	430.92a	564.12a	1.31
Inoculated	443.66b	398.75b	523.96b	1.32
	P-value
Levels	0.777	0.785	0.164	0.012
Contamination	<0.0001	<0.0001	<0.0001	0.731
Levels × contamination	0.535	0.524	0.148	0.748
CV (%)	3.20	3.55	2.78	4.09

EBA - encapsulated butyric acid; AW - average weight; WG - weight gain; FI - feed intake; FC - feed conversion; NS - not significant; CV - coefficient of variation (%).
a,b - Lowercase letters (ANOVA followed by Tukey’s test) in the same column indicate significant differences (P<0.05).

Table 3 Performance of 21-day-old broilers inoculated with Salmonella Enteritidis (SE) and treated with doses of butyric acid

EBA level	1 to 21 days
EBA level	AW (g)	WG (g)	FI (g)	FC (g/g)
Placebo	911.76b	866.76b	1414.40	1.63
0.03%	955.50a	910.56a	1448.20	1.59
0.075%	912.95b	868.06b	1435.50	1.65
0.15%	923.00b	878.03b	1426.40	1.63
Regression	NS	NS	NS	NS
Contamination with SE
Non-inoculated	929.85	884.86	1458.87a	1.65a
Inoculated	922.19	887.28	1402.91b	1.60b
	P-value
Level	0.040	0.040	0.203	0.167
Contamination	0.436	0.440	<0.0001	0.028
Levels × contamination	0.089	0.089	0.105	0.152
CV (%)	4.5	4.73	2.93	4.04

EBA - encapsulated butyric acid; AW - average weight; WG - weight gain; FI - feed intake; FC - feed conversion; NS - not significant; CV - coefficient of variation (%).
a,b - Lowercase letters (ANOVA followed by Tukey’s test) in the same column indicate significant differences (P<0.05).

Table 4 Performance of 42-day-old broilers inoculated with Salmonella Enteritidis (SE) and treated with doses of butyric acid

EBA level	1 to 42 days
EBA level	AW (g)	WG (g)	FI (g)	FC (g/g)
Placebo	2112.55	2067.60	4212.10	2.07
0.03%	2114.41	2069.50	4230.40	2.04
0.075%	2109.40	2064.50	4203.60	2.02
0.15%	2082.88	2037.90	4153.50	2.04
Regression	NS	NS	NS	NS
Contamination with SE
Non-inoculated	2113.92	2068.90	4214.10	2.03
Inoculated	2097.24	2052.30	4187.70	2.05
	P-value
Levels	0.798	0.798	0.758	0.429
Contamination	0.559	0.562	0.673	0.183
Levels × contamination	0.738	0.736	0.635	0.903
CV (%)	4.11	4.19	4.47	2.85

EBA - encapsulated butyric acid; AW - average weight; WG - weight gain; FI - feed intake; FC - feed conversion; NS - not significant; CV - coefficient of variation (%).

Table 5 Intestinal histomorphometry, average of villus height (VH), crypt depth (CD), and villi to crypt ratio (V:C) of the duodenum of 14- and 42-day-old chickens inoculated with Salmonella Enteritidis (SE) and treated with doses of encapsulated butyric acid (EBA)

EBA level	14 days			42 days
EBA level	VH (µm)	CD (µm)	V:C	VH (µm)	CD (µm)	V:C
Placebo	1,104.82	199.92	5.52	1,272.56	243.48	5.22
0.03%	1,112.57	225.20	4.94	1,264.06	228.62	5.52
0.075%	1,104.03	212.63	5.19	1,395.99	205.57	6.79
0.15%	1,031.74	221.67	4.65	1,287.15	213.42	6.03
Regression	NS	NS	NS	NS	NS	NS
Contamination with SE
Non-inoculated	1,176.12a	209.65	5.60a	1,259.93	221.16	5.85
Inoculated	1,013.92b	221.95	4.56b	1,352.69	224.91	6.01
	P-value
Levels	0.402	0.737	0.158	0.519	0.054	0.095
Contamination	0.002	0.227	0.0007	0.136	0.599	0.183
Levels × contamination	0.231	0.842	0.055	0.382	0.208	0.128
CV (%)	12.66	15.36	16.88	15.94	15.44	15.33

NS - not significant; CV - coefficient of variation (%).
a,b - Lowercase letters (ANOVA followed by Tukey’s test) in the same column and in the same age group indicate significant differences (P<0.05).

Table 6 Intestinal histomorphometry, average of villus height (VH), crypt depth (CD), and villi to crypt ratio (V:C) of the jejunum of 14- and 42-day-old chickens inoculated with Salmonella Enteritidis (SE) and treated with doses of encapsulated butyric acid (EBA)

EBA level	14 days			42 days
EBA level	VH (µm)	CD (µm)	V:C	VH (µm)	CD (µm)	V:C
Placebo	734.62ab	172.15	4.26	926.79	162.39	5.70
0.03%	822.99a	181.32	4.53	742.72	148.59	4.99
0.075%	740.21ab	171.12	4.32	946.73	160.37	5.90
0.15%	692.71b	160.19	4.32	837.64	157.61	5.31
Regression	NS	NS	NS	NS	NS	NS
Contamination with SE
Non-inoculated	790.96a	171.71	4.60a	839.88	145.90b	5.75
Inoculated	711.74b	170.30	4.17b	904.34	170.61a	5.30
	P-value
Levels	0.017	0.159	0.942	0.051	0.794	0.110
Contamination	0.008	0.860	0.044	0.225	0.016	0.676
Levels × contamination	0.484	0.397	0.635	0.484	0.397	0.635
CV (%)	11.18	12.49	17.17	11.18	12.49	17.17

NS - not significant; CV - coefficient of variation (%).
a,b - Lowercase letters (ANOVA followed by Tukey’s test) in the same column and in the same age group indicate significant differences (P<0.05).

Table 7 Frequency of Salmonella Enteritidis isolation in organs and cloacal swabs of inoculated chicks treated with doses of encapsulated butyric acid

Treatment	Contamination by Salmonella Enteritidis (%)
	Organs (liver and spleen)				Cloacal swabs
	8 d	15 d	28 d	42 d	8 d	20 d	40 d
PC¹	0	0	0	0	16.6	0	0
0.03%	0	0	0	0	0	16.6	0
0.075%	0	0	0	0	0	0	0
0.15%	0	0	16.6	0	0	16.6	0

¹ PC: positive control (inoculated with Salmonella Enteritidis; not treated).

Y_{i j k} = μ + S_{i} + α_{i j} + T_{k} + T_{i k} + β_{i j k^{'}}

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Effects of encapsulated butyric acid on general performance, intestinal health, and colonization in organs of poultry infected with <i>Salmonella</i> Enteritidis

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[1] *Corresponding author:ana_almeida@ufg.br