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Effect of Dietary Inclusion of Protected Sodium Butyrate on the Digestibility and Intestinal Histomorphometry of Commercial Laying Hens

ABSTRACT

The objective of this study was to evaluate the effects of dietary inclusion of protected sodium butyrate (PSB) on the intestinal development and feed nutrient metabolizability of commercial laying hens. The birds started to receive the treatment rations at 58 weeks of age. At 76 weeks of age the laying hens were distributed in a randomized block design to four treatments (0, 105, 210 and 300 g t-1/PSB), six replicates, and two birds/replicate. The nitrogen balance (NB), ether extract balance (EEB), dry matter metabolizability coefficient, nitrogen, ether extract, ash, apparent metabolizable energy (AME), and AME corrected by nitrogen (AMEn) were evaluated. For assessment of intestinal development, we evaluated the duodenum, jejunum, ileum, cecum, and colorectal lengths, the relative intestine weight and villus height, crypt depth, and villus:crypt ratio of the duodenum, jejunum, and ileum. A decreasing linear effect was observed in the duodenum length, while an increasing linear effect was observed in the height of the duodenum and jejunum villi. A quadratic effect was found in the jejunum crypt depth. A linear increasing effect was found on the villus:crypt ratio of the duodenum and jejunum, and a quadratic effect was observed in the ileum. Quadratic and increasing linear effects were observed in the NB and EEB, respectively. Additionally, increasing linear effects were observed in the AME and AMEn. The dietary addition of 300 g t-1 of PSB improved intestinal development and energy metabolizability of the diet.

Keywords:
Additive; intestinal health; metabolizability; nutrition; organic acids

INTRODUCTION

As laying hens age, they lay larger eggs with reduced shell thickness owing to the larger egg surface area; additionally, the calcium carbonate deposition per unit surface area decreases because the egg weight increase rate is higher than the shell volume increase rate in eggs laid by ageing birds (Carvalho et al., 2013Carvalho JX, Suárez RO, Mendes FQ, Fernandes RVB, Cunha MC, Carvalho AMX. Extensão da vida de prateleira de ovos pela cobertura com própolis. Semina: Ciências Agrárias 2013;34(5):2287-2296.; Oliveira et al., 2020Oliveira HF, Carvalho DP, Ismar MG, Rezende PM, Camargo SMP, Souto CN, et al. Fatores intrínsecos a poedeiras comerciais que afetam a qualidade físico-química dos ovos. PubVet 2020;14(3):1-11.). In addition, older birds have reduced ability to absorb calcium through the intestine owing to a reduction in their capacity to convert the inactive form of vitamin D into its active form; moreover, their retention rate of absorbed calcium is lower, as is their ability to mobilize bone calcium, owing to the lower enzymatic activity of carbonic anhydrase, which leads to reduced eggshell calcification (Vilela et al., 2016Vilela DR, Carvalho LSS, Fagundes NS, Fernandes EA. Qualidade interna e externa de ovos de poedeiras comerciais com cascas normal e vítrea. Ciência Animal Brasileira 2016;17(4):509-518.). However, according to Sengor et al. (2007Sengor E, Yardimci M, Cetingul S, Bayram I, Sahin H, Dogan I. Effects of short chain fatty acid (SCFA) supplementation on performance and egg characteristics of old breeder hens. South African Journal of Animal Science 2007;37(3):158-163.), as the birds get older, the intestinal mucosa cells weaken, thereby leading to a reduction in duodenal villus height, which hampers the absorption of the nutrients required for eggshell formation.

Along with the reduction in shell quality, the high cost of bird feed ingredients has led to research advances towards developing performance-enhancing additives that maximize nutrient uptake and, consequently, improve the egg quality, performance, and intestinal mucosa structure of laying hens, thereby promoting better nutrient absorption (Lemos et al., 2017Lemos M, Calixto LF, Souza D, Torres KA, Reis T, Coelho L, Filho CA. Efeito de diferentes aditivos zootécnicos sobre a qualidade de ovos em duas fases produtivas da codorna. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 2017;69(3):751-760.).

Sodium butyrate [Na(C3H7COO)], is a four-carbon short-chain organic acid in the form of a soluble salt derived from butyric acid; it can be used in its free or protected form in animal feeds. In its free form, it is absorbed in the proximal parts of the gastrointestinal tract, therefore it does not reach the distal parts. In its protected form, sodium butyrate is gradually released into the digestive tract, thereby increasing its mode of action at several parts of the intestine (Vallejos et al., 2015Vallejos PD, Carcelén CF, Jiménez AR, Perales CR, Santillán AG, Ara GM, et al. Efecto de la suplementación de butirato de sodio en la dieta de Cuyes(Cavia porcellus) de engorde sobre el desarrollo de las vellosidades intestinales y criptas de Lieberkühn. Revista de Investigaciones Veterinarias del Perú 2015;26(3):395-403.; Santos Junior et al., 2016Santos Junior, MM, Candia EWS, Jesus GFA, Seiffert WQ, Mouriño JLP, Vieira FN. Suplementação dietética com probiótico e butirato de sódio no pré-berçário de Litopenaeus vannamei. Boletim do Instituto de Pesca 2016;42(2):457-463.).

Sodium butyrate is readily transformed into butyric acid within the digestive tract of birds, where it improves intestinal health through various mechanisms. Its inclusion in the diet provides a readily available source of energy for the enterocytes of the intestinal mucosa, thereby increasing the cell proliferation rate and nutrient absorption from the feed. It improves the beneficial bacterial populations and reduces the colonization of harmful bacteria in the digestive tract (Van et al., 2004Van IF, Fievez V, Buck J, Pasmans F, Martel A, Haesebrouck F, et al. Microencapsulated short-chain fatty acids in feed modify colonization and invasion early after infection with Salmonella enteritidis in young chickens. Poultry Science 2004;83(1):69-74.; Chamba et al., 2014Chamba F, Puyalto M, Ortiz A, Torrealba H, Mallo JJ, Riboty R. Effect of partially protected sodium butyrate on performance, digestive organs, intestinal villi and E. coli development in broilers chickens. International Journal of Poultry Science 2014;13(7):390-396.; Ahsan et al., 2016Ahsan U, Cengiz Ö, Raza I, Kuter E, Chacher MFA, Iqbal Z, et al. Sodium butyrate in chicken nutrition:the dynamics of performance, gut microbiota, gut morphology, and immunity. World's Poultry Science Journal 2016;72(2):265-278.). Regarding improvements in dietary nutrient metabolism, sodium butyrate acts by acidifying the digestive tract, thereby increasing the duration of food retention in the stomach, improving the activity of the digestive enzymes, and increasing pancreatic secretions (Machinsky et al., 2010Machinsky TG, Kessler AM, Ribeiro AML, Moraes ML, Silva ICM, Cortés MEM. Digestibilidade de nutrientes e balanço de Ca e P em suínos recebendo dietas com ácido butírico, fitase e diferentes níveis de cálcio. Ciência Rural 2010;40(11):2350-2355.).

The objective of the present study was to investigate the effect of increasing levels of dietary protected sodium butyrate on the digestibility and intestinal histomorphometry of light laying hens aged 76 weeks.

MATERIAL AND METHODS

The research was approved by the Ethics Committee on Animal Use (protocol nº 74/14). The experiment was conducted in Goiânia, Goiás, Brazil (16º40’43”S, 49º15’14”W), in an area that has an altitude of 749 m.

A total of 400, 58-week-old, Dekalb White light laying hens were obtained from a commercial farm. They were all weighed individually, and 320 laying hens were selected. Birds with a live weight above or below the breed standard (average weight of 1.660 kg), the standard deviation of which was 10 %, were discarded. There was a 21-day adaptation period, which was followed by egg production in order to select birds according to their egg production capacity (maximum variation of 10 %). The laying hens received experimental feed when they were between 58 and 76 weeks old.

The birds were housed in pairs, in galvanized wire cages with linear feeders and nipple drinkers, in a brick laying house. Throughout the experimental period, feed was supplied twice daily, at 8 a.m. and 6 p.m., while ensuring that the birds received water and feed in accordance with the recommended daily consumption values established for the breed. The lighting schedule was adjusted to 16 h of light per day, in accordance with the recommendations for the breed, and was controlled by an automated clock.

We used a randomized block design for the experiment, the hens were assigned to blocks based on their bodyweight (light birds weighing 1.494 - 1.660 kg and heavy birds weighing 1.660 - 1.826 kg), with four treatments, and eight repetitions with ten birds each. When the birds became 76 weeks old, the metabolic test was performed, with six repetitions and two birds in each repetition. The treatments included 0 g.t-1, 105 g.t-1, 210 g.t-1, and 300 g.t-1 of protected sodium butyrate in the feed.

The statistical model used was:

y i j = u + b i + t j + e i j

yij: an observation in treatment i and block j;

μ: the overall mean;

bi: the fixed effect of the i-th treatment;

tj: the fixed effect of the j-th block;

eij: random error with a mean of 0 and variance σ2.

The experimental feed was prepared from a baseline feed consisting of maize and soybean meal in accordance with the Brazilian nutritional standards for birds and pigs Rostagno et al. (2011Rostagno HS, Albino LFT, Donzele JL, Gomes PC, Oliveira RF, Lopes DC, et al. Tabelas brasileiras para aves e suínos:composição de alimentos e exigências nutricionais. Viçosa: UFV; 2011.) (Table 1); the only difference among the diets was the protected sodium butyrate level. The commercial additive Adimix Precision® (30 % protected sodium butyrate) was used as a source of protected sodium butyrate. In order to obtain the aforementioned protected sodium butyrate levels in the treatments, we added 0 g.t-1, 350 g.t-1, 700 g.t-1, and 1.000 g.t-1 of Adimix Precision® in the hens’ rations.

Table 1
Composition and calculated nutritional value of the basal diet.

The metabolic test was performed using the total excrement collection method for four consecutive days. During this period, the feed consumption monitoring and excrement collection were performed twice daily (morning and afternoon). The excreta were stored in plastic bags identified and stored in a freezer until the end of the collection period. Subsequently, the samples were thawed, homogenized, and divided in aliquots that were weighed. Then, they were pre-dried in ventilated greenhouses at 55 °C for 72 h. Subsequently, the dry matter, nitrogen, and ethereal extract were analyzed according to the methodology described by Silva & Queiroz (2002Silva DJ, Queiroz AC. Análise de alimentos(métodos químicos e biológicos). Viçosa: UFV; 2002.). The crude energy was determined using a calorimeter pump (model 5000; Ika).

Based on the bromatological analyses, we calculated the nitrogen balance (NB), ether extract balance (EEB), dry matter metabolizability coefficient (DMMC), nitrogen metabolizability coefficient (NMC), ether extract metabolizability coefficient (EEMC), ash metabolizability coefficient (AMC), apparent metabolizable energy (AME), and AME corrected by nitrogen (AMEn) using the equations proposed by Sakomura & Rostagno (2016Sakomura NK, Rostagno HS. Métodos de pesquisa em nutrição de monogástricos. Jaboticabal; FUNEP; 2016.).

After the metabolic test was performed, one bird per repetition was euthanized by cervical dislocation to analyze its intestinal morphometry. The entire intestine was collected and weighed, and mensured lengths the duodenum (from the pylorus to the distal portion of the duodenal loop), jejunum (from the distal duodenal loop to the ileumcecal junction), ileum (from the anterior portion of the caecum to the ileumcecal junction), cecum (from its base to the summit), and colorectal (junction ileumcecal to the anterior portion of the cloaca). The relative weight of the intestine was obtained by the equation (gut weight/live weight of the bird) × 100.

For the histological analyses of the intestinal mucosa, we collected 5-cm samples from the segments of the small intestine (duodenum, jejunum, and ileum). The small intestine samples were opened, fixed in polystyrene, and immersed in 10 % formalin for 24 h. Next, they were stored in 70 % alcohol, processed according to the methodology described by Luna (1968Luna LG. Manual of the histologic staining methods of the armed forces institute of pathology. New York: McGraw Hill; 1968.), and stained by the hematoxylin-eosin (HE) method. The images of the blades were obtained with the aid of an optical microscope (DM 4000B; Leica) coupled to a microcomputer, and were then analyzed with the aid of ImageJ software, via which five measurements of villus height and crypt depth per blade were obtained, totaling 360 readings. The villus:crypt ratio was obtained by dividing the height of the villus by the depth of the crypt.

The data collected were subjected to analysis of variance with α = 0.05; polynomial regression was performed for all the protected sodium butyrate levels, using R statistical software.

RESULTS

The regression analysis showed that the addition of dietary protected sodium butyrate did not have an effect on the intestinal morphometry (relative weight of the intestine and length of the duodenum, ileum, cecum, and colon) of laying hens at 76 days of age (Table 2). However, the length of the duodenum decreased linearly (p<0.05) with increasing levels of sodium butyrate in the diet (Figure 1).

Figure 1
Linear effect for duodenal length (cm) of laying hens fed with different levels of protected sodium butyrate.

Table 2
Relative weight and intestine length of laying hens aged 76 weeks that were fed with different levels of protected sodium butyrate (PSB).

The histological analysis of the small intestine (Table 3) showed an increasing linear effect (p<0.05) on the villus height of the duodenum and jejunum with increasing sodium butyrate levels in the diet (Figure 2). The crypt depth of the duodenum and ileum was not influenced by the treatments. A quadratic effect was observed in the crypt depth of the jejunum, which decreased with protected sodium butyrate levels of up to 151 g t-1 (p<0.05) (Figure 3).

Figure 2
Linear effect for duodenal and jejunal villus height (µm) of laying hens fed with different levels of protected sodium butyrate.

Figure 3
Quadratic effect for jejunal crypt depth (µm) of laying hens fed with different levels of protected sodium butyrate.

Table 3
Villus height (µm), crypt depth (µm) and villus/crypt ratio in the duodenum, jejunum and ileum of light laying hens aged 76 weeks that were fed with different levels of protected sodium butyrate (PSB).

The villus:crypt ratio of the duodenum and jejunum increased linearly (p<0.05) with the inclusion of sodium butyrate in the ration (Figure 4). On the other hand, a quadratic effect (p<0.05) was observed in the villus:crypt ratio of the ileum, which peaked at a protected sodium butyrate level of 171 g t-1 (Figure 5).

Figure 4
Linear effect for the duodenal and jejunal villus/crypt ratio of laying hens fed with different levels of protected sodium butyrate.

Figure 5
Quadratic effect for the ileal villus/crypt ratio of laying hens fed with different levels of protected sodium butyrate.

In terms of the dietary nutrient metabolism (Table 4), significant regression was observed for the NB, EEB, AME, and AMEn. The regression analysis did not show any differences in terms of the feed nutrient metabolizability coefficients (DMMC, NMC, EEMC, and AMC) (p>0.05).

Table 4
Nitrogen balance (NB), ether extract balance (EEB), dry matter metabolizability coefficient (DMMC), nitrogen metabolizability coefficient (NMC), ether extract metabolizability coefficient (EEMC), ash metabolizability coefficient (AMC), apparent metabolizable energy (AME) and apparent metabolizable energy corrected by nitrogen (AMEn) of the feed of light laying hens containing protected sodium butyrate (PSB).

A quadratic effect was observed in the NB (p<0.05), as this increased with sodium butyrate levels of up to 93 g t-1. The EEB, AME, and AMEn increased linearly (p<0.05) with increasing sodium butyrate levels.

DISCUSSION

In the present study, the relative weight and length of the intestinal segments (duodenum, ileum, cecum, colon, and rectum) were not influenced by the treatments. Silva (2013Silva JL. Protease e butirato de sódio nas dietas pré-inicial e inicial de suínos [tese]. Goiás (GO): School of Veterinary and Zootechnics of the Federal University of Goiás; 2013.) evaluated the use of 300 g.t-1 of sodium butyrate in the feed of nursery-phase pigs and found that the relative weight of their small intestines was lower than that of the control group. According to Silva (2013), a better dietary nutrient uptake can reduce the feed bolus viscosity and the functional load of the intestine, thus decreasing the relative weight of the small intestine. However, this was not observed in the present study.

The length of the duodenum decreased with increasing sodium butyrate levels in the diet. Similarly, Viola et al. (2008Viola ES, Vieira SL, Torres CA, Freitas DM, Berres J. Desempenho de frangos de corte sob suplementação com ácidos lático, fórmico, acético e fosfórico no alimento ou na água. Revista Brasileira de Zootecnia 2008;37(2):296-302.) evaluated the addition of 4.5 kg.t-1 of an organic acid mixture (50 % lactic acid, 8 % formic acid, and 7 % acetic acid) in the diet of broiler chickens; their results showed that the organic acid treatment resulted in shorter jejunum lengths in 21-day-old chickens than in the control group.

The inclusion of protected sodium butyrate in the laying hens’ rations resulted in increased villus height in the duodenum and jejunum. According to Niwińska et al. (2017), this effect may have occurred because butyric acid is a source of energy readily available and rapidly absorbed by the intestinal mucosa, in order to produce adenosine triphosphate (ATP). Thus, sodium butyrate is able to accelerate the mitosis process that occurs in the crypt-villus region (Górka et al., 2014Górka P, Pietrzak P, Kotunia A, Zabielski R, Kowalski ZM. Effect of method of delivery of sodium butyrate on maturation of the small intestine in newborn calves. Journal of Dairy Science 2014;97(2):1026-1035.), thereby resulting in an increase in the cell proliferation rate and lower energy loss through turnover. The higher the cell number, the greater the intestinal villus height, thus, the larger the nutrient absorption surface area (Maiorka et al., 2004Maiorka A, Santin AME, Borges SA, Opalinski M, Silva AVF. Emprego de uma mistura de ácido fumárico, lático, cítrico e ascóbico em dietas iniciais de frangos de corte. Archives of Veterinary Science 2004;9(1):31-37.). In addition, sodium butyrate can influence positively the intestinal integrity because of its bactericide and bacteriostatic effects, since it decreases the intestinal cell desquamation, thereby favoring the structure and growth of intestinal villi (Ahsan et al., 2016Ahsan U, Cengiz Ö, Raza I, Kuter E, Chacher MFA, Iqbal Z, et al. Sodium butyrate in chicken nutrition:the dynamics of performance, gut microbiota, gut morphology, and immunity. World's Poultry Science Journal 2016;72(2):265-278.) and reducing the enterocyte turnover owing to the reduction of bacterial toxins and improved colonic barrier function (Guilloteau et al., 2010Guilloteau P, Martin L, Eeckhaut V, Ducatelle R, Zabielski R, Immerseel FV. From the gut to the peripheral tissues:the multiple effects of butyrate. Nutrition Research Reviews 2010;23(2):366-384.).

The results of the present study are corroborated by Herrera et al. (2009Herrera IS, Hernández EP, Ramírez ES, Martínez BF, Espinoza JH, Veja JLL, et al. Efecto del butirato de sodio en dietas para gallinas sobre el comportamiento productivo, calidad del huevo y vellosidades intestinales. Veterinaria México 2009;40(4):397-403.) who verified an increase in the duodenal villus height of laying hens that had been fed diets containing 300 g.t-1 and 500 g.t-1 of sodium butyrate for 73 weeks. In addition, Panda et al. (2009Panda AK, Rao SVR, Raju MVLN, Sunder GS. Effect of butyric acid on performance, gastrointestinal tract health and carcass characteristics in broiler chickens. Asian-Australasian Journal of Animal Science 2009;22(7):1026-1031.) evaluated the addition of increasing levels of sodium butyrate (200 g.t-1, 400 g.t-1, and 600 g.t-1) in broiler rations and observed higher duodenal villus heights in all sodium butyrate treatments compared to the control treatment.

No significant differences were found in the crypt depth of the duodenum and ileum; however, in the jejunum, the lowest crypt depth was found at the 151 g.t-1 dose. The jejunum crypt depth increased with increasing protected sodium butyrate levels. These results do not corroborate those of (Santos, 2013Santos LM. Digestibilidade de nutrientes e desempenho de codornas japonesas suplementadas com ácidos orgânicos após pico de postura [tese]. Goiás (GO): School of Veterinary and Zootechnics of the Federal University of Goiás; 2013.), who did not observe jejunum crypt depth increases with the use of sodium butyrate in the feed of Japanese quails. According to Oetting et al. (2006Oetting LL, Utiyama CE, Giani PA, Ruiz US, Miyada VS. Efeitos de extratos vegetais e antimicrobianos sobre a digestibilidade aparente, o desempenho, a morfometria dos órgãos e a histologia intestinal de leitões recém-desmamados. Revista Brasileira de Zootecnia 2006;35(4):1389-1397.), a crypt depth increase can indicate higher cell proliferation activity, thereby ensuring an appropriate cell renewal rate in the apical region of the villus.

A linear effect was observed in the villus:crypt ratio of the duodenum and jejunum. Therefore, as the levels of protected sodium butyrate in the feed increased, the intestinal absorption area also increased. In the ileum, a quadratic effect was observed in the villus:crypt ratio, as this peaked at a dose of 171 g.t-1 of protected sodium butyrate in the diet, thus indicating an increase in the nutrient absorption area. Santos (2013Santos LM. Digestibilidade de nutrientes e desempenho de codornas japonesas suplementadas com ácidos orgânicos após pico de postura [tese]. Goiás (GO): School of Veterinary and Zootechnics of the Federal University of Goiás; 2013.) did not detect any differences in the villus:crypt ratio in any of the segments of the small intestine of Japanese quails that were fed diets with 150 g.t-1 of protected sodium butyrate, compared with the control group.

According to Arouca et al. (2012Arouca CLC, Maciel MP, Aiura FS, Barbosa MM, Botelho LFR, Pereira FM, et al. Desempenho, morfometria de órgãos e histologia intestinal de suínos na fase de terminação tardia alimentados com cana-de-açúcar. Revista Brasileira de Saúde e Produção Animal 2012;13(4):1074-1083.), the higher the villus:crypt ratio, the better the nutrient absorption and the lower the energy losses owing to cell renewal. Similarly, the results of the present study showed that there was an increase in the nutrient absorption capacity and lower energy losses when protected sodium butyrate was used. According to the small-intestine histomorphometric analysis, the use of 300 g.t-1 of sodium butyrate was the most efficient, as it resulted in the greatest duodenum and jejunum villus heights as well as the highest villus:crypt ratios in the three segments of the small intestine.

The NB increased with the inclusion of up to 93 g.t-1 of sodium butyrate in the diet; as the sodium butyrate level increased, the NB decreased. However, the EEB increased with increasing sodium butyrate levels in the diet. An increasing linear effect was observed on the AME and the AMEn. Likewise, Riboty et al. (2016Riboty R, Chamba F, Puyalto M, Mallo JJ. Effect of partially-protected sodium butyrate and virginiamycin on nutrient digestibility, metabolizable energy, serum metabolites and performance of broiler chickens. International Journal of Poultry Science 2016;15(8):304-312.) observed that broiler chickens that had been fed diets with sodium butyrate had increased AMEn values compared with the control group.

The improved nutrient retention and increase in metabolizable energy (AME and AMEn) can be explained by the action of protected sodium butyrate in the intestine. According to Van et al. (2004Van IF, Fievez V, Buck J, Pasmans F, Martel A, Haesebrouck F, et al. Microencapsulated short-chain fatty acids in feed modify colonization and invasion early after infection with Salmonella enteritidis in young chickens. Poultry Science 2004;83(1):69-74.), protected sodium butyrate can reach the bird’s intestine without undergoing dissociation. Once in the intestine, the matrix that protects sodium butyrate is emulsified and hydrolyzed through the action of hepatic and pancreatic secretions, thus releasing the acid in a dissociated form and diminishing the pH of the digesta in the duodenum.

The low pH of the digesta stimulates the secretion of the hormone secretin by the duodenal cells. This stimulates the pancreas to secrete bicarbonate, thereby neutralizing the acidic pH in the duodenum and increasing the action of pancreatic enzymes. In addition, according to Niwińska et al. (2017), the presence of sodium butyrate in the duodenum stimulates the secretion of the hormone cholecystokinin (CCK), which stimulates the secretion of pancreatic enzymes. This also stimulates the secretion of bile by the gallbladder, which acts as a lipid emulsifier, thus facilitating the action of the enzyme pancreatic lipase as well as lipid transportation and absorption (Lan et al., 2020Lan R, Li S, Chang Q, An L, Zhao Z. Sodium butyrate enhances growth performance and intestinal development in broilers. Czech Journal of Animal Science 2020;65(1):1-12.).

The positive effects of protected sodium butyrate on the nutrient metabolizability of the feed can also be correlated with the antimicrobial effect of the organic acid. According to Costa et al. (2011Costa LB, Almeida VV, Berenchtein B, Tse MLP, Andrade C, Miyada VS. Aditivos fitogênicos e butirato de sódio como alternativas aos antibióticos para leitões desmamados. Archivos de Zootecnia 2011;60(231):733-744.), sodium butyrate acts on the pathogenic microbiota owing to its bactericidal and bacteriostatic effects, thereby reducing the competition for dietary nutrients, decreasing fermentation, and increasing the available energy that can be metabolized in the intestinal mucosa. Decreasing pathogenic microbiota levels result in a lower enterocyte turnover owing to the reduction of bacterial toxins (Ahsan et al., 2016Ahsan U, Cengiz Ö, Raza I, Kuter E, Chacher MFA, Iqbal Z, et al. Sodium butyrate in chicken nutrition:the dynamics of performance, gut microbiota, gut morphology, and immunity. World's Poultry Science Journal 2016;72(2):265-278.; Guilloteau et al., 2010Guilloteau P, Martin L, Eeckhaut V, Ducatelle R, Zabielski R, Immerseel FV. From the gut to the peripheral tissues:the multiple effects of butyrate. Nutrition Research Reviews 2010;23(2):366-384.).

Sodium butyrate also provides readily available energy to enterocytes, which can favor cell proliferation and, consequently, increase the villus size, thereby increasing the nutrient absorption area in the intestine. In the present study, we verified that protected sodium butyrate increased the villi of the duodenum and jejunum and resulted in a greater villus:crypt ratio in the duodenum, jejunum, and ileum, which may have favored nutrient retention and increased metabolizable energy (AME and AMEn).

With the results of the present study, that is, with improved intestinal development and energy metabolizability of the diet, it is possible to explain a better response in performance and eggshell quality. Pires et al. (2020Pires MF, Leandro NSM, Jacob DV, Carvalho FB, Oliveira HF, Stringhini JH, et al; Performance and egg quality of commercial laying hens fed with various levels of protected sodium butyrate. South African Journal of Animal Science 2020;50(5):758-765.) observed that the inclusion of protected sodium butyrate in the laying hens diets did not appear to affect the productive performance of the birds, but it did improve the eggshell quality of laying hens at 61-76 weeks of age, improving the thickness, resistance and percentage of shell and reducing the percentage of broken and dirty eggs. According to the authors, the observed improvement can be explained by the effects of the additive on the intestinal mucosa, as an energy source for the intestinal cells, and also in the increase of metabolizability and nutrient retention, as confirmed in the present study.

CONCLUSION

The addition of protected sodium butyrate in the diet of commercial laying hens improved the intestinal parameters. A level of 300 g t-1 of protected sodium butyrate is recommended for the improvement of the intestinal development and the energy metabolizability of the diet.

ACKNOWLEDGEMENTS

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) - Finance Code 001.

REFERENCES

  • Ahsan U, Cengiz Ö, Raza I, Kuter E, Chacher MFA, Iqbal Z, et al. Sodium butyrate in chicken nutrition:the dynamics of performance, gut microbiota, gut morphology, and immunity. World's Poultry Science Journal 2016;72(2):265-278.
  • Arouca CLC, Maciel MP, Aiura FS, Barbosa MM, Botelho LFR, Pereira FM, et al. Desempenho, morfometria de órgãos e histologia intestinal de suínos na fase de terminação tardia alimentados com cana-de-açúcar. Revista Brasileira de Saúde e Produção Animal 2012;13(4):1074-1083.
  • Carvalho JX, Suárez RO, Mendes FQ, Fernandes RVB, Cunha MC, Carvalho AMX. Extensão da vida de prateleira de ovos pela cobertura com própolis. Semina: Ciências Agrárias 2013;34(5):2287-2296.
  • Chamba F, Puyalto M, Ortiz A, Torrealba H, Mallo JJ, Riboty R. Effect of partially protected sodium butyrate on performance, digestive organs, intestinal villi and E. coli development in broilers chickens. International Journal of Poultry Science 2014;13(7):390-396.
  • Costa LB, Almeida VV, Berenchtein B, Tse MLP, Andrade C, Miyada VS. Aditivos fitogênicos e butirato de sódio como alternativas aos antibióticos para leitões desmamados. Archivos de Zootecnia 2011;60(231):733-744.
  • Górka P, Pietrzak P, Kotunia A, Zabielski R, Kowalski ZM. Effect of method of delivery of sodium butyrate on maturation of the small intestine in newborn calves. Journal of Dairy Science 2014;97(2):1026-1035.
  • Guilloteau P, Martin L, Eeckhaut V, Ducatelle R, Zabielski R, Immerseel FV. From the gut to the peripheral tissues:the multiple effects of butyrate. Nutrition Research Reviews 2010;23(2):366-384.
  • Herrera IS, Hernández EP, Ramírez ES, Martínez BF, Espinoza JH, Veja JLL, et al. Efecto del butirato de sodio en dietas para gallinas sobre el comportamiento productivo, calidad del huevo y vellosidades intestinales. Veterinaria México 2009;40(4):397-403.
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Publication Dates

  • Publication in this collection
    04 June 2021
  • Date of issue
    2021

History

  • Received
    06 Dec 2020
  • Accepted
    04 Jan 2021
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