SciELO - Scientific Electronic Library Online

 
vol.52 número5Effects of Bacillus subtilis on performance, immune system and gut in Salmonella-challenged broilersCorrelation between chemical composition, EHGE and TME of corn for ducks índice de autoresíndice de assuntospesquisa de artigos
Home Pagelista alfabética de periódicos  

Serviços Personalizados

Artigo

Indicadores

Links relacionados

  • Em processo de indexaçãoCitado por Google
  • Em processo de indexaçãoSimilares em Google

Compartilhar


South African Journal of Animal Science

versão On-line ISSN 2221-4062
versão impressa ISSN 0375-1589

S. Afr. j. anim. sci. vol.52 no.5 Pretoria  2022

http://dx.doi.org/10.4314/sajas.v52i5.03 

Protected sodium butyrate in chicken diets until 21 days of age improves intestinal development and performance

 

 

M. F. PiresI; N. S. M. LeandroI; M. B. CaféI; F. B. CarvalhoI; D. V. JacobII; R. A. Noleto-MendonçaIII, #; S. D. AssisIV; J. M. S. MartinsV

IFederal University of Goiás, Department of Animal Science, Goiânia, Goiás, Brazil
IIAdisseo, São Paulo, São Paulo, Brazil
IIIM&S Projetos Agropecuários, Uberaba, Minas Gerais, Brazil
IVFederal Institute of Education, Science and Technology of Mato Grosso, São Vicente Campus, Cuiabá, Brazil
VState University of Minas Gerais, Agronomic Engineering, Ituiutaba, Minas Gerais, Brazil

 

 


ABSTRACT

This study was developed to examine the performance, carcass and cut yields, nutrient digestibility, and intestinal histomorphometry of chickens fed diets supplemented with protected sodium butyrate until 21 days of age. Two experiments were conducted, both of which involved the following treatments: basal diet with inclusion of an antibiotic; basal diet without antibiotic or protected sodium butyrate (PSB; control); basal diet with inclusion of 225 g/t PSB in the pre-starter and starter phases; and basal diet with inclusion of 300 g/t PSB in the pre-starter and starter phases. In the first experiment, 784 male broiler chicks were distributed into the four treatments, with seven replicates of 28 birds, to evaluate performance and carcass and cut yields. In experiment II, 280 male broiler chicks were distributed into the four treatments, with seven replicates of 10 birds, to evaluate intestinal digestibility and histomorphometry. At 42 days of age, the broilers supplemented with 225 g/t PSB had a higher average final weight than the control group. At seven days, the chickens supplemented with 300 g/t PSB exhibited the highest duodenal villus height; those supplemented with 225 or 300g/t PSB or antibiotic showed the greatest jejunal villus height; and those treated with 225 g/t PSB exhibited the highest jejunal villus/crypt ratio. At 21 days of age, the broilers that received 225 g/t PSB showed the highest duodenal and jejunal villus height. The use of protected sodium butyrate in chicken diets up to 21 days of age improves intestinal development and performance until slaughter age.

Keywords: digestibility, intestinal health, nutrition, organic acids, poultry


 

 

Introduction

Studies aimed at improving nutrient utilisation in birds, and, consequently, their performance, point to the importance of development and maintenance of intestinal integrity and balance of the intestinal microbiota, which impede the fixation and multiplication of pathogenic microorganisms, preventing enteric diseases (Celi et al., 2017; Diaz Carrasco et al., 2019; Oviedo-Rondón, 2019).

A commonly employed nutritional strategy to increase poultry production rates by maintaining integrity and manipulating the intestinal microbiota is the use of antibiotics as growth promoters, at subtherapeutic levels. However, despite all the improvements achieved in intestinal physiology, in January 2006, the European Union - one of the world's largest importers of poultry products - decided to completely ban the use of growth-promoting antibiotics due to growing concerns about the presence of residues in products for human consumption, which can produce allergic reactions and toxicity or induce resistance in pathogenic bacteria (Huyghebaert et al., 2011).

This new scenario, coupled with market demands, has driven the search for substitutes for growth-promoting antibiotics that do not reduce productivity in poultry farming or increase its production costs. Among these alternatives, organic acids stand out. Graham Solomons & Fhyhle (2011) defined organic acids as any substance with a general R-COOH structure, known as derivatives of carboxylic acids, e.g., amino acids, fatty acids, coenzymes, and intermediate metabolites. Those associated with antimicrobial activity are short-chain fatty acids that produce fewer protons per molecule upon dissociation, which can be either monocarboxylic, such as formic, acetic, propionic and butyric acids; or carboxylated with the hydroxyl group, e.g., lactic, malic, tartaric, benzoic and citric acids, which are natural constituents of plants and animals (Picker et al., 2012).

Butyric acid, or butyrate, is known to be a safe alternative to antibiotics and, as such, has received great attention in the poultry industry. However, because butyrate is odorous and unstable, sodium butyrate is used as a substitute due to its stable and non-odoriferous properties (Lan et al., 2020); when administered in animal feed, it can be used in its free or protected form (micro-encapsulated). In its free form, it is rapidly absorbed in the early parts of the gastrointestinal tract, which substantially reduces the amount of butyrate reaching the distal parts of the intestine (Kaczmarek et al., 2016). Butyrate, in its protected form, is gradually released into the gastrointestinal tract, increasing its action throughout the intestine (Ogwuegbu et al., 2021).

The use of sodium butyrate in the diet of broiler chickens has shown positive effects on their intestinal health. This is mainly due to its trophic action, whereby it can increase nutrient absorption area by increasing the height of the villi (Adil et al., 2011; Chamba et al., 2014; Sikandar et al., 2017) and the number of goblet cells (Sikandar et al., 2017), and its ability to control pathogenic microorganisms (Ahsan et al., 2016). Sodium butyrate has been shown to play an important role as an energy source for gastrointestinal epithelial cells and to have antimicrobial, anti-inflammatory, and antioxidant properties (Liu et al., 2014; Song et al., 2017). As a result, improvements are seen in the digestibility of dietary nutrients (Kaczmarek et al., 2016; Riboty et al., 2016) and production performance (Chamba et al., 2014; Riboty et al., 2016; Bortoluzzi et al., 2017; Liu et al., 2019; Lan et al., 2020). In addition, butyrate in its protected form, when released into the duodenum, decreases the pH of the digesta, stimulating pancreatic and bicarbonate secretion, improving nitrogen retention, and nutrient digestibility coefficients of the diet (Ahsan et al., 2016; Kaczmarek et al., 2016).

Aiming at economic savings with the use of sodium butyrate only in the pre-starter and starter phases and considering the importance of the establishment of the microbiota and intestinal development until 21 days of age, this study investigated the performance, carcass and cut yields, digestibility of dietary nutrients, and intestinal histomorphometry of broilers fed diets supplemented with protected sodium butyrate up to 21 days of age.

 

Material and Methods

Two experiments were conducted. All procedures performed were previously approved by the Ethics Committee on Animal Use (CEUA) at the Federal University of Goiás (UFG) (approval no. CEUA/UFG 044/16).

The first experiment was carried out in an industrial shed with dimensions (W χ L) of 12 χ 125 m (1.500 m2), where the environment was controlled by a negative pressure system with the use of misters and evaporative cooling pads for air inlets. A total of 784 one-day-old male broiler chicks of the Cobb 500® commercial line, with an average initial weight of 46 ± 0.2 g were distributed into four treatments in a completely randomized design with seven replicates of 28 birds each. Treatments consisted of a basal diet with the inclusion of a performance-enhancing antibiotic; basal diet without antibiotic or protected sodium butyrate (PSB) (control); basal diet with inclusion of 225 g/t PSB in the pre-starter and starter phases; and basal diet with inclusion of 300 g/t PSB in the pre-starter and starter phases.

The experimental period was 42 days, which were divided into four phases: pre-starter (1 to 7 days), starter (8 to 21 days), grower (22 to 35 days) and finisher (36 to 42 days). The experimental diets were formulated based on maize, soybean meal, and animal-derived meals, in accordance with the recommendations of Rostagno et al. (2017). All diets included a variable portion of 0.165% to include the antibiotic or sodium butyrate and/or inert substance (kaolin), according to the treatments.

In the treatment involving the use of antibiotics, 165 g/t Stafac 100® (10% virginiamycin) was used in all rearing phases, which corresponds to 16.5 g/t virginiamycin. For the treatments with PSB (225 and 300 g/t), the commercial product Adimix® Precision (Nutriad, Groupe Adisseo's), containing 30% sodium butyrate, was used as a source, i.e., 750 and 1,000 g/t of the commercial product was added. The antibiotic and butyrate were added to the feed replacing the inert ingredient (Table 1).

All birds were housed in 28 experimental cages measuring 3.24 m2, at a housing density of 11 birds/m2. The boxes were set up in the central part of the shed and built using PVC pipes and 2-mm plastic mesh screens. Each cage, which housed 28 birds, was equipped with a line of nipple drinkers (10 nipples/cage) and a tube-type chick feeder until the seventh day of age and a tube-type adult poultry feeder from the 8th to the 42nd day of age.

Performance variables (average final weight [AFW], average weight gain [AWG], average feed intake (AFI), feed conversion ratio (FCR) and viability) were measured from 1 to 7, 1 to 21, 1 to 35 and 1 to 42 days of age, whereas the "production factor" was evaluated from 1 to 42 days of age. To this end, the chickens, the feed supplied, and orts were weighed weekly and the number and weight of dead chickens were recorded daily. Average final weight consisted of the average weight of chickens in each plot at the end of each experimental period. Weight gain was calculated as the difference between the final and initial weights of the chickens. Average feed intake was determined as the difference in the weight of the feed supplied and orts in each period, divided by the number of chickens (the number of dead chickens was used as a criterion for correcting intake values). Feed conversion was calculated as the ratio between average feed intake and AWG, which was later corrected for mortality according to Sakomura & Rostagno (2016). Viability was expressed as the percentage of surviving chickens relative to the initial number of housed animals. Finally, the production factor was calculated as an index that considers live weight, viability, age, and feed conversion.

At 42 days of age, two birds that represented the average weight of the plot (± 5%) were selected in each plot, fasted for 8 h, and slaughtered to measure the yields of carcass, breast, drumsticks + thighs, wings, abdominal fat, gizzard, and liver. The yield of the eviscerated carcass without head, neck and feet was calculated relative to the pre-slaughter body weight, as follows:

%CY = (carcass weight*100/live weight), whereas the yield of the carcass parts, namely, breast, drumsticks + thighs, wings and abdominal fat were calculated as a function of carcass weight: %PY = (part weight*100/carcass weight).

The second experiment involved 280 one-day-old male broiler chicks of the Cobb 500® commercial line, with an average initial weight of 46 ± 0.2 g. The birds were distributed into four treatments in a completely randomized design with seven replicates and 10 animals per replicate.

The treatments were the same as in Experiment I, as follows: basal diet with inclusion of a performance-enhancing antibiotic; basal diet without antibiotic or PSB (Control); basal diet with inclusion of 225 g/t PSB in the pre-starter and starter phases; and basal diet with inclusion of 300 g/t PSB in the pre-starter and starter phases. In all rearing phases, 165 g/t Stafac 100® (10% virginiamycin) was used, corresponding to 16.5 ppm virginiamycin. The diets used in Experiment II were the same as those formulated for the pre-starter and starter phases in Experiment I (Table 1).

Two digestibility trials were carried out, in two periods: the first from 4 to 7 days of age, and the second from 18 to 21 days of age. The digestibility coefficients of dietary nutrients and energy were determined using the total excreta collection method, as described by Sibbald & Slinger (1963) and adapted by Sakomura & Rostagno (2016). Feed intake, weight gain, and total excreta produced by the birds were measured throughout the experimental period. Excreta were collected twice daily (08h00 and 16h00) to avoid fermentation.

The chicks were housed in galvanised-wire battery cages with dimensions of 0.25 χ 0.75 χ 0.80 m (H χ W χ L), with mesh floors and equipped with excreta-collection trays and trough-type drinkers and feeders. The battery cages were located in a brick shed with internal dimensions of 12.96 χ 2.96 m (38.36 m2), covered with clay tiles, with concrete flooring and sides with a short wall, screen, and curtains.

Excreta were packed in properly identified plastic bags and stored in a freezer until the end of the collection period. Afterwards, the samples were thawed, homogenised, and aliquoted. Then, they were pre-dried in an air oven at 55 °C, for 72 h. Next, the dry matter was obtained using a rectilinear oven at 105 °C and the nitrogen content was determined using in a nitrogen distiller using the Kjeldahl method (INCT-CA N-001/1), as proposed by Detmann et al. (2012). The 6.25 factor was used to convert the nitrogen value into crude protein, due to the widespread use of this value by nutrition laboratories. Gross energy was determined using a calorimeter. The nutritional composition of the experimental diets was analysed in terms of dry matter, gross energy, and crude protein contents according to the aforementioned methodologies.

Once the results of the chemical analyses of excreta and feed were obtained, the digestibility coefficients of dry matter and crude protein as well as the nitrogen balance were calculated using equations proposed by Sakomura & Rostagno (2016). Apparent metabolizable energy and nitrogen-corrected apparent metabolizable energy were calculated as proposed by Matterson et al. (1965).

At 7 and 21 days of age, one bird that represented the average weight of the plot (± 5%) was selected per replicate, totalling seven birds per treatment. The selected bird was stunned by electronarcosis and later euthanized by cervical dislocation to collect intestinal fragments for a morphometric assessment of the intestinal mucosa. To make the histological slides, 2.0-cm segments of the duodenum (in the distal portion of the duodenal loop) and the jejunum (2.0 cm before the ileal diverticulum) were collected and fixed in a 10% buffered formaldehyde solution for 24 h. After fixation, they were stored in 70% alcohol, processed according to the methodology of Luna (1968), and stained using the Haematoxylin-Eosin method. Semi-serial sections of 5-μm thickness were performed with an electronic rotary microtome.

Images were obtained at 5x magnification, using an optical microscope connected to a computer. The images were analysed using ImageJ software, where 20 villus height and 20 crypt depth measurements were taken in each segment, per replicate. Villus height measurements were taken from the basal region of the villi to their apex and crypt measurements from their base to the villous-crypt transition region (Fukayama et al., 2005). The villus/crypt ratio was calculated by dividing villus height by crypt depth.

All data were checked for the presence of outliers (box-and-whisker plot), homogeneity of variances (Bartlett test), and normality of residuals (Cramér-von Mises). Subsequently, they were subjected to analysis of variance and the means were compared using the SNK test (P <0.05), using R statistical software (2019).

 

Results

In the pre-starter phase (one to seven days of age), the use of PSB in the diet did not influence (P>0.05) broiler performance. However, from 1 to 21 days of age, the inclusion of 225 g/t PSB and the use of the performance-enhancing antibiotic provided higher AFW and AWG (P<0.05), than the control treatment. The chickens fed 225 g/t PSB showed 59-g and 60-g higher AFW and AWG, respectively, than those which received the control treatment (Table 2).

In the evaluation of performance from 1 to 35 days of age (Table 2), the broilers that consumed PSB (225 or 300 g/t) up to 21 days of age had superior AFW and AWG results than the chickens in the control and antibiotic treatment groups (P < 0.05). The diets with 225 and 300 g/t PSB increased AFW by 78 and 56 g and AWG by 80 and 57 g, respectively.

When performance was evaluated for the total period (1 to 42 days of age), the broilers fed the diet supplemented with 225 g/t PSB showed higher AFW and AWG than the control group (P <0.05) but were statistically similar to the group fed 300 g/t PSB and the growth-promoting antibiotic (Table 3). In other words, the supply of 225 g/t PSB up to 21 days of age improved performance until 42 days of age.

There were no differences (P >0.05) between the treatments for the yields of carcass, breast, drumsticks + thighs, wings, abdominal fat, gizzard, or liver at 42 days of age (Table 4). In the period from 4 to 7 days of age, the use of PSB in the diet did not influence (P >0.05) the dietary metabolizable energy content, the digestibility coefficient of crude protein, or nitrogen balance. However, the inclusion of 300 g/t PSB in the diet induced a higher digestibility coefficient of dry matter than 225 g/t (P = 0.0328). The control and antibiotic treatments did not differ from each other or from the treatments with butyrate addition, for these parameters (Table 5). From 18 to 21 days of age, the digestibility coefficients of dry matter and crude protein, nitrogen balance, apparent metabolizable energy, and nitrogen-corrected apparent metabolizable energy did not differ (P >0.05) between the treatment groups (Table 5).

At seven days of age, the broilers supplemented with 300 g/t PSB had the highest duodenal villus height (P <0.001). Jejunal villus height was greater in the chickens supplemented with butyrate (225 and 300 g/t) and the performance-enhancing antibiotic than in those fed control treatment (P <0.001). The broilers supplemented with antibiotic exhibited a higher jejunal crypt depth than those supplemented with 225 g/t PSB (P =0.0097). Villus height/jejunal crypt depth ratio was highest in the broilers supplemented with 225 g/t PSBN (P <0.001) (Table 6).

At 21 days of age, the broilers fed the diet with 225 g/t PSB showed the greatest duodenal villus height (P <0.001). Villus height/crypt depth in the duodenum differed between the groups (P = 0.0146), with the lowest result seen in the antibiotic-treated group, which did not differ from the animals on the 300 g/t butyrate treatment, whereas the control, 225 g/t PSB and 300 g/t PSB treatment groups did not differ from each other. The use of antibiotic or inclusion 225 g/t PSB in the diet provided the greatest jejunal villus height (P <0.001) (Table 6).

 

Discussion

The inclusion of PSB as an additive in the broiler diet until 21 days of age proved to be able to improve final weight and average weight gain from 21 days of age to slaughter age. This result was likely due to the positive effect of butyrate on the development and maintenance of the intestinal epithelium in the early stages of life.

According to Obst & Diamond (1992) the development and maturation of the gastrointestinal tract in the starter phase can substantially affect production performance, since it is correlated with the growth rate of chickens. These processes are also important for the development of other tissues and organs, because it is in this phase that the broilers exhibit rapid development, which is marked by important physiological changes such as intestinal development; development of the thermoregulatory system; beginning of the development of immunocompetence; as well as development of muscle, bone system and fat (Abreu, 2021). The villi are well-developed within 14 days of hatching, whereas the intestine completes its development in the first 20 to 30 days of age (Ito et al., 2004)

Bortoluzzi et al. (2017) reported similar performance results in broilers in the starter phase. The authors found no difference in feed conversion using 700 g/t sodium butyrate, but observed greater weight gain. Ogwuegbu et al. (2021), when evaluating the inclusion of 2 and 4g/kg of partially-protected sodium butyrate in the ration of broiler chickens, also verified an increase in weight gain in relation to chickens in the control group, in the finisher phase of rearing. The authors attributed this result to the increase in nutrient digestibility in chickens that received feed containing sodium butyrate. In contrast, Lan et al. (2020) found no differences in live weight between broilers fed a diet containing a commercial PSB product (54% butyrate) at the product levels of 300 and 600 g/t (162 and 324 g of sodium butyrate/t), and the control group.

The present results show that the PSB level of 225 g/t had a positive effect in the starter phase; however, the 300 g/t level did not differ from the control or antibiotic treatments, which shows that the dose was not adequate for this phase. Similar results were observed by other researchers that used higher doses of sodium butyrate. González-Ortiz et al. (2019) used 1 kg/t of a PSB product (30% butyrate), i.e., 300 g of sodium butyrate/t, and observed a reduction in feed intake and weight gain in broilers in comparison to the control group. Similarly, Lan et al. (2020) evaluated PSB levels and found that the highest level (648 g/t) provided the lowest final weight at 21 days of age. It is suggested that the use of higher rates of butyrate may impair nutrient absorption due to a negative effect of butyrate on the intestinal epithelium. In a study examining the effect of butyrate at different concentrations in an in vitro assay with Caco-2 cells (human colon epithelial cell line), Peng et al. (2007) stated that high concentrations of butyrate have a detrimental effect on the intestinal barrier function, which is related to apoptosis of intestinal epithelial cells by mechanisms not yet fully understood.

In terms of production performance, from 1 to 35 days of age, the use of PSB in the diet (supplied until 21 days of age), at both tested levels (225 and 300 g/t), improved AFW and AWG when compared with the control treatment and the use of antibiotic. Similarly, at 42 days of age, the treatment with 225 g/t PSB provided higher AFW and AWG; however, the treatment with 300 g/t did not differ from the control or antibiotic treatments. Therefore, these results suggest that the PSB level of 225 g/t in the pre-starter (1 to 7 days of age) and starter (8 to 21 days of age) diets was conducive to improved weight gains until 42 days of age.

In the evaluation of carcass and cut yields, there were no effects of PSB at the different tested levels. Similarly, Zhang et al. (2011) used 400 g/t of PSB and found no differences between the treatment with butyrate and the control treatment. The present findings differ from the results described by Panda et al. (2009), who evaluated unprotected butyrate supplementation (200, 400 and 600 g/t) and obtained reduced abdominal fat and increased carcass weight.

The greater duodenal and jejunal villus height seen at 7 and 21 days of age can be explained by the fact that, once ingested, butyrate is converted to butyric acid due to the acidic pH. Butyric acid, in turn, is readily absorbed by enterocytes and used in cellular metabolism as a source of energy, contributing to the growth of villi and, consequently, increasing the area of nutrient absorption by enterocytes (Chamba et al., 2014). Butyrate is able to supply energy to intestinal cells after being transported into the cell, and, in the mitochondria, it is metabolised to Acetyl-CoA, which enters the citric acid cycle, producing ATP and CO2 (Donohoe et al., 2012). According to Kawamata et al. (2007), butyrate ions, in dissociated form, can also be absorbed as an energy source, but are transported by diffusion, by exchange with the bicarbonate ion (HCO3-), or by active transport using membrane transporters (MCT1 and SMCT1).

The improvement in intestinal development can also be explained by the ability of butyrate to reduce the pathogenic microbiota in the intestine, thereby reducing competition with the host for nutrients, epithelial cell desquamation and epithelial turnover, and, consequently, energy and nutrient expenditure for repair (Dibner & Buttin, 2002; Moquet et al., 2016). By reducing the pH of the proventriculus, the gizzard and the upper part of the intestine, butyrate has a bacteriostatic effect, as it favours the growth of lactic acid-producing bacteria, such as Lactobacilli and Bifidobacteria spp., which need an acidic medium to grow (Rolfe, 2000). Lactic acid-producing bacteria compete for space and nutrients with pathogenic bacteria within the intestine, thus reducing the population of pathogenic bacteria. In addition, lactic acid-producing bacteria produce bacteriocins, organic acids and bactericidal substances, maintaining a healthy environment. After sodium butyrate is converted to butyric acid, it is able to enter the bacterial cell wall by diffusion due to its lipid solubility, in a bactericidal effect. Inside the cell, the acid dissociates, lowering the internal pH, which causes toxicity within the bacterial cell. As a consequence, the purine bases are affected, which leads to denaturation of essential enzymes within the cell and bacterial death (Ahsan et al., 2016). Sodium butyrate has been shown to play an important role as an energy source for gastrointestinal epithelial cells and to have antimicrobial, anti-inflammatory and antioxidant properties (Ahsan et al., 2016; Bortoluzzi et al., 2017).

The results found in the histomorphometric evaluation corroborate those reported by Sikandar et al. (2017), where the use of PSB (500 and 1000 g/t) increased the length of duodenal and jejunal villi when compared with control treatment and the treatment including performance-enhancing antibiotics. In contrast with our study, Liu et al. (2019) found no effect of sodium butyrate on the intestinal histomorphometry of broiler chickens up to 21 days of age. Pascual et al. (2020) also observed no effects of using 500 g/t of a PSB product (30% butyrate) on intestinal histomorphometry at 45 days of age.

Although PSB provided an increase in intestinal villus height, butyrate did not improve nutrient digestibility or increase metabolizable energy. This may be due to the lack of challenges in experiment II (use of cages, clean environment, excreta removed frequently), since the positive effects of butyrate can be attributed to a lower pro-inflammatory response when birds experience nutritional, environmental, and immunological challenges (Moquet et al., 2016).

Disagreeing with the present results, Kaczmarek et al. (2016) observed that the use of protected calcium butyrate (300 g/t) increased the ileal digestibility of crude protein and total fat digestibility at 14 days of age, as well as the apparent ileal digestibility of threonine, serine, proline and histidine, and nitrogen-corrected apparent metabolizable energy at 35 days of age. According to the authors, this result may be related to the capacity of butyrate salt to stimulate increased secretion of pancreatic fluid, which, in turn, can improve the digestibility of nutrients and AMEn. Riboty et al. (2016) reported that the use of partially protected sodium butyrate (700 g/t) increased the digestibility coefficients of fat, dry matter and crude protein, apparent metabolizable energy, and nitrogen-corrected apparent metabolizable energy. Liu et al. (2017) found higher ileal digestible energy and energy digestibility coefficients with the use of PSB (500 and 1000 g/t), at 42 days of age, in comparison to the control treatment. Pires et al. (2020) verified that the apparent metabolizable energy and the apparent metabolizable energy corrected for nitrogen increased linearly with increasing protected sodium butyrate levels (0, 105, 210, and 300 g/kg) in the diet of commercial laying hens. According to the authors, the improvement observed may be related to the action of proteginous sodium butyrate in the intestine, stimulating the secretion of pancreatic enzymes, as well as the increase in the height of the duodenum and jejunum villi, favouring the increase in metabolizable energy (AME and AMEn).

The literature may feature discrepant data on the effect of butyrate on performance, nutrient digestibility, and intestinal histomorphometry due to variations between studies, e.g., in terms of animal health status, diet composition, environmental conditions, use of free or protected butyrate, effects of the levels used, and also the matrix used in the coating (Moquet et al., 2016).

The advantage obtained from the use of butyrate in the pre-starter and starter phases is the reduction in expenditure on additives, as it has proven to be efficient when used up to the starter phase and to influence performance until slaughter age.

 

Conclusion

The 225 g/t level of protected sodium butyrate can be used in diets for broilers in the starter rearing phase, since it increases weight gain until slaughter age (42 days) and improves intestinal development at seven and 21 days old.

 

Acknowledgements

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

 

Authors' Contributions

MFP, NSML, and DVJ conceived and designed the experiments. MFP, RANM, SDA, and JMSM performed the experiments. MFP analysed the data. NSML, MBC, and FBC contributed reagents, materials, and analytical tools. MFP and JMSM wrote the paper. JMSM edited the manuscript.

 

Conflicts of Interest Declaration

The authors declare they have no conflicts of interest regarding the work presented in this report.

 

References

Abreu, V.M.N. Manejo inicial e seus reflexos no desempenho do frango. Avicultura Industrial, p. 25-38, 1999.         [ Links ]

Adil, S, Banday, M.T, Bhat, G.A, Qureshi, S.D & Wani, S.A., 2011. Effect of supplemental organic acids on growth performance and gut microbial population of broiler chicken. Live. Res. Rural Dev. 23, 1-8. https://doi.org/10.4061/2010/479485        [ Links ]

Ahsan, U., Cengiz, Raza, I., Kuter, E., Chacher, M.F.A, Iqbal, Z., Umar, S. & Çakir, S., 2016. Sodium butyrate in chicken nutrition: The dynamics of performance, gut microbiota, gut morphology, and immunity. Worlds Poult. Sci. J. 72, 265-278. https://doi.org/10.1017/S0043933916000210        [ Links ]

Bortoluzzi, C., Pedroso, A.A., Mallo, J.J., Puyalto, M., Kim, W.K. & Applegate, T.J., 2017. Sodium butyrate improved performance while modulating the cecal microbiota and regulating the expression of intestinal immune-related genes of broiler chickens. Poult. Sci. 96, 3981-3993. https://doi.org/10.3382/ps/pex218        [ Links ]

Celi, P., Cowieson, A.J., Fru-Nji, F., Steinert, R.E., Kluenter, A.M. & Verlhac, V., 2017. Gastrointestinal functionality in animal nutrition and health: New opportunities for sustainable animal production. Anim. Feed. Sci. Technol. 234, 88-100. https://doi.org/10.1016/j.anifeedsci.2017.09.012        [ Links ]

Chamba, F., Puyalto, M., Ortiz, A., Torrealba, H., Mallo, J.J. & Riboty, R., 2014. Effect of partially protected sodium butyrate on performance, digestive organs, intestinal villi and E. coli development in broilers chickens. Int. J. Poult. Sci.13, 390-396. https://doi.org/10.3923/ijps.2014.390.396        [ Links ]

Cobb-Vantress. 2008. Manual de manejo de frangos de corte Cobb. Cobb-Vantress Brasil, Guapiaçu, São Paulo. Brazil.         [ Links ]

Detmann, E., Souza, M.A., Valadares Filho, S.C., Queiroz, A.C., Berchielli, T.T., Saliba, E.O.S., Cabral, L.S., Pina, D.S., Ladeira, M.M. & Azevedo, J.A.G. 2012. Métodos para análise de alimentos: Instituto Nacional de Ciência e Tecnologia de Ciência Animal. Suprema, Visconde do Rio Branco, Minas Gerais, Brazil.         [ Links ]

Diaz Carrasco, J.M., Casanova, N.A. & Fernández Miyakawa, M.E., 2019. Microbiota, gut health and chicken productivity: What is the connection? Microorganisms. 7, 374. https://doi.org/10.3390/microorganisms7100374        [ Links ]

Dibner, J.J. & Buttin, P., 2002 Use of organic acids as model to study the impact of gut microflora on nutrition and metabolism. J. Appl. Poult. Res. 11, 453-463. https://doi.org/10.1093/japr/11.4.453        [ Links ]

Donohoe, D.R., Collins, L.B., Wali, A., Bigler, R., Sun, W. & Bultman, S.J.,2012. The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol. Cell. 48, 612-626. https://doi.org/10.1016/j.molcel.2012.08.033        [ Links ]

Fukayama, E.H., Bertechini, A.G., Geraldo, A., Kato, R.K. & Murgas, L.D.S., 2005. Extrato de orégano como aditivo em rações para frangos de corte. Rev. Bras. Zootec. 34, 2316-2326. http://dx.doi.org/10.1590/S1516-35982005000700018.         [ Links ]

González-Ortiz, G., Santos, T.T., Vienola, K., Vartiainen, S., Apajalahti, J. & Bedford, M.R., 2019. Response of broiler chickens to xylanase and butyrate supplementation. Poult Sci., 98, 3914-3925. https://doi.org/10.3382/ps/pex092        [ Links ]

Graham Solomons, T.W. & Frylhe, C.B., 2011. Organic Chemistry. John Wiley & Sons, Hoboken, New Jersey.         [ Links ]

Huyghebaert, G., Ducatelle, R. & Van Immerseel, F., 2011. An update on alternatives to antimicrobial growth promoters for broilers. T. Vet. J., 187, 182-188. https://doi.org/10.1016/jtyjl.2010.03.003        [ Links ]

Ito, N.M.K., Miaji, C.I., Lima, A.E. & Okabahashi, S., 2004. Saúde gastrointestinal, manejos e medidas para controlar as enfermidades gastrointestinais. In: Mendes, A.A., Nääs, I.A. & Macari, M. Produção de frangos de corte. Campinas, Facta. pp.207-215.         [ Links ]

Kaczmarek, S.A., Barri, A., Hejdysz, M. & Rutkowski, A., 2016. Effect of different doses of coated butyric acid on growth performance and energy utilization in broilers. Poult. Sci. 95, 851-859. https://doi.org/10.3382/ps/pev382        [ Links ]

Kawamata, K., Hayashi, H. & Suzuki, Y., 2007. Propionate absorption associated with bicarbonate secretion in vitro in the mouse cecum. Pflügers. Archiv. 454, 253-262. https://doi.org/10.1007/s00424-006-0200-4        [ Links ]

Lan, R., Zhao, Z., Li, S. & Na, L., 2020. Sodium butyrate as an effective feed additive to improve performance, liver function, and meat quality in broilers under hot climatic conditions. Poult. Sci. 11, 5491-5500. https://doi.org/10.1016/j.psj.2020.06.042        [ Links ]

Liu, J. D., Bayir, H. O., Cosby, D. E., Cox, N. A., Williams S. M, & Fowler, J., 2017. Evaluation of encapsulated sodium butyrate on growth performance, energy digestibility, gut development, and Salmonella colonization in broilers. Poult. Sci. 96, 638-3644. http://dx.doi.org/10.3382/ps/pex174        [ Links ]

Liu, J.D., Lumpkins, B., Mathis, G., Williams, S.M. & Fowler, J.,2019. Evaluation of encapsulated sodium butyrate with varying releasing times on growth performance and necrotic enteritis mitigation in broilers. Poult. Sci. 98, 3240-3245. http://doi.org/10.2282/ps/pez049        [ Links ]

Liu, W., Yang, Y., Zhang, J., Gatlin, DM., Ring0, E. & Zhou, Z., 2014. Effects of dietary microencapsulated sodium butyrate on growth, intestinal mucosal morphology, immune response, and adhesive bacteria in juvenile common carp (Cyprinus carpio) pre-fed with or without oxidised oil. Br. J. Nutr. 112, 15-29. https://doi.org/10.1017/S0007114514000610        [ Links ]

Luna, L.G., 1968. Manual of Histologic. Staining Methods of the Armed Forces. Institute of Pathology. McGraw-Hill, New York, United States of America.         [ Links ]

Matterson, L.D., Potter, L.M., Stutz, M.W. & Singsen, E.P., 1965. The metabolizable energy of feeds ingredients for chickens. Research Report, Storrs, Connecticut, The University of Connecticut, Agricultural Experiment Station.         [ Links ]

Moquet, P.C.A., Onrust, L., Van Immerseel, F., Ducatelle, R., Hendriks, W.H. & Kwakkel, R.P., 2016. Importance of release location on the mode of action of butyrate derivatives in the avian gastrointestinal tract. Worlds Poult. Sci. J. 72, 61-80. https://doi.org/10.1017/S004393391500269X        [ Links ]

Obst, B.S. & Diamond, J., 1992. Ontogenesis of intestinal nutrient transport in domestic chickens (Gallus gallus) and its relation to growth. Auk. 109, 451-64. https://doi.org/10.1093/auk/109.3.451        [ Links ]

Ogwuegbu, M.C., Oyeagu, C.E., Edeh, H.O., Dim, C.E., Ani, A.O. & Lewu F.B., 2021. Effects of sodium butyrate and rosemary leaf meal on general performance, carcass traits, organ sizes, and nutrient digestibility of broiler chickens. Iranian J. Appl. Anim. Sci., 11, 365-379. https://doi.org/10.1590/S1516-635X2013000300003        [ Links ]

Oviedo-Rondón, E.O., 2019. Holistic view of intestinal health in poultry. Anim. Feed. Sci. Technol. 250, 1-8. https://doi.org/10.1016/j.anifeedsci.2019.01.009        [ Links ]

Panda, A.K., Rao, S.V.R., Raju, M.V.L.N. & Sunder, C.S., 2009. Effect of butyric acid on performance, gastrointestinal tract health, and carcass characteristics in broiler chickens. Asian Australias. J. Anim. Sci. 22, 1026-1031. https://doi.org/10.5713/ajas.2009.80298        [ Links ]

Pascual, A., Trocino, A., Birolo, M., Cardazzo, B., Bordignon, F., Ballarin, C., Carraro, L. & Xiccato, G., 2020. Dietary supplementation with sodium butyrate: Growth, gut response at different ages, and meat quality of female and male broiler chickens. Ital. J. Anim. Sci. 19, 1134-1145. https://doi.org/10.1080/1828051X.2020.1824590        [ Links ]

Peng, L., He, Z., Chen, W., Holzman, I.R. & Lin, J., 2007. Effects of butyrate on intestinal barrier function in a CACO-2 cell monolayer model of intestinal barrier. Pediatr. Res. 61, 37-41. https://doi.org/10.1203/01.pdr.0000250014.92242.f3        [ Links ]

Picker, L., Hayashi, R.M., Lourenço, M.C., Miglino, L.B., Caron, L.F., Beirão, B.C.B., Silva, A.V.F. & Santin, E., 2012. Avaliação microbiológica, histológica e imunológica de frangos de corte desafiados com Salmonella enteritidis e Minnesota e tratados com ácidos orgânicos. Rer. Vet. Bras. 32, 27-36. https://doi.org/10.1590/S0100-736X2012000100006        [ Links ]

Pires, M. F., Leandro, N. S. M., Oliveira, H. F., Jacob, D. V., Carvalho, F. B., Stringhini, J. H., Carvalho, D. P. & Andrade, C. L., 2020. Effect of dietary inclusion of protected sodium butyrate on the digestibility and intestinal histomorphometry of commercial laying hens. Braz. J. Poultry Sci. 23, 001-008. http://dx.doi.org/10.1590/1806-9061-2020-1406        [ Links ]

R Core Team. 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.         [ Links ]

Riboty, R., Chamba, F., Puyalto, M. & Mallo, J.J., 2016. Effect of partially-protected sodium butyrate and virginiamycin on nutrient digestibility, metabolizable energy, serum metabolites, and performance of broiler chickens. Int. J. Poult. Sci. 15, 304-312. http://doi.org/10.3923/ijps.2016.304.312        [ Links ]

Rolfe, R. D., 2000. The role of probiotic cultures in the control of gastrointestinal health. J. Nutr. 130, 396S-402S. https://doi.org/10.1093/jn/130.2.396S        [ Links ]

Rostagno, H.S., Albino, L.F.T., Hannas, M.I., Donzele, J.L., Sakomura, N.K., Perazzo, F.G., Saraiva, A., Abreu, M.L.T., Rodrigues, P.B., Oliveira, R.F., Barreto, S.L.T. & Brito, C.O., 2017. Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais. Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brasil.         [ Links ]

Sakomura, N.K. & Rostagno, H.S., 2016. Métodos de pesquisa em nutrição de monogástricos. Funep, Jaboticabal, São Paulo,Brasil.         [ Links ]

Sibbald, I.R. & Slinger, S.J., 1963. A Biological assay for metabolizable energy in poultry feed ingredients together with findings which demonstrate some of the problems associated with the evaluation of fats. Poult. Sci. 42, 313-325. https://doi.org/10.3382/ps.0420313.         [ Links ]

Sikandar, A., Zaneb, H., Younus, M., Masood, S., Aslam, A., Khattak, F., Ashraf, S., Yousaf, M.S. & Rehman, H., 2017. Effect of sodium butyrate on performance, immune status, microarchitecture of small intestinal mucosa and lymphoid organs in broiler chickens. Asian Australas. J. Anim. Sci. 30, 690-699.https://doi.org/10.5713/ajas.16.0824        [ Links ]

Song, B., Li, H., Wu, Y., Zhen, W., Wang, Z., Xia, Z. & Guo, Y., 2017. Effect of microencapsulated sodium butyrate dietary supplementation on growth performance and intestinal barrier function of broiler chickens infected with necrotic enteritis. Anim. Feed. Sci. Tech. 232, 6-15. https://doi.org/10.1016/j.anifeedsci.2017.07.009        [ Links ]

Zhang, W. H., Jiang, Y., Zhu, Q.F., Gao, D.F., Dai, S.F., Chen, J. & Zhou, G.H., 2011. Sodium butyrate maintains growth performance by regulating the immune response in broiler chickens. Br. Poult. Sci. 52, 292-301. https://doi.org/10.1080/00071668.2011.578121        [ Links ]

 

 

Submitted 26 July 2021
Accepted 4 November 2021
Published January 2023

 

 

# Corresponding author: raianazoo@hotmail.com

Creative Commons License Todo o conteúdo deste periódico, exceto onde está identificado, está licenciado sob uma Licença Creative Commons