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Prebiotics and butyric acid can replace colistin as a promoter of growth for nursery piglets

INTRODUCTION
In intensive pig farming, post-weaning challenges are usually associated with immaturity of the gastrointestinal tract and low immunocompetence, which results in poor functioning of the intestinal barrier and predisposition to diarrhea, thus impairing piglet performance (Jayaraman and Nyachoti, 2017). To minimize such damage, antibiotic growth promoters (GPA) have often been used at subtherapeutic doses in feed for years, with effective results in reducing populations of pathogenic microorganisms that adhere to the intestinal mucosa and subsequent reduction in toxin production and improved performance. animal (gavioli et al., 2013; liu et al., 2018). Among the various antibiotics available for this purpose, colistin, whose action is selective for Gram-negative enteric bacilli, particularly E. coli., is one of the most effective molecules used in pig farming (Mendes and Burdmann, 2009). However, given the recent identification of human resistance to the antibiotic, its use as GPA was banned worldwide. The consequences of removing colistin from swine production, associated with the restriction of other GPA, have driven industry interest in recent years for the use of alternative additives. Of the many actions that prebiotics have on weaned piglets, modulation of the beneficial microbiota in the gastrointestinal tract stands out. These agents use prebiotics as a substrate for their development in place of pathogenic microorganisms (Hustkins et al., 2016), which improves nutrient use, reduces the incidence of diarrhea, and increases weight gain and feed efficiency (Silva and Nornberg, 2003). As for butyric acid, its antimicrobial action (Biagi et al., 2007) and its role in increasing the production of short-chain fatty acids stand out. Such actions contribute to lower intestinal pH and reduce the ability of pathogens to colonize the intestine, in addition to providing energy for enterocytes, thus favoring the renewal of the intestinal mucosa (Liu et al., 2018). However, the multifactorial nature of weaning-related actions associated with the variety of prebiotics and acidifiers available, as well as the conditions under which they are used in the face of		the principles and the different doses and periods of use employed, must be seen as variables that may result in inconsistent responses to these additives when compared to GPAs. This study aimed to evaluate dietary supplementation with different prebiotic additives at different concentrations in addition to sodium butyrate on the performance of piglets in the nursery phase, diarrhea control and volatile fatty acid (VFA) profile in the cecum, in order to replace colistin as growth promoter.

MATERIAL AND METHODS
All procedures adopted in this research were previously reviewed and approved by the Ethics Committee in Research and Animal Experimentation of Akei Animal Research under protocol no. 013/2018.

  One hundred and twenty Agroceres PIC piglets (60 piglets and 60 gilts) weaned at 22 days of age with average initial weight of 5.475 ± 0.719 kg were evaluated during 42 days (22 to 64 days of age). The piglets were assigned to random blocks according to their weight and sex and submitted to six treatments with six repetitions each (three piglets of the same sex per pen represented the experimental unit). The treatments corresponded to the use of the following dietary additives: T1) colistin (40ppm); T2) β-glucans/mannanoligosaccharides (0.2%); T3) calcium butyrate (0.1%); T4) β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.01%) + galactooligosaccharides (0.09%); T5) β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.03%) + galactooligosaccharides (0.07%); and T6) β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.05%) + galactooligosaccharides (0.05%). The animals were housed in masonry pens measuring 2.55 m2 with a fully slatted floor, nipple drinkers and linear drinkers. The pens were heated with 200 W infrared lamps placed in the center of the pens 0.70 m above the ground and the barn curtains were also managed for temperature control. The experimental diets were isonutritive and isoenergetic and were prepared following the

Prebiotics and butyrics…

minimum recommendations by Rostagno et al🇧🇷 (2011) split into three phases: pre-initial I, pre-initial II, and initial (Table 1). The ration wasproportionate ad libitum and the animals had free access to water.

Table 1. Composition and calculated nutritional and energy values of experimental diets for piglets in the nursery phase

IngredientsPre-initial IPre-initial IIInitial
Corn 7%55,10362,62168,239
Soy Flour 47%22,00025,00028,300
Star Pro 25 (Auster)5,0002,000 
Prius L70 (Auster)10,9724,388–
Extruded soybean 36%2,6002,000 
Calcitic file 38%0,7501,1501,500
Dicalcium Phosphate 18%0,3000,3500,350
table salt0,4400,4600,480
L-lysine0,4700,3700,230
DL-Methionine0,1400,0900,010
L-threonine0,1750,1050,025
L-tryptophan0,030––
L-Valine 96.5%0,1500,050 
Choline Chloride 60%0,0470,0380,032
Phytase (50 g/ton)0,0050,0050,005
antioxidant0,0100,0100,010
Vitamin premix10,1500,1500,150
mineral premix20,1000,1000,100
Inert (kaolin or treatments3)1,5561,1111,136
Nutrients   
Moisture, %10,59611,56212,304
Metabolizable energy (kcal/kg)3,3653,2743,207
Crude protein, %18,50018,50018,500
Ether Extract, %2,4212,4162,137
Crude fiber, %2,6042,8973,069
Mineral matter, %4,5914,4454,402
Lactose, %9,7603,904 
Calcium, %0,6500,7540,846
Total Phosphorus, %0,4810,4490,413
Phosphor available, %0,4000,3460,296
Sodium, %0,2980,2480,218
Electrolyte balance, mEq/kg174,103175,067179,736
Digestible lysine, %1,2491,1481,028
Digestible methionine + cysteine, %0,6870,6390,564
Digestible tryptophan, %0,2130,1900,195
Digestible Trionine, %0,7490,6900,620

1levels per kg of vitamin premix: vitamin A (min.) 6,000 IU; vitamin D3 (min.) 1,500 IU; vitamin E (min.) 15,000mg; vitamin K3 (min.) 1,500mg; vitamin B1 (min.) 1,350mg; vitamin B2 4,000mg; vitamin B6 2,000mg; vitamin B12 (min.) 20mg; niacin (min.) 20,000mg; pantothenic acid (min.) 9,350mg; folic acid (min.) 600mg; biotin (min.) 80mg; selenium (min.) 300mg.

2levels per kg of mineral mixture: iron (min) 100mg; copper (min) 10mg; manganese (min) 40 g; cobalt (min) 1,000mg; zinc (min) 100mg; iodine (min) 1,500mg.

3 T1) colistin (40ppm); T2) β-glucans/mannanoligosaccharides (0.2%); T3) calcium butyrate (0.1%); T4) β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.01%) + galactooligosaccharides (0.09%); T5) β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.03%) + galactooligosaccharides (0.07%); and T6) β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.05%) + galactooligosaccharides (0.05%);(5: 5)

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Daily feed intake, daily weight gain and feed conversion were evaluated for each phase and throughout the study period. The incidence and intensity of diarrhea were evaluated throughout the experiment, according to Vassalo et al. (1997) and were classified as stools with regular consistency (0), soft stools (1), pasty stools (2), and watery stools (3). Results 0 and 1 meant that the feces were not considered as diarrhea, contrary to results 2 and 3. At the end of the experimental period (at 64 days of age), six animals from each treatment were slaughtered (chosen based on their average weight of the enclosure) and its cecum content was collected to determine the profile of short-chain volatile fatty acids (acetic, butyric and propionic) according to Erwin et al. (1961) using gas chromatography (FOCUS GC; Thermo Scientific – equipped with a glass column 3 m long and 0.25 m in diameter packed with 80/100 – Carbopack B-DA/4% Carbowax 20W).Data were subjected to analysis of variance and means were compared by Tukey's test using the statistical software R version 3.5.0. The chi-square test was used for non-parametric data. Both tests used an α of 0.05 as a significance threshold, which indicated trends when its value was below 0.10.

RESULTS AND DISCUSSION
No difference was found between treatments for any performance parameters in any of the evaluated phases or during the total experimental period (Table 2). This indicates that, regardless of the adopted program, the alternative additives to colistin acted positively and were in line with the GPA replacement trends. The results were similar to those reported by Luna et al. (2015), who, when working with piglets in the nursery phase fed diets supplemented with mannan oligosaccharides (0.33 and 1.83g/kg of feed), β-glucan (0.5g/kg of feed), and colistin ( 0.25g/kg feed), found no influence on weight gain, feed intake, or feed conversion between treatments.

Table 2. Average values of daily feed intake (DFI), daily weight gain (DWG), and feed conversion (FC) for nursery piglets, according to experimental treatments

Parameters (kg) Treatments 
T1T2T3T4T5T6CV (%)P-value
Pre-Start Phase I
DFI0,2220,2100,2120,2090,2170,1999,950,695
DWG0,1600,1470,1530,1450,1050,18247,700,517
FC1,5491,7461,8591,9411,6801,22752,970,821
initial phase II
DFI0,3910,3810,3720,3940,3740,36014,610,442
DWG0,2730,2720,2370,2700,2470,24729,180,592
FC1,5181,4871,6881,9941,5261,52923,700,139
Early stage        
DFI0,7800,7370,7500,7120,7210,75813,960,840
DWG0,3800,3460,3340,3450,3380,33623,380,897
FC2,1612,1212,2792,2322,1472,28215,800,919
Total        
DFI0,4630,4450,4450,4390,4370,43910,920,932
DWG0,2600,2490,2470,2290,2280,24820,130,809
FC1,8421,7861,9361,9901,9311,86214,290,751

T1) colistin (40 ppm); T2) β-glucans/mannanoligosaccharides (0.2%); T3) calcium butyrate (0.1%); T4) β-

glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.01%) + galactooligosaccharides (0.09%); T5) β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.03%) + galactooligosaccharides (0.07%); and T6) β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.05%) + galactooligosaccharides (0.05%).

Investigations into alternative additives to GPAs have been recurrent in recent years. saints et al🇧🇷 (2010), when working with different dietary levels of mannanoligosaccharides (0.25%, 0.50% and 0.75%),compared to diets supplemented with neomycin sulfate (56 ppm), found no distinct advantage (P>0.05) between treatments. Visentini et al🇧🇷 (2008), when using fructooligosaccharides  

Prebiotics and butyrics…

(0.2%), and Park et al🇧🇷 (2018), when evaluating different levels of β-glucan (0.1, 0.2 and 0.4%) versus tiamulin (30 ppm), also found no difference in performance between treatments for piglets in the nursery phase. An effect similar to that observed for the group treated with colistin was observed for butyrate, probably due to the increase in nutrient digestibility and better bioavailability of amino acids that this additive provides, as discussed by Moquet et al. (2017). Most studies with sodium butyrate have been carried out with farmed animals and have obtained several positive performance results, particularly in weight gain, as reported by Chiofalo et al. (2014) using doses of 440 ppm and by Hanczakowska et al. (2014) when using 3,000 ppm. However, the contradiction in the results of some studies that used butyrate may be related to the composition of the diet and the state of maturity of the intestines of the piglets (Biagi et al., 2007). Controversies regarding performance results when using prebiotics compared to GPAs, with advantages for the latter (Visentini et al., 2008; saints et al., 2010) are considered relatively common, particularly in cases where conditions of high sanitary challenge are found (Gebbink et al., 1999). However, some results contradict this, which allows us to infer that the bactericidal/bacteriostatic action of some GPAs against bacteria in the gastrointestinal tract may compromise the balance of this microbiome and, in some cases, lead to an increase in epithelial desquamation and a worse villus/crit ratio. (gavioli et al., 2013).GPAs can also compromise the fermentative efficiency of the intestinal microbiota, responsible for the production of VFAs, which represent an important source of energy for enterocyte rotation (Lin and Visek, 1991). On the other hand, particularly in the first weeks post-weaning, feed intake is low, in part due to the immature digestive system, which impairs the immune system and performance and increases the proliferation of diarrhea-causing bacteria (Jayaraman and Nyachoti, 2017). Prebiotics and acids have roles that are closely related to this scenario, minimizing the damage inherent to this critical stage in case of immaturity of the gastrointestinal tract (Biagi et al., 2007) and the immune system (Wu et al., 2017), thus increasing the use of nutrients (Silva and Nornberg, 2003). For incidence and intensity of diarrhea (Table 3), results for scores 2, 3, and total incidence (2+3) indicated that treatments with alternative additives (T2, T3, T4, T5, and T6) had significant effects. similar to those of the group treated with colistin. However, for score 3, the animals in groups T4 and T6, respectively β-glucan/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.01%) + galactooligosaccharides (0.09%) and β-glucan/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.05%) + galactooligosaccharides (0.05%) had better results than the other treatments. Adversely, T5, which contained the same prebiotic additive as T4 and T6, i.e. β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.03%) + galactooligosaccharides (0.07%), but a different proportion of prebiotic additive, did not have the same behavior as these groups.  

Table 3. Percentages of diarrhea for piglets in the nursery phase, according to the experimental treatments

TreatmentsGrades Fecal score (%) 
Grade IIGrade IIIGrades II + III
T188236b27b63b
T288242b24b66b
T388233ba20b53b
T488227ba11 to38 to
T588241b38b79b
T688223rd17 to40 to

T1) colistin (40 ppm); T2) β-glucans/mannanoligosaccharides (0.2%); T3) calcium butyrate (0.1%); T4) β-

glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.01%) + galactooligosaccharides (0.09%); T5) β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.03%) + galactooligosaccharides (0.07%); and T6) β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.05%) + galactooligosaccharides (0.05%).

a,b differences according to the chi-square test (P<0.05)

Silva et al.

The results match those reported by Grela et al. (2006), who, when evaluating the frequency of diarrhea in piglets from birth to 84 days of age, found that the addition of 3,000mg/kg and 5,000mg/kg of mannan-oligosaccharide and fructo-oligosaccharide, respectively, decreased the incidence of diarrhea. Such results are attributed to the possible improvement of the immune system and the integrity of the epithelium (Wu et al., 2017) and correspond to the findings of Budiño et al. (2010), Assisi et al🇧🇷 (2014), and Moon et al🇧🇷 (2015), who used fructooligosaccharides, mannanoligosaccharides and β-glucans + mannanoligosaccharides versus GPA respectively, and found no differences between treatments. Prebiotics can induce metabolic processes that are beneficial to the health of the host ecosystem due to the easy degradation of links in the structure of fructooligosaccharides and galactooligosaccharides by certain enzymes, such as β-fructosidase and β-galactosidase, commonly associated with beneficial bacteria of the genus Bifidobacterium (Markowiakautor and Śliżewska, 2018), which feed on these sugars, multiply and colonize the tract. In this line, the use of mannanoligosaccharides has been recommended, as it reduces colonization by pathogenic bacteria and, consequently, the incidence of post-weaning diarrhea (Silva and Nörnberg, 2003). The presence of fructooligosaccharides also improves the condition of the intestinal wall (villi), which increases the absorption capacity (Budinõ et al., 2010). kotunia et al🇧🇷 (2004) supplemented two-week-old piglet diets with butyrate (3,000mg/kg feed) for seven days and found increases in villus height, crypt depth, and mucosal thickness of the jejunum and ileum compared to animals that were not fed. fed with supplementation. Mazzoni et al🇧🇷 (2008), when supplementing the diet of piglets with sodium butyrate (3,000 mg/kg) before (4 to 28 days of age) and after weaning (29 to 40 days of age), observed an increase in positive parietal cells, enteroendocrines and somatostatins, which increased the gastric mucosa. The consequences were less intestinal damage and fewer cases of diarrhea. On the other hand, unprotected butyrate may have limited action in this segment of the intestine, as it may experience high absorption in the upper parts of the gastrointestinal tract (Piva et al., 2007). A significant difference in cecal fatty acids (Tab. 4) was found for propionic acid profile and total fatty acids (acetic, butyric and propionic). For propionic acid, T3, T5, and T6, respectively, β-glucan/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.03%) + galactooligosaccharides (0.07%) and β-glucan/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.051 TP3T) + galactooligosaccharides (0.05%), were better than the control treatment (40 ppm colistin) and did not differ (P>0.05) from the other treatments.

Table 4. Mean values of fatty acids in the cecum of piglets at 64 days of age, according to the experimental treatments

TreatmentsButyric (%)Acetic (%)Propionic (%)Total (%)
T10,130,320.23b0.67b
T20,140,360.29ab0.79ab
T30,180,380.32 to0.87ab
T40,290,370.31ab0.97 to
T50,160,350.36 to0.87ab
T60,170,380.37 to0.93ab
P-value0,2880,4570,0010,050
CV (%)73,9117,7020,6421,39

T1) colistin (40ppm); T2) β-glucans/mannanoligosaccharides (0.2%); T3) calcium butyrate (0.1%); T4) β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.01%) + galactooligosaccharides (0.09%); T5) β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.03%) + galactooligosaccharides (0.07%); and T6) β-glucans/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.05%) + galactooligosaccharides (0.05%).

a,b differences according to the chi-square test (P<0.1).

Prebiotics and butyrics…

A difference was found in the fatty acid profile between T4 (β-glucan/mannanoligosaccharides (0.1%) + fructooligosaccharides (0.01%) + galactooligosaccharides (0.09%) and control, with advantages for the former. combinations of β-glucans/mannanoligosaccharides with fructooligosaccharides + galactooligosaccharides in improving the fatty acid profile in the cecum, which is actually comparable to the use of butyrate Dietary supplementation with organic acids, including butyrate, classically modulates the VFAs profile in the cecum, as noted by Callegari et al. (2016), who found that, regardless of the combination of acids and their presentation – whether encapsulated or as salt – in the cecum, acetic, butyric and propionic acids, when present in larger amounts than in the control group (without fatty acid supplementation ). It can also be observed that the results found for the group treated with butyrate had a VFA production scenario similar to that obtained by Mallo et al. (2012), who observed a higher concentration of butyric acid in the colon when evaluating the effects of adding encapsulated sodium butyrate and butyric acid monoglyceride to the diet of piglets weaned at 21 days of age. These results are attributed to changes in the microbial population in the small and large intestines, which favors the survival of lactic acid bacteria and reduces the population of pathogenic bacteria (Michiels et al., 2009), which impacts the VFA profile. The results obtained in the increase of VFA through the action of prebiotics also correspond to the results of Wu et al. (2017), who, by adding isomaltooligosaccharides (6g/kg) to the diet of piglets between 21 and 49 days of age, reported a significant increase in the content of total fatty acids in the cecum and colon compared to the control group. As discussed, prebiotics favor the production of short-chain fatty acids in the cecum, which, in turn, promote epithelial cell proliferation and differentiation (Liu et al., 2018). The greater production of short-chain fatty acids (acetic, propionic and butyric) inhibits the development of pathogens through the reduction of the intestinal pH, which makes the environment unsuitable for the multiplication of pathogens, or through the direct effect of the acids on E. coli., Clostridium spp. and Salmonella sp., thus resulting in better digestive enzyme activity, nutrient use in the feed, and intestinal health (Rodrigues et al., 2017). Alternative treatments led to results similar to those of colistin, although with better results in controlling diarrhea, particularly at T4 and T5, and better rates of VFA production, which indicates its benefit and safety for the consumer by avoiding the risks of inducing resistance bacteria to colistin.CONCLUSION
The supplementation of different compositions and concentrations of prebiotics and butyric acid in the diet of nursery piglets proved to be feasible for animal performance and correctly replaces colistin as a growth promoter, in addition to having positive effects on the control of diarrhea and on the production of volatile fatty acids in the cecum.

THANKS
The authors wish to thank the company Yes Sinergy for their technical support.

REFERENCES
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