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The effect of synbiotic (inulin extracted from gembili tuber and Lactobacillus plantarum) on growth performance, intestinal ecology and haematological indices of broiler chicken

Sri Setyaningrum1,2, Vitus D Yunianto1, Dwi Sunarti1 and Luthfi D Mahfudz1

1 Faculty of Animal and Agricultural Sciences, Diponegoro-University, Semarang, Central Java, Indonesia
inditik@yahoo.com
2 Faculty of Sciences and Technology, University of Pembangunan Panca Budi, Medan, North Sumatera, Indonesia

Abstract

The objective of this study was to examine the effect of synbiotic (inulin extracted from gembili tuber and Lactobacillus plantarum on growth performance, intestinal ecology and haematological indices of broiler chicken. The material used was 144 unsexed broilers at 1 d of age with an average body weight of 45.7 1.52 g. The study was designed based on a completely randomized design with 4 treatments and 6 replications, each experimental unit contained 6 broiler chickens. These treatments included SB0 = 0 ml/100g of feed, SB1 = 1 ml/100 g of feed, SB2 = 2 ml/100 g of feed and SB3 = 3 ml/100 g of feed. The parameters observed were growth performance, protein digestibility, microbial population, intestinal morphology, immune organ and haematological parameters. The results showed that supplementation of synbiotic increased (p <0.05) the growth performance, protein digestibility, total lactic acid bacteria, villi height and ratio of villi height to crypt depth and decreasing the caecum pH and total coliform. However the treatment did not affect (p> 0.05) the ileum pH, crypt depth, immune organ and haematological parameters. In conclusion, supplementation of synbiotic (inulin extracted from gembili tuber and Lactobacillus plantarum) improved growth performance, protein digestibility and intestinal ecology of broiler chicken.

Keywords: broiler, Dioscorea esculenta, gut microbial, probiotic


Introduction

The utilization of antibiotic growth promoters (AGP) is generally used to suppress the growth of pathogenic bacteria in the gut, thereby reducing damage of villi (Huygghebaert et al 2011). However, the use of AGP is currently banned, because the application of AGP results in antibiotic resistance to livestock and humans (Isroli et al 2017), residues in livestock products, and imbalances in the intestinal microflora (Sugiharto 2016). One of the alternatives to replace AGP is synbiotics which is the combination of probiotic and prebiotic.

Probiotics are living microorganisms that maintain a balance of microflora in the digestive tract, increase stimulation of enzyme secretions, produce vitamins or antimicrobial and immune systems in the host (Hassanpour et al 2013). The commonly used of probiotic is Lactobacillus plantarum. Peng et al (2016) stated that the use of Lactobacillus plantarum B1 had a positive effect on the growth of broiler chickens, reduced the content of Escherichia coli in the caecum, and increased the of lactic acid bacteria in the caecum and ileum.

Prebiotics are a source of energy for microbes in the intestine and bacterial substrate for fermentation in the caecum that can stimulate the activity and growth of beneficial bacteria and inhibit the growth of bacterial pathogens (Alloui et al 2013). The inulin is one of prebiotic that was most widely used. Inulin is a fructan polymer connected by glycosidic β-2-1 bonds (Kelly, 2008), which is produced by many plants. One plant that has a high inulin content is gembili tuber (Dioscorea esculenta). The inulin content in gembili tuber is about 14.77% (Winarti et al 2011). The study by Zubaidah and Akhadiana (2013) reported that inulin from gembili tuber can support the growth of Lactobacillus plantarum.

In this current study, synbiotic was prepared from the inulin extracted from gembili tuber in combination with Lactobacillus plantarum. To best of knowledge, such synbiotic product has never been used in poultry. Therefore, we expected that such product could beneficially affect the health and growth of broiler chicken that was formerly played by AGP. Our preliminary study showed that the inulin extracted from gembili tuber was beneficially affect the growth and stability of Lactobacillus plantarum when tested against acid, bile salts, heat, and feed tolerance (unpublished data). The objective of this study was to examine the effect of synbiotic (inulin extracted from gembili tuber and Lactobacillus plantarum) on growth performance, intestinal ecology and haematological indices of broiler chicken.


Materials and Methods

Synbiotic preparation

Synbiotic preparation had begun with the extraction of inulin from gembili tuber based on Caleffi et al (2015) with some modification. Gembili tuber of 9 months old were peeled, sliced, dried and ground for the extraction of inulin. To extract the inulin, gembili tuber was added with hot water (90 C; 1:15), heated for 1 hours in waterbath 80 C, cooled and filtered. The filtrate was then precipitated with 40% concentration of ethanol (1:2.5), frozen for 6 hours, thawed, centrifuged at 5000 rpm for 5 minutes. The inulin obtained was dried and ground into powder.

The synbiotic product was prepared by mixing of 7 g / 100 ml of gembili tuber extract and 10 ml of Lactobacillus plantarum (InaCC B76; 1 x 109 cfu / ml) and incubated anaerobically for 24 hours at 37C.

In vivo study

The material used in the present study was 144 unsexed broiler chicken at 1 d of age with an average body weight of 45.7 g 1.52 g. The chick were purchased from a commercial hatchery and reared for 42 days. Broiler chickens were reared in litter-bedded pens (1 x 1 m) equipped with feeders and drinkers. During the research, the feed and water were provided ad libitum. The treatment was supplementation of synbiotic (combination of inulin extracted from gembili tubers and Lactobacillus plantarum) as follows SB0 = 0 ml/100g of feed, SB1 = 1 ml/100 g of feed, SB2 = 2 ml/100 g of feed and SB3 = 3 ml/100 g of feed. Basal diet was formulated according to the recommendation of NRC (1994). Basal diet composition is presented in Table 1.

Growth performance

The treatment began on d 1, where all chicken were weighed individually to determine the initial weight and then their body weight gain was recorded at weekly intervals. The feed intake was also recorded weekly. The feed conversion ratio was calculated based on the ratio between feed consumption and body weight gain.

Table 1. Basal diet composition
Ingredient %
Corn 48
Rice bran 12.9
Soy bean meal 28
Meat bone meal 10.8
Mix mineral1 0.3
Amount 100
Nutrient Content
Metabolizable Energy (kkal/kg) 3038
Crude protein (%) 22.1
Crude ether extract (%) 3.53
Crude fiber (%) 5.19
Calcium (%) 1.07
Phosphorus (%) 0.68
Arginine (%) 1.54
Methionine (%) 0.37
Lysine (%) 1.22
1Each 1 kilogram contained Ca 32.5%; P 1%; Fe 6 g; Mn 4 g; 0.075 g; Cu 0.3 g; Zn 3.75 g; Vitamin B12 0.5 g; Vitamin D3 50000 IU
Protein digestibility

The protein digestibility trial was conducted on 42 day old chicken with total collection method combined with Cr2O3 0.3% as an indicator based on Hahn et al 2006 with some modification. A total of 24 chickens were fed with diet mixed with Cr2O3 0.3% for 3 days and the excreta were then collected, weighed, dried and ground. The protein analysis was performed based on AOAC (2007) method.

Microbiological analysis

At the end of the experiment (day 42), 24 broiler chickens were randomly selected from each treatment for microbial analysis (pH, lactic acid bacteria and coliforms). The pH of ileum and caecum digesta was determined according to Nabizadeh (2012) with some modification. Briefly, one gram of fresh sample that was diluted with 10 ml of distilled water was measured using a pH meter.

Microbial population in the ileum and caecum (lactic acid bacteria and coliform) was measured based on the method of Peng et al (2016), in which one gram digesta sample that was transferred to 9 ml of sterile physiological saline solution was homogenized and diluted up to 10-8, plated in de Man Rogosa and Sharpe Agar (MRSA) and incubated anaerobically at 37C for 48 h for the enumeration of lactic acid bacteria. For the enumeration of coliform, the homogenized samples were diluted up to 10-6, plated in MacConkey Agar and incubated anaerobically at 37 C for 24 h. The bacterial population is presented as log10 colony forming units (cfu) g-1 digesta.

Intestinal morphology

Observations of intestinal morphology include villi height (VH), crypt depth (CD) and the ratio of villi to crypt depth in the duodenum, jejunum and ileum. The analysis was performed according to Ur Rahman et al (2017) with some modification. Specimens from duodenum, jejunum and ileum were cut around 2 cm and fixed in a 10% neutral buffer formalin solution for 2 days, dehydrated process and then embedded in paraffin. The sections were cut at 4 m and stained with haematoxylin and eosin. Villus height and crypt depth were measured under Leica ICC50HD microscope (4x magnification) with Leica Application Suite version 3.4.0 software. The height of the villi was measured from the end of villi to the intersection between villi - crypt. The crypt depth was measured based on the transition region between crypt and villi.

Immune organs

On d 42, 24 birds (1 birds from each pen) were randomly selected for measurement of immune organs. The chickens was weighed individually and killed. The spleen, thymus and bursa of Fabricius were removed, weighed and expressed as a percentage of live body weight according to Niu et al (2009).

Haematological parameters

Measurement of haematological and serum biochemical parameters were conducted at day 42 of age based on Khalaji et al (2011) method. Blood sample collected from wing vein was put in an Ethylenediaminetetraacetic acid (EDTA) tubes for the measurement of erythrocyte, haemaglobin (Hb), packed cell volume (PCV) and leukocyte. The number of erythrocytes and leukocytes were determined using hemocytometer method; Hb and PCV were determined using cyanmethemoglobin and microhematocrit methods.

Statistical analysis

Completely randomized design consisting of 4 treatments and 6 replications was used in this experiment. All data were analyzed by analysis of variance and if there were significant differences, it was followed by Duncan's multiple range test with SAS 9.0 software program.


Results and discussion

Growth performance

The average of feed intake, body weight gain (BWG), and feed conversion ratio are presented in Table 2. The results showed that the supplementation of synbiotics increased (p <0.05) the feed intake, body weight gain, and decreased the feed conversion ratio (FCR).

Data on Table 2 shows that the supplementation of synbiotics at 3 ml/100 g of feed increased feed intake compared to the supplementation of synbiotics at 0 ml/100 g of feed (SB0), 1 ml/100g of feed (SB1), and 2 ml/100 g of feed (SB2). The results were similar to the findings of Abdel-Wareth et al (2019) reporting that the supplementation of synbiotics increased feed intake of broilers. The increased feed intake in this study seemed to be that synbiotics stimulated the activity of digestive enzymes in the digestive tract. Therefore, the processes of digestion and absorption of nutrients become better. This was indicated in the present study by the increase in protein digestibility (Table 3). Pruszynska-Oszmalek et al (2015) reported that the supplementation of prebiotics and synbiotics by in ovo injection was able to increase the activity of pancreatic enzymes in broiler chicken which had an effect on the process of digestion of starch, protein, and triglycerides. The increased digestive enzymes activity and process of nutrient digestion thereby influenced the increase in feed intake (Park and Kim, 2014).

Table 2. Effects of synbiotic on broiler growth performance
Parameters Experiment treatment SEM p
SB0 SB1 SB2 SB3
Feed intake (g/bird) 2125b 2207b 2261b 2462a 70.5 0.0014
Body weight gain (g/bird) 1088d 1185c 1291b 1455a 11.6 <0.0001
Feed conversion 1.96a 1.86ab 1.75bc 1.69c 0.052 0.0011
abc Means in the same row without common letter are different at p<0.05. SB0, 0 ml/100g of feed, SB1, 1 ml/100 g of feed, SB2, 2 ml/100 g of feed and SB3, 3 ml/100 g of feed. SEM, standard error of mean

The body weight gain of broiler chickens in this study increased with the increase doses of the synbiotics supplementation. Supplementation of synbiotics at 3 ml/100 g of feed resulted in the highest body weight gain. This result was supported by the data of feed intake which was also highest in this respective chicks. Mousavi et al (2015) stated that synbiotics had the ability to increase the appetite of broilers, thereby increased the feed intake which ultimately increased the body weight of broiler. An increase in body weight gain in this research was similar to the findings of Hassanpour et al (2013), Mohammed et al (2018), and Abdel-Wareth et al (2019) who reported that the supplementation of synbiotics increased body weight gain of broiler chicken. Increased body weight gain in this research indicated that supplementation of synbiotics could improve microflora balance in the gastrointestinal tract (GIT). Therefore, the intestinal health also improved. This was indicated by the increase of the total of lactic acid bacteria (LAB) and the decrease on the total of coliform in the intestine by broiler in this present study (Table 4). Ibrahim and Desouky (2009) and Abdel-Wareth et al (2019) reported that synbiotics improved the balance of microflora in the intestine and increased digestive enzyme secretion, so it could increase the growth performance of broiler chickens.

Feed conversion ratio with the supplementation of synbiotics at 1 ml/100g of feed was not different from 0 ml/100 g of feed (control), but the supplementation of synbiotics as much as 2 ml/100 g of feed and 3 ml/100 g of feed showed decrease in FCR. This result was in line with of Mookiah et al (2014) and Mousavi et al (2015) reporting that the supplementation of synbiotics decreased FCR of broiler. The low FCR value in this research was supported by the data of feed intake and the increased body weights of broiler chickens, so the resulting FCR values became better. Rostami et al (2015) stated that the increase of FCR was influenced by an increase of body weight and feed intake. Cengiz et al (2015) stated that the increased body weight and feed intake would improve the performance of broiler chicken. This was indicated by the low FCR value. The FCR value was also influenced by the efficiency of digestion and absorption of nutrients in the digestive tract. The supplementation of synbiotics in this research increased the intestinal villi height (Table 5) which had an effect on the increase of nutrient absorption, thereby increasing growth and decreasing FCR. Shirani et al (2019) stated that the increase in villi height had an effect on increasing the absorption capacity of nutrients to increase the nutrient digestibility, feed efficiency, and growth performance.

Protein digestibility

The average protein intake and protein digestibility of broiler were presented at Table 3. The results showed that supplementation of synbiotics increased (p <0.05) protein intake and protein digestibility of broiler chicken. The results showed that supplementation of synbiotics at 2 and 3 ml/100 g of feed increased protein intake and protein digestibility when compared with controls. The increase of protein intake in this research was supported by the increase in data of feed intake (Table 2) that had increased with supplementation of synbiotics. This was in line with Apata (2008) who reported that protein intake increased with the increase of feed intake due to Lactobacillus supplementation in broiler chicken.

Table 3. Effects of synbiotic on protein digestibility
Parameters

Experiment treatment

SEM p
SB0 SB1 SB2 SB3
Protein intake (g/bird) 23.8b 25.7b 28.9a 29.1a 0.81 <0.0001
Protein digestibility (%) 68.6c 74.3b 79.9a 81a 2.41 0.0003
abc Means in the same row without common letter are different at p<0.05. SB0, 0 ml/100g of feed, SB1, 1 ml/100 g of feed, SB2, 2 ml/100 g of feed and SB3, 3 ml/100 g of feed. SEM, standard error of mean

Data in Table 3 showed that protein absorption in chickens that were given supplementation of synbiotics were more efficient compared to control. The results of this research was in line with Alzueta et al (2010) reporting that supplementation of inulin increased the ileum apparent value of protein digestibility. Synbiotic supplementation may improve the intestinal ecology and morphology as indicated by the increased lactic acid bacteria and decreased coliform population as well as the increased villi height. This may consequently improve the digestion and absorption of protein. Rubio (2018) stated that there was a relevant relationship between microbial composition and nutrient utilisation. Salim et al (2013) and Singh et al (2017) stated that probiotics could improve intestinal health and provided the conducive intestinal environment to increase enzyme activity, so the digestive process and nutrient utilisation were better. Wang and Gu (2010) stated that probiotics could stimulate the production of endogenous enzymes in the digestive tract, such as proteases, amylases, and lipases, which could break down the nutrients such as protein, carbohydrates, and lipids. Calik and Ergun (2015) showed that the improved development of intestinal morphology, which included the increase of villi height, width, and surface of the intestine, played an important role in improving the digestibility of nutrients. Palamidi et al (2016) stated that increase of digestibility was the result of increased digestive function due to increase of intestinal histomorphology.

Microbial population

The average of microbial population at ileum and cecum of broiler chickens was presented in Table 4. The results showed that supplementation of synbiotics decreased (p <0.05) the caecum pH but it did not affect (p> 0.05) the ileum pH. This research was in line with Wu et al (2019) who reported that the supplementation of Lactobacillus and inulin increased the beneficial bacteria and decreased pathogenic bacteria in the ileum and cecum of broilers. Synbiotics provided benefits to the host, because they offered a specific substrate for the fermentation process that supported the growth of probiotics, thereby increased the survival of beneficial bacteria in the intestine (Adil and Magray, 2012). The fermentation by lactic acid bacteria produced a high concentration of lactic acid, so it decreased the pH values and reduced the growth of harmful bacteria (Rolfe, 2000).

Table 4. Effects of synbiotic on microbial population of broiler chicken
Parameters Experiment treatment SEM p
SB0 SB1 SB2 SB3
pH
Ileum 6.7 6.67 6.58 6.48 0.15 0.49
Caecum 6.6a 6.58a 6.48ab 6.38b 0.063 0.0283
LAB
Ileum 9.01b 10.4a 10.5a 10.5a 0.54 0.0032
Caecum 9.35b 10.6a 10.8a 10.6a 0.73 0.05
Coliform
Ileum 8.28a 7.39a 5.65b 5.57b 0.75 0.007
Caecum 8.16a 6.89ab 5.81b 6.31b 0.70 0.03
abc Means in the same row without common letter are different at p<0.05.SB0, 0 ml/100g of feed, SB1, 1 ml/100 g of feed, SB2, 2 ml/100 g of feed and SB3, 3 ml/100 g of feed. LAB, lactic acid bacteria. SEM, standard error of mean

Data in Table 4 showed that the supplementation of synbiotics increased the total lactic acid bacteria and decreased the total coliform in the ileum and caecum. This research were in line with Dibaji et al (2014) and Mookiah et al (2014) who reported that the supplementation of synbiotics increased population of the lactic acid bacteria and decreased E. coli and total coliform in the intestine. This research was in line with Calik et al (2016) reporting that synbiotics increased the total population of beneficial bacteria and reduced the population of pathogenic bacteria in the caecum of broiler chickens.

Intestinal morphology

The supplementation of synbiotics showed higher (p <0.05) villi height (VH) and the ratio of villi height to crypt depth across the intestinal segments, but did not affect (p>0.05) the crypt depth in the duodenum, jejunum, and ileum (Table 5). The results showed that the supplementation of synbiotic increased villi height and the ratio of villi height to crypt depth in the duodenum, jejunum and ileum. This research was in line with Awad et al (2009), Abdel-Raheem (2012), Hassanpour et al (2013) reporting that the supplementation of synbiotics or prebiotic increased villi height and the ratio of villi height to crypt depth in the duodenum, jejunum, and ileum. Wang et al (2017) found that the supplementation of Lactobacillus plantarum increased the villi height and the ratio of villi height, crypt depth in the jejunum.

The increase in villi height seemed to be attributed to the increased total lactic acid bacteria and decrease of the total coliform in the ileum and caecum (Table 4). Shirani et al (2019) explained the increase in intestinal morphology was a response to the increase of microbial balance in GIT as a result of the decrease of pathogenic bacteria in the intestine, resulting in an improvement in structure and function of intestinal. Kim and Ho (2010) and Shirani et al (2019) stated that the increase of lactic acid bacteria in the intestine would increase mucin production which could protect the intestinal epithelial cells from damage due to effects the toxin of pathogenic bacteria.

Table 5. Effects of synbiotic on intestinal morphology broiler chicken
Parameters Experiment treatment SEM p
SB0 SB1 SB2 SB3
Duodenum
VH (µm) 1213b 1588a 1667a 1698a 99.9 0.0005
CD (µm) 299 335 348 343 23.8 0.17
VH : CD 4.07b 4.76a 4.84a 4.96a 0.15 <0.0001
Jejunum
VH (µm) 1291b 1310b 1624a 1748a 117.8 0.0121
CD (µm) 290 288 331 342 21.4 0.13
VH : CD 4.45b 4.53b 4.94a 5.10a 0.17 0.0011
Ileum
VH (µm) 1004b 1203a 1291a 1349a 89.3 0.0089
CD (µm) 231 246 259 255 19.5 0.49
VH : CD 4.36b 4.96a 5.01a 5.28a 0.25 0.0155
abc Means in the same row without common letter are different at p< 0.05. SB0, 0 ml/100g of feed, SB1, 1 ml/100 g of feed, SB2, 2 ml/100 g of feed and SB3, 3 ml/100 g of feed. VH, villi height. CD, crypt depth.SEM, standard error of mean
Immune organs

The effect of supplementation of synbiotics on the relative weight of spleen, thymus, and bursa of fabricius are presented in Table 6. The results of the study showed that the relative weight of spleen, thymus, and bursa of fabricius were not affected by supplementation of synbiotics. The results of this research were in line with Awad et al (2009), Madej et al (2015), Olnood et al (2015), Zhao et al (2016) and Wang et al (2019) reporting that probiotic, prebiotics and synbiotics supplementation did not affect the relative weight of the spleen, thymus, and bursa of fabricius of broiler chicken.

Table 6. Effects of synbiotic on relative weight immune organs of broiler chicken
Parameters Experiment treatment SEM p
SB0 SB1 SB2 SB3
Bursa fabricius (%) 0.15 0.19 0.17 0.17 0.029 0.79
Thymus (%) 0.19 0.23 0.21 0.21 0.047 0.74
Spleen (%) 0.12 0.11 0.10 0.10 0.016 0.61
SB0, 0 ml/100g of feed, SB1, 1 ml/100 g of feed, SB2, 2 ml/100 g of feed and SB3, 3 ml/100 g of feed. SEM, standard error of mean

There are many factors that may influence the effectiveness of synbiotics on the relative weight of the immune organ in broiler chicken. Those factors were dosage, type of probiotics and synbiotics, nature of probiotics and prebiotics (genera, species, or strains), diet, and location. Patterson and Burkhloder (2003), Abdurrahman et al (2011), Chambers and Gong (2011), and Mousavi et al (2015) stated that the efficiency of probiotics or synbiotic application was greatly influenced by the type of probiotics or synbiotics, probiotics strain, viability, level or dose, time of administration, method used, frequency, diet, age, strain of chicken or genotype, location, stress, and environment condition. It was very possible that the differences in data between this study and previous studies were due to the differences in the conditions mentioned above.

Haematological parameters

The data on the effect of supplementation of synbiotics on haematological parameters of broiler chicken are presented in Table 7. The results showed that supplementation of synbiotics did not affect erythrocytes, leukocytes, haemoglobin (Hb), and packed cell value (PCV). This study was in contrast with Beski et al (2015) reporting that supplementation of probiotic and synbiotic significantly increased erythrocytes, Hb and PCV of broiler chicken. These variations were due to the differences of inulin source, probiotic, synbiotic and diet composition. Borges et al (2004) and Hrabcakova et al (2014) stated that haematological parameters were remarkably influenced by species, age, sex, nutrition, physiological status, stress, and environmental temperature.

Table 7. Effects of synbiotic on haematological parameters of broiler chicken
Parameters Experiment treatment SEM p value
SB0 SB1 SB2 SB3
Erythrocytes (106/µl) 2.87 3.05 3.17 3.2 0.17 0.32
Haemoglobin (g/dL) 7.9 8.15 8.3 8.5 0.34 0.48
Packed cell volume (%) 28.2 30.5 31 31.8 2.25 0.44
Leukocytes (/µl) 10567 9933 10100 10108 1025 0.96
SB0, 0 ml/100g of feed, SB1, 1 ml/100 g of feed, SB2, 2 ml/100 g of feed and SB3, 3 ml/100 g of feed. SEM, standard error of mean


Conclusion


Acknowledgments

The research was funded by the Ministry Research, Technology and Higher Education of The Republic of Indonesia and was supported by Doctoral Dissertation Research Grant through Domestic Postgraduate Scholarship Program (BPP-DN).


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Received 22 September 2019; Accepted 24 September 2019; Published 2 November 2019

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