Effect of dietary lactulose supplementation on growth performance, nutrient digestibility, meat quality, relative organ weight, and excreta microflora in broilers

Effect of dietary lactulose supplementation on growth performance, nutrient digestibility, meat quality, relative organ weight, and excreta microflora in broilers P. Y. Zhao, H. L. Li, M. Mohammadi, and I. H. Kim1 Department of Animal Resource & Science, Dankook University, Cheonan, Chungnam 31116, South Korea total tract digestibility (ATTD) of DM and nitrogen (N) was increased (P < 0.05) in broilers fed the L15 diet compared with those fed the CON diet. Drip loss was decreased (P < 0.05) in L10 and L15 treatments compared with CON treatment on d 1, d 3, and d 5. On d 3, lowest (P < 0.05) drip loss was observed in the L15 treatment. Excreta E. coli counts in the L15 treatment were decreased (P < 0.05) on d 14, but Lactobacillus counts in the L15 treatment were increased (P < 0.05) on d 14 and d 35 compared with the CON diet. A linear effect (P < 0.05) was observed on BWG (d 22 to 35), FCR (d 0 to 35), the ATTD of DM and N, drip loss, E. coli (d 14), and Lactobacillus (d 14 and d 35) counts. In conclusion, dietary supplementation of 0.15% lactulose can improve growth performance and nutrient digestibility; as well as increase the proliferation of Lactobacillus and decrease E. coli counts in excreta.

Key words: lactulose, growth performance, nutrient digestibility, excreta microflora, broiler 2015 Poultry Science 00:1–6 http://dx.doi.org/10.3382/ps/pev324

INTRODUCTION

(Patterson and Burkholder, 2003a,b; Masanetz et al., 2011; Guerra-Ordaz et al., 2014). Krueger et al. (2002) demonstrated that ADG was increased in weanling pigs when they were fed lactulose 10 d prior weaning until 10 d following weaning. Moreover, dietary 0.1 or 0.2% lactulose increased growth performance, nutrient digestibility, and fecal Lactobacillus count, but reduced fecal E. coli in weanling pigs (Hossain et al., 2014). In broilers, Cho and Kim (2014) reported that dietary lactulose supplementation could improve growth performance and decrease excreta E. coli. Additionally, Calik and Erg¨ un (2015) found that lactulose addition could enhance performance and intestinal morphology of broilers. A dietary prebiotic such as chitooligosaccharide influenced relative organ weight and improved meat quality in broilers (Zhou et al., 2009), however, fructan had no effect on relative organ weight and meat quality (Zhao et al., 2013). As the research regarding the effects of lactulose on broilers is limited, this experiment was conducted to evaluate the effect of lactulose on broiler growth performance, nutrient digestibility, meat quality, relative organ weight, and excreta microflora.

Prebiotics are non-digestible but fermentable food ingredients that beneficially affect the host by selectively stimulating the growth and/or activity of one or a limited number of bacteria in the colon (Gibson and Roberfroid, 1995). The beneficial effects of prebiotics are known and they are widely used as an alternative to antibiotics in swine and poultry (Houdijk et al., 1998; Iji and Tivey, 1998; Liu et al., 2008; Zhao et al., 2012; Zhao et al., 2013). Lactulose is a disaccharide which is resistant to digestion in the small intestine, but is metabolized in the colon by bacterial flora into short chain fatty acids. As the numbers of Bifidobacteria and lactobacilli are increased, whereas the numbers of Clostridium, Salmonella, or E. coli in the gastrointestinal tract are reduced (Krueger et al., 2002; Schumann, 2002) by lactulose, it has been used as prebiotic for animals  C 2015 Poultry Science Association Inc. Received May 11, 2015. Accepted September 8, 2015. 1 Corresponding author: [email protected]

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ABSTRACT A 35 d trial was conducted to evaluate the effects of dietary lactulose on growth performance, nutrient digestibility, meat quality, relative organ weight, and excreta microflora in broilers. A total of 816 1-day-old male Ross broilers (40.2 ± 0.4 g) were allotted to 4 dietary treatments using 12 cages with 17 chicks per cage. Treatments were: 1) CON, basal diet; 2) L05, CON + 0.05% lactulose; 3) L10, CON + 0.10% lactulose; and 4) L15, CON + 0.15% lactulose. Higher (P < 0.05) body weight gain (BWG) and lower (P < 0.05) feed conversion ratio (FCR) were observed in broilers fed the L15 diet compared with those fed the CON diet during d 22 to 35. During d 0 to 35, BWG was higher (P < 0.05) and FCR was lower (P < 0.05) in broilers fed lactulose diets than those fed the CON diet. Additionally, broilers fed L15 diets had the highest BWG (P < 0.05) and lowest FCR (P < 0.05). The apparent

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ZHAO ET AL. Table 1. Basal diet composition for broilers (as-fed basis).1 Items

Finisher

52.45 32.60 5.70 5.00 1.80 1.40 0.40 0.15 0.10 0.20 0.20

60.60 26.01 5.00 4.80 1.20 1.50 0.30 0.04 0.15 0.20 0.20

12.59 22.14 1.03 1.12 0.89 0.46

12.93 19.46 0.91 1.00 0.71 0.34

22.15 1.02 1.10 0.89 0.45

19.48 0.94 1.00 0.73 0.35

1 Provided starter diets from d 0 to 21 and finisher diets from d 22 to 35. Replaced the same amount of corn with lactulose to create dietary treatments. 2 Provided per kilogram of diet: 15,000 IU vitamin A; 3,750 IU vitamin D3; 37.5 IU vitamin E; 2.55 mg vitamin K3 ; 3 mg vitamin B1 ; 7.5 mg riboflavin; 4.5 mg vitamin B6 ; 24 mg vitamin B12 ; 51 mg niacin; 1.5 mg folic acid; 126 mg biotin; and 13.5 mg pantothenic acid. 3 Provided per kilogram of diet: 37.5 mg Zn (as ZnSO4 ); 37.5 mg Mn (as MnO2 ); 37.5 mg Fe (as FeSO4 ·7H2 O); 3.75 mg Cu (as CuSO4 ·5H2 O); 0.83 mg I (as KI); and 0.23 mg Se (as Na2 SeO3 ·5H2 O).

MATERIALS AND METHODS The experimental protocol used in this study was approved by the Animal Care and Use Committee of Dankook University.

Experimental Design, Animals, and Housing In a 35 d trial, a total of 816 1-day-old male Ross 308 broiler chicks with an average body weight of 40.2 ± 0.4 g were allotted to 4 experimental diets according to their initial body weight. Dietary treatments were: 1) CON, basal diet; 2) L05, CON + 0.05% lactulose; 3) L10, CON + 0.10% lactulose; and 4) L15, CON + 0.15% lactulose. The composition of the basal diets is shown in Table 1. All diets were formulated to meet or exceed the nutritional requirements of broilers reported by the NRC (1994). Lactulose was included in the diet by replacing the same amount of corn. There were 12 replicate cages per treatment with 17 birds per cage. All birds were housed in stainless steel cages (1.75 m × 1.55 m) with concrete floors covered with clean rice bran, and continuous light was provided. The temperature of the room was maintained at 33 ± 1◦ C for the first 3 days, and decreased to 24◦ C until the end of the

Experimental Procedures and Sampling The broilers were weighed by cage and feed intake was recorded on d 0, 21, and 35 to calculate body weight gain (BWG), feed intake (FI), and feed conversion ratio (FCR). From d 29 to 35, broilers were fed diets mixed with chromic oxide (0.2%) as an indigestible marker to determine apparent total tract digestibility (ATTD) for DM and nitrogen (N) (Fenton and Fenton, 1979). On d 21 and 35, excreta samples from 2 broilers in each cage were collected and pooled. Pooled excreta samples for microflora were placed on ice for transportation to the laboratory where analysis was immediately carried out, whereas feed and excreta samples for digestibility were stored at −20◦ C until analysis. At the end of the experiment, 12 broilers were randomly selected from each treatment (1 bird per pen), weighed individually, and killed by cervical dislocation. The gizzard, breast meat, bursa of Fabricius, liver, spleen, and abdominal fat were then removed by trained personnel. The organs were stored at −20◦ C for the subsequent analyses.

Laboratory Analysis Before chemical analysis, excreta samples were dried at 57◦ C for 72 h, after which they were ground to pass through a 1 mm screen. All feed and excreta samples were analyzed for DM (method 930.15, AOAC International, 2007) and crude protein (method 990.03, AOAC International, 2007). Chromium was analyzed via UV absorption spectrophotometry (Shimadzu UV1201, Shimadzu, Kyoto, Japan). The gross energy (GE) was determined by measuring the heat of combustion in the samples using a Parr 6100 oxygen bomb calorimeter (Parr instrument Co., Moline, IL). The ATTD was calculated using the following formula:

Digestibility (%) = {1 − [(Nf × Cd)/(Nd × Cf)]} × 100, where Nf = nutrient concentration in excreta (% DM), Nd = nutrient concentration in diet (% DM), Cd = chromium concentration in diet (% DM), and Cf = chromium concentration in excreta (% DM). Broiler organs including the gizzard, breast meat, bursa of Fabricius, liver, spleen, and abdominal fat were weighed and expressed as a percentage of body weight in the laboratory. The breast muscle Hunter lightness (L∗ ), redness (a∗ ), and yellowness (b∗ ) values were determined (Minolta CR410 Chromameter; Konica

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Ingredient, % Corn Soybean meal, 44% CP Corn gluten meal, 60% CP Soybean oil Dicalcium phosphate, 18% CP Limestone Salt DL-Methionine L-Lys·HCl Vitamin premix2 Trace mineral premix3 Chemical composition (calculated) ME, MJ/kg CP, % Ca, % Lys, % Met + Cys, % Available P, % Analyzed composition, % CP Ca Lys, % Met + Cys Available P

Starter

experiment. The diets were fed in 2 phases consisting of a starter phase, from d 0 to 21, and a finisher phase, from d 22 to 35. The chicks were given free access to water and mash feed during the entire experiment.

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LACTULOSE IN BROILERS Table 2. Effect of dietary lactulose supplementation on growth performance in broilers.1,2 P-Value Items

3

L05

L10

L15

SEM

Linear

Quadratic

683 1,123 1.644

714 1,135 1.590

706 1,151 1.630

710 1,148 1.617

19 11 0.05

0.39 0.08 0.64

0.48 0.52 0.62

BWG, g FI, g FCR d 0 to 35

1,021b 1,605 1.572a

1,054a,b 1,605 1.523a,b

1,082a,b 1,581 1.461a,b

1,126a 1,576 1.400b

28 19 0.05

< 0.01 0.20 < 0.01

0.84 0.88 0.88

BWG, g FI, g FCR

1,704c 2,728 1.601a

1,768b 2,740 1.550b

1,789a,b 2,733 1.528b,c

1,836a 2,724 1.484c

18 20 0.02

< 0.01 0.84 < 0.01

0.64 0.61 0.77

1 CON, basal diet; L05, CON + 0.05% lactulose; L10, CON + 0.10% lactulose; L15, CON + 0.15% lactulose. 2 Each mean represents 12 replicates with 17 chicks/replicate (total of 816 one day-old male Ross 308 broilers with an initial BW of 40.2 ± 0.4 g). 3 BWG, body weight gain; FI, feed intake; FCR, feed conversion ratio. a–c Means in the same row with different superscripts differ (P < 0.05).

Minolta Sensing Inc., Osaka, Japan). Duplicate pH values for each sample were measured using a pH meter (Fisher Scientific, Pittsburgh, PA). Drip loss was measured using approximately 2 g of meat sample according to the plastic bag method described by Honikel (1998). One gram of the composite excreta sample from each cage for microflora was diluted with 9 mL of 1% peptone broth (Becton, Dickinson and Co., Franklin Lakes, NJ) and then homogenized. Viable counts of bacteria in the excreta samples were then conducted by plating serial 10-fold dilutions (in 1% peptone solution) onto lactobacilli medium III agar plates (Medium 638; DSMZ, Braunschweig, Germany), MacConkey agar plates (Difco Laboratories, Detroit, MI), and Salmonella Shigella agar plates (Difco Laboratories) to isolate the Lactobacillus, Escherichia coli, and Salmonella, respectively. The lactobacilli medium III agar plates were then incubated for 48 h at 37◦ C under anaerobic conditions. The MacConkey and Salmonella Shigella agar plates were both incubated for 24 h at 37◦ C. The microflora colonies were counted immediately after removal from the incubator. Concentration of microflora was finally expressed as log10 colonyforming units per gram of excreta.

Statistical Analysis All experimental data were analyzed using the GLM Procedure of SAS (SAS Inst. Inc., Cary, NC) as a randomized complete block design with 4 treatments in 12 blocks. The cage was used as the experimental unit. Tukey’s range test was adopted to compare the means of the treatments. Orthogonal polynomials were employed to assess the linear and quadratic effect of increasing the level of lactulose supplementation. Vari-

ability in the data was expressed as the pooled SEM and a P-value of <0.05 was considered statistically significant.

RESULTS Growth Performance During d 22 to 35, broilers fed the L15 diet had a higher (P < 0.05) BWG and lower (P < 0.05) FCR compared with those fed the CON diet (Table 2). During the overall period, BWG was higher (P < 0.05) and FCR was lower (P < 0.05) in broilers fed lactulose supplementation diets than those fed the CON diet. Additionally, broilers fed the L15 diet had the highest BWG (P < 0.05) and lowest FCR (P < 0.05) among the treatments. A linear effect (P < 0.01) was observed on BWG and FCR during d 22 to 35 and d 0 to 35.

Nutrient Digestibility During the entire experiment, the ATTD of DM and N increased (P < 0.05) in broilers fed the L15 diet compared with those fed the CON diet (Table 3). A linear effect was observed on the ATTD of DM (P < 0.01) and N (P = 0.04). However, no differences were observed on FI and the ATTD of GE during the experiment.

Meat Quality and Relative Organ Weight On d 1, drip loss decreased (P < 0.05) in broilers fed the lactulose supplementation treatments compared with the CON treatment (Table 4). On d 3 and 5, drip loss in the L10 and L15 treatments was lower (P < 0.05) than that in the CON treatment. Moreover, drip

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CON

d 0 to 21 BWG, g FI, g FCR d 22 to 35

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ZHAO ET AL. Table 3. Effect of dietary lactulose supplementation on nutrient digestibility in broilers.1,2 P-Value Items Dry matter Nitrogen Gross Energy

CON

L05

b

75.47 63.50b 79.40

L10

a,b

78.32 65.18a,b 80.76

L15

a,b

78.41 65.13a,b 80.75

a

80.40 66.84a 81.58

SEM

Linear

Quadratic

1.06 1.07 1.05

< 0.01 0.04 0.18

0.69 1.00 0.80

1 CON, basal diet; L05, CON + 0.05% lactulose; L10, CON + 0.10% lactulose; L15, CON + 0.15% lactulose. 2 Each mean represents 12 replicates with 17 chicks/replicate (total of 816 one day-old male Ross 308 broilers with an initial BW of 40.2 ± 0.4 g). a,b Means in the same row with different superscripts differ (P < 0.05).

P-Value Items

CON

pH value Breast muscle color Lightness (L∗ ) Redness (a∗ ) Yellowness (b∗ ) Drip loss, %

5.45

5.35

5.55

54.74 15.18 11.15

54.82 14.45 10.60

5.65a 7.41a 9.58a 12.04 2.32 0.10 0.19 15.89 1.04 1.39

d1 d3 d5 d7 Relative organ weight, % Liver Spleen Bursa of Fabricius Breast muscle Abdominal fat Gizzard

L05

L10

L15

SEM

Linear

Quadratic

5.51

0.11

0.41

0.77

54.58 14.97 11.30

53.07 15.04 11.11

0.98 0.53 0.69

0.24 0.96 0.85

0.42 0.46 0.80

3.56b 6.61a,b 8.97a,b 11.20

3.31b 5.66b,c 8.10b 11.01

2.86b 5.41c 7.69b 10.83

0.33 0.39 0.46 0.48

< 0.01 < 0.01 < 0.01 0.08

0.02 0.49 0.83 0.50

2.51 0.10 0.19 17.61 1.29 1.44

2.22 0.10 0.19 17.80 1.26 1.38

0.14 0.01 0.19 16.77 0.94 1.24

0.14 0.01 0.02 1.13 0.15 0.08

0.42 0.72 0.97 0.58 0.64 0.18

0.57 0.97 0.90 0.23 0.06 0.25

1 CON, basal diet; L05, CON + 0.05% lactulose; L10, CON + 0.10% lactulose; L15, CON + 0.15% lactulose. 2 Each mean represents 12 replicates with 17 chicks/replicate (total of 816 one day-old male Ross 308 broilers with an initial BW of 40.2 ± 0.4 g). a–c Means in the same row with different superscripts differ (P < 0.05).

loss in the L15 treatment was the lowest (P < 0.05) among the experimental treatments on d 3. A linear effect (P < 0.01) was detected on d 1, 3, and 5, as well as a quadratic effect (P = 0.02) on d 1. No effect was detected on pH value, breast muscle color, and relative weight of liver, spleen, bursa of Fabricius, breast muscle, abdominal fat, and gizzard due to lactulose supplementation.

Excreta Microflora Excreta E. coli concentrations in the L15 treatment were decreased (P < 0.05) on d 14, whereas Lactobacillus concentrations in the L15 treatment were increased (P < 0.05) on d 14 and 35 compared with the CON diet (Table 5). A linear effect (P < 0.01) was also detected for these parameters. There was no difference in concentrations of Salmonella on d 14 and 35.

DISCUSSION Growth Performance A number of researchers have previously demonstrated the beneficial effects of prebiotics on growth performance in broilers (Hajati and Rezaei, 2010; Zhao et al., 2013; Mookiah et al., 2014) by creating favorable conditions for beneficial bacteria (Steiner, 2006). It has also been reported that lactulose can selectively stimulate intestinal microflora growth as a prebiotic (Schumann, 2002; Calik and Erg¨ un, 2015). As there is currently not enough research related to the use of lactulose with broilers, we have had to draw a comparison with research which used alternative prebiotics. In broilers, ADG and FCR during wk 3 to 6 and wk 0 to 6 in the 0.3% fructooligosaccharide group were greater than in the CON group, and average daily intake was not affected during wk 0 to 3, wk 3 to 6, and wk 0 to 6 (Li et al., 2008). Additionally, Dizaji et al. (2012)

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Table 4. Effect of dietary lactulose supplementation on meat quality and relative organ weight in broilers.1,2

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LACTULOSE IN BROILERS Table 5. Effect of dietary lactulose supplementation on excreta microflora in broilers.1,2 P-Value Items, log10 cfu/g

CON

L05

L10

L15

SEM

Linear

Quadratic

Lactobacillus Escherichia coli Salmonella d 35

7.71b 6.57a 2.46

7.78a,b 6.52a,b 2.44

7.77a,b 6.50a,b 2.41

7.82a 6.41b 2.36

0.03 0.04 0.04

< 0.01 < 0.01 0.12

0.71 0.60 0.67

Lactobacillus Escherichia coli Salmonella

7.96b 6.53 2.41

8.01a,b 6.51 2.40

8.01a,b 6.46 2.37

8.06a 6.40 2.33

0.02 0.05 0.04

< 0.01 0.06 0.12

0.98 0.68 0.79

d 14

reported that broilers fed a 0.10% mannan oligosaccharides diet had higher BWG and a decreased FCR during d 15 to 28, d 29 to 42, and d 1 to 42 compared to those fed a basal diet. The results of the aforementioned research showed that the performance of broilers was improved at a later period due to prebiotics supplementation, which is consistent with our results that a 0.05% and 0.10% lactulose supplementation increased BWG during d 22 to 35 and d 0 to 35 with decreased FCR, and no effect on FI. However, our previous study showed that BWG during d 1 to 8 was increased with the 0.20% lactulose treatment (Cho and Kim, 2014). Calik and Erg¨ un (2015) also reported that a linearly improved BWG and decreased FCR were observed from d 0 to 21 as dietary lactulose was increased from 0.20 to 0.80%. Those two studies showed that lactulose concentration above 0.20% has a beneficial effect on broiler performance at an early period. The different results regarding performance among these studies may due to the different concentration of lactulose and the recorded period. We hypothesize that an interaction effect may exist between lactulose concentration and feeding period.

due to the use of prebiotics, which increase the absorption area and improves the birds’ energy and protein efficiency ratio by increasing the length of the intestinal mucosa (Santin et al., 2001). Tuohy et al. (2003) also reported that the increased nutrient digestibility in broilers supplied with oligosaccharide was contributed to by an improvement in gut health. Prebiotic supplementation can improve the health status of a bird’s gastrointestinal tract (Patterson and Burkholder, 2003b), which would be beneficial for nutrient digestibility. A recent study of Calik and Erg¨ un (2015) found that increases in dietary lactulose in broiler diets improved the morphological development of the intestine by increasing villus height, width, and surface area, which could explain the improved nutrient digestibility in the present study. However, no significant effects were observed for nutrient digestibility in broilers by 0.20% lactulose, (Cho and Kim, 2014), 0.05% lactose, and 0.10% lactulose in the present study. This indicates that the effects of lactulose on nutrient digestibility in broilers may be related to lactulose concentration. More studies are needed, concentrating on the effects of lactulose concentration on nutrient digestibility in broilers.

Nutrient Digestibility

Excreta Microflora

Cho and Kim (2014) reported that the ATTD of excreta N was increased by 0.10% lactulose supplementation on d 28 in broilers. In our study, the ATTD of DM and N was increased by the supplementation of 0.15% lactulose and a linear effect was also observed with the addition of lactulose. As studies on the effects of lactulose on broilers are limited, we have had to compare our results with research which employ alternative prebiotics. Dietary inulin improved the apparent ileal digestibility of crude protein and crude fat in broilers (Alzueta et al., 2010). Additionally, Li et al. (2007) demonstrated that adding 0.01% chito-oligosaccharide to broiler diets increased the ATTD of DM, GE, CP, Ca, and P. The enhancement in nutrient digestibility may

Prebiotics are exclusively fermented by beneficial bacteria such as Lactobacillus, Bifidobacteria, and Bacteroides, and thereby have the potential to modulate the composition of the microbial communities in the gut (Xu et al., 2003; Zhan et al., 2003). Cho and Kim (2014) found that 0.20% lactulose addition increased excreta Lactobacillus and decreased E. coli in broilers, but 0.10% lactulose did not show any significant effects on Lactobacillus and E. coli counts. Our results agree in that 0.15% lactulose increased excreta Lactobacillus and decreased E. coli counts in broilers, but no significant effects were observed by the addition of 0.10% lactulose. Lactulose canot be digested in the small intestine, but can be fermented in the colon by bacterial

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1 CON, basal diet; L05, CON + 0.05% lactulose; L10, CON + 0.10% lactulose; L15, CON + 0.15% lactulose. 2 Each mean represents 12 replicates with 17 chicks/replicate (total of 816 one dayold male Ross 308 broilers with an initial BW of 40.2 ± 0.4 g). a,b Means in the same row with different superscripts differ (P < 0.05).

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ZHAO ET AL.

flora. During the fermentation of lactulose, short-chain fatty acids are formed with consequent lowering of the colon pH and modification of the microflora, promoting the growth of lactic acid bacteria but inhibiting the E. coli and Salmonella count (Salminen and Salminen, 1997). In summary, lactulose has beneficial effects on microflora in excreta if supplemented at an appropriate level in broilers.

CONCLUSIONS

REFERENCES Alzueta, C., M. L. Rodr´ıguez, L. T. Ortiz, A. Rebol´e, and J. Trevi˜ no. 2010. Effects of inulin on growth performance, nutrient digestibility and metabolisable energy in broiler chickens. British. Poult. Sci. 51:393–398. AOAC International. 2007. Official Methods of Analysis of AOAC International. 18th ed. AOAC Int., Gaithersburg, MD, USA. Calik, A., and A. Erg¨ un. 2015. Effect of lactulose supplementation on growth performance, intestinal histomorphology, cecal microbial population, and short-chain fatty acid composition of broiler chickens. Poult. Sci. 94: 2173–2182. Cho, J. H., and I. H. Kim. 2014. Effects of lactulose supplementation on performance, blood profiles, excreta microbial shedding of Lactobacillus and Escherichia coli, relative organ weight and excreta noxious gas contents in broilers. J. Anim. Physiol. An. N. 98:424–430. Dizaji, B. R., S. Hejazi, and A. Zakeri. 2012. Effects of dietary supplementations of prebiotics, probiotics, synbiotics and acidifiers on growth performance and organs weights of broiler chicken. Eur. J. Exp. Biol. 2:2125–2129. Fenton, T. W., and M. Fenton. 1979. An improved method for chromic oxide determination in feed and feces. Can. J. Anim. Sci. 59:631–634. Gibson, G. R., and M. D. Roberfroid. 1995. Dietary modulation of the human colonic microbiota – Introducing the concept of prebiotics. J. Nutr. 125:1401–1412. Guerra-Ordaz, A. A., G. Gonz´ alez-Ortiz, R. M. La Ragione, M. J. Woodward, J. W. Collins, J. F. P´erez, and S. M. Mart´ın-Or´ ue. 2014. Lactulose and Lactobacillus plantarum, a potential complementary synbiotic to control postweaning colibacillosis in piglets. Appl. Environ. Microb. 80:4879–4886. Hajati, H., and M. Rezaei. 2010. The application of prebiotics in poultry production. Int. J. Poult. Sci. 9:298–304. Honikel, K. O. 1998. Reference methods for the assessment of physical characteristic of meat. Meat Sci. 49:447–457. Hossain, M. M., J. H. Cho, and I. H. Kim. 2014. Evaluation of lactulose on growth performance, nutrient digestibility, hematological characteristics, targeted E. coli colony, fecal score, moisture, and noxious gas emissions in weaning pigs. J. Anim. Sci. 92 (Suppl. 2):75–76 (Abstr.) Houdijk, J. G. M., M. W. Bosch, M. W. A. Verstegen, and H. J. Berenpas. 1998. Effects of dietary oligosaccharides on the growth

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Adding 0.15% lactulose to broiler diets improved BWG and decreased FCR during d 22 to 35 and d 0 to 35. The ATTD of DM and N was increased on d 35 by 0.15% lactulose supplementation, which also increased excreta Lactobacillus counts on d 14 and 35, decreased drip loss on d 1, 3, and 5, as well as excreta E. coli counts on d 14. In addition, lactulose had a linear effect on growth performance, nutrient digestibility, and excreta microflora in broilers.

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