Научная статья на тему 'Effects of Xylanase Supplementation on the Performance, Nutrient Digestibility, and Digestive Organ Profiles of Broiler Chickens: A Meta-analysis'

Effects of Xylanase Supplementation on the Performance, Nutrient Digestibility, and Digestive Organ Profiles of Broiler Chickens: A Meta-analysis Текст научной статьи по специальности «Животноводство и молочное дело»

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Broiler chickens / Nonstarch polysaccharide / Performance / Xylanase enzyme

Аннотация научной статьи по животноводству и молочному делу, автор научной работы — Sri Rahmani Inayah, Rita Mutia, Anuraga Jayanegara, Yulianri Rizki Yanza, Sri Amnah

Enzymes supplementation in broiler feeding is commonly applied to optimize animal feed utilization and reduce feed production costs. One of the enzymes widely used in the broiler industry is xylanase which breaks down complex fibrous compounds in feed, such as nonstarch polysaccharides, to simpler utilizable sugar molecules. However, the effects of xylanase enzymes on broiler growth performance, nutrient digestibility, and organ function in broiler chickens were variable and inconclusive. Therefore, the current study aimed to evaluate the effect of the xylanase enzyme in feed on the performance, nutrient digestibility, and digestive function of parrots using a meta-analysis approach. A dataset of 140 points obtained from 53 articles was analyzed using a mixed model methodology. The results showed that the xylanase enzyme supplementation increased the broiler’s body weight gain and decreased feed consumption and feed conversion ratio. In addition, xylanase supplementation also increased nutrient digestibility, such as dry matter, crude protein, starch, gross energy, fat, phosphorus, and calcium. Concerning broiler organ weights, the xylanase supplementation in broiler feed significantly reduced the weight of the duodenum, small intestine, and relative length of the duodenum, jejunum, and ileum. Xylanase supplementation also tended to reduce the relative weight of the proventriculus. The results also showed a negative response to the crypt depth ileum of broiler due to xylanase supplementation. It can be concluded that xylanase supplementation improves the performance, nutrient digestibility, and digestive function of broiler chickens.

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Текст научной работы на тему «Effects of Xylanase Supplementation on the Performance, Nutrient Digestibility, and Digestive Organ Profiles of Broiler Chickens: A Meta-analysis»

Effects of Xylanase Supplementation on the Performance, Nutrient Digestibility, and Digestive Organ Profiles of Broiler Chickens: A Meta-analysis

Sri Rahmani Inayah © , Rita Mutia1 © , Anuraga Jayanegara12* , Yulianri Rizki Yanza23 © , and Sri Amnah

1Department of Animal Nutrition and Feed Technology, IPB University, Jl. Agatis Kampus IPB Dramaga, Bogor 16680, Indonesia 2Animal Feed and Nutrition Modelling Research Group (AFENUE), Faculty of Animal Science, IPB University, Jl. Agatis Kampus

IPB Dramaga, Bogor 16680, Indonesia 3Department Biology Education, Universitas Islam Riau, Jl. Kaharuddin Nasution 113, Pekanbaru 28284, Indonesia

Corresponding author's E-mail: anuraga.jayanegara@gmail.com

Received: 27 June 2022 Accepted: 12 September 2022

ABSTRACT

Enzymes supplementation in broiler feeding is commonly applied to optimize animal feed utilization and reduce feed production costs. One of the enzymes widely used in the broiler industry is xylanase which breaks down complex fibrous compounds in feed, such as nonstarch polysaccharides, to simpler utilizable sugar molecules. However, the effects of xylanase enzymes on broiler growth performance, nutrient digestibility, and organ function in broiler chickens were variable and inconclusive. Therefore, the current study aimed to evaluate the effect of the xylanase enzyme in feed on the performance, nutrient digestibility, and digestive function of parrots using a meta-analysis approach. A dataset of 140 points obtained from 53 articles was analyzed using a mixed model methodology. The results showed that the xylanase enzyme supplementation increased the broiler's body weight gain and decreased feed consumption and feed conversion ratio. In addition, xylanase supplementation also increased nutrient digestibility, such as dry matter, crude protein, starch, gross energy, fat, phosphorus, and calcium. Concerning broiler organ weights, the xylanase supplementation in broiler feed significantly reduced the weight of the duodenum, small intestine, and relative length of the duodenum, jejunum, and ileum. Xylanase supplementation also tended to reduce the relative weight of the proventriculus. The results also showed a negative response to the crypt depth ileum of broiler due to xylanase supplementation. It can be concluded that xylanase supplementation improves the performance, nutrient digestibility, and digestive function of broiler chickens.

Keywords: Broiler chickens, Nonstarch polysaccharide, Performance, Xylanase enzyme

JWPR

2022, Scienceline Publication

J. World Poult. Res. 12(3): 199-211, September 25, 2022 Journal of World's

Research Paper, PII: S2322455X2200023-12 Poultry Research License: CC BY 4.0

DOI: https://dx.doi.org/10.36380/jwpr.2022.23

INTRODUCTION Some dietary interventions have been applied to

increase feed nutritional values and improve livestock The utilization and efficiency of feeds are critical factors production efficiently (Hidayat et al., 2021). Researchers'

for improving the performance and production rate in the interests are currently focusing on enzyme utilization

livestock industry, including the broiler chicken (Masey- supplemented in the ration to increase feed nutritional

O'Neill et al., 2014). High fiber content in feedstuffs is a major issue in broiler chicken feeding that affects feed utilization and efficiency (Liu and Kim, 2017). Hence, it is difficult to optimize the expected result of broiler production due to the inability of broiler chickens to utilize feed compounds and increased production costs resulting from low feed efficiency (Liu and Kim, 2017).

values and reduce livestock production costs (Francesch et al., 2012). For instance, nonstarch polysaccharide (NSP), a complex fiber compound in feedstuff, is difficult to digest properly by monogastric animals, such as poultry (Craig et al., 2019). The insufficient ability of poultry to digest NSP compounds is due to the lack of specific enzymes in their digestive tract that can dissolve undigestible fiber bounds

To cite this paper] Inayah SR, Mutia R, Jayanegara A, Yanza YR, and Amnah S (2022). Effects of Xylanase Supplementation on the Performance, Nutrient Digestibility, and Digestive Organ Profiles of Broiler Chickens: A Meta-analysis. J. World Poult. Res., 12 (3): 199-211. DOI: https://dx.doi.org/10.36380/jwpr.2022.23

like NSP, especially in broiler chickens. Hence, some studies reported utilizing the xylanase enzyme in the broilers' ration to increase broiler chickens' feed nutritional values and digestibility (Gonzalez-Ortiz et al., 2017; Lee et al., 2019). Xylanase is an enzyme that can dissociate plant cell walls and reduce hemicellulose integrity and the viscosity of feed consumed in the broiler digestive system. Thus, the released feed nutrients may be optimally utilized and improve broilers' performance (Gonzalez-Ortiz et al., 2017).

Besides reducing the viscosity of intestinal contents, the xylanase enzyme is also known to possess the growth-promoting effect and appears to be partly related to the modulation of gut microflora (Craig et al., 2019). Such improvement may increase the feed efficiency of broiler chickens (Sarangi et al., 2016). However, studies concerning the effects of xylanase on broiler chickens' performance, nutrient digestibility, and digestive organs are varied and remain inconclusive (Olukosi et al., 2020). It is necessary to summarize the published data to determine the effects of xylanase on broiler chickens. Therefore, the current study evaluated the impact of dietary xylanase supplementation on broiler chickens' performance, internal organs, and nutrient digestibility by summarizing research data from various published articles.

MATERIALS AND METHODS

Database development

The database was built from published articles related to the study of the xylanase utilization on broiler chickens. Articles were obtained from Scopus, Google Scholar, NCBI, and Science Direct search engines using "xylanase", "performance", "fiber", and "broiler chicken" keywords. Articles that were included in the database must accede to the following criteria. They described experiments on broiler chickens, treatments were based on the levels of xylanase supplementation in basal feeds, and they must include data about broilers' growth performance (feed intake and daily gain), organ weight and/or internal organ morphometrics, and the articles were written in English. Data from these articles were rigorously selected to be included in the database following some selection stages (Figure 1).

A total of 140 data points representing treatments from 53 articles were included in the database (Table 1). Articles expressed the xylanase supplementation unit as the international unit (IU) values were homogenized and expressed as per 1000 IU (n / 1000 IU). The data included performance parameters (body weight gain, feed

consumption, feed conversion ratio [FCR]), nutrient digestibility (dry matter [DM], gross energy, fat, starch, crude protein [CP], phosphorus, calcium digestibility), relative weight of internal organs and digestive tract (proventriculus, liver, pancreas, gizzard, duodenum, jejunum, ileum, small intestine, cecum), relative lengths of the duodenum, jejunum, ileum, cecum, and intestinal morphometrics (villus height [VH], crypt depth [CD], and VH: CD of the duodenum, jejunum, and ileum). Data expressed in different units were converted and adjusted into that of specified units to allow direct analysis within specified parameters. The statistical summary of the database included in the meta-analysis study is presented in Table 2.

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Browsing research article about xylanase enzyme studies on broiler chicken: Web of Science, Scopus, Google scholar, Science Direct

Keywords: xylanase, enzyme, broiler chicken, nutrient digestibility, performance

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Verifying the studies about xylanase enzyme on broiler chicken and their

experimental methods: 76 papers found with 102 experimental studies (n= 264)

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Selected studies: 56 experimental studies (n=148) V J

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Exclusion of non-relevant criteria: 3 studies excluded (n = 8) V J

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Included studies in the meta-analysis: 53

studies (n = 140)

Figure 1. Selection of studies related to the effect of xylanase enzyme on broiler chickens

Table 1. The selected and used studies on the effects of dietary supplementation of xylanase on the performance, nutrient digestibility, and digestive organ profiles of broiler chickens

No. References Period (day) Basal feed Broiler sex (103 IU/kg DM feed)

1 Selle et al. (2003) 4-24 Wheat Male 0 - 5.49

2 Wu and Ravindran (2004) 1-35 Wheat Male 0 - 1.00

3 Wu et al. (2004) 1-21 Wheat Male 0 - 1.00

4 Wu et al. (2004) 1-21 Wheat Male 0 - 1.00

5 Olukosi et al. (2007b) 1-21 Wheat - 0 - 32.0

6 Amerah et al. (2008) 1-21 Wheat Male 0 - 1.00

7 Woyengo et al. (2008) 1-21 Wheat Male 0 - 2.50

8 Yang et al. (2008) 8-21 Wheat - 0 - 1.00

9 Amerah et al. (2009) 1-21 Wheat Male 0 - 1.00

10 Lu et al. (2009) 1-35 Corn Male 0 - 2.00

11 Luo et al. (2009) 1-22 Wheat Male 0 - 5.00

12 Cowieson et al. (2010) 1-22 Corn Male 0 - 16.0

13 Liu et al. (2011) 22-42 Corn Mixed 0 - 3.60

14 Nian et al. (2011) 1-30 Wheat Male 0 - 4.00

15 Walk et al. (2011) 1-18 Corn Male 0 - 1.20

16 Amerah et al. (2012) 1-22 Wheat Male 0 - 2.00

17 Esmaelipour et al. (2012) 1-24 Wheat Male 0 - 1.00

18 Liu et al. (2012) 1-21 Wheat Male 0 - 5.50

19 Masey-O'Neill et al. (2012) 1-18 Corn Mixed 0 - 16.0

20 Singh et al. (2012) 1-22 Corn Male 0 - 16.0

21 Barekatain et al. (2013a) 1-35 Corn Male 0 - 1.00

22 Barekatain et al. (2013b) 1-21 Corn Male 0 - 1.00

23 Cowieson and and Masey O'neill (2013) 1-49 Wheat Male 0 - 16.0

24 Gehring et al. (2013) 1-25 Corn Female 0 - 32.0

25 Kiarie et al. (2014) 1-22 Wheat Male 0 - 1.25

26 Masey-O'Neill et al. (2014) 1-49 Corn Male 0 - 32.0

27 Zhang et al. (2014) 7-21 Wheat Male 0 - 3.20

28 Pirgozliev et al. (2015) 7-21 Soybean meal Male 0 - 2.00

29 Gonzalez-Ortiz et al. (2016) 1-24 Wheat Male 0 - 16.0

30 Kim et al. (2016) 14-35 Corn Male 0 - 6.00

31 Amerah et al. (2017) 1-22 Corn Male 0 - 2.00

32 dos Santos et al. (2017) 1-24 Sorghum Mixed 0 - 16.0

33 Gonzalez-Ortiz et al. (2017) 1-22 Wheat Male 0 - 16.0

34 Kiarie et al. (2017) 1-21 Wheat Male 0 - 5.00

35 Liu and Kim (2017) 1-35 Wheat Male 0 - 5.63

36 Mabelebele et al. (2017) 1-21 Sorghum Female 0 - 1.60

37 Pakel et al. (2017) 7-21 Corn Male 0 - 0.80

38 Tang et al. (2017) 1-22 Barley Mixed 0 - 16.0

39 Ghayour-Najafabadi et al. (2018) 1-22 Wheat Male 0 - 1.00

40 Lee et al. (2018) 1-22 Wheat Male 0 - 16.0

41 Moss et al. (2018) 10-21 Canola Male 0 - 2.00

42 Widodo et al. (2018) 1-21 Soybean meal Male 0 - 16.0

43 Arczewska-Wlosek et al. (2019) 1-22 Corn Male 0 - 1.00

44 Craig et al. (2019) 1-22 Wheat Male 0 - 32.0

45 Gonzalez-Ortiz et al. (2019) 1-24 Wheat Male 0 - 16.0

46 Lee et al. (2019) 1-32 Corn Mixed 0 - 11.3

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47 Olukosi and Bedford (2019) 1-28 Wheat Male 0 - 16.0

48 Craig et al. (2020a) 1-21 Wheat Male 0 - 16.0

49 Craig et al. (2020b) 1-28 Wheat Male 0 - 32.0

50 Melo-Duran et al. (2020) 1-21 Corn Male 0 - 16.0

51 Olukosi et al. (2020) 1-28 Wheat Male 0 - 16.0

52 Pirgozlive et al. (2021) 7-21 Wheat Female 0 - 0.10

53 Rabello et al. (2021) 1-49 Corn Male 0 - 32.0

Table 2. Descriptive statistics of the observed parameters in broiler chickens by using xylanase supplementation in diet

Response Parameters N Mean SEM Min Max

Performance and feed intake

BWG (g/chick) 138 1558 88.5 285 4206

ADG (g/d/chick) 138 50.2 1.71 21.0 124

FI (g/chick) 138 2574 156 551 7502

ADFI (g/d/chick) 138 82.0 3.35 27.0 207

FCR (g/g) 138 1.60 0.02 1.03 2.29

Nutrient digestibility

DM (%) 46 71.3 0.95 60.4 85.0

CP (%) 35 70.2 1.67 55.5 83.0

Starch (%) 19 77.8 6.64 0.92 98.1

Nitrogen (%) 24 79.0 1.50 64.0 90.0

Fat (%) 15 81.6 2.20 66.0 91.3

GE (%) 33 70.8 1.14 61.3 82.1

Phosphorus (%) 20 46.7 2.13 32.4 66.2

Calcium (%) 18 49.7 3.32 17.8 65.0

Relative weight

Proventriculus (%) 12 0.40 0.03 0.28 0.59

Liver (%) 20 2.65 0.18 0.93 3.80

Pancreas (%) 22 0.29 0.02 0.14 0.46

Gizzard (%) 31 1.50 0.08 0.87 2.33

Duodenum (%) 30 0.67 0.05 0.42 1.17

Jejunum (%) 30 1.17 0.06 0.75 2.08

Ileum (%) 30 0.95 0.05 0.62 1.74

Small intestine (%) 36 3.40 0.26 1.93 6.90

Cecum (%) 26 0.34 0.03 0.12 0.70

Relative length

Duodenum (cm/100g BW) 16 2.27 0.14 1.30 3.16

Jejunum (cm/100g BW) 16 6.07 0.37 3.63 7.87

Ileum (cm/100g BW) 16 6.08 0.37 3.71 7.85

Small intestine (cm/100g BW) 16 14 0.87 8.69 18.8

Cecum (cm/100g BW) 22 1.39 0.06 0.88 1.72

Villus Height (VH)

Duodenum (^m) 22 1257 90.9 772 1949

Jejunum (^m) 30 809 41.5 354 1467

Ileum (^m) 22 626 48.4 355 1142

Crypt Depth (CD)

Duodenum (^m) 22 249 33.6 56.8 480

Jejunum (^m) 30 204 23.0 38.6 402

Ileum (^m) 22 150 16.4 37.2 257

VH: CD

Duodenum (^m) 16 5.61 1.51 0.08 18.0

Jejunum (^m) 24 5.68 1.34 0.12 25.5

Ileum (^m) 20 5.58 1.10 0.13 14.5

N: Number

Statistical analysis

The recorded database was processed statistically using the mixed model method with SAS software version 9.1 (St-Pierre, 2001; Sauvant et al., 2008). Different studies were assigned as random effects, and the dose of xylanase enzyme was assigned as a fixed effect following Hidayat et al. (2021) and Yanza et al. (2021b) modification methods, in which the effects of xylanase were assessed to have a relationship with factors, such as type of basal diets (barley, canola meal, corn, sorghum, soybean meal, and wheat) and sex (male and female). The

mathematical model used in the present meta-analysis was accomplished as follows:

Yy = n + s, + Tj + sTjj + Bo + BXy + B-X2p + bXy + ev Where, Yj is the dependent variable, ^ denotes the average of all data,, si signifies the random effect of the ith trial, ij is defined as the fixed effect of the jth-level factor, sxij is the random interaction between the i-th test and the jth-level factor, B0 indicates the overall intercept in all experiments (fixed effect), B1 refers to the linear regression coefficient Y on X (fixed effect), Xij suggests the value of the continuous predictor variable

(xylanase/1000 IU), bi is the random effect of the study on the regression coefficient Y on X in the study -i, and eij show an unexplained residual error.

Due to the qualitative information, the class determination was based on the sex factor and the type of basal diet. Different studies were considered as random effects in the model. The number of replicates in the studies was determined based on the statement of weight available in the SAS as performed by Yanza et al. (2021a). The variables were considered significant at p < 0.05 and considered to have a tendency at 0.05 < p < 0.10.

RESULTS

Supplementation of xylanase enzyme in ration positively affected broiler chickens' growth performance and nutrient digestibility (Tables 3 and 4). The total body weight gain (BWG) and average daily gain (ADG) of broiler chickens increased by a quadratic response (p < 0.05). However, xylanase supplementation reduced the broiler chickens' feed consumption when expressed as a total feed intake (FI; p < 0.05) and tended to reduce when linearly expressed as an average daily feed intake (ADFI; p < 0.10). Consequently, xylanase supplementation in broiler's ration reduced FCR. The effects of xylanase supplementation on FCR interacted with the type of diet (p < 0.05).

Xylanase supplementation enhanced nutrient digestibility, such as DM, CP, and starch by a quadratic response (p < 0.05). The xylanase supplementation, however, did not alter fat digestibility. Digestibility of phosphorus, calcium, and total gross energy digestibility (GED) were also elevated by xylanase supplementation by a linear response (p < 0.05). The effects of xylanase on phosphorus and calcium digestibility interacted with the type of diet (p < 0.05).

The present study showed that xylanase supplementation tended to negatively affect proventriculus (p < 0.10) in a quadratic manner, which had an interaction with the type of diet (p < 0.05; Table 5). Furthermore, the xylanase supplementation negatively affected the weight of the duodenum (p < 0.05) and small intestine (p < 0.05), in a quadratic and linear manner, respectively. The xylanase supplementation negatively influenced duodenum, jejunum, and ileum lengths in a quadratic manner (p < 0.05), while the small intestine length was reduced linearly (p < 0.05). The xylanase supplementation did not affect VH, VH: CD ratio of duodenum, jejunum, and ileum, and the CD of duodenum and jejunum (Table

6). However, xylanase supplementation lowered the CD of the ileum in a linear manner (p < 0.05).

DISCUSSION

Effects of xylanase on performance and nutrient digestibility of broiler chickens

The inclusion level of the feed ingredients with relatively high polysaccharide content, such as xylan and pentosan, may increase due to the availability of exogenous enzymes used in animal feed (Olukosi et al., 2007a). However, the effects of exogenous enzymes on livestock animals, such as broiler chickens, depend on utilizable nutrients contained in the dietary ration, species, age of the animal, level of antinutrients in feed ingredients, or a combination of these and other factors (Olukosi et al., 2007b). Nonstarch polysaccharide in broiler chicken feed is known to be hydrolyzed using the xylanase enzyme. In addition, it randomly cleaves the arabinoxylan backbone, generating unsubstituted or branched

xylooligosaccharides, consequently increasing the polysaccharide substrate's bioavailability (Arczewska-Wlosek et al., 2019; Lee et al., 2017). Recently, results concerning the effects of xylanase on broiler chickens have been varied. Thus, it needs a systematic approach to obtain robust conclusions on several parameters. Hence, the present study was expected to determine the effects of the xylanase supplementation on the critical parameters in broiler chicken nutrition, such as performance (weight gain, feed consumption, and FCR), internal organs, and nutrient digestibility evaluated from published articles.

Xylanase is an exogenous degrading enzyme that can increase broiler chickens' bioavailability of dietary nutrients. The findings of the present study indicated an increased body weight of broiler chickens and decreased FCR, followed by increased levels of xylanase supplementation in feed ingredients. Therefore, it can be assumed that broiler chickens fed with ration supplemented xylanase may improve their performance (Liu and Kim, 2017). Previous studies reported positive effects of xylanase on broiler performance, such as body weight gain, feed intake, and FCR, which further positively increase the nutrient digestibility of broiler chickens (Cowieson, 2010; Kiarie et al., 2014). Xylanase degrades the polysaccharides structure of plant cell walls, especially NSP that is xylan, into xylose and releases other simple sugars or nutrients. Hence, the broiler chickens can readily utilize the released sugars or nutrients for further metabolism (Dornez e al., 2009).

Table 3. The effect of xylanase supplementation (per 1000 IU) on performance and feed intake in broiler chickens

Parameters N Model Parameter estimate Model statistics Interaction Trends

Intercept SE Intercept Slope SE Slope P-value RMSE AIC Enzyme x Diet Enzyme x Sex î / i

BWG (g/chick) 138 Q 1518 143 4.92 1.43 <0.001 33.02 1798 NS NS î

-0.12 0.05 0.022

ADG (g/chick) 138 Q 49.6 2.77 0.15 0.046 0.001 1.05 820 NS NS î

-0.003 0.002 0.042

FI (g/chick) 138 L 2525 253 -1.93 0.82 0.021 48.51 1917 NS NS 4

ADFI (g/d/chick) 138 L 81.3 5.47 -0.049 0.028 0.078 1.64 951 NS NS 4

FCR (g/g) 138 L 1.61 0.04 -0.003 0.0006 <0.001 0.04 -204 0.044 0.080 4

BWG: Body weight gain, ADG: Average daily gain, FI: Feed intake, ADFI: Average daily feed intake, FCR: Feed conversion ratio, L: Linear, Q: Quadratic, SE, Standard error, RMSE: Root mean square of errors, AIC: Akaike information criterion, L: Linear response, | / j: symbol to indicate increasing/decreasing effect of treatment, The model tends to be significant at p < 0.1, significant at p < 0.05, NS: Not significant, N: Number

Table 4. The effect of xylanase supplementation (per 1000 IU) on nutrient digestibility in broiler chickens

Parameters N Model Parameter estimate Model statistics Interaction Trends

Intercept SE Intercept Slope SE Slope P-value RMSE AIC Enzyme x Diet Enzyme x Sex î / i

DM (%) 46 Q 70.2 1.64 0.34 0.14 0.020 1.71 261 NS NS î

-0.011 0.004 0.025

CP (%) 35 Q 69.4 3.11 0.67 0.17 <0.001 0.85 173.4 NS NS î

-0.026 0.012 0.049

Starch (%) 19 Q 74.7 11.0 1.16 0.33 0.006 0.80 123 0.008 NS î

-0.067 0.021 0.011

Fat (%) 15 L 80.7 3.37 0.41 0.69 NS 2.36 94.4 0.019 0.001 î

GE (%) 33 Q 70.1 1.83 0.44 0.10 <0.001 1.09 165 NS NS î

Phosphorus (%) 20 L 45.2 3.64 0.44 0.12 0.003 1.87 119.7 0.025 NS î

Calcium (%) 18 L 46.6 6.29 0.55 0.16 0.005 2.51 117.3 NS NS î

DM: Dry matter, CP: Crude protein, GE: Gross energy, L: Linear, Q: Quadratic, SE: Standard error, RMSE: Root mean square of errors, AIC: Akaike information criterion, | / j: symbol to indicate increasing/decreasing effect of treatment. The model tends to be significant at p < 0.1, significant at p < 0.05, very significant at p < 0.001, NS: Not significant, N: Number

RhBIBmPerP Inayah SR, Mutia R, Jayanegara A, Yanza YR, and Amnah S (2022). Effects of Xylanase Supplementation on the Performance, Nutrient Digestibility, and Digestive Organ Profiles of Broiler Chickens: A Metaanalysis. J. World Poult. Res., 12 (3): 199-211. DOI: https://dx.doi.org/10.36380/jwpr.2022.23

Table 5. The effect of xylanase supplementation (per 1000 IU) on relative weight and length of digestive organs in broiler chickens

Parameters N Model Parameter estimate Model statistics Interaction Trends

Intercept SE Intercept Slope SE Slope P-value RMSE AIC Enzyme x Diet Enzyme x Sex î / i

Relative Weight (%)

Proventriculus 12 Q 0.4 0.05 -0.03 0.01 0.088 0.01 -9.7 0.003 NS J

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0.002 0.001 0.085

Liver 20 L 2.59 0.33 0.006 0.007 NS 0.12 23.5 NS NS î

Pancreas 22 L 0.3 0.03 0.00004 0.002 NS 0.02 -55.4 NS NS î

Gizzard 31 L 1.53 0.13 -0.002 0.004 NS 0.11 15.5 NS NS J

Duodenum 30 Q 0.74 0.08 -0.028 0.013 0.048 0.02 -40.1 NS NS J

0.0018 0.0008 0.044

Jejunum 30 L 1.24 0.1 0.0006 0.003 NS 0.05 -17 NS NS î

Ileum 30 L 0.99 0.09 0.0022 0.003 NS 0.05 -18.5 NS NS î

Small intestine 30 L 3.48 0.51 -0.021 0.007 0.009 0.11 36.1 NS NS J

Cecum 26 L 0.36 0.06 -0.0002 0.002 NS 0.02 -58.6 NS 0.09 J

Relative Length (cm/100 g BW)

Duodenum 16 Q 2.31 0.24 -0.2 0.08 0.042 0.1 25.5 NS NS J

0.013 0.005 0.04

Jejunum 16 Q 6.04 0.61 -0.39 0.14 0.024 0.17 43.4 NS NS J

0.025 0.009 0.024

Ileum 16 Q 6.07 0.62 -0.42 0.13 0.015 0.17 42.7 NS NS J

0.026 0.009 0.015

Small intestine 14 L 15.5 1.4 -0.84 0.35 0.044 0.5 49.4 NS NS J

Cecum 22 L 1.35 0.1 0.001 0.006 NS 0.05 -13.6 NS NS î

BW: Body weight, L: Linear, Q: Quadratic, SE: Standard error, RMSE: Root mean square of errors, AIC: Akaike information criterion, NS: Not significant, N: Number, î / J.: symbol to indicate increasing/decreasing effect of treatment. The model tends to be significant at p < 0.10, significant at p < 0.05, very significant at p < 0.001, NS: Not significant.

Table 6. The effect of xylanase supplementation (per 1000 IU) on morphometric traits of broiler's digestive tract

Parameter estimate Model statistics Interaction Trends

Parameters N Model Intercept SE Intercept Slope SE Slope P-value RMSE AIC Enzyme x Diet Enzyme x Sex î / I

Villus height (VH)

Duodenum (^m) 22 L 1357 159 3.27 3.58 NS 31.39 252 NS NS î

Jejunum (^m) 30 L 805 79.4 6.06 6.29 NS 57.2 362 NS NS î

Ileum (^m) 22 L 678 85 2.62 3.1 NS 37.78 254 NS NS î

Crypt depth (CD)

Duodenum (^m) 22 L 233 58.8 -0.25 0.69 NS 6.06 192 NS NS 4

Jejunum (^m) 30 L 189 40.8 -1.46 1.23 NS 11.09 283 NS NS 4

Ileum (^m) 22 L 144 28.5 -1.08 0.42 0.024 5.12 185.4 0.041 NS 4

VH: CD

Duodenum (^m) 16 L 5.08 3 0.03 0.11 NS 0.96 74.1 NS NS î

Jejunum (^m) 24 L 5.69 2.66 -0.02 0.19 NS 1.7 127.4 NS NS 4

Ileum (^m) 20 L 5.68 1.99 0.05 0.09 NS 1.08 97.3 NS NS î

L: Linear, Q: Quadratic, SE: Standard error, RMSE: Root mean square of errors, AIC: Akaike information criterion, N: Number; î / 4: symbol to indicate increasing/decreasing effect of treatment. The model tends to be significant at p < 0.1, significant at p < 0.05, very significant at p < 0.001, NS: Not significant;

However, the efficacy of xylanase to break down NSP structures are different, depending on the type of feed sources and NSP contained in feed materials. For example, poultry prefers to consume cereals that typically have high NSP. However, the polysaccharide composition and the solidness of NSP structural bounds of cereals are different and might influence animal nutrient digestibility (Gonzalez-Ortiz et al., 2017; Bryszak et al., 2020). For example, the corn diet contained 8.7% and 65.2% of NSP and starch, respectively, which is more rapidly digested by the broiler chicken, compared to wheat, which included 10.9% and 65.2% of NSP and starch, respectively (Peron and Amerah, 2012). Therefore, by adding xylanase to both types of feed, broiler chickens' digestibility might increase. However, xylanase seems more effective in dissociating NSP and fiber molecular structures in corn than in wheat. It was studied that broilers fed corn had a higher fiber and phosphorus digestibility than broilers fed with wheat in basal diets (Cowieson et al., 2010; Amerah et al., 2017; Kiarie et al., 2017; Liu and Kim, 2017). According to Bedford (2000), xylanase supplementation can reduce hemicellulose integrity and release previously encapsulated nutrients to improve digestive function and animal performance. However, broiler chicken's feed intake and FCR in the present meta-analysis were reduced by xylanase supplementation. Such xylanase mode of action may increase released nutrients and reduce hemicellulose integrity, and viscosity of feed consumed in the broiler chicken intestines (Kiarie et al., 2014; Khadem et al., 2016). Hence, available nutrients can be optimally absorbed in the broiler chicken hindgut. Nutrient utilization can improve broiler chickens' performance indicated by the increased weight gain and reduced feed

intake or simplified by the FCR value (Kiarie et al., 2014).

Results also showed that xylanase supplementation

interacted with FCR and fat digestibility in broiler chickens of different sexes. It was reported that the body weight gain, feed intake, and FCR of male chickens were higher than that of female chickens, indicating higher susceptibility of female chickens to disease than males (Ozkan et al., 2010; Quinteiro-Filho et al., 2010; Qurniawan et al., 2016).

The present study indicated that xylanase increased broiler chickens' nutrient digestibility, such as DM, CP, starch, fat, gross energy, phosphorus, and calcium. Kim et al. (2016) explained that adding xylanase to feed ration would increase the accessibility of encapsulated nutrients in the cell wall by demolishing plant cell wall structures through the arabinoxylan degradation. Therefore, it is

assumed that xylanase is activated when consumed feed is delivered to the small intestine. Thus, undegraded nutrients in the previous digestive track, with the activated xylanase enzyme, degraded nutrients were readily absorbed in the hindgut. According to Francesch et al. (2012), the xylanase enzyme in poultry feed generally reduces digesta viscosity and increases the digestibility of nutrients. As reported, NSP in wheat may exacerbate endogenous amino acid secretion, suppressing amino acid digestibility (Angkanaporn et al., 1994; Liu and Kim, 2017). Accordingly, xylanase can reduce intestinal viscosity and endogenous amino acid secretion, release trapped nutrients, and increase cell wall permeability to absorb utilizable nutrients (Liu and Kim, 2017).

Effects of xylanase on weights and morphometrics of broiler chicken's digestive organs

In this study, Xylanase supplementation in broiler chicken feed showed no effect on the observed organ weights, such as pancreas, gizzard, jejunum, ileum, and cecum. However, the relative weight of the proventriculus, duodenum, and small intestine as well as the relative length of the duodenum, jejunum, ileum, and small intestine decreased with the xylanase supplementation. However, the present study results showed that high fibrous in feed ration can be digested properly due to exogenous enzymes, such as xylanase. Previous studies revealed that fiber or NSP components in poultry feed ration could influence intestinal development, especially the gizzard, and consequently digestibility (Hetland et al., 2004). Yasar and Forbes (2000) reported that the tissue lining the gizzard and the thickness of the gizzard glands of broiler chickens could be reduced by adding enzymes to the feed. On the contrary, Gonzalez-Ortiz et al. (2017) confirmed that no change in organ size was observed in any organs as measured by xylanase enzyme supplementation. Although gizzard weight slightly decreased due to the xylanase supplementation, it was still in the acceptable weight range.

The excessive fiber in feed ingredients may impact digestive organ size with the increased thickness of the apparent organ layer; thus, the weight of some digestive organs increases. In contrast, the current results found that xylanase may not interfere with liver activity in the detoxification process and negatively affect liver size (Septinar et al., 2021). This study revealed that xylanase positively affects metabolic processes so that the degraded nutrients can be well absorbed in the small intestine. Therefore, the cecum of broilers does not need to be burdened because of the workload of the digestive process,

To cite this paper] Inayah SR, Mutia R, Jayanegara A, Yanza YR, and Amnah S (2022). Effects of Xylanase Supplementation on the Performance, Nutrient Digestibility, and Digestive Organ Profiles of Broiler Chickens: A Meta-analysis. J. World Poult. Res., 12 (3): 199-211. DOI: https://dx.doi.org/10.36380/jwpr.2022.23

which can affect the size of the cecum. With xylanase supplementation, the indigestible fiber becomes more easily digested. Therefore, increasing digestive metabolism has no detrimental effect on organ function (Sharifi et al., 2012).

Additionally, most organs are believed to work properly even though the xylanase has a detrimental effect on weight and relative length of specified digestive organs as indicated by increased broiler performance and nutrient digestibility in the present study. The xylanase supplementation also reduced ileal CD and increased intestinal VH. According to Mathlouthi et al. (2002), enzyme supplementation increases the mean villi height in broiler chickens. The lack of evidence on organ histological morphometrics could probably be due to the physical and chemical characteristics of the digested fiber in broilers chickens' digestive tracks. Several studies found that xylanase had no effect on intestinal morphology. However, Montagne et al. (2003) and Mateos et al. (2012) stated when broiler chickens were fed a diet high in fiber, fiber molecules were left behind in digestive villi, depending on the physico-chemical characteristics of the fiber in the diet, level of feed consumed, type of animal, the age and health status of the poultry. The effect of xylanase on the weight of proventriculus and CD of ileum also depended on the consumed feed types. Gonzalez-Ortiz et al. (2017) stated that the size of broiler chickens' internal organs and digestive tract is influenced by the type of feed given. Therefore, supplementing broiler chickens' ration with the high amount of fiber compounds influences the weight and morphometric traits of digestive organs because fiber can stimulate the physiological process of digestive organs mechanically and enzymatically.

CONCLUSION

The present study reveals the positive effects of xylanase supplementation on the performance and nutrient digestibility of broiler chickens. Broilers' body weight gain was increased and FCR value was reduced with the xylanase supplementation. However, the xylanase enzyme had no effects on the relative weight of organs (pancreas, gizzard, jejunum, ileum, and cecum) and the relative length of the cecum. Otherwise, xylanase supplementation reduced ileal crypt depth and increased intestinal villus height. Xylanase also interacts with decreasing FCR, increasing the digestibility of nutrients, namely fat, nitrogen, and phosphorus. In addition, it also interacts with reducing proventriculus size based on the type of feed.

Xylanase interacts with decreasing FCR, increasing fat digestibility, and decreasing cecum size based on the sex of broilers.

DECLARATION

Acknowledgments

This research was self-funded and did not receive any financial assistance from any party.

Authors' contribution

Sri Rahmani Inayah contributed to data collection, database creation, and preparation of the manuscript. Yulianri Rizki Yanza was also involved in preparing the manuscript and data analysis. Rita Mutia, Anuraga Jayanegara, and Sri Amnah guided the research, data analysis, and manuscript preparation. All authors read and approve the final manuscript for publication in the current journal.

Competing interests

The authors declared that there is no competing interest.

Ethical consideration

All authors have checked the ethical issue, including plagiarism, consent to publish, misconduct, data fabrication and/or falsification, double publication and/or submission, and redundancy.

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