CC BY
0JWPR
Journal of World's Poultry Research
2022, Scienceline Publication
J. World Poult. Res. 12(2): 77-84, June 25,
Review Paper, PII: S2322455X2200009-12 License: CC BY 4.0
DOI: https://dx.doi.org/10.36380/jwpr.2022.9
A Meta-analysis of Fiber Ratio Effects on Growth Performance, Gastrointestinal Traits, and Nutrient Digestibility of Broiler Chickens
Intan Nursiam © , Muhammad Ridla * © , Nahrowi Nahrowi © , Widya Hermana2 , and Anuraga Jayanegara2
1Graduate School of Nutrition and Feed Science, Faculty of Animal Science, IPB University, Bogor 16680, Indonesia 2Departement of Nutrition and Feed Technology, Faculty of Animal Science, IPB University, Bogor 16680, Indonesia
Corresponding author's Email: hmridla@apps.ipb.ac.id
Received: 18 April 2022 Accepted: 04 June 2022
ABSTRACT
Fiber is one of the essential nutrients for broiler chickens. This meta-analysis was carried out to investigate the impacts of fiber fraction ratio on broiler chickens growth performance, digestive characteristics, and nutritional digestibility. The database was compiled from 15 publications reports on the addition of fiber sources in broilers feed. To analyze the effect of acid detergent fiber (ADF) / neutral detergent fiber (NDF) ratio, the mixed model technique was utilized, with ADF/NDF ratio in the feed as a fixed effect and the experiment as a random effect. The ADF/NDF ratio in the feed had no effect on average daily gain, average daily feed intake, and feed per gain ratio in this research. Moreover, a decrease in ADF/NDF ratio in broiler chicken feed increased the relative weight of the gizzard. The relative weight and length of the small intestine and cecum were not affected by the ADF/NDF ratio in the feed. The ADF/NDF ratio in feed enhanced ileal digestibility and total tract apparent retention of most nutrients. The ADF/NDF ratio in the feed had no effect on the jejunal morphology. The minimum ADF/NDF ratio of 0.37 in the feed led to the maximum growth performance, digestive tract development, and optimal nutrient digestibility. In conclusion, controlling the ratio of fiber fraction in broiler chickens feed can improve broiler performance in the non-antibiotic growth promoters era.
Keywords: Broilers chickens, Fiber fraction, Meta-analysis, Performances
The prohibition of antibiotics growth promoters (AGP) in animal feed and antimicrobial resistance has become a global problem over the last three decades. Probiotics, prebiotics, symbiotics, organic acids, enzymes, phytogenics, antimicrobial peptides, hyperimmune egg antibodies, bacteriophages, clay, and minerals are examples of natural ingredients that can be used to replace AGP in broiler chicken feeds (Gadde et al., 2017; Stefanello et al., 2022). Apart from using a natural AGP alternative, Mateos et al. (2012) proposed that using whole grains, manipulating feed particle size, and increasing fiber in the feed could be effective ways to improve broiler chicken performance in the non-AGP era.
Broiler chickens need fiber to improve the function and development of the digestive system (Mateos et al., 2012). The capacity to promote development in broilers is
influenced by the physicochemical characteristics and particle size of the used fiber source. The use of fiber sources in broiler feed has been shown to improve the development of digestive organs, enzyme production, and performance, as well as encouraging the formation of beneficial bacteria (Gonzalez-Alvarado et al., 2007; Jimenez-Moreno et al., 2013a; Sacranie et al., 2012). The use of 2-3% fiber sources in broiler feed can help the growth of the gizzards (Mateos et al., 2012; Shivus, 2011). Fiber can increase the digestibility of amino acids in feed by stimulating the synthesis of hydrochloric acid in the proventriculus, which acts as a precursor for the formation of pepsinogen (Svihus, 2014).
The investigation of methods to improve broiler chicken performance in the era of the AGP ban is still ongoing. Optimizing the development of the digestive tract of broiler chickens by including fiber sources in feed has the potential to improve the performance of broiler
To cite this paper: Nursiam I, Ridla M, Nahrowi N, Hermana W, and Jayanegara A (2022). A Meta-analysis of Fiber Ratio Effects on Growth Performance, Gastrointestinal Traits, and Nutrient Digestibility of Broiler Chickens. J. World Poult. Res., 12 (2): 77-84. DOI: https://dx.doi.org/10.36380/jwpr.2022.9
chickens. The purpose of this study was to determine the effect of fiber fraction ratio in broiler chickens' feed and investigate the effect of using fiber on performance, development of the digestive tracts, and nutrient digestibility of broiler chickens.
MATERIALS AND METHODS
Database development
The database was created based on several types of literature that reported the effects of adding fiber sources on the growth performance of broiler chickens, gastrointestinal properties, and nutrient digestibility. Publication types were found using keywords such as "hull", "fiber", "broiler", and "performance" in Science Direct and Google Scholar. A total of 33 journal papers were included. After checking the suitability of the titles and abstracts, 15 articles were entered into the database (Table 1). The inclusion criteria were the English language of the article, the addition of fiber source, and the measured neutral detergent fiber (NDF) and acid detergent fiber (ADF) in the broiler feed. The Preferred Reporting Items for Systematic Review and Meta-Analysis Protocols (PRISMA-P) were followed in this meta-analysis investigation (Moher et al., 2009).
Cellulose, oat hulls, pea hulls, rice hulls, soy hulls, sugar beet pulp, sunflower hulls, wheat bran, and wood were some of the used fiber sources (Table 1). The amount of fiber sources added to the diet varied from 0 (control) to
9%. The assessed variables were growth performance (average daily gain [ADG], average daily feed intake [ADFI], and feed to gain ratio [FG]), gastrointestinal traits (relative organ weight, relative organ length, and pH), and nutrient digestibility (apparent ileal digestibility [AID] and total tract apparent retention [TTAR]).
Data with suitable units of measurement were handled statistically for meta-analysis using a mixed-procedure model (Jayanegara et al., 2019; Hidayat et al., 2021). The PROC MIXED technique was used to execute the analyses in SAS® OnDemand for Academics. The ADF/NDF ratio was assigned a fixed impact, whereas the study was assigned a random effect; hence, the analysis contained a random statement. The statistical significance level was set at p < 0.05, while the trend level was established at p = 0.05-0.10. The ADF/NDF ratio was regarded as a continuous predictor, and the response variables were regressed using the following mathematical model:
YlJ=Bo+B^j+sl+bXy+elJ,
Where, Yj is the dependent variable, B0 denotes the overall intercept across all studies (fixed effect), B1 refers to the linear regression coefficient of Y on X (fixed effect), Xj signals ADF/NDF ratio as a continuous predictor, s stands for the value of research random effect l, bl is the effect of random research on the regression coefficient of
Y on X in research I, residual error.
and ej signals the unexplained
Table 1. Literature included in the meta-analysis of fiber ratio effects on growth performance, gastrointestinal traits, and nutrient digestibility in broiler chickens
Fiber sources Inclusion Reference
Oat hulls 0-3% Barekatain et al (2017)
Oat hulls, Soy hulls 0-3% Gonzalez-Alvarado et al. (2007)
Oat hulls, Soy hulls 0-3% Gonzalez-Alvarado et al. (2008)
Oat hulls, Sugar beet pulp 0-3% Gonzalez-Alvarado et al. (2010)
Oat hulls, Sugar beet pulp, Cellulose 0-3% Jimenez-Moreno et al. (2009)
Oat hulls, Sugar beet pulp, Cellulose 0-3% Jimenez-Moreno et al. (2010)
Pea hulls 0-7.5% Jimenez-Moreno et al. (2011)
Oat hulls, Sugar beet pulp 0-7.5% Jimenez-Moreno et al. (2013ab)
Oat hulls, Rice hulls, Sunflower hulls 0-5% Jimenez-Moreno et al. (2015, 2019)
Wood 0-1% Monika et al. (2019)
Oat hulls 0-9% Scholey et al. (2020)
Wheat bran 0-3% Shang et al. (2020)
RESULTS AND DISCUSSIONS
The effect of the ADF/NDF ratio on broiler chicken performance
Broiler chickens had 40.59±15.97 g/day ADG, 57.38±27.19 g/day ADFI, and 1.38±0.1 FG in this meta-analysis (Table 2). According to the results of the meta-analysis, the ADF/NDF ratio in broilers feed did not have a negative effect on ADG, ADFI, and FG (Table 3). As the ADF/NDF ratio in the feed reveals the proportion of fiber fraction in the broiler feed; the greater value of the ADF/NDF ratio, and the higher fraction of insoluble fiber (cellulose and lignin). Acid detergent fiber consists of cellulose and lignin, which are the two main components
of insoluble fiber (Choct, 2009; Choct, 2015a; Choct, 2015b).
Fiber sources are high in insoluble fiber fractions and may resist enzymatic digestion processes in the digestive system and so they cannot be fermented by bacteria in the digestive tract (Mateos et al., 2012). A soluble fiber fraction is a form of fiber that is quickly fermented and has the potential to increase feed viscosity in the digestive system (Sozcu, 2019). Insoluble fiber promotes the development of the upper part of the digestive systems, such as the gizzard, while soluble fiber may be fermented into organic acid, both of which are advantageous to broiler chicken performance (Svihus, 2014; Shang et al., 2020).
Table 2. Descriptive statistics of the studies included in the meta-analysis of fiber ratio effects on growth performance, gastrointestinal traits, and nutrient digestibility in broiler chickens_
Parameter N Mean SD Minimum Maximum
ADG (g/bird/day) 49 40.59 15.97 28.60 95.84
Performance ADFI (g/bird/day) 46 57.38 27.19 39.30 142.40
FG 46 1.38 0.10 1.25 1.60
Proventriculus 39 4.73 0.65 3.20 6.10
Gizzard 47 17.47 5.95 9.50 32.90
Relative organ weight Liver 42 30.02 5.33 21.2 42.3
(g/kg BW) Pancreas 14 3.20 0.31 2.70 3.80
Small intestine 10 47.97 24.61 21.30 77.60
Caeca 30 5.01 1.79 3.30 10.40
Relative organ length Small intestine 33 162.78 46.98 78.80 226.00
(cm/kg BW) Caeca 24 23.52 2.60 20.10 29.20
Proventriculus 27 4.23 0.50 3.37 5.19
pH Gizzard 33 3.28 0.58 2.38 4.78
Duodenum 11 6.13 0.09 5.96 6.23
DM 23 71.27 2.31 66.90 75.30
OM 21 74.76 2.43 70.70 79.30
Apparent Ileal CP 23 76.72 3.08 71.30 83.90
Digestibility (%)
Ash 10 48.65 4.08 42.30 55.60
Starch 21 94.39 2.36 90.20 98.00
DM 33 77.59 2.14 73.50 81.60
OM 33 82.20 2.11 77.80 86.20
Total Tract Apparent Soluble Ash 33 41.19 6.70 23.40 53.40
Retention (%)
Nitrogen 33 66.90 2.91 61.30 71.60
EE 33 88.40 3.45 79.80 93.50
AMEn (Kcal) 33 3177.95 80.79 2974.00 3298.46
Villus Height (^m) 15 929.53 210.27 719.00 1449.00
Jejunal Morphology Crypt Depth (^m) 15 11.93 21.53 98.00 186.00
Villus Height/Crypt Depth 15 8.24 1.87 6.72 14.49
N: Number of the sample, SD: Standart Deviation, ADG: Average Daily Gain, ADFI: Average Daily Feed Intake, FG: Feed to Gain ratio, DM: Dry Matter, OM: Organic Matter, CP: Crude Protein, EE: Ether Extract, AMEn: Apparent Metabolish Energy.
The effect of the ADF/NDF ratio on the digestive system of broiler chicken
The ADF/NDF ratio in feed affects each digestive organ differently (Table 3). An increase in the ADF/NDF ratio had a negative effect on the proventriculus and gizzard relative weight but had no effect on the liver and pancreas relative weights. According to the model, the ideal ADF/NDF ratio for obtaining the best relative weight of the gizzard is 0.41. According to Svihus (2011), proventriculus produces mucous, hydrochloric acid, pepsinogen, and lipases, on the other hand, the main functions of gizzard include increasing digestibility through feed particle size reduction, mechanical-chemical nutrient degradation of feed ingredients, and regulating the flow rate of feed in the digestive tract.
The physicochemical properties of the fiber source added to the feed are thought to stimulate an increase in the relative weight of the gizzard. According to Jimenez-Moreno et al. (2010), broilers fed oat hulls with particle sizes of 386 ^m and 462 ^m had relative gizzard weights of 2.73% and 3.3%, respectively. Fiber sources are high in lignin and can linger in the gizzard longer, causing the gizzard muscles to work harder to digest it, thereby stimulating better development of the gizzard (Gonzalez-Alvarado et al., 2008).
The ADF/NDF ratio in the feed had no effect on the relative weight or length of the small intestine. These findings contradict those of Kimiaetalab et al. (2018), who found that the fiber supplementation in broiler feed affects the weight and relative length of the small intestine. Dietary fiber helps the maintenance of small and large intestine integrity by strengthening mucosal structure and functions and increasing the population and diversity of commensal bacteria in the gastrointestinal tract (Jha and Mishra, 2021). Maintaining a balance of soluble and insoluble fiber in the small intestine is of utmost importance; in case there is too much soluble fiber, the viscosity will increase and the flow rate of feed in the small intestine will decrease; the addition of non-starch polysaccharide enzymes is expected to reduce the negative effects of this issue. Broiler chickens need some insoluble fiber for fermentation, in this regard, short-chain fatty acid can be utilized by broiler chickens as an energy source.
The weight and relative length of cecum had no effect on the ADF/NDF ratio in the feed. Through the help of bacteria in the cecum, the cecum aids in water and salt reabsorption as well as the fermentation of uric acid and carbohydrates into ammonia and volatile fatty acid (Svihus et al., 2013a; Svihus et al., 2013b). According to Shang et
al. (2020), the addition of 3% wheat bran can enhance the population of Lachnoclostridium and Butyricicoccus, which can have a role in the production of butyric acid in broiler chicken. The proportion of soluble fiber is directly connected to the ratio of ADF/NDF to cecum function since bacteria in the cecum require a particular quantity of soluble fiber for effective fermentation.
The ratio of ADF/NDF in the feed altered the pH of the proventriculus and gizzard, while the ratio of the fiber fraction in the feed did not affect the pH of the duodenum (Table 3). To create a low pH gizzard, the minimal ADF/NDF ratio in the feed is 0.37. Changes in pH are closely related to the proventriculus and gizzards' increased ability to produce hydrochloric acid, which acts as a precursor for the enzyme pepsinogen (Svihus, 2011) and increases the reflux mechanism between the proventriculus-gizzard and gizzard duodenum resulting in a more optimal level of nutrient digestibility (Hetland et al., 2004).
Jejunal morphology (villus height, crypt depth, and villus height/crypt depth ratio) was unaffected by the ADF/NDF ratio in the feed (Table 3). Monika et al. (2019) reported that increasing the lignocellulose content in the feed causes shortness of jejunal crypt. The use of pea hull as a fiber source up to 7.5% in the feed can minimize the villus height and crypt depth (Jimenez-Moreno et al., 2011). This finding suggests that each organ requires a distinct type of fiber than the others. It is hypothesized that broiler chickens require a suitable composition of soluble fiber, which can function as a prebiotic to support improved intestinal health, in order to produce better jejunal morphology.
The effect of the ADF/NDF ratio on the nutrient digestibility of broiler chickens
The apparent ileal digestibility (AID) of dry matter (DM), organic matter (OM), and Ash, as well as the total tract apparent retention (TTAR) of DM, soluble ash, nitrogen (N), and ether extract (EE), were affected by the ADF/NDF ratio in feed (Table 3). The maximal ADF/NDF ratio values for producing AID DM, OM, and Ash were 0.44, 0.43, and 0.49, respectively, whereas TTAR DM, soluble ash, N, and EE were 0.46, 0.45, 0.44, and 0.51, respectively. The amount of digesta viscosity in the digestive system is related to the fiber ratio in feed. The higher the soluble fiber fraction in the diet, the higher the viscosity, and the lower the amount of nutritional digestibility. Maintaining a balance between the quantity of insoluble fiber and soluble fiber in the feed reduces
viscosity, allowing the feed to be digested more easily (Nursiam et al., 2021).
Apparent metabolizable energy (AMEn) was unaffected by the ADF/NDF ratio in the feed (Table 3). The improved DM and nitrogen digestibility in broilers given more fiber in the feed was strongly tied to proventriculus and gizzard's capacity to produce hydrochloric acid, which functions as a precursor for the
enzyme pepsinogen (Svihus, 2011). According to Hetland et al. (2003), adding fiber sources, such as oat hulls can boost bile acid production and amylase enzyme activity. Jimenez-Moreno et al. (2019) reported that the increased levels of fat digestibility in broiler chickens fed oat hulls, sunflower hulls, and rice hulls as a source of fiber in the feed were 89.4%, 89.35%, and 89.9%, respectively, compared to 87% in the control groups.
Table 3. The effect of fiber fraction ratio on growth performance, gastrointestinal traits, and nutrient digestibility in broiler chickens
Respon Parameter N Model Intercept SE intercept Slope SE slope p-value RMSE R2 AIC
Performance
ADG (g/bird/day) 49 L 42.168 5.7 49 4.1 93 3.3 32 0.2 16 3.5 59 0.9 94 248
ADFI (g/bird/day) 46 L 61.684 10.028 4.729 3.995 0.245 4.265 0.997 252.4
Feed/Gain Ratio 46 L 1.415 0.042 -0.046 0.072 0.532 0.079 0.918 -135.2
Relative organ weight (g/Kg BW)
Proventriculus 39 L 5.5 21 0.4 07 -1.878 0.8 02 0.0 26 0.7 51 0.8 25 48 .5
Gizzard 47 Q 1.504 7.294 82.846 -100.11 32.851 37.090 0.011 9.512 0.701 260.3
Liver 42 Q 31.799 4.088 -11.678 12.216 16.129 16.822 0.473 3.145 0.954 171.2
Pancreas 14 Q 4.894 1.894 -8.691 10.383 9.916 12.658 0.433 0.524 0.519 -1.2
Small Intestine 10 L 31.163 17.112 21.286 14.034 0.18 8.424 0.985 56.7
Caeca 30 L 5.907 0.936 -1.777 1.14 0.134 0.882 0.968 60.1
Relative organ length (cm/Kg BW)
Small Intestine 33 Q 151.34 22.592 43.492 -50.411 59.718 71.292 0.486 12.92 0.990 221.5
Caeca 24 L 24.697 2.011 -3.003 3.837 0.444 2.386 0.886 80
pH
Proventriculus 27 L 3.744 0.3 74 1.263 0.6 18 0.0 54 0.472 0.8 77 10
Gizzard 33 Q 4.515 1.117 -7.127 9.513 4.994 4.978 0.098 0.883 0.697 38.3
Duodenum 11 Q 5.443 0.735 4.416 -6.255 3.906 4.978 0.249 0.228 0.148 -19.9
Apparent Ileal Digestibility (%)
DM 23 Q 57.51 6.538 70.029 -79.696 28 .3 30.243 0.018 5.253 0.335 86
OM 21 Q 63.664 7.187 58.331 -68.482 31.325 33.575 0.059 5.475 0.322 80
CP 23 Q 71.961 7.326 31.145 -39.25 30.125 31.559 0.232 4.381 0.74 91.2
Ash 10 Q 5.676 23.529 199.76 -204.34 90.326 80.125 0.044 8.45 0.445 32.5
Starch 21 Q 86.428 7.36 39.435 -44.171 31.986 34.23 0.216 5.146 0.364 80.8
Total Tract Apparent Retention (%)
DM 33 Q 69.812 4.318 35.335 -38.425 19.612 21.977 0.093 3.809 0.574 121.7
OM 33 Q 80.205 4.209 9.79 -12.34 19.104 21.406 0.57 3.461 0.64 120.3
Soluble Ash 33 Q 5.268 12.901 168.2 -186.54 58.184 65.125 0.009 12.153 0.541 188.2
Nitrogen 33 Q 51.585 6.258 74.197 -83.941 28.739 32.266 0.016 6.05 0.411 142.7
EE 33 Q 74.383 3.76 59.715 -59.002 16.434 18.353 0.004 3.457 0.856 116.8
AMEN (Kcal) 33 Q 2901.79 168.76 1168.02 -1178.38 769.41 862.74 0.185 145.682 0.562 341.2
Jejunal Morphology
Villus Height (|im) 15 L 845.2 269.49 261.8 538.36 0.636 250.816 0.814 167.4
Crypt Depth (^m) 15 L 145.06 34.931 -72.016 81.359 0.395 48.109 0.346 119.8
Villus Height/Crypt Depth 15 Q -4.269 13.888 64.238 -78.818 70.027 86.008 0.381 4.314 0.3 46.1
N: Number of sample, SE: Standard error, RMSE: Daily Feed Intake, FG: Feed to Gain ratio, DM: Energy, L: Linear, Q: Quadratic.
Root Mean Standard error; AIC: Akaike information criterion, ADG: Average Daily Gain, ADFI: Average Dry Matter, OM: Organic Matter, CP: Crude Protein, EE: Ether Extract, AMEn: Apparent Metabolish
CONCLUSION
In conclusion, broiler chickens require a certain amount of fiber to support optimal growth. The ADF/NDF ratio in the feed should be kept at a minimum of 0.37 to achieve high growth performance, digestive tract development, and optimal nutrient digestibility. Each fiber fraction has a unique impact on the function and growth of the digestive tract. Therefore, it is critical to consider the balance of each fiber fraction in order to promote health, nutritional digestibility, and welfare in broiler chickens.
DECLARATION
Acknowledgments
This research was self-financed and did not receive funding assistance from any party.
Competing interest
The authors declare no conflict of interest.
Authors' contribution
Intan Nursiam contributed to data mining, building a database, data analysis, and preparing the manuscript. Muhammad Ridla, Nahrowi Nahrowi, Widya Hermana, and Anuraga Jayanegara contributed to the design and supervision of the research, the analysis of the results, and the writing of the manuscript. All authors read and
approved the final version of the manuscript to publish in the present journal.
Ethical consideration
All authors have checked the ethical issues, including plagiarism, consent to publish, misconduct, data fabrication and/or falsification, double publication and/or submission, and redundancy.
REFERENCES
Barekatain R, Swick RA, Toghyani M, and de Koning CT (2017). Interactions of full-fat canola seed, oat hulls as an insoluble fiber source and pellet temperature for nutrient utilization and growth performance of broiler chickens. Poultry Science, 96: 2233-2242. DOI: https://www. doi. org/10.3382/ps/pex008.
Choct M (2009). Managing gut health through nutrition. British Poultry Science, 50: 9-15. DOI:
https://www.doi.org/10.1080/00071660802538632.
Choct M (2015a). Feed non-starch polysaccharides for monogastric animals: Classification and function. Animal Production Science, 55: 1360-1366. DOI: https://www. doi. org/10.1071 /AN15276.
Choct M (2015b). Fibre-chemistry and function in poultry nutrition. LII Simposio Cientifico de Avicultura, Malaga, Spain. Available at: https://www.wpsa-
aeca.es/aeca imgs docs/16478 fibra mingan.pdf.
Gadde U, Kim WH, Oh ST, and Lillehoj HS (2017). Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: A review. Animal Health Research
Review, 18(1): 26-45. DOI:
https://www.doi.org/10.1017/S1466252316000207.
Gonzalez-Alvarado JM, Jimenez-Moreno E, Gonzalez-Sanchez D, Lazaro R, and Mateos GG (2010). Effect of inclusion of oat hulls and sugar beet pulp in the diet on productive and digestive traits of broilers from 1 to 42 days of age. Animal Feed Science and Technology, 162: 37-46. DOI: https://www.doi.org/10.1016/j.anifeedsci.2010.08.010.
González-Alvarado JM, Jiménez-Moreno E, Lázaro R, and Mateos GG (2007). Effects of type of cereal, heat processing of the cereal, and inclusion of fiber in the diet on productive performance and digestive traits of broilers. Poultry Science, 86: 1705-1715. DOI: https://www.doi.org/10.1093/ps/86.8.1705.
González-Alvarado JM, Jiménez-Moreno E, Valencia DG, Lázaro R, and Mateos GG (2008). Effects of fiber source and heat processing of the cereal on the development and pH of the gastrointestinal tract of broilers fed diets based on corn or rice. Poultry Science, 87: 1779-1795. DOI: https://www.doi.org/10.3382/ps.2008-00070.
Hetland H, Choct M, and Svihus B (2004). Role of insoluble non-starch polysaccharides in poultry nutrition. Worlds Poultry Science, 60: 415-422. DOI: https://www.doi.org/10.1079/WPS200325.
Hetland H, Svihus B, and Krogdahl A (2003). Effect of oat hull and wood shavings on digestion in broilers and layers fed diets based on whole or ground wheat. British Poultry Science, 44: 275-282. DOI:
https://www.doi.org/10.1080/0007166031000124595.
Hidayat C, Irawan A, Jayanegara A, Sholikin MM, Prihambodo TR, Yanza YR, Wina E, Sadarman S, Krisnan R, and Isbandi I (2021). Effect of dietary tannins on the performance, lymphoid organ weight, and amino acid ileal digestibility of broiler chickens: A meta-analysis. Veterinary World, 14(6): 1405-1411. DOI: https://www.doi.org/10.14202/vetworld.2021.1405-1411.
Jayanegara A, Sujarnoko TUP, Ridla M, Kondo M, and Kreuzer M (2019). Silage quality as influenced by concentration and type of tannins present in the material ensiled: A meta-analysis. Journal Animal Physiology and Animal Nutrition, 103: 456-465. DOI:
https://www.doi.org/10.1111/jpn.13050.
Jha R and Mishra P (2021). Dietary fiber in poultry nutrition and their effects on nutrient utilization, performance, gut health, and on the environment: A review. Journal of Animal Science and Biotechnology, 12: 51. DOI: https://www.doi.org/10.1186/s40104-021-00576-0.
Jimenez-Moreno E, Chamorro S, Frikha M, Safaa HM, Lazaro R, and Mateos GG (2011). Effects of increasing levels of pea hulls in the diet on productive performance, development of the gastrointestinal tract, and nutrient retention of broilers from one to eighteen days of age. Animal Feed Science and Technology, 168: 100-112. DOI:
https://www.doi.org/10.1016/j.anifeedsci.2011.03.013.
Jimenez-Moreno E, de Coca-Sinova A, Gonzalez-Alvarado JM, and Mateos GG (2015). Inclusion of insoluble fiber sources in mash or pellet diets for young broilers. 1. Effects on growth performance and water intake. Poultry Science, 95(1): 1-12. DOI: https://www.doi.org/10.3382/ps/pev309.
Jimenez-Moreno E, Frikha M, de Coca-Sinova A, Garcia J, and Mateos GG (2013a). Oat hulls and sugar beet pulp in diets for broilers 1. Effects on growth performance and a nutrient digestibility. Animal Feed Science Technology, 182: 33-43. DOI: https://www.doi.org/10.1016/j.anifeedsci.2013.03.011.
Jimenez-Moreno E, Frikha M, de Coca-Sinova A, Garcia J, and Mateos GG (2013b). Oat hulls and sugar beet pulp in diets for broilers 2. Effects on the development of the gastrointestinal tract and on the structure of the jejunal mucosa. Animal Feed Science and Technology, 182: 44-52. DOI: https://www.doi.org/10.1016/i.anifeedsci.2013.03.012.
Jimenez-Moreno E, Gonzalez-Alvarado J M, de Coca-Sinova A, Lazaro R, and Mateos GG (2009). Effect of source of fibre on the development and pH of the gastrointestinal tract of broilers. Animal Feed Science and Technology, 154: 93101. DOI: https://www.doi.org/10.1016/j.anifeedsci.2009.06.020.
Jimenez-Moreno E, Gonzalez-Alvarado JM, de Coca-Sinova A, Lazaro RP, and Mateos GG (2019). Inclusion of insoluble fiber sources in mash or pellet diets for young broilers. 2. Effects on gastrointestinal tract development and nutrient digestibiliy. Poultry Science, 6: 1-17. DOI: https://www.doi.org/10.3382/ps/pey599.
Jimenez-Moreno E, Gonzalez-Alvarado JM, Gonzalez-Sanchez D, Lazaro R, and Mateos GG (2010). Effect of type and particle size of dietary fiber on growth performance and digestive traits of broilers from 1 to 21 days of age. Poultry Science, 89: 2197-2212. DOI:
https://www.doi.org/10.3382/ps.2010-00771.
Kimiaeitalab MV, Mirzaie Goudarzi S, Jimenez-Moreno E, Camara L, and Mateos GG (2018). A comparative study on the effects of dietary sunflower hulls on growth performance and digestive tract traits of broilers and pullets fed a pullet diet from 0 to 21 days of age. Animal Feed Science and Technology, 236: 57-67. DOI: https://www.doi.org/10.1016/j.anifeedsci.2017.11.023.
Mateos GG, Jiménez-Moreno E, Serrano MP, and Lázaro R (2012). Poultry response to high levels of dietary fiber sources varying in physical and chemical characteristics. Journal of Applied Poultry Research, 21:156-174. DOI: https://www.doi.org/10.3382/iapr.2011-00477.
Moher D, Liberati A, Tetzlaff J, Altman DG, and Group P (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med, 6(7): e1000097. DOI:
https://www.doi.org/10.1371/iournal.pmed.1000097.
Monika BIT, Bogucka J, Dankowiakowska A, and Walasik K (2019). Small Intestine morphology and ileal biogenic amines content in broiler chickens feed diets supplemented with lignocellulose. Livestock Science, 241: 104189. DOI: https://www.doi.org/10.1016/Uivsci.2020.104189.
Nursiam I, Ridla M, Hermana W, and Nahrowi N (2021). Effet of fiber source on growth performance and gastrointestinal tract in broiler chickens. IOP Conf. Series: Earth and Environmental Science, 788: 012058. DOI: https://www.doi.org/10.1088/1755-1315/788/1/012058.
Saadatmand N, Toghyani M, and Gheisari A (2019). Effects of dietary fiber and threonine on performance, intestinal morphology and immune responses in broiler chickens.
Animal Nutrition, 5: 248-255. DOI: https://www.doi.org/10.1016/j.aninu.2019.06.001.
Sacranie A, Svihus B, Denstadli V, Moen B, Iji P A, and Choct M (2012). The effect of insoluble fiber and intermittent feeding on gizzard development, gut motility, and performance of broiler chickens. Poultry Science, 91: 693700. DOI: https://www.doi.org/10.3382/ps.2011-01790.
Sadeghi A, Toghyani M, and Gheisari A (2015). Effect of various fiber types and choice feeding of fiber on performance, gut development, humoral immunity, and fiber preference in broiler chicks. Poultry Science, 94: 27342743. DOI: https://www.doi.org/10.3382/ps.pev292.
Sadeghi A, Toghyani M, Tabidiyan SA, Foroozandeh AD, and Ghalamkari G (2020). Efficacy of dietary supplemental insoluble fibrous materials in ameliorating adverse effects of coccidial chalange in broiler chickens. Archives of Animal Nututrition, 74: 362-379. DOI: https://www.doi.org/10.1080/1745039X.2020.1764811.
Scholey DV, Marshall A, and Cowan AA (2020). Evaluation of oats with varying hull inclusion in broiler diets up to 35 days. Poultry Science, 99: 2566-2572. DOI: https://www.doi.org/10.1016/i.psi.2019.12.043.
Shang QH, Liu SJ, He TF, Liu HS, Mahfuz S, Ma XK, and Piao XS (2020). Effects of wheat bran in comparison to antibiotics on growth performance, intestinal immunity, barrier function, and microbial composition in broiler chickens. Poultry Science, 99: 4929-4938. DOI: https://www.doi.org/10.1016/j.psj.2020.06.031.
Sozcu A (2019). Growth performance, pH Value of gizzard, hepatic enzyme activity, immunologic indicators, intestinal histomorphology, and cecal microflora of broilers fed diets supplemented with processed lignocellulose. Poultry Science, 98(12): 1-8. DOI:
https://www. doi. org/10.3382/ps/pez449.
Stefanello C, Moreira B, Graf WM, Robalo S, Costa ST, Vieira IM, and Miranda DJ (2022). Effects of a proprietary blend of quillaja and yucca on growth performance, nutrient digestibility, and intestinal measurements of broilers. Journal Applied Poultry Research, 31: 100251. DOI: https://www.doi.org/10.1016/ijapr.2022.100251.
Svihus B (2011). The gizzard: Function, influence of diet structure and effects on nutrient availability. Worlds Poultry Science, 67: 207-223. DOI:
https://www.doi.org/10.1017/S0043933911000249.
Svihus B (2014). Function of the digestive system. Journal of Applied Poultry Research, 23: 1-9. DOI: https://www.doi.org/10.3382/iapr.2014-0.00937.
Svihus B, Choct M, and Classen HL (2013b). Function and nutritional roles of the avian caeca: A review. Worlds' Poulry Science, 69: 249-263. DOI: https://www.doi.org/10.3382/iapr.2014.009.
Svihus B, Lund VB, Borjgen B, Bedford MR, and Bakken M (2013a). Effect of intermittent feeding, structural components and phytase on performance and behavior of broiler chickens. British Poultry Science, 54: 222-230. DOI: https://www. .doi.org/10-1080/00071668.2013.772952.
