Influence of Levels of Dietary Fiber Sources on the Performance, Carcass Traits, Gastrointestinal Tract Development, Fecal Ammonia Nitrogen, and Intestinal Morphology of Broilers

ABSTRACT

The present study was conducted to investigate the effects of dietary fiber source levels on the fecal ammonia nitrogen, growth performance, carcass traits, gastrointestinal tract development, and intestinal morphology of broilers. A total of 420 one-day-old unsexed broiler chicks were individually weighed and randomly divided into 5 groups, each with seven replicates of twelve chicks. Rice hulls (RH) and soybean hulls (SH) were ground through a hammer mill with a 2-mm screen. The RH and SH experimental diets were as follows: 0% (control); 2.5% RH; 2.5% SH; 5% RH; and 5% SH. No significant differences were found in growth performance and fecal ammonia nitrogen among the dietary treatment groups (p>0.05). Compared with the control, the experimental diets with 2.5% SH significantly decreased the wing weight of chickens (p<0.05), while no significant differences in the weight of the other visceral organs were observed. Compared with the control, broilers in the 5% SH group had a longer jejunum and ileum (p<0.05). Feeding the broilers SH and RH had no effect on the villus area and crypt depth of the intestine. Compared with the control, the experimental diet with 2.5% RH significantly increased the duodenal villus height of chickens (p<0.05). These findings suggest that the inclusion of 5% SH in the diets resulted in improved intestinal morphology without negatively affecting growth performance and carcass traits.

Keywords:
Rice hulls; soybean hulls; broilers; intestinal morphology; ammonia nitrogen

INTRODUCTION

The majority of ammonia (NH₃) emissions are from livestock production such as cattle, poultry, and swine farming (Battye et al., 1994). In Thailand, swine farms are the largest source of NH₃ emissions; however, poultry farms also cause air pollution through the release of NH₃. Nitrogen (N) in feces, containing undigested dietary N, endogenous N and microbial N (Jha & Berrocoso, 2016), is lost to the atmosphere as volatile ammonia (Ferket et al., 2002). NH₃ emission from manure has become a significant problem not only for human and chicken health but also in poultry production, with effects such as lower egg production and growth performance (Carlile, 1984; Miles et al., 2004). Consequently, many researchers have used diet composition improvement to decrease manure pollutants.

In Thailand, rice is the major locally produced crop, which amounted to 20.7 million metric tons in 2018/19 (USDA, 2018). Rice hulls (RH) account for 20% on average of the whole grain, and the most efficient use of this by-product is as a litter material for livestock production. Moreover, soybean hulls (SH) are also a by-product of the soybean oil processing. Some researchers have demonstrated that the inclusion of soluble fiber leads to a decrease in NH₃ emission from swine manure (Kreuzer et al., 1998; Beccacia et al., 2015). Bindelle et al. (2009) found that the inclusion of oat hulls did not reduce the urinary nitrogen excretion ratio. In contrast, the dietary10% corn dried distillers’ grains with solubles, 7.3% wheat middlings, or 4.8% SH decreased NH₃ emission from laying hen manure (Roberts et al., 2007). As previously noted, dietary fiber extends the fermentation of microbes in the large intestine, and therefore the suitability of that fiber diets to lower NH₃ emission from the manure (Roberts et al., 2007).RH increase retention time in the upper part of the GIT, thus a well-developed gizzard will improve the nutrient absorption and digestibility (Mateos et al., 2002; Hetland et al., 2003; Hetland et al., 2005). Moreover, the insoluble fiber in broiler diets improved their intestinal morphology and growth performance (Sarikhan et al., 2010) and increased the secretion of hydrochloric acid (González-Alvarado et al., 2007). These improvements might be associated with increased nutrient digestibility (Amerah et al., 2009), as well as improved digestive tract health (Perez et al., 2011). Besides, the inclusion of feed ingredients with an adequate type and amount of fiber might improve the gastrointestinal tract (GIT), leading to reduced antibiotic use in the feed (Mateos et al., 2002; Montagne et al., 2003).

To the best of our knowledge, little is known about the effect of the use of rice hulls and soybean hulls as a fiber source in broiler diets. The differences in the structure and properties of fiber sources might affect nutritional and physiological effects (Santos et al., 2019). Therefore, this study aimed to investigate the effects of dietary fiber source levels on the fecal ammonia nitrogen, growth performance, carcass traits, gastrointestinal tract development, and intestinal morphology of broilers.

MATERIALS AND METHODS

Birds, management, and diets

A total of 420 one-day-old unsexed broiler chicks (Ross 308) were individually weighed and randomly divided into five groups of chicks with similar mean body weights, each with seven replicates of twelve chicks. These chicks were placed in litter-floored pens under an average environmental temperature of 32°C (12 birds per pen). The RH and SH were ground in a hammer mill to pass through a 2-mm sieve. Subsequently, the chemical composition of the fiber samples was analyzed as described by AOAC (2000) and Van Soest et al. (1991) (Table 1). Experimental diets were in mash form and formulated according to NRC (1994). These diets including RH and SH were as follows: 0% (control); 2.5% RH; 2.5% SH; 5% RH; and 5% SH (Table 2, Table 3). Feed and water were given ad libitum for 42 d and light was provided 24 h a day.

Table 1
Chemical composition of rice hull (RH) and soybean hull (SH).

Item	RH	SH
Dry matter(%)	94.98	93.74
Crude protein (%)	1.04	5.00
Ether extract (%)	5.67	8.46
Neutral detergent fiber (%)	71.07	61.57
Acid detergent fiber (%)	52.52	38.90
Acid detergent lignin (%)	18.60	3.58
Acid insoluble ash (%)	0.11	0.00
Gross energy, kcal/kg	3309.20	3866.90

Table 2
Feed compositions and calculated nutrient value of experimental diets (0 - 21 days of age).

Item	Control	2.5% RH	2.5% SH	5.0% RH	5.0% SH
Ingredient (%)
Corn	43.10	38.72	39.32	34.35	35.55
Soybean meal	40.10	40.68	40.38	41.26	40.67
Soybean oil	7.12	8.41	8.10	9.71	9.09
Rice bran	5.00	5.00	5.00	5.00	5.00
Rice hull	-	2.50	-	5.00	-
Soybean hull	-	-	2.50	-	5.00
Monocalcium phosphate	2.09	2.10	2.10	2.11	2.11
Limestone	1.22	1.21	1.22	1.21	1.21
Premixa	0.60	0.60	0.60	0.60	0.60
Salt	0.42	0.42	0.42	0.42	0.42
D,L-methionine	0.17	0.17	0.17	0.18	0.18
Choline Chloride	0.07	0.07	0.07	0.07	0.07
L-lysine	0.05	0.04	0.04	0.03	0.03
L-threonine	0.02	0.02	0.02	0.02	0.02
Calculated analysis
Crude protein	23	23	23	23	23
Metabolizable energy (kcal/kg)	3,200	3,200	3,200	3,200	3,200
Crude fiber	3.20	4.06	3.96	4.92	4.71
Crude fat	9.70	11.06	10.83	12.32	11.87
Ash	5.90	5.93	6.02	5.91	6.09
Calcium	0.90	0.90	0.90	0.90	0.90
Available phosphorus	0.50	0.50	0.50	0.50	0.50
Available lysine	1.15	1.15	1.15	1.15	1.15
Available methionine	0.47	0.47	0.47	0.47	0.47

• RH = rice hulls; SH = soybean hulls.
• ^a
  Premix included the following (per kg of diet): retinol, 8,250 IU; cholecalciferol, 2,750 IU; tocopherol, 17.9 IU; menadione, 1.1 mg; thiamine, 1.4 mg; riboflavin, 5.5 mg; pyridoxine, 1.1 mg; cyanocobalamin, 12 µg; niacin, 41.3 mg; pantothenic acid, 11 mg; biotin, 41 µg; folic acid, 1.4 mg; manganese, 125 mg; iron, 282 mg; copper, 27.5 mg; zinc, 275 mg; iodine, 844 µg; selenium, 250 µg.

Table 3
Feed compositions and calculated nutrient value of experimental diets (22 - 42 days of age).

Item	Control	2.5% RH	2.5% SH	5.0% RH	5.0% SH
Ingredient (%)
Corn	52.22	47.85	48.45	43.47	44.69
Soybean meal	32.40	32.98	32.69	33.56	32.95
Soybean oil	5.69	6.99	6.68	8.28	7.67
Rice bran	5.00	5.00	5.00	5.00	5.00
Rice hull	-	2.50	-	5.00	-
Soybean hull	-	-	2.50	-	5.00
Monocalcium phosphate	1.87	1.88	1.88	1.89	1.89
Limestone	1.36	1.35	1.35	1.34	1.35
Premixa	0.60	0.60	0.60	0.60	0.60
Salt	0.42	0.42	0.42	0.42	0.42
D,L-methionine	0.16	0.17	0.16	0.17	0.17
Choline Chloride	0.70	0.07	0.07	0.07	0.07
L-lysine	0.11	0.11	0.11	0.10	0.10
L-threonine	0.04	0.04	0.04	0.04	0.05
Calculated analysis
Crude protein	20	20	20	20	20
Metabolizable energy (kcal/kg)	3,200	3,200	3,200	3,200	3,200
Crude fiber	3.10	3.96	3.86	4.81	4.61
Crude fat	8.65	9.91	9.69	11.18	10.73
Ash	5.53	5.51	5.60	5.49	5.67
Calcium	0.90	0.90	0.90	0.90	0.90
Available phosphorus	0.45	0.45	0.45	0.45	0.45
Available lysine	1.03	1.03	1.03	1.03	1.03
Available methionine	0.43	0.43	0.43	0.43	0.43

• RH = rice hulls; SH = soybean hulls.
• ^a
  Premix included the following (per kg of diet): retinol, 8,250 IU; cholecalciferol, 2,750 IU; tocopherol, 17.9 IU; menadione, 1.1 mg; thiamine, 1.4 mg; riboflavin, 5.5 mg; pyridoxine, 1.1 mg; cyanocobalamin, 12 µg; niacin, 41.3 mg; pantothenic acid, 11 mg; biotin, 41 µg; folic acid, 1.4 mg; manganese, 125 mg; iron, 282 mg; copper, 27.5 mg; zinc, 275 mg; iodine, 844 µg; selenium, 250 µg.

The experiment was carried out following the guidelines and rules for animal experiments of the Faculty of Animal Sciences and Agricultural Technology, Silpakorn University, Thailand.

Growth performance and fecal ammonia nitrogen

During the experiment, feed intake and body weight were measured weekly, and the feed conversion ratio was calculated. At 22 d of age, birds with similar mean body weights were randomly allocated to the five dietary treatment groups (4 birds/group). They were moved to individual cages. Subsequently, feces were collected over three consecutive 24-h periods in each cage. The feces from each of the 24-h periods were pooled by a group and stored at -20°C until analysis. Fecal ammonia nitrogen was analyzed by the method of AOAC (2000).

Carcass traits and digestive organ development

At 42 d of age, seven birds from each group were weighed individually and slaughtered to determine digestive organ development and carcass traits. The head, digestive organs, and shanks were removed and then weighed. Wings, abdominal fat, thighs, and drumsticks were removed and weighted individually. In the digestive organs, the lengths of the duodenum, jejunum, and ileum were measured separately. The weights of the proventriculus, gizzard, duodenum, jejunum, and ileum were then recorded after the digesta content had been removed. The weight of empty organs was expressed relative to 100 g of body weight.

Intestinal morphological observation

At 42 d of age, another seven birds per group were used for intestinal morphological observations. Immediately following the decapitation, the midpoint of each intestinal segment (duodenum, jejunum, and ileum) was removed and fixed in 10% neutral-buffered formalin. After dehydration through varying concentrations of alcohol, each intestinal part was embedded in paraffin wax. A 4-µm-thick transverse section was cut and stained with hematoxylin-eosin, and the following values were measured using Toup View 3.7 software (Irwin, U.S.A).

The villus height was measured as the length from the tip to the base, excluding the intestinal crypt. A total of 8 villus heights from eight sections were measured and averaged for each bird. The villus area was calculated from the villus height, basal width, and apical width (Iji et al., 2001). The eight calculations of villus area were averaged for each bird. Crypt depth was measured as the distance from the villus base to the muscularis layer, not including the intestinal muscularis (Rezaei et al., 2011).

Statistical analysis

The data from the experimental groups were statistically analyzed using one-way analysis of variance (ANOVA) in SPSS statistical software (version 19.0; IBM Corp. Armonk, NY, US). The Tukey’s test was used to compare mean. Statistical significance was accepted at p<0.05.

RESULTS

Growth performance and fecal ammonia nitrogen

The influence of different sources and levels of fiber on growth performance and fecal ammonia nitrogen in broiler chickens is presented in Table 4. No significant differences were observed in feed intake, body weight gain, or feed efficiency among the dietary treatment groups (p>0.05). Feeding the chickens fiber did not affect the fecal ammonia nitrogen (p>0.05).

Table 4
The effects of different sources and levels of fiber on growth performance (mean ± SE; n = 7) and fecal ammonia nitrogen (mean ± SE; n = 4) in 42 days old broiler chickens.

Item	Level of fiber (%)	Feed intake (g)	Bodyweight gain (g)	Feed conversion ratio	Fecal ammonia nitrogen (mg/g)
Control	0	3134.71	1405.04	2.23	0.06
RH	2.5	3159.85	1469.27	2.14	0.10
	5.0	3283.00	1494.20	2.20	0.10
SH	2.5	3311.83	1414.64	2.34	0.08
	5.0	3175.71	1401.77	2.26	0.09
SEM		47.87	14.99	0.03	0.007
p-value		0.732	0.167	0.503	0.354

• RH = rice hulls; SH = soybean hulls.
• There are no significant differences between each groups (p>0.05).

Carcass traits and digestive organ development

Compared with the control, the experimental diets with 2.5% SH significantly decreased the wing weight of chickens (p<0.05) (Table 5). In addition, no significant differences in the weight of the other visceral organs were observed (Table 5). The intestinal weight and length of broilers are presented in Table 6. Compared with the control, broilers in the 5% SH group had a longer jejunum and ileum (p<0.05). In terms of intestinal weight and duodenal length, there were no significant differences among the dietary treatment groups (p>0.05).

Table 5
The effects of different sources and levels of fiber on carcass and visceral organs weight (g/100 g BW) in 42 day old broiler chickens (mean ± SE; n = 7).

Item	Level of fiber (%)	Carcass	Thigh+ drumstick	Wings	Abdominal fat	Liver	Proven-triculus	Gizzard
Control	0	87.01	23.05	8.31a	1.56	2.13	0.44	1.22
RH	2.5	86.25	22.89	8.09ab	1.52	2.09	0.44	1.29
	5.0	84.35	22.81	7.84ab	1.45	2.13	0.42	1.37
SH	2.5	84.59	22.14	7.26b	1.53	2.38	0.43	1.30
	5.0	82.91	21.62	7.95ab	1.49	2.36	0.44	1.38
SEM		0.62	0.25	0.11	0.10	0.06	0.01	0.03
p-value		0.248	0.344	0.026	0.997	0.352	0.982	0.558

• RH = rice hulls; SH = soybean hulls.
• ^a,bValues with different superscripts in the same column are significantly different (p<0.05).

Table 6
The effects of different sources and levels of fiber on intestinal weight (g/100 g BW) and length (cm/100 g BW) in 42 days old broiler chickens (mean ± SE; n = 7).

Item	Level of fiber (%)	Intestinal weight (g/100 g BW)			Intestinal length (cm/100 g BW)
		Duodenum	jejunum	Ileum	Duodenum	jejunum	Ileum
Control	0	0.63	1.14	0.90	1.24	3.04b	2.96c
RH	2.5	0.65	1.11	0.84	1.26	3.06b	3.03bc
	5.0	0.60	1.10	0.88	1.32	3.55ab	3.62ab
SH	2.5	0.66	1.11	0.89	1.35	3.14b	3.18bc
	5.0	0.67	1.16	0.96	1.42	3.72a	3.90a
SEM		0.01	0.02	0.02	0.02	0.07	0.08
p-value		0.636	0.963	0.584	0.103	0.002	<0.001

• RH = rice hulls; SH = soybean hulls.
• a,b,c Values with different superscripts in the same column are significantly different (p<0.05).

Intestinal morphological measurements

Feeding the broilers SH and RH did not affect the villus area and crypt depth of the intestine (Table 7). Compared with the control, the experimental diets with 2.5% RH significantly increased the duodenal villus height of chickens (p<0.05).

Table 7
The effects of different sources and levels of fiber on intestinal morphological measurements in 42 days old broiler chickens (mean ± SE; n = 7).

Item	Level of fiber (%)	Villus height (mm)			Villus area (mm2)			Crypt depth (mm)
		Duodenum	jejunum	Ileum	Duodenum	jejunum	Ileum	Duodenum	jejunum	Ileum
Control	0	1.04b	1.04	0.61	0.15	0.14	0.07	0.27	0.25	0.17
RH	2.5	1.38a	0.87	0.71	0.19	0.11	0.08	0.26	0.20	0.15
	5.0	1.14ab	0.95	0.68	0.16	0.10	0.07	0.26	0.20	0.16
SH	2.5	1.35ab	0.86	0.74	0.21	0.10	0.09	0.31	0.26	0.21
	5.0	1.34ab	0.91	0.67	0.21	0.12	0.07	0.32	0.23	0.16
SEM		0.043	0.039	0.033	0.010	0.007	0.005	0.009	0.011	0.010
p-value		0.020	0.673	0.842	0.338	0.401	0.719	0.163	0.393	0.444

• RH = rice hulls; SH = soybean hulls.
• a,bValues with different superscripts in the same column are significantly different (p<0.05).

DISCUSSION

Effect of different sources and levels of fiber on growth performance and fecal ammonia nitrogen

It is commonly reported that dietary fiber decreases nutrient digestibility and chicken performance (Sklan et al., 2003). This result is similar to that from Santos et al. (2019), who found decreased body weight gain when diets with 2.5% SH were fed to broilers from 1 to 21 d of age. Similarly, Sklan et al. (2003) found that the inclusion of up to 3% soybean hulls in diets decreased body weight gain in turkeys (1 to 4 wk of age). However, turkeys at 14 wk of age fed 6 or 9% soybean hulls had more body weight gain than those fed 3% soybean hulls. Similar to the present findings, there was no significant difference between the fiber groups and the control group in broilers from 22 to 42 d of age. Contrary to these findings, González-Alvarado et al. (2007) reported that the inclusion of a fiber source (oat hulls or soybean hulls) reduced average daily feed intake without affecting average daily gain and is consequence of the improved feed conversion ratio. This finding might be due to the differences in the level and type of dietary fiber, as well as the age of the chicken.

The addition of fiber to diets reduces the amount of NH₃ emitted from the manure of laying hens (Roberts et al., 2007) and pigs (Canh et al., 1997; Shriver et al., 2003). In typical cases, the nitrogen excreted in feces consists of undigested dietary nitrogen and endogenous nitrogen, mainly as amino acids and bacterial protein. In poultry feces, the ammonia volatilization has been attributed to the microbial decomposition of nitrogenous compounds, primarily uric acid (Li et al., 2008). Therefore, nitrogen content was determined in broiler feces. Kirchgessner et al. (1994) reported that the inclusion of moderate amounts of different fiber sources in pig diets affects the growth of bacterial populations in the large intestine, resulting in decreased NH₃ emission. Consistent with this finding, our previous study (Santos et al., 2019) found that the fecal ammonia nitrogen of broilers from 1 to 21 d of age decreased in the 2.5% RH and 5.0% SH groups. González-Alvarado et al. (2007) found that a large and well-developed gizzard improves nutrient utilization, resulting in decreased fecal ammonia nitrogen. However, in the present study, from 22 to 42 d of age, there was no significant difference in fecal ammonia nitrogen between the fiber groups and the control group. This effect might be due to the reduced grinding activity of the gizzard in the present study.

Effect of different sources and levels of fiber on carcass traits and digestive organ development

Lu et al. (1996) reported that relative organ weight could be used as an indicator of organ function. In the present study, the experimental diets with 2.5% SH significantly decreased the wing weight of chickens compared with the control. Similarly, Shahin & Abdelazim (2005) found that high fiber inclusion in broiler diets decreased carcass weight. Mateos et al. (2012) reported that dietary fiber decreased the intestinal length and weight of the organs of birds. Consequently, these changes might reduce carcass yield (Jørgensen et al., 1996).

Our present trial is in agreement with a few others (Preston et al., 2000; Taylor & Jones, 2001; Mourão et al., 2008) in which dietary fiber increased the relative length of the small intestine. The longer relative length of the small intestine in the fiber groups might be due to the increased effort of this organ to adapt to improve feed consumption and nutrient uptake (Mourão et al., 2008). However, the results of our study did not agree with those of a few other reviews. For example, Amerah et al. (2009) and Sklan et al. (2003) found that increasing the insoluble fiber in the diet reduced the length of the small intestine. These conflicting findings may be due to the differences in the physicochemical characteristics and amount of the fiber sources as well as its particle size (Mateos et al., 2012).

Effect of different sources and levels of fiber on intestinal morphology

Histologically, increased villus height and cell mitosis number in the intestine are indicators of activated villus function (Langhout et al., 1999). Intestinal crypt development affects the maintenance of crypt-cell turnover rates and intestinal maturation. Therefore, deeper crypts result in an increased intestinal absorption surface area (Geyra et al., 2001). Caspary (1992) reported that greater villus height contributes to an increased surface area for greater absorption of available nutrients. A deeper crypt indicates faster tissue turnover and higher demand for new tissue (Yason et al., 1987). This higher demand for faster turnover lowers the efficiency of the animals (Xu et al., 2003). Some researchers have demonstrated that the physicochemical characteristics of dietary fiber induce physiological and histological changes in the intestine (Jankowski et al., 2009; Juskiewicz et al., 2009). In the present study, dietary fiber in broiler diets contributed to an increase in the duodenal villus height. Sittiya et al. (2016) and Jiménez-Moreno et al. (2011) reported an improvement in the villus height:crypt depth ratio in broilers with the inclusion of whole rice grain and pea hulls, respectively. In addition, Sklan et al. (2003) found that the surface area of the small intestine of turkeys increased as the level of crude fiber in the diet increased from 2.7 to 7.9%. Awad et al. (2006) found that a greater villus height contributed to an increased surface area for greater absorption of available nutrients. The higher duodenal villus of broilers fed 2.5% RH might be related to the longer relative length of the small intestine in the fiber groups. This combined change might be because of the increasing effort of the small intestine to adapt to improve feed consumption and nutrient uptake (Mourão et al., 2008). However, the results of our study did not agree with those of Kalmendal et al. (2011), who observed that high-fiber sunflower cake inclusion resulted in linear reductions in villus height.

CONCLUSION

The inclusion of different fiber sources in the broiler diets led to the development of intestinal morphology, whereas there were few changes in the digestive organ. These results suggest that the inclusion of fiber in the diet enhances the development of the gastrointestinal tract without negatively affecting growth performance and carcass traits.

ACKNOWLEDGEMENTS

The authors wish to thank Siriruk Mongkalakittichai, Aumpajaroon Srilaoor, Sarocha Sukaiem, Sureerat Foithupthim, Pirat Wongchaikong, and Phoorichaya Soponsiri for their help during sampling.

REFERENCES

• AOAC. Association of Official Analytical Chemists. Official method of analysis. 17th ed. Gaithersburg (MD); 2000.
• Amerah AM, Ravindran V, Lentle RG. Influence of insoluble fiber and whole wheat inclusion on the performance, digestive tract development and ileal microbiota profile of broiler chickens. British Poultry Science 2009;50(3):366-375.
• Awad WA, Böhm J, Razzazi-Fazeli E, Ghareeb K, Zentek J. Effect of addition of a probiotic microorganism to broiler diets contaminated with deoxynivalenol on performance and histological alterations of intestinal villi of broiler chickens. Poultry Science 2006;85(6):974-979.
• Battye R, Battye W, Overcash C, Fudge S. Development and selection of ammonia emission factors [report PB-95-123915/XAB]. Durham: Research Triangle Park; 1994.
• Beccaccia A, Calvet S, Cerisuelo A, Ferrer P, Garcia-Rebollar P, De Blas C. Effects of nutrition on digestion efficiency and gaseous emissions from slurry in growing-finishing pigs. I. Influence of the inclusion of two levels of orange pulp and carob meal in isofibrous diets. Animal Feed Science and Technology 2015;208:158-169.
• Bindelle J, Buldgen A, Delacollette M, Wavreille J, Agneessens R, Destain JP, et al. Influence of source and concentrations of dietary fiber on in vivo nitrogen excretion pathways in pigs as reflected by in vitro fermentation and nitrogen incorporation by fecal bacteria. Journal of Animal Science 2009;87(2):583-593.
• Canh TT, Verstegen MWA, Aarnink AJA, Schrama JW. Influence of dietary factors on nitrogen partitioning and composition of urine and feces of fattening pigs. Journal of Animal Science 1997;75(3):700-706.
• Carlile FS. Ammonia in poultry houses: a literature review. World's Poultry Science Journal 1984;40(2):99-113.
• Caspary WF. Physiology and pathophysiology of intestinal absorption. The American Journal of Clinical Nutrition 1992;55Suppl:299S-308S.
• Ferket PR, Van Heugten E, Van Kempen TA, Angel R. Nutritional strategies to reduce environmental emissions from nonruminants. Journal of Animal Science 2002;80 E-Suppl:E168-E182.
• Geyra A, Uni Z, Sklan D. The effect of fasting at different ages on growth and tissue dynamics in the small intestine of the young chick. British Journal of Nutrition 2001;86(1):53-61.
• González-Alvarado JM, Jiménez-Moreno E, Lázaro R, Mateos GG. Effect 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 2007;86(8):1705-1715.
• Hetland H, Svihus B, Choct M. Role of insoluble fiber on gizzard activity in layers. Journal of Applied Poultry Research 2005;14(1):38-46.
• Hetland H, Svihus B, Krogdahl Å. Effects of oat hulls and wood shavings on digestion in broilers and layers fed diets based on whole or ground wheat. British Poultry Science 2003;44(2):275-282.
• Iji PA, Saki A, Tivey DR. Body and intestinal growth of broiler chicks on a commercial starter diet. 1. Intestinal weight and mucosal development. British Poultry Science 2001;42(4):505-513.
• Jankowski J, Juskiewicz J, Gulewicz K, Lecewicz A, Slominski BA, Zdunczyk Z. The effect of diets containing soybean meal, soybean protein concentrate, and soybean protein isolate of different oligosaccharide content on growth performance and gut function of young turkeys. Poultry Science 2009;88(10):2132-2140.
• Jha R, Berrocoso JF. Dietary fiber and protein fermentation in the intestine of swine and their interactive effects on gut health and on the environment: A review. Animal Feed Science and Technology 2016;212:18-26.
• Jiménez-Moreno E, Chamorro S, Frikha M, Safaa HM, Lázaro R, Mateos GG. 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 2011;168:100-112.
• Jørgensen H, Zhao XQ, Knudsen KEB, Eggum BO. The influence of dietary fiber source and level on the development of the gastrointestinal tract, digestibility and energy metabolism in broiler chickens. British Journal of Nutrition 1996;75(3):379-395.
• Juskiewicz J, Jankowski J, Zdunczyk Z, Lecewicz A, Przybylska-Gornowicz B, Zieba M. Effect of diets with different contents of soybean [alpha]-galactosides and crude fiber on modification of duodenal microstructure and selected parameters of nutrient utilization in young turkeys. Polish Journal of Veterinary Science 2009;12(4):455.
• Kalmendal R, Elwinger K, Holm L, Tauson R. High-fiber sunflower cake affects small intestinal digestion and health in broiler chickens. British Poultry Science 2011;52(1):86-96.
• Kirchgessner M, Kreuzer M, Machmüller A, Roth-Maier DA. Evidence for a high efficiency of bacterial protein synthesis in the digestive tract of adult sows fed supplements of fibrous feedstuffs. Animal Feed Science and Technology 1994;46(3-4):293-306.
• Kreuzer M, Machmüller A, Gerdemann MM, Hanneken H, Wittmann M. Reduction of gaseous nitrogen loss from pig manure using feeds rich in easily-fermentable non-starch polysaccharides. Animal Feed Science and Technology 1998;73(1/2):1-19.
• Langhout DJ, Schutte JB, Van Leeuwen P, Wiebenga J, Tamminga S. Effect of dietary high-and low-methylated citrus pectin on the activity of the ileal microflora and morphology of the small intestinal wall of broiler chicks. British Poultry Science 1999;40(3):340-347.
• Li H, Xin H, Liang Y, Burns RT. Reduction of ammonia emissions from stored laying hen manure through topical application of zeolite, Al+ Clear, Ferix-3, or poultry litter treatment. Journal of Applied Poultry Research 2008;17(4):421-431.
• Lu CD, Schoknecht PA, Ellis KJ, Shypailo R, Su DR, Pond WG. Differential compensatory organ growth in young pigs after short-term rehabilitation from protein deficiency. Nutrition Research 1996;16(4):627-637.
• Mateos GG, Jiménez-Moreno E, Serrano MP, Lázaro RP. Poultry response to high levels of dietary fiber sources varying in physical and chemical characteristics. Journal of Applied Poultry Research 2012;21(1):156-174.
• Mateos GG, Lázaro R, Gracia MI. The feasibility of using nutritional modifications to replace drugs in poultry feeds. Journal of Applied Poultry Research 2002;11(4):437-452.
• Miles DM, Branton SL, Lott BD. Atmospheric ammonia is detrimental to the performance of modern commercial broilers. Poultry Science 2004;83(10):1650-1654.
• Montagne L, Pluske JR, Hampson DJ. A review of interactions between dietary fiber and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Animal Feed Science and Technology 2003;108(1-4):95-117.
• Mourão JL, Pinheiro VM, Prates JAM, Bessa RJB, Ferreira LMA, Fontes CMGA, et al. Effect of dietary dehydrated pasture and citrus pulp on the performance and meat quality of broiler chickens. Poultry Science 2008;87(4):733-743.
• NRC - National Research Council. Nutrient requirements of poultry, 9thed. Washington: National Academy Press; 1994.
• Perez VG, Jacobs CM, Barnes J, Jenkins MC, Kuhlenschmidt MS, Fahey Jr GC, et al. Effect of corn distillers dried grains with solubles and Eimeria acervulina infection on growth performance and the intestinal microbiota of young chicks. Poultry Science 2011;90(5):958-64.
• Preston CM, McCracken KJ, McAllister A. Effect of diet form and enzyme supplementation on growth, efficiency and energy utilisation of wheat-based diets for broilers. British Poultry Science 2000;41(3):324-331.
• Rezaei M, Karimi Torshizi MA, Rouzbehan Y. The influence of different levels of micronized insoluble fiber on broiler performance and litter moisture. Poultry Science 2011;90(9):2008-2012.
• Roberts SA, Xin H, Kerr BJ, Russell JR, Bregendahl K. Effects of dietary fiber and reduced crude protein on ammonia emission from laying-hen manure. Poultry Science 2007;86:1625-1632.
• Santos dos S, Laosutthipong C, Yamauchi K, Thongwittaya N, Sittiya J. Effects of dietaryfiber on growth performance, fecal ammonia nitrogen. Proceedings of the 4th Industrial Revolution and Its Impacts; 2019 March 27-30; Thailand: Walailak Procedia; 2019. p.4-73.
• Sarikhan M, Shahryar HA, Gholizadeh B, Hosseinzadeh MH, Beheshti B, Mahmoodnejad A. Effects of insoluble fiber on growth performance, carcass traits and ileum morphological parameters on broiler chick males. International Journal of Agriculture and Biology 2010;12(4):531-536.
• Shahin KA, Abd Elazeem F. Effects of breed, sex and diet and their interactions on carcass composition and tissue weight distribution of broiler chickens. Archives Animal Breeding 2005;48(6):612-626.
• Shriver JA, Carter SD, Sutton AL, Richert BT, Senne BW, Pettey LA. Effects of adding fiber sources to reduced-crude protein, amino acid-supplemented diets on nitrogen excretion, growth performance, and carcass traits of finishing pigs. Journal of Animal Science 2003;81(2):492-502.
• Sittiya J, Yamauchi K, Takata K. Effect of replacing corn with whole-grain paddy rice and brown rice in broiler diets on growth performance and intestinal morphology. Journa lof Animal Physiology and Animal Nutrition 2016;100(2):381-390.
• Sklan D, Smirnov A, Plavnik I. The effect of dietary fiber on the small intestines and apparent digestion in the turkey. British of Poultry Science 2003;44(5):735-740.
• Taylor RD, Jones GPD. The effect of whole wheat, ground wheat and dietary enzymes on performance and gastro-intestinal morphology of broilers. Proceedings of Australian Poultry Science Symposium; 2001; Sydney. Australia: Australian Poultry Science Symposium; 2001. p.187-190.
• USDA. Grain: world markets and trade. Washington; 2018.
• Van Soest PV, Robertson JB, Lewis BA. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 1991;74(10):3583-3597.
• Xu ZR, Hu CH, Xia MS, Zhan XA, Wang MQ. Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poultry Science 2003;82(6):1030-1036.
• Yason CV, Summers BA, Schat KA. Pathogenesis of rotavirus infection in various age groups of chickens and turkeys: pathology. American Journal of Veterinary Research 1987;48(6):927-938.

• FUNDING

  This work was supported by a grant from The Thailand Research Fund (TRF), project no. MRG6080075.

Publication Dates

• Publication in this collection
  05 June 2020
• Date of issue
  2020

History

• Received
  25 Sept 2019
• Accepted
  10 Dec 2019