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Effect of Dietary Almond Hull on Growth Performance, Nutrient Digestibility, Organ Weight, Caecum Microbial Counts, and Noxious Gas Emission in Broilers.

ABSTRACT

This study was conducted to investigate the impact of a diet supplemented with almond hulls on growth performance, nutrient utilization, cecum microbiota, noxious gas emissions, and the organ weight of broilers. A total of 540, one-day-old Ross-308 broilers were used in this 35-day-long feeding trial. All birds were divided into 3 treatment groups of 10 replicates, each with 18 chicks (18 birds/replication), according to a completely randomized design. The Tukey’s test was used to compare the differences among the 3 treatments. The dietary treatments were a basal diet supplemented with 0%, 1%, and 2% almond hull, respectively. The body weight gain (BWG) of broilers supplemented with almond hull improved (p<0.05) during days 1-7 and in the overall period, whereas it tended to increase (p<0.10) during days 22-35. Additionally, feed intake (FI) tended to increase (p<0.10) during days 1-7 and in the overall experiment period. However, the feed conversion ratio (FCR) remained unchanged (p>0.05) through the supplementation of almond hull up to 2%. The nutrient digestibility of nitrogen and energy tended to increase (p<0.10), whereas the digestibility of dry matter was unchanged (p>0.05). Inclusion of almond hull in broiler diets showed a tendency to decrease (p<0.10) caecal Salmonella count. Moreover, broilers fed a diet supplemented with almond hull decreased (p<0.05) their excreted NH3 emissions. Similar (p>0.05) organ weights were found in broilers with a 2% almond hull-supplemented diet as compared to the control diet. In summary, incorporating up to 2% of almond hulls into broiler diets can enhance growth performance, increase nutrient digestibility, and reduce both microbial count and noxious gas emissions, thereby establishing almond hulls as a promising ingredient for broiler feed.

Keywords:
Almond husk; poultry; productivity; emanations; and nutrient utilization

INTRODUCTION

Almond hulls, a byproduct of almond processing, offer a unique composition that includes fibers, nutrients, and bioactive compounds (Salgado-Ramos et al., 2022Salgado-Ramos M, Martí-Quijal FJ, Huertas-Alonso AJ, et al. Almond hull biomass: preliminary characterization and development of two alternative valorization routes by applying innovative and sustainable technologies. Industrial Crops Productions 2022;179:114697.). In recent years, both researchers and producers have been exploring alternative feed resources to enhance the economic and nutritional aspects of broiler diets. Among these alternatives, the supplementation of almond hulls has gained attention for its potential to contribute to broiler nutrition while addressing sustainability concerns. In response to this growing demand, it is urgent for the poultry industry increase feed production to adjust the growth of poultry farming. This need leads to increased exploration of alternative feed ingredients that can be produced locally, aiming to replace more expensive feed components in poultry farming. Some examples of unconventional feed components considered for the broiler industry are corn gluten meal, distillers’ dried grains with solubles, wheat middlings, brewers’ spent grain, almond hulls, and soybean hulls. While almond hulls themselves are not among the most expensive ingredients, their inclusion in the diet can partially replace more expensive components, such as some portions of corn or soybean meal. This substitution helps manage costs while maintaining dietary balance. It’s important for nutritionists to carefully formulate diets to optimize cost-effectiveness without compromising the nutritional needs of the broilers. The amount of available surplus of this ingredient is due to the rapid increase in almond production for humans. It is recognized as a fibrous resource, and possesses moderate nutritive value for ruminants and swine (Williams et al., 2018Williams SRO, Chaves A V., Deighton MH, et al. Influence of feeding supplements of almond hulls and ensiled citrus pulp on the milk production, milk composition, and methane emissions of dairy cows. Journal of Dairy Science 2018;101(3):2072-83. https://doi.org/10.3168/jds.2017-13440.
https://doi.org/10.3168/jds.2017-13440...
; Yalchi & Kargar, 2010Yalchi T, Kargar S. Chemical composition and in situ ruminal degradability of dry matter and neutral detergent fiber from almond hulls. Journal of Food, Agriculture and Environment 2010;8(2):781-4.). Despite dietary fibers being traditionally regarded as nutrient diluters on nutrient digestion and absorption, their importance in boosting immunity and sustaining gut health in broilers has recently gained attention (Jha & Leterme, 2012Jha R, Leterme P. Feed ingredients differing in fermentable fibre and indigestible protein content affect fermentation metabolites and faecal nitrogen excretion in growing pigs. Animal 2012;6(4): 603-11. https://doi.org/10.1017/S1751731111001844.
https://doi.org/10.1017/S175173111100184...
). Conversely, some previous researches has shown that insoluble fibers in minimal quantities improve growth performance, digestion, absorption, and gut flora in broilers (Gemen et al., 2011Gemen R, De Vries JJF, Slavin JL. Relationship between molecular structure of cereal dietary fiber and health effects: Focus on glucose/insulin response and gut health. Nutrition Reviews 2011;69(1):22-33. https://doi.org/10.1111/j.1753-4887.2010.00357.x.
https://doi.org/10.1111/j.1753-4887.2010...
; Jiménez-Moreno et al., 2013aJiménez-Moreno E, Frikha M, De Coca-Sinova A, et al. Oat hulls and sugar beet pulp in diets for broilers 1. Effects on growth performance and nutrient digestibility. Animal Feed Science and Technology 2013a;182(1-4):33-43. https://doi.org/10.1016/j.anifeedsci.2013.03.011.
https://doi.org/10.1016/j.anifeedsci.201...
b; Sadeghi et al., 2015Sadeghi A, Toghyani M, Gheisari A. Effect of various fiber types and choice feeding of fiber on performance, gut development, humoral immunity, and fiber preference in broiler chicks. Poultry Science 2015;94(11):2734-43. https://doi.org/10.3382/ps/pev292.
https://doi.org/10.3382/ps/pev292...
). Broilers fed diets with insoluble fiber from oat hulls perform better in terms of growth when their inclusion level is between 2 and 3% (Mateos et al., 2012Mateos GG, Jiménez-Moreno E, Serrano MP, et al. Poultry response to high levels of dietary fiber sources varying in physical and chemical characteristics. Journal of Applied Poultry Research 2012;21(1):156-74. https://doi.org/10.3382/japr.2011-00477.
https://doi.org/10.3382/japr.2011-00477...
). Beyond dietary fibers, almond hulls reportedly contain a total sugar content ranging from 25 to 46%, a potential energy source in broiler diets (Holtman et al., 2015Holtman KM, Offeman RD, Franqui-Villanueva D, et al. Countercurrent extraction of soluble sugars from almond hulls and assessment of the bioenergy potential. Journal of agricultural and food chemistry 2015;63(9):2490-8. https://doi.org/10.1021/jf5048332
https://doi.org/10.1021/jf5048332...
). Moreover, almond hulls are abundant in antioxidants like polyphenols, triterpenoids, betulinic acid, oleanolic acid, and ursolic acid, all known for their robust antioxidative activities (Esfahlan et al., 2010Esfahlan AJ, Jamei R, Esfahlan RJ. The importance of almond (Prunus amygdalus L.) and its by-products. Food Chemistry 2010;120(2):349-60. https://doi.org/10.1016/j.foodchem.2009.09.063.
https://doi.org/10.1016/j.foodchem.2009....
; Prgomet et al., 2017Prgomet I, Goncalves B, Domínguez-Perles R, et al. Valorization challenges to almond residues: Phytochemical composition and functional application. Molecules 2017;22(10):1774. https://doi.org/10.3390/molecules22101774.
https://doi.org/10.3390/molecules2210177...
). The dietary fibers, fermentable sugars, and antioxidants in almond hulls could present valuable nutrients for broilers (Takeoka & Dao, 2003Takeoka GR, Dao LT. Antioxidant constituents of almond [Prunus dulcis (Mill.) D.A. Webb] hulls. Journal of Agricultural and Food Chemistry 2003;51(2):496-501. https://doi.org/10.1021/jf020660i.
https://doi.org/10.1021/jf020660i...
; Jha & Leterme, 2012). As broilers cannot digest higher amounts of fiber due to the absence of microbial digestion like ruminants (Mateos et al., 2012), we planned to work with a smaller amount of almond hull in this experiment. We hypothesized that the incorporation of the lower level (2%) of almond hulls in a broiler diet would result in improved growth performance, nutrient digestibility, microbial count, and lowered noxious gas emissions. The objective of this study was to assess the impact of dietary supplementation of almond hulls on the growth performance, nutritional digestibility, organ weight, caecum microbial counts, and noxious gas emissions of broilers.

MATERIALS AND METHODS

The Institutional Animal Care and Use Committee of Dankook University, South Korea, investigated and approved the experimental protocols (DK-1-2220) on the management and care of animals.

Processing of almond hull

Almond hulls are the outer protective layer of the almond seed and are obtained after the almond kernels are removed.

The process typically involves the following steps:

  1. Harvesting Almonds: Almond trees produce almonds, which consist of an outer hull containing an edible kernel inside.

  2. Hulling: The almonds are mechanically hulled to remove the outer hull, leaving the edible almond kernel.

  3. Separation: The hulled almonds are then separated from the hulls.

  4. Processing Almond Hulls: The separated almond hulls can be processed to create a feed ingredient suitable for poultry diets. This processing may involve grinding, drying, and possibly pelleting.

Experimental design, animals, and diets

In a 35-day study, 540 broilers (one-day-old male ROSS 308) with average body weights of 47.91± 0.28 g were analyzed to assess growth performance, nutritional digestibility, caecum microbiota, noxious gas emission, and organ weight. Broilers were allotted to three treatments, each with ten replications and 18 birds per pen, according to a completely randomized design. The following diet treatment groups were set up: 1) CON, Basal diet, 2) TRT1, CON + 1% almond hull, and 3) TRT2, CON + 2% almond hull.

The experiment was carried out at the Dankook University research farm in Sejong, South Korea. The guidelines of NRC (1994) were used to formulate the composition of the basic diet (Table 1). The broiler house room temperature was 33 ± 1°C for the first week, and then it was consistently reduced to 24 ± 1°C, with more than 60% retaining moisture (Munezero et al., 2022Munezero O, Zhang ZF, Kim IH. The Effects of Yucca Schidigera Extract and Multi-carbohydrase in Different Crude Protein Diets on Growth Performance, Nutrient Digestibility, Carcass Parameters and Excreta Noxious Gas Contents in Broilers. Brazilian Journal of Poultry Science 2022;25(1). https://doi.org/10.1590/1806-9061-2022-1650
https://doi.org/10.1590/1806-9061-2022-1...
). A nipple drinker and a plastic feeder were attached to each pen, through which birds had free access to feed and water during the experiment. The measurement of each pen was 1m× 1.6m (three-layer battery cages), and the density of birds was 12 birds/square meter. Light and dark periods were respectively maintained at 18 h and 6 h every day. The poultry house was duly maintained under proper biosecurity and hygienic conditions.

Table 1
Broiler feed composition (as fed-basis).

Chemical analysis, sampling, and measurements

Growth performance

Body weight was calculated per treatment on days 0, 7, 21, and the last day (35 days). Feed intake was measured according to this formula:

F e e d c o n v e r s i o n r a t i o ( F C R ) = F e e d int a k e B W G

Feed conversion ratio (FCR) was calculated following this calculation:

Nutrient Digestibility

Chromium oxide (Cr2O3, 0.20%), an indigestible marker mixed diet, was given to broilers 7 days before the end of the experiment. On day 35, excreta were collected to evaluate nutrient digestibility. The feed and excreta sample, dried in an oven at 60 °C for 72 hours, was pulverized to a fine consistency, enough for passing through a 1 mm screen. After that, the dried samples were analyzed using AOAC standard methods (2022) for GE, DM, and N. UV absorption spectrophotometry (UV-1201, Shimadzu, Japan) was used to determine the levels of chromium. We followed the following formula to calculate digestibility: Digestibility=1-[(Nf×Cd)/(Nd×Cf)] ×100, where Nf = concentration of nutrient in excreta (% DM), Nd = concentration of nutrient in the diet, Cd = concentration of chromium in the diet, and Cf = concentration of chromium in the excreta (Munezero et al., 2022Munezero O, Zhang ZF, Kim IH. The Effects of Yucca Schidigera Extract and Multi-carbohydrase in Different Crude Protein Diets on Growth Performance, Nutrient Digestibility, Carcass Parameters and Excreta Noxious Gas Contents in Broilers. Brazilian Journal of Poultry Science 2022;25(1). https://doi.org/10.1590/1806-9061-2022-1650
https://doi.org/10.1590/1806-9061-2022-1...
).

Organ weight

At the end of the experiment (35 days), samples including breast meat, liver, bursa of fabricius, abdominal fat, spleen, and gizzard were weighed using an electronic balance (Sartorius BCE323I-1S Entris II Essential Balance Int. Cal., 320g, 1mg). A total of 60 broilers were slaughtered, with 20 birds randomly selected per treatment (2 birds per replication). The weight of all organs was indicated as a percentage of body weight.

Caecum microbial counts

Excreta samples were sourced from 10 pens per treatment and pooled before being transported to the study site and submitted to a microbiological examination while being kept chilled. One gram of excreta was diluted in sterile peptone water, and the mixture was vortexed for one minute. Escherichia coli, Lactobacillus, and Salmonella were isolated by adding live bacteria via a series of 10-fold dilutions. Three kinds of agar were used for these bacteria: MRS agar (Difco, USA) for Lactobacillus, MacConkey agar (Difco, USA) for E.coli, and SS agar (Difco, USA) for Salmonella. Before colony counting, Lactobacillus, E. coli, and Salmonella were incubated at 39 °C for 48 hours, 37 °C for 24 hours, and 37 °C for 24 hours, respectively. After adding up the colonies, the results were displayed as log10 converted data (Shanmugam et al., 2022Shanmugam S, Park JH, Cho S, et al. Silymarin seed extract supplementation enhances the growth performance, meat quality, and nutrients digestibility, and reduces gas emission in broilers. Animal Bioscience 2022 ;35(8): 215. https://doi.org/10.5713/ab.21.0539
https://doi.org/10.5713/ab.21.0539...
).

Noxious gas emission

300g of excreta samples were taken from each pen and combined uniformly. The samples were collected using a stainless-steel collection tray and stored in pairs in 2.6-L plastic boxes. A small hole was first drilled in the center of the side wall of the plastic boxes to be prepared, and then the hole was sealed with adhesive plastic items. Fermentation of the samples required storage at room temperature for seven days. After the fermentation period, the MultiRAE (MultiRAE Lite model PGM-6208, RAE, USA) was used for gas detection for ammonia (NH3), hydrogen Sulfide (H2S), methyl mercaptans, carbon dioxide (CO2) and acetic acid. In these measurements, a hole was made in the adhesive plaster, and 100 mL of overhead air was sampled approximately two centimeters above the fecal surface. Each box was again wrapped with adhesive plaster after air sampling. After 48 hours, head space measurements were once more carried out. Two readings from the same box were averaged to determine the gas contents.

Statistical Analyses

The GLM technique was applied to analyze the data using the SAS software (Version 9.4; SAS Inst. Inc., Cary, NC, US). Data on growth performance, nutrient digestibility, organ weight, caecum microbial counts, and noxious gas emission were observed on a pen basis, whereas data on organ weight was calculated for individual broilers. The Tukey’s test was used to compare the differences among the three treatments. Linear, quadratic polynomial contrasts were applied to examine the effect of the dietary treatments. The standard error of the mean (SEM) was used to account for the variability of the data, the level of significance was determined at p<0.05, and tendencies were identified at p<0.10.

RESULTS AND DISCUSSION

Almond hulls as fiber sources showed the same physical and chemical traits as the hulls of other cereals, such as oats, rice, and soybeans. The effect of the dietary supplementation with almond hulls at up to 2% in broiler diets is shown in Table 2. Body weight gain (p<0.05) and feed intake (p<0.10) were increased through the supplementation of the almond hull during the first week of the experiment. During days 22-35, body weight gain tended to increase (p<0.10) through the supplementation of almond hulls. and in the overall experimental period, there was an improved body weight gain (p<0.05) and feed intake (p<0.10) through the supplementation of the almond hulls. Similarly, according to Jiménez-Moreno et al. (2013aJiménez-Moreno E, Frikha M, De Coca-Sinova A, et al. Oat hulls and sugar beet pulp in diets for broilers 1. Effects on growth performance and nutrient digestibility. Animal Feed Science and Technology 2013a;182(1-4):33-43. https://doi.org/10.1016/j.anifeedsci.2013.03.011.
https://doi.org/10.1016/j.anifeedsci.201...
), 50 g of oat hulls in diets had a linear influence on the total relative weight of the intestinal tract and a quadratic effect on the body weight gain of broilers. Additionally, Adewole et al. (2020) reported that incorporating 3% of oat hulls in the diet resulted in enhanced broiler growth performances and reduced FCR. Although the major fibers found in almond hulls (such as cellulose, hemicellulose, and lignin) are insoluble in water and not easily fermentable (Holtman et al., 2015Holtman KM, Offeman RD, Franqui-Villanueva D, et al. Countercurrent extraction of soluble sugars from almond hulls and assessment of the bioenergy potential. Journal of agricultural and food chemistry 2015;63(9):2490-8. https://doi.org/10.1021/jf5048332
https://doi.org/10.1021/jf5048332...
), almond hulls still contain energy in the form of fermentable sugars, including glucose, fructose, and sucrose. Although the fermentation process may not be as significant as in ruminants, the positive impact on the gut environment can indirectly influence broilers’ body weight and performance. When comparing the starch present in cereals to sugars, it can be observed that sugars have a lower molecular weight and are absorbed more easily (Aller et al., 2011Aller EEJG, Abete I, Astrup A, et al. Starches, sugars, and obesity. Nutrients 2011;3(3):341-369. https://doi.org/10.3390/nu3030341.
https://doi.org/10.3390/nu3030341...
). Thus, insoluble fibers could improve body weight and nutrient utilization in broilers (Adedokun et al., 2012Adedokun SA, Ajuwon KM, Romero LF, et al. Ileal endogenous amino acid losses: response of broiler chickens to fiber and mild coccidial vaccine challenge. Poultry Science 2012;91(4):899-907. https://doi.org/10.3382/ps.2011-01777.
https://doi.org/10.3382/ps.2011-01777...
). Jiménez-Moreno et al. (2013ab) also reported that a moderate level of 3% dietary fiber was deemed appropriate for broilers, while including dietary fiber up to 3.6% in their diets could promote the growth and development of the gastrointestinal tract organs in young broilers. However, including a high amount of dietary fibers could have a negative impact on the growth of broilers (Mateos et al., 2012Mateos GG, Jiménez-Moreno E, Serrano MP, et al. Poultry response to high levels of dietary fiber sources varying in physical and chemical characteristics. Journal of Applied Poultry Research 2012;21(1):156-74. https://doi.org/10.3382/japr.2011-00477.
https://doi.org/10.3382/japr.2011-00477...
). Furthermore, a diet containing 9% of almond hulls had more significant adverse effects on broilers’ body weight gain (BWG), feed intake (FI), and feed conversion ratio (FCR) during the 0-19-day period (Wang et al., 2021aWang J, Kong F, Kim WK. Effect of almond hulls on the performance, egg quality, nutrient digestibility, and body composition of laying hens. Poultry Science 2021a;100(9):101286. https://doi.org/10.1016/J.PSJ.2021.101286
https://doi.org/10.1016/J.PSJ.2021.10128...
). According to the previous study, it was indicated that broilers fed 10% of almond hulls had reduced body weight and lower fat percentage (Wang et al., 2021b). The slight reduction in body weight gain (BWG) resulting from the inclusion of a high level of almond hulls can be attributed to the high-fiber nature of the diet, which is known to promote weight loss, particularly in terms of body fat (Walugembe et al., 2014Walugembe M, Rothschild MF, Persia ME. Effects of high fiber ingredients on the performance, metabolizable energy and fiber digestibility of broiler and layer chicks. Animal Feed Science and Technology 2014;188:46-52. https://doi.org/10.1016/j.anifeedsci.2013.09.012.
https://doi.org/10.1016/j.anifeedsci.201...
). The study suggests that utilized 1% and 2% almond hulls, despite being water insoluble, may still be digested and absorbed by the body. This digestion and absorption of fiber likely contributed to the observed improvement in body weight gain (BWG).

Table 2
The effect of dietary almond hull supplementation on growth performance of broilers1

The nutrient digestibility of broilers in different treatment groups is shown in Table 3. The current study showed that the inclusion of almond hulls at 0-2% tended to increase the digestibility of nitrogen and energy. However, 0-2% inclusion rates had no significant influence on the digestibility of DM. Similarly, almond hull at inclusion levels of 7.5-15% improved the gross energy and N digestibility of poultry but had no impact on apparent dry matter digestibility (Wang et al., 2021aWang J, Kong F, Kim WK. Effect of almond hulls on the performance, egg quality, nutrient digestibility, and body composition of laying hens. Poultry Science 2021a;100(9):101286. https://doi.org/10.1016/J.PSJ.2021.101286
https://doi.org/10.1016/J.PSJ.2021.10128...
). Additionally, Scholey et al. (2020Scholey DV, Marshall A, Cowan AA. Evaluation of oats with varying hull inclusion in broiler diets up to 35 days. Poultry Science 2020;99(5):2566-72. .) stated that the digestibility of broilers is increased without any adverse impacts on gut fill and intake when the diet contains a lower level of oat hull (3% of the total diet). However, the performance of broilers and nutrient digestibility were unaffected by the addition of 2% lignocellulose, according to Kheravii et al. (2017Kheravii SK, Swick RA, Choct M, et al. Coarse particle inclusion and lignocellulose-rich fiber addition in feed benefit performance and health of broiler chickens. Poultry Science 2017;96(9):3272-81. https://doi.org/10.3382/ps/pex123.
https://doi.org/10.3382/ps/pex123...
). On the other hand, according to Wang et al. (2021b), the ileal digestibility of DM and energy was reduced when 3% and 9% almond hulls were used, but the inclusion of the 6% almond hull had no significant effect on DM, ME, or ileal protein digestibility. The present research revealed that nitrogen digestibility and energy digestibility tend to increase, suggesting that the almond hull’s entire fiber content (lower amount of hulls, at 2%) has likely been properly ingested. Consequently, almond hulls in the diet exhibit functional properties similar to those of proper insoluble fibers, contributing to their beneficial effects. Jiménez-Moreno et al. (2010Jiménez-Moreno E, González-Alvarado JM, González-Sánchez D, et al. Effects 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 2010;89(10):2197-212. https://doi.org/10.3382/ps.2010-00771.
https://doi.org/10.3382/ps.2010-00771...
) found that the inclusion of insoluble fiber in broiler diets significantly stimulates the proventriculus to produce a substantial amount of hydrochloric acid (HCl). The substantial production of HCl in the proventriculus has the potential to enhance pepsin activity, promote protein synthesis, and improve nutrient utilization in broilers (Macelline et al., 2021Macelline, SP, Chrystal PV, Liu SY, et al. The dynamic conversion of dietary protein and amino acids into chicken-meat protein. Animals 2021; 11(8):2288. https://doi.org/10.3390/ani11082288.
https://doi.org/10.3390/ani11082288...
).

Table 3
The effect of dietary almond hull supplementation on nutrient digestibility of broilers1

The main site of microbial fermentation in poultry is the cecum. The microbiota of the caeca can change in response to changes in dietary fiber levels, which may indicate that fiber components have been transported to the caeca (Svihus et al., 2013Svihus B, Choct M, Classen HL. Function and nutritional roles of the avian caeca: a review. World's Poultry Science Journal 2013;69(2):249-64. https://doi.org/10.1017/S0043933913000287.
https://doi.org/10.1017/S004393391300028...
). Previous research has indicated that the greater fiber contents in oat hull may boost bacterial population (Kheravii et al., 2018). The fiber sources from almond hulls, which are primarily lignin and cellulose, may contribute to microbial diversity (Wang et al., 2021bWang J, Singh AK, Kong F, et al. Effect of almond hulls as an alternative ingredient on broiler performance, nutrient digestibility, and cecal microbiota diversity. Poultry Science 2021b;100(3):100853. https://doi.org/10.1016/j.psj.2020.11.030.
https://doi.org/10.1016/j.psj.2020.11.03...
c). The effect of dietary almond hull supplementation on the caecum microbial count is shown in Table 4. Caecal Salmonella counts tended to reduce (p<0.05), whereas the caecal Lactobacillus and E. coli counts remained unchanged through the dietary supplementation of almond hull. According to Xu et al. (2003Xu ZR, Hu CH, Xia MS, et al. Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poultry Science 2003;82(6)1030-36. https://doi.org/10.1093/ps/82.6.1030.
https://doi.org/10.1093/ps/82.6.1030...
), when a fructo-oligosaccharide was introduced to broiler chicken diets, the overall number of anaerobes, including Bifidobacteria and Lactobacilli, increased in the caeca, while the amount of E. Coli declined. The addition of 0.2% xylo-oligomers did not significantly alter the number of caecal enterobacteria or Lactobacilli, but the inclusion of these oligosaccharides in the diet significantly increased the number of Bifidobacteria, from 103 to 108, in just one week (Courtin et al., 2008Courtin CM, Swennen K, Broekaert WF, et al. Effects of dietary inclusion of xylooligo- saccharides, arabinoxylooligosaccha- rides and soluble arabinoxylan on the microbial composition of caecal contents of chickens. Journal of the Science of Food and Agriculture 2008;88(14):2517-22.). Rougière and Carré (2010Rougière N, Carré B. Comparison of gastrointestinal transit times between chickens from D + and D- genetic lines selected for divergent digestion efficiency. Animal 2010;4(11):1861-72. https://doi.org/10.1017/S1751731110001266.
https://doi.org/10.1017/S175173111000126...
) discovered just a modest trend for the caecal microbial count to increase when broiler chicks were fed diets containing 15% sunflower hulls. At a dose of 0.5% lignocellulose (insoluble fibre source), it was demonstrated that Lactobacillus spp. and Bifidobacterium spp. populations increased, while E. coli populations decreased (Boguslawska-Tryk et al., 2015Boguslawska-Tryk M, Szymeczko R, Piotrowska A, et al. Ileal and cecal microbial population and short-chain fatty acid profile in broiler chickens fed diets supplemented with lignocellulose. Pakistan Veterinary Journal 2015;35(2).). Receiving fermentable lignocellulose in the cecum is necessary for the diversity of the bacterial population in the cecum of broilers (Zeitz et al., 2019Zeitz JO, Neufeld K, Potthast C, et al. Effects of dietary supplementation of the lignocelluloses FibreCell and OptiCell on performance, expression of inflammation-related genes and the gut microbiome of broilers. Poultry Science 2019;98(1):287-97. https://doi.org/10.3382/ps/pey345.
https://doi.org/10.3382/ps/pey345...
). However, no significant differences in the diversity of the caecal microbiota were found between treatments at 3%, 6%, and 9% inclusion levels of the almond prime hull (Wang et al., 2021a). Indeed, the variation in results regarding the effects of almond hull inclusion on caecum microbial population in broilers could be influenced by factors such as the level of almond hull inclusion, the source of fiber used, and the specific strain of birds used in our study. Furthermore, we know that protein utilization may occur while birds may also have lower pH in the upper digestive tract (Macelline et al., 2021Macelline, SP, Chrystal PV, Liu SY, et al. The dynamic conversion of dietary protein and amino acids into chicken-meat protein. Animals 2021; 11(8):2288. https://doi.org/10.3390/ani11082288.
https://doi.org/10.3390/ani11082288...
), which was not detected in our study. The later digestive tract pathogenic bacteria may be affected by this lower pH, which encourages the growth of helpful bacteria (Engberg et al., 2004Engberg RM, Hedemann MS, Steenfeldt S, et al. Influence of whole wheat and xylanase on broiler performance and microbial composition and activity in the digestive tract. Poultry Science 2004 ;83(6):925-938. https://doi.org/10.1093/ps/83.6.925.
https://doi.org/10.1093/ps/83.6.925...
). In the current study, Salmonella counts decreased, which may be due to lower digestive tract pH and the phenolic compound contents of almond hulls.

Table 4
The effect of dietary almond hull supplementation on the caecum microbial counts of broilers1

The effect of dietary supplementation of almond hull in broiler diets on the excretal noxious gas emission is shown in Table 5. In this current study, NH3 reduced significantly, but there was no effect on other noxious gases such as H2S, Methyl mercaptans, CO2, and Acetic acid. Excreta noxious gas levels in broilers are influenced by the nutrient digestibility of the feed and gut microbiota (Park & Kim, 2020Park JH, Kim IH. Effects of dietary Achyranthes japonica extract supplementation on the growth performance, total tract digestibility, cecal microflora, excreta noxious gas emission, and meat quality of broiler chickens. Poultry Science 2020; 99(1):463-70. https://doi.org/10.3382/ps/pez533
https://doi.org/10.3382/ps/pez533...
). According to (Xu et al., 2003Xu ZR, Hu CH, Xia MS, et al. Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poultry Science 2003;82(6)1030-36. https://doi.org/10.1093/ps/82.6.1030.
https://doi.org/10.1093/ps/82.6.1030...
), higher digestibility means less substrate is accessible for microbial fermentation in the large intestine, which promotes proper digestion and lessens noxious gas emissions. A decrease in harmful bacteria results in a reduction in the levels of ammonia gases (Li et al., 2012Li H, Xin H, Burns RT, Roberts SA, et al. Reducing ammonia emissions from laying-hen houses through dietary manipulation. Journal of the Air & Waste Management Association 2012;62(2):160-9. https://doi.org/10.1080/10473289.2011.638414.
https://doi.org/10.1080/10473289.2011.63...
). We assume that decreased salmonella populations and improved nitrogen digestibility in broiler chickens may be responsible for the decrease in excreta ammonia gas contents.

Table 5
The effect of dietary almond hull supplementation on noxious gas emission of broilers1

The organ weight of broilers in different treatment groups is shown in Table 6. The current study shows that there was no significant disparity in the breast muscle, liver, spleen, abdominal fat, bursa of Fabricius, and gizzard weights of broilers after the study period. Similarly, González-Alvarado et al. (2007González-Alvarado JM, Jiménez-Moreno E, Lázaro R, et al. 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):1705-15. https://doi:10.1093/ps/86.8.1705.
https://doi:10.1093/ps/86.8.1705...
) found that the gross organ weight of broilers had no significant difference at the inclusion level of 3% soy hulls in the diet, compared to the control group. Additionally, inclusion level of 4%-8% of soybean hulls had no significant impact on internal organs, except for the liver (Tejeda & Kim, 2020Tejeda OJ, Kim WK. The effects of cellulose and soybean hulls as sources of dietary fiber on the growth performance, organ growth, gut histomorphology, and nutrient digestibility of broiler chickens. Poultry Science 2020;99(12) :6828-36. https://doi.org/10.1016/j.psj.2020.08.081.
https://doi.org/10.1016/j.psj.2020.08.08...
). Moreover, Moradi et al. (2021) indicated that sweet almond hull doses of 7%, 14%, 21%, and 28% had no tangible effects on the bursa of Fabricius and spleen of broilers. Arjomandi et al. (2015Arjomandi MA, Salarmoini M, Asadikaram G. The use of sweet almond meal as a protein source in japanese quails diets. Poultry Science Journal 2015;3(2):129-34.) showed that the inclusion of sweet almond hulls in the diet had no impact on the relative weight of the various internal organs of quails. However, Rezaei et al. (2018Rezaei M, Karimi Torshizi MA, Wall H, et al. Body growth, intestinal morphology and microflora of quail on diets supplemented with micronised wheat fibre. British Poultry Science 2018;59(4):422-9. https://doi.org/10.1080/00071668.2018.1460461.
https://doi.org/10.1080/00071668.2018.14...
) showed that a greater amount of dietary fiber promotes the size of internal organs (i.e., gizzard and intestines) to make up for the increased volume of feed going through intestines as a result of bulky diets. Moreover, insoluble fibers have indeed been demonstrated to impact the weights of various organs, as well as the gastrointestinal tract’s propensity to digest feed and the conversion of feed in chickens (Hetland et al., 2004Hetland H, Choct M, Svihus B. Role of insoluble non-starch polysaccharides in poultry nutrition. World's Poultry Science Journal 2004;60(4):415-22., 2005; Mateos et al., 2012Mateos GG, Jiménez-Moreno E, Serrano MP, et al. Poultry response to high levels of dietary fiber sources varying in physical and chemical characteristics. Journal of Applied Poultry Research 2012;21(1):156-74. https://doi.org/10.3382/japr.2011-00477.
https://doi.org/10.3382/japr.2011-00477...
). Yokhana et al. (2016Yokhana JS, Parkinson G, Frankel TL. Effect of insoluble fiber supplementation applied at different ages on digestive organ weight and digestive enzymes of layer-strain poultry. Poultry Science 2016;95(3):550-9. https://doi.org/10.3382/ps/pev336.
https://doi.org/10.3382/ps/pev336...
) stated that the liver and gizzard’s weights increased noticeably after being fed insoluble fiber diets for an additional five weeks, until 18 weeks of age (but not for the proventriculus). No significant effects of almond hulls on broiler organ weight could be attributed to factors such as low inclusion levels, length of study duration, nutrient composition, and strain of broiler population. There are few studies on the impact of the almond hull on the carcass characteristics of broilers, and further research is necessary to determine the real causes.

Table 6
The effect of dietary almond hull supplementation on the organ weight of broilers1

CONCLUSION

Supplementation of broiler diets with almond hulls enhanced the growth performance and nutrient digestibility, decreasing salmonella counts in the broilers’ excreta microflora and reducing ammonia gases at 35 days. Therefore, a supplementation at the inclusion level of 2% of almond hulls in diets could be recommended for the overall performance of broilers.

ACKNOWLEDGMENTS

Dankook University’s Innovation Support program provided funding for the Department of Animal Resource & Science as part of the Research-Focused Department Promotion & Interdisciplinary Convergence Research Projects in 2022.

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Publication Dates

  • Publication in this collection
    08 Apr 2024
  • Date of issue
    2024

History

  • Received
    20 July 2023
  • Accepted
    14 Jan 2024
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