Investigation of Egg Productivity, Egg Quality, Egg Storability, Organ Characteristics, Gut Microbiota, and Health Parameters with Different Addition Levels of Fermented Allium TuberosumABSTRACT
Allium tuberosum (Chinese chives; CC) contains large amounts of metabolites that have antibacterial, antioxidant, and anti-inflammatory properties. In our previous study, fermented CC was shown to improve physiological functions and have positive results in broilers. In this study, we investigated egg productivity, egg quality, blood parameters, organ and intestinal characteristics, and gut microbiota by adding solid-state fermented CC (FCC) to laying hen diets. A total of 120 laying hens (40-weeks-old) were randomly assigned to one of the three dietary treatment groups: (1) basal diet + carrier mixture (CM) 1.5% (CC juice concentration 0%; CON); (2) basal diet + 0.5% FCC + 1.0% CM (CC juice concentration 0.1%; FCC 0.1%); (3) basal diet + 1.5% FCC (CC juice concentration 0.3%; FCC 0.3%). Each treatment was designed with 10 replicates, and 4 hens were assigned to each replicate. The experiment lasted for 5 weeks. As a result, the FCC 0.1% group had a heavier egg weight, and the FCC 0.3% group had higher feed intake (p<0.05). However, feed conversion ratio (FCR) was similar in all treatments (p>0.05). Egg quality was also not observed to be affected by the supplementation of FCC (p>0.05). However, interestingly, when eggs were stored for 4 weeks, FCC treatment hens showed lower malondialdehyde (MDA) concentrations than CON (p<0.05). Although the content of blood components was similar (p>0.05), FCC 0.1% affected ileum length and potential pathogen growth (p<0.05). This study suggests that FCC as a feed additive for laying hens improves egg productivity, and storage period, and helps maintain health.
Keywords:
Biological activity; laying performance; phytogenic feed additive; solid-statefermentation
INTRODUCTION
Antibiotic feed additives have been extensively used in the livestock industry to meet increased demand for animal-derived products due to the growing population since the 1960s (Mingmongkolchai & Panbangred, 2018). The original purpose of antibiotics was the management of clinical infectious diseases as chemotherapeutic agents. However, antibiotics were revealed to be effective in improving industrial growth performance, feed efficiency, mortality, and quality of animal products in livestock animals at a sub-therapeutic dosage, and began to be used as feed additives worldwide (Moore et al., 1946; Chattopadhyay, 2014). Despite providing these beneficial effects for both animals and producers from an economical perspective, the ban on the use of antibiotic feed additives is expanding worldwide, with growing concerns about the emergence of antimicrobial resistance, which is one of the biggest threats to global health and food security nowadays (Vanaerschot et al., 2020; Moon et al., 2021). Therefore, research for feed resources, additives, feeding management, and welfare has been focused on improving or maintaining productivity without conventional anti-microbial substances.
Phytogenic feed additives (PFAs) are one of the economically ideal products with confirmed positive effects on productivity performance, intestinal health, and antioxidant and anti-inflammatory status of poultry through numerous studies over the past few years (Kothari et al., 2019; Singh et al., 2020; Abdelli et al., 2021). The PFA itself could exert antioxidant, antimicrobial, anti-viral, and anti-inflammatory activity, and has this has been shown to improve feed intake, digestive enzyme secretions, enhance immunity, and regulate gut microbiota in poultry (Abou-Elkhair et al., 2018; Kothari et al., 2019; Sharma et al., 2020; Abdelli et al., 2021). In this context, the genus Allium, consisting of approximately 915 species, holds exorbitant potential due to the presence of a variety of bioactive compounds, including polyphenols, saponins, organosulfur compounds (OSCs), fructans, and fructo-oligosaccharides (FOS) (Teshika et al., 2019; Kothari et al., 2020). Several studies have reported the benefits of using Allium sp. (in particular garlic and onion) in poultry diets, with growth-improving, antioxidant activity, and immune-modulating properties (Lee et al., 2016; Omer et al., 2019; Ismail et al., 2021). Furthermore, natural herbal plants such as garlic, onion, moringa, and several seeds have been reported to have positive effects on livestock due to their flavonoids and other phenolic compounds (Dehshahri et al., 2012; Abdelrahman et al., 2015; Lee et al., 2020).
Allium tuberosum (Chinense chive, CC) is also a plant belonging to the Allium plant genus, and is a natural product used worldwide as food, spice, and herbal medicine, similarly to garlic, onion, chives, and rakkyo (Lee et al., 2022). This plant contains various major bioactive components such as organosulfur compounds (OSCs) and polyphenols, and is widely used in folk medicine due to its excellent antioxidant and antibacterial properties (Ni et al., 2019; Putnik et al., 2019). In particular, fermentation using Lactobacillus plantarum is known to improve the content of metabolites such as kaempferol, isorhamnetin, and quercetin in CC, enhancing antibacterial and antioxidant activity (Kothari et al., 2020). For this reason, various studies have been conducted on functional feed additives using CC (Moon et al., 2021; Niu et al., 2020; Lee et al., 2022). However, there are few research cases that analyze changes in productivity, livestock product quality, and differences in body condition when fermented CC are applied used in livestock feed.
Therefore, in this study, the effect of adding solid-state fermented CC (FCC) in the diet of laying hens was investigated. Egg productivity, egg quality, malondialdehyde (MDA) difference between stored eggs, blood parameters, organ and intestinal characteristics, and gut microbiota were investigated according to the addition level. These results are expected to prove that FCC is an effective feed additive for maintaining productivity, and improving egg quality and health status in laying hens.
MATERIALS AND METHODS
Ethical statement
The experimental protocol was reviewed and approved by the Institutional Animal Care and Use Committee (Approval number: KU21192) of Konkuk University (Seoul, Republic of Korea).
Feed additives and feed composition
The CC were purchased from a local market (Gwangjin-gu, Seoul, Republic of Korea) and CC juice was prepared by squeezing it using a juicer (Angel-7700, Angel Juicer, Busan, Republic of Korea). In addition, the fermentation strain used in this study was L. plantarum SK4719, a microorganism that was isolated from CC juice during our previous research, and used to manufacture fermented feed additives for broilers (Kothari et al., 2020; Lee et al., 2022). Briefly, L. plantarum SK4719 was initially inoculated into de Man Rogosa Sharpe (MRS, Difco, USA) culture medium and cultured at 30oC and 100 rpm for 18 h. After washing three times with sterilized distilled water, the same volume of sterilized distilled water as the MRS culture medium used during culture was dispensed. Afterwards, feed additives for each treatment group were prepared by mixing each raw material at the ratio shown in Table 1, which also contains ingredient analysis results. FCC was mixed and packaged in a rigid plastic container and incubated at 30oC for 24 h (number of L. plantarum SK4719 in final product: over 107 colony forming units (CFU)/mL).
The basal diet for all treatments was based on NRC (1994), and a corn-soybean meal-based diet was formulated to meet or exceed the nutritional requirements of laying hens (Table 2).
Experimental animal and design
A total of 120 ISA Brown laying hens (40-weeks-old) were randomly assigned to three treatment groups of 4 birds, in 10 replicates. The experimental facility was a 1-tier battery-cage with a length of 43 cm, a depth of 45 cm, and a height of 42 cm, and two birds were raised per cage (two cages per replicate). Three treatments were designed based on the final CC juice concentration in the feed for each treatment, as follows: (1) basal diet + 1.5% CM (CC juice concentration 0%; CON); (2) basal diet + 0.5% FCC + 1.0% CM (CC juice concentration 0.1%; FCC 0.1%); (3) basal diet + 1.5% FCC (CC juice concentration 0.3%; FCC 0.3%). Each experimental diet was mixed using a feed mixer (DKM-350SU, DAE KWANG CO., LTD., Hwaseong-si, Korea) for 10 min.
All hens were allocated into cages randomly and housed for a 2-weeks-long adaptation period during which they were fed the basal diet without any experimental additive and the egg production rate of hens was measured in each cage. After the adaptation period, all hens were weighed and assigned to one of the three dietary treatment groups to equalize the initial egg production rate (89.44 ± 0.07%) and BW (1982.50 ± 5.02 g) between the treatment groups under a completely randomized design (CRD). The experimental period lasted for 5 weeks (43 to 47 weeks of age). During the entire experimental period, feed in mash form and water were provided ad libitum. The environmental conditions were maintained at controlled temperature (23 ± 2oC), humidity (25 ± 1%), and light (16L:8D) settings throughout the entire experimental period.
Egg productivity
The number of eggs laid by birds in each replicate was noted every day at 10 am and expressed as the percentage of egg production. The egg production rate was calculated from the total number of eggs laid during each week divided by the total number of hen days in that week on a replicate basis. All collected eggs were weighed on a daily basis to obtain the average weight of the eggs. Egg mass was calculated as a multiplication of the egg production rate by the average egg weight. Feed intake was calculated as the difference between the amount of supplied feed and remaining feed at a weekly basis. The feed conversion ratio (FCR) was calculated by dividing feed intake by egg mass.
Egg quality
30 eggs per treatment group (3 eggs per replicate) were randomly collected after each week and used to measure egg quality. Haugh unit, eggshell breaking strength, and egg yolk color were measured using a digital egg tester (DET6000, NABEL Co., Ltd., Kyoto, Japan). Haugh unit is calculated using the following equation: 100 × log(H + 7.57-1.7 × W0.37), where H = albumen height (mm) and W = egg weight (g). The eggshell thickness was measured using a digital egg caliper (Digital Caliper, NABEL Co., Ltd., Mitutoyo, Japan) after removing the eggshell membrane.
Determination of malondialdehyde concentration in egg yolk
In the last week of the experiment, a total of 90 eggs (30 eggs per treatment group) were collected and stored in an incubator at 25oC for 4 weeks. Lipid peroxidation assays of the egg yolk according to egg storage were compared and analyzed by measuring thiobarbituric acid reactive substances (TBARS), following the method described by Botsoglou et al. (1994). Briefly, two egg yolk samples stored for 4 weeks were pooled together, homogenized, and considered as one replicate. Then, 1.5 g of pooled egg yolk was mixed with 5% aqueous trichloroacetic acid solution containing 0.8% butylated hydroxytoluene, and homogenized at 4,000 rpm for 5 min. Next, it was reacted with thiobarbituric acid reagent and incubated at 70oC for 30 mins. The mixture was cooled to room temperature and then the absorbance of the mixture was measured at 532 nm relative to the blank reaction mixture. The TBARS concentrations were calculated using MDA as the reference standard.
Sample collection
At the end of the experiment, 30 hens (10 hens per treatment group) were randomly selected from each treatment. Selected laying hens were euthanized using CO2 gas, and then individual samples were collected to analyze blood parameters, organ and intestinal characteristics, and intestinal microbial flora.
Biochemical properties in blood plasma
After euthanasia, blood samples were collected through cardiac puncture, immediately dispensed into vacutainer serum tubes (BD, New Jersey, USA), and stored at 4oC. The collected blood was then centrifuged at 1,500 rpm for 10 min to collect serum and stored at -20oC until analysis. As analysis indicators, total cholesterol (TCHO), high-density lipoprotein-cholesterol (HDL-C), triglyceride (TG), and lactate dehydrogenase (LDH) were analyzed. These were analyzed using an automated clinical chemistry analyzer (FUJI DRI-CHEM 7000i, FUJIFILM Corporation, Japan), and the concentration of low-density lipoprotein + very low-density lipoprotein (LDL + VLDL) was calculated considering the concentration of TCHO and HDL-C.
Organ and intestinal characteristics
The organs collected were the liver and spleen, which are related to immune function. Each organ sample was weighed and expressed as relative organ mass (g/100 g body weight). The samples of intestinal sections were obtained from the pancreatic loop (duodenum), between the pancreatic loop and Meckel’s diverticulum (jejunum), between Meckel’s diverticulum and the ileocecal junction (ileum), and cecum on both sides (cecum) of the intestine. The lengths of the duodenum, jejunum, ileum, and cecum were expressed as relative length (cm/100 g of body weight).
Viable microbial cell counts in cecal microbiota
The number of viable bacteria in the cecum was measured with the standard agar plating method using MacConkey (MAC), Salmonella shigella (SS), MRS, Bifidobacteria selective agar (BSA) and nutrient agar (NA) (Difco, Franklin Lakes, NJ, USA). This method was performed by following procedure described by Lee et al. (2022). Briefly, samples taken from the cecum were immediately kept on ice, transported to the laboratory, and analyzed within 24 h of collection. The mixture was suspended by mixing 1 g of sample with 9 mL of distilled water and serially diluted by repeating the same procedure. Then, 10 uL was spotted on each plate, and the dispensed medium was cultured in an incubator at 37oC for 24 or 48 h. The number of bacterial colonies was then counted and expressed as log10CFU/g.
Statistical analysis
The experimental data were analyzed using SAS software version 9.4 (SAS Institute, Cary, NC, USA), through the generalized linear model (GLM) procedure. Orthogonal polynomial contrasts were used to determine the linear and quadratic effects of dietary dosage of FCC considering significance difference at p<0.05 between treatment groups. The data of laying performance were analyzed by considering replicates as the experimental units. The mean of collected eggs for each replicate was considered the experimental unit. For the analysis of blood biochemical properties, organ and intestine characteristics, and intestinal microbiota, the individual bird was considered the experimental unit. Data were presented as the mean and standard error of means (SEM).
RESULTS
Egg productivity
Table 3 shows the supplemental effect of the FCC on the egg productivity of laying hens in our study. There was no significant difference in the egg laying rate and amount according to the addition of FCC between treatment groups (p>0.05). However, the average egg weight was highest in the group supplemented with FCC 0.1% (Quadratic, p<0.05), and feed intake increased linearly with the addition level (Linear, p<0.05). FCR was similar for all treatments.
Egg quality
The egg quality results of laying hens according to FCC addition levels are summarized in Table 4. The analyzed indicators (Haugh unit, egg yolk color, eggshell breaking strength, and eggshell thickness) were all similar regardless of the amount of FCC added (p>0.05).
Malondialdehyde content of stored eggs
Table 5 shows the difference in MDA levels after the storage of eggs in each treatment group at room temperature for 4 weeks. Interestingly, the FCC groups had lower MDA levels than the CON group (Linear, p<0.05).
Blood biochemical properties
The biochemical properties of the blood plasma of laying hens are shown in Table 6. Total cholesterol content, HDL, LDL+VLDL, triglyceride, and LDH contents were not affected by FCC supplementation (p>0.05).
Organ and intestinal characteristics
Results for the organ characteristics are shown in Table 7. The weight of liver and spleen was similar in all treatments. No significant differences were observed in the duodenum, jejunum, and cecum (p>0.05), but the length of the ileum was shortest in the FCC treatment group (Quadratic, p<0.05).
Viable microbial cell counts in cecal microbiota
Table 8 shows the distribution of microbes in the cecum for each treatment group. In the case of MAC, Escherichia coli selective media, the FCC 0.1% treatment group showed the lowest number of viable bacteria (Quadratic, p<0.05), and the number of microorganisms observed in MRS and NA was also lowest in the FCC 0.1% treatment group (Quadratic, p<0.05). However, the number of microorganisms observed in SS and BSA media was similar for all treatments (p>0.05).
DISCUSSION
Generally, Allium-based phytobiotics have been recognized to improve production performances in hens by many studies, including laying performance (Damaziak et al., 2017; Omer et al., 2019; Abad et al., 2020; Kothari et al., 2021; Moon et al., 2021). Abad et al. (2020) reported that supplementation of commercial Allium extracts increased the egg weight and egg productivity of laying hens. In the studies by Damaziaki et al. (2017) and Omer et al. (2019), A. sativum, A. cepa, and their mixture improved the general health parameters, egg weight, and feed efficiency. Indeed, the genus Allium stores selenium compounds that can be absorbed into egg yolk (Kothari et al., 2019). These studies may support the finding that egg weight was higher in the FCC 0.1% supplemented diet in our study, which may be due to the absorption of compounds present in FCC into the egg yolk and egg white, leading to increased egg weight. Furthermore, the improvement of feed palatability in poultry fed with phytogenic additives consisting of Allium spp. has been reported by numerous studies (Goodarzi et al., 2014; Kothari et al., 2021; Moon et al., 2021). Our previous study reported that supplementation of a phytogenic blend containing CC juice at 0.3% of dosage improved feed intake without affecting other performance parameters in laying hens (Moon et al., 2021). A study by Kothari et al. (2020) reported that microbial fermentation could increase the palatability of livestock by reducing the tannin content of CC. In our study, feed intake increased as the added level of FCC increased. This is believed to be due to the increased feed palatability of laying hens due to microbial fermentation and the addition of PFA.
One of the beneficial effects of photobiotic antioxidants, which have been proposed as natural food preservatives, is their ability to inhibit oxidation and enhance food freshness more effectively than synthetic antioxidants (Al-Harthi, 2014). Several researchers reported that egg quality, including Haugh units, improved when natural products such as brown algae, papaya, pine needles, and CCs were added to laying hen feed (Al-Harthi, 2014; Moon et al., 2021; Dissa et al., 2023). However, interestingly, in some studies, the addition of natural products containing functional substances in the feed of laying hens had no effect on improving egg quality or, on the contrary, resulted in its decrease (Saki et al., 2014; Park et al., 2018; Kothari et al., 2021). Additionally, egg quality has shown different results depending on the level of addition of natural products (Abou-Elkhair et al., 2018; Dilawar et al., 2021). Moon et al. (2021) noted that even if the same PFA is supplemented, the quality improvement effect varies depending on livestock breed, age, rearing environment, and amount of additives used. In our study, despite varying the level of use and addition of natural products, there was no positive effect on egg quality. Considering this, it seems necessary to conduct research on the appropriate addition levels to improve egg quality.
During food storage, lipid oxidation is a particularly important factor affecting quality (Radwan Nadia et al., 2008). As polyunsaturated lipids are oxidized, hydrogen peroxide is formed (Radwan Nadia et al., 2008). This has a negative impact on the overall quality of the food, including flavor and taste, and can cause a decrease in nutritional value and the production of toxins (Radwan Nadia et al., 2008). Meanwhile, natural products with abundant antioxidant effects can be a potential means to increase the storage capacity of livestock products by reducing lipid peroxidation (Kara et al., 2016). MDA, a lipid peroxidation product, is an important biomarker that can evaluate oxidation status (Xie et al., 2019). A decrease in MDA and an increase in the activity and mRNA expression of antioxidant enzymes mean that the antioxidant capacity of laying hens is improved (Xie et al., 2019). In our study, when comparing MDA levels in egg yolk of eggs stored for 4 weeks, the FCC-treated group showed lower MDA content in egg yolk. Carotenoids, xanthophylls, and carotenes in egg yolk are associated with egg yolk color and act as antioxidants that prevent lipid oxidation (Saleh et al., 2021). These are influenced by the diet consumed by the laying hens, and plants of the genus Allium are known to contain large amounts of xanthophylls (Khoo et al., 2011; Saleh et al., 2021). In this context, our study also shows that the antioxidant components in FCC consumed by laying hens reduced lipid peroxidation in egg yolk.
Supplementing poultry feed with aromatic plants is known to stimulate the digestive system by improving digestive enzyme production and strengthening liver function (Abou-Elkhair et al., 2014). These natural products are a cheap and easily available way to alleviate lipid deposition and liver damage in laying hens (Zhu et al., 2022). The liver-damage-alleviating effects of natural products can be evaluated through the accumulation of fat in the liver, and the state of inflammatory response suppression (Zhu et al., 2022). In addition, the liver and spleen are important immune organs of poultry, and many researchers have investigated the effects of using natural products with strong antioxidant activity on poultry health (Lee et al., 2022). In our previous study (Lee et al., 2022), when FCC was added to broiler diets, it had a positive effect on immune parameters by lowering spleen weight compared to CON. Additionally, in a study using garlic, another plant of the Allium genus, a decrease in the weight of the liver and bursa of Fabricius was reported (Lee et al., 2016; Ismail et al., 2021). However, in this study, there was no difference in the weight of the liver and spleen of laying hens despite the addition of FCC. In the future, detailed studies on liver function and immune status are needed, including liver fat content, immunoglobulin, and antibody titers,.
In our study, the length of the ileum in the FCC treatment group was shorter than in the CON group. The structure of the small intestine plays an important role in the digestion and absorption of nutrients, and it is known that the digestibility of nutrients varies depending on its length and weight (Lee et al., 2022). Ege et al. (2019) reported that feed conversion efficiency improves as small intestine length decreases. This suggests that the short intestine allocates more energy to productivity than maintenance, and absorbs and uses nutrients more efficiently. These properties can be influenced by the composition of feed ingredients or the addition of feed additives (Lee et al., 2022). The same fermented CCs product had no effect on the length of the small intestine in broiler chickens, but showed a heavy weight compared to body weight (Lee et al., 2022). From this, it is believed that the use of fermented chives has a positive effect on the intestinal and digestive characteristics of poultry.
Infection with pathogenic microorganisms causes intestinal damage and diarrhea, as well as economic losses in the global poultry industry (Huang et al., 2022). Pathogenic microorganisms that infect poultry cause impaired nutrient absorption, decreased poultry productivity, and pose a serious threat to human health through the livestock products (Huang et al., 2022). Meanwhile, many studies have reported that plant-based additives inhibit the growth of bacteria such as Salmonella and E. coli, showing a similar effect to antibiotics (Bajagai et al., 2022). It is known that this antibacterial activity varies depending on the species of plant used, whether multiple plants are mixed, and the manufacturing process, including fermentation (Kothari et al., 2020; Bajagai et al., 2022). Kothari et al. (2022) reported that fermented CCs showed stronger antibacterial activity than unfermented CCs, and revealed that the content of substances with antibacterial activity was improved through fermentation (Kothari et al., 2020). This can also be explained by the results of the previous study on the ability of feed additives containing fermented chives and non-fermented chives to inhibit intestinal pathogens in broiler chickens (Lee et al., 2022). A study by Park et al. (2016) also revealed that when fermented vegetable additives were offered, the intestinal E. coli population decreased as the addition level increased. When looking at our results from this perspective, it appears that the functional substances exerted anti-pathogen action and improved the health of laying hens that consumed FCC.
Blood characteristics are important indicators of the stability of feed additives for livestock (Lee et al., 2022). Among them, LDH, along with AST and ALT, are indicators of abnormal liver function when feed additives are applied (Lee et al., 2022). Meanwhile, plants of the Allium genus have lipid- and cholesterol-lowering properties in poultry (Kothari et al., 2019). Due to these functions, these plants are used as lipid-lowering and hypocholesterolemic agents around the world (Kothari et al., 2019). Among them, garlic is known to lower cholesterol in the body by inhibiting major enzymes such as malic enzyme, fatty acid synthase, and glucose-6-phosphate dehydrogenase (Kothari et al., 2019). Additionally, one study found that onions, another Allium genus plant, increased HDL levels and lowered triglyceride levels in broiler chickens (Goodarzi et al., 2013). This was reported to be due to onion-derived sulfur components that oxidize the thiol compounds that exist in free form or are bound to proteins and nicotinamide adenine dinucleotide phosphate hydrogen (NADPH) required for lipid synthesis (Goodarzi et al., 2013). However, in our study, LDH levels were similar between experimental groups and the CON, were stable upon intake, and additive supplementation did not show a positive effect on lipid metabolism in the body. Therefore, it seems necessary to set the optimal addition amount and to explore specific mechanisms for lipid metabolism in laying hens using FCCs.
CONCLUSION
FCC supplementation positively influenced the health and nutrient digestibility of laying hens, as evidenced by a reduction in potential intestinal pathogens and a shorter ileum length. Additionally, the improvement in the shelf life of eggs, demonstrated by lower MDA content after 4 weeks of storage, suggests that FCC can be an effective and safe feed additive for enhancing egg quality and promoting hen health.
ACKNOWLEDGEMENTS
This paper was supported by Konkuk University Researcher Fund in 2022.
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FUNDING
This study was supported by the Konkuk University Researcher Fund in 2022. No external funding was received.
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DATA AVAILABILITY STATEMENT
The data are available upon request from the corresponding author.
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DISCLAIMER/PUBLISHER’S NOTE
The published papers’ statements, opinions, and data are those of the individual author(s) and contributor(s). The editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions, or products referred to in the content.
The data are available upon request from the corresponding author.
