https://orcid.org/0000-0002-3908-7102
Abstract
Gelatine (GL) is widely available as a microencapsulated material that prevents the decomposition of canthaxanthin (CX). However, there are still disadvantages such as instability, poor safety, and chromium overload. Our study aimed to determine the effects of using Lignosulfonate (LS) as a potential substitute to GL microencapsulation of CX on the productive performance, egg quality, yolk colour, and serum biochemical indicators of laying hens, as well as the optimal dosage. 1458 healthy ISA brown hens were divided into 9 treatments (162 birds in each group): basal diet containing 0 mg/kg CX (Control), basal diet containing 2 mg/kg GL-microencapsulated CX (GMC2), 4 mg/kg GL-microencapsulated CX (GMC4), 6 mg/kg GL-microencapsulated CX (GMC6), 8 mg/kg GL-microencapsulated CX (GMC8), basal diet containing 2 mg/kg LS-microencapsulated CX (LMC2), 4 mg/kg LS-microencapsulated CX (LMC4), 6 mg/kg LS-microencapsulated CX (LMC6), 8 mg/kg LS-microencapsulated CX (LMC8). The productive performance of each group was recorded daily for 4 weeks. Egg samples were collected and analysed weekly. Serum samples were taken at the end of the experimental period. The results showed that CX-containing diets had no significant effects on laying performance and egg quality (p > .05). The yolk colour level of the CX group was higher than the control group (p < .05), and the LMC group showed better colouring than the GMC group at the same CX concentration (p < .05). Meanwhile, with the increasing of CX concentration, the yolk colour increased by linear and quadratic (p < .001). CX-treatment improved serum total superoxide dismutase (T-SOD) level (p < .05). In conclusion, LMC was superior to GMC in improving egg yolk colour, and antioxidant function, and there was no adverse impact on productive performance, and 8 mg/kg was the optimal dosage of LMC. Therefore, LS could be used as a potential substitute for GL in the CX microencapsulation industry of laying hens.
HIGHLIGHTS
CX significantly improved yolk colour, and the effect of Lignosulfonate was significantly better than Gelatine.
Explored the optimal dosage (8 mg/kg) for Lignosulfonate microencapsulation on canthaxanthin.
Lignosulfonate is a potential substitute for Gelatine in the CX microencapsulation industry of laying hens.
Introduction
Canthaxanthin (4,4′-diketo-β-carotene, CX), as a kind of naturally occurring ketocarotenoid, has attracted much attention as a pigment for its excellent colouring properties and high safety to enhance egg yolk colour (Poole et al. Citation2000; Asker and Ohta Citation2002; Mortimer et al. Citation2016; Umar Faruk et al. Citation2017; Naz et al. Citation2021). As we all know, the good appearance of egg yolk is an important indicator of attracting customers’ consumption, most consumers believe that orange-red yolks are richer in carotenoids than yellow yolks (Berkhoff et al. Citation2020). Therefore, the natural CX market has been projected to grow from 75 million to 85 million from 2018 to 2024, at a compound annual growth rate (CAGR) of 3.5% (https://www.gminsights.com/industryanalysis/canthaxanthin-market).
Most animals including laying hens are incapable of synthesis carotenoids, they can only eat carotenoid-rich foods such as maize, algae, and insects to obtain carotenoids. CX can be released in vivo by enzymes and absorbed by the small intestine, and finally transported to the liver, egg yolk, etc. (Bortolotti et al. Citation2003). In addition, CX can be deposited as lipophilic compounds mainly in the liver, skin, and fat (Bohn Citation2008; Jackson et al. Citation2008; Borel Citation2012; Dose et al. Citation2016; Esatbeyoglu and Rimbach et al. Citation2017). Therefore, CX can significantly improve the colour of egg yolk, which ranges from yellow to orange-red (Meléndez-Martínez et al. Citation2007). Most carotenoids, including CX, are highly unsaturated molecules and highly susceptible to environmental conditions such as oxygen, light, and water. Therefore, CX is prone to be impaired during production, transport, and storage. Research has begun to suggest that microencapsulation technology can protect the unstable carotenoids (Higuera-Ciapara et al. Citation2004). It has been demonstrated that microencapsulation can improve the stability and effectiveness of CX (Hojjati et al. Citation2014; Ravaghi et al. Citation2016). Gelatine (GL) is currently the most commonly used material for microencapsulation (Wang et al. Citation2012). However, GL has a negative role in causing chromium overload and other hazards. Chromium is severely toxic and can easily enter cells, making it difficult to normal excrete and causing damage to the liver, kidneys, and other organs (Bai et al. Citation2019; Wu et al. Citation2020). Lignosulfonate (LS), whose products have excellent dispersibility, binding, complexation, and emulsifying properties, is often utilised as animal feed pellet binders (Cecilia et al. Citation2008; Corey et al. Citation2014). Saleh et al. found that Ca-LS as pellet binders could decrease FCR in broiler compared with non-binders (Saleh et al. Citation2021). Recently, LS also as a new microencapsulated material that is capable of the characteristic on resisting UV damage, photodegradation, and volatilisation, has become a microencapsulate active substance with up to 50% efficiency in the CX industry (Fernández-Pérez et al. Citation2014; Gao et al. Citation2018).
Previous research has shown that LS was more effective than GL in CX microencapsulation (Wen et al. Citation2022), but the appropriate concentration of LS addition is not yet clear. Our present study aimed to compare the effect of GL and LS as microencapsulated materials for CX on yolk colour, egg quality, and serum indicators, and to provide a theoretical basis for the appropriate concentration application of LS-microencapsulated CX (LMC) in laying hens.
Materials and methods
All procedures involving animals in this study were approved by the Zhejiang University Animal Research Ethics Committee and conducted following the National Institutes of Health guidelines.
Birds, housing, and feeding
In this experiment, the birds were reared at Jianhua Poultry Co., Ltd., Jiande County, Hangzhou City, Zhejiang Province, respectively. A total of 1458 ISA Brown hens (40 weeks old, 1.80 ± 0.15 kg) of similar initial body condition and laying rates were selected and randomly divided into 9 groups of 6 replicates each, with 27 hens per replicate. Each group was fed a basal diet or the basal diet supplemented with 2, 4, 6, and 8 mg/kg GL-microencapsulated CX (GMC) or LMC, respectively. During the 1 week acclimation period and 4 weeks-experimental period, all hens were housed in 3-tier ladder cages with 3 hens per cage, replicated in 9 upper and lower cages. Each cage (45 cm × 45 cm × 50 cm) was equipped with 2 nipple drinkers and 1 feeder. Birds had free access to water throughout the entire experimental period. Housing temperature and relative humidity were maintained at 24 ± 2 °C and 60%, respectively. The photoperiod was 16 h light/8 h dark.
Treatment
The corn-soybean meal-based mass feed diet (Table ) was formulated according to the recommendations of the National Research Council of the American Academy of Sciences (NRC, Citation1994). Specifically, we first mix the additives (encapsulated CX) and premix evenly, subsequently, add the additives to corn and soybean meal for stirring.
Table 1. Basic diet and nutritional level (air-dry basis).
Diet design
The 9 dietary treatments:
Control: Basal diets with 0 mg/kg CX
GMC2: Basal diets with 2 mg/kg GMC
GMC4: Basal diets with 4 mg/kg GMC
GMC6: Basal diets with 6 mg/kg GMC
GMC8: Basal diets with 8 mg/kg GMC
LMC2: Basal diets with 2 mg/kg LMC
LMC4: Basal diets with 4 mg/kg LMC
LMC6: Basal diets with 6 mg/kg LMC
LMC8: Basal diets with 8 mg/kg LMC
Laying performance
Feed intake (FI) was determined weekly by subtracting the ending feed weight of each replicate from the beginning feed weight. Egg production, and egg weight of each group were recorded daily. Based on these data, hen-day egg production (EP), average daily feed intake (ADFI), egg weight (EW), egg mass (EM), and feed conversion ratio (FCR) were calculated. The EM was calculated as EM = EW × EP. The FCR was the ratio of ADFI to EM.
Egg quality and yolk colour
36 eggs (6 eggs from each replicate) were randomly collected to assess egg quality parameters every 7 days. Subsequently, the eggs were transported by car to Zhejiang University for quality testing. Each egg was measured for eggshell strength, albumin height, Haugh unit, and yolk colour using an egg quality multitester (DET-6000, Nabel, JPN). eggshell thickness was measured at the blunt end, tip, and middle end of the egg using a spiral micrometer (JDB03, SanLiang, CHN), and the average value was determined as the eggshell thickness (accurate to 0.01 mm). The weight of the yolk after separation from the egg white was measured (accurate to 0.001 g) using an analytical balance (XPE204, Mettler Toledo, USA), respectively.
Blood collection and biochemical indicators Analysis
At the end of the 4-weeks feeding trial, after 12 h of starvation, 8 birds were randomly selected from each treatment group. Blood samples were collected from the wing vein and then centrifuged at 3500 × g for 10 min at 4 °C. Serum samples were obtained and stored at −20 °C for later analysis. After analysing the data on egg yolk colour, we selected the most effective groups for the next step of serum biochemical indicators detection, including GMC6, GMC8, LMC6, and LMC8 for serum biochemical indicators detection. Serum contents of albumin (ALB), globulin (GLOB), total protein (TP), triglycerides (TG), total cholesterol (TCHO), low-density lipoprotein (LDL), high-density lipoprotein (HDL), total bilirubin (T-BIL), total bile acids (TBA) were determined by an automatic biochemical analyser (UniCel DxC 600 Synchron, Beckman Coulter, USA). Serum malondialdehyde (MDA) level, total superoxide dismutase (T-SOD) level, and glutathione peroxidase (GSH-Px) level were measured using colorimetric kits following the manufacturer’s protocol (RY-12193, RY-12378, and RY-12628, Runyu Biotechnology Co., Ltd., China).
Statistical Analysis
Microencapsulated materials, CX concentrations and their interaction were analysed using the General Linear Model (GLM) in SPSS software, version 26.0 (SPSS Inc., US), data were presented as The Mean Value ± Standard Error of Mean (SEM). Whenever significant differences (p < .05) were found, Duncan’s tests were conducted.
Results
Laying performance
The results of the laying performance were shown in Table . There was no significant difference (p > .05) in EP, ADFI, EW, EM, and FCR of laying hens among groups.
Table 2. Effects of different concentrations of canthaxanthin microencapsulated with gelatin or lignosulfonate on productive performance of laying hens.
Egg quality and yolk colour
During 1 to 4 wk, neither GMC nor LMC had a significant difference (p > .05) in eggshell strength, albumin height, Haugh unit, eggshell thickness, and relative yolk weight (Tables ). Compared with the control group, dietary supplemented with GMC and LMC improved (p < .05) yolk colour, and with the increasing of CX concentration, the yolk colour increased by linear or quadratic (p < .001) (Table and Figure ). Moreover, in 14, 21, and 28 days, the interaction of microencapsulated materials and CX concentrations was significant (p < .05). Table showed the effects of different concentrations of GMC and LMC on the yolk colour of laying hens on different days. We found there were no significant effects on yolk colour on different days and the interaction between materials and concentrations (p > .05), but different concentrations of CX had significant effects on yolk colour (p < .05).
Figure 1. Effects of different concentrations of canthaxanthin with gelatine or lignosulfonate microencapsulated on yolk colour. Control: basal diets with 0 mg/kg CX; GMC2: basal diets with 2 mg/kg GMC; GMC4: basal diets with 4 mg/kg GMC; GMC6: basal diets with 6 mg/kg GMC; GMC8: basal diets with 8 mg/kg GMC; LMC2: basal diets with 2 mg/kg LMC; LMC4: basal diets with 4 mg/kg LMC; LMC6: basal diets with 6 mg/kg LMC; LMC8: basal diets with 8 mg/kg LMC
Table 3. Effects of different concentrations of canthaxanthin microencapsulated with gelatin or lignosulfonate on egg quality in 7 days of laying hens.
Table 4. Effects of different concentrations of canthaxanthin microencapsulated with gelatin or lignosulfonate on egg quality in 14 days of laying hens.
Table 5. Effects of different concentrations of canthaxanthin microencapsulated with gelatin or lignosulfonate on egg quality in 21 days of laying hens.
Table 6. Effects of different concentrations of canthaxanthin microencapsulated with gelatin or lignosulfonate on egg quality in 28 days of laying hens.
Table 7. Effects of different concentrations of canthaxanthin microencapsulated with gelatin or lignosulfonate on yolk colour of laying hens.
Table 8. Effects of different concentrations of canthaxanthin microencapsulated with gelatin or lignosulfonate on yolk colour in different days of laying hens.
Serum biochemical indices and lipid metabolism traits
As indicated in Tables and , CX did not affect the concentrations of T-BIL, TBA, TP, ALB, GLOB, A/G, TG, TCHO, LDL, and HDL (p > .05).
Table 9. Effects of different concentrations of canthaxanthin microencapsulated with gelatin or lignosulfonate on serum biochemical indicators of laying hens.
Table 10. Effects of different concentrations of canthaxanthin microencapsulated with gelatin or lignosulfonate on serum lipid metabolism indices of laying hens.
Serum antioxidant capacity
The results showed that there was no significant difference in serum MDA and GSH-Px levels between the CX groups and the control group (p > .05). We found that different microencapsulated materials, concentrations, and their interaction have a significant effect on serum T-SOD (p < .001) (Table ). Compared with GMC, LMC had a higher T-SOD level, and with the increasing of CX concentration, the T-SOD level significantly increased (p < .001).
Table 11. Effects of different concentrations of canthaxanthin microencapsulated with gelatin or lignosulfonate on serum antioxidant capacity of laying hens.
Discussion
To find a safer and more effective CX microencapsulated material and its optimal application concentration, we compared the different concentrations effects of GMC and LMC to diets on the laying performance, egg quality, yolk colour, and serum biochemical indicators ofhens.
The effects of CX treatment on laying performance and egg quality of poultry have attracted much public attention. A previous experiment indicated that 0.011% or 0.021% dietary CX did not significantly affects the ADFI and egg quality of 36 weeks ISA Brown layers (Cho et al. Citation2012). In addition, it was reported that CX supplementation at 0 mg/kg, 8 mg/kg, or 80 mg/kg in the diet of Lohmann’s hens at 43–51 weeks had no significant effects on egg weight and yolk weight (Weber et al. Citation2013). In this study, we found that CX had no significant effect on laying performance and egg quality, which was following the previous reports. A recent study suggests that dietary 4–10 mg/kg CX supplementation significantly increased the ADFI, EP, and EW, promoted the ovulation process and maintained the reproductive hormones by improving the antioxidant levels in their serum and ovaries of the Huaixiang hens, especially, the best CX concentration was the 6 mg/kg (Zhao et al. Citation2023). A previous study found that dietary CX supplementation could improve EP in broiler breeders in 54–65 weeks, but not 42–53 weeks (Bonilla et al. Citation2017). Similarly, Johnson-Dahl et al. found that dietary supplementation of 6 mg/kg CX increased EP in Ross 308 broiler breeder hens, but more CX (12 mg/kg) was deposited into the egg and chick liver (Johnson-Dahl et al. Citation2017). The possible reasons for improving the laying performance of hens were that β-carotene, such as CX, stimulated the expression of oestrogen enzymes in vitro, and oestrogen further regulates the synthesis of yolk lipids and proteins, in addition, CX had the free radical-scavenging properties, which could improve the body’s antioxidant enzyme activity, thereby reducing oxidative stress in the ovary and improving laying performance (Ng et al. Citation2000; Chang et al. Citation2013; Araújo et al. Citation2020). The reasons for the above differences might be due to the breed, age, experiment duration, feeding conditions, and concentration of CX in the hens. Taken together, our findings indicated that the addition of 2–8 mg/kg GL or LS microencapsulated CX to the diet had no detrimental effect on the economic value of laying hens.
To assess the internal characteristics of the egg, albumen height and Haugh unit were important indices to measure egg albumen quality and freshness (Roberts Citation2004). We found that Haugh unit was lower than some studies (Tufarelli et al. Citation2016; Cai et al. Citation2016; Muir et al. Citation2022), possibly due to the decline in Haugh unit caused by the high temperatures of summer, long-distance transportation and untimely testing (Gogo et al. Citation2021). The yolk colour is an important indicator to evaluate the quality of the egg, consumers value the yolk colour more than other egg characteristic (Berkhoff et al. Citation2020). After being ingested into the animal body, CX must first be released from the food substrate before it can be absorbed (Faulks et al. Citation2005), the released CX is mixed with a mixture of free fatty acids, bile salts, cholesterol, phospholipids, and other lipids, and then it is absorbed into intestinal epithelial cells through passive diffusion or SR-BI receptors (Reboul Citation2013). Therefore, CX can be efficiently deposited and distributed in the ovary, embryo, and egg yolk in birds (Nys Citation2000). Our study found all CX treatment groups significantly improved the yolk colour of fresh eggs, which agrees with the results of previous study (Chan et al. Citation2009). In addition, the yolk colour in the LMC group was higher than that of the GMC group at the same concentration of CX addition. We also found that at a CX dose of 0–8 mg/kg, the yolk colour may increase in a CX dose-dependent manner. Thus, our data strongly suggested that LS has better bioavailability and yolk colouration than GL, which may imply a higher economic value as a CX microencapsulated material. It might be since LS is more water-soluble than GL, therefore, canthaxanthin in LS is dispersed more finely in water, which makes it easier to absorb in the gastrointestinal (Piombino et al. Citation2020).
Oxidative stress is associated with poor embryonic development, lower hatchability, and chick growth impairment (Eid et al. Citation2021). CX has a strong antioxidant activity, which has been indicated in numerous in vitro models and in animal experiments in vivo. For example, CX affects the innate immune function and antioxidant capacity of chicks by protecting antioxidant substances (Araujo et al. Citation2019; Jalali et al. Citation2021). Another example, it has been found that CX dietary supplementation in the female breeder’s diet significantly improves the anti-oxidative status of egg yolk (Surai Citation2012). The body’s self-antioxidant enzymes such as T-SOD and GSH-Px play an essential role in quenching the reactive oxygen species (Mathimaran et al. Citation2021). A previous study suggested that when Chinese Three Yellow broiler breeder hens were supplemented with 6 mg/kg CX, the chicks had lower serum MDA level at 1 and 7 d of age and higher T-SOD at 1 d of age (Zhang et al. Citation2011). In the present study, we found that CX attenuated oxidative stress by increasing the level of T-SOD, and LMC group has a higher serum T-SOD level than that in the GMC group. However, CX-treatment had no significant effects on MDA and GSH-Px levels, which were slightly different from previous studies and there might be a discrepancy between the results due to differences in the bird’s age, diet type, and duration of the experiment. Meanwhile, our study revealed that LS may have a better antioxidant capacity than GL as a coating material.
The liver of hens is the main organ responsible for lipid metabolism and plays a key role in the formation of yolk precursors (Cui et al. Citation2020). Liver damage affects hepatic lipid synthesis and metabolism, and may ultimately lead to a decrease in egg yolk quality and egg production (Zhu et al. Citation2020). TG, TCHO, HDL, and LDL are common representative indicators for lipid metabolism (Zhang et al. Citation2021). In the present study, the addition of CX had no significant effects on serum TG, TCHO, HDL, and LDL levels of laying hens, which indicated that CX was harmless to lipid metabolism. We also detected the serum biochemical indicators and the results suggested that serum T-BIL, TBA, TP, ALB, GLOB and A/G levels were not affected by CX supplementation.
Conclusions
To summarise, the addition of CX to the diets had no negative effects on laying performance and egg quality. Also, CX significantly improved yolk colour, and the effect of LMC groups was significantly better than that of GMC groups. In terms of antioxidant capacity, CX-treatment improved serum T-SOD level. These findings implied that LS is a potential substitute for GL when the concentrations 0–8 mg/kg, and 8 mg/kg is the optimal concentration for LMC.
Ethical approval
The experimental protocol for animal studies was reviewed and approved by Zhejiang University Animal Research Ethics Committee.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Data availability statement
The data sets are available upon request from the corresponding author.
Additional information
Funding
References
- Araújo ICS, Café MB, Mesquita MA, Caiado BN, Faria AM, Mello HHC, Stringhini JH, Leandro NSM. 2020. Effect of a commercial product containing canthaxanthin for in ovo feeding to broiler embryos on hatchability, chick quality, oxidation status, and performance. Poult Sci. 99(11):5598–5606. doi: 10.1016/j.psj.2020.08.044.
- Araujo LF, Araujo CSS, Pereira RJG, Bittencourt LC, Silva CC, Cisneros F, Hermes RG, Sartore YGA, Dias MT. 2019. The dietary supplementation of canthaxanthin in combination with 25OHD3 results in reproductive, performance, and progeny quality gains in broiler breeders. Poult Sci. 98(11):5801–5808. doi: 10.3382/ps/pez377.
- Asker D, Ohta Y. 2002. Production of canthaxanthin by Haloferax alexandrinus under non-aseptic conditions and a simple, rapid method for its extraction. Appl Microbiol Biotechnol. 58(6):743–750. doi: 10.1007/s00253-002-0967-y.
- Bai Y, Long C, Hu G, Zhou D, Gao X, Chen Z, Wang T, Yu S, Han Y, Yan L. 2019. Association of blood chromium and rare earth elements with the risk of DNA damage in chromate exposed population. Environ Toxicol Pharmacol. 72:103237. doi: 10.1016/j.etap.2019.103237.
- Berkhoff J, Alvarado-Gilis C, Keim JP, Alcalde JA, Vargas-Bello-Pérez E, Gandarillas M. 2020. Consumer preferences and sensory characteristics of eggs from family farms. Poult Sci. 99(11):6239–6246. doi: 10.1016/j.psj.2020.06.064.
- Bohn T. 2008. Bioavailability of non-provitamin A carotenoids. CNF. 4(4):240–258. doi: 10.2174/157340108786263685.
- Bonilla CEV, Rosa AP, Londero A, Giacomini CBS, Orso C, Fernandes MO, Paixão SJ, Bonamigo DV. 2017. Effect of broiler breeders fed with corn or sorghum diet and canthaxanthin supplementation on production and reproductive performance. Poult Sci. 96(6):1725–1734. doi: 10.3382/ps/pew442.
- Borel P. 2012. Genetic variations involved in interindividual variability in carotenoid status. Mol Nutr Food Res. 56(2):228–240. doi: 10.1002/mnfr.201100322.
- Bortolotti GR, Negro JJ, Surai PF, Prieto P. 2003. Carotenoids in eggs and plasma of red-legged partridges: effects of diet and reproductive output. Physiol Biochem Zool. 76(3):367–374. doi: 10.1086/375432.
- Cai L, Nyachoti CM, Hancock JD, Lee JY, Kim YH, Lee DH, Kim IH. 2016. Rare earth element-enriched yeast improved egg production and egg quality in laying hens in the late period of peak egg production. J Anim Physiol Anim Nutr (Berl). 100(3):492–498. doi: 10.1111/jpn.12376.
- Cecilia M, Toledo F, Kuznesof PM. 2008. Calcium lignosulfonate chemical and technical assessment. Rome, Italy. 69th JECFA. p. 1–8.
- Chan KC, Mong MC, Yin MC. 2009. Antioxidative and anti-inflammatory neuroprotective effects of astaxanthin and canthaxanthin in nerve growth factor differentiated PC12 cells. J Food Sci. 74(7):H225–231. doi: 10.1111/j.1750-3841.2009.01274.x.
- Chang CS, Chang CL, Lai GH. 2013. Reactive oxygen species scavenging activities in a chemiluminescence model and neuroprotection in rat pheochromocytoma cells by astaxanthin, beta-carotene, and canthaxanthin. Kaohsiung J Med Sci. 29(8):412–421. doi: 10.1016/j.kjms.2012.12.002.
- Cho JH, Zhang ZF, Kim IH. 2012. Effects of canthaxanthin on egg production, egg quality, and egg yolk color in laying hens. J Agr Sci-Cambridge. 5(1):269–274. doi: 10.5539/jas.v5n1p269.
- Corey AM, Wamsley KGS, Winowiski TS, Moritz JS. 2014. Effects of calcium lignosulfonate, mixer‐added fat, and feed form on feed manufacture and broiler performance. J Appl Poult Res. 23(3):418–428. doi: 10.3382/japr.2013-00916.
- Cui Z, Amevor FK, Feng Q, Kang X, Song W, Zhu Q, Wang Y, Li D, Zhao X. 2020. Sexual maturity promotes yolk precursor synthesis and follicle development in hens via liver-blood-ovary signal axis. Animals. 10(12):2348. doi: 10.3390/ani10122348.
- Dose J, Matsugo S, Yokokawa H, Koshida Y, Okazaki S, Seidel U, Eggersdorfer M, Rimbach G, Esatbeyoglu T. 2016. Free radical scavenging and cellular antioxidant properties of astaxanthin. Int J Mol Sci. 17(1):103. doi: 10.3390/ijms17010103.
- Eid Y, Kirrella AA, Tolba A, El-Deeb M, Sayed S, El-Sawy HB, Shukry M, Dawood MAO. 2021. Dietary pomegranate by-product alleviated the oxidative stress induced by dexamethasone in laying hens in the pre-peak period. Animals. 11(4):1022. doi: 10.3390/ani11041022.
- Esatbeyoglu T, Rimbach G. 2017. Canthaxanthin: from molecule to function. Mol Nutr Food Res. 61(6):1600469. doi: 10.1002/mnfr.201600469.
- Faulks RM, Southon S. 2005. Challenges to understanding and measuring carotenoid bioavailability. Biochim Biophys Acta. 1740(2):95–100. doi: 10.1016/j.bbadis.2004.11.012.
- Fernández-Pérez M, Flores-Céspedes F, Daza-Fernández I, Vidal-PeA F, Villafranca-Sánchez M. 2014. Lignin and lignosulfonate-based formulations to protect pyrethrins against photodegradation and volatilization. Ind Eng Chem Res. 53(35):13557–13564. doi: 10.1021/ie500186e.
- Gao F, Yu S, Tao Q, Tan W, Duan L, Li Z, Cui H. 2018. Lignosulfonate improves photostability and bioactivity of abscisic acid under ultraviolet radiation. J Agric Food Chem. 66(26):6585–6593. doi: 10.1021/acs.jafc.7b02002.
- Gogo JA, Atitwa BE, Gitonga CN, Mugo DM. 2021. Modelling conditions of storing quality commercial eggs. Heliyon. 7(8):e07868. doi: 10.1016/j.heliyon.2021.e07868.
- Higuera-Ciapara I, Felix-Valenzuela L, Goycoolea FM, Argüelles-Monal W. 2004. Microencapsulation of astaxanthin in a chitosan matrix. Carbohyd Polym. 56(1):41–45. doi: 10.1016/j.carbpol.2003.11.012.
- Hojjati M, Razavi SH, Rezaei K, Gilani K. 2014. Stabilization of canthaxanthin produced by Dietzia natronolimnaea HS-1 with spray drying microencapsulation. J Food Sci Technol. 51(9):2134–2140. doi: 10.1007/s13197-012-0713-0.
- Jackson H, Braun CL, Ernst H. 2008. The chemistry of novel xanthophyll carotenoids. Am J Cardiol. 101(10a):50d–57d. doi: 10.1016/j.amjcard.2008.02.008.
- Jalali TS, Malekifard F, Esmaeilnejad B, Asri Rezaie S. 2021. Toxicities of the copper and zinc oxide nanoparticles on Marshallagia marshalli (Nematoda: trichostrongylidae): evidence on oxidative/nitrosative stress biomarkers, DNA damage and egg hatchability. J Helminthol. 95:e70. doi: 10.1017/S0022149X21000584.
- Johnson-Dahl ML, Zuidhof MJ, Korver DR. 2017. The effect of maternal canthaxanthin supplementation and hen age on breeder performance, early chick traits, and indices of innate immune function. Poult Sci. 96(3):634–646. doi: 10.3382/ps/pew293.
- Mathimaran A, Kumar A, Prajapati G, Ampapathi RS, Bora HK, Guha R. 2021. Partially saturated canthaxanthin alleviates aging-associated oxidative stress in D-galactose administered male Wistar rats. Biogerontology. 22(1):19–34. doi: 10.1007/s10522-020-09898-4.
- Meléndez-Martínez AJ, Britton G, Vicario IM, Heredia FJ. 2007. Relationship between the colour and the chemical structure of carotenoid pigments. Food Chem. 101(3):1145–1150. doi: 10.1016/j.foodchem.2006.03.015.
- Mortimer CL, Misawa N, Ducreux L, Campbell R, Bramley PM, Taylor M, Fraser PD. 2016. Product stability and sequestration mechanisms in Solanum tuberosum engineered to biosynthesize high value ketocarotenoids. Plant Biotechnol J. 14(1):140–152. doi: 10.1111/pbi.12365.
- Muir WI, Akter Y, Bruerton K, Groves PJ. 2022. An evaluation of bird weight and diet nutrient density during early lay on ISA Brown performance, egg quality, bone characteristics, and liver health at 50 weeks of age. Poult Sci. 101(5):101765. doi: 10.1016/j.psj.2022.101765.
- National Research Council (NRC). 1994. Nutrient requirements of poultry. 9th ed. Washington (DC): National Academy Press.
- Naz T, Yang J, Nosheen S, Sun C, Nazir Y, Mohamed H, Fazili ABA, Ullah S, Li S, Yang W, et al. 2021. Genetic modification of Mucor circinelloides for canthaxanthin production by heterologous expression of beta-carotene ketolase gene. Front Nutr. 8:756218. doi: 10.3389/fnut.2021.756218.
- Ng JH, Nesaretnam K, Reimann K, Lai LC. 2000. Effect of retinoic acid and palm oil carotenoids on oestrone sulphatase and oestradiol-17beta hydroxysteroid dehydrogenase activities in MCF-7 and MDA-MB-231 breast cancer cell lines. Int J Cancer. 88(1):135–138. doi: 10.1002/1097-0215(20001001)88:1<135::aid-ijc21>3.0.co;2-s.
- Nys Y. 2000. Dietary carotenoids and egg yolk coloration – a review. Arch für Geflugelkunde. 64(2):45–54.
- Surai PF. 2012. The antioxidant properties of canthaxanthin and its potential effects in the poultry eggs and on embryonic development of the chick. World Pouit Sci J. 68(4):717–726. doi: 10.1017/S0043933912000840.
- Piombino C, Lange H, Sabuzi F, Galloni P, Conte V, Crestini C. 2020. Lignosulfonate microcapsules for delivery and controlled release of thymol and derivatives. Molecules. 25(4):866. doi: 10.3390/molecules25040866.
- Poole WR, Webb JH, Matthews MA, Youngson AF. 2000. Occurrence of canthaxanthin in Atlantic salmon, Salmo salar L., fry in Irish rivers as an indicator of escaped farmed salmon. Fisheries Management Eco. 7(5):377–385. doi: 10.1046/j.1365-2400.2000.00209.x.
- Ravaghi M, Razavi SH, Mousavi SM, Sinico C. 2016. Stabilization of natural canthaxanthin produced by Dietzia natronolimnaea HS-1 by encapsulation in niosomes. LWT. 73(4):498–504. doi: 10.1016/j.lwt.2016.06.027.
- Reboul E. 2013. Absorption of vitamin A and carotenoids by the enterocyte: focus on transport proteins. Nutrients. 5(9):3563–3581. doi: 10.3390/nu5093563.
- Roberts JR. 2004. Factors affecting egg internal quality and egg shell quality in laying hens. Jpn Poult Sci. 41(3):161–177. doi: 10.2141/jpsa.41.161.
- Saleh AA, Elnagar AM, Eid YZ, Ebeid TA, Amber KA. 2021. Effect of feeding wheat middlings and calcium lignosulfonate as pellet binders on pellet quality growth performance and lipid peroxidation in broiler chickens. Vet Med Sci. 7(1):194–203. doi: 10.1002/vms3.344.
- Tufarelli V, Ceci E, Laudadio V. 2016. 2-Hydroxy-4-methylselenobutanoic acid as new organic selenium dietary supplement to produce selenium-enriched eggs. Biol Trace Elem Res. 171(2):453–458. doi: 10.1007/s12011-015-0548-4.
- Umar Faruk M, Roos FF, Cisneros-Gonzalez F. 2017. A meta-analysis on the effect of canthaxanthin on egg production in brown egg layers. Poult Sci. 97(1):84–87. doi: 10.3382/ps/pex236.
- Wang Y, Ye H, Zhou C, Lv F, Bie X, Lu Z. 2012. Study on the spray-drying encapsulation of lutein in the porous starch and gelatin mixture. Eur Food Res Technol. 234(1):157–163. doi: 10.1007/s00217-011-1630-6.
- Weber GM, Machander V, Schierle J, Aureli R, Roos F, Pérez-Vendrell AM. 2013. Tolerance of poultry against an overdose of canthaxanthin as measured by performance, different blood variables and post-mortem evaluation. Anim Feed Sci Tech. 186(1–2):91–100. doi: 10.1016/j.anifeedsci.2013.09.005.
- Wen C, Xu X, Zhou D, Yu Q, Wang T, Zhou Y. 2022. The effects of canthaxanthin microencapsulation on yolk color and canthaxanthin deposition in egg yolk of laying hens. Poult Sci. 101(6):101889. doi: 10.1016/j.psj.2022.101889.
- Wu YH, Lin JC, Wang TY, Lin TJ, Yen MC, Liu YH, Wu PL, Chen FW, Shih YL, Yeh IJ. 2020. Hexavalent chromium intoxication induces intrinsic and extrinsic apoptosis in human renal cells. Mol Med Rep. 21(2):851–857. doi: 10.3892/mmr.2019.10885.
- Zhang K, Shi Y, Huang C, Huang C, Xu P, Zhou C, Liu P, Hu R, Zhuang Y, Li G, et al. 2021. Activation of AMP-activated protein kinase signaling pathway ameliorates steatosis in laying hen hepatocytes. Poult Sci. 100(3):100805. doi: 10.1016/j.psj.2020.10.059.
- Zhang W, Zhang KY, Ding XM, Bai SP, Hernandez JM, Yao B, Zhu Q. 2011. Influence of canthaxanthin on broiler breeder reproduction, chick quality, and performance. Poult Sci. 90(7):1516–1522. doi: 10.3382/ps.2010-01126.
- Zhao Z, Wu J, Liu Y, Zhuang Y, Yan H, Xiao M, Zhang L, An L. 2023. Dietary canthaxanthin supplementation promotes the laying rate and follicular development of Huaixiang hens. Biology. 12(11):1375. doi: 10.3390/biology12111375.
- Zhu MK, Li HY, Bai LH, Wang LS, Zou XT. 2020. Histological changes, lipid metabolism, and oxidative and endoplasmic reticulum stress in the liver of laying hens exposed to cadmium concentrations. Poult Sci. 99(6):3215–3228. doi: 10.1016/j.psj.2019.12.073.