Abstract
This study aimed to investigate the effects of dietary curcumin supplementation on laying performance, egg quality, egg metabolites, lipid metabolism, antioxidant activity, and intestinal microbial composition of quails in the late laying period. A total of 960 late-laying quails (240-day-old) were randomly divided into 4 groups of 6 replicates each (n = 40/replicate). The experimental diets of the 4 groups consisted of basal diets supplemented with 0, 50, 100, and 200 mg/kg curcumin, respectively. The feeding experiment lasted for 8 wk. The results showed that 200 mg/kg curcumin supplementation decreased mortality and increased eggshell thickness and strength compared with the 0 mg/kg curcumin supplementation during wk 5 to 8. In addition, dietary supplementation of curcumin promoted lipid metabolism, enhanced antioxidant activity, and modified intestinal microbiota structure. In conclusion, dietary supplemented with 200 mg/kg curcumin significantly improved the egg quality of quails in the late laying period, primarily by improving lipid metabolism and selectively regulating the intestinal microbial community.
Key words: curcumin, egg quality, antioxidant activity, intestinal microbiota, quail
INTRODUCTION
The quail industry stands as the third-largest sector within the global poultry domain, with its breeding segment showing gradual expansion (Abdelfattah et al., 2023; Batool et al., 2023). Quails exhibit a noteworthy laying rate, sustaining at roughly 80% even beyond the peak laying period. However, it should be noted that their mortality rate and egg breakage rate tend to increase during this phase (Onderci et al., 2006; Sahin et al., 2007). Hence, there has been a growing interest in enhancing late laying period conditions to bolster the economic viability of the quail industry.
In the poultry industry, intensive production practices are frequently adopted, involving the utilization of feed additives to bolster poultry growth, health, and overall productivity. Nevertheless, concerns have been raised regarding the potential ramifications of certain commercial feed additives on human health, including butylated hydroxytoluene (BHT), antioxidants, and antibiotics (Dhama et al., 2014; El-Sabrout et al., 2023). A study uncovered that subchronic administration of BHT led to an increase in liver weight and cytoplasmic disruption of hepatocytes in rats (Safer and al-Nughamish, 1999). Additionally, research has indicated that antibiotics present in poultry feeds may persist in milk, eggs, and meat, potentially fostering the transfer of antibiotic-resistant bacteria, immune-related pathologies, carcinogenicity, and hepatotoxicity in humans (Darwish et al., 2013). As an alternative to commercial feed additives, the utilization of natural feed additives, such as traditional Chinese medicine (TCM) supplements, has been proposed to enhance both laying performance and egg quality (Abdallah et al., 2019; Gao et al., 2022; Wu et al., 2022). TCM additives have several advantages, including natural activity, low toxicity, and low risk of drug resistance. Therefore, research on the replacement of antibiotics with TCM additives has attracted increasing attention of researchers.
Curcumin, a hydrophobic polyphenol derived from turmeric root, comprises 2 methoxylated phenols connected by α- and β-unsaturated carbonyls (Nelson et al., 2017). Multiple studies have confirmed curcumin's antioxidant and anti-inflammatory attributes, which enable it to counteract oxygen free radicals, inhibit lipid peroxidation, and safeguard cellular macromolecules from oxidative stress (Kocaadam and Şanlier, 2017; Memarzia et al., 2021). Furthermore, epidemiological, clinical, and experimental research has affirmed curcumin's pharmacological safety in treating various conditions, such as wounds, diabetes, liver ailments, and cancer (Wanninger et al., 2015; Lopresti, 2018; Ma et al., 2019). The application of curcumin in animal husbandry has also shown promise. Curcumin mitigates oxidative stress by modulating the Nrf2/HO-1 pathway in heat-stressed quails (Sahin et al., 2012) and enhances the antioxidant enzyme activity and immune function of laying hens (Liu et al., 2020). In addition, dietary supplementation of biological curcumin nanoparticles regulates antioxidant status, immunity, and microbiota of quails (Reda et al., 2020).
During the late laying period, poultry is susceptible to gut microbiota imbalances and a reduction in egg production. Although curcumin's effects have been examined in laying hens, its impact on quails during the late laying period and its underlying mechanism remain unreported. Notably, there exist significant distinctions in the intestinal microbiota and egg composition between quails and laying hens. Consequently, this study seeks to assess the influence of curcumin dietary supplementation on egg quality, antioxidant activity, and intestinal microbial composition in quails during the late laying phase. Furthermore, it endeavors to elucidate the regulatory mechanism of curcumin in enhancing the laying performance of quails during the late laying period. The findings of this investigation can serve as a foundational framework for implementing curcumin within the quail industry.
MATERIALS AND METHODS
Animal Experiments
A total of 960 late-laying quails (240-day-old) were randomly divided into 4 groups of 6 replicates each and 40 quails per replicate. The quails were housed in cages (n = 40/cage) at 25°C ± 2°C, 60 ± 5% humidity, and 16:8 h light:dark cycle. The diets of the 4 groups consisted of basal diets supplemented with 0, 50, 100, and 200 mg/kg curcumin (98% purity; Kehu Bio-technology Research Center, Guangzhou, China), respectively. The basal diet was first mixed with curcumin in small batches, and then an additional amount of basal diet was added to prepare evenly mixed feeds. Quails had ad libitum access to water and feed and were adapted to the experimental diet for 10 d, and the feeding experiment lasted for 8 wk (56 d). The animal experiments were approved by the Experimental Animal Ethics Committee of the Mudanjiang Medical University (IACUC-20220819-001).
Determination of Laying Performance
The number of eggs, egg weight, deaths, and feed intake were recorded daily during the feeding experiment. The feed-to-egg ratio was calculated by dividing feed intake by egg weight. Egg mass was calculated as the weight of eggs laid per quail per day. The laying rate was calculated as the percentage of laying quails to the total quail population, and the mortality rate was calculated as the percentage of quail deaths to the total quail population.
Determination of Egg Quality
To evaluate egg quality, 6 eggs were randomly selected from each experimental group (n = 1/replicate) on d 28 and 56. Eggshell thickness, albumen height, yolk height, egg length, egg width, and yolk diameter were measured using a vernier caliper. Eggshell weight and egg weight were determined using an analytical balance. Eggshell strength was measured using an eggshell force gauge (Robotmation Co. Ltd., Tokyo, Japan). Yolk color was determined using a Roche Egg Yolk Color Fan (Basel, Switzerland). The relative eggshell weight, egg-shape index, yolk index, and Haugh unit were calculated as described previously (Shang et al., 2020).
Determination of Egg Nutrient Composition
To evaluate egg nutrient composition, 6 eggs were randomly selected from each experimental group (n = 1/replicate) on d 28 and 56. The moisture, ash, crude fat, and crude protein contents in the eggs were determined by the Association of Official Agricultural Chemists method.
Analysis of Serum Biochemical Indexes
To analyze serum biochemical indexes, 6 quails were randomly selected from each experimental group (n = 1/replicate) on d 28 and 56. Blood samples were obtained from the wing vein of the quails. The blood samples were centrifuged at 3,000 × g for 10 min to obtain the serum samples. The serum levels of triglyceride (TG), total cholesterol (TC), low-density lipoprotein (LDL), glutathione peroxidase (GPX), and malondialdehyde (MDA) were detected using the corresponding kits from Nanjing Jiancheng Bioengineering Institute (Nanjing, China) according to the manufacturer's instructions.
Untargeted Metabolomics Analysis
For metabolomic analysis, 3 eggs were randomly selected from each experimental group on d 56. Mass spectrometry and bioinformatics analyses were performed by the Wuhan Bioacme Biological Technology Co. Ltd. (Wuhan, China). Albumen and yolk samples were obtained and analyzed by Agilent 6545 Quadrupole-Time of Flight (Q-TOF) High-resolution mass spectrometer. The Agilent Profinder software was used to correct retention time; identify, extract, integrate, and match peaks; and produce CEF files. Then Agilent Massive Parallel Processor software was used for statistical processing, and the Metlin database was used for substance identification. Principal component analysis (PCA) and orthogonal partial least-squares discriminant analysis (OPLS-DA) were performed using the “vegan” and “ropls” R packages, respectively. Metabolites with P < 0.05 and variable importance in projection (VIP) > 1 were identified as differential metabolites and visualized using the “ggplot2” and “pheatmap” R packages.
Analysis of Gut Microbiota
For the analysis of gut microbiota, 3 quails were randomly selected from each experimental group on d 56. The selected quails were euthanized and their digesta samples were obtained from the right cecum and stored at −80°C. Sequencing and bioinformatics analysis were conducted by the Wuhan Bioacme Biological Technology Co. Ltd. The raw data obtained from high-throughput sequencing were transformed into raw sequences by base call analysis and stored in the FASTQ file format. Thereafter, the amplified primers were removed using the Cutadapt software (Martin, 2011) and quality control was performed using the Fastp software (Chen et al., 2018). QIIME2 software was used for denoising, splicing, and chimera removal (Callahan et al., 2016) to obtain the feature sequence. The richness and diversity of microbiota were estimated by Chao1, ACE, Shannon, and Simpson indexes. Sample clustering was evaluated by PCA and principal coordinate analysis (PCoA). Species annotation of the feature sequence was performed using the QIIME2 software combined with the SILVA database (Quast et al., 2013; Bokulich et al., 2018). Kyoto Encyclopedia of Genes and Genomes (KEGG) and clusters of orthologous groups (COG) function prediction were performed using the PICRUSt2 software (Douglas et al., 2020).
Histopathological Analysis
For histopathological analysis, 6 quails were randomly selected from each experimental group (n = 1/replicate) on d 28 and 56. The selected quails were euthanized and the ovarian, liver, and intestinal tissues were collected. The tissue samples were then paraffin-embedded, sectioned, and hematoxylin and eosin (H&E)-stained, as described previously (Pereira et al., 2019; Yuan et al., 2021; Hou et al., 2023). Structural integrity of ovarian tissue and follicle, cell alignment and tightness, and inflammatory cell infiltration were observed to assess ovarian damage. Oil red O staining was used to assess lipid accumulation in liver tissues as described previously (Yuan et al., 2019).
Western Blot Assay
Total protein was extracted from the liver tissues and subjected to sodium dodecyl-sulfate polyacrylamide gel electrophoresis as described previously (Yuan et al., 2022). The proteins were transferred to polyvinylidene fluoride membranes and blocked with 5% milk powder. The membranes were then incubated with anti-acyl-CoA oxidase 2 (ACOX2), anti-stearoyl-CoA desaturase (SCD1), and anti-glyceraldehyde-3-phosphate dehydrogenase (GAPDH) (Affinity, Cincinnati, OH) at 4°C overnight and subsequently incubated with HRP-labeled goat anti-rabbit IgG. The protein bands were quantified using the ImageJ software.
Statistical Analysis
The data are presented as mean ± SEM. One-way analysis of variance was performed using the SPSS software v21.0 (SPSS Inc., Chicago, IL) and visualized using the GraphPad Prism software v9.0 (San Diego, CA) and R software v3.6.3. P < 0.05 was considered statistically significant.
RESULTS
Effects of Curcumin Supplementation on the Laying Performance of Quails During the Late Laying Period
The results revealed no significant effects of curcumin supplementation on the egg mass, laying rate, and feed-to-egg ratio during wk 1 to 4 and 5 to 8 of the feeding experiment (Table 1). In addition, curcumin supplementation did not improve the mortality rate of quails during wk 1 to 4; however, 100 and 200 mg curcumin supplementation significantly reduced the mortality rate of quails in the late laying period during wk 5 to 8 (Table 1). To further explore the effect of curcumin on ovarian structure, the d 28 and 56 ovarian tissue sections were H&E stained and observed. As shown in Figure 1, the ovarian tissue samples from the 0, 50, and 100 mg curcumin-supplemented groups showed slight damage with heterologous granulocyte infiltration compared to the 200 mg curcumin-supplemented group.
Table 1.
Effects of curcumin supplementation on the laying performance of quails during the late laying period.
| Parameters | 0 mg | 50 mg | 100 mg | 200 mg | P value |
|---|---|---|---|---|---|
| Egg mass (g/quail per d) | |||||
| Wk 1–4 | 8.87 ± 0.07 | 8.82 ± 0.04 | 8.79 ± 0.07 | 8.85 ± 0.06 | 0.827 |
| Wk 5–8 | 8.30 ± 0.04 | 8.37 ± 0.05 | 8.39 ± 0.05 | 8.34 ± 0.04 | 0.527 |
| Laying rate (%) | |||||
| Wk 1–4 | 86.11 ± 0.69 | 86.44 ± 0.50 | 86.00 ± 0.29 | 86.78 ± 0.42 | 0.686 |
| Wk 5–8 | 84.19 ± 0.64 | 85.16 ± 0.44 | 85.34 ± 0.86 | 85.39 ± 0.83 | 0.609 |
| Feed to egg ratio | |||||
| Wk 1–4 | 2.99 ± 0.03 | 2.95 ± 0.03 | 2.97 ± 0.02 | 2.98 ± 0.02 | 0.807 |
| Wk 5–8 | 3.15 ± 0.02 | 3.12 ± 0.02 | 3.12 ± 0.03 | 3.11 ± 0.03 | 0.742 |
| Mortality rate (%) | |||||
| WK 1–4 | 5.31 ± 0.38 | 5.24 ± 0.33 | 5.18 ± 0.20 | 5.07 ± 0.07 | 0.936 |
| Wk 5–8 | 7.04 ± 0.15a | 6.65 ± 0.23a | 6.06 ± 0.11b | 5.57 ± 0.08c | <0.001 |
Dietary curcumin levels: 0 mg, commercial diet; 50 mg, commercial diet mixed with 50 mg/kg curcumin; 100 mg, commercial diet mixed with 100 mg/kg curcumin; and 200 mg, commercial diet mixed with 200 mg/kg curcumin.
Values are expressed as mean ± standard error of the mean (n = 6).
The mean values of different superscripts in the same row were significantly different (P < 0.05).
Figure 1.
Effects of curcumin supplementation on ovarian damage in quails during the late laying period. Representative images of hematoxylin and eosin-stained ovarian tissue samples on d 28 and 56 of the feeding experiment. Scale bar, 50 μm.
Effects of Curcumin Supplementation on the Egg Quality of Quails During the Late Laying Period
Egg quality affects the edible and commercial value of eggs and is significant for the development of the egg industry. As shown in Table 2, curcumin supplementation had no significant effect on egg weight, relative eggshell weight, yolk color, egg-shape index, yolk index, and Haugh unit during wk 1 to 4 and 5 to 8 of the dietary feeding experiment. In addition, curcumin supplementation had no effect on the eggshell thickness and strength on d 28; however, on d 56, the eggshell thickness and eggshell strength increased significantly with an increase in curcumin supplementation level.
Table 2.
Effects of curcumin supplementation on the egg quality of quails during the late laying period.
| Items | 0 mg | 50 mg | 100 mg | 200 mg | P value |
|---|---|---|---|---|---|
| Egg weight (g) | |||||
| D 28 | 11.13 ± 0.20 | 12.00 ± 0.18 | 11.53 ± 0.47 | 11.60 ± 0.20 | 0.245 |
| D 56 | 11.18 ± 0.26 | 11.54 ± 0.24 | 12.12 ± 0.27 | 11.69 ± 0.19 | 0.094 |
| Eggshell thickness (mm) | |||||
| D 28 | 0.19 ± 0.02 | 0.21 ± 0.02 | 0.18 ± 0.03 | 0.22 ± 0.02 | 0.513 |
| D 56 | 0.15 ± 0.01c | 0.16 ± 0.01bc | 0.19 ± 0.01ab | 0.21 ± 0.01a | 0.003 |
| Relative eggshell weight (%) | |||||
| D 28 | 16.62 ± 1.01 | 14.64 ± 0.76 | 18.17 ± 1.54 | 15.32 ± 0.96 | 0.158 |
| D 56 | 12.65 ± 0.33 | 13.46 ± 0.27 | 13.77 ± 0.82 | 14.71 ± 0.65 | 0.119 |
| Eggshell strength (Pa) | |||||
| D 28 | 12.85 ± 0.45 | 13.48 ± 0.71 | 13.08 ± 0.72 | 14.90 ± 0.92 | 0.222 |
| D 56 | 11.76 ± 0.31b | 12.56 ± 0.39b | 12.51 ± 0.31b | 13.56 ± 0.14a | 0.006 |
| Yolk color | |||||
| D 28 | 3.20 ± 0.37 | 4.20 ± 0.37 | 3.80 ± 0.37 | 4.00 ± 0.45 | 0.340 |
| D 56 | 4.80 ± 0.58 | 5.00 ± 0.45 | 6.00 ± 0.32 | 4.40 ± 0.51 | 0.146 |
| Egg-shape index (%) | |||||
| D 28 | 1.25 ± 0.03 | 1.27 ± 0.01 | 1.33 ± 0.04 | 1.33 ± 0.03 | 0.203 |
| D 56 | 1.30 ± 0.03 | 1.25 ± 0.01 | 1.34 ± 0.03 | 1.33 ± 0.03 | 0.103 |
| Yolk index (%) | |||||
| D 28 | 50.86 ± 0.51 | 50.14 ± 1.36 | 50.93 ± 0.99 | 48.44 ± 1.27 | 0.362 |
| D 56 | 51.35 ± 2.80 | 47.98 ± 2.23 | 50.91 ± 1.35 | 52.08 ± 3.29 | 0.682 |
| Haugh unit | |||||
| D 28 | 86.64 ± 1.06 | 84.71 ± 2.04 | 90.52 ± 1.88 | 85.92 ± 1.88 | 0.148 |
| D 56 | 92.60 ± 1.57 | 87.28 ± 2.76 | 87.92 ± 1.68 | 93.99 ± 1.35 | 0.059 |
Dietary curcumin levels: 0 mg, commercial diet; 50 mg, commercial diet mixed with 50 mg/kg curcumin; 100 mg, commercial diet mixed with 100 mg/kg curcumin; and 200 mg, commercial diet mixed with 200 mg/kg curcumin.
Values are expressed as mean ± standard error of the mean (n = 6).
The mean values of different superscripts in the same row were significantly different (P < 0.05).
Effects of Curcumin Supplementation on the Egg Nutrient Composition of Quails During the Late Laying Period
The nutritional composition of quail eggs is shown in Table 3. Compared with the 0 mg curcumin-supplemented group (control), the 50, 100, and 200 mg curcumin-supplemented groups showed significantly reduced crude fat content and increased crude protein and ash contents on d 28 and 56 of the dietary feeding experiment, with the most prominent effect at 200 mg supplementation.
Table 3.
Effects of curcumin supplementation on the egg nutrient composition of quails during the late laying period.
| Nutrients | 0 mg | 50 mg | 100 mg | 200 mg | P value |
|---|---|---|---|---|---|
| Crude fat (%) | |||||
| D 28 | 12.21 ± 0.61a | 8.40 ± 0.16b | 9.05 ± 0.18b | 8.53 ± 0.26b | <0.001 |
| D 56 | 11.37 ± 0.28a | 8.88 ± 0.19b | 8.90 ± 0.24b | 8.64 ± 0.15b | <0.001 |
| Ash (%) | |||||
| D 28 | 0.83 ± 0.02c | 0.90 ± 0.03bc | 0.97 ± 0.03ab | 0.99 ± 0.03a | 0.003 |
| D 56 | 0.86 ± 0.01b | 0.90 ± 0.02ab | 0.95 ± 0.03a | 0.98 ± 0.04a | 0.036 |
| Crude protein (%) | |||||
| D 28 | 12.54 ± 0.03c | 15.35 ± 0.05b | 14.92 ± 0.03b | 15.42 ± 0.03a | <0.001 |
| D 56 | 12.34 ± 0.02c | 15.64 ± 0.08c | 15.11 ± 0.05b | 15.33 ± 0.04a | <0.001 |
Dietary curcumin levels: 0 mg, commercial diet; 50 mg, commercial diet mixed with 50 mg/kg curcumin; 100 mg, commercial diet mixed with 100 mg/kg curcumin; and 200 mg, commercial diet mixed with 200 mg/kg curcumin.
Values are expressed as mean ± standard error of the mean (n = 6).
The mean values of different superscripts in the same row were significantly different (P < 0.05).
Effects of Curcumin Supplementation on the Albumen and Yolk Metabolites of Quails During the Late Laying Period
To further investigate the curcumin-induced improvement of egg nutrient composition, we performed untargeted metabolomics to reveal the metabolic characteristics of albumen and yolk after 56 d of curcumin treatment. As shown in Figure 2A, the PCA score of albumen was not significantly different between the 4 groups. Thus, the characteristics of matching conditions were analyzed and visualized using OPLS-DA to detect outliers and identify the actual clusters, with good distinction between the 4 groups (Figure 2B–E). S-plots were used to identify differential metabolites between the 4 groups (Figure 2B–E). A total of 13 differential metabolites (VIP > 1 and P < 0.05) were identified in the albumen samples of the 4 groups (Figure 2F and Table 4). Compared with the control group, fasciculol E showed an increasing trend in the 50 and 100 mg curcumin-supplemented group, while it was significantly decreased in the 200 mg curcumin-supplemented group. In addition, the levels of (20S)-20-hydroxypregn-4-en-3-one, TG(17:1(9Z)/18:0/19:1(9Z))[iso6], Cer(d14:2(4E,6E)/20:1(11Z)), α,β-methylene ATP, 4′-hydroxyanigorootin, nudicauline, ikarisoside F, coumermic acid, 6,6′-dibromoindigotin, hexaflumuron, lapatinib, and formononetin 7-O-rutinoside were significantly increased in the 100 and 200 mg curcumin-supplemented groups.
Figure 2.
Effects of curcumin supplementation on the albumen metabolites of quails during the late laying period. (A, B) Score plots of principal component analysis (A) and orthogonal partial least-squares discriminant analysis (OPLS-DA) (B). (C–E) OPLS-DA score plots and S-plots for 0 mg and 50 mg curcumin-supplemented groups (C); 0 mg and 100 mg curcumin-supplemented groups (D); and 0 mg and 200 mg curcumin-supplemented groups (E). Variables marked in red in the S-plot could be treated as potential biomarkers. (F) Heatmap of differential metabolites in the albumen of quail eggs in the late laying period.
Table 4.
Effects of curcumin supplementation on the albumen metabolites of quails during the late laying period.
| Metabolites | 0 mg | 50 mg | 100 mg | 200 mg | VIP |
|---|---|---|---|---|---|
| Fasciculol E | 10.04 ± 8.70a | 15.18 ± 0.65a | 16.71 ± 0.19a | 0.00 ± 0.00b | 1.172 |
| (20S)-20-Hydroxypregn-4-en-3-one | 18.10 ± 1.28b | 19.69 ± 0.10a | 19.61 ± 0.04a | 19.69 ± 0.03a | 1.120 |
| TG(17:1(9Z)/18:0/19:1(9Z))[iso6] | 14.35 ± 0.68b | 15.48 ± 1.23ab | 16.68 ± 0.61a | 16.32 ± 0.21a | 1.297 |
| Cer(d14:2(4E,6E)/20:1(11Z)) | 4.71 ± 8.16b | 14.69 ± 0.52a | 16.45 ± 0.92a | 17.46 ± 2.04a | 1.396 |
| α,β-Methylene ATP | 0.00 ± 0.00b | 0.00 ± 0.00b | 9.13 ± 7.91a | 14.08 ± 0.50a | 1.725 |
| 4′-Hydroxyanigorootin | 14.29 ± 0.77b | 14.64 ± 0.85b | 16.12 ± 0.50a | 16.13 ± 0.79a | 1.496 |
| Nudicauline | 0.00 ± 0.00b | 0.00 ± 0.00b | 9.49 ± 8.22a | 14.41 ± 0.99a | 1.703 |
| Ikarisoside F | 0.00 ± 0.00b | 0.00 ± 0.00b | 9.44 ± 8.18a | 14.20 ± 0.90a | 1.697 |
| Coumermic acid | 14.43 ± 0.88b | 14.30 ± 0.46b | 16.10 ± 0.51a | 15.99 ± 0.88a | 1.725 |
| 6,6′-Dibromoindigotin | 0.00 ± 0.00c | 0.00 ± 0.00c | 13.57 ± 0.61b | 15.02 ± 1.07a | 1.813 |
| Hexaflumuron | 0.00 ± 0.00b | 0.00 ± 0.00b | 14.06 ± 0.32a | 14.29 ± 0.65a | 1.755 |
| Lapatinib | 0.00 ± 0.00b | 0.00 ± 0.00b | 14.28 ± 0.20a | 14.44 ± 0.31a | 1.752 |
| Formononetin 7-O-rutinoside | 0.00 ± 0.00b | 0.00 ± 0.00b | 14.17 ± 0.25a | 14.26 ± 0.20a | 1.748 |
VIP, variable importance in projection.
Dietary curcumin levels: 0 mg, commercial diet; 50 mg, commercial diet mixed with 50 mg/kg curcumin; 100 mg, commercial diet mixed with 100 mg/kg curcumin; and 200 mg, commercial diet mixed with 200 mg/kg curcumin.
Values are expressed as mean ± standard error of the mean (n = 3).
The mean values of different superscripts in the same row were significantly different (P < 0.05).
The results of yolk PCA and OPLS-DA analyses were similar to those of the albumen (Figure 3A–E), and a total of 14 differential metabolites (VIP > 1 and P < 0.05) were identified in the yolk samples of the 4 groups (Figure 3F and Table 5). Compared with the control group, the levels of 9Z-tritriacontene, AVE-1625, DG(16:0/17:0/0:0)[iso2], and DG(14:0/14:0/0:0) were significantly increased in the 100 and 200 mg curcumin-supplemented groups. In contrast, the levels of 2,3,3′,4,4′,5,5′-heptachlorobiphenyl, C.I. Acid Yellow 17, 8-hydroxyluteolin 8-glucoside-3′-sulfate, 11,12,13,15,16-pentachloro-14-hydroxytetracos-1Z-enyl sulfate, aflatoxin B1exo-8,9-epoxide-GSH, N-tert-butyloxycarbonyl-deacetyl-leupeptin, DG(22:0/24:1(15Z)/0:0), benzphetamine, 14-methyl-1-hexadecanol, and lignoceroyl-EA were decreased in the 100 and 200 mg curcumin-supplemented groups.
Figure 3.
Effects of curcumin supplementation on the yolk metabolites of quails during the late laying period. (A, B) Score plots of principal component analysis (A) and orthogonal partial least-squares discriminant analysis (OPLS-DA) (B). (C–E) OPLS-DA score plots and S-plots for 0 mg and 50 mg curcumin-supplemented groups (C); 0 mg and 100 mg curcumin-supplemented groups (D); and 0 mg and 200 mg curcumin-supplemented groups (E). Variables marked in red in the S-plot could be treated as potential biomarkers. (F) Heatmap of differential metabolites in the yolk of quail eggs in the late laying period.
Table 5.
Effects of curcumin supplementation on the yolk metabolites of quails during the late laying period.
| Metabolites | 0 mg | 50 mg | 100 mg | 200 mg | VIP |
|---|---|---|---|---|---|
| 9Z-Tritriacontene | 0.00 ± 0.00b | 0.00 ± 0.00b | 12.67 ± 10.97a | 19.21 ± 0.61a | 1.987 |
| AVE-1625 | 0.00 ± 0.00b | 16.57 ± 14.37a | 24.93 ± 0.50a | 25.50 ± 0.35a | 1.785 |
| DG(16:0/17:0/0:0)[iso2] | 15.62 ± 0.35c | 17.47 ± 0.43ab | 16.48 ± 0.78bc | 17.63 ± 0.63a | 1.222 |
| DG(14:0/14:0/0:0) | 16.28 ± 0.31c | 16.84 ± 0.04ab | 16.64 ± 0.22bc | 17.04 ± 0.12a | 1.222 |
| 2,3,3′,4,4′,5,5′-Heptachlorobiphenyl | 18.62 ± 0.22a | 18.42 ± 0.08ab | 17.96 ± 0.34c | 18.21 ± 0.10bc | 1.591 |
| C.I. Acid Yellow 17 | 19.39 ± 0.88a | 19.95 ± 0.29a | 17.10 ± 1.32b | 18.68 ± 0.78ab | 1.250 |
| 8-Hydroxyluteolin 8-glucoside-3′-sulfate | 20.87 ± 0.30ab | 21.07 ± 0.15a | 19.78 ± 0.75c | 20.19 ± 0.29bc | 1.587 |
| 11,12,13,15,16-pentachloro-14-hydroxytetracos-1Z-enyl sulfate | 20.70 ± 0.39a | 20.64 ± 0.47a | 18.68 ± 1.05b | 19.56 ± 0.58ab | 1.650 |
| Aflatoxin B1exo-8,9-epoxide-GSH | 19.54 ± 0.36a | 19.63 ± 0.33a | 17.89 ± 1.00b | 18.75 ± 0.57ab | 1.480 |
| N-tert-Butyloxycarbonyl-deacetyl-leupeptin | 18.55 ± 0.21a | 17.98 ± 0.48a | 17.91 ± 0.11ab | 17.13 ± 0.68b | 1.815 |
| DG(22:0/24:1(15Z)/0:0) | 18.71 ± 0.03a | 18.56 ± 0.06a | 18.54 ± 0.07ab | 18.36 ± 0.18b | 1.904 |
| Benzphetamine | 21.04 ± 0.09a | 20.76 ± 0.87a | 7.06 ± 12.23b | 0.00 ± 0.00b | 1.779 |
| 14-Methyl-1-hexadecanol | 23.22 ± 0.14a | 23.12 ± 0.09ab | 22.97 ± 0.06b | 22.96 ± 0.08b | 1.626 |
| Lignoceroyl-EA | 23.80 ± 0.10a | 23.70 ± 0.10ab | 23.40 ± 0.10bc | 23.35 ± 0.30c | 1.749 |
VIP, variable importance in projection.
Dietary curcumin levels: 0 mg, commercial diet; 50 mg, commercial diet mixed with 50 mg/kg curcumin; 100 mg, commercial diet mixed with 100 mg/kg curcumin; and 200 mg, commercial diet mixed with 200 mg/kg curcumin.
Values are expressed as mean ± standard error of the mean (n = 3).
The mean values of different superscripts in the same row were significantly different (P < 0.05).
Effects of Curcumin Supplementation on the Lipid Metabolism and Antioxidant Activity of Quails During the Late Laying Period
The serum parameters of all the groups are presented in Table 6. Analysis of serum biochemical indexes revealed that curcumin supplementation significantly reduced the TG, TC, and LDL levels on d 28 and 56, especially at 200 mg supplementation. Additionally, on d 28 and 56, curcumin supplementation significantly inhibited liver fat accumulation as observed by H&E and oil red O staining, especially at 200 mg supplementation (Figure 4A–C). Furthermore, curcumin supplementation decreased SCD1 levels and increased ACOX2 levels, particularly at 200 mg supplementation, as observed by Western blot analysis (Figure 4D, E). Among the serum antioxidant indicators, curcumin supplementation significantly increased GPX content and decreased MDA content on d 28 and 56 (Table 6), especially at 200 mg supplementation. These results indicate that curcumin regulates lipid metabolism and antioxidant activity of quails during the late laying period.
Table 6.
Effects of curcumin supplementation on the serum biochemical parameters of quails during the late laying period.
| Serum parameters | 0 mg | 50 mg | 100 mg | 200 mg | P value |
|---|---|---|---|---|---|
| TG (mmol/L) | |||||
| D 28 | 11.22 ± 0.10a | 5.39 ± 0.07b | 3.82 ± 0.10c | 3.37 ± 0.09d | <0.001 |
| D 56 | 15.66 ± 0.04a | 14.04 ± 0.26b | 7.14 ± 0.13c | 2.78 ± 0.02d | <0.001 |
| TC (mmol/L) | |||||
| D 28 | 4.63 ± 0.12a | 3.10 ± 0.09b | 2.69 ± 0.01c | 2.51 ± 0.13c | <0.001 |
| D 56 | 12.63 ± 0.56a | 7.81 ± 0.09b | 3.52 ± 0.21c | 1.73 ± 0.01d | <0.001 |
| LDL (mmol/L) | |||||
| D 28 | 0.28 ± 0.01a | 0.15 ± 0.01b | 0.10 ± 0.01c | 0.05 ± 0.01d | <0.001 |
| D 56 | 0.94 ± 0.05a | 0.65 ± 0.01b | 0.35 ± 0.05c | 0.17 ± 0.01d | <0.001 |
| GPX (U/L) | |||||
| D 28 | 386.73 ± 132.0c | 788.78 ± 77.21bc | 1164.29 ± 195.83b | 1941.84 ± 61.03a | <0.001 |
| D 56 | 665.31 ± 173.5c | 1178.57 ± 101.91bc | 1678.57 ± 250.66b | 2686.73 ± 80.50a | <0.001 |
| MDA (nmol/mL) | |||||
| D 28 | 17.59 ± 0.53a | 14.38 ± 0.05b | 13.29 ± 1.87b | 9.64 ± 0.19c | <0.001 |
| D 56 | 24.22 ± 0.46a | 19.99 ± 0.06b | 15.26 ± 1.63c | 14.11 ± 0.52c | <0.001 |
TG, triglyceride; TC, cholesterol; LDL, low-density lipoprotein; GPX, glutathione peroxidase; MDA, malondialdehyde.
Dietary curcumin levels: 0 mg, commercial diet; 50 mg, commercial diet mixed with 50 mg/kg curcumin; 100 mg, commercial diet mixed with 100 mg/kg curcumin; and 200 mg, commercial diet mixed with 200 mg/kg curcumin.
Values are expressed as mean ± standard error of the mean (n = 6).
The mean values of different superscripts in the same row were significantly different (P < 0.05).
Figure 4.
Effects of curcumin supplementation on liver fat accumulation in quails during the late laying period. (A) Representative images of hematoxylin and eosin- and oil Red O-stained liver tissue samples. Scale bar, 50 μm. (B, C) Statistical analysis of the results of oil red O staining. a, bThe mean values of different superscripts were significantly different (P < 0.05). (D, E) Western blot analysis of the levels of acyl-CoA oxidase 2 (ACOX2) and stearoyl-CoA desaturase (SCD1) in the liver tissues. Protein density was quantified using densitometry. ACOX2 and SCD1 were normalized to glyceraldehyde-3-phosphate dehydrogenase. a–cThe mean values of different superscripts were significantly different (P < 0.05).
Effects of Curcumin Supplementation on the Intestinal Microbial Composition of Quails During the Late Laying Period
To further investigate the effects of curcumin supplementation on intestinal morphology and function of quails during the late laying period, we performed H&E staining and microbiome analysis. The results of H&E staining of d 28 and 56 intestinal samples revealed epithelial cell shedding as the primary intestinal injury. The severity of intestinal injury decreased with increasing curcumin supplementation, with the highest severity in the control group and essentially no injury in the 200 mg curcumin-supplemented group (Figure 5). The intestinal microbiota composition was analyzed after 56 d of curcumin treatment using Chao1 and ACE indexes to estimate species abundance and Shannon and Simpson indexes to estimate microbial diversity. As shown in Figure 6A–C, there were no significant differences in the Chao1, ACE, and Simpson diversity indexes of the intestinal microbiota of the 4 groups; however, the Shannon diversity of the 200 mg curcumin-supplemented group was significantly higher than that of the control group (Figure 6D). As shown in Figure 6E, the 0, 50, 100, and 200 mg curcumin-supplemented groups shared 364 gut microbiota features and had 441, 454, 685, and 662 unique features, respectively. These results indicate that curcumin supplementation improves the gut microbial diversity of quails during the late laying period. PCA and PCoA showed significant differences in the gut microbial composition of the control group and that of the 100 and 200 mg curcumin-supplemented groups (Figure 6F, G).
Figure 5.
Effects of curcumin supplementation on the intestinal injury in quails during the late laying period. Representative images of hematoxylin and eosin-stained intestinal tissue samples on d 28 and 56 of the feeding experiment. Scale bar, 50 μm.
Figure 6.
Effects of curcumin supplementation on the intestinal microbiota composition of quails during the late laying period. (A–D) Chao1 (A); ACE (B); Shannon (C); and (D) Simpson indexes. a, bThe mean values of different superscripts were significantly different (P < 0.05). (E) Venn diagram of shared and unique features of the 0, 50, 100, and 200 mg curcumin-supplemented groups. (F, G) principal component analysis (F) and orthogonal partial least-squares discriminant analysis plots (G). (H, I) Bar plots of the intestinal microbial composition at phylum (H) and genus (I) levels.
Based on these results, we further explored the gut microbiota composition and abundance of late-laying quails. At the phylum level (Figure 6H), Firmicutes, Actinobacteriota, and Bacteroidetes were the dominant bacteria in the 4 groups. Compared with the control group, the relative abundance of Actinobacteriota decreased in the 100 mg (20.12 vs. 24.66%) and 200 mg (21.29 vs. 24.66%) curcumin-supplemented groups. However, compared with the control group, the relative abundances of Firmicutes increased (56.07 vs. 48.20%) and Bacteroidetes decreased (16.56 vs. 18.86%) in the 100 mg curcumin-supplemented group, while the relative abundances of Firmicutes decreased (44.63 vs. 48.20%) and Bacteroides increased (28.04 vs. 18.86%) in the 200 mg curcumin-supplemented group. Figure 6I shows the dominant bacteria in the 4 groups at the genus level. Compared with the control group, the abundances of Enterococcus, Lactobacillus, Bifidobacterium, Rikenellaceae_RC9_gut_group, Bacteroides, Enorma, Corynebacterium, Saccharimonadales, and Aerococcus were altered in the curcumin-supplemented groups. The opposite trend was observed between the 100 mg and 200 mg curcumin-supplemented groups.
PICRUSt2 was used to align the feature sequences with the reference sequences of the microbial genome database, and the gene information of the unknown species was predicted based on the gene and abundance information of the known species, to predict the gene function. We performed COG function prediction, and the results revealed that compared with the control group, the 200 mg curcumin-supplemented group showed significantly improved biological function, including lipid metabolism. The significant COG functions are presented in Figure 7. In addition, we conducted the KEGG pathway enrichment analysis (Supplementary Table S1), and consistent with COG prediction, the results of the KEGG pathway enrichment analysis revealed that the 200 mg curcumin-supplemented group showed significantly improved biological function compared with the control group. The top 20 significantly enriched KEGG pathways are presented in Figure 8.
Figure 7.
Clusters of orthologous groups (COG) function prediction of intestinal microbiota genes of quails during the late laying period. Heatmap of significant COG functions in the 0, 50, 100, and 200 mg curcumin-supplemented groups.
Figure 8.
Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway prediction of intestinal microbiota genes of quails during the late laying period. Heatmap of the top 20 significant KEGG pathways in the 0, 50, 100, and 200 mg curcumin-supplemented groups.
DISCUSSION
Curcumin has strong antioxidant and anti-inflammatory activities owing to its phenolic structure. The application of curcumin in livestock and poultry production has attracted increasing attention in recent years. As a natural feed additive, curcumin contributes to the growth and disease resistance of livestock and poultry animals (Pan et al., 2022; Sureshbabu et al., 2023). However, the effects of curcumin on quails, especially in the late laying period, have rarely been reported. Therefore, this study aimed to investigate the effects of curcumin supplementation on the egg quality of quails in the late laying period. The results of our study showed that dietary supplementation of curcumin significantly improved egg quality, antioxidant activity, and intestinal microbiota structure of quails in the late laying period, especially at 200 mg supplementation.
Egg quality is a crucial factor affecting the economic benefits of the poultry industry. The late laying period in quails is characterized by a decreased laying rate, increased soft-shell egg production, and increased mortality rate. Previous studies found that curcumin improved the antioxidant enzyme activity and immune function of laying hens (Galli et al., 2018; da Rosa et al., 2020; Liu et al., 2020). Eggshell thickness and strength are important indicators of egg quality and are crucial factors for egg transportation and storage (Cheng and Ning, 2023). The availability of intestinal calcium during eggshell calcification has been reported to be essential for providing sufficient calcium to meet eggshell quality requirements (Skřivan et al., 2010). The results of our study showed that dietary supplementation of curcumin significantly enhanced eggshell thickness and strength on d 56 of the feeding experiment, suggesting an increased calcium absorption rate in quails with increasing curcumin supplementation.
Eggs are rich in proteins, fats, vitamins, and minerals, and their compositions may be affected by the laying period (Kuang et al., 2018). Albumen contains antioxidants, such as ovalbumin, which can covalently bind to polysaccharides to enhance its antioxidant activity (Rakonjac et al., 2014). Yolk contains high levels of cholesterol and saturated fatty acids and its consumption increases the risk of cardiovascular diseases (Weggemans et al., 2001). The results of our study revealed that dietary supplementation of curcumin increased protein content and decreased fat content in quail eggs in the late laying period.
Previous studies found that curcumin regulates lipid metabolism and inhibits hepatic steatosis (Feng et al., 2019). Therefore, we further examined the serum biochemical indicators associated with lipid metabolism and antioxidant activity in all the groups. Our results revealed that dietary supplementation of curcumin decreased liver fat accumulation by promoting lipid metabolism and significantly improved the antioxidant activity by increasing GPX level and decreasing MDA level. This decrease in fat accumulation and increase in antioxidant activity may be associated with the decreased mortality of late-laying quails with curcumin supplementation.
Intestinal microbiota and their metabolites act as signaling molecules within the gut, liver, and reproductive tract and may directly or indirectly affect poultry health and egg quality (Nicholson et al., 2012; Cryan et al., 2020; Agus et al., 2021). Curcumin enhances the intestinal antioxidant capacity of ducklings by regulating antioxidant gene expression (Ruan et al., 2019). Additionally, curcumin plays a protective role against oxidative damage by regulating lipid metabolism and intestinal microbiota (Zhai et al., 2020) These findings are consistent with the results of this study, thus further confirming the positive effects of curcumin on the intestinal health of late-laying quails.
CONCLUSIONS
This study confirmed that dietary supplementation of curcumin (particularly at 200 mg/kg) increased eggshell thickness, promoted lipid metabolism, and enhanced the antioxidant activity of quails in the late laying period. These beneficial effects of curcumin may be attributed to the selective modulations of the intestinal microbiota. Therefore, curcumin can be used as a natural and safe feed additive to reduce mortality and improve the egg quality of quails in the late laying period.
ACKNOWLEDGMENTS
The authors acknowledge the financial and technical support provided by the College of Veterinary Medicine, Northeast Agriculture University, and College of Life Sciences of the Mudanjiang Medical University. This work was financially supported by the Young Innovative Talents Project of the Education Department of Heilongjiang Province (UNPYSCT-2020060).
DISCLOSURES
There was no conflict of interest.
Footnotes
Supplementary material associated with this article can be found in the online version at doi:10.1016/j.psj.2023.103233.
Appendix. Supplementary materials
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