Skip to main content
NCBI home page
Poultry Science logoLink to Poultry Science
. 2023 Feb 2;102(6):102545. doi: 10.1016/j.psj.2023.102545

Effects of dietary theabrownins on production performance, egg quality, and ovarian function of laying hens with different ages

Wenwen Xu 1,1, Yuxiang Ayu 1,1, Jianping Wang 1, Qiufeng Zeng 1, Shiping Bai 1, Xuemei Ding 1, Li Lv 1, Huanwei Peng 1, Yue Xuan 1, Keying Zhang 1,2
PMCID: PMC10106962  PMID: 37019071

Abstract

This experiment was conducted to investigate the effect of theabrownins (TB) on production performance, egg quality, and ovarian function of laying hens at different ages. A total of 240 Lohmann laying hens were assigned in a 2 × 2 factorial design, which encompassed 2 layers ages (47-wk-old and 67-wk-old) and 2 dietary levels of TB (0 and 100 mg/kg) for 12 wk. Results showed that older layers had lower laying rate, egg mass, and higher feed-to-egg ratio (F/E), egg weight and unqualified egg rate than the younger layers (P(AGE) < 0.01) during all the experimental period. The effect of TB was found to increase egg laying rate and feed efficiency during 5 to 8 wk, 9 to 12 wk and the overall phases and decreased unqualified egg rate during 1 to 4 wk and the overall phases (P(TB) ≤ 0.05). The eggshell quality (strength, thickness), albumen quality (albumen height and Haugh unit) of eggs from older layers were decreased during overall phases (P(AGE) ≤ 0.05). TB increased eggshell strength during all phases and enhanced eggshell thickness at the end of wk 4 and 8 and increased albumen height and Haugh unit at the end of wk 8 and 12 of older layers (P(Interaction) ≤ 0.05). In addition, TB also increased egg quality of older layers after 14 d storage. A decrease in the serum concentration of progesterone, melatonin, follicle stimulating hormone, estradiol was observed in the older compared to the younger ones (P(AGE) < 0.05), while the increase in serum concentration of progesterone, melatonin, anti-Müllerian hormone (AMH) were more emphasized when older hens received TB supplemented diet (P(Interaction) < 0.05). The older layer demonstrated lower the concentration of glutathione (GSH) (P(AGE) < 0.05). And the activity of glutathione-s-transferase (GST) was significantly decreased in layers under 67-wk-old (P(AGE) <0.05). The increase in concentration of GSH and the decrease in concentration of malondialdehyde (MDA) were more pronounced when TB were supplemented in 67-wk-old layers (P(Interaction) ≤ 0.05). Layers at 67-wk-old had lower mRNA expression of Heme oxygenase 1 (HO-1) (P(AGE) < 0.01) in ovary. Dietary TB supplementation upregulated mRNA gene expression of HO-1, Nuclear factor E2 related factor 2 (Nrf2), Quinone oxidoreductase 1 (NQO1) (P(TB) < 0.01). Dietary TB upregulated mRNA expression of ovarian reproductive hormone receptor (estrogen receptor 1 [ESR1] and steroidogenic acute regulatory protein 1 [StAR1]]; P(TB) < 0.01). The results suggest feeding TB (100 mg/kg) could improve the egg production rate, egg quality, and antioxidant capacity of the ovary. Moreover, the effect of TB was more pronounced in older layers (64-wk-old vs. 47-wk-old).

Key words: Pu-erh tea theabrownins, laying hens, egg quality, antioxidant capacity, ovary function

INTRODUCTION

For sexually mature female chicken, reproductive performance decreases with age. The reproductive system ages earlier than other systems and aging of the ovary plays a major role in initiating or accelerating a series of other aging changes (Joyner et al., 1987). As we all know, ovarian senescence will cause its functional decline. The ovarian function of laying hens is divided into reproductive function and endocrine function, which are of great significance to maintain the health of laying hens (Rojas, 1995; Pan et al., 2014) Many studies have shown that the follicular growth rate of laying hens tends to decrease in the later stage of laying, and the reproductive function and endocrine of ovaries decrease, which eventually leads to the decline of egg laying ability (Liu et al., 2018b; Yao et al., 2020; Hao et al., 2021; Zhou et al., 2022). So, it is very important to delay the deterioration of ovarian function, improve the function of ovary, and prolong the laying period of laying hens.

The adjustment of diet structure can effectively alleviate the aging. Studies have found that tea diet is rich in polyphenols, which has a protective effect on the body and is closely related to the health of the body. Tea polyphenols can reduce free radical damage and enhance the antioxidant capacity of the body (Yuan et al., 2016; Zhou et al., 2020; Zhu et al., 2020). Theabrownins (TB), a complex product formed by oxidative polymerization of polyphenols in the process of accelerated oxidation or natural oxidation by pile fermentation unique to Pu-erh tea (Liang et al., 2005; Gong et al., 2010). As one of the main bioactive components in Pu-erh tea, the average content of TB in Pu-erh tea is about 12% (Liu et al., 2018a). TB is a brown, water-soluble tea pigment that is insoluble in chloroform, ethyl acetate, and n-butanol, could lower cholesterol levels significantly. And it contains a considerable amount of protein, sugars, acids with low acute toxicity (Yue et al., 2019; Ding et al., 2022b). And some studies have proved that TB have the functions of decreasing blood lipids (Gong et al., 2010; Kuang et al., 2020), lowering blood glucose (Huang et al., 2019; Yue et al., 2019), anticancer (Jin et al., 2018), antioxidation, and antiaging (Lei et al., 2022) and so on. However, literatures on the effect of TB on reproductive performance and ovarian function in late laying phases of laying hens are limited.

Therefore, in this study, the purpose was to verify the hypothesis that dietary theabrownins can alleviate ovarian senility of laying hens through antioxidant effects, thereby improving performance, egg quality, and ovarian function of laying hens.

MATERIALS AND METHODS

Animals, Experiment Design, and Management

The experiment was carried out according to the Chinese guidelines for Animal Welfare and approved by the Animal Care and Use Committee of Sichuan Agricultural University. A total of 240 healthy Lohmann gray laying hens with 2 different ages from the same parental generation were fed with a same basal diet and reared in the same house. Hens were assigned in a 2 × 2 factorial design, which encompassed 2 layers ages (47-wk-old and 67-wk-old) and 2 dietary levels of TB (0 and 100 mg/kg diet) for 12 wk. 120 hens of each age were randomly assigned to 2 treatments with 10 replicates of 6 hens. Theabrownins was obtained from Yunnan Tangren Biotechnology Co., Ltd (Yunnan, China), with the purity of 81%.

All birds were fed a corn-soybean meal basal diet in this experiment. The basic diet composition and nutrition level were prepared according to NRC (1994) and Chinese Chicken Feeding Standard (2004). The experimental feed was a particle size of about 4.5 mm powder. The composition and nutrition level of basic diet are shown in Supplementary Table 1. The experiment adopted a 3-layer ladder cage (45 × 45 × 43), with 3 chickens in each cage and 2 adjacent cages as one replicate. All the laying hens were evenly distributed in the middle layer. The housing conditions (20°C–22°C, 16 h light-8 h dark cycle; regular daily ventilation and weekly strict disinfection) were carefully controlled throughout the duration of study.

Sample Collection

Egg quality, egg weights, and unqualified eggs (including those with sand-shell, double-yolk, soft-shell, dirty, cracked, and broken egg) were recorded daily. The relevant weekly data were summarized in the unit of repetition, and the stage laying performance indicators were calculated according to the "Nominals and Statistical Methods for Measurement of Poultry Performance" (NY/T823-2020), which mainly included laying rate, egg weight, average daily feed intake, feed-to-egg ratio (F/E), and unqualified egg rate. At the end of feeding period, 10 chickens for each treatment (one bird per replicate) were selected randomly, and 10 mL of blood was collected from the jugular vein or the inferior wing vein. Blood samples were placed at room temperature for 1 h, and centrifuged at 3,000 r/min for 15 min. Then serum was stored at −20°C for later analysis. Thereafter, the birds were euthanized by exsanguination and necropsied, ovarian tissues (ovary cortex) were separated and immediately stored at −80℃ till analysis.

Egg Quality

At the end of wk 4, 8, and 12 of the experiment, 30 eggs were collected randomly in 3 continuous days from each group (3 eggs/replicate, 30 eggs/treatment) for the measurement of regular egg quality. At the end of wk 12 of the experiment, eggs were selected (3 eggs/replicate, 30 eggs/treatment) and stored at 25℃ for 14 d to determine the regular egg quality. The eggshell thickness was measured using a Peacock dial gauge (P-1 Model, Meg Co Ltd., Ozaki, Japan) after removing the shell membrane and it is represented as the average thickness of the blunt end, tip, and equator of the shell. Eggshell strength was measured by eggshell force gauge model II (Robotmation Co., Ltd., Tokyo, Japan). Egg internal quality (including Haugh unit [HU], albumen height, and yolk color) were analyzed via an Egg Multi-tester (EMT-5200, Robotmation Co., Ltd.). Eggshell was separated from the albumen and yolk, washed to remove residual albumen, and dried at 65°C for 4 h, then weighed.

Serum Reproductive Hormones Content

Serum concentration of progesterone (Prog), melatonin (MT), follicle stimulating hormone (FSH), 17β-estradiol (E2), luteinizing hormone (LH), and anti-Müllerian hormone (AMH) were assessed by ELISA kits (Nanjing Jiancheng Biotechnology Co., Ltd., Nanjing, China)

Ovarian Antioxidant Capacity

Antioxidant kit (Nanjing Jiancheng Biotechnology Co., Ltd.) was used to determine the indexes related to ovarian antioxidant capacity, including activities of glutathione (GST), glutathione peroxidase (GSH-Px), and content of glutathione (GSH) and malondialdehyde (MDA).

Real-Time PCR for Ovarian Function Related mRNA Expression

Total RNA for ovary tissue (1 layers/replicate, 8 replicates/treatment) was prepared using TRIzol reagent (TaKaRa, Dalian, China) and assessed using nucleic acid concentration analyzer NanoDrop 2,000 (Thermo Fisher, Waltham, MA). Complementary DNA (cDNA) was synthesized was synthesized using PrimeScript RT reagent Kit with gDNA Erase (RR047 A, Takara) following the manufacturer's recommended protocol. ABI Prism 7000 Real-time Detection System using SYBR Premix Ex Taq II kit (TaKaRa) were used to conduct the quantitative real-time PCR. The primer sequence for all the genes (Nuclear factor E2 related factor 2 [Nrf2], Heme oxygenase 1 [HO-1], Quinone oxidoreductase 1 [NQO1], Androgen receptor [AR], Estrogen receptor 1 [ESR1], Steroidogenic acute regulatory protein 1 [StAR1]) are presented in Supplementary Table 2. The house keeping gene (β-actin) was assessed for the stability of expression. The expression of each gene was calculated by using the 2−ΔΔCT method (Livak and Schmittgen, 2001).

Statistical Analysis

Data were analyzed 2-way analysis of variance (ANOVA) using GLM procedure of SAS 9.2 (SAS Institute, Cary, NC) and GraphPad Prism (GraphPad Inc., La Jolla, CA). The model included the main effects of the age of chickens and addition of theabrownins, as well as their interaction. The results are presented as mean and SEM.

RESULTS

Production Performance

As shown in Table 1, Table 2, Table 3-4, the 67-wk-old hens presented lower egg laying rate, egg mass, and higher egg weight, FCR, unqualified egg rate (P(AGE) < 0.01) during all the experimental period. Dietary supplementation with TB significantly increased egg laying rate and feed efficiency during 5 to 8 wk, 9 to 12 wk and the overall phases and decreased unqualified egg rate during 1 to 4 wk and the overall phases (P(TB) ≤ 0.05). The decreasing effect of TB on egg weight, unqualified egg rate, and FCR was significantly higher in 67 wk old layers than that in 47 wk old layers during 1 to 4 wk and the overall phases (P(Interaction) ≤ 0.05).

Table 1.

Effect of theabrownins on production performance of different age laying hens during 1 to 4 wk.1

Item Laying rate, % Egg weight, g Egg mass, g/hen/d ADFI, g Feed-to-egg ratio (F/E) Unqualified egg rate, %
Age TB
47 wk 0 93.16 61.22b 57.01 109.21ab 1.92 0.96c
47 wk 100 93.61 61.15b 57.23 111.11a 1.94 1.35c
67 wk 0 68.24 63.86a 43.60 109.95a 2.55 12.65a
67 wk 100 74.26 62.04b 46.05 105.38b 2.33 6.59b
SEM 2.34 0.44 1.46 1.42 1.42 1.14
Main effect
Age
 47-wk-old 93.38 61.18 57.12 110.16 1.93 1.16
 67-wk-old 71.25 62.95 44.83 107.66 2.44 9.62
TB, mg/kg
 0 80.70 62.54 50.30 109.58 2.23 6.81
 100 83.93 61.59 51.64 108.25 2.14 3.97
SEM 1.66 0.31 1.03 1.01 0.05 0.80
P-value
 Age <0.01 <0.01 <0.01 0.09 <0.01 <0.01
 TB 0.18 0.04 0.36 0.36 0.18 0.02
 Age × TB 0.24 0.05 0.45 0.03 0.10 <0.01
Open in a new tab
a,b

Means within a column with different superscripts differ significantly (P ≤ 0.05).

1

Each mean represents 6 layers/replicate, 10 replicates/treatment.

Abbreviations: ADFI, average daily feed intake; FCR, feed conversation ratio; SEM, standard error of the mean; TB, theabrownins (0 or 100 mg/kg feed).

Table 2.

Effect of theabrownins on production performance of different age laying hens during 5 to 8 wk.1

Item Laying rate, % Egg weight, g Egg mass, g/hen/d ADFI, g Feed-to-egg ratio (F/E) Unqualified egg rate, %
Age TB
47 wk 0 87.09 61.37 53.47 102.81 1.94 0.77
47 wk 100 92.73 61.46 56.98 104.22 1.83 0.74
67 wk 0 68.51 63.90 43.72 104.11 2.40 11.57
67 wk 100 73.51 62.98 46.37 104.21 2.28 8.44
SEM 2.18 0.47 1.45 1.30 0.07 1.31
Main effect
Age
 47-wk-old 89.91a 61.42b 55.23a 103.52 1.88b 0.75b
 67-wk-old 71.01b 63.44a 45.05b 104.16 2.34a 10.00a
TB, mg/kg
 0 77.80b 62.63 48.59b 103.46 2.17 6.17
 100 83.12a 62.22 51.68a 104.21 2.06 4.59
SEM 1.54 0.33 1.03 0.92 0.05 0.92
P-value
 Age <0.01 <0.01 <0.01 0.62 <0.01 <0.01
 TB 0.02 0.38 0.04 0.56 0.14 0.23
 Age × TB 0.88 0.29 0.77 0.62 0.93 0.24
Open in a new tab
a,b

Means within a column with different superscripts differ significantly (P ≤ 0.05).

1

Each mean represents 6 layers/replicate, 10 replicates/treatment.

Abbreviations: ADFI, average daily feed intake; FCR, feed conversation ratio; SEM, standard error of the mean; TB, theabrownins (0 or 100 mg/kg feed).

Table 3.

Effect of theabrownins on production performance of different age laying hens during 9 to 12 wk.1

Item Laying rate, % Egg weight, g Egg mass, g/hen/d ADFI, g Feed-to-egg ratio (F/E) Unqualified egg rate, %
Age TB
47 wk 0 84.05 61.23 51.51 101.46 1.99 1.24
47 wk 100 91.70 61.00 55.91 102.57 1.84 0.41
67 wk 0 63.87 63.66 40.66 105.28 2.62 12.26
67 wk 100 71.08 62.75 44.72 104.80 2.42 8.81
SEM 2.55 0.45 1.75 1.10 0.10 1.26
Main effect
Age
 47-wk-old 87.87a 61.11b 53.71a 102.02b 1.91b 0.82b
 67-wk-old 67.47b 63.20a 42.69b 105.04a 2.52a 10.53a
TB, mg/kg
 0 73.96b 62.45 46.08b 103.37 2.30 6.75
 100 81.38a 61.87 50.31a 103.69 2.13 4.61
SEM 1.80 0.32 1.23 0.78 0.07 0.89
P-value
 Age <0.01 <0.01 <0.01 <0.01 <0.01 <0.01
 TB <0.01 0.21 0.02 0.78 0.09 0.10
Age × TB 0.93 0.45 0.92 0.47 0.84 0.30
Open in a new tab
a,b

Means within a column with different superscripts differ significantly (P ≤ 0.05).

1

Each mean represents 6 layers/replicate, 10 replicates/treatment.

Abbreviations: ADFI, average daily feed intake; FCR, feed conversation ratio; SEM, standard error of the mean; TB, theabrownins (0 or 100 mg/kg feed).

Table 4.

Effect of theabrownins on production performance of different age laying hens during 1 to 12 wk.1

Item Laying rate, % Egg weight, g Egg mass, g/hen/d ADFI, g Feed-to-egg ratio (F/E) Unqualified egg rate, %
Age TB
47 wk 0 88.10 61.28 53.99 104.49 1.94c 0.99c
47 wk 100 92.68 61.20 56.71 105.97 1.87c 0.83c
67 wk 0 66.88 63.81 42.68 106.45 2.50a 12.81a
67 wk 100 74.84 62.59 46.88 104.80 2.25b 7.95b
SEM 1.39 0.40 0.98 1.04 0.04 1.18
Main effect
Age
 47-wk-old 90.39 61.24 55.35 105.23 1.91 0.91
 67-wk-old 70.86 63.20 44.78 105.62 2.37 10.38
TB, mg/kg
 0 77.49 62.54 48.33 105.47 2.22 6.90
 100 83.76 61.90 51.80 105.38 2.06 4.39
SEM 0.98 0.28 0.69 0.74 0.03 0.83
P-value
 Age <0.01 <0.01 <0.01 0.71 <0.01 <0.01
 TB <0.01 0.12 <0.01 0.93 <0.01 0.04
 Age × TB 0.23 0.16 0.45 0.14 0.04 0.05
Open in a new tab
a,b

Means within a column with different superscripts differ significantly (P ≤ 0.05).

1

Each mean represents 6 layers/replicate, 10 replicates/treatment.

Abbreviations: ADFI, average daily feed intake; FCR, feed conversation ratio; SEM, standard error of the mean; TB, theabrownins (0 or 100 mg/kg feed).

Egg Quality

As shown in Table 5, Table 6, Table 7-8, eggshell strength, eggshell thickness, albumen height, and Haugh unit of eggs from older hens were significantly lower during the overall phases (P(AGE) ≤ 0.05). The effect of TB was found to enhance the eggshell strength during all phases and enhanced eggshell thickness at the end of wk 4 and 8 and increased albumen height and Haugh unit at wk 8 and 12 of older layers (P(Interaction) ≤ 0.05). TB was also observed to increase egg quality of older layers after 14 d of storage.

Table 5.

Effect of theabrownins on egg quality of different age laying hens in the 4th wk.1

Item Eggshell strength, kg/cm2 Albumen height, mm York color Haugh unit Eggshell thickness, mm
Age TB
47 wk 0 4.02 7.92a 6.38 88.48 0.376a
47 wk 100 4.58 7.85a 6.30 88.78 0.381a
67 wk 0 3.39 6.86b 6.68 83.46 0.311b
67 wk 100 3.92 7.84a 5.94 83.44 0.389a
SEM 0.16 0.27 0.23 1.78 0.007
Main effect
Age
 47-wk-old 4.30 7.88 6.34 88.63 0.378
 67-wk-old 3.66 7.35 6.30 83.45 0.350
TB, mg/kg
 0 3.70 7.39 6.53 85.97 0.343
 100 4.25 7.85 6.12 86.11 0.385
SEM 0.11 0.19 0.16 1.26 0.005
P-value
 Age <0.01 0.05 0.86 <0.01 <0.01
 TB <0.01 0.09 0.09 0.94 <0.01
 Age × TB 0.90 0.05 0.17 0.93 <0.01
Open in a new tab
a,b

Means with different superscripts within a column differ significantly (P ≤ 0.05).

1

Each mean represents 3 eggs/replicate, 10 replicates/treatment.

Abbreviations represented: SEM, standard error of the mean; TB, theabrownins (0 or 100 mg/kg feed), AGE (47-wk-old or 67-wk-old).

Table 6.

Effect of theabrownins on egg quality of laying hens with different ages in the 8th wk.1

Item Eggshell strength, kg/cm2 Albumen height, mm York color Haugh unit Eggshell thickness, mm
Age TB
47 wk 0 3.99 7.26bc 6.11 84.19b 0.362a
47 wk 100 4.40 7.68ab 6.10 87.18a 0.364a
67 wk 0 3.45 6.81c 6.28 80.48c 0.319b
67 wk 100 4.19 8.00a 6.44 88.32a 0.368a
SEM 0.16 0.16 0.17 1.07 0.007
Main effect
Age
 47-wk-old 4.20 7.47 6.10 85.69 0.363
 67-wk-old 3.82 7.41 6.36 84.40 0.344
TB, mg/kg
 0 3.72 7.03 6.20 82.33 0.340
 100 4.30 7.84 6.27 87.75 0.366
SEM 0.12 0.11 0.12 0.76 0.005
P-value
 Age 0.03 0.71 0.14 0.23 <0.01
 TB <0.01 <0.01 0.69 <0.01 <0.01
 Age × TB 0.31 0.02 0.63 0.03 <0.01
Open in a new tab
a,b

Means with different superscripts within a column differ significantly (P ≤ 0.05).

1

Each mean represents 3 eggs/replicate, 10 replicates/treatment.

Abbreviations: SEM, standard error of the mean; TB, theabrownins (0 or 100 mg/kg feed), AGE (47-wk-old or 67-wk-old).

Table 7.

Effect of theabrownins on egg quality of laying hens with different ages in the 12th wk.1

Item Eggshell strength, kg/cm2 Albumen height, mm York color Haugh unit Eggshell thickness, mm
Age TB
47 wk 0 4.20 7.76 5.70 86.67 0.366a
47 wk 100 4.49 7.90 5.67 88.58 0.356a
67 wk 0 3.45 6.69 5.56 79.59 0.336b
67 wk 100 3.81 7.78 5.64 86.18 0.356a
SEM 0.10 0.25 0.23 1.46 0.005
Main effect
Age
 47-wk-old 4.34 7.83 5.68 87.63 0.361
 67-wk-old 3.63 7.24 5.60 82.88 0.346
TB, mg/kg
 0 3.82 7.22 5.63 83.13 0.351
 100 4.15 7.84 5.66 87.38 0.356
SEM 0.07 0.18 0.16 1.03 0.003
P-value
 Age <0.01 0.02 0.71 <0.01 <0.01
 TB <0.01 0.02 0.91 <0.01 0.25
 Age × TB 0.71 0.07 0.79 0.12 <0.01
Open in a new tab
a,b

Means with different superscripts within a column differ significantly (P ≤ 0.05).

1

Each mean represents 3 eggs/replicate, 10 replicates/treatment.

Abbreviationsd: SEM, standard error of the mean; TB, theabrownins (0 or 100 mg/kg feed), AGE (47-wk-old or 67-wk-old).

Table 8.

Effect of theabrownins on egg quality of laying hens with different ages after 14 d storage.1

Item Eggshell strength, kg/cm2 Albumen height, mm York color Haugh unit Eggshell thickness, mm
Age TB
47 wk 0 4.26a 5.05 5.81 67.89 0.376a
47 wk 100 4.23a 5.92 6.08 73.75 0.381a
67 wk 0 3.49b 4.64 5.59 57.78 0.334b
67 wk 100 4.19a 5.55 5.50 68.32 0.382a
SEM 0.13 0.18 0.15 1.43 0.007
Main effect
Age
 47-wk-old 4.34 5.48 5.94 70.82 0.379
 67-wk-old 3.84 5.10 5.54 63.05 0.358
TB, mg/kg
 0 3.88 4.84 5.70 62.84 0.355
 100 4.31 5.74 5.79 71.03 0.381
SEM 0.09 0.13 0.10 1.01 0.005
P-value
 Age <0.01 0.04 0.01 <0.01 <0.01
 TB <0.01 <0.01 0.53 <0.01 <0.01
 Age × TB 0.04 0.92 0.23 0.11 <0.01
Open in a new tab
a,b

Means with different superscripts within a column differ significantly (P ≤ 0.05).

1

Each mean represents 3 eggs/replicate, 10 replicates/treatment.

Abbreviations: SEM, standard error of the mean; TB, theabrownins (0 or 100 mg/kg feed), AGE (47-wk-old or 67-wk-old).

Serum Reproductive Hormone

As indicated in Table 9, a decrease in the serum concentration of Prog, MT, FSH, E2 were observed in 67-wk-old hens compared to 47-wk-old hens (P(AGE) < 0.05). Dietary supplementation with TB significantly increased the serum concentration of Prog, MT, FSH, E2, and LH (P(TB) < 0.05), while the increase in serum concentration of Prog, MT, AMH were more emphasized when hens received TB supplemented diet under 67-wk-old (P(Interaction) < 0.05).

Table 9.

Effect of theabrownins on serum hormone of laying hens with different ages.1

Item Prog, ng/mL MT, ng/L FSH, mIU/mL E2, ng/L LH, mIU/mL AMH, ng/L
Age TB
47 wk 0 54.34b 4,514.70a 60.38 244.54 48.35 2,242.44a
47 wk 100 64.15a 4,503.19a 73.34 255.63 59.60 2,185.40ab
67 wk 0 31.86c 3,582.21c 53.00 203.09 43.01 2,163.56b
67 wk 100 57.52ab 4,189.11b 57.14 253.01 57.66 2,210.02ab
SEM 2.92 20.39 3.36 9.76 2.72 23.92
Main effect
Age
 47-wk-old 59.24 4,508.95 66.86 250.08 53.98 2,213.92
 67-wk-old 44.69 3,885.66 55.07 228.05 50.34 2,186.79
TB, mg/kg
 0 43.10 4,048.46 56.69 223.82 45.68 2,203.00
 100 60.84 4,346.15 65.24 254.32 58.63 2,197.71
SEM 2.07 14.42 2.38 6.90 1.92 16.91
P-value
 Age <0.01 <0.01 <0.01 0.03 0.19 0.27
 TB <0.01 <0.01 0.02 <0.01 <0.01 0.83
 Age × TB 0.01 <0.01 0.20 0.06 0.54 0.04
Open in a new tab
a,b

Means with different superscripts within a column differ significantly (P ≤ 0.05).

1

Each mean represents 1 layer/replicate, 10 replicates/treatment.

Abbreviations: AMH, anti-Müllerian hormone; FSH, follicle-stimulating hormone; E2, estradiol; MT, melatonin; LH, luteinizing hormon; Prog, progesterone ; SEM, standard error of the mean e; TB, theabrownins (0 or 100 mg/kg feed), AGE (47-wk-old or 67-wk-old).

Ovarian Antioxidant Capacities

As shown in Figure 1, the concentration of GSH and the activity of GST was significantly decreased in 67-wk-old layers (P(AGE) < 0.05). After feeding TB, the content of GSH, enzyme activity of GSH-Px and GST were increased, while the content of MDA was decreased (P(TB) < 0.05). While the increase in concentration of GSH and the decrease in concentration of MDA were more pronounced when hens received TB supplemented diet under 67-wk-old (P(Interaction) ≤ 0.05).

Figure 1.

Figure 1

Open in a new tab

Effect of theabrownins on antioxidant capacity in ovary of laying hens with different ages. Abbreviations: GSH-Px, glutathione peroxidase; GST, glutathione S-transferase; GSH, glutathione; MDA, malondialdehyde; TB, theabrownins (0 or 100 mg/kg feed), AGE (47-wk-old or 67-wk-old). a,b means with different superscript within a bar differ significantly (P ≤ 0.05).

Ovarian Antioxidant Related Gene Expression

As shown in Figure 2, a decrease in the relative mRNA expression of ovarian HO-1 was observed in 67-wk-old hens group compared to the younger hens (P(AGE) < 0.01). Compared with the control, dietary supplementation with TB increased mRNA expression of HO-1, Nrf2, and NQO1 (P(TB) < 0.01).

Figure 2.

Figure 2

Open in a new tab

Effect of dietary theabrownins supplementation on antioxidant related gene mRNA expression in ovary. Abbreviation: HO-1, heme oxygenase 1; Nrf2, nuclear factor E2 related factor 2; NQO1, quinone oxidoreductase 1; TB, theabrownins (0 or 100 mg/kg feed), AGE (47-wk-old or 67-wk-old).

Ovarian Reproductive Receptor Gene Expression

As indicated in Figure 3, a decrease in the relative mRNA expression of ovarian StAR1 was observed in 67-wk-old hens group compared to the younger ones (P(AGE) < 0.01). While the effect of TB was found to increase reproductive receptor mRNA expression, including StAR1 and ESR1 compared with the control (P(TB) ≤ 0.05)

Figure 3.

Figure 3

Open in a new tab

Effect of dietary theabrownins supplementation on reproduction related hormone receptor mRNA gene expression in ovary. Abbreviations: AR, androgen receptor, ESR1, estrogen receptor 1, StAR1, steroidogenic acute regulatory protein 1; TB, theabrownin (0 or 100 mg/kg feed), AGE (47-wk-old or 67-wk-old).

DISCUSSION

Studies have shown that physiological aging will have a negative effect on the reproduction function and production performance of laying hens (Iqbal et al., 2020; Wang et al., 2021b). In our study, we observed that laying rate, egg production, and feed conversion rate of laying hens decreased with increasing age. This is consistent with the results of previous studies on laying hens.(Joyner et al., 1987; Silversides and Scott, 2001; Rizzi and Chiericato, 2005). Wang et al. (2019) show that ovomucin plays a major role in maintaining the natural viscoelasticity of proteins, and the ovomucin content in eggs decreases with the increase of storage time. This is closely related to the n-glycosylation of ovomucin during egg storage (Offengenden et al., 2011). In addition, protein height and Haugh unit decreased in older laying hens (Silversides and Scott, 2001; Silversides and Budgell, 2004), which may be related to the decrease of lecithin content with increasing age of laying hens (Tůmová and Gous, 2012). The decreased level of calcium ions in laying hens will directly affect the eggshell quality (Pongmanee et al., 2020; Wang et al., 2021a), and the eggshell strength and thickness of eggshell in aged laying hens are lower, which may be due to the decreased absorption and utilization of calcium in aged laying hens, thus inhibiting ion transfer and the formation of the inner uterine shell membrane, leading to the degradation of eggshell structure and performance (Rodriguez-Navarro et al., 2002; Gu et al., 2021).

A number of studies have shown that adding tea and its extract to the diet can improve the performance of laying hens (Xia et al., 2018; Zhu et al., 2020; Ding et al., 2022a). We found that the laying rate and feed conversion rate of hens increased significantly by adding 100 mg/kg TB to the diet, and the improvement of production performance of layers in the aged group was more obvious, which indicated that feeding TB could alleviate the decrease in production performance caused by increasing age, and it was similar to the results of Feng et al. (2017), they found that resveratrol could improve the feed efficiency of laying hens in the later stage of laying. Yuan et al. (2016) found that tea polyphenols could alleviate the decrease of protein height and Haugh unit induced by vanadium. This is consistent with Wang's report that tea polyphenols improved the protein quality of Hy-Line Brown laying hens at the later stage of laying (Wang et al., 2018). Ding et al. (2022a) found that adding resveratrol to diet could improve the decline of protein quality and eggshell quality caused by oxidative stress induced by tert-butyl hydrogen peroxide (tBHP). In these studies, we found that the feeding effects of tea polyphenols and resveratrol were better under the stress conditions of laying hens (late laying period, oxidative stress caused by heavy metals, and oxidative stress induced by TBHP), which provided a new idea for the better feeding effects of theabrownin on aged laying hens, but its mechanism of action needs to be further studied. In addition, our study found that TB could improve the intrinsic quality of eggs (protein height, Haugh units) and eggshell quality (eggshell strength, eggshell thickness), which may be an important reason for the significant decrease in the rate of unqualified eggs.

Aging is an inevitable decline process of physiological function, one of its main characteristics is the gradual decline of antioxidant function and formation of a variety of free radicals (Liu et al., 2020). More and more studies have shown that almost all organs in the body are vulnerable to oxidative damage, which is closely related to aging (Ben-Meir et al., 2015; Margalef et al., 2016; Okudan and Belviranli, 2016). Ovary as the main reproductive organ of laying hens, aging, and frequent ovulation accelerate the accumulation of ROS in ovarian tissue of laying hens, aggravate protein oxidation, decrease the number of free sulfhydryl groups, and cause oxidative damage (Sena and Chandel, 2012; Lim et al., 2015). In this study, it was found that the GSH content and GST activity in ovarian tissue decreased significantly as the age increase. Nrf2, HO-1 and NQO1 are genes closely related to the antioxidant capacity of tissues. Nrf2 is a key factor involved in the regulation of oxidative stress, the expression of HO-1 gene and the biosynthesis of GSH are regulated by Nrf2 (Townsend et al., 2003; Kobayashi et al., 2004; Qiang, 2013). NQO1 protects endogenous antioxidants by maintaining reduced forms of panquinone and α-tocopherol quinone, thereby reducing cellular oxidative damage (Oppermann, 2007; Salehabadi et al., 2022). Studies have shown that Nrf2 is the central controlling factor of NQO1 expression under normal homeostasis and oxidative stress (Jung and Kwak, 2010). The activation of Nrf2/HO-1 pathway can relieve the oxidative stress of cells, which is a protective mechanism of the organism (Dai et al., 2015). In the report of Liu et al. (2018c), it was found that the activity of Nrf2/HO-1 pathway decreased with the increase of age in laying hens. These hormones regulate the growth, development and maturation of follicles mainly through the hypothalamus-pituitary-ovary axis (Proudman and Siopes, 2006). In laying hen production, the decrease of the number of follicles and the increase of follicular atresia rate will lead to the decrease of laying rate (Hubbard et al., 2012). In addition to the decrease of antioxidant ability, ovarian aging is also accompanied by changes in the secretion of reproductive hormones, which are closely related to the production performance of laying hens. Moreover, the ability to secrete hormones and the response to pituitary hormones are also important manifestations of ovarian function. Ciccone et al. (2005) found that the plasma concentrations of LH and FSH in 60-wk-old laying hens were lower than those in 30-wk-old laying hens. This is consistent with the results of this study, the level of plasma Prog, MT, FSH, E2 decreased significantly with the increase of age, which further revealed the reason why the laying rate decreased with age.

The extract of Pu'er tea has antioxidant effect (Yang et al., 2022). Theabrownin, as the main active ingredient in Pu'er tea, also has antioxidant effect (Xie et al., 2012; Lei et al., 2022). In our study, we found that feeding 100 mg/kg TB could increase the content of GSH, the activities of GSH-Px and GST, and decrease the content of MDA in ovary, indicating that TB can improve the antioxidant capacity of layers' ovaries and alleviate ovarian oxidative stress. Nrf2 is a key target for a variety of plant polyphenols to play an antioxidant role. Kim et al. (2018) found that resveratrol can prevent oxidative stress by activating Nrf2 and sirt1 signal transduction. Green tea polyphenols can effectively alleviate the imbalance of Nrf2 and its downstream target gene expression induced by D-Gal in mouse liver (Wang et al., 2022). Li et al. (2021) also found that after treatment with theaflavins, the Nrf2-NQO1/HO-1 signal pathway in the liver of mice with renal Imax R injury was activated and the antioxidant capacity was significantly enhanced. In addition, in this study, TB, which is also plant polyphenols, significantly upregulated the expression levels of Nrf2 and HO-1 mRNA in laying hens' ovaries. Therefore, we speculated that TB can improve the antioxidant status of layers' ovaries through Nrf2/HO-1 signal pathway, thus improving ovarian function. In addition, it was also found that dietary supplementation of 100 mg/kg TB could significantly increase the level of plasma Prog, MT, FSH, E2, LH. MT is an antiaging agent that can alleviate the oxidative damage of cells. Tamura et al. (2017) have found that melatonin treatment can significantly delay the aging process of mouse ovary. At the same time, some scholars found in human follicles cultured in vitro that the higher the concentration of E2, the better the quality of follicles and the higher the embryo score (Wolff et al., 2021). Whether TB could improve the follicular development of aging layers by increasing the concentration of MT and E2 remains to be further studied. In our current study, we found that dietary TB significantly upregulated the expression of StAR1, ESR1 mRNA. Steroid hormone synthesis acute regulatory protein (StAR) plays a key role in the process of steroid synthesis. Some studies have found that overexpression of StAR can improve insulin resistance and systemic inflammatory response in obese mice (Qiu et al., 2017). Therefore, we speculated that TB may upregulate the expression of StAR in the ovary of laying hens to alleviate the inflammatory response caused by ovarian senescence and promote the secretion of ovarian steroid hormones, so as to ensure the normal development of follicles. It is well known that estrogen regulates female reproduction through the estrogen receptor (ER) in the ovary. The decreased expression of estrogen receptor is closely related to the decrease of the ability of liver to synthesize yolk precursor during the aging process of laying hens (Liu et al., 2018b). It is suggested that TB may improve ovarian reproductive function and egg quality by stimulating ovarian estrogen secretion and acting on estrogen receptor, but there is no study similar to the results of this experiment. Further studies were necessary to research on the mechanism within the aging in ovarian function in order to extend the productivity cycle of laying hens.

CONCLUSIONS

In summary, production performance and egg quality declined when layers became old, while the theabrownins (100 mg/kg) improved the egg production rate, egg quality, and ovarian function (antioxidant capacity), and this improving effect were more pronounced when layers were at older age. These findings indicated that theabrownins could alleviate the negative effects of aging.

ACKNOWLEDGMENTS

Research was funded by grants from the National Key Research and Development Program of China (Grant No. 2021YFD1300204, 2022YFD1301200), National Natural Science Foundation of China (Grant No. 31872792), and Sichuan Provincial Science and Technology Projects (Grant No. 2022YFH0070). This study was also partially supported by the 111 Project too.

DISCLOSURES

No conflict of interest exits in the submission of this manuscript, and manuscript is approved by all authors for publication. I would like to declare on behalf of my co-authors that the work described was original research that has not been published previously, and not under consideration for publication elsewhere, in whole or in part. All the authors listed have been approved the manuscript that is enclosed.

Footnotes

Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.psj.2023.102545.

Appendix. Supplementary materials

mmc1.docx (20.7KB, docx)

REFERENCES

  1. Ben-Meir A., Burstein E., Borrego-Alvarez A., Chong J., Wong E., Yavorska T., Naranian T., Chi M., Wang Y., Bentov Y., Alexis J., Meriano J., Sung H.K., Gasser D.L., Moley K.H., Hekimi S., Casper R.F., Jurisicova A. Coenzyme Q10 restores oocyte mitochondrial function and fertility during reproductive aging. Aging Cell. 2015;14:887–895. doi: 10.1111/acel.12368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ciccone N.A., Sharp P.J., Wilson P.W., Dunn I.C. Changes in reproductive neuroendocrine mRNAs with decreasing ovarian function in ageing hens. Gen. Comp. Endocrinol. 2005;144:20–27. doi: 10.1016/j.ygcen.2005.04.009. [DOI] [PubMed] [Google Scholar]
  3. Dai C., Tang S., Deng S., Zhang S., Zhou Y., Velkov T., Li J., Xiao X. Lycopene attenuates colistin-induced nephrotoxicity in mice via activation of the Nrf2/HO-1 pathway. Antimicrob. Agents Chemother. 2015;59:579–585. doi: 10.1128/AAC.03925-14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ding X., Cai C., Jia R., Bai S., Zeng Q., Mao X., Xu S., Zhang K., Wang J. Dietary resveratrol improved production performance, egg quality, and intestinal health of laying hens under oxidative stress. Poult. Sci. 2022;101 doi: 10.1016/j.psj.2022.101886. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ding X., Han C., Hu W., Fu C., Zhou Y., Wang Z., Xu Q., Lv R., He C., Zuo Z., Huang J. Acute and subacute safety evaluation of black tea extract (herbt tea essences) in mice. Toxics. 2022;10:286. doi: 10.3390/toxics10060286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Feng Z.H., Gong J.G., Zhao G.X., Lin X., Liu Y.C., Ma K.W. Effects of dietary supplementation of resveratrol on performance, egg quality, yolk cholesterol and antioxidant enzyme activity of laying hens. Br. Poult. Sci. 2017;58:544–549. doi: 10.1080/00071668.2017.1349295. [DOI] [PubMed] [Google Scholar]
  7. Gong J., Peng C., Chen T., Gao B., Zhou H. Effects of theabrownin from Pu-erh tea on the metabolism of serum lipids in rats: mechanism of action. J. Food Sci. 2010;75:H182–H189. doi: 10.1111/j.1750-3841.2010.01675.x. [DOI] [PubMed] [Google Scholar]
  8. Gu Y.F., Chen Y.P., Jin R., Wang C., Wen C., Zhou Y.M. A comparison of intestinal integrity, digestive function, and egg quality in laying hens with different ages. Poult. Sci. 2021;100 doi: 10.1016/j.psj.2020.12.046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hao E.Y., Wang D.H., Chen Y.F., Zhou R.Y., Chen H., Huang R.L. The relationship between the mTOR signaling pathway and ovarian aging in peak-phase and late-phase laying hens. Poult. Sci. 2021;100:334–347. doi: 10.1016/j.psj.2020.10.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Huang F., Zheng X., Ma X., Jiang R., Zhou W., Zhou S., Zhang Y., Lei S., Wang S., Kuang J., Han X., Wei M., You Y., Li M., Li Y., Liang D., Liu J., Chen T., Yan C., Wei R., Rajani C., Shen C., Xie G., Bian Z., Li H., Zhao A., Jia W. Theabrownin from Pu-erh tea attenuates hypercholesterolemia via modulation of gut microbiota and bile acid metabolism. Nat. Commun. 2019;10:4971. doi: 10.1038/s41467-019-12896-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hubbard V.M., Valdor R., Macian F., Cuervo A.M. Selective autophagy in the maintenance of cellular homeostasis in aging organisms. Biogerontology. 2012;13:21–35. doi: 10.1007/s10522-011-9331-x. [DOI] [PubMed] [Google Scholar]
  12. Iqbal Z., Drake K., Swick R.A., Taylor P.S., Perez-Maldonado R.A., Ruhnke I. Effect of pecking stones and age on feather cover, hen mortality, and performance in free-range laying hens. Poult. Sci. 2020;99:2307–2314. doi: 10.1016/j.psj.2019.11.068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jin W., Zhou L., Yan B., Yan L., Liu F., Tong P., Yu W., Dong X., Xie L., Zhang J., Xu Y., Li C., Yuan Q., Shan L., Efferth T. Theabrownin triggers DNA damage to suppress human osteosarcoma U2OS cells by activating p53 signalling pathway. J. Cell. Mol. Med. 2018;22:4423–4436. doi: 10.1111/jcmm.13742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Joyner C.J., Peddie M.J., Taylor T.G. The effect of age on egg production in the domestic hen. Gen. Comp. Endocrinol. 1987;65:331–336. doi: 10.1016/0016-6480(87)90117-1. [DOI] [PubMed] [Google Scholar]
  15. Jung K.A., Kwak M.K. The Nrf2 system as a potential target for the development of indirect antioxidants. Molecules. 2010;15:7266–7291. doi: 10.3390/molecules15107266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kim E.N., Lim J.H., Kim M.Y., Ban T.H., Jang I.A., Yoon H.E., Park C.W., Chang Y.S., Choi B.S. Resveratrol, an Nrf2 activator, ameliorates aging-related progressive renal injury. Aging. 2018;10:83–99. doi: 10.18632/aging.101361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kobayashi A., Ohta T., Yamamoto M. Unique function of the Nrf2-Keap1 pathway in the inducible expression of antioxidant and detoxifying enzymes. Methods Enzymol. 2004;378:273–286. doi: 10.1016/S0076-6879(04)78021-0. [DOI] [PubMed] [Google Scholar]
  18. Kuang J., Zheng X., Huang F., Wang S., Li M., Zhao M., Sang C., Ge K., Li Y., Li J., Rajani C., Ma X., Zhou S., Zhao A., Jia W. Anti-adipogenic effect of theabrownin is mediated by bile acid alternative synthesis via gut microbiota remodeling. Metabolites. 2020;10:475. doi: 10.3390/metabo10110475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lei S., Zhang Z., Xie G., Zhao C., Miao Y., Chen D., Zhang G., Liu H., Peng C., Hou Y., Gong J. Theabrownin modulates the gut microbiome and serum metabolome in aging mice induced by D-galactose. J. Funct. Food. 2022;89 [Google Scholar]
  20. Li Z., Zhu J., Wan Z., Li G., Chen L., Guo Y. Theaflavin ameliorates renal ischemia/reperfusion injury by activating the Nrf2 signalling pathway in vivo and in vitro. Biomed. Pharmacother. 2021;134 doi: 10.1016/j.biopha.2020.111097. [DOI] [PubMed] [Google Scholar]
  21. Liang Y., Zhang L., Lu J. A study on chemical estimation of pu-erh tea quality. J. Sci. Food Agric. 2005;85:381–390. [Google Scholar]
  22. Lim J., Nakamura B.N., Mohar I., Kavanagh T.J., Luderer U. Glutamate cysteine ligase modifier subunit (gclm) null mice have increased ovarian oxidative stress and accelerated age-related ovarian failure. Endocrinology. 2015;156:3329–3343. doi: 10.1210/en.2015-1206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Liu R., Fu Z., Zhang F., Mao Q., Luan C., Han X., Xue J., Wang D., Qin S., Hao F. Effect of yellow rice wine on anti-aging ability in aged mice induced by d-galactose. Food Sci. Hum. Wellness. 2020;9:184–191. [Google Scholar]
  24. Liu X.T., Lin X., Mi Y.L., Zeng W.D., Zhang C.Q. Age-related changes of yolk precursor formation in the liver of laying hens. J. Zhejiang Univ. Sci. B. 2018;19:390–399. doi: 10.1631/jzus.B1700054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Liu X., Lin X., Zhang S., Guo C., Li J., Mi Y., Zhang C. Lycopene ameliorates oxidative stress in the aging chicken ovary via activation of Nrf2/HO-1 pathway. Aging. 2018;10:2016–2036. doi: 10.18632/aging.101526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Liu T., Xiang Z., Chen F., Yin D., Huang Y., Xu J., Hu L., Xu H., Wang X., Sheng J. Theabrownin suppresses in vitro osteoclastogenesis and prevents bone loss in ovariectomized rats. Biomed. Pharmacother. 2018;106:1339–1347. doi: 10.1016/j.biopha.2018.07.103. [DOI] [PubMed] [Google Scholar]
  27. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-Delta Delta C(T) method. Method. 2001;25:402–408. doi: 10.1006/meth.2001.1262. [DOI] [PubMed] [Google Scholar]
  28. Margalef M., Iglesias-Carres L., Pons Z., Bravo F.I., Muguerza B., Arola-Arnal A. Age related differences in the plasma kinetics of flavanols in rats. J. Nutr. Biochem. 2016;29:90–96. doi: 10.1016/j.jnutbio.2015.11.007. [DOI] [PubMed] [Google Scholar]
  29. Offengenden M., Fentabil M.A., Wu J. N-glycosylation of ovomucin from hen egg white. Glycoconj. J. 2011;28:113–123. doi: 10.1007/s10719-011-9328-3. [DOI] [PubMed] [Google Scholar]
  30. Okudan N., Belviranli M. Effects of exercise training on hepatic oxidative stress and antioxidant status in aged rats. Arch. Physiol. Biochem. 2016;122:180–185. doi: 10.1080/13813455.2016.1199574. [DOI] [PubMed] [Google Scholar]
  31. Oppermann U. Carbonyl reductases: the complex relationships of mammalian carbonyl- and quinone-reducing enzymes and their role in physiology. Annu. Rev. Pharmacol. Toxicol. 2007;47:293–322. doi: 10.1146/annurev.pharmtox.47.120505.105316. [DOI] [PubMed] [Google Scholar]
  32. Pan L., Gong W., Zhou Y., Li X., Yu J., Hu S. A comprehensive transcriptomic analysis of infant and adult mouse ovary. Genomics Proteomics Bioinform. 2014;12:239–248. doi: 10.1016/j.gpb.2014.08.002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pongmanee K., Kuhn I., Korver D.R. Effects of phytase supplementation on eggshell and bone quality, and phosphorus and calcium digestibility in laying hens from 25 to 37 wk of age. Poult. Sci. 2020;99:2595–2607. doi: 10.1016/j.psj.2019.12.051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Proudman J.A., Siopes T.D. Potential role of thyroid hormones and prolactin in the programming of photorefractoriness in turkey hens. Poult. Sci. 2006;85:1457–1461. doi: 10.1093/ps/85.8.1457. [DOI] [PubMed] [Google Scholar]
  35. Qiang M. Role of Nrf2 in Oxidative Stress and Toxicity. Annu. Rev. Pharmacol. Toxicol. 2013;53:401–426. doi: 10.1146/annurev-pharmtox-011112-140320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Qiu Y., Sui X., Cao S., Li X., Ning Y., Wang S., Yin L., Zhi X. Steroidogenic acute regulatory protein (StAR) overexpression reduces inflammation and insulin resistance in obese mice. J. Cell. Biochem. 2017;118:3932–3942. doi: 10.1002/jcb.26046. [DOI] [PubMed] [Google Scholar]
  37. Rizzi C.P.U.I., Chiericato G.M.P.U. Organic farming production. Effect of age on the productive yield and egg quality of hens of two commercial hybrid lines and two local breeds. Ital. J. Anim. Sci. 2005;4:160–162. [Google Scholar]
  38. Rodriguez-Navarro A., Kalin O., Nys Y., Garcia-Ruiz J.M. Influence of the microstructure on the shell strength of eggs laid by hens of different ages. Br. Poult. Sci. 2002;43:395–403. doi: 10.1080/00071660120103675. [DOI] [PubMed] [Google Scholar]
  39. Rojas F.J. Ovulation induction. Effects of ovulation induction with gonadotrophins on the ovary and uterus and their implications for assisted reproduction. Hum. Reprod. 1995;10:2219–2224. doi: 10.1093/oxfordjournals.humrep.a136271. [DOI] [PubMed] [Google Scholar]
  40. Salehabadi A., Farkhondeh T., Harifi-Mood M.S., Aschner M., Samarghandian S. Role of Nrf2 in bisphenol effects: a review study. Environ. Sci. Pollut. Res. 2022;29:55457–55472. doi: 10.1007/s11356-022-20996-3. [DOI] [PubMed] [Google Scholar]
  41. Sena L.A., Chandel N.S. Physiological roles of mitochondrial reactive oxygen species. Mol. Cell. 2012;48:158–167. doi: 10.1016/j.molcel.2012.09.025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Silversides F.G., Budgell K. The relationships among measures of egg albumen height, pH, and whipping volume. Poult. Sci. 2004;83:1619–1623. doi: 10.1093/ps/83.10.1619. [DOI] [PubMed] [Google Scholar]
  43. Silversides F.G., Scott T.A. Effect of storage and layer age on quality of eggs from two lines of hens. Poult. Sci. 2001;80:1240–1245. doi: 10.1093/ps/80.8.1240. [DOI] [PubMed] [Google Scholar]
  44. Tamura H., Kawamoto M., Sato S., Tamura I., Maekawa R., Taketani T., Aasada H., Takaki E., Nakai A., Reiter R.J., Sugino N., Long-term melatonin treatment delays ovarian aging [e-pub ahead of print], J. Pineal. Res., 62, 2017, doi: 10.1111/jpi.12381, accessed March 27, 2023. [DOI] [PubMed]
  45. Townsend D.M., Tew K.D., Tapiero H. The importance of glutathione in human disease. Biomed. Pharmacother. 2003;57:145–155. doi: 10.1016/s0753-3322(03)00043-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Tůmová E., Gous R.M. Interaction of hen production type, age, and temperature on laying pattern and egg quality. Poult. Sci. 2012;91:1269–1275. doi: 10.3382/ps.2011-01951. [DOI] [PubMed] [Google Scholar]
  47. Wang Y., Jin T., Zhang N., Li J., Wang Y., Kulyar M.F., Han Z., Li Y. Effect of stocking density and age on physiological performance and dynamic gut bacterial and fungal communities in Langya hens. Microb. Cell. Fact. 2021;20:218. doi: 10.1186/s12934-021-01707-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wang D., Wang T., Li Z., Guo Y., Granato D. Green Tea polyphenols upregulate the Nrf2 signaling pathway and suppress oxidative stress and inflammation markers in d-galactose-induced liver aging in mice. Front. Nutr. 2022;9 doi: 10.3389/fnut.2022.836112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Wang J., Wang W., Qi G., Cui C., Wu S., Zhang H., Xu L., Wang J. Effects of dietary Bacillus subtilis supplementation and calcium levels on performance and eggshell quality of laying hens in the late phase of production. Poult. Sci. 2021;100 doi: 10.1016/j.psj.2020.12.067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Wang Y., Wang Z., Shan Y. Assessment of the relationship between ovomucin and albumen quality of shell eggs during storage. Poult. Sci. 2019;98:473–479. doi: 10.3382/ps/pey349. [DOI] [PubMed] [Google Scholar]
  51. Wang X.C., Wang X.H., Wang J., Wang H., Zhang H.J., Wu S.G., Qi G.H. Dietary tea polyphenol supplementation improved egg production performance, albumen quality, and magnum morphology of Hy-Line Brown hens during the late laying period. J. Anim. Sci. 2018;96:225–235. doi: 10.1093/jas/skx007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Wolff M.V., Mitter V.R., Jamir N., Stute P., Bersinger N.A. The endocrine milieu in naturally matured follicles is different in women with high serum anti-Müllerian hormone concentrations. Reprod. Biomed. Online. 2021;43:329–337. doi: 10.1016/j.rbmo.2021.01.021. [DOI] [PubMed] [Google Scholar]
  53. Xia B., Liu Y., Sun D., Liu J., Zhu Y., Lu L. Effects of green tea powder supplementation on egg production and egg quality in laying hens. J. Appl. Anim. Res. 2018;46:927–931. [Google Scholar]
  54. Xie G., Zhao A., Zhao L., Chen T., Chen H., Qi X., Zheng X., Ni Y., Cheng Y., Lan K., Yao C., Qiu M., Jia W. Metabolic fate of tea polyphenols in humans. J. Proteome Res. 2012;11:3449–3457. doi: 10.1021/pr300318m. [DOI] [PubMed] [Google Scholar]
  55. Yang C.Y., Hung K.C., Yen Y.Y., Liao H.E., Lan S.J., Lin H.C. Anti-oxidative effect of pu-erh tea in animals trails: a systematic review and meta-analysis. Foods. 2022;11:1333. doi: 10.3390/foods11091333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Yao J., Ma Y., Zhou S., Bao T., Mi Y., Zeng W., Li J., Zhang C. Metformin prevents follicular atresia in aging laying chickens through activation of PI3K/AKT and calcium signaling pathways. Oxid. Med. Cell. Longev. 2020;2020 doi: 10.1155/2020/3648040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Yuan Z.H., Zhang K.Y., Ding X.M., Luo Y.H., Bai S.P., Zeng Q.F., Wang J.P. Effect of tea polyphenols on production performance, egg quality, and hepatic antioxidant status of laying hens in vanadium-containing diets. Poult. Sci. 2016;95:1709–1717. doi: 10.3382/ps/pew097. [DOI] [PubMed] [Google Scholar]
  58. Yue S., Zhao D., Peng C., Tan C., Wang Q., Gong J. Effects of theabrownin on serum metabolites and gut microbiome in rats with a high-sugar diet. Food Funct. 2019;10:7063–7080. doi: 10.1039/c9fo01334b. [DOI] [PubMed] [Google Scholar]
  59. Zhou L., Ding X., Wang J., Bai S., Zeng Q., Su Z., Xuan Y., Wu A., Zhang K. Oxidized oils and oxidized proteins induce apoptosis in granulosa cells by increasing oxidative stress in ovaries of laying hens. Oxid. Med. Cell. Longev. 2020;2020 doi: 10.1155/2020/2685310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Zhou S., Zhao A., Wu Y., Mi Y., Zhang C. Protective effect of grape seed proanthocyanidins on oxidative damage of chicken follicular granulosa cells by inhibiting foxo1-mediated autophagy. Front. Cell. Dev. Biol. 2022;10 doi: 10.3389/fcell.2022.762228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Zhu Y.F., Wang J.P., Ding X.M., Bai S.P., Qi S.R.N., Zeng Q.F., Xuan Y., Su Z.W., Zhang K.Y. Effect of different tea polyphenol products on egg production performance, egg quality and antioxidative status of laying hens. Anim. Feed Sci. Technol. 2020;267 [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

mmc1.docx (20.7KB, docx)

Articles from Poultry Science are provided here courtesy of Elsevier

RESOURCES