| Livestock Research for Rural Development 35 (12) 2023 | LRRD Search | LRRD Misssion | Guide for preparation of papers | LRRD Newsletter | Citation of this paper |
Turmeric powder (TP) has been extensively used as a feed additive alternative for antibiotic growth promoters. Turmeric's bioactive components not only enhance laying hen performance but also the quality of laying hen eggs. The objectives of this meta-analysis were to assess the effectiveness of supplementation with turmeric powder on egg weight (EW), haugh unit (HU), eggshell thickness (EST), yolk color (YC) and yolk cholesterol level (YCL) of laying hen eggs. Peer-reviewed randomized controlled trials (RCTs) published in English were found using databases such as PubMed, Scopus, Science Direct and Google Scholar. The meta-analysis required information on moderators (breed of hens, age of the hen at the start of the intervention, inclusion level and turmeric powder treatment duration), a sufficient description of randomization, performance data and associated measures of variance such as standard deviation (SD) or standard error (SE). All analyses were carried out using the Open Meta-analyst for Ecology and Evolution (OpenMEE) program. Data from the 17 studies included in the meta-analysis were pooled and presented as standardized mean differences (SMDs) at a 95% confidence interval (CI) using a random-effects model. Results indicate that dietary TP supplementation improves HU (SMD = 0.88; 95% CI: 0.30 to 1.47), EST (SMD = 0.62 mm ; 95% CI: 0.13 to 1.11), YC (SMD = 2.06; 95% CI: 1.32 to 2.80) and YCL (SMD = -1.19; 95% CI: -2.23 to -0.15) compared with the controls. Restricted subgroup analysis indicated that brown laying hen showed the beneficial effect of dietary turmeric powder. Subgroup analysis found that studies that used TP in <11 g/kg had significant egg quality. The meta-analysis explains that turmeric powder is an ingredient that could be used as a feed additive in laying hens to increase egg quality.
Keywords: commercial laying hens, egg quality, feed additives, meta-analysis, turmeric powder
Several years ago, antibiotics were commonly used as feed additives in poultry diets to prevent diseases and maximize chicken production, with the aim of improving feed utilization and reducing mortality caused by pathogens (Muaz et al 2018). All commonly used feed antibiotic-growth promoters have been banned and not used in feeds in certain countries due to increased concerns about the potential for antibiotic-resistant strains of bacteria and residues of antibiotics in animal tissues (Denlİ and Demİrel 2018). Increasing concerns about the negative impact of AGPs have led to research on the use of natural feed additives in poultry feed to ascertain better performance and safety in the food chain (Mohamed and Hassan 2023).
Curcuma longa L. is a rhizomatous herbaceous perennial plant belonging to the Zingiberaceae family (Wang and Yu 2015). It is native to countries in southern Asia as well as China, Bangladesh and Java (Košťálová et al 2013). The rhizomes of the plant are the most relevant part and are harvested for various products (Patra et al 2018). Turmeric a widely used spice and medicinal plant, contains several bioactive compounds that exhibit antimicrobial, anti-inflammatory and antioxidant properties (Sharifi-Rad et al 2020). Curcuminoids are naturally occurring major content of turmeric, consisting of curcumin, demethoxycurcumin and bisdemethoxycurcumin (Tayyem et al 2006).
Recent research reports have suggested the efficacy of turmeric in poultry feed in order to replace antibiotic use (Hanif et al 2023). Supplementation with turmeric in the diet can have beneficial effects on health status, growth and production in poultry (Gouda and Prabhakar Bhandary 2018). Moreover, dietary turmeric powder can improve egg quality (Mosayyeb Zadeh et al 2022). In addition, turmeric is one supplement that can modulate the lipid profile and cholesterol content (Zava et al 1998). The hypocholesterolemic effect of turmeric is due to curcumin content. Curcumin was effective in reducing both liver and serum cholesterol levels (Rao et al 1970).
Several studies have shown that supplementing the laying hen diet with turmeric powder can improve egg quality but some of them have no effect (Dalal et al 2018). The results of studies conducted in different locations and under different conditions may produce varying results, leading to ambiguous and unclear conclusions. Meta-analysis is a sophisticated statistical method for combining the findings of independent studies to identify patterns, address uncertainties, identify knowledge gaps and generate new insights (Ogbuewu and Mbajiorgu 2022). There is currently no information on the effect of dietary turmeric powder on the egg quality of laying hens. Thus, this study aims to determine the effect of feed with or without turmeric powder supplementation on egg quality characteristics. Will be determined through subgroup and meta-regression stratification analyses.
Empirical studies reporting the use of turmeric powder in the diets of laying hens published in peer-reviewed journals were compiled from the online database of Scopus (www.scopus.com), PubMed Central (www.ncbi.nlm.nih.gov/pmc/) and google scholar (https://scholar.google.com/). The literature was searched by using two keywords "turmeric powder" and "egg quality" as queries in the online platform without being restricted by publication year. The output of each platform's articles was imported into a reference manager for selection reasons, in accordance with the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) criteria (Liberati et al 2009). papers in duplicate and review or non-research papers were first omitted from the database. In addition, inclusion criteria were created to evaluate the quality of the publications referencing a prior meta-analysis (Ogbuewu et al 2021).
Articles were included in the database in the current meta-analysis if they matched the following criteria: (1) In vivo study published in an English-language peer-reviewed publication; (2) reported the use of dietary turmeric powder, hens breed, hens age, inclusion level and duration experiment as treatment; (3) reported at least one response variable (egg weight, EW; haugh unit, HU; eggshell thickness, EST; yolk color, YC; yolk cholesterol level, YCL) with the respective variance (standard deviation, SD or standard error, SE) or allowing the variable to be calculated; (4) reported hens strain used and country. Once SE was obtained, SD was computed using the equation (Higgins et al 2011), where n = number of replications. Other substances were not included in the database because they could interact with the outcome factors. Furthermore, research that used microorganisms or environmental circumstances (e.g., heat stress challenged) were excluded. The selection procedure, as shown in Figure 21, yielded 17 final publications that met the eligibility requirements and were eventually extracted for database construction.
For studies that satisfied the eligibility requirements, data on the first author's surname, publication year and research location were retrieved, as well as modifiers (layer breed/strain, age of the hen at the start of the study, inclusion level and supplementation duration). The number of layers contained in the treatment and control groups was retrieved. Treatment and control mean, as well as their corresponding measures of variance [standard error (SE) or standard deviation (SD)] for each response variable, were also retrieved. When research gave SE instead of SD, the SE was converted to SD using Higgins and Deeks' method (Higgins et al 2011): , where n is the number of laying hens in each treatment group. In a study that had multiple treatment groups, we compared each treatment group with the control group.
Each study that satisfied the inclusion criteria retrieved moderators such as layer strain, hen age at the start of the trial, inclusion level and supplementation duration that may alter the size of the response of laying hens to turmeric powder therapy. Meta-regression and limited subgroup analyses were used to examine the influence of moderators on effect sizes. In one or more of these subgroups, meta-regression and subgroup analyses were performed: chicken breed/strain (Brown and white), hen age (40 weeks and >40 weeks), supplementation duration (9 weeks and >9 weeks), inclusion level (11 and >11 g/kg feed). The inclusion level, breed of hens, age of hens and supplementation duration were classified based on the various ranges employed by the individual studies included in the current meta-analysis. Meta-regression analysis was not conducted in response variables with less than 10 studies since the test power from such analysis is usually low (Borenstein et al 2009). Heterogeneity was evaluated using Q statistics, a measure that partitions total heterogeneity into variance explained by the model and residual error not explained by the model (Egger and Smith 2001) and quantified using I2 statistics (Higgins and Thompson 2002). Evidence of publication bias was assessed through Rosenberg’s fail-safe number (Nfs) and funnel graphs (Koricheva et al 2013). The meta-analysis results were considered robust despite the possibility of publication bias if Nfs > 5 (n = number of animals in each treatment group) + 10 as stated by (Jennions et al 2013).
OpenMEE software by Brown University USA (Wallace et al 2017) was used to analyze outcome measures in laying hens by standardized mean difference (SMD), which is also called effect size analysis. Data were pooled using the random-effects model (REM) and expressed as SMD at a 95% confidence interval (CI). The choice of the REM was based on the assumptions that data included in the meta-analysis were not identical; therefore, variance must be divided into within–studies and between–studies variance plus sampling error (Borenstein et al 2009). The effects of turmeric powder treatment on outcome measures were displayed as forest plots. SMD value is said to be positive if turmeric powder treatment results to an increase in the outcome measure of interest; otherwise, the reverse is the case. The thick vertical line connotes that there is no effect or that SMD = 0. The pooled effect estimate was considered significantly different from zero if its confidence interval did not include zero (Koricheva et al 2013). The SMD values of 0.2 and 0.5 were regarded as low and medium effect sizes, respectively, while the value of 0.8 was considered as a large effect size.
|
| Figure 1. Flow charts of the articles selection process utilized for the meta-analysis |
|
Table 1. Characteristics of studies included in the meta-analysis |
||||||||
|
Study |
Reference |
Country |
Breed |
Age |
Dose |
Duration |
Variables |
|
|
1 |
(Malekizadeh et al 2012) |
Iran |
Hy-Line W-36 |
103 |
0, 10, 30 |
9 |
EW |
|
|
2 |
(Park et al 2012) |
Korea |
Lohman Brown |
60 |
0, 1.0, 2.5, 5.0 |
7 |
EW, HU, EST, YC, YCL |
|
|
3 |
(Riasi 2012) |
Iran |
Hy-Line W-36 |
100 |
0, 0.5,1.0, 1.5, 2.0 |
4 |
HU, EST, YC |
|
|
4 |
(Rahardja et al 2015) |
Indonesia |
Hisex Brown |
80 |
0, 10, 20, 40 |
12 |
EW |
|
|
5 |
(Hassan 2016) |
Saudi Arabia |
Hisex White |
52 |
0, 20, 40 |
8 |
EW, HU, YC |
|
|
6 |
(Mirbod et al 2017) |
Iran |
Hy-Line W-36 |
37 |
0, 2.0, 4.0, 6.0 |
11 |
EW, HU, EST, YC, YCL |
|
|
7 |
(Attia 2018) |
Egypt |
Lohman White |
43 |
0, 1.5, 3.0 |
8 |
EW, YC |
|
|
8 |
(Hadj Ayed et al 2018) |
Iran |
Novogen White |
27 |
0, 5.0, 10,15,20 |
7 |
EW, YC |
|
|
9 |
(Mutlag et al 2018) |
Iraq |
Shaver White |
24 |
0, 5.0 |
16 |
EW |
|
|
10 |
(Ooi et al 2018) |
Malaysia |
Bovans Brown |
32 |
0, 10 |
4 |
EW |
|
|
11 |
(Singh et al 2019) |
India |
White Leghorn |
28 |
0, 10 |
12 |
EW, EST, YCL |
|
|
12 |
(Ayeni et al 2020) |
Nigeria |
Isa Brown |
64 |
0, 30 |
12 |
EW, HU, YC |
|
|
13 |
(Kinati et al 2021) |
Ethiopia |
White Leghorn |
26 |
0, 5.0 |
11 |
EW, HU, EST, YC |
|
|
14 |
(Kujero et al 2021) |
Nigeria |
Isa Brown |
23 |
0, 15, 30 |
37 |
EW, HU, EST, YC |
|
|
15 |
(Ait-Kaki et al 2021) |
Algeria |
Lohmann Brown |
36 |
0, 5 |
8 |
EW, HU, EST |
|
|
16 |
(Fawaz et al 2022) |
Egypt |
Bovans Brown |
55 |
0, 2.5, 5.0, 7.5 |
12 |
EW, HU, EST |
|
|
17 |
(Mosayyeb Zadeh et al 2022) |
Iran |
Hy-Line W-36 |
53 |
0, 2.5, 5.0 |
10 |
EW, HU, EST, YC, YCL |
|
| EW, egg weight; HU, haugh unit; EST, egg shell thickness; YC, yolk color; YCl, yolk cholesterol level | ||||||||
A total of 17 studies conducted in 11 countries worldwide were aggregated, mainly shown in Iran (5/11), Egypt (2/11) and Nigeria (2/11). Inclusion levels of turmeric powder varied among studies, from 0.1 g/kg diet to 40 g/kg diet. The duration of turmeric powder treatment varies from 4 to 37 weeks (Table 1). Information on the nutrient composition of brown laying hens studies is presented in Table 3 and white laying hens in Table 4 for ME (kcal/kg), CP (%), CF (%), methionine (%), lysine (%), met-cys (%), calcium (%), phosphor (%) and available phosphor (%). As indicated in Table 3 and Table 4, the nutritional specifications were appropriate to the nutrient recommendation of Rostagno et al (2017) and NRC (1994).
| Table 2. Number of studies and hens included in the meta-analysis | |||||||
|
Variables |
Number of |
Comparison |
Number of hens |
Total of number |
|||
|
control |
treatment |
||||||
|
Egg weight |
16 |
32 |
511 |
1077 |
1588 |
||
|
Haugh unit |
9 |
18 |
370 |
802 |
1172 |
||
|
Eggshell thickness |
9 |
20 |
341 |
737 |
1078 |
||
|
Yolk color |
10 |
24 |
393 |
977 |
1370 |
||
|
Yolk cholesterol level |
4 |
9 |
120 |
320 |
440 |
||
|
Total |
559 |
1229 |
1788 |
||||
|
Table 3. Descriptive statistics of nutrient specifications of the brown laying hen diets used in the meta-analysis |
||||||||
|
Nutrient |
N |
Mean |
SD |
Min |
Max |
|||
|
ME (kcal/kg) |
13 |
2753 |
163 |
2459 |
2983 |
|||
|
Crude Protein (%) |
19 |
17.1 |
0.74 |
16.1 |
18.3 |
|||
|
Crude Fiber (%) |
15 |
3.2 |
0.85 |
2.3 |
4.8 |
|||
|
Methionine (%) |
7 |
0.40 |
0.01 |
0.39 |
0.41 |
|||
|
Met-Cys (%) |
4 |
0.65 |
0.00 |
0.65 |
0.65 |
|||
|
Lysine (%) |
7 |
0.91 |
0.05 |
0.85 |
0.96 |
|||
|
Calcium (%) |
13 |
3.8 |
0.07 |
3.7 |
3.9 |
|||
|
Phosphor (%) |
4 |
0.59 |
0.00 |
0.59 |
0.59 |
|||
|
Available Phosphor (%) |
7 |
0.49 |
0.01 |
0.47 |
0.50 |
|||
|
N, number of samples; SD, standard deviation; Max, maximum; Min, minimum; ME, metabolizable energy |
||||||||
|
Table 4. Descriptive statistics of nutrient specifications of the white laying hen diets used in the meta-analysis |
||||||||
|
Nutrient |
N |
Mean |
SD |
Min |
Max |
|||
|
ME (kcal/kg) |
30 |
2731 |
45.3 |
2601 |
2815 |
|||
|
Crude Protein (%) |
27 |
16.5 |
0.91 |
15.0 |
18.3 |
|||
|
Crude Fiber (%) |
12 |
3.9 |
0.95 |
3.2 |
5.8 |
|||
|
Methionine (%) |
16 |
0.40 |
0.05 |
0.35 |
0.48 |
|||
|
Met-Cys (%) |
18 |
0.63 |
0.03 |
0.54 |
0.72 |
|||
|
Lysine (%) |
19 |
0.84 |
0.12 |
0.70 |
1.1 |
|||
|
Calcium (%) |
27 |
4.0 |
0.32 |
3.6 |
4.6 |
|||
|
Phosphor (%) |
10 |
0.65 |
0.05 |
0.61 |
0.73 |
|||
|
Available Phosphor (%) |
17 |
0.37 |
0.02 |
0.30 |
0.44 |
|||
|
N, number of samples; SD, standard deviation; Max, maximum; Min, minimum; ME, metabolizable energy |
||||||||
 |
| Figure 2. Forest plot of the effect of dietary turmeric powder on egg weight |
|
Table 5. Subgroup analysis of the effect of dietary turmeric powder on egg weight |
||||||||
|
Covariates |
N |
SMD |
CI 95% |
SE |
p- value |
Heterogeneity |
||
|
Lower |
Upper |
I2 |
p- value |
|||||
|
Overall |
32 |
0.19 |
-0.28 |
0.66 |
0.24 |
0.429 |
80.1 |
<0.001 |
|
Hens breed |
||||||||
|
Brown hens |
14 |
0.62 |
0.00 |
1.2 |
0.31 |
0.049 |
74.8 |
<0.001 |
|
White hens |
18 |
-0.20 |
-0.92 |
0.53 |
0.37 |
0.597 |
83.5 |
<0.001 |
|
Hens age |
||||||||
|
<40 week |
14 |
0.62 |
0.06 |
1.2 |
0.29 |
0.031 |
64.8 |
<0.001 |
|
>40 weeks |
18 |
-0.17 |
-0.86 |
0.53 |
0.36 |
0.355 |
84.3 |
<0.001 |
|
Inclusion rate |
||||||||
|
<11 g/kg |
22 |
0.62 |
0.07 |
1.2 |
0.28 |
0.028 |
84.7 |
<0.001 |
|
>11 g/kg |
10 |
-0.69 |
-1.5 |
0.09 |
0.40 |
0.082 |
81.6 |
<0.001 |
|
Treatment duration |
||||||||
|
<9 week |
14 |
0.10 |
-0.87 |
1.1 |
0.50 |
0.836 |
87.7 |
<0.001 |
|
>9 week |
18 |
0.27 |
-1.2 |
0.74 |
0.24 |
0.259 |
81.6 |
<0.001 |
|
SMD and I 2 were considered significant at p <0.05; N, number of comparisons; SMD, standardized mean differences between the turmeric powder and controls; CI, confidence interval; SE, standard error; p, probability value |
||||||||
Meta-analysis to evaluate the effect of TP on EW of laying hens was performed using 16 articles where the pooled mean effect estimate was 0.19 (95% CI: -0.28 to 0.66). Overall, there wasn’t an effect of dietary TP inclusion on EW. Moreover, TP treatment increased the EW of laying hens in brown laying hens (p <0.05). Restricted subgroup analysis on hens age also showed that TP increased in <40 (p <0.05). Sub-group analysis of the inclusion rate showed that <11 g/kg increased EW (p <0.05).
 |
| Figure 3. Forest plot of the effect of dietary turmeric powder on haugh unit |
|
Table 6. Subgroup analysis of the effect of dietary turmeric powder on haugh unit |
||||||||
|
Covariates |
N |
SMD |
CI 95% |
SE |
p- value |
Heterogeneity |
||
|
Lower |
Upper |
I2 |
p- value |
|||||
|
Overall |
18 |
0.88 |
0.30 |
1.5 |
0.30 |
0.003 |
78.2 |
<0.001 |
|
Hens breed |
||||||||
|
Brown hens |
10 |
1.1 |
0.10 |
2.2 |
0.53 |
0.031 |
85.2 |
<0.001 |
|
White hens |
8 |
0.64 |
0.06 |
1.2 |
0.30 |
0.031 |
56.2 |
0.025 |
|
Hens age |
||||||||
|
<40 week |
7 |
1.2 |
0.66 |
1.7 |
0.27 |
<0.001 |
14.4 |
0.320 |
|
>40 week |
11 |
0.75 |
-0.05 |
1.5 |
0.41 |
0.066 |
82.8 |
<0.001 |
|
Inclusion rate |
||||||||
|
<11 g/kg |
13 |
1.2 |
0.80 |
1.6 |
0.21 |
<0.001 |
27.0 |
0.172 |
|
>11 g/kg |
5 |
0.01 |
-1.0 |
1.0 |
0.52 |
0.988 |
82.1 |
<0.001 |
|
Treatment duration |
||||||||
|
<9 week |
8 |
0.80 |
0.19 |
1.4 |
0.31 |
0.010 |
51.7 |
0.043 |
|
>9 week |
10 |
0.89 |
-0.06 |
1.9 |
0.49 |
0.066 |
85.7 |
<0.001 |
|
SMD and I 2 were considered significant at p <0.05; N, number of comparisons; SMD, standardized mean differences between the turmeric powder and controls; CI, confidence interval; SE, standard error; p, probability value |
||||||||
Grand estimates obtained from SMD suggested that TP increased on HU of laying hens (SMD = 0.88, 95% CI: 0.30 to 1.5, p = 0.003). The increase in HU was consistent across all types of laying hens (brown and white laying hens). TP supplementation increased the HU of <40-week-old laying hens ( p <0.05). Sub-group analysis of the inclusion rate showed that <11 g/kg increased HU ( p <0.05) in low heterogeneity ( I2 = 27.0%, Q = 0.172). Duration of TP administration of <9 weeks also improves HU.
 |
| Figure 4. Forest plot of the effect of dietary turmeric powder on eggshell thickness |
|
Table 7. Subgroup analysis of the effect of dietary turmeric powder on eggshell thickness |
||||||||
|
Covariates |
N |
SMD |
CI 95% |
SE |
p- value |
Heterogeneity |
||
|
Lower |
Upper |
I2 |
p- value |
|||||
|
Overall |
20 |
0.62 |
0.13 |
1.1 |
0.25 |
0.013 |
69.9 |
< 0.001 |
|
Hens breed |
||||||||
|
Brown hens |
9 |
1.4 |
0.66 |
2.0 |
0.35 |
<0.001 |
51.5 |
0.04 |
|
White hens |
11 |
0.09 |
-0.45 |
0.63 |
0.28 |
0.746 |
65.0 |
0.001 |
|
Hens age |
||||||||
|
<40 week |
8 |
0.12 |
-0.52 |
0.77 |
0.33 |
0.705 |
0.00 |
0.54 |
|
>40 week |
12 |
0.92 |
0.14 |
1.7 |
0.40 |
0.021 |
80.5 |
<0.001 |
|
Inclusion rate |
||||||||
|
<11 g/kg |
18 |
0.68 |
0.16 |
1.2 |
0.27 |
0.010 |
71.5 |
<0.001 |
|
>11 g/kg |
2 |
0.00 |
-1.7 |
1.7 |
0.87 |
1.000 |
63.7 |
0.10 |
|
Treatment duration |
||||||||
|
<9 week |
9 |
0.57 |
-0.20 |
1.3 |
0.39 |
0.145 |
75.5 |
<0.001 |
|
>9 week |
11 |
0.67 |
-0.01 |
1.3 |
0.34 |
0.050 |
66.6 |
<0.001 |
|
SMD and I 2 were considered significant at p <0.05; N, number of comparisons; SMD, standardized mean differences between the turmeric powder and controls; CI, confidence interval; SE, standard error; p, probability value; NA, not available |
||||||||
Nine papers satisfied the inclusion criteria for the meta-analysis to evaluate the effect of supplementing with TP on EST of laying hens, according to the REM in the general SMD estimations revealed that the TP treatment increased EST (SMD = 0.62; 95% CI: 0.13 to 1.1; p= 0.013). TP increased the EST of brown laying hens ( p <0.001), while TP treatment on white laying hens had no effect. Restricted subgroup analysis on hens age also showed that TP increased EST in >40-week hens old ( p <0.05). Sub-group analysis of the inclusion rate showed that <11 g/kg increased EST ( p <0.05) in high heterogeneity (I2 = 72.7%, Q = <0.001). Moreover, TP supplementation for 9 to 12 weeks increased EST ( p <0.001) in high heterogeneity (I2 = 83.7%, Q = <0.001).
 |
| Figure 5. Forest plot of the effect of dietary turmeric powder on yolk color |
|
Table 8. Subgroup analysis of the effect of dietary turmeric powder on yolk color |
||||||||
|
Covariates |
N |
SMD |
CI 95% |
SE |
p- value |
Heterogeneity |
||
|
Lower |
Upper |
I2 |
p- value |
|||||
|
Overall |
24 |
2.1 |
1.3 |
2.8 |
0.38 |
<0.001 |
87.9 |
<0.001 |
|
Hens breed |
||||||||
|
Brown hens |
6 |
3.1 |
0.44 |
5.8 |
1.4 |
0.022 |
93.6 |
<0.001 |
|
White hens |
18 |
1.6 |
0.90 |
2.2 |
0.34 |
<0.001 |
82.4 |
<0.001 |
|
Hens age |
||||||||
|
<40 week |
10 |
1.4 |
0.64 |
2.2 |
0.41 |
<0.001 |
74.1 |
<0.001 |
|
>40 week |
14 |
2.6 |
1.5 |
3.8 |
0.59 |
<0.001 |
91.6 |
<0.001 |
|
Inclusion rate |
||||||||
|
<11 g/kg |
17 |
1.6 |
0.93 |
2.3 |
0.35 |
<0.001 |
79.7 |
<0.001 |
|
>11 g/kg |
7 |
2.8 |
0.66 |
4.9 |
1.1 |
0.010 |
94.5 |
<0.001 |
|
Treatment duration |
||||||||
|
<9 weeks |
16 |
1.4 |
0.72 |
2.1 |
0.36 |
<0.001 |
82.0 |
<0.001 |
|
>9 weeks |
8 |
3.0 |
1.2 |
4.9 |
0.94 |
0.001 |
91.7 |
<0.001 |
|
SMD and I 2 were considered significant at p <0.05; N, number of comparisons; SMD, standardized mean differences between the turmeric powder and controls; CI, confidence interval; SE, standard error; p, probability value; NA, not available |
||||||||
Assessing the effect of turmeric powder supplementation on YC in laying hen eggs, 10 articles with 24 comparisons that met the eligibility rule for inclusion in the meta-analysis were used. The Grand mean estimate revealed no evidence of treatment effect on YC (SMD = 2.1; 95% CI: 1.3 to 2.8; p <0.001). The increase in YC was consistent across all subgroups
 |
| Figure 6. Forest plot of the effect of dietary turmeric powder on yolk cholesterol level |
|
Table 9. Subgroup analysis of the effect of dietary turmeric powder on yolk cholesterol level |
||||||||
|
Covariates |
N |
SMD |
CI 95% |
SE |
p- value |
Heterogeneity |
||
|
Lower |
Upper |
I2 |
p- value |
|||||
|
Overall |
9 |
-1.2 |
-2.2 |
-0.15 |
0.53 |
0.025 |
78.2 |
<0.001 |
|
Hens breed |
||||||||
|
Brown hens |
3 |
-2.6 |
-3.7 |
-1.5 |
0.56 |
<0.001 |
19.0 |
0.29 |
|
White hens |
6 |
-0.42 |
-1.5 |
0.61 |
0.53 |
0.421 |
70.7 |
0.004 |
|
Hens age |
||||||||
|
<40 week |
5 |
-1.0 |
-2.7 |
0.71 |
0.88 |
0.250 |
56.0 |
0.10 |
|
>40 weeks |
4 |
-1.4 |
-2.9 |
0.09 |
0.75 |
0.065 |
80.9 |
<0.001 |
|
Inclusion rate |
||||||||
|
1 – 10 g/kg |
9 |
-1.2 |
-2.2 |
-0.15 |
0.53 |
0.025 |
78.2 |
<0.001 |
|
Treatment duration |
||||||||
|
<9 week |
4 |
-1.86 |
-3.6 |
-0.08 |
0.91 |
0.041 |
81.1 |
0.001 |
|
>9 week |
5 |
-0.65 |
-1.9 |
0.64 |
0.66 |
0.321 |
75.4 |
0.003 |
|
SMD and I 2 were considered significant at p < 0.05; N, number of comparisons; SMD, standardized mean differences between the turmeric powder and controls; CI, confidence interval; SE, standard error; p, probability value; NA, not available |
||||||||
The pooled SMD estimates indicated that dietary turmeric powder decreased on YCL of laying hens (SMD = -1.2; 95% CI: -2.2 to -0.15; p = <0.001) in 1 to 10 g/kg dose. Restricted analysis considering the hen's breed showed that turmeric powder decreased YCL in brown hens in low heterogeneity. Duration of TP administration of <9 weeks also decreased YCL (p<0.05).
In the meta-regression analysis, we analyzed the relationship between the Hedges’ g effect size from the outcome variables with the inclusion levels of turmeric powder in the diet as a predictor variable considering there were wide ranges of inclusion rates of turmeric powder in the layer diet (g/kg diet, Table 1). The results of the meta-regression revealed that inclusion levels had no effects on final EW (p = 0.775), EST ( p = 0.736), YC (p= 0.307 and YCL (p = 0.266). However, the inclusion level showed an increase in HU (p = 0.005) (Table 10; Figure 7).
|
Table 10. Meta-regression analysis for moderator variable that influenced the effect of dietary turmeric powder on egg quality (standardized mean differences) |
||||||
|
Response Variable |
Parameter Estimates |
p-value |
||||
|
Intercept |
SE Intercept |
Slope |
SE Slope |
|||
|
Egg weight |
0.32 |
0.56 |
-0.01 |
0.04 |
0.78 |
|
|
Haugh unit |
1.4 |
0.30 |
-0.05 |
0.02 |
0.01 |
|
|
Eggshell thickness |
0.64 |
0.27 |
-0.01 |
0.03 |
0.74 |
|
|
Yolk color |
1.9 |
0.78 |
0.05 |
0.05 |
0.31 |
|
|
Yolk cholesterol level |
-0.07 |
1.2 |
-0.29 |
0.26 |
0.27 |
|
|
p, probability value; SE, standard error |
||||||
 |
|
Figure 7. Meta-regression
analysis to evaluate the relationship between turmeric powder inclusion
levels in the layer diet as predictor variable with outcome variables (a) egg weight, (b) haugh unit, (c) eggshell thickness, (d) yolk color and (e) yolk cholesterol level |
The funnel plots evaluating the effects of turmeric powder supplementation on all parameters in laying hens indicate that the funnel plots were almost symmetrical (Figure 8). There was evidence of publication bias in the studies used in the analysis to assess the effect of turmeric powder treatment on EW, HU, EST, YC and YCL in laying hens, as affirmed by Rosenberg’s Nfs observed significance level of p-value being lower than the target significance level of P<0.050 needed to show the presence of publication bias. However, the Rosenberg Nfs of 471 for YC is above the threshold of 60 and needed to consider the results of the pooled effect size robust. The presence of publication bias was therefore not an issue in this meta-analysis because a substantial number of unpublished papers would be required to modify the statistically significant results.
 |
 |
 |
 |
 |
|
| Figure 8. Funnel plots analysis on (a) egg weight, (b) haugh unit, (c) eggshell thickness (d) yolk color and (e) yolk cholesterol level to detect publication bias between-study | |
|
Table 11. Fail-safe N calculating using the Rosenthal and Rosenberg approach to detect publication bias |
||||||||
|
Variable |
Rosenthal |
Rosenberg |
||||||
|
Observed |
Target |
Fail- |
Average |
Observed |
Target |
Fail- |
||
|
Egg weight |
0.036 |
0.05 |
7 |
0.20 |
0.053 |
0.05 |
0 |
|
|
Haugh unit |
<0.001 |
0.05 |
172 |
0.48 |
<0.001 |
0.05 |
41 |
|
|
Eggshell thickness |
<0.001 |
0.05 |
182 |
0.45 |
<0.001 |
0.05 |
43 |
|
|
Yolk color |
<0.001 |
0.05 |
1444 |
1.2 |
<0.001 |
0.05 |
571 |
|
|
Yolk cholesterol level |
<0.001 |
0.05 |
48 |
-0.70 |
0.003 |
0.05 |
12 |
|
The aim of the literature study to investigate the effect of turmeric powder on egg quality of commercial laying hens. Overall, the meta-analysis revealed that supplementing with turmeric powder did not affect egg weight. However, dietary turmeric powder can improve egg weight of brown laying hens while the treatment on white laying hen studies had no effect. Genotype differences that result in changes in egg size should be expected to result in changes in the weight of the egg components. Similarly, some researchers determined that egg, yolk, albumen and shell weights of brown eggs were greater than those of white eggs (Basmacioğlu and Ergül 2005; North and Bell 1990).
The egg white (albumen) of Lohmann brown layers was shown to be superior in terms of weight and height when compared to Lohmann white, resulting in a higher haugh unit of around 74% compared to 67.7% for the Lohmann white strains (Hagan and Eichie 2019). The study by Flecther et al (1981) has shown that the shell weight of brown-shelled eggs was greater than that of white-shelled eggs. This might explain why egg weight increased in brown laying hens following turmeric powder feeding.
Curcumin has been shown to have a number of beneficial impacts on gut morphology and flora. It stimulates the release of enzymes, such as amylase, protease and bile acids, in the stomach, promoting digestion and nutrient absorption (Rajput et al 2012). The gastrointestinal system of chickens, which houses diverse and complex microbiota, can benefit from adjustments in feed composition to include turmeric. Studies have shown that feeding phenolic compounds, such as curcumin, reduces gastrointestinal inflammation and enhances nutrient absorption (Shang et al 2018). The feed nutrients will influence egg quality, one of which is the weight of the eggs produced (Molnár et al 2018).
Supplementing with turmeric powder increased haugh unit of laying hen eggs. According to (Saraswati et al 2013), an increase in albumen showed that active substances in turmeric powder stimulated the growth of the epithelial cells and tubular gland cells in the magnum to synthesize and secrete albumen. During the spawning period, the gland cells of the magnum can periodically express a variety of specific proteins, including ovomucin (OV), ovalbumin (OVA), lysozyme (LYZ), ovomucoid (OVM), anti-biotin (AVD), etc (Sah et al 2018). Previous studies have indicated that about 90% of OVA is synthesized and secreted in the magnum tissue (He et al 2017; Hu et al 2016).
Turmeric powder supplementation also improves eggshell thickness. the eggshell would become an important factor that influences the bacteria trans-shell penetration (Messens et al 2005). The improvement of eggshell quality is mainly due to the increased feed intake of laying hens, which frees calcium in the serum combined with plasma proteins or other components so that there is enough Ca 2+ in the blood to participate in the formation of eggshells (Liu et al 2020). The improvements in eggshell‐related parameters might be caused by environmental and morphological improvements in the uterus, especially calcium-storing cells, due to turmeric supplementation in the laying hen diet. Besides, we think that the calcium secretion per egg remained constant and the egg production performance was reduced (Nadia et al 2008).
Furthermore, dietary turmeric powder also increases yolk color. Turmeric supplementation increased the yolk color index in the present study. It has been proven that the yolk colour depends on the pigments derived from the feed ingredients (Mosayyeb Zadeh et al 2022). Turmeric is used in food as natural colorant and flavoring (Wang et al 2015). The higher use of turmeric flour has an impact on the quality of the egg yolk which gives a very yellow color (Jaelani et al 2021). Enhancement of yolk color could result from the yellowish pigment of turmeric (curcuminoid, curcumin and its related compounds) (Riasi 2012). The color of yolk is a typical sensory attribute that is not necessarily related to the nutritive value of the respective egg. Consumers believe that an intense yellow or even golden-orange color indicates a healthy egg that can be used manifold in food preparation (Grashorn 2016).
In the current study, yolk cholesterol levels decreased in layers fed diet supplemented with turmeric powder. Turmeric powder may reduce cholesterol by increasing the activity of cholesterol-7-αhydrolase or inhibit the activity of HMG Co-A reductase (Malekizadeh et al 2012). It is believed that curcumin suppresses the activity of HMG-CoA through the inhibition of transcription (Shin et al 2011) and stimulates the conversion of cholesterol to bile acid, to eliminate cholesterol from the body (Srinivasan and Sambaiah 1991). and hence, increased the excretion of cholesterol (Qinna et al 2012).
From meta-analysis studies, it can be concluded that turmeric flour supplementation can increase egg weight, haugh units, eggshell thickness and decrease yolk cholesterol levels. In addition, dietary turmeric powder can improve the color of egg yolk which is one indicator of egg quality for consumers. Turmeric powder inclusion, in brown laying hens, young laying hens (<40 weeks) and low dose treatment (<11 g/kg) showed good effect.
The authors are grateful to The Directorate General of Higher Education, Research and Technology, Ministry of Education, Culture, Research and Technology, Indonesia, for financial support through the Pendidikan Magister menuju Doktor untuk Sarjana Unggul (PMDSU) research scheme with the grant no. 089/E5/PG.02.00.PT/2022 and contract no. 2009/UN1/DITLIT/Dit-Lit/PT.01.03/2022
Ait-Kaki A, Chebli Y, El Otmani S and Moula N 2021 Effects of yellow mealworm larvae (Tenebrio molitor) and turmeric powder (Curcuma) on laying hens performance, physical and nutritional eggs quality. J. Indonesian Trop. Anim. Agric., Volume 47, Issue 2, Article #1 Retrieved September 2023, from https://doi.org/10.14710/jitaa.47.2
Attia F A 2018 The influence of supplementing chamomile and turmeric powder on productive performance and egg quality of laying hens. Egypt. Poult. Sci., Volume 38, Issue 2, Article #9 Retrieved September 2023, from https://journals.ekb.eg/article_8218.html
Ayeni A O, Oladedun A E and Agbede J O 2020 Performance and egg qualities of old-laying hens fed with diets containing selected phytogenic feed additives. J. Food Nutr. Agric., Volume 3, Article #4 Retrieved September 2023, from https://doi.org/10.21839/jfna.2020.v3.330
Basmacioğlu H and Ergül M 2005 Research on the factors affecting cholesterol content and some other characteristics of eggs in laying hens: the effects of genotype and rearing system. Turk J. Vet. Anim. Sci., Volume 29, Number 1, Article #26 Retrieved September 2023, from https://journals.tubitak.gov.tr/veterinary/vol29/iss1/26/
Borenstein M, Hedges L V, Higgins J P T and Rothstein H R 2009 Introduction to meta-analysis. John Wiley & Sons, Ltd. United Kingdom. DOI:10.1002/9780470743386
Dalal R, Kosti D and Tewatia B 2018 Effect of turmeric powder on egg quality, gut morphology, ecology and on immune system of laying hen: A review. J. Entomol. Zool. Stud., Volume 6, Issue 3, Article #26 Retrieved September 2023, from https://www.entomoljournal.com/archives/2018/vol6issue3/PartN/6-3-26-149.pdf
Denlİ M and Demİrel R 2018 Replacement of antibiotics in poultry diets. CABI Reviews, Volume 13, Article #13 Retrieved September 2023, from https://doi.org/10.1079/PAVSNNR201813035
Egger M and Smith G D 2001 Principles of and procedures for systematic reviews. In M. Egger and G. D. Smith (Eds.), Systematic reviews in health care: Meta-analysis in context (pp. 23–42). Brit Med J Books. https://doi.org/10.1002/9780470693926.ch2
Fawaz M A, Südekum K, Hassan H A and Abdel‐Wareth A A A 2022 Productive, physiological and nutritional responses of laying hens fed different dietary levels of turmeric powder. J. Anim. Physiol. Anim. Nutr. (Berl), Volume 107, Article #1 Retrieved September 2023, from https://doi.org/10.1111/jpn.13686
Flecther D L, Britton W M, Rahn A P and Savage S I 1981 The influence of layer flock age on egg component yields and solids content. Poult. Sci., Volume 60, Issue 5, Article #17 Retrieved September 2023, from https://doi.org/10.3382/ps.0600983
Gouda M M and Prabhakar Bhandary Y 2018 Natural antibiotic effect of turmeric in poultry management. Int. J. Poult. Fish. Sci., Volume 2, Issue 2, Article #1 Retrieved September 2023, from https://doi.org/10.15226/2578-1898/2/2/00109
Grashorn M 2016feed additives for influencing chicken meat and egg yolk color. Handbook on Natural Pigments in Food and Beverages. Elsevier Ltd. pp. 283–302. https://doi.org/10.1016/B978-0-08-100371-8.00014-2
Hadj Ayed M, Aďssa A and Noumi M 2018 A comparative study between the effects of feed inclusion with garlic (Allium sativum), cloves and turmeric (Curcuma longa) rhizome powder on laying hens’ performance and egg quality. Iran. J. Appl. Anim. Sci., Volume 8, Issue 4, Article #19 Retrieved September 2023, from https://ijas.rasht.iau.ir/article_544795.html
Hagan J K and Eichie F O 2019 Egg quality of two layer strains as influenced by extended storage periods and storage temperatures. Livest. Res. Rural. Dev., Volume 31, Number 9, Article #145 Retrieved September 2023, from http://www.lrrd.org/lrrd31/9/jhagan31145.html
Hanif M F, Ariyadi B, Muhlisin and Agus A 2023 Response of turmeric powder supplementation on commercial laying hens performance: a meta-analysis. Livest. Res. Rural. Dev., Volume 35, Number 9, Article #85 Retrieved September 2023, from http://www.lrrd.org/lrrd35/9/3585alia.html
Hassan S M 2016 Effects of adding different dietary levels of turmeric ( Curcuma longa Linn) powder on productive performance and egg quality of laying hens. Int. J. Poult. Sci., Volume 15, Issue 4, Retrieved September 2023, from https://doi.org/10.3923/ijps.2016.156.160
He T, Zhang H, Wang J, Wu S, Yue H and Qi G 2017 Proteomic comparison by iTRAQ combined with mass spectrometry of egg white proteins in laying hens (Gallus gallus) fed with soybean meal and cottonseed meal. PLoS ONE, Volume 12, Issue 8, Retrieved September 2023, from https://doi.org/10.1371/journal.pone.0182886
Higgins J P T, Altman D G, Gotzsche P C, Juni P, Moher D, Oxman A D, Savovic J, Schulz K F, Weeks L and Sterne J A C 2011 The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ, Volume 343, Article #d5928 Retrieved August 2023, from https://doi.org/10.1136/bmj.d5928
Higgins J P T and Thompson S G 2002 Quantifying heterogeneity in a meta-analysis. Stat Med., Volume 21. Issue 11, Retrieved August 2023, from https://doi.org/10.1002/sim.1186
Hu S, Qiu N, Liu Y, Zhao H, Gao D, Song R and Ma M 2016 Identification and comparative proteomic study of quail and duck egg white protein using 2-dimensional gel electrophoresis and matrix-assisted laser desorption/ionization time-of-flight tandem mass spectrometry analysis. Poult. Sci., Volume 95, Issue 5, Retrieved September 2023, from https://doi.org/10.3382/ps/pew033
Jaelani A, Abelina N, Samudera R, Rostini T, Masganti and Setyowati A I 2021 The effect of additional turmeric flour in rations on the performance and egg quality of laying chicken isa brown strain age 70 th weeks. IOP Conf. Ser.: Earth Environ. Sci., Volume 888, Article #012054. Retrieved September 2023, from https://doi.org/10.1088/1755-1315/888/1/012054
Jennions M D, Lortie C J, Rosenberg M S and Rothstein H R 2013 Publication and related bias. In J. Koricheva, J. Gurevitch and K. Mengersen (Eds.), Handbook of meta-analysis in ecology and evolution (pp. 207–236). Princeton University Press.
Kinati C, Ameha N, Girma M and Nurfeta A 2021 Efective microorganisms, turmeric (Curcuma longa) as feed additiveson production performance and sensory evaluation of eggs from white leghorn hens. Livest. Res. Rural. Dev., Volume 33, Issue 1, Article #3 Retrieved September 2023, from https://www.lrrd.org/lrrd33/1/kinat3303.html
Koricheva J, Gurevitch J and Mengersen K 2013 Handbook of meta-analysis in ecology and evolution. Princeton University Press.
Košťálová D, Bezáková L, Račkovác L, Mošovská S and Šturdík E 2013 Therapeutic potential of curcumin in medicinal chemistry. ACS, Volume 6, Issue 1, Retrieved September 2023, from https://doi.org/10.2478/acs-2013-0015
Kujero G O, Oke O E, Adeyemi O A, Sogunle O M and Sobayo R O 2021 Reproductive and physiological responses and egg quality traits of isa brown chickens fed diets supplemented with ginger or turmeric powder. Research Square. Retrieved September 2023, from https://doi.org/10.21203/rs.3.rs-985543/v1
Liberati A, Altman D G, Tetzlaff J, Mulrow C, Gřtzsche P C, Ioannidis J P A, Clarke M, Devereaux P J, Kleijnen J and Moher D 2009 The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Medicine, Volume 6, Issue 7, Article #e1000100 Retrieved September 2023, from https://doi.org/10.1371/journal.pmed.1000100
Liu M, Lu Y, Gao P, Xie X, Li D, Yu D and Yu M 2020 Effect of curcumin on laying performance, egg quality, endocrine hormones and immune activity in heat-stressed hens. Poult. Sci., Volume 99, Issue 4, Retrieved September 2023, from https://doi.org/10.1016/j.psj.2019.12.001
Malekizadeh M, Moeini M M and Ghazi S 2012 The effects of different levels of ginger ( Zingiber officinale Rosc) and turmeric ( Curcuma longa Linn) rhizomes powder on some blood metabolites and production performance characteristics of laying hens. J. Agr. Sci. Tech., Volume 14, Issue 1, Article #12 Retrived September 2023, from https://jast.modares.ac.ir/article-23-4117-en.html
Messens W, Grijspeerdt K and Herman L 2005 Intrinsic and extrensic factors influencing eggshell penetration by Salmonella enteritidis. Proceedings XVIIth European Symposium on the Quality of Poultry Meat & XIth Symposium on the Quality of Eggs and Egg Products, 17th European Symposium on the Quality of Poultry Meat and 11th Symposium on the Quality of Eggs and Egg Products (2005), Doorwerth, Netherlands.
Mirbod M, Mahdavi A H, Samie A H and Mehri M 2017Effects of Curcuma longa rhizome powder on egg quality, performance and some physiological indices of laying hens fed different levels of metabolizable energy. J. Sci. Food Agric., Volume 97, Issue 4, Retrieved September 2023, from https://doi.org/10.1002/jsfa.7862
Mohamed M A and Hassan H M A 2023 Phytogenic substances as safe growth promoters in poultry nutrition. Int. J. Vet. Sci, Volume 12, Issue 1, Article #13 Retrieved September 2023, from https://doi.org/10.47278/journal.ijvs/2022.134
Molnár A, Hamelin C, Delezie E and Nys Y 2018Sequential and choice feeding in laying hens: Adapting nutrient supply to requirements during the egg formation cycle. World’s Poultry Sci. Journal., Volume 74, Issue 2, Retrieved September 2023, from https://doi.org/10.1017/S0043933918000247
Mosayyeb Zadeh A, Mirghelenj S A, Hasanlou P and Shakouri Alishah H 2022 Effects of turmeric (Curcuma longa) powder supplementation in laying hens’ diet on production performance, blood biochemical parameters and egg quality traits. J Anim. Physiol. Anim. Nutr. (Berl), Volume 107, Issue 2, Retrieved September 2023, from https://doi.org/10.1111/jpn.13746
Muaz K, Riaz M, Akhtar S, Park S and Ismail A 2018 Antibiotic residues in chicken meat: global prevalence, threats and decontamination strategies: a review. J. Food Prot., Volume 81, Issue 4, Retrieved September 2023, from https://doi.org/10.4315/0362-028X.JFP-17-086
Mutlag N A, Al-Norri M A and Farhan S M 2018 The effect of adding turmeric and artemisia herba powder to ration on productive performance of white laying hens. IJVS, Volume 32, Issue 2, Retrieved September 2023 from https://www.mosuljournals.com/article_153855.html
Nadia L R, Hassan R A, Qota E M and Fayek H M 2008 Effect of natural antioxidant on oxidative stability of eggs and productive and reproductive performance of laying hens. Int. J. Poult. Sci., Volume 7, Issue 2, Retrieved September 2023 from https://doi.org/10.3923/ijps.2008.134.150
North M D and Bell D 1990 Commercial Chicken Production Manual, 4th edition (4th ed.). Van Nostrand Reinhold.
NRC 1994 Nutrient Requirements of Poultry (9th ed.). National Academy Press.
Ogbuewu I P and Mbajiorgu C A 2022 Meta-analysis of zinc supplementation on laying performance, egg quality characteristics and blood zinc concentrations in laying hens. Biol. Trace Elem. Res., Volume 200, Issue 12, Retrieved August 2023 from https://doi.org/10.1007/s12011-021-03080-8
Ogbuewu I P, Okoro V M and Mbajiorgu C A 2021 Meta-analysis of the responses of laying hens to garlic (Allium sativum) supplementation. Anim. Feed Sci. Technol., Volume 275, Article #114866. Retrieved August 2023 from https://doi.org/10.1016/j.anifeedsci.2021.114866
Ooi P S, Rohaida A R, Nur Hardy A D, Devina D, Borhan A H, Kartini S, Jupikely J S, Abdul Rahman M and Alimon A R 2018 Effect of local medicinal herbs as feed additives on production performance and faecal parameters in laying hens. Mal. J. Anim. Sci., Volume 21, Issue 2, Retrieved September 2023, from https://mjas.my/mjas-v2/rf/pages/journal/v21i2/6-HensRohaida.pdf
Park S S, Kim J M, Kim E J, Kim H S, An B K and Kang C W 2012 Effects of Dietary Turmeric Powder on Laying Performance and Egg Qualities in Laying Hens. KJPS, Volume 39, Issue 1, Retrieved September 2023, from https://doi.org/10.5536/kjps.2012.39.1.027
Patra J K, Das G, Lee S, Kang S S and Shin H S 2018 Selected commercial plants: a review of extraction and isolation of bioactive compounds and their pharmacological market value. Trends Food Sci Technol., Volume 82, Retrieved September 2023, from https://doi.org/10.1016/j.tifs.2018.10.001
Qinna N A, Kamona B S, Alhussainy T M, Taha H, Badwan A A and Matalka K Z 2012 Effects of prickly pear dried leaves, artichoke leaves, turmeric and garlic extracts and their combinations on preventing dyslipidemia in rats. ISRN Pharmacol., Retrieved September 2023, from https://doi.org/10.5402/2012/167979
Rahardja D P, Hakim M R and Lestari V S 2015 Egg production performance of old laying hen fed dietary turmeric powder. Int. J. Vet. Sci., Volume 9, Issue 7, Retrived September 2023, from https://doi.org/10.4172/2167-1206.1000133
Rajput N, Muhammah N, Yan R, Zhong X, Wang T and Wang T 2012 Effect of dietary supplementation of curcumin on growth performance, intestinal morphology and nutrients utilization of broiler chicks. J. Poult. Sci., Volume 50, Issue 1, Retrieved September 2023, from https://doi.org/10.2141/jpsa.0120065
Rao D S, Sekhara N C, Satyanarayana M N and Srinivasan M 1970 Effect of curcumin on serum and liver cholesterol levels in the rat. J. Nutr., Volume 100, Issue 11, Retrieved September 2023, from https://doi.org/10.1093/jn/100.11.1307
Riasi A 2012 Production performance, egg quality and some serum metabolites of older commercial laying hens fed different levels of turmeric rhizome (Curcuma longa) powder. J. Med. Plant Res., Volume 6, Issue 11, Retrieved September 2023, from https://doi.org/10.5897/jmpr11.1316
Rostagno H S, Albino L F T, Hannas M I, Donzele J L, Sakomura N K, Perazzo F G, Saraiva A, de Abreu M L T, Rodrigues P B, de Oliveira R F, Barreto S L T and Brito C O 2017 Brazilian Tables for Poultry and Swine: Feedstuff Composition and Nutritional Requirements (H. S. Rostagno, Ed.; 4 th). Universidade Federal de Viçosa, Departamento de Zootecnia.
Sah N, Kuehu D L, Khadka V S, Deng Y, Peplowska K, Jha R and Mishra B 2018 RNA sequencing-based analysis of the laying hen uterus revealed the novel genes and biological pathways involved in the eggshell biomineralization. Sci. Rep., Volume 8, Issue 1, Retrieved September 2023, from https://doi.org/10.1038/s41598-018-35203-y
Saraswati T R, Manalu W, Ekastuti D R and Kusumorini N 2013 The role of turmeric powder in lipid metabolism and its effect on quality of the first quail’s egg. J. Indonesian Trop. Anim. Agric., Volume 38, Issue 2, Retrieved September 2023, from https://doi.org/10.14710/jitaa.38.2.123-130
Shang Y, Kumar S, Oakley B and Kim W K 2018 Chicken gut microbiota: Importance and detection technology. Front. Vet. Sci., Volume 5, Article #254 Retrieved September 2023, from https://doi.org/10.3389/fvets.2018.00254
Sharifi-Rad J, Rayess Y, Rizk A, Sadaka C, Zgheib R, Zam W, Sestito S, Rapposelli S, Neffe-Skocińska K, Zielińska D, Salehi B, Setzer W, Dosoky N, Taheri Y, El Beyrouthy M, Martorell M, Ostrander E, Suleria H, Cho W, Maroyi A and Martins N 2020 Turmeric and its major compound curcumin on health: bioactive effects and safety profiles for food, pharmaceutical, biotechnological and medicinal applications. Front. Pharmacol., Volume 11, Article #01021 Retrieved September 2023, from https://doi.org/10.3389/fphar.2020.01021
Shin S K, Ha T Y, McGregor R A and Choi M S 2011 Long-term curcumin administration protects against atherosclerosis via hepatic regulation of lipoprotein cholesterol metabolism. Mol. Nutr. Food Res., Volume 55, Issue 12, Retrieved September 2023, from https://doi.org/10.1002/mnfr.201100440
Singh P K, Kumar A and Tiwari D P 2019 Effects of dietary supplementation of black cumin, garlic and turmeric on the production performance and egg quality of white leghorn hens. Anim. Nutr. Feed Technol., Volume 19, Issue 3, Retrieved September 2023, from https://doi.org/10.5958/0974-181X.2019.00034.9
Srinivasan K and Sambaiah K 1991The effect of spices on cholesterol 7 alpha-hydroxylase activity and on serum and hepatic cholesterol levels in the rat. Int. J. Vitam. Nutr. Res., Volume 61, Issue 4, Retireved September 2023, from https://pubmed.ncbi.nlm.nih.gov/1806542/
Tayyem R F, Heath D D, Al-Delaimy W K and Rock C L 2006 Curcumin content of turmeric and curry powders. Nutr. Cancer, Volume 55, Issue 2, Retireved September 2023, from https://doi.org/10.1207/s15327914nc5502_2
Wallace B C, Lajeunesse M J, Dietz G, Dahabreh I J, Trikalinos T A, Schmid C H and Gurevitch J 2017 OpenMEE: Intuitive, open-source software for meta-analysis in ecology and evolutionary biology. Methods Ecol. Evol., Volume 8, Issue 8, Retireved August 2023, from https://doi.org/10.1111/2041-210X.12708
Wang D, Huang H, Zhou L, Li W, Zhou H, Hou G, Liu J and Hu L 2015 Effects of dietary supplementation with turmeric rhizome extract on growth performance, carcass characteristics, antioxidant capability and meat quality of wenchang broiler chickens. Ital. J. Anim. Sci., Volume 14, Issue 3, Article #3870 Retireved September 2023, from https://doi.org/10.4081/ijas.2015.3870
Wang P and Yu Z 2015 Species authentication and geographical origin discrimination of herbal medicines by near infrared spectroscopy: a review. J. Pharm. Anal., Volume 5, Issue 5, Retireved September 2023, from https://doi.org/10.1016/J.JPHA.2015.04.001
Zava D T, Dollbaum C M and Blen M 1998 Estrogen and progestin bioactivity of foods, herbs and spices. Exp. Biol. Med. (Maywood), Volume 217, Issue 3, Retireved September 2023, from https://doi.org/10.3181/00379727-217-44247