Next Article in Journal
A Forest Wildlife Detection Algorithm Based on Improved YOLOv5s
Next Article in Special Issue
Organic Trace Elements Improve the Eggshell Quality via Eggshell Formation Regulation during the Late Phase of the Laying Cycle
Previous Article in Journal
A Text-Mining Analysis of Research Trends in Animal-Assisted Therapy
Previous Article in Special Issue
Influence of Molybdenum and Organic Sources of Copper and Sulfur on the Performance, Carcass Traits, Blood Mineral Concentration, and Ceruloplasmin Activity in Lambs
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Animals
Volume 13
Issue 19
10.3390/ani13193132
animals-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Effect of Organic Trace Mineral Supplementation in the Form of Proteinates on Performance and Sustainability Parameters in Laying Hens: A Meta-Analysis

by
Laurann Byrne
1,*,
Stephen Ross
2,
Jules Taylor-Pickard
1 and
Richard Murphy
1
1
Alltech Biotechnology Centre, Summerhill Road, A86 X006 Dunboyne, Ireland
2
Alltech E-CO2, Ryhall Road, Stamford PE9 1TZ, UK
*
Author to whom correspondence should be addressed.
Animals 2023, 13(19), 3132; https://doi.org/10.3390/ani13193132
Submission received: 16 June 2023 / Revised: 23 August 2023 / Accepted: 5 October 2023 / Published: 7 October 2023
(This article belongs to the Special Issue The Role of Trace Minerals in Livestock and Poultry Production)
Browse Figures
Versions Notes

Abstract

:

Simple Summary

This work aims to highlight the importance of mineral form on production performance and egg quality traits using meta-analysis. Sustainability impacts, which focused on the carbon footprint of egg production, were also assessed. Results demonstrated that the inclusion of organic trace minerals, in the form of proteinates, positively impacted key parameters such as hen-day production, feed conversion ratio, egg mass, egg weight, and egg loss. Eggshell parameters such as thickness, strength, weight, and eggshell percentage were also higher, and Haugh unit was 1 point greater with the inclusion of proteinate minerals.

Abstract

The effect of supplementing organic trace minerals (OTM), in the form of mineral proteinates (Bioplex® Cu, Fe, Mn, and Zn, Alltech Inc., Nicholasville, KY, USA), in the diets of laying hens was examined using Comprehensive Meta-Analysis (CMA) statistical software. The impact on production performance, egg quality traits, and sustainability parameters related to the carbon footprint of egg production was assessed. Data were obtained from 32 global studies, comprising 107 dietary assessments of 30,992 laying hens. Overall pooled effect size (raw mean difference) of production performance when dietary organic trace minerals were supplemented either in basal diets, partial replacement of inorganic trace minerals (ITM), or total replacement of ITM, indicated that use of Bioplex minerals resulted in 2.07% higher hen-day production (HDP), whilst feed conversion ratio (FCR) was lower by 51.28 g feed/kg egg and 22.82 g feed/dozen eggs, respectively. For egg quality traits, daily egg mass was 0.50 g/hen/day higher and egg weight was 0.48 g per egg greater when Bioplex minerals were incorporated in the diet. The mean difference in egg loss was −0.62%. Eggshell thickness was greater by 0.01 mm, and a higher eggshell strength of 0.14 kgf was observed. Eggshell weight was heavier by 0.20 g, eggshell percentage was higher by 0.15%, and Haugh unit was 1 point higher (0.89). We also carried out a meta-regression of the effects of the study factors (location, year of study, hen breed/strain, age of hens, number of hens, and study duration) on the overall pooled effect size of the production performance and egg quality traits in response to supplementary OTM inclusion, and it indicated that certain factors had a significant (p < 0.05) impact on the results. Finally, a life cycle assessment (LCA) model was selected to evaluate the impact of feeding organic trace mineral proteinates on the carbon footprint (feed and total emission intensities) of the egg production using the data generated from the meta-analysis. Results showed that the inclusion of OTM proteinates resulted in an average drop in feed and total emission intensities per kg eggs of 2.40% and 2.50%, respectively, for a low-global-warming-potential (GWP) diet and a drop of 2.40% and 2.48% for feed and total emissions, respectively, based on high-GWP diet. Based on the overall results, the inclusion of organic trace mineral proteinates in layer diets can benefit production performance and egg quality traits while contributing to a lower carbon footprint.

1. Introduction

Mineral nutrition plays a key role in poultry production; however, many diets are routinely formulated based on outdated data [1,2,3]. Cognisant of optimising the genetic potential of modern breeds, research on mineral supplementation has become a necessity [4]. Inorganic mineral salts are regularly overformulated to ensure adequate levels are included to meet dietary requirements; however, uptake and utilisation are limited, resulting in poor performance results [5,6,7]. Mineral levels have also come under additional scrutiny from an environmental perspective, and providing more than required will become a less acceptable practice [8,9]. Organic trace minerals (OTM) are noted to be more bioavailable than inorganic sources, with enhanced performance and lower mineral excretion being reported [10]. These responses can have positive environmental benefits, but different forms of OTM exist, varying greatly in efficacy [10,11,12,13]. As poultry genotypes have evolved, birds are required to produce more with less inputs; however, the underlying physiological mechanisms for mineral uptake remain the same. High-performance breeds may exceed standard mineral absorption mechanisms, and the only way to achieve a constant mineral supply at a cellular level is by increasing dietary levels or using sources with higher relative bioavailability [13]. Nutritionists have started to redefine the mineral levels used in poultry diets for several reasons, including decreasing feed costs while improving performance, enhancing the sustainability of poultry production, and lowering antagonist interactions with other dietary nutrients. The formulation of such diets, that target precision nutrition, will require the most bioavailable sources of minerals.
Numerous trials under various conditions have been conducted globally to investigate the total replacement of Cu, Fe, Mn, and Zn in their inorganic salt form with lower amounts of the same minerals in proteinate form. Results have indicated that the use of lower OTM proteinate amounts could not only maintain or optimise growth and reproductive performance, but also lower the mineral content of excreta [1]. With an abundance of published trial data in existence, confusion or misinterpretation can occur. Employing methods such as meta-analyses to systematically combine data from multiple trials provides evidence-based conclusions to aid in alleviating such issues. The objective of this study was to apply this type of statistical procedure to examine the impact of supplementing OTM in the form of proteinate minerals on the production performance and egg quality attributes of laying hens. Carbon footprint (CFP; total GHG emissions associated with the production of a functional unit of output) was also calculated using the meta-analysis results, enabling the effect of feeding proteinate trace minerals on the CFP of egg production to be quantified. A scenario simulation was also developed using a life cycle assessment (LCA) model to provide a method for quantifying the CFP of livestock products from cradle to farmgate [14].

2. Materials and Methods

2.1. Literature Search and Selection Criteria

A comprehensive data search was carried out using Google Scholar, Mendeley, PubMed, Web of Science, CAB Direct, and Scopus databases to obtain peer-reviewed articles evaluating the effect of a commercial organic trace mineral product (Bioplex Cu, Fe, Mn, and Zn, Alltech Inc., Nicholasville, KY, USA) on layer performance. Furthermore, the company’s internal bibliographic database was searched to retrieve published and unpublished trial reports presented in a Ph.D. dissertation or at international scientific conferences. Keywords used for the digital search included “layers”, “poultry”, “organic trace element”, “organic trace mineral”, “Bioplex”, “total replacement”, partial replacement”, and “layer performance”. The literature search and study selection applied in this meta-analysis, carried out according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) Statement [15,16,17], are reported in Figure 1. Two reviewers, working independently, screened each record and collected the data. The final literature search to obtain relevant data was conducted in February 2023 and there was no date restriction imposed on the literature search, to cover the entire duration that the OTM products have been investigated in layers.
A total of 70 research articles were initially identified for screening and were subjected to the following criteria: (1) the study was reported in English; (2) the trial was conducted in layers and adequate randomisation of birds into treatments was reported; (3) the study contained at least one negative control (basal diet) and/or positive control (inorganic trace mineral diet) and a diet supplemented with Bioplex® as the organic trace mineral product; (4) the trace mineral dosage application rate and feeding duration were reported; (5) information describing the study factors of the experiments was provided or available upon request from authors; and (6) information on one or more performance parameters and egg quality attributes was reported or available upon request from authors. Post-initial screening, 32 trials were selected for inclusion in the meta-analysis; they are outlined in Table 1.

2.2. Data Extraction

Using the data extracted from the 32 selected trials, a database was developed consisting of 107 comparisons of basal or inorganic trace mineral supplemented diets vs. organic trace mineral supplemented diets. Basal diets represented a comparison of basal diets vs. basal + supplementary OTM. Partial replacement (PR) represented a comparison of basal diets + supplementary inorganic trace minerals (ITM) vs. basal diets + partial replacement of supplementary ITM with OTM. Total replacement (TR) represented a comparison of basal diets + supplementary ITM vs. basal diets + total replacement of supplementary ITM with OTM.
Trace mineral concentration, form (ITM/OTM), and type (Cu, Fe, Mn, and Zn) were recorded (Table 2). Mean OTM levels from all studies assessed were lower than mean ITM inclusion rates for all minerals, indicating that lower OTM levels can be included without a detrimental impact on performance parameters. Data on production performance parameters (feed intake (g/day/hen), hen-day production (%), FCR (g feed/kg egg), and FCR (g feed/dozen eggs)) and egg quality traits (egg mass (g/hen/day), egg weight (g), egg loss (%), eggshell thickness (mm), eggshell strength (kgf), eggshell weight (g), eggshell percentage (%), and Haugh unit) were also extracted (Table 3). The measure of variance was documented as standard deviation (SD). Additionally, data on various study factors including location, year of study, hen breed/strain, age of hens, number of hens and study duration were obtained.

2.3. Statistical Analysis

Comprehensive Meta-analysis software (version 3, Biostat Inc., Englewood, NJ, USA) was utilised to analyse the effect of treatment comparisons in a random-effects model. A random-effects model allowed the true effect to vary from study to study and include between-study variability (true heterogeneity) as well as sampling error [47]. Raw mean difference (RMD) and standardised mean difference (SMD) at a 95% level of confidence interval (CI) were used to estimate the effect size of dietary OTM supplementation on layer performance parameters and egg quality variables. Effect size estimates (RMD and SMD) of all trial comparisons (OTM diets vs. basal and ITM diets) on performance variables were declared significant when p ≤ 0.05, and a tendency for effect was observed when 0.05 < p ≤ 0.10. Furthermore, sub-databases were created to perform a meta-analysis of subgroups, evaluating how study factors influence the response of selected production performance and egg quality variables (feed intake, HDP, FCR, egg weight, egg loss, and eggshell strength) to OTM supplementation. Study factors consisted of location (Africa, Europe, North America, Oceania, South America, Asia), year of study, hen breed/strain (Black Harco, Bovans, Brown Yaffa, H&N Brown Nick, Hy-Line, ISA Brown, Jinghong, Roso SL hybrid, White Leghorn, Lohmann), age of hens, number of hens, and study duration.

2.4. Heterogeneity

Variation across studies was assessed using the I2 statistic and the associated significance level of chi-squared statistic [47]. I2 values of <25%, 25 to 50%, and >50% suggest low, moderate, and high heterogeneity, respectively [48].

2.5. Publication Bias

Funnel plots were created for each outcome to assess the risk of bias in the studies included in the meta-analysis. The standard error of the observed outcomes as a predictor was used to check for funnel plot asymmetry with symmetrical distribution of studies around the calculated mean difference (MD), indicative of no bias risk. The potential risk of bias was identified through an observed asymmetrical distribution around MD and confirmed by Egger’s test with p < 0.05 indicative of the presence of bias in the funnel plot [49].

2.6. Life Cycle Assessment

2.6.1. Scope

Life cycle assessment (LCA) simulation modelling was conducted to assess the impact of feeding organic trace minerals on the carbon footprint (CFP) of layer production. The system boundary encompassed all processes involved in layer production up to finished birds being ready to leave the farm (i.e., cradle to farmgate). As such, modelling accounted for both pre-farm supply chain emissions, including the production burden of purchased feeds and raw materials, and the on-farm emissions from layer production and litter management. Subsequent emissions attributed to post-farm processing, packaging, or transport of products beyond the farm gate were not considered, consistent with previous LCA studies analysing egg production systems [50,51,52,53]. A flow diagram describing the LCA system boundary is outlined in Figure 2.
Outputs from the system are spent hens, saleable eggs, and litter. All litter was exported to be land-spread as fertiliser and allocated a carbon credit in the model through system expansion; thus, the eggs and spent hens were considered co-products of the system. The functional unit of the layer assessment was the primary egg product from the system. Emission intensity was presented using three functional units, kg CO2-eq/dozen eggs, g CO2-eq/egg, and kg CO2-eq/kg eggs, leaving the farm gate. The partitioning of total emissions between eggs and sold spent hens was determined based on economic allocation. The assessment period was defined as the birds’ lay period (62 weeks), and all scenarios started with a flock of 100,000 birds on the farm.

2.6.2. Production System and Scenarios

Production systems modelled in this LCA were based upon an average conventional European housed layer system. Four scenarios were defined within this production system: a baseline scenario (i.e., without OTM supplementation) and an intervention scenario (i.e., with OTM supplementation) for two different diets defined by the level of global warming potential (GWP) attributed to each. The low-GWP diet consisted of low-level soybean meal (SBM) inclusion, whereas the high-GWP diet consisted of a higher inclusion level of SBM (Supplementary Table S1). For the low-GWP diet, soybean meal inclusion rates were 15.21%, 15.34%, 6.52%, and 3.60% for the pre-lay, early-lay, mid-lay, and late-lay stages, respectively. For the high-GWP diet, soybean meal inclusion rates were 15.21%, 24.35%, 9.35%, and 3.60% for the pre-lay, early-lay, mid-lay, and late-lay stages, respectively. Feed ingredients were consistent in the baseline and OTM diets, other than the OTM supplementation. All feed ingredients were assumed purchased and delivered onto the layer farm. Birds in all scenarios were managed on 4 successive formulated rations (pre-, early-, peak- and late-lay diets) according to industry practice (Supplementary Tables S1 and S2). Pullets were delivered to the farm after a 16-week rearing period and placed in a flock of 100,000 birds. The subsequent laying period lasted 62 weeks equally across all systems after a 2-week pre-lay period.

2.6.3. Inventory Analysis

Input data on production system parameters were averaged from 300 commercial European layer farm environmental assessments conducted by Alltech E-CO2 of the same system type over a two-year period (2018–2020) (Alltech E-CO2, Stamford, UK). Baseline metrics on entry into the lay cycle were measured as: laying cycle (62 weeks), hen-day production (85%), eggs produced per bird (369), egg weight (65 g), total egg mass per hen (23.99 kg), mortality (3.5%), egg loss (1.5%), total feed per hen (50.35 kg), and FCR (2100 g/kg eggs). Bird age milestones were: on entry (17 weeks), point of lay (19 weeks), end of lay/life (81 weeks), and total laying period (62 weeks). In total, there were 4 phase diets and the period of each included the pre-lay (2 weeks), early-lay (26 weeks), peak-lay (19 weeks), and late-lay (16 weeks) periods. Production performance parameters and egg quality traits when managed in the baseline and OTM scenarios are presented in Supplementary Table S3. The OTM results were derived using the observed results from the meta-analysis, applying the higher relative percentage values observed in production performance parameters compared to the baseline. Commercial data were also used to obtain average input values for general resource use (e.g., bedding, fossil fuels, electricity, water use, and disinfectant). The study assumed that all litter was exported for use as organic fertiliser after being stored on-farm until the flock clear-out. All viable birds were sold at the production period end, and dead birds were assumed sent to a rendering plant.

2.6.4. Impact Assessment

The Alltech E-CO2 Poultry EA™ (layer) model (Alltech E-CO2, Stamford, UK), an industry-specific layer CFP calculator, was employed to conduct the environmental impact assessment. Independently accredited to the LCA international standards PAS:2050 (BSI, 2011) and ISO 14067 (ISO, 2018), this bespoke model has been utilised in commercial layer CFP assessments since 2014. The model follows the Intergovernmental Panel on Climate Change (IPCC) guidelines for tier 2 methodology for on-farm emissions and has the ability to implement case-specific farm data at a tier 3 level [54]. Nitrogen excreted by hens was estimated from the total feed intake per bird, the weighted protein content of the formulated rations, and the estimated percentage of dietary nitrogen excreted by the animal, following IPCC (2006) [54]. Emissions arising from manure and litter management (i.e., CH4, direct and indirect N2O) were also estimated using tier 2 equations from IPCC (2006) [54].
Publicly available data from the software FeedPrint (v2020.00), developed by Wageningen University and Research (WUR), The Netherlands, were used to estimate emissions embedded in the production, processing, and supply of purchased feeds [55]. Data sourced from the WUR model were noted to be derived according to PAS:2050, with an economic allocation of co-products; therefore, they were considered directly compatible with the methodology employed in the present study. Feed ingredients were assumed to be typical of the European market mix, and SBM was assumed to originate from South America (including emissions associated with land-use change). Emission factors derived for each formulated ration are outlined in Supplementary Table S2.
Embedded emissions in pullets placed on the farm were taken to be 4.06 kg CO2-eq per bird, as retrieved from Alltech’s E-CO2 commercial database. Emission factors for all electricity, fossil fuels, and transportation (i.e., of chicks, feed, and dead birds’ removal) were sourced from the UK Department for Environment, Food and Rural Affairs, DEFRA (2020) [56]. Exported litter was assumed destined to be used as fertiliser, and accordingly, a carbon credit was applied via the method of system expansion. Coefficients for nutrient content and availabilities in layer litter were described by DEFRA (2010) [57], and data on the avoided emissions of inorganic fertiliser production were provided by Hoxha and Christensen [58].
Layer production life cycle emissions were calculated using GHG species’ particular global warming potentials for 100 years (GWP100), stated as 25 and 298 times greater than CO2 for CH4 and N2O, respectively [59]. Feed emission intensity (i.e., kgCO2-eq attributed to the feed use per functional unit) and total emission intensity (i.e., total kgCO2-eq per functional unit) of the production system were subsequently estimated for each of the four scenarios for the production life cycle of 100,000 birds placed in the layer system.

3. Results and Discussion

3.1. Study Characteristics

The 32 studies selected for this meta-analysis are outlined in Table 1. Studies were obtained from 14 countries: USA (5), Canada (3), Brazil (6), Peru (2), Nigeria (2), Turkey (2), China (2), Iran (1), Australia (2), Romania (1), Switzerland (1), Slovakia (1), Poland (1), and Czech Republic (3) over a 21-year time period (1999–2020). A total of 30,992 laying hens were involved in the 107 dietary comparisons comprised of Basal/ITM vs. Bioplex supplementation.
Table 2 outlines the trace mineral concentrations supplemented in layer diets and details the treatment comparisons involving total replacement of ITM with OTM (Bioplex Cu, Fe, Mn, and Zn). Results clearly show that supplementation levels of OTM are lower for all minerals compared to ITM levels. Many studies have confirmed that lower inclusion levels of OTM proteinates are possible due to their enhanced bioavailability and absorption, resulting in a lower requirement without negatively impacting animal health or performance [1,9,28,32,36,37,60,61,62,63,64,65,66,67,68,69].
Considerable variation exists in the dataset of production performance and egg quality parameters included in the meta-analysis (Table 3). The global diversity of studies can account for this variation in the dataset, and a wide representation enables meaningful conclusions to be drawn from this meta-analysis.

3.2. Production Performance and Egg Quality

The results of the overall pooled effect size of production performance and egg quality traits when dietary OTM were supplemented either in basal diets, partial replacement for ITM, or total replacement for ITM are presented in Table 4. Corresponding forest plots for each variable are presented in Supplementary Figures S1–S12. For feed intake, no effect was observed with OTM supplementation (p > 0.05) (Table 4, Supplementary Figure S1). HDP was significantly higher (RMD = +2.07), and FCR was significantly lower (RMD = −51.28 g feed/kg egg), in OTM-supplemented flocks (Table 4 and Supplementary Figures S2–S4). Compared to the control, the overall pooled effects of OTM on HDP was +2.48% higher. FCR (g feed/kg egg) was 2.39% lower.
For egg quality traits, incorporating OTM resulted in higher egg mass (RMD = +0.50 g/hen/day) and egg weight (RMD = +0.48 g) (Table 4 and Supplementary Figures S5 and S6). The mean difference in egg loss was −0.62%, which equates to a 39.24% lower egg loss (Table 3 and Supplementary Figure S7). Eggshell thickness was significantly higher (RMD = +0.01 mm, p < 0.001), by 2.94%, and eggshell strength was also significantly higher (RMD = +0.14 kgf, p < 0.001), by 3.84% (Table 4 and Supplementary Figures S8 and S9). Significantly higher values (p < 0.001) were also noted for both eggshell weight (RMD = +0.20 g), which was 2.39% higher, and eggshell percentage (RMD = +0.15%), which was 1.76% higher (Table 4 and Supplementary Figures S10 and S11). Haugh unit was also significantly higher (p < 0.001), by 1 point (RMD = +0.89) (Table 4 and Supplementary Figure S12).
Visual inspection of the funnel plots for all experiments selected for meta-analysis indicates the absence of bias due to the symmetrical distribution of the weighted mean difference in most experiments around the standard error (Figure 3 and Figure 4). Additional analyses using Egger’s test returned nonsignificant values for all parameters with the exception of egg loss, eggshell thickness, and FCR (g/dozen eggs), which returned p values of <0.05, indicating possible publication bias; however, the observed asymmetry could be explained by considering meta-regression residuals [70].
Table 5 outlines the effect size of production performance and egg quality traits when dietary OTM were supplemented in basal diets, whereas Table 6 consists of effect size data when OTM were supplemented as total replacement for ITM. Comparing the resultant data in each table for all parameters, no effect on feed intake was observed with OTM supplementation (p > 0.05) in either scenario. HDP was significantly higher when OTM supplementation was included as total replacement of ITM (RMD = +1.52) (Table 6), and tended towards significance (p = 0.017) when supplemented in basal diets (Table 5). FCR was significantly lower (p < 0.001) with total replacement (RMD = −73.09 g feed/kg egg) (Table 6). Examining the data obtained for egg quality traits, totally replacing ITM with OTM resulted in higher egg mass (RMD = +0.50 g/hen/day) and significantly higher (p < 0.001) egg weight (RMD = +0.76 g) (Table 6). The mean difference in egg loss was −0.57%, which equates to 41.30% lower egg loss (Table 6). Eggshell thickness was significantly greater (RMD = +0.01 mm, p < 0.001), by 3.13%, and eggshell strength was also significantly higher (RMD = +0.15 kgf, p < 0.001), by 3.99%. Significantly higher values (p < 0.001) were also noted for eggshell weight (RMD = +0.11 g) and Haugh unit (p < 0.05). Positive impacts were also seen when including OTM in basal diets, but a far greater number of highly significant (p < 0.001) results were found in studies when total replacement of ITM with OTM occurred. Significant heterogeneity (p < 0.001) was observed in all comparisons, except when the dataset was analysed for total replacement of ITM with OTM for eggshell weight (Table 5 and Table 6). Subgroup analysis was carried out to assess this further, with the meta-regression indicating effects from a number of study factors. This heterogeneity was expected, considering that the studies were performed in different countries under different production management systems.
Based on the results obtained for production performance and egg quality traits, incorporating OTM, in place of ITM, either partially or fully, has a positive impact on the metrics assessed. Previous publications have discussed the benefits of incorporating OTM in poultry nutrition, and the findings in this meta-analysis confirm such results [28,37,65,67].

3.3. Subgroup Analysis

Results from subgroup analysis of the effect of various study factors on the overall pooled effect size of production performance parameters and egg quality traits in response to supplementary OTM are presented in Table 7 and Table 8, respectively. The list of study factors is not exhaustive; other factors such as diet composition, housing, hygiene, genetics, and the type of production system may also contribute.
Feed intake, certain location, breed, and the age of hens had an impact (Africa (p < 0.001), Black Harco (p < 0.001), Brown Yaffa (p < 0.05), age (p < 0.05)) (Table 7). In relation to HDP, many of the study factors had a highly significant (p < 0.001) impact, including location, year of study, hen breeds, age of hens, number of hens, and study duration (Table 7). Key impacts on FCR (g feed/kg egg) included particular locations (Africa (p < 0.001), North America (p < 0.05), certain hen breeds (Bovans (p < 0.05), Brown Yaffa (p < 0.001), H&N Brown Nick (p < 0.05), Hy-Line (p < 0.05)), age of hens (p < 0.001), and study duration (p < 0.001)).
Three egg quality traits (egg weight, egg loss, and eggshell strength) were also assessed using a meta-regression of the effects of study factors on the overall pooled effect size in response to OTM supplementation (Table 8). For egg weight, only the hen breed (Bovans, Brown Yaffa, and H&N Brown Nick) had a significant effect (p < 0.05). For egg loss, the number of hens and the study duration, in addition to the hen breed (H&N Brown Nick, Hy-Line and Isa Brown), had a significant effect (p < 0.05). Location (North America) (p < 0.001), hen breed (Hy-Line, Isa Brown, and Jinghong) (p < 0.05), age of hens (p < 0.05), and study duration (p < 0.05) had a significant effect on eggshell strength.
Inclusion of a meta-regression ensures that additional factors of potential variance are assessed and incorporated into the overall meta-analysis findings, further reducing bias and explaining additional contributing factors of heterogeneity. From the meta-regression results in this study, it is clear that the factors assessed had a notable impact on overall results, demonstrating the importance of including extended methods of statistical analysis.

3.4. Simulated Environmental Impact

Metrics selected for quantifying the effect of supplementing OTM on the carbon footprint of egg production were feed emission intensity and total emission intensity, expressed as three functional units (emissions per dozen eggs, emissions per egg, and emissions per kg eggs). Feed emission intensities per kg eggs were lower in the OTM-supplemented diets for both the low-GWP and high-GWP diet scenarios, by an average of 2.40% (−0.04 and −0.05 kg CO2-eq/kg eggs, respectively) (Table 9). Emissions per egg were lower by 1.65% on average for both diets supplemented with OTM (−1.76 and −2.10 g CO2-eq/egg), and emissions per dozen eggs, on average, were 1.65% lower for both diets supplemented with OTM (−0.02 and −0.02 kg CO2-eq/ dozen eggs). Similarly, total emission intensity per kg eggs was lower by an average of 2.50% in the low-GWP diet and by 2.48% in the high-GWP diet (−0.05 and −0.07 kg CO2-eq/kg eggs, respectively). Emissions per egg were lower, on average, by 1.75% (low-GWP) and 1.73% (high-GWP) for both diets supplemented with OTM (−2.5 and −3.0 g CO2-eq/egg, respectively), and emissions per dozen eggs were lower by an average of 1.75% (low-GWP) and 1.73% (high-GWP) for diets supplemented with OTM (−0.03 and −0.04 kg CO2-eq/ dozen eggs). Previous LCAs for swine and poultry have also noted the appropriateness of the method for assessing the effect of specific feeding practices on the environmental performance of a farm’s product supplied to the market [71,72].
Trace minerals are required to support development and improve the productive performance of laying hens; however, the form that in which the trace mineral is supplemented in the diet plays a crucial role [10,11,28,36,37,67]. Mineral proteinates show higher retention rates and relative bioavailability values than inorganic trace minerals, and the results from this meta-analysis indicate that positive results on production performance and egg quality traits by incorporating OTM in layer diets. Sustainability impacts were also assessed, which focused on the carbon footprint of egg production and, the results indicate that lower feed emissions can be achieved by incorporating OTM.

4. Conclusions

With minerals including Cu, Fe, Mn, and Zn being essential for the growth and development of chickens and their involvement in various physiological processes, selecting the most bioavailable form is essential to optimise health and performance. The results from the meta-analysis demonstrate higher values for a number of key production performance parameters by using organic trace minerals, even at substantially lower inclusion rates, in the form of proteinates (Bioplex Cu, Fe, Mn, and Zn, Alltech Inc., Nicholasville, KY, USA). Hen-day production was greater by +2.07% and FCR was lowered by 51.28 g feed/kg egg and 22.82 g feed/dozen eggs, respectively. Positive impacts were also observed on egg quality traits, with egg mass greater by 0.50 g/hen/day and egg weight higher by 0.48 g per egg, on average. The mean difference in egg loss was lower by −0.62%, which equates to 39.24% less egg loss. Eggshell thickness was greater by 2.94% (0.01 mm), and a greater eggshell strength, by 3.84% (0.14 kgf), was observed. Eggshell weight was greater by 2.39% (0.20 g) and eggshell percentage was greater by 1.76% (0.15). Haugh unit was 1 point higher. With correct formulation, more cost-effective, environmentally sustainable feeds can be produced, resulting in a greater return on investment (ROI) and a lower carbon footprint.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ani13193132/s1, Figure S1: Forest plot of the effect of organic trace mineral supplementation on feed intake (g/day/hen) of laying hens; Figure S2: Forest plot of the effect of organic trace mineral supplementation on hen-day production (%) of laying hens; Figure S3: Forest plot of the effect of organic trace mineral supplementation on FCR (g feed/kg egg) of laying hens; Figure S4: Forest plot of the effect of organic trace mineral supplementation on FCR (g feed/dozen egg) of laying hens; Figure S5: Forest plot of the effect of organic trace mineral supplementation on egg mass (g/hen/day) of laying hens; Figure S6: Forest plot of the effect of organic trace mineral supplementation on egg weight (g) of laying hens; Figure S7: Forest plot of the effect of organic trace mineral supplementation on egg loss (%) of laying hens; Figure S8: Forest plot of the effect of organic trace mineral supplementation on eggshell thickness (mm) of laying hens; Figure S9: Forest plot of the effect of organic trace mineral supplementation on eggshell strength (kgf) of laying hens; Figure S10: Forest plot of the effect of organic trace mineral supplementation on eggshell weight (g) of laying hens; Figure S11: Forest plot of the effect of organic trace mineral supplementation on eggshell percentage (%) of laying hens; Figure S12: Forest plot of the effect of organic trace mineral supplementation on Haugh unit of laying hens; Table S1: Data describing production characteristics and laying performance of baseline and organic trace mineral (OTM) scenarios; Table S2: Ingredient composition of formulated low- and high-soybean-meal (SBM) diets in different laying phases; Table S3: Summary of daily feed intake, crude protein content, and estimated global warming potential (GWP) of formulated low- and high-soybean-meal (SBM) diets.

Author Contributions

Conceptualisation, L.B., S.R., J.T.-P. and R.M.; formal analysis, L.B. and S.R.; data curation, L.B.; data curation (LCA), S.R.; writing—original draft preparation, L.B.; writing—review and editing, R.M.; supervision, J.T.-P. and R.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

All data and related tables generated during this meta-analysis are included in the published review and its Supplementary Information files. The review was not registered previously. The review protocol followed previous meta-analysis publications and was not prepared for external accession.

Acknowledgments

Sincere thanks to Alltech Inc. for providing the resources and facilities to complete this work.

Conflicts of Interest

Authors are employed by Alltech Inc., a manufacturer of Bioplex proteinates.

Abbreviations

CFPCarbon Footprint
CMAComprehensive Meta-Analysis
CuCopper
CIConfidence Interval
DEFRADepartment for Environment, Food and Rural Affairs
FCRFeed Conversion Ratio
FeIron
GHGGreenhouse Gas
GWPGlobal Warming Potential
HDPHen-Day Production
IPCCIntergovernmental Panel on Climate Change
ITMInorganic Trace Minerals
LCALife Cycle Assessment
MDMean difference
MnManganese
OTMOrganic Trace Minerals
PRPartial Replacement
PRISMA Preferred Reporting Items for Systematic Reviews and Meta-Analyses
RBVRelative Bioavailability
RMDRaw Mean Difference
ROIReturn On Investment
SBMSoybean Meal
SDStandard Deviation
SMDStandardised Mean Difference
TRTotal Replacement
ZnZinc

References

  1. Ao, T.; Pierce, J. The replacement of inorganic mineral salts with mineral proteinates in poultry diets. World’s Poult. Sci. J. 2013, 69, 5–16. [Google Scholar] [CrossRef]
  2. Kong, J.; Qiu, T.; Yan, X.; Wang, L.; Chen, Z.; Xiao, G.; Feng, X.; Zhang, H. Effect of replacing inorganic minerals with small peptide chelated minerals on production performance, some biochemical parameters and antioxidant status in broiler chickens. Front. Physiol. 2022, 13, 1027834. [Google Scholar] [CrossRef] [PubMed]
  3. Zafar, M.H.; Fatima, M. Efficiency Comparison of Organic and Inorganic Minerals in Poultry Nutrition: A Review. PSM Vet. Res. 2018, 3, 53–59. [Google Scholar]
  4. Brugger, D.; Windisch, W.M. Environmental responsibilities of livestock feeding using trace mineral supplements. Anim. Nutr. 2015, 1, 113–118. [Google Scholar] [CrossRef] [PubMed]
  5. Bao, Y.M.; Choct, M. Trace mineral nutrition for broiler chickens and prospects of application of organically complexed trace minerals: A review. Anim. Prod. Sci. 2009, 49, 269–282. [Google Scholar] [CrossRef]
  6. Bhagwat, V.G.; Balamurugan, E.; Rangesh, P. Cocktail of chelated minerals and phytogenic feed additives in the poultry industry: A review. Vet. World 2021, 14, 364–371. [Google Scholar] [CrossRef]
  7. Santos, V.L.; Silva, J.B.d.; Figueiredo, F.C.d.; Ronchi, C.P.H.; Lecznieski, J. Total Replacement of Inorganic Minerals with Organic Ones Improves the Productive Performance of Broilers. Int. J. Poult. Sci. 2023, 22, 40–45. [Google Scholar] [CrossRef]
  8. Zhao, J.; Shirley, R.B.; Vazquez-Anon, M.; Dibner, J.J.; Richards, J.D.; Fisher, P.; Hampton, T.; Christensen, K.D.; Allard, J.P.; Giesen, A.F. Effects of chelated trace minerals on growth performance, breast meat yield, and footpad health in commercial meat broilers. J. Appl. Poult. Res. 2010, 19, 365–372. [Google Scholar] [CrossRef]
  9. Leeson, S.; Caston, L. Using minimal supplements of trace minerals as a method of reducing trace mineral content of poultry manure. Anim. Feed Sci. Technol. 2008, 142, 339–347. [Google Scholar] [CrossRef]
  10. Byrne, L.; Murphy, R.A. Relative Bioavailability of Trace Minerals in Production Animal Nutrition: A Review. Animals 2022, 12, 1981. [Google Scholar] [CrossRef]
  11. Byrne, L.; Hynes, M.J.; Connolly, C.D.; Murphy, R.A. Influence of the Chelation Process on the Stability of Organic Trace Mineral Supplements Used in Animal Nutrition. Animals 2021, 11, 1730. [Google Scholar] [CrossRef]
  12. Suttle, N.F. Mineral Nutrition of Livestock, 5th ed.; CAB International: Wallingford, UK, 2022. [Google Scholar]
  13. Kleyn, R.J.; Ciacciariello, M. Mineral nutrition in broilers: Where are we at? In Proceedings of the Arkansas Nutrition Conference, Rogers, AR, USA, 31 August–2 September 2021.
  14. de Vries, M.; de Boer, I.J.M. Comparing environmental impacts for livestock products: A review of life cycle assessments. Livest. Sci. 2010, 128, 1–11. [Google Scholar] [CrossRef]
  15. Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.G. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. BMJ 2009, 339, b2535. [Google Scholar] [CrossRef]
  16. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ 2021, 372, n71. [Google Scholar] [CrossRef]
  17. Page, M.J.; Moher, D.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. PRISMA 2020 explanation and elaboration: Updated guidance and exemplars for reporting systematic reviews. BMJ 2021, 372, n160. [Google Scholar] [CrossRef]
  18. Murakami, A.; Franco, J. Effect of Bioplex Poedeiras in diets fed layers on egg quality and stability during storage. In Proceedings of the Alltech 20th International Feed Industry Symposium, Lexington, KY, USA, 23–26 May 2004; Alltech Inc.: Nicholasville, KY, USA, 2004. [Google Scholar]
  19. Sara, A.; Odagiu, A.; Bentea, M.; Clapa, L. Effect of Eggshell 49™ in hens more than 49 wk of age on egg production and eggshell quality. In Proceedings of the Alltech 24th International Feed Industry Symposium, Lexington, KY, USA, 20–23 April 2008; Alltech Inc.: Nicholasville, KY, USA, 2008. [Google Scholar]
  20. Schäublin, H.; Wiedmer, H.; Zweifel, R.; Spring, P. Comparison of performance from laying hens fed diets with inorganic or organic trace minerals at reduced levels in floor systems. In Proceedings of the Alltech 24th International Feed Industry Symposium, Lexington, KY, USA, 20–23 April 2008; Alltech Inc.: Nicholasville, KY, USA, 2008. [Google Scholar]
  21. Nunes, J.; Rossi, P.; Rocha, A.; Anciuti, M.; Maier, J.; Rutz, F. Performance of layers fed Bioplex® minerals. In Proceedings of the Alltech 23rd International Feed Industry Symposium, Lexington, KY, USA, 20–23 May 2007; Alltech Inc.: Nicholasville, KY, USA, 2007. [Google Scholar]
  22. MacIsaac, J.; Anderson, D.; Butt, S.; Rathgeber, B. Evaluation of a mineral chelate for late-cycle laying hens. Poult. Sci. 2006, 85 (Suppl. S1), 63. [Google Scholar]
  23. Güçlü, B.K.; Kara, K.; Beyaz, L.; Uyanik, F.; Eren, M.; Atasever, A. Influence of dietary copper proteinate on performance, selected biochemical parameters, lipid peroxidation, liver, and egg copper content in laying hens. Biol. Trace Elem. Res. 2008, 125, 160–169. [Google Scholar] [CrossRef] [PubMed]
  24. Leeson, S.; Sefton, A.; Jacques, K. Layer excreta mineral content: Bioplex® versus inorganic dietary trace mineral sources. Poult. Sci. 2010, 659 (Suppl. S1). [Google Scholar]
  25. Sefton, A.; Leeson, S. Mineral content of excreta and eggs from laying hens fed Bioplex® or inorganic minerals. In Proceedings of the Alltech 27th International Feed Industry Symposium, Lexington, KY, USA, 22–25 May 2011; Alltech Inc.: Nicholasville, KY, USA, 2011. [Google Scholar]
  26. Ao, T.; Pierce, J.; Pescatore, A.; Cantor, A.; Paul, M.; Ford, M. Effects of supplementing different forms and levels of trace minerals in layer diet on the efficacy of phytase. In Proceedings of the 24th World’s Poultry Congress, Salvador, Bahia, Brazil, 5–9 August 2012. [Google Scholar]
  27. Revell, D.; Zarrinkalam, M.; Hughes, R. Iron content of eggs from hens given diets containing organic forms of iron, serine and methyl group donors, or phytoestogens. Br. Poult. Sci. 2009, 50, 536–542. [Google Scholar] [CrossRef]
  28. Stefanello, C.; Santos, T.; Murakami, A.; Martins, E.; Carneiro, T. Productive performance, eggshell quality, and eggshell ultrastructure of laying hens fed diets supplemented with organic trace minerals. Poult. Sci. 2014, 93, 104–113. [Google Scholar] [CrossRef]
  29. Nolan, L.W. Evaluation of Current and Emerging Techniques for Measuring Eggshell Integrity of the Domestic Fowl. Ph.D. Dissertation, University of Kentucky, Lexington, KY, USA, 2019. [Google Scholar]
  30. Ceylan, N.; Scheideler, S.E. Effects of the eggshell-49, dietary calcium level and hen age on performance and egg shell quality. In Proceedings of Biotechnology in the Feed Industry. In Proceedings of the Alltech’s 15th Annual Symposium, Lexington, KY, USA, 17–20 May 2015; University Press Nottingham: Nottingham, UK, 2015; pp. 61–73. [Google Scholar]
  31. Carlos, F.; Solano, A. Evaluation of Bioplex® Layer in Hy-Line Brown hens, at two different ages, from week 23 to 37 and from week 54 to 68 of age. In Proceedings of the Alltech 21st International Feed Industry Symposium, Lexington, KY, USA, 22–25 May 2005; Alltech Inc.: Nicholasville, KY, USA, 2005. [Google Scholar]
  32. Boruta, A.; Swierczewska, E.; Glebocka, K.; Nollet, L. Trace organic minerals as a replacement of inorganic sources for layers: Effects on productivity and mineral excretion. Rev. Científica Eletrônica Med. Veterinária 2007, 13, 491–494. [Google Scholar]
  33. Siske, V.; Zeman, L.; Klecker, D. The egg shell: A case study in improving quality by altering mineral metabolism—Naturally. In Proceedings of Alltech’s 16th Annual Symposium, The Future of Food; Lyons, T.P., Jacques, K.A., Eds.; Nottingham University Press: Nottingham, UK, 2000; pp. 327–346. [Google Scholar]
  34. Xavier, G.; Rutz, F.; Dionello, N.; Goncalves, F.; Zauk, N.; Ribeiro, C. Performance of layers fed diets containing organic selenium, zinc and manganese, during a second cycle of production. In Proceedings of the Alltech 20th International Feed Industry Symposium, Lexington, KY, USA, 23–26 May 2004; Alltech Inc.: Nicholasville, KY, USA, 2004. [Google Scholar]
  35. Ao, T.; Paul, M.; Macalintal, L.; Pescatore, A.; Cantor, A.; Samuel, R.; Ford, M.; Dawson, K. Total replacement of inorganic microminerals with reduced levels of proteinates in laying hen diets: Impact on productive performance, egg characteristics and bone quality. Poult. Sci. 2016, 95 (Suppl. S1), 156. [Google Scholar]
  36. Ao, T.; Pescatore, A.; Paul, M.; Nolan, L.; Macalintal, L.; Ford, M.; Dawson, K. Impact of replacing inorganic trace minerals with reduced levels of proteinates in laying hen diets with or without phytase on the performance and egg shell quality of layers in a single lay cycle. In Proceedings of the Poultry Science Forum, Georgia World Congress Center, Atlanta, GA, USA, 29–30 January 2018. [Google Scholar]
  37. Qiu, J.; Lu, X.; Ma, L.; Hou, C.; He, J.; Liu, B.; Yu, D.; Lin, G.; Xu, J. Low-dose of organic trace minerals reduced fecal mineral excretion without compromising performance of laying hens. Asian Australas. J. Anim. Sci. 2020, 33, 588. [Google Scholar] [CrossRef] [PubMed]
  38. Yıldız, A.; Cufadar, Y.; Olgun, O. Effects of dietary organic and inorganic manganese supplementation on performance, egg quality and bone mineralisation in laying hens. Rev. Med. Vet. 2011, 162, 482–488. [Google Scholar]
  39. Idowu, O.; Ajuwon, R.; Oso, A.; Akinloye, O. Effects of zinc supplementation on laying performance, serum chemistry and Zn residue in tibia bone, liver, excreta and egg shell of laying hens. Int. J. Poult. Sci. 2011, 10, 225–230. [Google Scholar] [CrossRef]
  40. Idowu, O.; Laniyan, T.; Kuye, O.; Oladele-Ojo, V.; Eruvbetine, D. Effect of copper salts on performance, cholesterol, residues in liver, eggs and excreta of laying hens. Arch. Zootec. 2006, 55, 327–338. [Google Scholar]
  41. Venglovska, K.; Gresakova, L.; Placha, I.; Ryzner, M.; Cobanova, K. Effects of feed supplementation with manganese from its different sources on performance and egg parameters of laying hens. Czech J. Anim. Sci 2014, 59, 147–155. [Google Scholar] [CrossRef]
  42. Torki, M.; Akbari, M.; Kaviani, K. Single and combined effects of zinc and cinnamon essential oil in diet on productive performance, egg quality traits, and blood parameters of laying hens reared under cold stress condition. Int. J. Biometeorol. 2015, 59, 1169–1177. [Google Scholar] [CrossRef]
  43. Li, L.; Zhang, N.; Gong, Y.; Zhou, M.; Zhan, H.; Zou, X. Effects of dietary Mn-methionine supplementation on the egg quality of laying hens. Poult. Sci. 2018, 97, 247–254. [Google Scholar] [CrossRef]
  44. Stringhini, J.; Santos, B.; Tanure, C.; Oliveira, E.; Castejon, F.; Moreira, J.; Navas, T. Eggshell Quality of Commercial Laying Hens Fed Diets Containing Inorganic or Chelated Micro minerals from 60 to 80 Weeks of Age. In Proceedings of the XXII European Symposium on the Quality of Poultry Meat and the XVI European Symposium on the Quality of Eggs and Egg Products, Nantes, France, 11–13 May 2015. [Google Scholar]
  45. Kocher, A.; Kumar, A.; Nicholson, S.; Tiller, T. Use of commercial premixes with low levels of organic trace minerals on egg production performance, and egg shell characteristics in layers. In Proceedings of the 31st Annual Australian Poultry Science Symposium, Sydney, NSW, Australia, 16–19 February 2020; p. 17. [Google Scholar]
  46. Fernandes, J.; Murakami, A.; Sakamoto, M.; Souza, L.; Malaguido, A.; Martins, E. Effects of organic mineral dietary supplementation on production performance and egg quality of white layers. Braz. J. Poult. Sci. 2008, 10, 59–65. [Google Scholar] [CrossRef]
  47. Borenstein, M.; Hedges, L.; Higgins, J.; Rothstein, H. Introduction to Meta-Analysis; John Wiley & Sons: Hoboken, NJ, USA, 2021. [Google Scholar] [CrossRef]
  48. Higgins, J.P.T.; Thompson, S.G.; Deeks, J.J.; Altman, D.G. Measuring inconsistency in meta-analyses. BMJ 2003, 327, 557–560. [Google Scholar] [CrossRef] [PubMed]
  49. Egger, M.; Smith, G.D.; Schneider, M.; Minder, C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997, 315, 629–634. [Google Scholar] [CrossRef] [PubMed]
  50. Wiedemann, S.G.; McGahan, E.J. Environmental Assessment of an Egg Production Supply Chain Using Life Cycle Assessment; Australian Egg Corporation Limited: Sydney, Australia, 2011. [Google Scholar]
  51. Leinonen, I.; Williams, A.G.; Wiseman, J.; Guy, J.; Kyriazakis, I. Predicting the environmental impacts of chicken systems in the United Kingdom through a life cycle assessment: Egg production systems. Poult. Sci. 2012, 91, 26–40. [Google Scholar] [CrossRef] [PubMed]
  52. Tallentire, C.W.; Mackenzie, S.G.; Kyriazakis, I. Environmental impact trade-offs in diet formulation for broiler production systems in the UK and USA. Agric. Syst. 2017, 154, 145–156. [Google Scholar] [CrossRef]
  53. Salami, S.A.; Ross, S.A.; Patsiogiannis, A.; Moran, C.A.; Taylor-Pickard, J. Performance and environmental impact of egg production in response to dietary supplementation of mannan oligosaccharide in laying hens: A meta-analysis. Poult. Sci. 2022, 101, 101745. [Google Scholar] [CrossRef]
  54. IPCC. 2006 IPCC Guidelines for National Greenhouse Gas Inventories; IGES: Kanagawa, Japan, 2006. [Google Scholar]
  55. Vellinga, T.V.; Blonk, H.; Marinussen, M.; van Zeist, W.-J.; Starmans, D. Methodology Used in FeedPrint: A Tool Quantifying Greenhouse Gas Emissions of Feed Production and Utilization; 2013. Wageningen UR Livestock Research, Wageningen, the Netherlands. Version 2020.00. Available online: http:/webapplicaties.wur.nl/software/feedprintNL/index.asp (accessed on 1 October 2022).
  56. DEFRA. UK Government GHG Conversion Factors for Company Reporting; DEFRA: Norwich, UK, 2020. [Google Scholar]
  57. DEFRA. The Fertiliser Manual (RB209); DEFRA: Norwich, UK, 2010. [Google Scholar]
  58. Hoxha, A.; Christensen, B. The Carbon Footprint of Fertiliser Production: Regional Reference Values; International Fertiliser Society: Colchester, UK, 2019. [Google Scholar]
  59. IPCC. Changes in atmospheric constituents and in radiative forcing. In Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the 4th Assessment Report of the Intergovernmental Panel on Climate Change; Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., Miller, H.L., Eds.; Cambridge University Press: Cambridge, UK; New York, NY, USA, 2007. [Google Scholar]
  60. Ao, T.; Pierce, J.; Pescatore, A.; Cantor, A.; Dawson, K.; Ford, M. Effects of feeding reduced levels of trace mineral proteinates (Bioplex (R)) to brown layer pullets during development. Poult. Sci. 2008, 87, 114–115. [Google Scholar]
  61. Ao, T.; Pierce, J.; Pescatore, A.; Cantor, A.; Dawson, K.; Ford, M. Effects of feeding reduced levels of organic minerals (Bioplex®) on the development of white layer pullets. Poult. Sci. 2009, 88, 197. [Google Scholar]
  62. Ao, T.; Pierce, J.L.; Pescatore, A.J.; Cantor, A.H.; Dawson, K.A.; Ford, M.J.; Paul, M. Effects of feeding different concentration and forms of zinc on the performance and tissue mineral status of broiler chicks. Br. Poult. Sci. 2011, 52, 466–471. [Google Scholar] [CrossRef]
  63. Samuel, R.S.; Ao, T.; Paul, M.A.; Ford, M.J.; Brennan, K.M.; Spry, M.L.; Pescatore, A.J.; Cantor, A.H.; Pierce, J.L. Early-life trace mineral nutrition affects growth performance and mineral deposition in broilers through 21 days. In Proceedings of the IPSF & IPPE, Atlanta, GA, USA, 24–26 January 2012; p. 53. [Google Scholar]
  64. Tavares, T.; Mourão, J.L.; Kay, Z.; Spring, P.; Vieira, J.; Gomes, A.; Vieira-Pinto, M. The effect of replacing inorganic trace minerals with organic Bioplex® and Sel-Plex® on the performance and meat quality of broilers. J. Appl. Anim. Nutr. 2013, 2, e10. [Google Scholar] [CrossRef]
  65. Wang, G.; Liu, L.J.; Tao, W.J.; Xiao, Z.P.; Pei, X.; Liu, B.J.; Wang, M.Q.; Lin, G.; Ao, T.Y. Effects of replacing inorganic trace minerals with organic trace minerals on the production performance, blood profiles, and antioxidant status of broiler breeders. Poult. Sci. 2019, 98, 2888–2895. [Google Scholar] [CrossRef]
  66. Nollet, L.; van der Klis, J.D.; Lensing, M.; Spring, P. The Effect of Replacing Inorganic With Organic Trace Minerals in Broiler Diets on Productive Performance and Mineral Excretion. J. Appl. Poult. Res. 2007, 16, 592–597. [Google Scholar] [CrossRef]
  67. Vieira, R.; Ferket, P.; Malheiros, R.; Hannas, M.; Crivellari, R.; Moraes, V.; Elliott, S. Feeding low dietary levels of organic trace minerals improves broiler performance and reduces excretion of minerals in litter. Br. Poult. Sci. 2020, 61, 574–582. [Google Scholar] [CrossRef]
  68. Vieira, R.A.; Malheiros, R.; Albino, L.F.T.; Hannas, M.I.; Crivellari, R.; Borges, L.L.; Ferket, P. Replacing dietary inorganic trace minerals with lower concentrations of organic trace minerals can improve broiler performance. Poult. Sci. 2014, 93 (Suppl. S1). [Google Scholar]
  69. Vieira, R.A.; Ribeiro, V.; de Araujo, W.A.G.; Salquero, S.C.; Teixeira Albino, L.F.; Hannas, M.I. The effects of chelated, organic trace minerals and selenium yeast on broiler performance. J. Poult. Sci. 2013, 92. [Google Scholar]
  70. Doleman, B.; Freeman, S.C.; Lund, J.N.; Williams, J.P.; Sutton, A.J. Funnel plots may show asymmetry in the absence of publication bias with continuous outcomes dependent on baseline risk: Presentation of a new publication bias test. Res. Synth. Methods 2020, 11, 522–534. [Google Scholar] [CrossRef] [PubMed]
  71. Anestis, V.; Papanastasiou, D.K.; Bartzanas, T.; Giannenas, I.; Skoufos, I.; Kittas, C. Effect of a dietary modification for fattening pigs on the environmental performance of commercial pig production in Greece. Sustain. Prod. Consum. 2020, 22, 162–176. [Google Scholar] [CrossRef]
  72. Giannenas, I.; Bonos, E.; Anestis, V.; Filioussis, G.; Papanastasiou, D.K.; Bartzanas, T.; Papaioannou, N.; Tzora, A.; Skoufos, I. Effects of Protease Addition and Replacement of Soybean Meal by Corn Gluten Meal on the Growth of Broilers and on the Environmental Performances of a Broiler Production System in Greece. PLoS ONE 2017, 12, e0169511. [Google Scholar] [CrossRef]
Animals 13 03132 g001
Figure 1. PRISMA flow diagram describing the literature search strategy and study selection for the meta-analysis.
Figure 1. PRISMA flow diagram describing the literature search strategy and study selection for the meta-analysis.
Animals 13 03132 g001
Animals 13 03132 g002
Figure 2. The structure and system boundary of the egg production system considered in the life cycle assessment (adapted from Salami et al., 2022 [53]).
Figure 2. The structure and system boundary of the egg production system considered in the life cycle assessment (adapted from Salami et al., 2022 [53]).
Animals 13 03132 g002
Animals 13 03132 g003
Figure 3. Funnel plots of standardised mean differences against their inverse standard errors and the associated significance (p-value for Egger’s test) for testing the publication bias of studies included in the meta-analysis for production performance parameters: feed intake, hen-day production, and feed conversion ratio. Open circles represent individual study comparisons included in the meta-analysis.
Figure 3. Funnel plots of standardised mean differences against their inverse standard errors and the associated significance (p-value for Egger’s test) for testing the publication bias of studies included in the meta-analysis for production performance parameters: feed intake, hen-day production, and feed conversion ratio. Open circles represent individual study comparisons included in the meta-analysis.
Animals 13 03132 g003
Animals 13 03132 g004
Figure 4. Funnel plots of standardised mean differences against their inverse standard errors and the associated significance (p-value for Egger’s test) for testing the publication bias of studies included in the meta-analysis for egg quality traits: egg mass, egg weight, egg loss, eggshell thickness, eggshell strength, eggshell weight, and eggshell percentage. Open circles represent individual study comparisons included in the meta-analysis.
Figure 4. Funnel plots of standardised mean differences against their inverse standard errors and the associated significance (p-value for Egger’s test) for testing the publication bias of studies included in the meta-analysis for egg quality traits: egg mass, egg weight, egg loss, eggshell thickness, eggshell strength, eggshell weight, and eggshell percentage. Open circles represent individual study comparisons included in the meta-analysis.
Animals 13 03132 g004
Table 1. Overview of studies included in the meta-analysis to evaluate the effects of supplementing organic trace minerals (Bioplex Cu, Fe, Mn, and Zn) in the diets of laying hens.
Table 1. Overview of studies included in the meta-analysis to evaluate the effects of supplementing organic trace minerals (Bioplex Cu, Fe, Mn, and Zn) in the diets of laying hens.
ReferenceStudy LocationBreed/StrainAge of Hens (wk)Number of Hens per TreatmentTreatment Comparison 1Supplementary OTM/ITMStudy
Duration (wk)
Murakami and Franco [18]BrazilLohmann32160BasalZn, Mn20
Sara, Odagiu [19]RomaniaRoso SL hybrid4978BasalZn, Mn, Cu23
Schäublin, Wiedmer [20]Switzerland-211872TRCu, Fe, Mn, Zn60
Nunes, Rossi [21]BrazilHisex Brown3064TRZn, Mn, Cu, Fe12
MacIsaac, Anderson [22]CanadaWhite Leghorn5572BasalZn, Mn, Cu, Fe12
Güçlü, Kara [23]TurkeyBovans3018BasalCu4
Leeson, Sefton [24]CanadaLohmann18360TRZn, Mn, Cu52
Sefton and Leeson [25]CanadaLohmann3636TRZn, Mn, Cu, Fe6.6
Ao, Pierce [26]USAHy-Line Brown1696TRZn, Mn, Cu, Fe44
Revell, Zarrinkalam [27]AustraliaHisex Brown3412Basal, TRFe6
Stefanello, Santos [28]BrazilHy-Line W364740Basal, TRZn, Mn, Cu15
Nolan [29]USAHy-Line W36 and Hy-Line Brown2948Basal, TRZn36
Ceylan and Scheideler [30]USAHy-Line W362036BasalZn, Mn40
Carlos and Solano [31] (trial 1)PeruHy-Line274000PRZn, Mn, Cu, Fe10
Carlos and Solano [31] (trial 2)PeruHy-Line543525PRZn, Mn, Cu, Fe14
Boruta, Swierczewska [32]PolandHy-Line3048PRZn, Mn, Cu, Fe40
Siske, Zeman [33] (trial 1)Czech RepublicIsa Brown17213PRZn, Mn50
Siske, Zeman [33] (trial 2)Czech RepublicIsa Brown17160PRZn, Mn55
Siske, Zeman [33] (trial 3)Czech RepublicIsa Brown53320BasalZn, Mn, Cu19
Xavier, Rutz [34]BrazilIsa Brown7764BasalZn, Mn24
Ao, Paul [35]USAHy-Line W361784TRZn, Mn, Cu, Fe53
Ao, Pescatore [36] 2USAHy-Line Brown-120TRZn, Mn, Cu, Fe80
Qiu, Lu [37]ChinaHy-Line White50135TRZn, Mn, Cu, Fe8
Yıldız, Cufadar [38]TurkeyH&N Brown Nick4915TRMn12
Idowu, Ajuwon [39] 2NigeriaBrown Yaffa-60Basal, TRZn10
Idowu, Laniyan [40]NigeriaBlack Harco3030Basal, TRCu10
Venglovska, Gresakova [41]SlovakiaLohmann Brown2324Basal, TRMn8
Torki, Akbari [42]IranLohmann LSL-Lite4230BasalZn8
Li, Zhang [43]ChinaJinghong-15396TRMn10
Stringhini, Santos [44]BrazilBovans White6096PR, TRZn, Mn, Cu, Fe20
Kocher, Kumar [45]AustraliaIsa Brown6470TRZn, Mn, Cu, Fe30
Fernandes, Murakami [46]BrazilHy-Line W366764BasalZn, Mn 16
OTM: organic trace minerals (Bioplex Zn, Mn, Cu, and Fe); ITM: inorganic trace minerals. 1 Treatment comparison: Basal represents comparison of basal diets (conventional diets) vs. basal diets + supplementary OTM; PR (partial replacement) represents comparison of basal diets + supplementary ITM vs. basal diets + partial replacement of supplementary ITM with OTM; TR (total replacement) represents comparison of basal diets + supplementary ITM vs. basal diets + total replacement of supplementary ITM with OTM. 2 Hens used in these trials were at the point of laying/start of egg production, which is usually between 15 and 18 weeks of age.
Table 2. Trace mineral concentration supplemented in layer diets of treatment comparisons involving total replacement of inorganic trace minerals (ITM) with organic trace minerals (OTM; Bioplex Cu, Fe, Mn, and Zn).
Table 2. Trace mineral concentration supplemented in layer diets of treatment comparisons involving total replacement of inorganic trace minerals (ITM) with organic trace minerals (OTM; Bioplex Cu, Fe, Mn, and Zn).
Trace MineralITM Treatments (mg/kg)OTM Treatments (mg/kg)
MeanMinimumMaximumSDMeanMinimumMaximumSD
Zn77.712.5140.038.353.910.0140.044.4
Mn61.415.0125.029.945.810.0125.029.2
Cu38.41.3250.073.027.10.6150.050.9
Fe70.611.3450.0104.245.02.5450.0108.6
SD: standard deviation.
Table 3. Descriptive statistics of productive performance and egg quality traits included in the meta-analysis.
Table 3. Descriptive statistics of productive performance and egg quality traits included in the meta-analysis.
ItemNMeanMinimumMaximumSD
Productive performance
Feed intake (g/day/hen)71114.9180.43145.0012.09
Hen-day production (%)9284.2266.2998.117.09
FCR (g feed/kg egg)632117.481480.004300.00509.13
FCR (g feed/dozen eggs)421813.211120.03450.00544.74
Egg quality
Egg mass (g/hen/day)4557.5945.4663.774.46
Egg weight (g)8764.7156.5168.913.06
Egg loss (%)491.270.224.730.91
Eggshell thickness (mm)430.350.110.500.08
Eggshell strength (kgf)583.722.534.490.52
Eggshell weight (g)418.455.479.771.65
Eggshell percentage (%)438.606.8114.601.15
Haugh unit 4079.2039.2798.5212.10
N: number of comparisons; SD: standard deviation.
Table 4. Overall pooled effect size of productive performance and egg quality traits when dietary organic trace minerals (Bioplex Cu, Fe, Mn, and Zn) were supplemented either in basal diets, partial replacement for inorganic trace minerals (ITM), or total replacement for ITM.
Table 4. Overall pooled effect size of productive performance and egg quality traits when dietary organic trace minerals (Bioplex Cu, Fe, Mn, and Zn) were supplemented either in basal diets, partial replacement for inorganic trace minerals (ITM), or total replacement for ITM.
Item Effect Size EstimatesHeterogeneity Tests
NControl Mean (SD)RMD (95% CI)SEp-ValueI2 (%)p-Value
Productive performance
Feed intake (g/day/hen)71115.06 (11.45)−0.66 (−2.23, 0.91)0.800.41299.98<0.001
Hen-day production (%)9283.63 (7.91)2.07 (1.83, 2.31)0.12<0.00199.67<0.001
FCR (g feed/kg egg)632143.73 (606.45)−51.28 (−75.39, −27.18)12.30<0.00198.50<0.001
FCR (g feed/dozen eggs)421869.21 (570.15)−22.82 (−39.42, −6.23)8.470.00780.89<0.001
Egg quality
Egg mass (g/hen/day)4557.13 (4.41)0.50 (0.13, 0.88)0.190.00879.25<0.001
Egg weight (g)8764.41 (2.73)0.48 (0.20, 0.77)0.150.00189.29<0.001
Egg loss (%)491.58 (1.04)−0.62 (−0.73, −0.51)0.06<0.00198.65<0.001
Eggshell thickness (mm)430.34 (0.08)0.01 (0.01, 0.02)0.00<0.00197.06<0.001
Eggshell strength (kgf)583.65 (0.49)0.14 (0.07, 0.21)0.04<0.00194.28<0.001
Eggshell weight (g)418.37 (1.71)0.20 (0.12, 0.27)0.04<0.00183.36<0.001
Eggshell percentage (%)438.53 (1.09)0.15 (0.07, 0.22)0.04<0.00195.58<0.001
Haugh unit4078.86 (12.75)0.89 (0.49, 1.29)0.20<0.00189.73<0.001
N: number of comparisons; SD standard deviation; RMD: raw mean difference and its associated 95% confidence interval; SE: standard error. I2: percentage of variation and associated significance level (p-value) of chi-squared statistic.
Table 5. Effect size of productive performance and egg quality traits when dietary organic trace minerals (Bioplex Cu, Fe, Mn, and Zn) were supplemented in basal diets.
Table 5. Effect size of productive performance and egg quality traits when dietary organic trace minerals (Bioplex Cu, Fe, Mn, and Zn) were supplemented in basal diets.
Item Effect Size EstimatesHeterogeneity Tests
NControl Mean (SD)RMD (95% CI)SEp-ValueI2 (%)p-Value
Productive performance
Feed intake (g/day/hen)17108.12 (13.59)−2.12 (−5.66, 1.42)1.810.24199.21<0.001
Hen-day production (%)2879.63 (7.82)3.09 (0.55, 5.63)1.300.01799.19<0.001
FCR (g feed/kg egg)202011.40 (600.67)−9.82 (−67.66, 48.03)29.510.73994.85<0.001
FCR (g feed/dozen eggs)141811.21 (539.64)−62.68 (−126.21, 0.84)32.410.05383.55<0.001
Egg quality
Egg mass (g/hen/day)953.50 (4.67)0.69 (−0.35, 1.74)0.530.19386.20<0.001
Egg weight (g)2563.52 (3.42)0.25 (−0.45, 0.94)0.350.48693.37<0.001
Egg loss (%)92.13 (1.26)−1.07 (−1.56, −0.59)0.25<0.00199.10<0.001
Eggshell thickness (mm)160.35 (0.08)0.02 (0.01, 0.03)0.01<0.00198.62<0.001
Eggshell strength (kgf)103.38 (0.31)0.11 (−0.09, 0.32)0.100.27293.35<0.001
Eggshell weight (g)56.89 (1.71)0.69 (0.29, 1.10)0.210.00196.12<0.001
Eggshell percentage (%)178.58 (1.43)0.27 (0.09, 0.44)0.090.00397.00<0.001
Haugh unit1781.77 (10.12)1.35 (0.52, 2.17)0.420.00179.43<0.001
N: number of comparisons; SD standard deviation; RMD: raw mean difference and its associated 95% confidence interval; SE: standard error; I2: percentage of variation and associated significance level (p-value) of chi-squared statistic.
Table 6. Effect size of productive performance and egg quality traits when dietary organic trace minerals (Bioplex Cu, Fe, Mn, and Zn) were supplemented as total replacement for inorganic trace minerals.
Table 6. Effect size of productive performance and egg quality traits when dietary organic trace minerals (Bioplex Cu, Fe, Mn, and Zn) were supplemented as total replacement for inorganic trace minerals.
Item Effect Size EstimatesHeterogeneity Tests
NControl Mean (SD)RMD (95% CI)SEp-ValueI2 (%)p-Value
Productive performance
Feed intake (g/day/hen)51116.76 (9.93)−0.05 (−1.91, 1.82)0.950.96399.99<0.001
Hen-day production (%)5785.06 (7.62)1.52 (1.16, 1.88)0.18<0.00199.71<0.001
FCR (g feed/kg egg)412201.44 (620.89)−73.09 (−107.24, −38.94)17.42<0.00198.82<0.001
FCR (g feed/dozen eggs)251865.60 (619.92)−19.32 (−37.14, −1.49)9.100.03481.12<0.001
Egg quality
Egg mass (g/hen/day)3658.04 (3.91)0.50 (0.09, 0.90)0.210.01776.07<0.001
Egg weight (g)5364.81 (2.47)0.76 (0.43, 1.08)0.17<0.00184.82<0.001
Egg loss (%)331.38 (0.91)−0.57 (−0.75, −0.40)0.09<0.00197.42<0.001
Eggshell thickness (mm)210.32 (0.09)0.01 (0.01, 0.02)0.00<0.00192.77<0.001
Eggshell strength (kgf)433.76 (0.51)0.15 (0.07, 0.24)0.04<0.00194.92<0.001
Eggshell weight (g)328.89 (1.43)0.11 (0.06, 0.16)0.03<0.0014.340.397
Eggshell percentage (%)258.46 (0.82)0.07 (−0.01, 0.143)0.040.07093.81<0.001
Haugh unit2376.70 (14.22)0.52 (0.10, 0.95)0.220.01688.60<0.001
N: number of comparisons; SD standard deviation; RMD: raw mean difference and its associated 95% confidence interval; SE: standard error; I2: percentage of variation and associated significance level (p-value) of chi-squared statistic.
Table 7. Meta-regression of the effects of study factors on the overall pooled effect size of productive performance (feed intake, hen-day production, and feed conversion ratio) in response to supplementary organic trace minerals (Bioplex Cu, Fe, Mn, and Zn).
Table 7. Meta-regression of the effects of study factors on the overall pooled effect size of productive performance (feed intake, hen-day production, and feed conversion ratio) in response to supplementary organic trace minerals (Bioplex Cu, Fe, Mn, and Zn).
Study FactorsFeed Intake (g/day/hen)Hen-Day Production (%)Feed Conversion Ratio
(g feed/kg egg)
CoefficientSEp-ValueR2 (%) CoefficientSEp-ValueR2 (%) CoefficientSEp-ValueR2 (%)
Location
Africa−15.212.31<0.0011.07.400.41<0.00117.0−731.0038.45<0.00141.0
Europe−3.562.600.171−0.680.390.08232.6068.550.634
North America−2.232.790.424−0.550.450.22562.8429.400.033
Oceania------−46.4073.500.528
South America−2.012.140.347−0.710.380.063−30.5323.740.199
AsiaReferent 1 Referent 1 Referent 1
Year of study0.280.210.1701.0−0.180.02<0.0012.00.352.920.9040.0
Hen breed/strain
Black Harco−15.743.61<0.0012.09.240.43<0.00118.0---56.0
Bovans3.445.620.5414.110.76<0.001209.3567.270.002
Brown Yaffa−8.613.810.0246.420.78<0.001−637.9356.83<0.001
H&N Brown Nick3.202.940.277−1.040.680.12698.3350.130.050
Hisex Brown 4.554.460.3081.470.840.080---
Hy-Line−0.492.890.8650.860.370.022100.2548.990.041
Isa Brown---1.560.45<0.001−30.6858.200.598
Roso SL hybrid−0.476.840.9465.931.28<0.001---
White Leghorn---0.480.720.501---
LohmannReferent 1 Referent 1 Referent 1
Age of hens0.160.060.0041.0−0.050.01<0.0011.04.850.91<0.0010.0
Number of hens0.000.000.8640.0−0.000.00<0.0010.0−0.010.020.7000.0
Study duration0.030.050.5551.0−0.050.01<0.0011.06.241.39<0.0010.0
SE: standard error; R2: proportion of between-study variance (heterogeneity) explained by the study factors. 1 Study location and hen breed/strain were estimated by using Europe and Lohmann as the baseline, respectively.
Table 8. Meta-regression of the effects of study factors on the overall pooled effect size of egg quality traits (egg weight, egg loss and eggshell strength) in response to supplementary organic trace minerals (Bioplex Cu, Fe, Mn, and Zn).
Table 8. Meta-regression of the effects of study factors on the overall pooled effect size of egg quality traits (egg weight, egg loss and eggshell strength) in response to supplementary organic trace minerals (Bioplex Cu, Fe, Mn, and Zn).
Study FactorsEgg Weight (g)Egg Loss (%)Eggshell Strength (kgf)
CoefficientSEp-ValueR2 (%) CoefficientSEp-ValueR2 (%) CoefficientSEp-ValueR2 (%)
Location
Africa0.550.480.2480.0---0.0---5.0
Europe−0.740.460.110−0.270.150.083−0.130.110.225
North America−0.630.480.1880.300.410.466−0.340.09<0.001
Oceania0.351.340.796---−0.400.250.106
South America−0.540.440.2180.170.140.2160.010.100.893
AsiaReferent 1 Referent 1 Referent 1
Year of study−0.000.030.9060.0−0.020.010.1410.0−0.010.010.0870.0
Hen breed/strain
Black Harco−0.290.510.57444.0---20.0---10.0
Bovans−2.140.620.001------
Brown Yaffa2.890.56<0.001------
H&N Brown Nick1.110.480.0211.190.22<0.001---
Hy-Line−0.240.420.5651.400.23<0.001−0.190.080.012
Isa Brown0.360.480.4551.370.25<0.001−0.210.110.046
Jinghong0.090.760.908---−0.340.130.010
Roso SL hybrid0.151.140.896------
White Leghorn−0.000.620.998------
LohmannReferent 1 Referent 1 Referent 1
Age of hens−0.000.010.9460.00.000.010.4070.00.010.000.0141.0
Number of hens−0.000.000.5200.00.000.000.0278.0−0.000.000.5050.0
Study duration−0.020.010.0940.00.010.000.0240.0−0.010.000.0024.0
SE: standard error; R2: proportion of between-study variance (heterogeneity) explained by the study factors. 1 Study location and hen breed/strain were estimated by using Europe and Lohmann as the baseline, respectively.
Table 9. Effect of supplementing organic trace minerals (OTM; Bioplex Cu, Fe, Mn, and Zn) on the carbon footprint of egg production.
Table 9. Effect of supplementing organic trace minerals (OTM; Bioplex Cu, Fe, Mn, and Zn) on the carbon footprint of egg production.
Low-GWP Diet High-GWP Diet
Category/Functional UnitBaselineOTM% Change BaselineOTM% Change
Feed emission intensity
Emissions per dozen eggs
(kg CO2-eq/dozen eggs)		1.271.25−1.65%1.581.56−1.65%
Emissions per egg
(g CO2-eq/egg)		105.86104.10−1.65%131.80129.70−1.65%
Emissions per kg eggs
(kg CO2-eq/kg eggs)		1.631.59−2.40%2.031.98−2.40%
Total emission intensity
Emissions per dozen eggs
(kg CO2-eq/dozen eggs)		1.711.68−1.75%2.031.99−1.73%
Emissions per egg
(g CO2-eq/egg)		142.70140.20−1.75%168.90165.90−1.73%
Emissions per kg eggs
(kg CO2-eq/kg eggs)		2.192.14−2.50%2.602.53−2.48%
GWP: global warming potential.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Byrne, L.; Ross, S.; Taylor-Pickard, J.; Murphy, R. The Effect of Organic Trace Mineral Supplementation in the Form of Proteinates on Performance and Sustainability Parameters in Laying Hens: A Meta-Analysis. Animals 2023, 13, 3132. https://doi.org/10.3390/ani13193132

AMA Style

Byrne L, Ross S, Taylor-Pickard J, Murphy R. The Effect of Organic Trace Mineral Supplementation in the Form of Proteinates on Performance and Sustainability Parameters in Laying Hens: A Meta-Analysis. Animals. 2023; 13(19):3132. https://doi.org/10.3390/ani13193132

Chicago/Turabian Style

Byrne, Laurann, Stephen Ross, Jules Taylor-Pickard, and Richard Murphy. 2023. "The Effect of Organic Trace Mineral Supplementation in the Form of Proteinates on Performance and Sustainability Parameters in Laying Hens: A Meta-Analysis" Animals 13, no. 19: 3132. https://doi.org/10.3390/ani13193132

APA Style

Byrne, L., Ross, S., Taylor-Pickard, J., & Murphy, R. (2023). The Effect of Organic Trace Mineral Supplementation in the Form of Proteinates on Performance and Sustainability Parameters in Laying Hens: A Meta-Analysis. Animals, 13(19), 3132. https://doi.org/10.3390/ani13193132

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop