Home Meta-analysis of zinc feed additive on enhancement of semen quality, fertility and hatchability performance in breeder chickens
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Meta-analysis of zinc feed additive on enhancement of semen quality, fertility and hatchability performance in breeder chickens

  • Ifeanyichukwu Princewill Ogbuewu EMAIL logo and Christain Anayo Mbajiorgu
Published/Copyright: August 3, 2022

Abstract

The incorporation of zinc in the diets of breeding chickens to enhance reproductive performance has been highlighted. However, no consensus has been reached on the effect of dietary zinc supplementation on the reproductive outcomes of breeding chickens. Therefore, the current study assessed the effects of dietary zinc supplementation on semen quality, fertility and hatchability percentage of breeding chickens using meta-analysis. Furthermore, subgroup analysis was also used to assess the effect of zinc sources (organic versus inorganic) on the reproductive outcomes of breeding chickens. A systematic search conducted on four electronic databases following the Preferred Reporting Items for Systematic Reviews and Meta-analyses yielded 521 candidate studies; 8 of the 521 studies that examined the effects of zinc supplementation on reproductive outcomes of breeding chickens met the selection criteria and were used for the meta-analysis. Outcome measures were pooled using random-effects model and expressed as standardized mean difference (SMD) at a 95% confidence interval (CI) for each study. OpenMEE software was used for the analysis. The results indicate significant increase in semen output (SMD = 1.32 mL, 95% CI: 0.76, 1.89), sperm motility (SMD = 1.10 %, 95% CI: 0.81, 1.39), sperm concentration (SMD = 4.28 × 106/mL, 95% CI: 2.78, 5.79), live sperm percent (SMD = 0.96%, 95% CI: 0.69, 1.23) and significant reductions in percentage dead sperm (SMD = –2.80%; 95% CI: –3.43, –2.17), and abnormal sperm (SMD = –4.64%; 95% CI: –5.74, –3.53) when compared to controls, taking cognizance of heterogeneity. In contrast, zinc supplementation had no effect on fertility and hatchability percentage. The subgroup analysis results revealed that zinc sources influenced aspects of the reproductive outcomes of breeding chickens. We conclude that dietary zinc supplementation had a positive influence on reproductive outcomes of breeding chickens, but did not affect percentage fertility and hatchability.

1 Introduction

The fertility status of the breeder cocks is critical to the success of the chicken enterprise. The influence of dietary mineral supplementation on the fertility status of chicken has been reported [1,2,3,4]. The effect of zinc, one such mineral in chicken reproduction, has been documented [5]. Zinc is a key part of numerous enzymes in animals. Chicken cannot store zinc; thus, it must be provided via the diet. In chickens, tissue zinc distribution is highly controlled and its toxicity rarely occurs [6].

Avian sperm contain a considerable amount of zinc in its membrane, which is an integral part of the antioxidant system that helps to counteract the harmful effects of free radicals produced by the sperm membrane [7]. Many studies have assessed the potential of zinc supplements on fertility markers in chickens with inconsistent results [1,2,3,8,9]. Evidence exists [9] that broiler breeder chickens fed diets supplemented with 150 mg ZnSO4/kg or a mixture of ZnAA and ZnSO4 at 75 mg/kg each had similar percentage fertility and hatchability compared to the control (without zinc supplementation). In contrast, increased percentage fertility (78–85%) and hatchability (68–73%) in breeders fed diets supplemented with zinc in the form of ZnO or zinc methionine at 152 mg/kg feed compared to the control has been reported [8]. The reasons for the observed disparity are not clear but could be attributed to dosage and source of zinc. It might also be a result of low statistical power due to the small number of chickens used in these studies. Thus, the meta-analytic method becomes a desirable choice, since it employs quantitative methods that enable the combination of results of individual studies addressing the same research question in statistical analysis to boost statistical strength and resolve conflicting findings.

Currently, there is no meta-analysis of the effect of diets with and without zinc supplementation on reproductive outcomes in breeder chickens. Therefore, this study is aimed at determining the effects of zinc and its source on the reproductive outcomes of breeding chickens using meta-analysis.

2 Materials and methods

2.1 Data source and paper selection criteria

The meta-analysis followed the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines. Studies on the responses of breeder chickens to diets with and without zinc supplementation were identified from a systematic search conducted in Google Scholar, ScienceDirect, PubMed and Scopus databases using the keywords: (i) chickens, (ii) zinc, (iii) semen quality, (iv) percentage hatchability and (v) percentage fertility. The references of all the studies retrieved were checked for related studies. Identified studies were independently reviewed by the authors and controversy was resolved by consensus. Inclusion criteria for the meta-analysis were (i) peer-reviewed studies published in English that evaluated the effect of dietary zinc supplements against control, (ii) studies conducted with chickens only, (iii) studies that reported means of the control and treatment group in at least one of the outcomes of interest, and (iv) studies that reported the number of chickens used in each experimental group. Reviews and studies not performed on chickens were excluded. Studies that fed zinc in combination with other feed additives were also removed from the analysis. Trials without quantitative data on any of the outcomes of interest were excluded.

  1. Ethical approval: The conducted research is not related to either human or animal use.

2.2 Data synthesis

Five hundred and twenty-one publications were identified from the systematic search performed on selected databases of which eight studies after screening met the inclusion criteria following the PRISMA procedure as presented in Figure 1. Information on the name of the first author, the year the article was published and the country of the study was extracted from control and zinc treatments. In addition, zinc source (organic vs inorganic), chicken age (18–66 weeks), duration of supplementation (5–25 weeks), dosage (1.2–100 mg/kg feed) and a number of birds per treatment group were extracted and used as covariates. Data on the mean and standard deviation (SD) of the control and zinc treatments were also extracted. Where a study reported standard error (SE) instead of SD, the SE value was converted to SD using the formula of Higgins and Deeks [10]: SD = SE × √n, where n is the number of chickens in each group. In studies with multiple treatment groups, the control means were compared to each treatment group.

Figure 1 
                  Flowchart of the article selection process for the meta-analysis.
Figure 1

Flowchart of the article selection process for the meta-analysis.

2.3 Statistical analysis

Statistical analysis was performed using the OpenMEE software [11] developed by Brown University USA. The effect size was pooled using random-effect model expressed as standardized mean difference (SMD) at 95% confidence interval (CI) [12,13]. Pooled results were displayed in forest plots with the points to the left side of the thick vertical line (SMD = 0) meaning a reduction in the outcome of interest, whereas the opposite was the case when it is the right. Pooled estimation was deemed significant when the lower and upper CIs do not include zero [14]. The mean effect sizes were categorized as 0.2 (low), 0.5 (medium) and > 0.8 (large). Q-Statistics [15] and I 2-statistics [16] were used to evaluate heterogeneity, and I 2-statistics was said to be significant at a 5% probability level. We conducted a restricted subgroup analysis to determine the influence of zinc sources on reproductive outcomes in breeder chickens. The relationships between treatment effect and covariates (age, dosage, duration of supplementation and Zn type) were performed using mixed effect meta-regression analysis and were considered significant at a 5% probability level.

3 Results

3.1 Characteristics of eligible studies

Eight studies satisfied the eligibility conditions and were added to our meta-analysis (Figure 1). The details of the eight studies used for the analysis are presented in Table 1. Among the 8 eligible studies, 3 were published before 2010, and others were published after 2010. Three studies were conducted in India, while one study each was performed in USA, Iraq, Egypt, Turkey and Italy.

Table 1

Characteristics of studies included in the analysis

Authors Location Light cycle Breed Covariates Number of birds Outcomes
Zinc source Age (week) Dose (mg/kg feed) DOS (week) Cont Expt
[17] India Dahlem red OZ 29 0, 100 8 10 10 2, 3, 4, 5, 6, 7
[18] Iraq 16 L:8D Cobb 500 IZ 66 0, 50 75, 100 22 9 9 1, 2, 3, 4, 5, 6
[19] Egypt 16 L:8D Inshas OZ 60 0, 100 21 3 9 1, 2, 3, 4, 5, 6, 7
[20] Italy 14 L:10D Cobb 500 OZ 18 0, 1.2 16 25 50 2, 3
[21] Turkey 16 L:8D IZ 62 0, 90 16 72 72 7, 8
[22] USA 16 L:8D Cobb 500 OZ/IZ 20 0, 3.2 25 192 192 7, 8
[23] India IZ 45 0, 2.5 5 10 10 7, 8
[24] India OZ 30 0, 100 5 72 144 1, 2

OZ – organic zinc; IZ – inorganic zinc; DOS – duration of supplementation; 1 – semen output; 2, – sperm motility; 3 – sperm concentration; 4 – Live sperm; 5 – dead sperm cell egg; 6 – abnormal sperm; 7 – fertility; 8 – hatchability.

3.2 Male reproductive markers

The analysis of 22 data sets with 209 breeder cocks indicated that zinc supplementation increased semen output when compared to the controls with a large SMD of 1.32 mL (95% CI: 0.76, 1.89; Figure 2). There was a high degree of heterogeneity in semen output estimate amongst studies included in the analysis (I 2-statistic = 80.88%; p <0.01; Figure 2). In addition, breeder cocks offered inorganic zinc had higher semen output than the controls (SMD = 1.53 mL, 95% CI: 0.94, 2.12; Table 2), while those on organic zinc treatment had similar semen output to the controls (SMD = 0.67 mL, 95% CI:–0.60, 1.94; Table 2). Meta-analysis of 20 data sets with 232 breeder cocks revealed that chickens on zinc treatment recorded higher sperm motility than chickens on the control (SMD = 1.10%, 95% CI: 0.81, 1.39; Figure 3). Sperm motility was significantly influenced when the analysis was disaggregated into organic zinc (SMD = 1.05%, 95% CI: 0.06, 2.04; Table 2) and inorganic zinc (SMD = 1.16%, 95% CI: 0.89, 1.43; Table 2) compared to the controls. Furthermore, the pooled effect size of 4 studies, 19 data sets, with 212 birds indicated that zinc supplementation improved sperm concentration when compared to the control (SMD = 4.28 × 106/mL, 95% CI: 2.78, 5.79; Figure 4). Sperm concentration differed from the controls when the analysis was partitioned based on zinc source (inorganic zinc: SMD = 5.58 × 106/mL, 95% CI: = 3.73, 7.43 and Organic zinc: SMD = 2.15 × 106/mL, 95% CI: = 0.26, 4.05: Table 2).

Figure 2 
                  Impact of dietary zinc additive on semen output. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in semen output, while points to the right depict an increase in semen output. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.
Figure 2

Impact of dietary zinc additive on semen output. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in semen output, while points to the right depict an increase in semen output. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.

Table 2

Effect of zinc source on reproductive markers in breeder chickens

Parameters SMD (95% CI)
Organic zinc Inorganic zinc
Semen output (mL) 0.67 (–0.60, 1.94) 1.53 (0.94, 2.12)
Sperm motility (%) 1.05 (0.06, 2.04) 1.16 (0.89, 1.43)
Sperm concentration (×106/mL) 2.15 (0.26, 4.05) 5.58 (3.73, 7.43)
Live sperm cell (%) 1.02 (0.49, 1.55) 0.94 (0.62, 1.27)
Dead sperm cell –5.05 (–7.55, –2.54) –4.54 (–5.95, 3.14)
Abnormal sperm (%) –2.05 (–2.84, –1.27) –3.18 (–4.03, –2.34)
Fertility rate (%) 0.34 (0.09, 0.59) –0.03 (–0.18, 0.11)
Hatchability (%) 0.29 (–0.02, 0.60) 0.03 (–0.08, 0.13)

SMD – standardized mean difference; CI – confidence interval.

Figure 3 
                  Impact of dietary zinc additive on sperm motility. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in sperm motility, while points to the right show an increase in sperm motility. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.
Figure 3

Impact of dietary zinc additive on sperm motility. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in sperm motility, while points to the right show an increase in sperm motility. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.

Figure 4 
                  Influence of dietary zinc additive on sperm concentration. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in sperm concentration, while points to the right depict an increase in sperm concentration. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.
Figure 4

Influence of dietary zinc additive on sperm concentration. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in sperm concentration, while points to the right depict an increase in sperm concentration. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.

Meta-analysis of 18 data sets with 162 cocks found that zinc supplementation significantly increased live sperm percent (SMD = 0.96%, 95% CI: 0.69, 1.23; Figure 5) and reduced dead sperm percent (SMD = –4.64%, 95% CI: –5.74, –3.53; Figure 6) in comparison with controls. Zinc sources had a significant influence on live and dead sperm percent (Table 2). The meta-analysis of 16 data sets having 162 male chickens found that zinc supplementation reduced sperm with abnormal morphology in comparison with the control (SMD = –2.80%, 95% CI: –3.43, –2.17; Figure 7). Abnormal sperm percent was significantly influenced when the analysis was disaggregated into organic zinc (SMD = –2.05%, 95% CI: –2.84, –1.27; Table 2) and inorganic zinc (SMD = –3.18%, 95% CI: –4.03, –2.34; Table 2).

Figure 5 
                  Impact of diets with or without zinc additive on live sperm percent. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in live sperm percent, whereas points to the right depict an increase in live sperm percent. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.
Figure 5

Impact of diets with or without zinc additive on live sperm percent. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in live sperm percent, whereas points to the right depict an increase in live sperm percent. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.

Figure 6 
                  Impact of dietary zinc additive on dead sperm percent. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in dead sperm percent, while points to the right depict an increase in dead sperm percent. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.
Figure 6

Impact of dietary zinc additive on dead sperm percent. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in dead sperm percent, while points to the right depict an increase in dead sperm percent. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.

Figure 7 
                  Impact of dietary zinc supplement on abnormal sperm percent. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in abnormal sperm percent, while points to the right depict an increase in abnormal sperm percent. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.
Figure 7

Impact of dietary zinc supplement on abnormal sperm percent. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in abnormal sperm percent, while points to the right depict an increase in abnormal sperm percent. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.

3.3 Analysis of heterogeneity and moderators

There is evidence of significant heterogeneity (I 2 = 66.29–94.24%) among the studies analysed (Figures 2 and 4 and 6 and 7). These I 2 values imply that 66–94% of the reported variance is due to real differences between studies and, as a result, can be explained by the moderators. Meta-regression as shown in Table 3 found significant relationships between moderators (chicken age and duration of Zn supplementation) and semen output (Q M = 9.12; p < 0.001), with age and supplementation duration accounting for 57% of the treatment effect. Furthermore, meta-regression found a large effect for the duration of supplementation, age and dosage as moderators, with these moderators explaining 100% of the study effect on sperm motility. Results also demonstrated significant linear relationships between sperm concentration and aspects of studied moderators (i.e. duration of supplementation, age and Zn source), with these moderators accounting for the majority of the heterogeneity. For abnormal sperm percent, meta-regression found a moderate effect for age as a moderator, with age explaining 55% of the Zn effect.

Table 3

Results of a simple meta-regression of outcome measures versus covariates

Outcomes Covariates Q M p-Value R 2-Index (%)
Semen output Age 13.90 0.043 29.56
Duration of supplementation 9.12 0.028 27.19
Dosage 6.98 0.222 14.64
Zn source 1.67 0.196 6.16
Sperm motility Age 27.90 <0.001 100.00
Duration of supplementation 27.00 <0.001 100.00
Dosage 23.10 0.002 100.00
Zn source 0.001 0.972 0.00
Sperm concentration Age 37.40 <0.001 70.38
Duration of supplementation 12.30 0.007 37.74
Dosage 8.55 0.382 1.00
Zn source 5.68 0.017 21.04
Live sperm percent Age 10.00 0.074 100.00
Duration of supplementation 0.20 0.905 0.00
Dosage 3.40 0.846 0.00
Zn source 0.09 0.770 0.00
Dead sperm percent Age 2.52 0.774 0.00
Duration of supplementation 0.10 0.950 0.00
Dosage 8.39 0.300 12.96
Zn source 0.10 0.747 0.00
Abnormal sperm percent Age 20.70 <0.001 55.22
Duration of supplementation 3.20 0.202 0.88
Dosage 4.23 0.517 0.00
Zn source 3.42 0.065 12.96

3.4 Female reproductive markers

The meta-analysis of 14 data sets, with 1,267 breeder hens indicated that the fertility rate calculated as the number of fertile eggs to the number of eggs set was not affected by dietary zinc supplementation (SMD 0.12%, 95% CI: –0.05, 0.28; Figure 8). Similarly, eggs from hens offered diets supplemented with and without inorganic zinc had comparable fertility rates (SMD = –0.03, 95% CI: –0.18, 0.11; Table 2). In contrast, fertility of eggs from hens fed organic zinc supplemented diets differed significantly from zero (SMD = 0.34, 95% CI: 0.09, 0.59; Table 2). The analysis of 16 data sets with 1,341 breeder hens revealed that dietary zinc supplementation had no significant effect on hatchability measured as the number of live chicks divided by the number of fertile eggs set when compared to the control (SMD = 0.09%, 95% CI: –0.05, 0.24; I 2-statistic = 49.32%, Q-statistic: p = 0.05; Figure 9). Mean effect estimation also revealed that zinc source had no effect on hatchability performance (Table 2).

Figure 8 
                  Influence of dietary zinc additive on fertility rate in breeder hens. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in fertility rate, whereas points to the right depict an increase in fertility rate in breeder hens. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.
Figure 8

Influence of dietary zinc additive on fertility rate in breeder hens. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in fertility rate, whereas points to the right depict an increase in fertility rate in breeder hens. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.

Figure 9 
                  Impact of dietary zinc additive on hatchability in breeder hens. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in egg hatchability, while points to the right depict an increase in egg hatchability. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.
Figure 9

Impact of dietary zinc additive on hatchability in breeder hens. The thick vertical line is the line of no effect (i.e. SMD = 0). Points to the left of this thick vertical line connote a decrease in egg hatchability, while points to the right depict an increase in egg hatchability. The dotted line shows the overall SMD. The result is considered significant the 95% CI of the overall SMD did not include zero.

4 Discussion

The present meta-analysis was performed to give clarity on the impact of diets with and without zinc supplementation on reproductive indices of breeder chickens. In both natural mating and artificial insemination, male fertility is strongly correlated with semen quality markers. The results of this meta-analysis demonstrated that zinc supplements improved semen output and quality in chickens. Seminal plasma is an essential component in most natural mating processes because it serves as a vehicle and source of nutrition for spermatozoa. Its measurement in the form of semen volume is vital in semen analysis because it aids in the calculation of sperm concentration. The observed significant increase in semen output in cocks fed zinc-supplemented diets compared to the controls could be attributed to the ability of zinc to stimulate the proximal efferent ducts, epididymis and the deferent duct to produce semen. This result is in agreement with the findings of Hudson et al. [22], who reported that zinc had a positive effect on reproductive markers in chickens. Results indicated that zinc source had no effect on semen output; however, breeder cocks on inorganic zinc intervention had a significantly high magnitude of effect size compared to the controls. The lack of significance in semen output in birds fed diets supplemented with organic zinc when compared to the controls suggests the similarity of the diets. The physiological explanation for the difference between the semen outputs of cocks fed diets with and without organic zinc in the current meta-analysis is not clear and merits further investigation. However, the disparity reported between cocks fed diets with and without organic zinc may be due to factors such as age and duration of supplementation demonstrated to affect semen output in this meta-analysis, and dosage and supplementation level found to influence semen quality in synthetic line broilers [24].

The significantly higher sperm concentration recorded in breeder cocks on zinc intervention when compared to controls indicates the high ability of zinc supplemented diets to support spermatogenesis, leading to a better fertilizing ability. This agrees with the findings of Irani et al. [25] that oral zinc supplementation leads to an increase in sperm concentration in rats. Similarly, Zn supplementation improves sperm concentration in bulls [26,27] and goats [28,29]. Zinc source had a significant positive effect on sperm concentration expressed as the number of sperm cells in one millilitre of semen. This finding agrees with the earlier report of Kumar et al. [26] that crossbred bulls offered Zn propionate had better sperm concentration compared to those fed diets supplemented with ZnSO4. Sperm motility which is considered the most important index of fertilization ability was significantly high in cocks on dietary zinc supplementation over the controls. This suggests that diets with zinc supplements have a positive effect on sperm motility. One possible reason for this is that the addition of zinc to the chicken diet may lead to an increase in copper-zinc superoxide dismutase and zinc metalloenzyme activities in the ejaculate which previous research has found to protect spermatozoa membrane against oxidative damage [7]. In addition to the above observations, other authors [2,3] found that oral zinc administration improves sperm concentration and motility in animals other than chickens. The significantly higher sperm motility witnessed in breeder cocks on dietary zinc supplements could be attributed to an increase in the production of adenosine triphosphate through glycolysis which plays a vital part in the maintenance of flagellar motility and fertilization capacity [26,30]. This finding disagreed with the results of Glogowski et al. [1], who found similar sperm motility and sperm concentration in turkey toms on varying zinc supplementation levels. Our results are at variance with Cappai et al. [31], who discovered that semen traits (i.e. sperm concentration, motility and straightness index) in stallions housed in individual boxes and fed hay and concentrate were not affected by Zn/selenium supplementation at 100 g/animal/day for 56 days. The reported difference might be ascribed to animal species, dosage, duration of zinc supplementation and genetic differences. Also, the higher sperm motility in cocks on zinc treatment suggests that zinc supplementation levels of up to 100 mg/kg feed enhanced sperm motility. However, this result disagreed with Egwurugwu et al. [32], who reported significantly reduced sperm motility in rats administered zinc as ZnSO4 at 200, 400, 600 and 800 mg for 6 weeks via water compared to the control (without zinc supplementation). This is to be expected given that higher zinc levels have a severe adverse effect on sperm motility in animal models [28].

In the present study, the percentage of live spermatozoa were positively influenced by dietary zinc supplements compared to the controls, and this could be attributed to increased semen antioxidant enzyme activity as corroborated by other researchers [1,2,3,4,7] that zinc reduces oxidative stress in sperm membrane. Furthermore, our results show that zinc sources increased live sperm percent and reduced dead sperm percent. However, the magnitude of effect estimates was higher in cocks offered diets supplemented with inorganic zinc than those on organic zinc intervention. Sperm morphology, a term used to describe the appearance (size and shape) of a sperm, which when abnormal, can decrease fertility and make it more difficult to fertilize the egg. Pooled results showed that dietary zinc supplementation reduced the number of sperm cells with abnormal morphology, suggesting that dietary zinc had a positive effect on sperm morphology in breeder cocks. Chicken spermatozoa have high concentrations of long-chain polyunsaturated fatty acids which make them prone to free radical attack emanating from dead sperm cells and environmental stressors. The significant reduction in abnormal sperm percent in cocks on zinc treatments compared to the controls may have been achieved via increased expression levels of metallothionein and zinc-containing superoxide dismutase in the semen that aid to protect spermatozoa membrane against oxidative damage [7].

The age at which semen is collected from an animal affects its quality traits. The results of this study showed that age is a limiting factor in this meta-analysis and has direct implications on the semen results. The observed significant linear relationship between semen traits and age in this meta-analysis implies that semen parameters are dependent on the age of the breeder cocks, which is consistent with the findings of other researchers [31,33,34,35,36,37] that young breeder cocks respond better to Zn supplementation than older cocks. Similarly, Cerolini et al. [34] found that sperm concentration in breeder cocks increased from 24 to 39 weeks and then remained stable, before declining by 72 weeks of age. This reduction confirmed the earlier statement by Shanmugam et al. [37] that sperm from older cocks have a higher DNA fragmentation index. Additionally, our meta-analysis suggested that duration of supplementation is a predictor of Zn’s effect on semen output, sperm motility and sperm concentration in breeder cocks and explained most of the between-study variance. Results also showed that dosage is a significant predictor of the impact of Zn intervention on sperm motility. Similarly, meta-regression revealed that the Zn source had little effect as a covariate and explained only 21% of the Zn effect on sperm concentration. However, factors, like environmental stressors, strain, natural light cycle, frequency of semen collection, and others known to influence semen quality in chicken [38,39] that were not analysed in this study due to insufficient data, may have been responsible for the unexplained variability. The magnitude of response to Zn treatment was greater in cocks fed diets having Zn from organic sources than in cocks fed diets containing Zn from inorganic sources, supporting the recent finding of Ogbuewu et al. [40] that broilers offered organic Zn sources had better bioavailability than their inorganic counterparts and could meet the Zn requirements of breeder cocks at lower dietary concentrations. Our results are in agreement with those of Kumar et al. [26], who reported improved sperm concentration and mass motility in animals fed Zn propionate when compared to those fed ZnSO4.

Pooled effect results suggest that zinc treatment had no effect on percentage fertility and hatchability performance in breeder hens. These results supported Barber et al. [9], who reported that supplementation of breeder broiler hen diets with 150 mg ZnSO4/kg or a mixture of ZnAA and ZnSO4 at 75 mg/kg each had no effect on hatchability performance. Contrary to the present findings, Barber et al. [9] found increased percentage of fertility (78–85%) and hatchability (68–73%) of eggs from broiler breeders fed diets supplemented with ZnO or zinc methionine at 152 mg/kg feed when compared to hens fed the control diet. The observed difference may be ascribed to zinc supplementation levels, bioavailability to the birds and duration of supplementation. Our sub-analysis results indicated that hens offered diets supplemented with organic zinc had significantly increased fertility in comparison to those fed control; this may imply higher bioavailability of organic zinc [41]. On the other hand, the fertility of eggs from breeder hens was not affected by inorganic zinc supplementation. Research has shown that the inclusion of organic zinc at 110 mg/kg feed in layer diet had no effect on hatchability performance [42]. The mechanisms of action responsible for the increased fertility rate in hens fed organic zinc-supplemented diets in comparison with those with a control diet are not well known. However, the observed difference could be ascribed to bioavailability, as organic mineral sources are proposed to be more available than inorganic sources [41].

5 Conclusion

The pooled results indicated that dietary zinc supplementation improved semen quality markers in breeder cocks when compared to the controls. In addition, the results also pointed out that dietary zinc supplementation had no effect on percentage fertility and hatchability. The sub-analysis results demonstrated that zinc source positively influenced percentage fertility and semen characteristics in chickens. However, more research effort should be directed towards ascertaining the effect of long-term dietary zinc supplementation on the reproductive performance of breeder chickens as the studies included in the present meta-analysis supplemented zinc in chicken feed for a short period (5–25 weeks). This is to increase the uptake of the research findings by commercial breeder farmers.



  1. Funding information: The authors state no funding involved.

  2. Author contributions: O.I.P.: conceptualization, methodology, literature search, data analysis, writing – original draft. M.AC.: conceptualization, data visualization, writing – review and editing.

  3. Conflict of interest: The authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

[1] Glogowski J, Jankowski J, Suszynska D, Polak M, Ciereszko A. Quality and biological value of semen collected from turkey-toms fed diets with different zinc content. Arch Geflugelk. 2004;68:235–8.Search in Google Scholar

[2] Ghasemi N, Babaei H, Azizallahi S, Kheradmand A. Effect of long-term administration of zinc after scrotal heating on mice spermatozoa and subsequent offspring quality. Andrologia. 2009;41:222–8.10.1111/j.1439-0272.2009.00920.xSearch in Google Scholar PubMed

[3] Rafique M, Naqvi A, Nankani K. Zinc improves the quality of semen lab rats. Med Chan. 2010;16:619–22.Search in Google Scholar

[4] Vickram S, Muthugadhalli S, Jayaraman G, Kamini R, Ramesh PM, Sridharan B. Influence of trace elements and their correlation with semen quality in fertile and infertile subjects. Turkish J Med Sci. 2013;43:1000–7.10.3906/sag-1211-54Search in Google Scholar

[5] Lee SR. Critical role of zinc as either an antioxidant or a prooxidant in cellular systems. Oxid Med Cell Longev. 2018;915:6285–11.10.1155/2018/9156285Search in Google Scholar PubMed PubMed Central

[6] Beyersmann D, Haase H. Functions of zinc in signaling, proliferation and differentiation of mammalian cells. Biomet. 2001;14:331–41.10.1007/978-94-017-3728-9_8Search in Google Scholar

[7] Ao T, Pierce J. The replacement of inorganic mineral salts with mineral proteinates in poultry diets. World’s Poult Sci J. 2013;69:5–16.10.1017/S0043933913000019Search in Google Scholar

[8] Kidd M, Anthony NB, Johnson Z, Lee S. Effect of Zinc methionine supplementation on the performance of mature broiler breeder. J Appl Poult Res. 1992;1:207–11.10.1093/japr/1.2.207Search in Google Scholar

[9] Barber SJ, Virden WS, Ward TL, Johnson AB, Zumwalt CD, Kidd MT, et al. Broiler breeder reproductive performance as affected by Availa Zinc and Availa Manganese. Poult Sci. 2002;81(Suppl. 1):119.Search in Google Scholar

[10] Higgins JPT, Deeks JJ. Chapter 7: Selecting studies and collecting data. In: Higgins JP, Green S, (Eds). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 (updated March 2011). The Cochrane Collaboration; 2011. Available from. http://handbook.cochrane.org/. (Accessed on 10 April 2021).Search in Google Scholar

[11] Wallace BC, Lajeunesse MJ, Dietz G, Dahabreh IJ, Trikalinos TA, Schmid CH, et al. Open MEE: intuitive, open-source software for meta-analysis in ecology and evolutionary biology. Methods Ecol Evol. 2016;8:941–7.10.1111/2041-210X.12708Search in Google Scholar

[12] Borenstein M, Hedges LV, Higgins JPT, Rothstein HR. Introduction to Meta-analysis. Chichester, UK: Wiley; 2009.10.1002/9780470743386Search in Google Scholar

[13] Higgins JPT, Green S. Cochrane handbook for systematic reviews of reviews of intervention version 5.0.2 [Updated September 2009]. The Cochrane collaboration 2009. Available from www.cochrane-handbook.org.10.1002/9780470712184Search in Google Scholar

[14] Koricheva J, Gurevitch J, Mengersen K. Handbook of Meta-analysis in Ecology and Evolution. Princeton and Oxford, UK: Princeton University Press; 2013.10.1515/9781400846184Search in Google Scholar

[15] Higgins JP, Altman DG, Gotzsche PC, Juni P, Moher D, Oxman AD, et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. Bio Med J. 2011;343:d5928.10.1136/bmj.d5928Search in Google Scholar PubMed PubMed Central

[16] Egger M, Smith GD. Principles of and procedures for systematic reviews. In: Egger M, Smith GD, editors. Systematic reviews in health care: Meta-analysis in context. London, UK: British Medical Journal Books; 2001. 23–42.10.1002/9780470693926.ch2Search in Google Scholar

[17] Shanmugam M, Prakash B, Reddy PEK, Panda A. Dietary organic zinc and selenium supplementation improves semen quality and fertility in layer breeders. Indian J Anim Sci. 2015;85:202–4.10.56093/ijans.v85i2.46617Search in Google Scholar

[18] Mahmood HMA, Hazim JA. Effect dietary zinc on semen quality of cobb-500 broiler breeder males. Int J Poult Sci. 2011;10:477–82.10.3923/ijps.2011.477.482Search in Google Scholar

[19] Alm El-Dein AK, Soliman MM, Rezk AM, Khattab MA, Mousa SMM. An attempt to improve some productive, reproductive and physiological performance of male and female aged Inshas strain laying hens by using zinc methionine. Egypt Poult Sci. 2017;37:37–56.10.21608/epsj.2017.5410Search in Google Scholar

[20] Gallo R, Veronico M, Nacucchi O, Tafaro E, Barile P, Nicastro F, et al. The effects of selenium, zinc and vitamin E supplementation on performance of broiler breeder males. Italian J Anim Sci. 2003;2:471–3.Search in Google Scholar

[21] Durmus I, Atasoglu C, Mizrak C, Ertas S, Kaya M. Effect of increasing zinc concentration in the diets of brown parent stock layers on various production and hatchability traits. Arch Tierz Dummerstorf. 2004;47:483–9.10.5194/aab-47-483-2004Search in Google Scholar

[22] Hudson BP, Dozier WA, Wilson JL, Sander JE, Ward TL. Reproductive performance and immune status of caged broiler breeder hens provided diets supplemented with either inorganic or organic sources of zinc from hatching to 65 week of age. J Appld Poult Res. 2004;13:349–59.10.1093/japr/13.2.349Search in Google Scholar

[23] Prabhakar R, Moorthy M, Edwin SC, Mani R, Sarvanakumar VR. Effect of dietary levels of calcium carnitine and zinc on semen characteristics of cross-bred chicken. Indian J Vet Anim Sci Res. 2014;43:180–6.Search in Google Scholar

[24] Prabakar G, Gopi M, Kolluri G, Rokade JJ, Khillare G, Pearlin BV, et al. Effect of supplementation of zinc-methionine on egg production, semen quality, reproductive hormones, and hatchability in broiler breeders. Biol Trace Elem Res. 2021;199:4721–30. 10.1007/s12011-021-02590-9.Search in Google Scholar PubMed

[25] Irani M, Amirian M, Sadeghi R, Lez JL, Latifnejad RR. The effect of folate and folate plus zinc supplementation on endocrine parameters and sperm characteristics in sub-fertile men: A Systematic Review and Meta-analysis. Urol J. 2017;14:4069–78.Search in Google Scholar

[26] Kumar N, Verma RP, Singh LP, Varshney VP, Dass RS. Effect of different levels and sources of zinc supplementation on quantitative and qualitative semen attributes and serum testosterone level in crossbred cattle (Bos indicus x Bos taurus) bulls. Reprod Nutr Dev. 2006;46:663–75.10.1051/rnd:2006041Search in Google Scholar

[27] Majumder A, Thakur M, Bhakat M, Saha M, Mohanty TK, Mondal G. Effect of dietary copperand zinc supplementation on semen quality of murrah bulls. Indian JAnim Res. 2020;54:1260–4.10.18805/ijar.B-3887Search in Google Scholar

[28] Liu H, Sun Y, Zhao J, Dong W, Yang G. Effect of zinc supplementation on semen quality, sperm antioxidant ability, and seminal and blood plasma mineral profiles in Cashmere goats. Biol Trace Elem Res. 2020;196:438–45.10.1007/s12011-019-01933-xSearch in Google Scholar PubMed

[29] Kaewma S, Suphappornchai S, Suwimonteerabutr J, Am-In N, Techakumphu M. Zinc supplementation improves semen quality in boars. Thai J Vet Med. 2021;51:489–500.10.56808/2985-1130.3144Search in Google Scholar

[30] Santiago-Moreno J, Blesbois B. Functional aspects of seminal plasma in bird reproduction. Int J Mol Sci. 2020;21:5664. 10.3390/ijms21165664.Search in Google Scholar PubMed PubMed Central

[31] Cappai MG, Taras A, Cossu I, Cherchi R, Dimauro C, Accioni F, et al. Effects of dietary Zn/Se and α-tocopherol supplementation on metabolic milieu, haemogram and semen traits of breeding stallions. Biol Trace Elem Res. 2021;199:3287–96.10.1007/s12011-020-02447-7Search in Google Scholar PubMed PubMed Central

[32] Egwurugwu JN, Ifedi CU, Uchefuna RC, Ezeokafor EN, Alagwu EA. Effects of zinc on male sex hormones and semen quality in rats. Nig J Physiol Sci. 2013;28:17–22.Search in Google Scholar

[33] Chyb J, Kime DE, Mikolajczyk T, Szczerbik P, Epler P. The influence of zinc on sperm motility of common carp-a computer assisted studies. Arch Pol Fish. 2000;8:5–14.Search in Google Scholar

[34] Cerolini S, Kelso KA, Noble RC, Speake BK, Pizzi F, Cavalchini LG. Relationship between spermatozoan lipid composition and fertility during aging of chickens. Biol Reprod. 1997;57:976–80.10.1095/biolreprod57.5.976Search in Google Scholar PubMed

[35] Hocking PM, Bernard R. Effects of dietary crude protein content and food intake on the production of semen in two lines of broiler breeder males. Brit Poult Sci. 1997;38:199–202.10.1080/00071669708417969Search in Google Scholar PubMed

[36] Shanmugam M, Rajkumar U, Reddy MR, Rama, Rao SV. Effect of age on semen quality in naked neck and dwarf chicken under tropical climatic conditions. Anim Prod Sci. 2012;52:964–8.10.1071/AN12033Search in Google Scholar

[37] Shanmugam M, Vinoth A, Rajaravindra KS, Rajkumar U. Evaluation of semen quality in roosters of different age during hot climatic condition. Anim Reprod Sci. 2014;145:81–5.10.1016/j.anireprosci.2013.12.015Search in Google Scholar PubMed

[38] Zhang X, Berry WD, McDaniel GR, Roland DA, Liu P, Calvert C, et al. Body weight and semen production of broiler breeder males as influenced by crude protein levels and feeding regimens during rearing. Poult Sci. 1999;78:190–6.10.1093/ps/78.2.190Search in Google Scholar PubMed

[39] Karaca AG, Parker HM, McDaniel CD. Elevated body temperature directly contributes to heat stress infertility of broiler breeder males. Poult Sci. 2002;81:1892–7.10.1093/ps/81.12.1892Search in Google Scholar PubMed

[40] Ogbuewu IP, Modisaojang-Mojanaga MMC, Mokolopi BG, Mbajiorgu CA. A meta-analysis of responses of broiler chickens to dietary zinc supplementation: feed intake, feed conversion ratio and average daily gain. Biol Trace Elem Res. 2022. 10.1007/s12011-022-03320-5.Search in Google Scholar PubMed

[41] Aliarabi H, Ahmadi A, Siyar SAH, Tabatabaie MM, Saki A, Zaboli KH, et al. Effect of different levels and sources of zinc on egg quality and layer performance. Proceedings of the 19th Austral. Poult. Sci. Symp., Sydney, New South Wales, Australia, 12-14; February 2007. 2007. p. 102–5.Search in Google Scholar

[42] Zhu YW, Li WX, Lu L, Zhang LY, Ji C, Lin X, et al. Impact of maternal heat stress in conjunction with dietary zinc supplementation on hatchability, embryonic development, and growth performance in offspring broilers. Poult Sci. 2017;96:2351–9.10.3382/ps/pew481Search in Google Scholar PubMed

Received: 2022-03-04
Revised: 2022-07-06
Accepted: 2022-07-07
Published Online: 2022-08-03

© 2022 Ifeanyichukwu Princewill Ogbuewu and Christain Anayo Mbajiorgu, published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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