zinc

Zinc, an essential trace element for live organisms, is present as a co-factor in over 300 metaloenzymes, representing all six classes of enzymes, and plays an important role in many metabolic processes, including protein synthesis (O'Dell, Reference O'DELL1992; Salim et al., Reference SALIM, JO and LEE2008). Deficiency of zinc exerts a negative influence on protein and carbohydrate metabolism in animals and leads to reduced feed intake, decreased growth, poor FCR, abnormalities in immunological and reproductive processes and skeletal and skin issues (Underwood and Suttle, Reference UNDERWOOD and SUTTLE1999).

One of the most important ways to evaluate the efficacy of different sources of minerals in poultry is to assay their relative bioavailability in relation to standard, inorganic forms, for instance, feed-grade sulphates of microelements. The results of most experiments performed in recent years have demonstrated the high relative bioavailability of organic Zn sources, even if this has not always been reflected in improved performance parameters. For example, the study of Star et al. (Reference STAR, VAN DER KLIS, RAPP and WARD2012) aimed at determining the bioavailability of an organic, amino acid complexed zinc form (Availa-Zn®) compared with zinc sulphate. A basal, practical European broiler wheat-maize-soya diet containing 33.5 ppm of Zn was supplemented with increasing levels of Zn from zinc sulphate or organic Zn. It was found, based on the slope ratio of the linear response curves for both zinc sources and using tibia zinc content as a response parameter, that organic Zn was characterised by higher bioavailability (164%) than inorganic zinc sulphate (100%). For comparison, in a previous study by Swiatkiewicz et al. (Reference SWIATKIEWICZ, KORELESKI and ZHONG2001) the relative bioavailability of Zn from organic Zn was calculated at 121, 116 and 139% (versus ZnSO₄ at 100%), with body weight gain (BWG), FCR and Zn content in tibia bones used as response indices. The results of a more recent study with broilers fed conventional corn-soybean meal indicated that the relative bioavailability of organic Zn chelated to amino acids and peptides (Bio-Plex®), as compared to inorganic Zn sulphate, was very high and reached values of 147-200%, based on slope ratio methods from the regression of BWG on supplemental Zn intake (Sahraei et al., Reference SAHRAEI, JANMMOHAMDI, TAGHIZADEH, ALI MOGHADAM and ABBAS RAFAT2013).

The high relative bioavailability of Zn provided in organic form was reported when a corn-soybean protein concentrate broilers’ diet was supplemented with Zn propionate (Brooks et al., Reference BROOKS, GRIMES, LLOYD, VERISSIMO and SPEARS2013). Using a relative slope assay, with BWG, tibia Zn concentration, and total tibia Zn used as response parameters, the relative bioavailability of Zn propionate was 119, 116, and 116%, respectively, compared with feed grade Zn sulphate (100%). Liu et al. (Reference LIU, LI, LU, XIE, ZHANG, WANG and LUO2013) observed the positive effect of diet supplementation with Zn proteinate on BWG, feed intake, and Zn concentration in plasma and in tibia ash of broilers; however, based on the slope ratios from multiple linear regressions of tibia ash Zn concentration and pancreas metallothionein mRNA levels, there was no difference in bioavailability between Zn proteinate and Zn sulphate, which might be explained by the low chelation strength of the Zn proteinate.

The results of a substantial portion of research papers indicated that organic Zn had no influence on performance indices in poultry; however, a majority demonstrated other benefits for animal metabolism. Thus, Salim et al. (Reference SALIM, LEE, JO, LEE and LEE2012) did not find any effect of diet supplementation with organic Zn (25 ppm) on the growth performance of broiler chickens or on skin quality, i.e., skin thickness and shear force; however, organic Zn increased the Zn content in thigh meat and Ca content in plasma. In the authors’ previous work, there were no differences in the chickens’ performance; however, skin thickness was increased through increased collagen content in the skin of birds fed a diet supplemented with organic Zn (Salim et al., Reference SALIM, LEE, JO, LEE and LEE2011). Correspondingly, El-Wahab et al. (Reference EL-WAHAB, RADKO and KAMPHUES2013) observed the positive effect of a combination of organic Zn-methionine (150 ppm) and high biotin supplementation on skin quality, resulting in significantly decreased severity of food pad dermatitis in broilers exposed to high litter moisture levels. Improvement of skin quality and reduction of the severity and incidence of food pad dermatitis in broilers was observed when inorganic dietary Zn was partly replaced with organic complexed Zn (Saenmahayak et al., Reference SAENMAHAYAK, BILGILI, HESS and SINGH2010).

Yalcinkaya et al. (Reference YALCINKAYA, CINAR, YILDIRIM, ERAT, BASALAN and GUNGOR2012) reported no effects of dietary organic Zn (80 ppm, Bio-Plex®) on growth performance and most blood biochemical indices; however, the simultaneous addition of organic Zn and prebiotic (MOS) increased serum Cu and Fe levels, which, as the authors suggested, may indicate the synergetic, positive influence of organic Zn and MOS on mineral absorption. The results of a study by Sahraei et al. (Reference SAHRAEI, JANMMOHAMDI, TAGHIZADEH and CHERAGHI2012) showed no positive influence of dietary organic Zn Bio-Plex®, in comparison to Zn oxide, on tibia morphology and ash content.

Some beneficial effects were found when Zn glycine chelate, as a source of organic zinc for broiler chickens, was evaluated. The addition of high levels (90-120 ppm) of Zn glycine to the basal diet had a beneficial effect on growth performance and immunological characteristics (IgA, IgG and IgM blood concentrations); however, there were no differences between groups fed diets supplemented with the same level (120 ppm) of Zn glycine and inorganic Zn sulphate (Feng et al., Reference FENG, MA, NIU, Wu and WANG2010). The results of a more recent study showed that high dietary levels of Zn glycine led to an improvement in the activity of Cu/Zn superoxide dismutase and glutathione peroxidase, a decrease in malondialdehyde content in chickens’ livers, an increase in the height of intestinal villi, a decrease in crypt depth, and a reduction in the thickness of intestinal walls (Ma et al., Reference MA, NIU, FENG, WANG and FENG2011).

The influence of diet supplementation with an organic Zn source on the quality of broilers’ meat was determined by Saenmahayak et al. (Reference SAENMAHAYAK, SINGH, BILGILI and HESS2012). Overall, as compared to an inorganic Zn source (sulphate), the addition of organic Zn did not affect meat quality indices (among others, water holding capacity, cooking loss, or oxidative stability of breast meat during refrigerated storage). It did however, significantly enhance drip loss in fillets at 24 h post deboning and increased redness of fillets (a* value) after 28 days of storage. In previous work by the same authors (Saenmahayak et al., Reference SAENMAHAYAK, BILGILI and HESS2007), diet supplementation with organic Zn positively affected meat quality, i.e., reduced cooking loss.

The goal of an experiment by Bun et al. (Reference BUN, GUO, GUO, JI and CAO2011) was to investigate the effect of organic Zn (methionine hydroxyl analogue-Zn chelate) supplementation on the performance, antioxidant status, and immune responses of broilers infected with Eimeria tenella. Dietary Zn supplementation did not affect growth performance; however, the obtained results demonstrated that organic Zn supplementation reduced oxidative stress and improved some immune responses indices, irrespective of whether birds were healthy or challenged with E. tenella (Bun et al., Reference BUN, GUO, GUO, JI and CAO2011). Vieira et al. (Reference VIEIRA, RIBEIRO, KESSLER, MORAES, KUNRATH and LEDUR2013) evaluated the efficacy of an organic source of dietary Zn (a complex with 2-hydroxy-4-(methylthio) butanoic acid/Mintrex Zn) in chickens exposed to immunological, nutritional or environmental challenges. As compared to Zn sulphate, organic Zn had no effect on humoral immune response (antibody titres against BSA), Zn concentration in the carcass, or performance (feed intake, BWG, and FCR); however, it reduced the incidence of footpad lesions. Similar results were recently obtained by Yogesh et al. (Reference YOGESH, DEO, SHRIVASTAVA, MANDAL, WADHWA and SINGH2013), who found no differences in growth performance or humoral (antibody titres against SRBC) or cellular (footpad index to phytohaemagglutinin-P) immune response in broilers fed diets supplemented with organic (Zn proteinate) and inorganic (Zn oxide or Zn sulphate) forms of Zn.

In a recent study with White Pekin broiler ducks, Attia et al. (Reference ATTIA, ABD AL-HAMID, ZEWEIL, QOTA, BOVERA, MONASTRA and SAHLEDOM2013) evaluated the efficacy of inorganic (ZnO) and organic (Bio-Plex®) Zn sources, added to the diets at levels of 30, 60, and 120 ppm. The obtained results did not indicate a high level of usefulness of organic Zn for ducks, since BWG and FCR during the entire trial period (1-56 days of age) were better in birds fed a diet supplemented with ZnO. The Zn source did not affect Zn concentrations in tibia, liver, or excreta; however, plasma Zn was significantly higher when a diet containing organic Zn was used. The authors of this work emphasised that the observed negative effect of an organic Zn source on the growth performance of ducks was unexpected and warranted further study (Attia et al., Reference ATTIA, ABD AL-HAMID, ZEWEIL, QOTA, BOVERA, MONASTRA and SAHLEDOM2013).

The number of research papers evaluating organic Zn sources with laying hens has been considerably lower compared to broiler studies. The results of an experiment with post-moult hens (Stanley et al., Reference STANLEY, SHANKLYN, DALEY, GRAY, VAUGHAN, HINTON and HUME2012) indicated that organic Zn (Bio-Plex®) significantly decreased mortality and increased egg production, but significantly reduced egg, albumen and shell weights. In contrast, Swiatkiewicz and Koreleski (Reference SWIATKIEWICZ and KORELESKI2008) reported no effect of organic Zn amino acid complexes on egg production; however, in older layers, organic Zn positively affected eggshell quality measured as eggshell breaking strength, alleviating the negative effect of the hens’ age on this measurement. In an experiment with laying quails, supplementing the diet with up to 40 ppm of organic Zn positively affected the weight, fertility and hatchability of eggs (El-Samee et al., Reference EL-SAMEE, EL-WARDANY, ALI and ABO-EL-AZAB2012). The results of a study by Idowu et al. (Reference IDOWU, AJUWON, OSO and AKINLOYE2011) showed that Zn proteinate, compared to inorganic zinc sources, improved egg production and Zn retention and alleviated environmental stress in tropical conditions. In a study with broiler breeder hens, Soni et al. (Reference SONI, MISHRA, SWAIN, DAS, CHICHILICHI and SETHY2013) found a positive effect of a substantial dietary addition of organic Zn (Zn-methionine, 80 ppm) on immunity, measured as cellular immune response to PHA-P and antibody titres against SRBC.

manganese

Manganese, as a crucial component of enzymes which are involved in the antioxidative defence system, protein metabolism, and bone formation as superoxide dismutase, transferases, hydrolases and lygases (Keen et al., Reference KEEN, ENSUNSA, WATSON, BALY, DONOVAN, MONACO and CLEGG1999; Reference KEEN, ENUNSA and CLEGG2000) is an important trace element for live organisms.

One of the most popular commercial organic manganese sources is Mn proteinate. Wang et al. (Reference WANG, LU, LI, LIU, ZHANG, YAO and LUO2012) evaluated the bioavailability of organic Mn proteinate in relation to inorganic Mn sulphate for broilers fed a conventional corn-soybean meal basal diet. Based on multiple linear regressions of such indices as Mn concentration, Mn superoxide dismutase activity (MnSOD) and MnSOD mRNA level in heart tissue on added Mn level, they did not find any significant differences in bioavailability between tested Mn sources. Different results were obtained by Brooks et al. (Reference BROOKS, GRIMES, LLOYD, VALDEZ and SPEARS2012) in a study with chickens fed a corn- and soybean-meal-based diet with increased levels of Ca and P. They reported that the relative bioavailability of Mn propionate, as compared to feed-grade Mn sulphate (100%), calculated using the relative slope assay and Mn concentration in bone as a response parameter, was 139% (Brooks et al., Reference BROOKS, GRIMES, LLOYD, VALDEZ and SPEARS2012).

The goal of two research projects, i.e. experiments in situ with ligated duodenal loops and in vivo, by Bai et al. (Reference BAI, LU, WANG, XI, ZHANG and LUO2012) was to investigate the influence of Mn sources on Mn transport and gene expression of divalent metal transporter 1 (DMT1) in broilers’ small intestines. The obtained results indicated that organic chelates of Mn with amino acids with moderate or strong chelation strength significantly increased the maximum transport rate of Mn and DMT1 mRNA levels in the duodenum as compared to Mn sulphate (Bai et al., Reference BAI, LU, WANG, XI, ZHANG and LUO2012). Similarly, a positive effect was reported for a dietary organic chelate of Mn and an amino acid with moderate chelation strength on activation of the expression of the manganese-containing superoxide dismutase gene at both the transcriptional and translational levels in the heart tissue of chickens (Li et al., Reference LI, LU, HAO, WANG, ZHANG, LIU, LIU, LI and LUO2011).

In a study with laying hens, a dietary organic source of manganese (Mn proteinate) gave better results, in terms of weight gain, egg weight, percentage of undamaged eggs, and tibia bone quality indices, than inorganic Mn sulphate (Yildiz et al., Reference YILDIZ, CUFADAR and OLGUN2011). As indicated by the authors, this beneficial influence was probably related to changes in the mineral element repartition in the hens and in particular to Mn accumulation in bones, promoted by the use of organic forms of Mn (Yildiz et al., Reference YILDIZ, CUFADAR and OLGUN2011).

copper

Copper is an essential microelement for animals, present in many enzyme systems in the body, e.g. superoxide dismutase, cytochrome oxidase, and lysyl oxidase, or ceruloplasmin (Klasing, Reference KLASING1998; Underwood and Suttle, Reference UNDERWOOD and SUTTLE1999), where it serves as a co-factor.

Liu et al. (Reference LIU, LU, LI, XIE, ZHANG, WAMG and LUO2012) evaluated the bioavailability of organic Cu proteinate relative to inorganic Cu sulphate in broilers fed a conventional corn-soybean meal diet. Based on slope ratios from multiple linear regressions of log¹⁰ liver and bile Cu concentrations with daily Cu intake, the estimated relative bioavailability of Cu proteinate was 78.8% and 79.3%, respectively, as compared to inorganic Cu sulphate (100%); however, these differences were not statistically significant. Das et al. (Reference DAS, MONDAL, BISWAS, BAIRAGI and SAMANTA2010) reported that the substitution of inorganic Cu sulphate with Cu proteinate in broiler chickens diet positively affected BWG and FCR, as well as nutrient utilisation, measured as digestibility of dry matter, nitrogen-free extracts, total carbohydrates and organic matter. The results of a recent experiment by Shamsudeen and Shrivastava (Reference SHAMSUDEEN and SHRIVASTAVA2013) indicated that Cu proteinate, compared to inorganic Cu sulphate, may alleviate the detrimental effect of aflatoxicosis on broiler chickens, improving the growth performance of birds fed a diet containing a high level of aflatoxin B₁.

Kim et al. (Reference KIM, SEO, SHIN, RHEE, HAN and PAIK2011) evaluated the potential efficacy of high dietary doses of organic Cu (100 ppm, Cu-Methionine or Cu proteinate) as replacements for feed antibiotics in broiler chickens’ nutrition. The results of this experiment showed that diet supplementation with both organic Cu sources improved the growth performance of broilers, an improvement comparable with that from supplementation with an antibiotic (avilamycin), and increased populations of lactobacilli while decreasing those of E. coli in the intestine. Hence the authors concluded that the organic Cu products were potential replacements for antibiotics (2011). Kwiecien et al. (Reference KWIECIEN, WINIARSKA-MIECZAN, ZAWISLAK and SROKA2014) did not find any differences in performance indices of chicks fed diet supplemented with Cu sulphate or organic Cu glycinate chelate, however organic Cu positively affected the biomechanical properties of femur bones.

An experiment with growing pullets (Jegede et al., Reference JEGEDE, ODUGUWA, OSO, FAFIOLU, IDOWU and NOLLET2012) determined the effect of different sources of Cu on growth performance, blood characteristics and plasma lipids. The basal diet was supplemented with increasing levels (50, 100, and 150 ppm) of an organic (proteinate) or inorganic (sulphate) Cu source. The forms of Cu used had no significant effect on growth indices; however, Cu proteinate decreased plasma cholesterol, low-density lipoprotein (LDL) and triglyceride in comparison to Cu sulphate. In a study with laying hens, Pekel and Alp (Reference PEKEL and ALP2011), comparing the efficacy of inorganic (Cu sulphate) and organic (Cu lysine or Cu proteinate) sources of Cu used at a high dietary level (250 ppm), did not find any beneficial effects of organic Cu in terms of egg production, egg mass, FCR, egg quality, egg yolk cholesterol, plasma total cholesterol, high-density lipoprotein cholesterol, triglycerides, or glutathione peroxidase activity. Dobrzanski et al. (Reference DOBRZANSKI, KORCZYNSKI, CHOJNACKA, GORECKI and OPALINSKI2008) indicated that diet supplementation with organic Cu (Saccharomyces cerevisiae yeast enriched with Cu) significantly increased Cu concentration in the egg content and eggshell, as well as in the blood and feathers, which proved the superior availability of organic Cu compared to Cu sulphate. The results of a recent study with layers (Witkowska et al., Reference WITKOWSKA, CHOJNACKA, KORCZYNSKI, SWINIARSKA, SAEID, OPALINSKI and DOBRZANSKI2014) showed that the replacement of Cu sulphate with soybean meal enriched by biosorption with Cu (which the authors called a ‘biological’ form of Cu) may positively affect eggshell quality.

The goal of an experiment with White Pekin ducks was to compare the efficacy of inorganic Cu sulphate and organic Cu lysine added to the diet in increasing amounts (4, 8, 12, and 150 ppm Cu) (Attia et al., Reference ATTIA, QOTA, ZEWEIL, BOVERA, ABD AL-HAMID and SAHLEDOM2012). The Cu source had no significant effect on BWG over the entire experimental period (1-56 days of age), while feed intake was increased and FCR was worsened by dietary organic Cu lysine. As compared to Cu sulphate, the organic Cu source increased Cu excretion, Cu concentration in the liver and plasma cholesterol concentration, but decreased plasma triglycerides.

different microelements used in combination

Many recent research projects with poultry have aimed at evaluating the efficiency of several microelements added simultaneously, in organic forms, to diets. In a study with female broilers, El-Husseiny et al. (Reference EL-HUSSEINY, HASHISH, ALI, ARAFA, EL-SAMEE and OLEMY2012) showed that partial replacement (50%) of inorganic sources of Zn (ZnO), Mn (MnO) and Cu (CuSO₄) with organic forms of these microelements (Zn proteinate, Mn methionine hydroxy analogue chelate and Cu methionine hydroxy analogue chelate) improved growth performance, carcass characteristics, and tibia quality indices, accompanied with decreasing levels of trace minerals in tibia, liver and excreta. Manangi et al. (Reference MANANGI, VAZQUEZ-ANON, RICHARDS, CARTER, BURESH and CHRISTENSEN2012) reported that the simultaneous replacement of inorganic Zn, Cu and Mn sulphate with significantly reduced levels (32, 8 and 32 ppm, respectively) of organic sources of these microelements (a complex with 2-hydroxy-4-(methylthio)butanoic acid, Mintrex) did not negatively affect chickens’ performance, carcass yield, immune response, tibia breaking strength, or bone and tissue mineral concentrations, but resulted in an improvement in footpad health and a significant reduction in litter microelement concentrations. As highlighted by the authors, this may provide an opportunity to reduce the environmental impact of the commercial poultry industry. Similar results were obtained by Zhao et al. (Reference ZHAO, SHIRLEY, VAZQUEZ-ANON, DIBNER, RICHARDS, FISHER, HAMPTON, CHRISTENSEN, ALLARD and GIESEN2010), who found no differences in the growth performance of broilers fed a diet containing standard levels of inorganic Zn, Mn, and Cu (as sulphates) and a diet containing significantly lower amounts, but consisting of 50% organic forms (Mintrex). These authors observed positive effects of organic minerals on footpad health. Correspondingly, Aksu et al. (Reference AKSU, AKSU, ÖZSOY and BAYTOK2010; Reference AKSU, ÖZSOY, AKSU, YORUK and GUL2011) showed no negative effects from the substitution of inorganic sources of Zn, Mn and Cu with much lower amounts, i.e. 1/3 of the levels recommended by NRC (1994), of organic forms of these minerals (Bio-Plex®) on growth performance parameters or antioxidant defence systems in broilers, measured as plasma malondialdehyde concentration and activity of antioxidant enzymes, while enabling a significant decrease in the volume of minerals excreted in faeces. Similarly, there were no negative influences on broiler chickens’ performance parameters, dressing percentage, lymphoid organ weights, or tibia bone mineralisation when dietary inorganic Zn, Mn and Cu oxides, used at the levels 100, 100 and 10 ppm, respectively, were replaced with organic amino acid chelates of these minerals (Gheisari et al., Reference GHEISARI, RAHIMI-FATHKOOHI, TOGHYANI and MRHDI2010). Bao et al. (Reference BAO, CHOCT, IJI and BRUERTON2007) performed a 29-day cage study to compare the response of broiler chickens to inorganic and organic mineral dietary sources. The results showed that supplementation with 4 ppm of Cu and 40 ppm each of Fe, Mn, and Zn from organic complexes can be sufficient for normal broiler growth to 29 d of age. Therefore the authors discussed the possibility of using these lower levels of organic microelements in broiler diets to avoid high levels of trace mineral excretion.

The results of a study by Yuan et al. (Reference YUAN, XU, HUANG, ZHOU and GUO2011) showed that complete replacement of dietary inorganic Zn and Mn sulphates with organic forms of these trace elements (Mintrex-Zn/Mn) positively affected the growth performance of broiler chickens (up to three weeks of age) and significantly decreased mineral excretion, with no influence on the mRNA abundance of Zn/Mn transfer proteins. The replacement of sulphates with a lower level (80%) of organic Mintrex-Zn/Mn decreased serum alkaline phosphatase activity (P<0.05); however, it did not affect growth performance, mRNA abundance of Zn/Mn transfer proteins or bone mineralisation and reduced the excretion of minerals in faeces (Yuan et al., Reference YUAN, XU, HUANG, ZHOU and GUO2011).

In the recent research of Oviedo-Rondon et al. (Reference OVIEDO-RONDON, LEANDRO, ALI, KOCI, MORAES and BRAKE2013) it was reported that partial (30%) replacement of inorganic sources of Zn, Mn and Cu with organic sources of this microelement in a diet for broiler breeders had a positive effect on the humoral immune response of their progeny, i.e. on serum antibody levels against Newcastle disease virus after vaccination.

In a study with older laying hens (72-80 weeks of age) partial (i.e. 50%) replacement of inorganic microelements (Zn, Mn and Cu) with organic sources positively influenced egg weight and significantly decreased egg loss, without affecting egg production, FCR, or eggshell quality (Maciel et al., Reference MACIEL, SARAIVA, AGUIAR, PASSOS and SILGA2010). In a recent experiment (Stefanello et al., Reference STEFANELLO, SANTOS, MURAKAMI, MARTINS and CARNEIRO2014), diet supplementation with increasing levels of Zn, Mn, and Cu proteinates did not affect egg production or FCR; however, it had a positive influence on eggshell quality, i.e. shell breaking strength, thickness and reduced egg loss. A beneficial effect of organic microelements in laying hen nutrition was reported by Gheisari et al. (Reference GHEISARI, SANEI, SAMIE, GHEISARI and TOGHYANI2011), who found that supplementation of a corn-soybean diet with Zn, Mn, and Cu amino acid complexes, at a dosage 50% to 75% lower than NRC recommendations, was sufficient to obtain good egg performance, and was able to improve eggshell and egg albumen qualities.

Recent studies by Favero et al. (Reference FAVERO, VIEIRA, ANGEL, BESS, CEMIN and WARD2013a; Reference FAVERO, VIEIRA, ANGEL, BOS-MIKICH, LOTHHAMMER, TASCHETTO, CRUZ and WARD2013b) evaluated organic amino acid complexes of Zn, Mn, and Cu added to Cobb 500 breeder hen diets containing inorganic sulphates of these microelements. The obtained results indicated that diet supplementation with simultaneous inorganic and organic forms of Zn, Mn, and Cu significantly improved eggshell quality, in terms of eggshell weight and thickness, decreased early embryo mortality, and improved selected bone mineralisation parameters, i.e. tibia calcification, thickness, and moment of inertia in embryos and hatching chicks. Sun et al. (Reference SUN, GUO, MA, YUAN, AN and LI2012) reported that organic sources of Zn, Mn, Cu and Se (Mintrex) added to the diet for broiler breeders instead of inorganic forms of these microelements had a positive effect on lipid metabolism (decreased plasma cholesterol and triglycerides, increased yolk triglycerides via increasing HDL and decreasing LDL, and very low-density lipid protein cholesterol (VLDL) in plasma) and on the growth performance of their offspring. As the authors concluded, organic mineral supplementation in the diets protected breeders from lipid peroxidation, increased egg nutrition retention, and benefitted the growth of subsequent broiler progeny (Sun et al., Reference SUN, GUO, MA, YUAN, AN and LI2012).