Effects of Replacing Inorganic with Respective Complexed Glycinate

Minerals on Apparent Mineral Bioavailability and Deposition Rate

in Tissues of Broiler Breeders

Wanjing Sun

1,2

& Geng Wang

1,2

& Xun Pei

1,2

& Lujie Liu

1,2

& Zhiping Xiao

1,2

& Wenjing Tao

1,2

Muhammad Umar Yaqoob

1,2

& Minqi Wang

1,2

& Mingyan Huai

& Lily Li

& Wolf Pelletier

Received: 3 December 2019 /Accepted: 27 February 2020

Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract

The study was conducted to evaluate the effects of replacing inorganic trace minerals (ITMs) with respective low-dose com-

plexed glycinate minerals (CGMs) on their bioavailability and retention during peak laying period of broiler breeders. In this

experiment, 648 ZhenNing broiler breeders (23 weeks old) were randomly allocated to four treatments with six replicates (27

birds/replicate) and fed for 14 weeks including 2 weeks adaptation period. The treatments were T1—ITM, commercially

recommended levels of ITMs (Cu, Zn, Fe, and Mn sulphates); T2—MIX, half of the minerals were supplemented with ITMs

and half with CGMs; T3—L-CGMs, minerals were supplemented with CGMs (50% level of T1); and T4—M-CGMs, minerals

were supplemented with CGMs (70% level of T1). The results showed that birds fed on ITM had lower bioavailability of Fe, Mn,

andZn(P < 0.05) than those fed on L-CGMs, but the highest (P < 0.01) bioavailability of Cu was found in those fed on MIX.

Mineral retention (in serum, muscle, bone, and tissues) was not affected by reducing supplementation levels of trace minerals up

to 50% of ITMs, but Zn (in serum, liver, kidney, heart, and albumen) and Fe (in serum and the yolk) retention was negatively

affected (P < 0.05). In conclusion, replacing dietary ITMs with low-dose complexed glycinate minerals increases the apparent

bioavailability of Fe, Mn, and Zn without compromising the mineral retention rates in most of the tissues tested.

Keywords Trace mineral

Complexed glycinates

Bioavailability

Deposition

Excretion

Broiler breeders

Introduction

Trace minerals play a vital role in the metabolic processes [1]

by acting as catalysts in many hormonal and enzymatic path-

ways which affect growth, feathering, structure, and overall

production performance of birds [2]. Iron (Fe) is a significant

component of myoglobin and haemoglobin for oxygen trans-

port and cellular use [3] and participates in energy supplying,

immunization, and the process of antioxidation [4]. Severe

manganese (Mn) deficiency shows long bone thickening and

shortening, joint deformity and swelling, and curved and

distorted tibial bone [5]. Similarly, zinc (Zn) is an important

structural and function constituent of metalloenzymes [6, 7].

Despite tremendous advances in poultry technology and pro-

duction, the research on trace mineral nutrition has lagged far

behind other nutrient fields [8]. At a commercial level, inor-

ganic trace minerals (ITMs) are supplemented more than the

NRC recommendation [9, 10] to maximize production perfor-

mance. Due to supplementation of high safety margin and low

retention rates, majority of ingested minerals are excreted to

the environment [11]. Poultry manure is used as fertilizer, but

the contents of Zn and copper are about 660% and 560%

above the standard levels, respectively, [12] which negatively

affect the crop requirements; thence, supplementation with a

high level of ITMs not only wastes the resources but also

pollutes the environment irreversibly. In recent years, aware-

ness on preventing livestock manure pollution, reduction of

mineral supplementation in livestock, and poultry nutrition

without compromising health and growth performance have

become very popular [11].

* Minqi Wang

wangmq@zju.edu.cn

College of Animal Science, Zhejiang University, Hangzhou 310058,

China

Key Laboratory of Animal Nutrition and Feed Science in Eastern

China, Ministry of Agriculture, Zhejiang University,

Hangzhou 310058, China

BASF SEA Pte Ltd, Singapore 038987, Singapore

BASF SE, 78354 Ludwigshafen, Germany

Biological Trace Element Research

https://doi.org/10.1007/s12011-020-02102-1

Organic trace minerals (OTMs) have higher bioavailability

than ITMs, so OTMs could be supplemented at a lower level

without any negative effect on growth and production perfor-

mance in broilers [13, 14]. In literature, most studies on OTMs

in broiler breeders focused on replacing one or two elements,

and limited data are available on the simultaneous replace-

ment of ITMs, i.e. Cu, Zn, Fe, and Mn, by OTMs at different

levels in order to identity the economically viable and nutri-

tionally optimal replacement ratio. This study was designed to

establish the optimal replacement level of ITMs (Cu, Zn, Fe,

and Mn) with OTMs for their optimal retention rate in serum,

tissue, and egg and bioavailability in broiler breeders during

the peak laying phase.

Materials and Methods

The conduct and design of this experiment were approved by

the Zhejiang University Animal Research Ethics Board and

were in accordance with the standard of the China Council for

Animal Care (No.11992).

Bird Husbandry

In this experiment, 648 “ZhenNing” yellow feather broiler

breeders (23 w eeks old, pr ovided by Ning bo ZhenNing

Animal Husbandry Ltd.) with similar body weight (1.40 ±

0.002 kg) were randomly allocated to four dietary treatments

with six replicates (27 breeders per replicate) and fed for

12 weeks after 2 weeks adaption period. The breeders were

fed twice a day, and the water was offered ad libitum. Three

birds were housed in a cage (cage dimensions were 50 × 50 ×

50 cm

) under ambient environmental conditions, and all

managements were conduc ted according to commercial

operations.

Dietary Treatments

A corn-soybean meal-based diet (Table 1) was formulated

according to National Research Council (NRC 1994) [9]rec-

ommendations and supplemented with different doses and

sources of mineral premix (Table 2). The dietary treatments

consisted of T1—ITM, basal diet + 100% ITMs (commercial-

ly recommended levels of Cu, Fe, Mn, and Zn sulphate were

supplemented, and their concentrations were 8, 60, 60, and

80 mg/kg feed, respectively); T2—MIX, basal diet + 50%

ITMs + 50% complexed glycinate minerals (CGMs) (concen-

tration of Cu, Fe, Mn, and Zn was maintained at the level of

T1, but in each case, half of the minerals were inorganic and

half were complexed glycinates); T3—L-CGMs, basal diet +

50% CGMs (concentration of Cu, Fe, Mn, and Zn was re-

duced to 50% than T1, and all minerals were complexed

glycinates) ; and T4—M-CGMs, basal diet + 70% CGMs

(concentration of Cu, Fe, Mn, and Zn was reduced to 70%

than T1, and all minerals were complexed glycinates).

Inorganic trace minerals (Cu, Zn, Fe, and Mn sulphates)

were purchased from the market. Glycine-complexed trace

Table 1 Composition and nutrient levels of basal diets (%)

Ingredients (%) Nutrient levels

Corn 63.50 ME (MJ/kg) 11.41

Soybean meal 19.00 CP 16.73

Fish meal 2.50 EE 4.08

Wheat bran 1.50 CF 3.29

Soybean oil 1.60 Lys 0.84

Shell powder 7.50 Met 0.39

Limestone 1.80 Ca 3.88

CaHPO4 1.10 TP 0.61

NaCl 0.20 Cu 14.7

NaHCO

0.30 Fe 281.6

Met 0.10 Zn 83.9

Choline (50%) 0.10 Mn 91.6

Titanium dioxide 0.30

Vitamin premix

0.20

Trace element premix

0.30

Phytase

Total 100%

Provided per kilogram of diet: VA 8000 IU, VD 1600 IU, VE 5 mg, VK

0.5 mg, VB1 0.8 mg, VB2 2.5 mg, VB5 2.2 mg, VB3 20 mg, VB6 3 mg,

VB7 0.1 mg, VB9 0.25 mg, VB12 0.004 mg

Premix according to the experimental design

BASF SE, Natuphos E 10000, 50 g/t feed, which was premixed with

vitamin and trace mineral premixes prior to feed preparation

ME based on calculated values; others are measured values

Table 2 Ex perimental treatments and supplemental levels of trace

minerals (mg/kg)

mg/kg ITM MIX L-CGMs M-CGMs

Supplemental

Cu 8.0 8.0 4.0 5.6

Fe 60 60 30 42

Zn 80 80 40 56

Mn 60 60 30 42

Analyzed

Cu 22.0 22.5 18.3 20.8

Fe 331.5 337.3 305.7 320.7

Zn 165.3 164.6 123.4 140.2

Mn 147.8 153.5 124.6 136.9

The calculated level of Cu, Fe, Zn, and Mn in basal diet is 15.9, 274.1,

87.3, and 86.7 mg/kg. Glycinate minerals were used in both L-CGMs and

M-CGMs, and inclusion level was reduced to 50% and 70%, respectively

ITM inorganic minerals (sulphate salts), MIX 50% inorganic + 50%

glycinate

Sun et al.

minerals (min 21% Fe-glycinate Fe, min 26% Zn-glycinate

Zn, min 21% Mn-glycinate Mn, and min 24% Cu-glycinate

Cu) were provided by BASF (China) Co., Ltd.

Sample Collection and Analysis

At the end of the feeding trial, three broiler breeders were

randomly selected from each replicate (18 hens per treatment)

and fasted for approximately 12 h before slaughtering. Blood

samples were collected from the main wing vein and placed in

a coagulant tube; serum samples were isolated from the blood

by centrifuging (TDL-80-2B, Anting Scientific Instrument

Factory, Shanghai, China) at 630×g for 15 min at 4 °C and

stored at −80 °C until future analysis. Birds were killed by

cervical dislocation and dissected to get samples of different

tissues (heart, liver, kidney, pancreas, right tibia, and pectoral

muscle) and stored at −80 °C for later analysis. For egg min-

eral retention analysis, six eggs per replicate were collected

(total, 144 eggs) on the 12th week. Faecal samples were col-

lected in the middle (6th week) and the last day of the feeding

trial (12th week). The faeces, feed, and tibia samples were

oven dried at 105 °C for 24 h until constant weight, ground

to particle size of 0.425 mm, mixed, and then kept in a desic-

cator for further analysis.

The samples were subjected to microwave (MARS 5, CEM

Corp., USA) digestion to analyze the content of Cu, Zn, Fe,

and Mn by a fl ame atomic abs orpt ion spect ro phot om ete r

(ICE-3500, Thermo Corp., USA). The mineral contents of

selected organs and muscles were expressed on a wet basis

whereas those of feeds, excreta, and tibia on a dry basis.

Approximately 1 g of tissue sample was predigested with

6 mL nitric acid in the microwave digestion system for

3 min at 120 °C, 8 min at 180 °C, and 4 min at 230 °C until

the solution turned to faint yellow in color, followed by dilu-

tion of residual acid with double distilled water up to 50 mL.

The feeds, excreta, and tibia samples were carbonized in a

fume hood until the samples get dark, then burned in a muffle

furnace at 600 °C for 4 h, dissolved in nitric acid, and diluted

with double distilled water for mineral retention analysis.

To determine the apparent bioavailability of trace minerals

(BTM), using Ti as the indicator, the concentration of Ti in

feed and faeces was measured using the similar method. BTM

(%) = 100 × (1-Ir × Nf/(If × Nr)), where Ir is the content of

indicator in feed (%), If is the content of indicator in faeces

(%), Nr is the content of trace minerals in feed (%), and Nf is

the content of trace minerals in faeces (%).

Statistical Analysis

All data were analyzed by one-way ANOVA using SPSS 20.0,

in which each replicate was defined as the statistical unit. Data

were expressed as the mean and SEM (standard error of the

mean). Statistically significant differences among treatments

were found by LSD test. A significant level of 0.05 and ex-

tremely significant level of 0.01 were used for estimating dif-

ferences among treatments, respectively. A probability of

P < 0.1 was described as a trend.

Fig. 1 Effect of replacing

inorganic with respective

complexed glycinate minerals on

apparent bioavailability of trace

minerals in broiler breeders. All

data were presented as mean and

SEM, n = 6. One asterisk (*)

indicates significant difference

(P < 0.05), and two asterisks (**)

indicate highly significant

difference (P <0.01)

Table 3 Effect of replacing inorganic with respective complexed

glycinate minerals on serum mineral concentration in broiler breeders

Index/Treatment ITM MIX L-CGMs M-CGMs SEM P value

Cu (mg/kg) 0.57 0.56 0.56 0.56 0.012 0.981

Fe (mg/kg) 1.31

1.24

1.21

0.016 0.058

Mn (mg/kg) 0.30 0.30 0.30 0.30 0.012 0.999

Zn (mg/kg) 0.29

0.27

0.23

0.25

0.007 0.003

Within the same row, values with different superscripts indicate signifi-

cant difference (P <0.05)

Effects of Replacing Inorganic with Respective Complexed Glycinate Minerals on Apparent Mineral...

Results

Apparent Bioavailability of Trace Minerals

The apparent bioavailability of trace minerals in broiler

breeders offered different mineral sources and levels is shown

in Fig. 1. Supplementation of OTMs differently affected the

BTM. Bioavailability of Fe (P <0.001), Mn (P =0.023), and

Zn (P = 0.030) was significantly higher in the L-CGMs than in

the ITM treatment while the MIX treatment had significantly

higher bioavailability of Cu (P < 0.001) than the ITM treatment.

The Fe bioavailability of ITM was significantly lower than that

of M-CGMs (P < 0.05) and extremely lower than that of MIX

andL-CGMsby9.51%and10.98%,respectively(P <0.001).

Mineral Retention in Serum

Data regarding serum mineral contents are presented in

Table 3. Birds fed on the ITM diet (100% sulphate) had sig-

nificantly higher (P < 0.05) Fe and Zn concentration in serum

than those fed on either the L-CGMs or M-CGMs diet. No

significant effect of the different dietary treatments was ob-

served on Cu and Mn retention in serum, and results suggested

that supplementation of CGMs at a lower level had no nega-

tive effect on Cu and Mn concentrations in serum.

Mineral Retention in Different Tissues and Eggs

Trace mineral deposition in the muscle and various tissues

was not affe cted (P > 0.05) by the supplemental levels or

source of trace minerals in the diet, except Zn retention in

the liver, kid ney, and heart which was significantly lower

(P < 0.05) in L-CGMs than in ITM (Tables 4, 5, 6, 7, 8,and

9). Similarly, trace mineral deposition in the pancreas, pectoral

muscle, and tibia was not affected by the dietary treatment.

AsshowninTable10, replacing ITMs with low-dose

CGMs influenced albumen Zn and yolk Fe contents.

Albumen Zn in L-CGMs was significantly lower (P <0.004)

than the rest of the treatments. Fe deposition in the yolk was

higher (P < 0.001) in the ITM and MIX than in the L-CGMs

and M-CGMs treatments.

Mineral Excretion in Faeces

Data regarding mineral excretion under different dietary treat-

ments is presented in Fig. 2. Significantly lower Cu excretion

was found in L-CGMs (P < 0.01) and MIX (P < 0.05) than in

the ITM treatment. Faecal Mn and Zn excretion in L-CGMs

and M-CGMs was significantly (P < 0.01) lower than that of

the ITM and MIX treatments. Similarly, the significantly

(P < 0.01) lowest Fe excretion was observed in the L-CGMs

treatment.

Discussion

Superior bioavailability of organically bound Mn [15]andZn

[16 ] in broilers and extra nutritional benefits of other trace min-

erals to laying hens [17], pigs [18], and turkey [19] have been

reported, and corresponding results were found in the present

experiment. The actual reason for higher bioavailability of

Table 4 Effect of replacing inorganic with respective complexed

glycinate minerals on liver mineral concentration in broiler breeders

Index/

Treatment

ITM MIX L-CGMs M-CGMs SEM P value

Cu (mg/kg) 6.03 5.73 5.56 5.62 0.143 0.698

Fe (mg/kg) 159.00 152.86 147.87 151.20 3.681 0.777

Mn (mg/kg) 4.83 4.49 4.24 4.29 0.111 0.228

Zn (mg/kg) 66.59

63.04

56.00

59.16

1.738 0.149

Within the same row, values with different superscripts indicate signifi-

cant difference (P <0.05)

Table 5 Effect of replacing

inorganic with respective

complexed glycinate minerals on

kidney mineral concentration in

broiler breeders

Index/

Treatment

ITM MIX L-CGMs M-CGMs SEM P value

Cu (mg/kg) 4.12 3.94 3.64 3.83 0.112 0.504

Fe (mg/kg) 90.09 88.52 82.00 82.91 2.224 0.511

Mn (mg/kg) 3.45 3.44 3.29 3.22 0.072 0.620

Zn (mg/kg) 34.16

32.29

28.70

31.32

0.717 0.043

Within the same row, values with different superscripts indicate significant difference (P <0.05)

Table 6 Effect of replacing inorganic with respective complexed

glycinate minerals on heart mineral concentration in broiler breeders

Index/

Treatment

ITM MIX L-CGMs M-CGMs SEM P value

Cu (mg/kg) 1.10 1.11 1.10 1.07 0.011 0.691

Fe (mg/kg) 55.87 54.62 52.77 53.60 0.879 0.657

Mn (mg/kg) 0.23 0.23 0.23 0.23 0.005 0.990

Zn (mg/kg) 32.37

30.82

28.22

29.38

0.687 0.160

Within the same row, values with different superscripts indicate signifi-

cant difference (P <0.05)

Sun et al.

OTMs is not yet clear , but it is proposed that the organically

bound trace minerals may go through an alternative absorption

pathway at the tissue and cellular level, which might be the

reason for less excretion of minerals and hence meet the optimal

growth requirements [2, 8]. Results of the current experiment

exhibited that CGMs at reduced levels have a potential to pro-

vide more Fe, Mn, and Zn than at higher levels of ITMs, as

anticipated earlier that reduced supplementation of organic Mn

improved its intestinal assimilation than at higher levels in in-

organic form [20]. Higher BTM in complexed glycinate form

might be due to the small molecular weight of glycine and its

good stability in the gastrointestinal tract; glycine prevents the

release of ferrous ion at an undesired place and restricts it from

involving in undesirable biochemical responses during its tran-

sit through the gastrointestinal tract which negatively affected

the absorption of Fe [21].

Retention of trace minerals in different tissues and organs is

also an important parameter regarding proper growth and de-

velopment of birds and essentially required to produce good-

quality eggs in breeders. In this experiment, serum levels of

Zn and Fe were increased with increasing their dietary supple-

mental levels. However, no difference was observed for serum

Cu and Mn levels by reducing their dietary levels in glycine-

complexed form than at higher levels in ITMs form; enhanced

retention in organic form might be due to its less interactive

conditions under this form [22]. On the contrary, reduced se-

rum Cu concentration was detected in chicken fed on dietary

supplemental amino acid-hydrate complex [23]. The inconsis-

tency in this result might be due to various reasons including

different organic sources, supplementation levels of trace min-

eral, strain of the bird, and experiment conditions.

Tissue mineral concentrations are usually determined to

assess the mineral status of humans and animals. A positively

linear relationship between dietary and whole-body Fe con-

centration in swine when FeSO

was supplemented in the diet

hasbeenreported[24], and corresponding results were found

in the present study. Consistent with our study, Cao et al. [25]

reported that Fe concentrations in the liver, spleen, and kidney

were enhanced with the increasing dietary levels of Fe.

Kulkarni et al. [21] reported that supplementation of glycinate

minerals enhanced the Fe retentions in tissues than inorganic

ferrous sulphate. Additionally, elevated liver and kidney status

of Fe was found by dietary supplementation of glycine-

complexed Fe [26], might be due to easier absorption of Fe-

glycinate (Fe-Gly) than FeSO

. A combination of iron and

glycine sequestration improved the membrane permeability

and stability of Fe-Gly [27] which enhanced the passive ab-

sorption of Fe and could be the reason for better absorption of

Fe than its inorganic form. The results of the present study

Table 8 Effect of replacing inorganic with respective complexed

glycinate minerals on pectoral muscle mineral concentration in broiler

breeders

Index/

Treatment

ITM MIX L-CGMs M-CGMs SEM P value

Cu (mg/kg) 0.55 0.55 0.52 0.54 0.009 0.576

Fe (mg/kg) 5.85 5.85 5.15 5.74 0.159 0.364

Mn (mg/kg) 0.13 0.13 0.13 0.13 0.002 0.927

Zn (mg/kg) 5.74 5.80 5.31 5.55 0.116 0.463

Within the same row, values with different superscripts indicate signifi-

cant difference (P <0.05)

Table 7 Effect of replacing inorganic with respective complexed

glycinate minerals on pancreas mineral concentration in broiler breeders

Index/

Treatment

ITM MIX L-CGMs M-CGMs SEM P value

Cu (mg/kg) 2.06 2.00 1.91 1.95 0.062 0.860

Fe (mg/kg) 50.60 49.74 46.94 48.43 1.713 0.899

Mn (mg/kg) 3.27 3.25 3.19 3.25 0.098 0.994

Zn (mg/kg) 52.80 51.30 49.56 50.97 1.423 0.898

Within the same row, values with different superscripts indicate signifi-

cant difference (P <0.05)

Table 9 Effect of replacing inorganic with respective complexed

glycinate minerals on tibia mineral concentration in broiler breeders

Index/

Treatment

ITM MIX L-CGMs M-CGMs SEM P value

Cu (mg/kg) 0.81 0.81 0.74 0.69 0.068 0.922

Fe (mg/kg) ––– – ––

Mn (mg/kg) 6.47 5.95 6.20 6.03 0.320 0.950

Zn (mg/kg) 143.72 147.90 154.26 141.16 2.881 0.420

Fe was not detected. Within the same row, values with different super-

scripts indicate significant difference (P <0.05)

Table 10 Effect of re placing inorganic wi th respective complexed

glycinate minerals on egg mineral concentration in broiler breeders

Index/

Treatment

ITM MIX L-CGMs M-CGMs SEM P value

Albumen

Cu (mg/kg) 0.30 0.29 0.27 0.28 0.007 0.367

Fe (mg/kg) 6.54 6.44 6.25 6.29 0.111 0.802

Mn (mg/kg) 1.62 1.62 1.60 1.61 0.012 0.961

Zn (mg/kg) 0.62

0.60

0.52

0.58

0.011 0.004

Yolk

Cu (mg/kg) 1.11 1.12 1.09 1.10 0.011 0.766

Fe (mg/kg) 2.83

2.72

2.20

2.41

0.064 <0.001

Mn (mg/kg) 13.97 13.97 13.68 13.69 0.150 0.847

Zn (mg/kg) 15.84 15.44 15.24 15.79 0.190 0.654

Within the same row, values with different superscripts indicate signifi-

cant difference (P <0.05)

Effects of Replacing Inorganic with Respective Complexed Glycinate Minerals on Apparent Mineral...

proposed that CGMs have the potential to fulfil the trace min-

eral requirements of the tested organs at lower levels than

higher levels of ITMs. Mn is one of the least toxic trace min-

erals in animals due to its low intestinal absorption rate and the

great ability of the liver to excrete Mn [28]. The liver plays a

pivotal role in Mn homeostasis; when Mn is absorbed over the

requirement, the liver excreted it via the bile. The bone is a

complex heterogeneous organization that sustains muscle tis-

sue [29]. Analyzing the concentration of Mn in the tibia is a

good indicator for predicting the whole-body growth because

Mn deficiency could cause abnormal bone development

which negatively affected the overall growth performance;

additionally, Mn requirements of poultry are much higher than

that of ruminants and swine [30]. In this experiment, no sig-

nificant difference was observed for Mn retention in the tibia

by feeding low-dose CGMs than high-level supplementation

of ITMs.

Minerals are deposited into the eggs via two different ways,

i.e. through the oviduct to the egg albumen or ovary to ovum

yolk [31]. The yolk plays a crucial role in the storage of nu-

trients required for proper growth and development for future

offspring. Results of the current study exhibited a positive

relationship between dietary and yolk Fe concentration; how-

ever, albumen Fe contents were not affected by dietary treat-

ments. No significant effect of dietary treatments was ob-

served for different trace mineral retentions in different com-

ponents of the egg except lower albumen Zn and yolk Fe in L-

CGMs and only yolk Fe in the M-CGMs treatment. A lower

dose of Cu and Mn in CGMs form was enough to fulfil their

requirements in egg retention.

Dietary supplementation of CGMs significantly reduced

the mineral excretion in the excreta. Only 50% replacement

of ITMs with CGMs decreased the excreta content of Cu, Fe,

Mn, and Zn by 19.2%, 7.8%, 10.6%, and 19.5%, respectively,

and these results are supported by the findings of El-Husseiny

et al. [14]. Similarly, Zhao et al. [32] also reported that broilers

fed on diet supplemented with a lower level of chelated Zn,

Mn, and Cu had decreased mineral excretion in faeces com-

pared with the high levels of ITM. The results of the present

study demonstrate that supplementation of OTM at lower

levels (50% of commercially recommended levels) reduced

the mineral excretion and ultimately decreased the harmful

effects on the environment.

Conclusion

In summary, it could be stated that complexed glycinate min-

erals are biologically more available even at lower supple-

mented levels than ITMs. Reduced dietary levels (50% of

ITMs) of complexed glycinate minerals have the potential to

accomplish the serum, muscle, bone, and selected organ min-

eral retention requirements except Zn in the liver, kidney,

heart, and albumen and Fe in the yolk.

Acknowledgements This study was supported by the Three Agricultural

and Six-Party Research Cooperation Project of Zhejiang Province, China

(No. CTZB-F180706LWZ-SNY1). We acknowledge the great support

from the Ningbo ZhenNing Animal Husbandry Ltd. and Lei Lu for the

technical support in sample collection.

Compliance with Ethical Standards

Competing Interests The authors declare that there are no conflicts of

interests.

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