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Cholesterol quality of edible eggs produced by quail fed diets containing probiotic and/or ginger (Zingiber officinale)

Marwa Ibrahim Khalifa and Enas Ahmed Noseer1

Department of Food Hygiene, Faculty of Veterinary Medicine, Aswan University, 81528 Sahary City, Egypt
mrwakhalifa@yahoo.com
1 Department of Biochemistry, Faculty of Veterinary Medicine, Aswan University, 81528 Sahary City, Egypt

Abstract

Quail eggs are nutritious food. But its high contents of cholesterol make it limited in use for some consumers of hyperlipidemia. Probiotics (Lactobacillus and Saccharomyces) and ginger (Zingiber officinale) were inoculated in laying quail diet to investigate the effect on serum and yolk cholesterol. Three groups of laying quail were fed on a basal diet with; probiotics, ginger, and probiotic plus ginger and compared with control group which feed on basal diet only. The obtained results declared that the group fed on combination of probiotics with ginger was the lowest in total cholesterol levels in serum and yolk (107.05 mg/dl and 10.6 mg/g) respectively comparing to control group (158 mg/dl and 14.1 mg/dl), along with an increase in high density lipoprotein-cholesterol and decrease of low density lipoprotein-cholesterol (P < 0.001). This study concludes that probiotics are the alternative strategy in breeding of quail instead of antibiotics.

Keywords: egg traits, feed additives, probiotic, yolk cholesterol


Introduction

Quail eggs are considered as healthy nutritious food. Quail eggs having very high levels of vitamin A, thiamine and riboflavin improve immunity, vision, and nerve health. Moreover, quail egg is recommended to allergic patients who couldn't consume chicken egg due to ovomucoid (glycoprotein enzyme in quail egg white) is a natural anti-allergic protein and powerful inhibitor of the human trypsin. Their modes of action differ from common antihistaminic agents -which blocking histamine receptors, ovomucoid contacts with allergens and preventing it before activating immune cells and initiation of physiological cascade and therefore protect viability and wellness of cells.

On the other hand, the formation of the quail egg is characterized by a higher yolk to white concentration. That yolk is a cholesterol stock. Cholesterol levels in quail egg are about 844 mg/ 100 g while chicken egg contains 372 mg/ 100g (USDA 2018).

Cholesterol is a type of fat that is part of all animal cells in which composes 30% of animal cell membranes and produced by the liver and made by most cells. (Sadava et al 2011). It is essential for building and maintains the body’s metabolic processes. Several molecules synthesized by different biochemical pathways including all steroid hormones and vitamin D. But the major risk for cardiac problems is higher concentrations of circulating cholesterol. ATP III (2002).

That huge cholesterol amount in quail eggs may be unsuitable for consumers with hypercholesterolemia. This means depriving hyper-cholesterol patients of other benefits of quail eggs.

To reduce this amount of cholesterol in quail eggs farmers may add hypocholesterolimic drugs like statins, HMG‐CoA reductase inhibitors, acyltransferase inhibitors, fibrates, bile resins, sodium bile transporter inhibitor. These drugs may of adverse effects on bird fertility, muscle activity or human health. The medicinal plants look like a suitable solution. (Cenedella 2003; West et al 2004).

Among medicinal plants family of Zingiberaceae members such as ginger and turmeric (curium) are known by its hypocholestremic effects and classified as safe for use according to FDA. (Alternative Medical Review 2003).

Ginger (Zingiber officinale) is a herbal plant rich in pharmacological active compounds. These compounds make ginger -besides being a spice- of great medicinal activities. It acts as anti-inflammatory, antimicrobial, circulation stimulator and thus helps in lowering total cholesterol levels. Ginger can keep the viability of the blood vessels walls by inhibiting oxidation of low density lipoproteins (LDL-c) as well as lowering absorption of cholesterol by the liver. (Bahat et al 2013).

Several former studies were used ginger in poultry diet as additives to improve production and performance (Akbarian et al 2011; Herve et al 2019).

Probiotics particularly lactic acid producing organisms are a pure culture of desirable microorganisms of great health consequence. It is improving the intestinal environment to increase the absorption of nutrients and minerals. Besides it acts as a natural antimicrobial against gut pathogens through preventing its adherence to the gut wall. Probiotics were inoculated into animal and poultry diets in order to enhance performance by controlling the ratio of both pathogens and beneficial bacteria in the gut (Kabir 2009).

Therefore, this experiment was designed as an attempt to lowering the cholesterol levels in quail egg or at least improving high density lipoproteins (HDL-c) ratio through inoculation of ginger with probiotics in the laying quail diet.


Materials and Methods

Experimental design and birds grouping

This study was performed in the faculty of veterinary medicine, Aswan University. A total of 60 quail hens aged 35- 37 days were randomly distributed into 4 groups. Each group contains three replicates of 5 birds per each housed in clean cages at room temperature of 24 C.

All groups were feed on a basal diet for one week (age 42- 44 d) till producing the first egg. Next, the first group kept feeding on the basal diet as a control group. The other three groups feed on basal diets containing 1% ginger powder, and a combination of ginger (1%) with probiotic in water, one group feed on basal diet plus probiotic in water (2 g/ L). As shown in Table 1.

Table 1. Classification of quail groups
Groups Code Basal diet Ginger Water
Group 1 CONT basal diet 0 Normal water
Group 2 PRBT basal diet 0 Plus, probiotic
Group 3 GNGR basal diet 1% Normal water
Group 4 PBGN basal diet 1% Plus, probiotic

The balanced diets and water were given ad libitum for all groups. The investigational practice applied in this experiment was in accordance with ethical committee approval at Aswan University.

Probiotic added

Probiotic used in the experiment was a commercial product consists of a mixture of Lactobacillus acidophilus 6 billion/cfu, Saccharomyces cervisiae 2 billion/cfu.

Table 2. Quail diet composition
Ingredient Amount (%)
Yellow maize 59.9
Soybean meal 44% 24.5
Fish meal 6.5
Mazie meal 1.7
Di Ca phosphate 5.7
Bone meal 0.9
Salt 00.15
Premix 0.34
Ca carbonate 0.3
Calculated Value
Crud protein 20.1
ME, Kcal /Kg diet# 2900
Calcium 2.4 g
Available phosphorus 0.32
Suppliers per Kg ration: vit A 500 IU, vit D 1100 IU, riboflavin 4.4 mg, Ca pantothenate 12mg, Nicotinic acid 4.4 mg,Vit B12 6.6 g, folic acid 0.55 mg, menadione 1.1 mg, thiamin 2.2 mg, biotin 0.11 mg, Mn 60 mg, Zn 50 mg, Fe 30 mg Cu 5 mg, Selenium 2mg
*ME, Kcal/Kg diet = Metabolized energy
Lipids profile

The experiment considered the laying phase and extended for 2 weeks. Total cholesterol (TC), triacyolglycerol (TG), high density lipoproteins-cholesterol (HDL-c), low density lipoproteins-cholesterol (LDL-c) in serum and yolk were measured at day 15 of experiment (57 d age). Blood samples were collected from the heart on plain tubes, centrifuged, and the separated serum was submitted for analysis. The yolk measures were applied in a similar method with minor modifications. The commercial kits were purchased from Bio-diagnostic lab, Giza, Egypt.

TC and TG were analyzed through Enzymatic Colorimetric Method. In which 2 reagents (buffer – chromogen and Enzymes) were used and measured against blank, at 500nm. (492 - 550) as the method described by Fassati and Prencipe (1982).

HDL-c and LDL-c were measured according to Wieland and Seidel (1983) as described in kits pamphlet.

Egg quality tests

The external and internal egg qualities were tested:

The egg production, the egg weight, shell thickness, albumin weight, yolk weight, yolk/albumin ratio were recorded. Egg production was calculated by collecting and counting the eggs from each replicate group every day across 15 days of experiment.

Egg weight: the egg was independently weighted on a sensitive balance then broken; yolk and egg whites were isolated, weighted individually, and related as rate to entire egg weight.

The thickness of eggshell was measured by a micrometer after removal of inner membrane.

The sensory properties of eggs

The sensory properties of produced eggs were estimated to inspect consumer acceptance (taste, odor, and over all acceptability) were recorded by 7 non experienced panelists from quail breeders. The panelists were asked to examine 4 groups of quail eggs each group consists of 6 eggs (3 boiled and 3 fried) and score the quality in a 5-degree hedonic scale as previously described (Karmi et al 2019).


Results and Discussion

Cholesterol is generally required to mammalian body. Cholesterol is needed in the biosynthesis of certain hormones, vitamin D, as well as, cell walls and other physiological processes. But its high levels, especially if in the form of LDL-c, indicates high health risk factor (ATP III 2002).

External and internal egg traits

The external and internal quality of eggs produced from quail fed on probiotic and ginger indicated that treatment groups exhibited differences in egg production, egg weight, and shell thickness (Table 3). Only the group supplemented with probiotic in drinking water (PRBT) and (PBGN) induced the highest production of eggs at a rate of 316 and 320 eggs/2 weeks, respectively, as well as the highest egg weight (14.5 and 13.2 g) and shell thickness (0.220 and 0.192 mm), respectively.

The increase in egg production may be referred to low mortality rate in groups supplemented with probiotic, as the probiotics enhance absorption of calcium and phosphorus from small intestine, increase the mineralization in eggs and keep the intestinal environment healthy through competing the pathogens. Additionally, the phenolic compounds in ginger act as antioxidant, promote the ovarian health and in subsequent the egg production (Zade et al 2013). The antimicrobial properties of both ginger and probiotics minimizing inflammation and save energy for egg production. (Tchoffo et al 2017).

According to egg weight increase, the albumin and yolk weights were increased, which shadowed by an increase in yolk/ albumin ratio from 56.6 in control group to 58.9 in group 2 that supplemented by probiotic in drinking water. These findings are similar to that recorded by Akbarian et al (2011) and Kalsum et al (2012) and Zhang et al (2015).

In spite of the young age of quails used in this experiment (45- 50 d), as well as the short experimental duration (15 days), a promising result is achieved.

Previous researches conducted by Panda et al (2007) and Aghaii et al (2010) reported significant increase (p < 0.001) in egg production and egg weight of White Leghorn hens feed on probiotics containing Bacillus spp they suggested that the species variation and age of birds may be responsible for such variation.

Table 3. External and Internal Egg Quality
CONT PBRT GNGR PBGN SEM p
External egg quality
Egg production (Average no. /2wk) 294 316 310 320 0.120 0.085
Egg weight (g) 12.8 14.5 13.1 13.2 0.497 0.217
Shell thickness (mm) 0.18 0.22 0.18 0.19 0.0045 0.092
Internal egg quality
Albumin weight, g 7.53 7.94 7.55 7.68 0.062 0.
Yolk weight (g) 4.26 4.68 4.33 4.51 0.052 0.251
Yolk/Albumin ratio (%)# 56.6 58.9 57.4 58.7 - -
# Yolk / Albumin ratio was calculated by dividing mean of yolk to mean of albumin
Serum lipid profile

The species of bird, age, ration, and season of breeding may influence the levels of TC in serum and yolk, Vorlova 2001.

TC level in serum of female quail aged 59 d (8.5 wk.) and feed on basal diet was 158.5 mg/dl. This is lower than those recorded by Yalcin et al (2007) who examined serum of quail aged 21 weeks of age. The old age of birds in their experiment could explain such high TC levels.

The groups supplied with probiotic in water for 15 days, nonetheless the ginger was added or not, showed lower serum TC levels than the control group. The probiotic+ginger group (PBGN) showed the lower level of serum TC (107.1 mg/dl) among the three groups. Zeweil et al 2006 recorded similar conclusions when supplied probiotics and medicinal plants in diet of quail hens. The ability of lactobacilli to reduce gallbladder acids and decrease digestion of fats is responsible for low cholesterol and lipid levels (Corcoran et al 2005). In this study the levels of HDL-c and LDL-c in serum were significantly (P < 0.001) improved to the side of HDL-c. This indicates good health condition due to HDL-c associates in reverse cholesterol transport which remove cholesterol through liver and bile.

TG accordingly decreased in both serum and yolk in group 4 from (90.0 to 66.1 mg/dl) in serum and from (3.4 to 1.1 mg/ g) in yolk.

Figure 1. Serum lipid profile of quail groups Values represent the mean SEM of 15 quails. Paired sample T-test.
Means with (***), (**) and (*) were statistical represented compared to control group as follow: p*** < 0.001, p** < 0.01, p* < 0.05
Yolk lipid profile

The low level of serum TC leads to a decrease in yolk cholesterol too. In the present study, an increase in HDL-c and decrease in LDL-c were recorded in egg yolk of quail group (PBRT) diet on probiotic (77.1/ 49.7 mg/g), nonetheless the group 4 showed more significant rising in HDL-c/ LDL-c ratio when compared to the control group (65.4/37.6 vs. 52.2/97.1 mg/g). (Fig. 2) The hypocholesteremic effect of ginger in quail diet was accelerated when probiotic was added to water. These findings are in line with Zeweil et al 2006, Akbarian et al 2011, Kalsum et al 2012. In this context, Lokapirnasari et al 2018 reported that probiotics supplied to birds in drinking water is more effective than those in diet.

Owing to the synergism between the two mechanisms of probiotic and ginger, oligosaccharides excreted from Saccharomyces cells enhance colonization and number of lactobacilli and rheostat the pathogens (Zeweil et al 2006). Lactobacilli decrease the bile acids (cholic and deoxycholic) recycling, and adsorp cholesterol that leading to reduction of its absorption from the intestine, with subsequent lowering its level in blood, meat, and eggs (Hassanein et al 2010).

Ginger reduces intestinal sterols absorption and stimulates the blood circulation and prevents deposition of lipids on the vascular wall. (Zhang et al 2015).

The rising of HDL-c levels in quail egg more than LDL-c means that such egg is a functional food suitable for all consumers even those suffering from hypercholesterolemia, over-weight, allergy, and can inoculated safely in diet of athletics. The high HDL-c levels are a grantee against atherosclerosis by reducing oxidation of LDL-c and enhancing anti-inflammatory agents from endothelial cells.

Figure 2. Yolk lipid profiles Values represent the mean SEM of 15 quails. Paired sample T-test.
Means with (***), (**) and (*) were statistical represented compared to control group as follow: p*** < 0.001, p** < 0.01, p* < 0.05
Sensory properties & consumer acceptance of egg

The sensory traits of quail eggs were investigated as an indicator of consumer acceptance. The panelists regard that (PBRT) probiotic- treated group is the best one in taste, odor (characteristic non- pronounced) and over all acceptability (Fig. 3). On the other hand, group GNGR (ginger-treated group) was the less acceptable one due to a tiny bitter flavor sensed at the end of eating. Group PBGN (probiotic and ginger combination-treated group) may soften this defect as the probiotic overcome the bitterness taste of ginger.

Probiotics alone or in combination with ginger in quail diet is considered the active safe scheme to improve egg cholesterol quality and rising HDL-c ratio with subsequent avoidance of risk on human or bird health, harmful residues, or withdrawal period.

Figure 3. Sensory evaluation of quail egg


Conclusions


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Received 3 September 2019; Accepted 18 September 2019; Published 2 October 2019

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