Hypocholesterolemic effects of organic and inorganic copper supplements: O.M.O. Idowu et al.
The effects of dietary intake and dietary concentration of
organic and inorganic copper supplements on egg and
plasma cholesterol levels
O.M.O. IDOWU*, O.A. KUYE, V.O. OLADELE-OJO, and D. ERUVBETINE
Department of Animal Nutrition, University of Agriculture, Abeokuta, Nigeria
*[email protected]
Keywords: copper source and dosage; cholesterol status; residue in egg and tissue
Summary
To evaluate the effect of source and dosage of supplemental copper on cholesterol contents of the
egg, blood plasma, liver and excreta, and to determine the levels of copper residue in the liver, egg
yolk, whole egg and excreta of laying hens. One hundred and eight 35-week old Black Harco laying
hens were randomly assigned to 6 dietary treatments in a 2 X 3 factorial arrangement of treatments.
The copper sources were copper proteinate (CuP) and copper sulphate pentahydrate (CuSO4.5H2O)
fed at three dosages (0, 125 and 250 mgCu kg -1) respectively for a 10 weeks periods. Whole egg and
egg yolk cholesterol concentrations of CuP supplemented diets were significantly (P<0.05) lowered
than those of CuSO 4.5H2O supplemented diets. However, more cholesterol were excreted by hens fed
CuP supplemented diets. Liver and plasma (free, ester and total) cholesterol concentrations of hens
fed CuSO4.5H2O supplemented diets were higher than those on CuP diets. Similar trend was also
noticed in the plasma lipoprotein fractions and triacylglyceride concentrations. Egg, yolk cholesterol,
plasma cholesterol, lipoprotein and liver cholesterol concentrations reduced linearly (P<0.05) as Cu
dosage increased from 0 to 250 mgCu kg-1 . Significant interaction (P<0.05) of Cu source and dosage
was noticed in the egg and yolk cholesterol concentrations. Hens fed diets supplemented with CuP
had a higher (P<0.05) liver and excreta Cu residue than those fed CuSO4.5H2O. There was no
difference (P>0.05) in Cu residues values of the excreta, whole egg and egg yolk in both Cu sources.
Cu residue levels in the liver, whole egg, egg yolk and the excreta increased in a Cu dosage
dependent manner. Cu residue levels were significantly influenced by the interaction of Cu source and
dosage.
Introduction
The cholesterol levels in eggs has been reported to be about twice the cholesterol content of butter
and freeze meat products and was 5-10 times more than cholesterol found in most dairy products
(Anon,1990). Efforts have therefore been made to lower egg cholesterol through manipulation of
dietary protein and energy contents and the use of dietary fibre which are known to be
hypocholesterolemic (Lirette et al., 1993 and idowu et al., 2002). Pesti and Bakalli (1998) obtained a
reduction in egg yolk cholesterol concentration when 125mg Cu / kg diet was fed to White Leghorn
hens and further decline in egg cholesterol was noticed when 250mg Cu / kg was fed. Pesti and
Bakalli (1998) demonstrated that pharmacological levels of Cu ( > 250mg/kg diet) caused changes in
17 β –estradiol and enzymes involved in carbohydrate, lipid and amino acid metabolism in matured
hens.
Research evidences have shown that copper regulates cholesterol biosynthesis by reducing hepatic
glutathione concentrations (Kim et al., 1992). Glutathione is known to regulate cholesterol biosynthesis
through the stimulation of the enzyme 3- hydroxy-3-methyl glutaryl coenzyme A (HMG-Co A)
reductase in rats (Valsala and Kurup, 1987). The HMG-Co A reductase activity is the rate –limiting
step of mevalonate and ultimately, cholesterol synthesis.
However the maximum dietary tolerable level of copper for poultry was set at 300mg kg-1 according
to NRC (1994). In a study on the estimation of the relative bioavailability of inorganic copper sources
for chicks using tissue uptake, Ledoux and Henry (1991) reported that high level of dietary copper in
the sulphate form significantly increased copper concentration in the liver. Jensen et al. (1991)
observed slight to severe oral and gizzard damage upon an increase of dietary copper to 500mg kg-1 .
Jackson et al. (1979) noted that concentration of copper in the liver increased rapidly at 600 and 800
XI th European Symposium on the Quality of Eggs and Egg Products
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Hypocholesterolemic effects of organic and inorganic copper supplements: O.M.O. Idowu et al.
mg kg-1 dietary level of copper. Chiou et al. (1997) reported that copper residues in the liver and
excreta were significantly (P<0.05) increased as dietary copper increased. Copper residue in egg was
reported by the same worker to be 4.7mg kg-1 at 400 mg kg-1 dietary copper. This study was aimed at
determining the comparative effects of organic and inorganic copper source on egg and plasma
cholesterol in laying hens as well as the copper residue in egg and tissues.
Materials and methods
EXPERIMENTAL DESIGN AND FEEDING
A total of one hundred and eight Black Harco layer strain (35 weeks of age) were allocated into six (6)
dietary treatment groups in a 2 X 3 factorial arrangement of treatments replicated thrice. Treatments
were basal diet supplemented with inorganic Cu (CuSO4.5H2O, Sigma Chemical, St! Louis, MO,
U.S.A.) and organic Cu ( Cu Proteinate, Bioplex Copper, Alltech, Nicholasville, KY, U.S.A) at 0,125
and 250mg Cu/kg of basal diet respectively. The basal diet was a standard ration which is known to
support good performance and it contained in grams per kilogram : ground white corn, 400; soyabean
meal,100; groundnut cake, 100; fishmeal, 10; wheat offal, 185; palm kernel cake, 100; bone meal, 20;
oyster shell, 80; vitamin-mineral premix (Roche Nutripol 5 ®), 2.5 and salt, 2.5. The diet contained per
kilogram: 2398.98 kcal ME, 175.0g crude protein, 588.4g nitrogen free extract, 60g ether extract, 75g
fibre, 61g ash, 38.9g Ca, 9.0g available P and 5.9 mg Cu/kg (determined absorption
spectrophotometry). Each of the six dietary treatments was fed for ten (10) weeks. The experimental
birds were kept in a standard battery cage with automatic nipple drinkers and standard feeding trough.
Feed and water were provided ad-libitum throughout the experimental period. All recommended health
and management practices were strictly observed.
EGG COLLECTION AND CHOLESTEROL ANALYSES.
Eighteen eggs (6 per replicate ) from each treatment were sampled at the expiration of ten weeks for
egg yolk cholesterol determination.. Sampled eggs were weighed and hard cooked by immersion in
boiling water for 8min. Yolks were individual weighed and oven-dried at 70 oC and prepared by pooling
and blending six yolk per treatment sample. Yolk dry matter was determined individually before
blending and expressed as percentage. Egg total lipid was extracted with chloroform: methanol (2:1
v/v) using the procedure described by Folch et al. (1957). Cholesterol determination was done using a
commercial test kit for cholesterol analysis (Sigma diagnostic cholesterol reagent procedure No 352’
Sigma Chemical Co., St Louis, MO, USA). All sample extracts were analyzed in triplicate. Cholesterol
concentration were determined from the absorbance read at 500nm using a spectrophotometer
(Idowu, 2004).
PLASMA LIPID ANALYSIS
At the termination of the experiment, 5ml of blood was drawn from the brachial vein of 9 birds per
treatment (3 per replicate) into heparinized tubes. Plasma was immediately separated by
centrifugation for 10 min at 1400. Plasma triglyceride, total, free, and lipoproteins and LDL, HDL and
VLDL cholesterol were determined using enzymatic – colorimetric method (according to Randox
diagnostic reagent kit – CHOD –PAP (R)). The lipoprotein fractions were precipitated before assay
using polyvinyl sulphate according to the Boehringer – Mannheim (Meylan, France) procedure
(Rouanet et al., 1993). Cholesterol determination was done using a commercial test kit for cholesterol
analysis (Sigma diagnostic cholesterol reagent procedure No 352’ Sigma Chemical Co., St Louis, MO,
USA).
COPPER RESIDUE DETERMINATION
Nine samples per treatment of egg (whole egg and yolk) and excreta samples were collected weekly,
pre-ashed and pooled together at end of the tenth week collection prior the dry ashing in muffle
furnace. Three laying hens per replicate group were slaughtered and liver excised at the end of the
feeding trial. Weight of liver samples excised were recorded . Part of the liver sample was pre-ashed
before dry ashing. The ashed samples of the liver, whole egg, egg yolk and excreta were analyzed
chemically for copper content. The copper content was analysed by atomic spectrophotometry
XI th European Symposium on the Quality of Eggs and Egg Products
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Hypocholesterolemic effects of organic and inorganic copper supplements: O.M.O. Idowu et al.
(Perkin- Elmer, Atomic Absorption Spectrophotometer ) at wavelength of 324.7nm ( Chiou et al.,
1998).
STATISTICAL ANALYSES
Data collected were analyzed by ANOVA using General Linear Model (GLM) procedure of SAS
(1985). Significant differences between treatment means were determined at P<0.05 using Duncan’s
new multiple range test.
Results and discussion
FEED INTAKE AND BODY
The body weight of birds tended to (P>0.05) to lower hen fed CuP than in those fed inorganic form
(Table 1). Hens fed diet supplemented with Cu consumed less(P<0.05) feed than hens fed diet
supplemented with CuSo4 (Table 1). Increasing the dietary additive of Cu supplement from 0 to 250
mg Cu kg-1 (Table 2) significantly decreased feed intake in dosage dependent manner (P<0.05).
Similar trend (P>0.05) was noticed in body weight of the hens. There was a significant interaction
(P<0.05) in feed intake between Cu supplemented level and Cu form (Table 3). Copper proteinate
decreased feed intake more than CuSo 4 at 250mgCukg-1 supplementation. Feed intake was highest in
the control group. Funk and Baker (1991) and Ledoux et al. (1991) reported a dosage dependent
reduction in feed intake of chicks fed graded levels of CuSo 4 and acetate respectively. Guo et al.
(2001) also notice that no significant effects (P>0.05) of Cu source, Cu concentration and source x
concentration interaction. Guo et al. (2001) also noticed that no significant effects (P>0.05) on body
weight of chicks fed diets supplemented with CuSO4, Cu-Lysine and Cu-proteinate. This result was in
line with the observation of Miles et al., (1998), which stated that, feed intake decreased in chicks
given increasing dietary Cu concentration.
PLASMA CHOLESTEROL
Table 1 showed that the birds fed inorganic copper (CUSO 4) recorded significantly higher values in all
the parameters measured. The higher value recorded in birds fed with inorganic copper (CuSO4)
showed that proteinate form of copper was more effective in reducing cholesterol level than sulphate
when fed to laying birds. This observation agreed with the reports of Cromwell et al. (1989) who
reported that sulphate form of copper resulted in higher values than other forms. Table 2 indicated that
higher values were obtained in all the blood parameters measured. Higher values were obtained in the
control group (0 mg Cu level). The values decreased as the level of inclusion of copper increased
(from 125mg to 250mg/kg of feed ). Similar observation has been reported by Bakali et al. (1995) that
high level of copper reduces GSH (Glutathione) which in turn stimulates the reduction of HMG-CO A
(3- hydroxy-3 methylglutaryl Coenzyme reductase activity which ultimately reduced cholesterol
synthesis. The esters of cholesterol contributed the greatest proportion of the total cholesterol and
values followed a decreasing order (LDL, free cholesterol, HDL and VLDL). This observation
corroborated the findings of Idowu et al. (2002). Results obtained in this study also agreed with Bakalli
et al. (1995), Pesti and Bakalli (1996) and Konjufca et al. (1997) who noticed a reduction in plasma
concentrations of young broiler chickens due to addition of pharmacological levels of copper
pentahydrate or copper citrate to their diet. Paik et al. (1999) also reported that copper-chelate
reduced plasma total cholesterol.
However, research evidences have shown that copper regulates cholesterol biosynthesis by
reducing hepatic glutathione concentrations (Kim, et al., 1992). The combined effects (Table 3) of
sources and level of copper inclusion (Interaction) showed no statistical significance (P>0.05). It was
also observed that birds fed higher level of copper inclusion (250mg Cu) irrespective of copper
sources had lower feed intake than those fed with other diets i.e. the higher the level of copper
inclusion, the lower the feed intake.
XI th European Symposium on the Quality of Eggs and Egg Products
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Hypocholesterolemic effects of organic and inorganic copper supplements: O.M.O. Idowu et al.
EGG CHOLESTEROL
There was no effect (P>0.05) of Cu source or supplementary level of Cu and the interaction between
Cu source and levels of supplement on egg weight. However, cholesterol concentration in the yolk,
whole and excreta were significantly influenced by Cu source, levels of Cu supplementation and their
interaction (Tables 1, 2 and 3) Here diets supplemented with organic Cu lay eggs has lower yolk
cholesterol and cholesterol per egg values (P<0.05) than hen diet supplemented with CuSo 4 (Table 1),
while the amount of cholesterol excreted was more in the treatment group fed diet supplemented with
inorganic Cu source. Yolk cholesterol and cholesterol per egg also decreased (P<0.05) linearly as the
supplemental levels increased from 0 to 250mgCu kg-. 1 . The cholesterol excreted tended to increase
with Cu supplementation levels (Table 2). The interaction between Cu supplemental level and Cu form
showed that CuP reduced yolk cholesterol and cholesterol per egg than CuSo4 at both 125 and 250
mg Cu supplementation (Table 3). Cholesterol contents of the yolk and whole egg was highest in the
control groups (O mg Cu) to indicate that additive copper actually reduced the cholesterol
concentration. The lowest cholesterol content was obtained in eggs laid by hens fed diet
supplemented with 250 mg CuP. Inverse relationship was observed between the cholesterol contents
of yolk contents of yolk/egg and the cholesterol excreted. Al-Ankari et al. (1998) also obtained a
significant linear reduction in yolk and serum cholesterol as dietary copper content increased from 0 to
250 mg kg-1 diet.
Cu source, supplemental levels ant the interaction of Cu source and supplemental level has no
effect on the liver fresh weight. However, relative liver weight values were significantly influenced by
supplemental levels of Cu and the interaction between Cu source and supplemental levels (Tables 1,
2 and 3). Relatively heavier liver samples were excised from the hens fed diets supplemented with
inorganic form of Cu (Tables 1 and 2). The fresh and the relative liver weights decreased linearly
(P>0.05) as the level of Cu supplementation increased from 0 to 250mg Cu kg -1 (Tables 2 and 3). Low
(P<0.05) cholesterol content was noticed in the groups fed CuP (Tables 1 and 3). Liver cholesterol
contents reduced linearly in a Cu dosage dependent manner (Tables 2 and 3). Higher (P<0.05) liver
cholesterol contents were noticed in the hens fed diets supplemented with inorganic Cu form.
Supplementation with CuP decreased (P<0.05) cholesterol content more than CuSO4 (Table 1 and 3).
A significant interaction between Cu source and levels of supplementation was detected (Table 3).
CuP reduced liver cholesterol content more than CuSO4 at 125 and 250mg supplementation. The
results obtained further corroborate the reports of Lubert (1981) that the rate of cholesterol formation
by the liver was responsive to the amount of dietary Cu absorbed. .Egg yolk cholesterol is reported to
be synthesized in the liver of laying hens and transported to the developing follicles via plasma Very
Low Density Lipoprotein (VLDL) where it is deposited by receptor-mediated endocytosis (Nimpt and
Schneider, 1991).
COPPER RESIDUE
Table 4 shows the main effects and the interaction effects of Cu source and levels of supplementation
on the copper contents of the liver, egg yolk, whole egg and excreta of laying hens. The main effects
of Cu source was not significant on yolk, whole egg and excreta Cu contents, however more Cu
accumulated in the liver of hens fed diets supplemented with inorganic Cu form (P<0.05). This may be
due to higher feed intake noticed among hen receiving diets supplemented with inorganic Cu form. Cu
concentration of the liver was higher than those of the yolk and whole egg. This is expected because
the liver is the major site of Cu metabolism and storage (Chiou et al., 1998). Increasing the level of Cu
supplementation resulted in a linear increase in the Cu concentration of the liver, yolk, whole egg and
excreta (P<0.05). The interaction of the source and level of supplementation of Cu was significant on
all the parameters measured (Table 4). The Cu concentrations in the liver , yolk and whole egg were
significantly higher in the hen fed inorganic Cu at all levels of supplementation than those on organic
Cu. This implied that the interaction between Cu source and levels of supplementation significantly
influenced copper accumulation the liver and egg.
The Cu content of the excreta from the laying hens used in this study significantly increased
as the level of supplemental Cu increased (P<0.05). This was in line with observations of Chiou et al.
(1998). There was no significant difference between mean values of the Cu sources used (P>0.05).
The interactive effects between Cu source and supplemental level showed significant differences
(P<0.05) in the amount of Cu excreted, as more inorganic copper was excreted than the organic form
of Cu. The differences between the control group and 125 - 250mg Cu groups were about 7 – 9 fold
increase.
XI th European Symposium on the Quality of Eggs and Egg Products
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Hypocholesterolemic effects of organic and inorganic copper supplements: O.M.O. Idowu et al.
Conclusion
Elevated concentration of supplemental Cu resulted in a significant decrease in feed intake. Inclusion
of copper (organic and inorganic salts) up to 250mg Cu significantly reduced plasma cholesterol and
egg cholesterol in laying hens. Organic salt (Copper proteinate) was more effective and efficient in
reduction of plasma cholesterol and egg cholesterol. More inorganic copper was excreted than the
organic Cu form.
References
AL-ANKARI, A., H. NAJIB, A. AL-HAZAB (1998) Yolk and serum cholesterol and production traits as
affected by incorporating a supra-optimal amount of copper in the diet of the leghorn hen. British
Poult. Sci. 39(3): 393-399.
ANON, P. (1990) Cholesterol oxides in foods of animal origin. Journal of Food Science and Agric., 72:
171-178.
BAKALLI, R.I., G. M. PESTI, W.L. RAGLAND AND KONJUFCA (1995) Dietary copper in excess of
Nutritional requirement reduces plasma and breast muscle cholesterol of chickens, Poult. Sci. 70:
177-179
CHIOU P. W., K. CHEN. AND B. YU (1997) Toxicity, tissue accumulation and residue in egg and
excreta of copper in laying hens. J. of Anim. Feed Sci. and Tech. 67: 49 – 60.
CHIOU P. W., K. CHEN. AND B. YU (1998) Effects of dietary organic arsenicals and cupric sulfate on
copper toxicity, liver accumulation and residue in eggs and excreta in laying hens. J. of Anim. Feed
Sci. and Tech. 73: 161 – 171.
CROMWELL, G.L, T.S STHLY AND H.J MONGUE (1989) Effect of source and level of copper on
Performance and liver copper store in weanling pigs. J Anim.Sci.67:2996- 3002
FOLCH J, LEES M AND SLOANE – SLANLEY. G.S (1957). A simple method for the isolation and
purification of total lipids from animal tissues. J. Biol Chem. 226: 497 – 509.
FUNK, M.A. AND BAKER, D.H. (1991) Toxicity and tissue accumulation of copper in chicks fed
casein and soy-based diets. J. Anim. Sci. 69: 4505 – 4511.
GUO, R., HENRY, P.R., HOLWERDA, R.A., CAO, J., LITTELL, R.C., MILES, R.D. AND
AMMERMAN, C.B. (2001) Chemical characteristics and relative bioavailability of supplemental
organic copper sources for poultry. J. Anim. Sci. 79 :1132 – 1141.
IDOWU, O.M.O. (2004) Effects of unpeeled cassava based-diets on performance and cholesterol
levels in laying hens. PhD Thesis, University of Agriculture Abeokuta, Nigeria.
IDOWU, O.M.O., ODUWEFO, A. AND ERUVBETINE, D. (2002) Hypo-cholesterolemic effects
of
cassava root sievate in laying chickens diets. Proc. 7th Ann. Conf. Anim. Sci. Ass. Of Nig.
(ASAN), Sept. 16-19, 2002, Univ. of Agric., Abeokuta
JACKSON, N., STEVENSON, M.H. AND KIRKPATRICK, G.M. (1979) Effects of protracted feeding of
copper sulfate-supplemented diets to laying, domestic fowl on egg production and on specific
tissues, with special reference to mineral content. Br. J. Nutr. 42 : 253 – 266.
JENSEN, L.S. RUNN, P.A. AND DOLSON, K.N. (1991) Induction of oral lesion in broiler chicks by
supplementing the diet with copper. Avian Dis. 35: 969 – 973.
KIM, J. W. , CHAO , P.Y. AND ALLEN, A. (1992) Inhibition of elevated hepatic glutathione abolishes
copper deficiency cholesterolemia. FASEB J. 6:2467- 2471.
KONJUFCA V.H, G.M. PESTI AND R. I. BAKALLI (1997) Modulation of cholesterol levels in boiler
meat by dietary garlic and copper. Poult. Sci. 76: 1264 – 1274.
LIRETTE A., A. R. ROBINSON, D. C. CROBER, P.D. LAWSON AND N.L. FIRTH (1993) Effect of oat
bran, cotton seed hulls and guar gum on chicken egg and blood lipids during the early laying period
Can. J. Anim. Sci. 73:673-677.
LEDOUX, D.R. AND HENRY, P.R. (1991) Estimation of the relative bio available of inorganic copper
sources for chicks using tissue uptake of copper. Poult. Sci. 69: 215 – 222.
LEDOUX, D.R. HENRY, P.R., AMMERMAN, C.B, RAO, P.V. AND MILES, R.D. (1991) Estimation of
the relative bioavailability of inorganic copper sources for chicks using tissue uptake of copper. J.
Anim. Sci. 69: 215-222.
LUBERT, S. (1981) Biochemistry, Pub. W.H., Freeman & Co., New York. 2nd. Ed. Pp. 464 – 475.
MILES R. D., S. F. O’KEEFE, P.R. HENRY C.B. AMMERMAN AND X. G. LUO (1998) The effect of
dietary supplementation with copper sulfate or tribasic copper chloride in broiler performance,
Relative copper bioavailability and dietary prooxidant activity. J. of Poul. Sci. 77; 416 –425.
NIMPT, J. AND SCHNEIDER, W.J. (1991) Receptor – mediated lipoprotein transport in laying hens. J.
Nutr. 121: 1471 – 1474.
XI th European Symposium on the Quality of Eggs and Egg Products
Doorwerth, The Netherlands, 23-26 May 2005
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Hypocholesterolemic effects of organic and inorganic copper supplements: O.M.O. Idowu et al.
N.R.C. (1994) National Research Council – Nutrient Requirements of Poultry, 9th Revised edition.
National Academy Press, Washington , D.C.
PAIK, I.K. SEO, S.H., UM, J.S., CHANG, M.B. AND LEE, B.H. (1999) Effects of supplementary
copper-chelate on the performance and cholesterol level in plasma and breast muscle of broiler
chickens. Asian-Austr. Vol. 12. No.5: 794-798.
PESTI, G.M. AND BAKALLI, R.I. (1998) Studies on the effects of feeding cupric sulphate
pentahydrate to laying hens on egg cholesterol content. Poultry Sci. 77: 1540-1545.
ROUANENT, J., LAURENT, C. AND BESANCON, P. (1993) Rice bran and wheat bran: selective
effect on plasma and liver cholesterol in high-cholesterol fed rats. Food: Chemistry 47 (1993) 67-71.
SAS (1985) SAS/STAT® User’s Guide (Released 6.08) SAS Institute Inc. Cary, North Caroline ,USA.
SCOTT, M., NESHEIM, M.C. AND YOUNG, R.J. (1982) Nutrition of the Chicken 3rd ed. Pp. 121 –
302. McGraw Pub. USA.
VALSALA, P. AND P. A. KURUP (1987) Investigations on the mechanism of hypercholesterolemia
Observed in copper deficiency in rats. J. Biosci. (Bangalore) 12:137-142.
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Table 1 Effect of copper salts source on egg cholesterol levels.
Types of copper salt
Parameters
Organic (CuP)
Inorganic (CuSO4)
SEM
Body weight / hen (g)
Daily feed intake/hen (g)
Egg Cholesterol
Egg weight
Yolk Cholesterol (mg/g)
Cholesterol/Egg (mg/egg)
Cholesterol excreted (mg/d/hen)
Plasma Cholesterol
Triacylglycerol
Free
Ester
Total
Lipoproteins
HDL
LDL
VLDL
Liver Cholesterol
Fresh liver wt.
Relative liver wt.
Liver Cholesterol (mg/g)
1.84
10.14
1.86
109.09
0.08
6.56
62.16
11.81 b
180.93 b
157.60a
62.07
15.49a
207.57a
150.44b
0.39
2.19
6.23
12.77
110.78b
34.67 b
76.00 b
110.78b
125.89a
40.11a
86.22a
125.89a
3.41
1.13
2.29
3.41
22.44b
74.11b
14.22b
25.55a
84.44a
16.33a
0.69
2.24
0.46
29.84
16.22 b
0.21b
33.57
18.05a
0.37a
0.30
1.09
0.11
abc
Means without or the same superscript are not significantly different (P>0.05)
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Hypocholesterolemic effects of organic and inorganic copper supplements: O.M.O. Idowu et al.
Table 2 Effect of levels of copper inclusion levels on egg cholesterol levels.
Copper levels (mg/kg feed)
Parameters
0
Body weight / hen (g)
Daily feed intake/hen (g)
Egg Cholesterol
Yolk Cholesterol (mg/g)
Cholesterol/Egg (mg/egg)
Cholesterol excreted (mg/d/hen)
Plasma Cholesterol
Triacylglycerol
Free
Ester
Total
Lipoproteins
HDL
LDL
VLDL
Liver Cholesterol
Fresh liver wt.
Relative liver wt.
Liver Cholesterol (mg/g)
125
250
SEM
1.84
121.18a
1.88
107.53b
1.90
95.63c
0.02
10.69
15.60a
223.92a
133.15c
12.97b
193.4b
147.36b
12.40b
165.39c
182.25a
0.24
17.63
14.98
82.67a
40.67a
87.83a
128.67a
76.17b
37.17b
80.83b
118.00b
69.83c
34.33b
74.67c
108.17c
2.50
1.19
1.97
1.29
26.00a
86.00a
16.67a
23.83b
79.00b
15.17b
22.17b
72.83c
14.00c
0.68
12.26
0.44
32.47
7.65
0.34a
31.71
16.87
0.30b
31.35
16.50
0.23c
0.21
0.67
0.10
abc Means with the same superscript are not significantly different (P>0.05)
Table 3 Interactive effects of types of copper salts and levels of inclusion on egg cholesterol.
Organic Cu (CuP) mg/kg
Inorganic Cu (CuSO4) mg/kg
Parameter
0
125
250
0
Body weight / hen (g)
Feed intake/hen/d (g)
Egg Cholesterol
Yolk Cholesterol (mg/g)
Cholesterol (mg/egg)
Daily Cholesterol
excreted (mg/hen)
Plasma Cholesterol
Triacylglycerol
Free
Ester
Total
Plasma Lipoproteins
HDL
LDL
VLDL
Liver Cholesterol
Fresh liver wt.
Relative liver wt.
Liver Cholesterol (mg/g)
1.81
112.25a
1.83
105.30c
1.89
83.75d
12.17 c
216.78
11.83c
182.56d
135.50c
abc
125
250
SEM
1.87
110.12a
1.85
109.64b
1.90
107.50b
0.03
0.97
11.43c
143.44e
19.02a
231.06a
14.11b
204.33c
13.34b
187.33d
0.02
0.11
153.60b
184.30a
130.80c
141.11bc
180.20a
16.31
80.67
39.33
85.67
125.33
69.67
34.00
74.67
108.67
63.00
30.67
67.67
98.33
84.67
42.00
90.00
132.00
82.67
40.33
87.00
127.33
76.67
38.00
81.67
118.33
2.23
1.25
1.93
3.25
25.33
83.67
16.33
21.67
73.33
13.67
20.33
65.33
12.67
26.67
88.33
17.00
26.00
84.67
16.67
24.00
80.33
15.33
0.70
2.29
0.45
30.65
16.93
0.25c
29.67
16.21
0.20c
29.35
15.53
0.16d
34.29
18.34
0.43a
33.75
18.24
0.39b
33.31
17.53
0.29c
0.91
1.67
0.18
Means without or the same superscript are not significantly different (P>0.05)
XI th European Symposium on the Quality of Eggs and Egg Products
Doorwerth, The Netherlands, 23-26 May 2005
408
Hypocholesterolemic effects of organic and inorganic copper supplements: O.M.O. Idowu et al.
Table 4 Effects of source of copper and levels of supplementation on copper residue.
Source
Cu Level
Liver Cu
-1
(mg Cu/kg )
Yolk Cu
-1
(mg Cu/kg )
Whole egg
-1
(mg Cu/kg )
-1
Excreta
(mg Cu/kg )
(mg Cu/kg-1)
Main effects of source of supplementary Cu
Organic Cu
70.94a
1.01
7.49
820.62
Inorganic Cu
60.24b
0.94
7.13
782.45
5.10
0.08
0.10
28.98
0.77c
0.99b
1.17a
0.10
6.46b
7.53a
7.93a
0.13
173.74c
1021.11b
1236.78a
32.11
SEM
Main effects of supplementary levels of Cu
0
125
250
SEM
14.00c
38.77b
142.44a
23.48
Interaction effects of source and levels of Cu supplementation
14.00e
0.81b
6.61c
169.44d
125
48.44c
1.00a
7.86b
1017.11b
250
150.37a
1.23a
8.00a
1275.32a
0
14.00e
0.73c
6.32d
178.03d
125
29.10d
0.98b
7.19ab
971.10c
250
134.50b
1.11a
7.87b
1198.23a
28.91
0.43
0.68
55.19
Organic Cu 0
Inorganic Cu
SEM
abc
Means without or the same superscript are not significantly different (P>0.05)
XI th European Symposium on the Quality of Eggs and Egg Products
Doorwerth, The Netherlands, 23-26 May 2005
409