use of silybum marianum fruit extract in broiler chicken nutrition influence on performance and meat...

OR IGINAL AR TIC LE

Use of Silybum marianum fruit extract in broiler chickennutrition: influence on performance and meat qualityA. Schiavone1, F. Righi2, A. Quarantelli1, R. Bruni3, P. Serventi4 and A. Fusari4

1 Dipartimento di Produzioni Animali, Epidemiologia ed Ecologia, Universita di Torino, Grugliasco (TO),

2 Dipartimento di Produzioni Animali, Biotecnologie Veterinarie, Qualita e Sicurezza degli Alimenti, Universita di Parma, Parma,

3 Dipartimento di Biologia Evolutiva e Funzionale, and

4 Dipartimento di Salute Animale, Universita di Parma, Parma, Italy

Introduction

Nutritional deficiencies or disturbances can depend

on different factors and cause a variety of diseases.

Moreover, interactions between dietary and environ-

mental factors can alter metabolic pathways. Such

imbalances can result in the alteration of the anti-

oxidant defence system which is an effective scaven-

ger of free radicals and lipid peroxides generated

during cell metabolism, division and differentiation

and during hormone and prostaglandin biosynthesis

(Mezes et al., 1997). Lipid peroxides can also be

introduced into the organism by feed, absorbed in

the form of unsaturated cheto-compounds and initi-

ate tissue lipid peroxidation. Uncontrolled lipid oxi-

dation plays a key role in poultry diseases, toxicoses

and affects egg and meat quality.

Several studies have been conducted in vivo in

order to test natural compounds that are capable of

improving lipid stability in meat. It has been demon-

strated that dietary supplementation with both syn-

thetic and natural antioxidants like vitamin E,

ascorbic acid, selenium, oat polyphenols, rosemary,

sage and oregano extracts can improve antioxidant

defences and meat shelf life (Lopez-Bote et al.,

1998a; Avanzo et al., 2001; Young et al., 2002,

2003; Carreras et al., 2004).

Silymarin is a poliphenolic compound extract from

Silybum marianum and Cynara cardunculus seeds,

fruits and, in lower amounts, from leaves. Its active

Keywords

chicken, meat quality, sylimarin, Silybum

marianum, thiobarbituric acid reactive

substances

Correspondence

Dr Achille Schiavone, Dipartimento di

Produzioni Animali, Epidemiologia ed Ecologia,

Universita di Torino, Via Leonardo da Vinci,

44, 10095 Grugliasco (TO), Italy.

Tel: +39 011 6709208; Fax: +39 011 2369208;

E-mail: [email protected]

Summary

The present study aimed at evaluating the effects of different doses of

silymarin in diet on broiler performances and meat quality. For the trial,

180 male chicks (ROSS 508), were allocated in to three groups (S0, S40

and S80) of 60 animals each receiving a basal diet supplemented with

0 ppm, 40 ppm and 80 ppm of a sylimarin (provided by a dry extract of

Silybum marianum fruits) respectively. During the trial feed consumption

and live body weight were taken every 20 days. At the age of 40 and

60 days blood samples were taken in order to evaluate protein, aspartate

aminotransferase, cholesterol, tryglicerides and uric acid. At the age of

60 days animals were slaughtered, dressing percentages were evaluated

and samples of breast and meat were taken to evaluate chemical compo-

sition and susceptibility of lipid peroxidation by means of thiobarbituric

acid reactive substances. Silymarin at the tested doses did not affect

growth performances but slightly affected slaughtering yields negatively,

no specific hepatoprotective effect was found. Treatments reduced lipid

content of both breast and thigh and increased muscles resistance to oxi-

dative stress.

256 Journal of Animal Physiology and Animal Nutrition 91 (2007) 256–262 ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd

constituents, the flavonolignans silybin, isosilybin,

silydianin and silycristin, are well-known for their

hepatoprotectivity (Dehmlow et al., 1996 and 1996a;

Lang et al., 1990; Halim et al., 1997). Moreover,

liver protection relies on the potent antioxidant

properties of the silymarin complex. In fact, silybin

is the most bio-active compound and the extracts

are usually standardized to contain 70–80% of sily-

bin, expressed as the sum of silybin and isosylibin

isomers (Luper, 1998). It has been demonstrated that

silymarin acts as an antioxidant, reducing free radical-

mediated damage in tissues and inhibiting lipid perox-

idation (Bosisio et al., 1992). Silymarin also shows

anti-inflammatory effects (Fiebrich and Koch, 1979;

Fantozzi et al., 1986; De La Puerta et al., 1996; Dehm-

low et al., 1996a), it improves liver glucuronidation

of xenobiotics (Halim et al., 1997; Baer-Dubowska

et al., 1998), it reduces hepatic glutathione consump-

tion (Campos et al., 1989), it plays an important role

in hepatic protein synthesis by DNA-dependent RNA

polymerase I activation and thus improves liver cell

regeneration (Sonnenbichler et al., 1986). Different

experiments and clinical trials showed that silymarin

inclusion in diet or silymarin administration increased

productive and reproductive performances and

improved livestock health status (Tedesco, 2001).

Broiler chickens are exposed to a multitude of

long- and short-acting stressors (e.g. heat stress,

immune challenges, catching, transport) which can

alter their internal homeostasis and oxidant/anti-

oxidant balance, leading to oxidative stress (Sies,

1991), which can have detrimental effects on meat

shelf life (Sheldon et al., 1997; Young et al., 2003).

Moreover, toxic substances in feedstuff and the rapid

growth rate of modern broiler strains can lead to sig-

nificant metabolic and oxidative stress, which can

reduce feed conversion efficiency and can affect both

growth performance and meat quality (Carreras

et al., 2004; Erdogan et al., 2005). Thus, the aim of

this study was to evaluate the effects of different

doses of silymarin in diet on broiler performance

and meat quality.

Materials and methods

For the trial, 180 male chicks (ROSS 508), were allo-

cated into three groups (S0, S40 and S80) of 60 ani-

mals. Each group was divided into two replicates of

30 chicks. All animals were fed ad libitum a commer-

cial diet for the first (from d1 to d21) and second

(from d22 to d60) periods (Table 1). The control

group (S0) was fed the diet with no additions. Ani-

mals belonging to the two experimental groups (S40

and S80) were fed the same basic diet added with a

dried extract of Silybum marianum fruit (PLUSIL�;

BIOTRADE snc, Mirandola, Modena, Italy) for sup-

plementation 40 ppm (group S40) and 80 ppm

(group S80) of silymarin.

Silybum marianum extract composition was previ-

ously analyzed via HPLC using a gradient elution

method described by Bilia et al. (2001) (Table 2).

Briefly, HPLC analyses were performed using a

modular Jasco HPLC unit (Tokyo, Japan), which

consisted of a PU-980 pump, a LG-1580-02 ternary

gradient unit, a DG-980-503-line degasser and an

UV/vis 975 detector set at an excitation wavelenght

of 280 nm. The analyses were carried out using a

Lichrosorb (Teknokroma, Barcelona, Spain) RP-18

column (250 · 4 mm i.d., 5 l) at room temperature.

To protect the integrity of the analytical column, all

Table 1 Composition of diets

Periods

First Second

Ingredients (%)

Corn meal 56.850 59.635

Soybean meal 34.400 28.000

Corn gluten 2.500 3.500

Fat 2.000 5.000

Bicalcium phosphate 2.150 2.000

Calcium carbonate 0.850 0.750

D–L Methionin 0.150 0.115

Lysin 0.300 0.200

Salt 0.200 0.200

Sodium carbonate 0.100 0.100

Mineral and vitamin complex 0.500 0.500

Chemical analysis (%)

Moisture 12.57 12.24

Crude protein 22.62 20.40

Fat 4.55 7.55

Crude fiber 3.12 2.93

Ash 5.90 5.36

Lysin 1.368 1.126

Methionin 0.500 0.457

Methionin + cystin 0.867 0.801

Metabolizable energy (Mj) 12.62 13.61

Table 2 Content (% of dry wt) of flavonolignans in the commercial

Silymarin extract and in reference standard Silymarin complex

Compound

Commercial extract

(% of dry weight)

Reference extract

(% of dry weight)

Taxifolin 4.62 � 0.07 4.25 � 0.11

Silychristin + Silydianin 28.21 � 0.83 32.31 � 0.88

Silybin isomers 45.47 � 0.77 36.92 � 0.91

Isosylibin isomers 21.7 � 0.71 26.52 � 0.57

A. Schiavone et al. Silybum marianum in chicken nutrition

Journal of Animal Physiology and Animal Nutrition. ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd 257

analyses were performed with a coupled Lichrosorb

RP-18 guard column (4 · 4 mm, 5 l). The mobile

phase was a four-step, 45 min, linear gradient pre-

pared from CH3CN and water (pH 3.0, H3PO4). The

flow rate was 1.3 ml/min. All extracts and standard

solutions were filtered through a 0.45-mm PTFE fil-

ter into a HPLC vial and capped. The sample injec-

tion volume was 20 ll and three injections were

performed for each sample. Peaks were identified by

comparison with those of a standard Silymarin mix-

ture (Sigma-Aldrich Italia, Milan, Italy) and con-

firmed by spiking the extracts with a pure silymarin

standard.

During the trial, health status was evaluated daily,

whereas live weight and feed intake were measured

every 20 days. At 40 and 60 days of age, six blood

samples per group were randomly taken for protein,

aspartato aminotransferase (AST), cholesterol, try-

glicerides and uric acid measurements. Blood

analyses were performed with commercial kits

(Chemetron Chimica SPA; Rozzano (MI) and Senti-

nel Diagnostics, Milan, Italy).

At 60 days of age, birds were starved for 6 h

before slaughtering and 20 animals per group were

killed. Plucked and eviscerated carcasses were

weighed after removal of the head, neck, feet and

abdominal fat to obtain ready-to-cook carcasses and

refrigerated for 6 h at 4 �C. Yields from chilled car-

casses, breast and thighs were evaluated.

Breast and thigh samples were vacuum-packaged

and kept frozen ()20 �C) until analyses were per-

formed. These analyses included chemical composi-

tion and evaluation of susceptibility to lipid

oxidation by means of thiobarbituric acid reactive

substances (TBARS). AOAC (1984) methods were

used for moisture, ash, protein and ether extract

determination of breast and thigh samples; results

were expressed as percentage over fresh matter

basis.

Thiobarbituric acid reactive substances evaluation

was performed according to the procedure described

by Huang and Miller (1993). Briefly, 3 g of minced

tissue (m. pectoralis major for breast and m. gastrocnem-

ius for thigh) was homogenized in 57 ml of a 1.15%

KCl chilled solution. A total of 30 ml of the homogen-

ate was incubated at 37 �C in shaking water bath with

8.34 mg FeSO4Æ7H2O (final concentration 1 mm Fe+3)

as oxidative agent. TBARS assay was performed at

0 min (T0), 30 min (T30), 60 min (T60) and 120 min

(T120) of incubation of the sample at 37 � C and the

absorbance was read at 532 nm. Liquid Malonalde-

hyde bis(diethyl acetal) (MDA; Aldrich Chemical,

Dorset, UK) was used as standard to determine the

linear standard response and recovery. Thiobarbituric

acid reactive substances values were calculated multi-

plying the absorbance by a constant coefficient K

(23.58) combining standard response, recovery

(93.4%), molecular weight of the MDA and sample

weight. Thiobarbituric acid reactive substances values

were expressed as milligrams of malondialdehyde

(MDA) per kilogram of meat. Data were analysed by

one-way Analysis of Variance, the only factor consid-

ered was the diet. Post-hoc Tukey’s test was used to

study the differences among groups. A statistical level

of 0.05% was considered as significant (SPSS, 2003).

Results

The commercial silymarin complex added to the feed

was obtained from a dried hydroalcoholic extract of

Silybum marianum fruits and was similar in composi-

tion to that found in common commercial sources

(e.g. with Silymarin standard provided by Sigma-

Aldrich). A slightly higher amount of Silybin was,

however, observed and it must be underlined that

the content of such isomer is usually a good quality

indicator for Silymarin. The relative amounts of tax-

ifolin, silychristin and silydianin, silybin and isosyli-

bin isomers are reported in Table 2.

Table 3 shows that silymarin given at doses of

40 ppm and 80 ppm did not significantly modify

growth performances and only slightly reduced feed

intake, with a sparing of feedstuff of 3.68% and

2.63% for group S40 and S80 respectively. Carcass

and thigh yields were negatively affected by dietary

treatments (p < 0.05).

Several blood parameters (Table 4) were influ-

enced by treatments. Group S80 showed higher pro-

tein plasma levels (p < 0.05) (2.94 � 0.26 vs.

3.08 � 0.19 vs. 3.30 � 0.34) at 40 days of age and

both treatment groups showed a slight, but not sig-

nificant, increase in triglycerides (64.28 � 28.19 vs.

87.78 � 25.63 vs. 83.48 � 24.28). An increase in

AST levels was observed both at 40 and 60 days of

age, and differences between group S0 and S80 were

statistically significant at 60 days of age

(103.00 � 16.40 vs. 122.42 � 15.00).

Lipid content of breast and thigh meat (Table 5)

was affected by silymarin supplementation, and the

lowest amount of lipid content was observed in

group S40 (p < 0.05). Moisture, protein and ash

content of both breast and thigh were not affected

by dietary treatments.

Silymarin at 40 ppm significantly reduced

(p < 0.05) TBARS values (Table 5) at T30 in both

tested muscles (m. pectoralis major: 0.84 � 0.16 vs.

Silybum marianum in chicken nutrition A. Schiavone et al.

258 Journal of Animal Physiology and Animal Nutrition. ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd

0.92 � 0.14 vs. 1.40 � 0.26; m. gastrocnemius:

0.94 � 0.12 vs. 1.08 � 0.12 vs. 1.39 � 0.69). At

80 ppm, only the TBARS of m. pectoralis major was

affected (p < 0.05) at T0 (0.12 � 0.01 vs.

0.12 � 0.01 vs. 0.16 � 0.01).

Discussion

Even though no significant dose-dependent effect

was observed for in vivo performance (Table 3), the

decrease in feed intake observed could be due to

Table 3 Growth performances and slaughter-

ing yields (mean � SD) S0 S40 S80

Live performances

Final body weight (g) 4302.50 � 324.23 4206.02 � 327.67 4247.40 � 325.07

Feed consumption (g) 8174.45 7697.02 7857.69

FCR 1.90 1.83 1.85

Slaughtering yields

Carcase weight (g)

(% of body weight)

3228.84 � 68.32 a

(75.04)

3009.81 � 163.21b

(71.56)

3071.73 � 129.11b

(72.32)

Thigh (g)

(% of carcase)

930.31 � 58.09a

(28.81)

861.17 � 49.74b

(28.66)

900.76 � 65.11ab

(29.34)

Breast (g)

(% of carcase)

924.94 � 41.31

(28.66)

891.57 � 71.10

(29.62)

877.39 � 44.92

(28.59)

Abdominal fat

(% of carcase)

63.46 � 9.66

(1.69)

62.21 � 15.68

(1.69)

58.38 � 18.17

(1.60)

a,bp < 0.05.

Table 4 Blood parameters (mean � SD)

Group

Age

(days)

Protein

(g/100 ml)

AST

(U/1000 ml)

Cholesterol

(mg/100 ml)

Trygliceride

(mg/100 ml)

Uric acid

(mg/100 ml)

S0 40 2.94 � 0.26a 127.10 � 29.90 111.49 � 11.00 64.28 � 28.19 7.20 � 0.74

S40 3.08 � 0.19ab 139.68 � 13.10 122.78 � 29.80 87.78 � 25.63 6.96 � 1.95

S80 3.30 � 0.34b 144.66 � 24.43 108.96 � 17.92 83.48 � 24.28 8.88 � 2.19

S0 60 2.96 � 0.34 103.00 � 16.40a 132.15 � 12.58 85.60 � 26.17 5.86 � 1.76

S40 2.85 � 0.41 118.86 � 16.66ab 127.74 � 14.24 80.15 � 15.97 5.51 � 1.00

S80 2.79 � 0.35 122.42 � 15.00b 131.32 � 13.51 90.27 � 32.61 6.06 � 1.21

a,bp < 0.05.

Table 5 Meat traits (mean � SD)

Breast (pooled muscles) Thigh (pooled muscles)

S0 S40 S80 S0 S40 S80

Chemical composition (% on fresh matter)

Moisture 74.14 � 0.81 74.83 � 0.44 74.42 � 0.72 75.23 � 0.73 75.98 � 0.53 75.51 � 0.71

Protein 21.56 � 1.44 21.35 � 1.04 21.68 � 1.82 18.18 � 0.62 18.54 � 0.41 18.50 � 0.49

Lipid 2.15 � 0.35a 1.19 � 0.12b 1.74 � 0.15a 4.79 � 0.60a 3.81 � 0.13b 4.22 � 0.17ab

Ash 1.09 � 0.06 1.05 � 0.05 1.09 � 0.03 1.07 � 0.05 1.04 � 0.04 1.10 � 0.05

m. pectoralis major m. gastrocnemius

TBARS (mg MDA/kg meat)

0¢ 0.16 � 0.01a 0.12 � 0.01b 0.12 � 0.01b 0.19 � 0.04 0.17 � 0.07 0.16 � 0.04

30¢ 1.40 � 0.26a 0.92 � 0.14b 0.84 � 0.16b 1.39 � 0.19a 1.08 � 0.12b 0.94 � 0.12b

60¢ 3.21 � 0.35 2.39 � 1.11 1.54 � 0.57 2.94 � 1.63 1.85 � 0.57 1.81 � 0.35

120¢ 9.16 � 2.09 6.23 � 3.47 4.18 � 2.57 5.56 � 2.73 3.36 � 1.88 4.13 � 0.86

a,bp < 0.05.



reduced palatability of the experimental diet follow-

ing addition of the dried Silybum marianum extract.

We have previously observed the same effect in

other trials with laying hens (Quarantelli et al.,

2005). The level of feed consumption is a basic and

important factor that determines the rate of growth

and body composition achieved by animals through-

out their lifecycles (Richards, 2003). One of the

direct physiological consequences of reducing feed

consumption is the reduction of the passage rate of

the ingesta through the gastrointestinal tract and

enhanced pancreatic enzymatic activity (de Pinheiro

et al., 2004), which lead to increased digestibility of

the diet (Bonnet et al., 1997). Smaller meals have

been associated with a slight reduction in growth

rate and to an improved FCR in various studies

(Sorensen et al., 1999; Su et al., 1999; Skinner-

Noble and Teeter, 2004a,b). The observed lower FCR

and final body weight, even if not statistically signifi-

cant, could be explained by this mechanism.

As a result of the reduction in feed intake, the

lower amount of metabolizable energy and protein

ingested by the birds, could also explain the differ-

ences observed in carcass and thigh yields (Table 3),

which were negatively affected (p < 0.05) by dietary

treatments. Similarly, the lower availability of meta-

bolizable energy in treated groups could be responsi-

ble for the observed reduced content of lipid

deposition in breast and thigh muscles (p < 0.05)

and the reduced, but not significant, amount of

abdominal fat (Table 3). As reported by Richards

(2003), when given unrestricted access to feed, broil-

ers exhibit hyperphagia leading to an excessive accu-

mulation of energy (fat) stores, making these birds

prone to obesity and other health-related problems.

Blood parameters (Table 4) appeared to be of par-

ticular interest mainly at the age of 40 days, when

group S80 showed higher protein plasma levels. In

addition, a slight, but not significant, increase in tri-

glyceride levels was observed in both treated groups,

probably indicating an increase in metabolism, a

reduction in hepatic storage of lipids or increased lipid

mobilisation. Overall serum AST activity was higher

for treated groups and a higher value (p < 0.05) was

recorded for S80 group at the age of 60 days. AST

activity was found to be the most sensitive indicator

of liver damage by Lumeij (1997) and was indicated

as useful for the diagnosis of Fatty Liver–Hemorrhagic

Syndrome by Yousefi et al. (2005). Normal birds have

been reported to show serum AST activity up to

230 UI/l (Coles, 1986). On this basis, we can con-

clude that all the values observed in the present trial

were included in the normal range of AST activity. In

this study, silimaryn did not display the hepatopro-

tective effect suggested by others authors (Lang et al.,

1990; Erdogan et al., 2005).

Dietary treatments reduced TBARS values

in both tested muscles (m. pectoralis major and

m. gastrocnemius). This effect could be related to

both the improvement in post mortem antioxidant

defences and to the reduction in tissue lipid con-

tent. The increased post mortem oxidative stability

could rely on an increased silymarin concentration

in tissues with direct inhibition of lipid peroxidation

(Bosisio et al., 1992) but also on a sparing of other

antioxidant molecules and enzymes (Campos et al.,

1989). The magnitude of the antioxidant action of

silymarin displayed in this trial is not comparable

with vitamin E (Lauridsen et al., 1997; Morrissey

et al., 1997; Maraschiello et al., 1998), either with

those of other natural extracts like oat polyphenols

(Lopez-Bote et al., 1998a), or with oil extracts from

rosemary and sage (Lopez-Bote et al., 1998b).

Conclusions

Silymarin did not significantly affect growth per-

formances but slightly reduced slaughtering yields

probably by feed consumption reduction and modu-

lation. Lipid deposition was reduced in both muscu-

lar tissue and abdominal fat pad probably as a direct

consequence of reduced feed intake which negat-

ively affected energy balance. Silymarin at the tes-

ted doses and in these specific experimental

conditions did not show any specific hepatoprotec-

tive effect, according to the tested blood parameters.

However, treatments increased muscles’ resistance

to oxidative stress. In conclusion, silymarin supple-

mentation could contribute to improving meat qual-

ity and shelf life by the modulation of post-mortem

oxidative stability.

Acknowledgements

Mr. Luigi Faroldi for technical support. Research

supported by BIOTRADE snc, Mirandola, Modena

(Italy) and University of Torino (‘Fondo Ricerca

Locale- ex 60%’ – 2004).

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use of silybum marianum fruit extract in broiler chicken nutrition influence on performance and meat...

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