International Dairy Journal 21 (2011) 901e906

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International Dairy Journal

journal homepage: www.elsevier.com/locate/idairyj

Antioxidant and anti-platelet properties of milk from goat, donkey

and cow: An in vitro, ex vivo and in vivo study
Yannis Simos a, *, Apostolos Metsios a, Ioannis Verginadis a, Angela-Gabriella DAlessandro b,
Pasquale Loiudice c, Emilio Jirillo d, Pavlos Charalampidis a, Valantis Kouimanis a,
Athina Boulaka a, Giovanni Martemucci b, Spyridon Karkabounas a
a

Laboratory of Experimental Physiology, Faculty of Medicine, University of Ioannina, 45110 Ioannina, Greece
Dept. PRO.GE.S.A., University of Bari, Italy
Azienda Ospedaliero Universitaria Pisana, Via Paradisa, 2 e Cisanello, 56124 Pisa, Italy
d
Immunology, Faculty of Medicine, University of Bari, Bari, Italy
b
c

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 16 December 2010
Received in revised form
10 May 2011
Accepted 27 May 2011

A study was conducted to evaluate the biological properties of milk from different animals and breeds
such as cows, goats (Prisca, Ionica or Saanen breeds) and donkeys (Martina Franca breed). Methods
included in vitro, ex vivo and in vivo experiments to evaluate the activity of milks on platelet aggregation
and antioxidant capacity. The in vitro trials results demonstrated the highest total antioxidant
capacity (TAC) in goats milk, especially from Prisca breed. Ex vivo trials showed that Prisca goats milk
inhibits platelet aggregation at lower amounts than milk from other species. Consumption for 40 days of
0.6 L day
1 of Prisca goats milk signicantly increased TAC in healthy volunteers. This study contributes
to dening the biological properties of milk from these animals/breeds. Goats milk from the autochthonous Greek breed (Prisca) provided the best antioxidant capacity and inhibitory properties on platelet
aggregation of the milk samples tested.
2011 Elsevier Ltd. All rights reserved.

1. Introduction
Milk contains several physiologically functional components
including proteins, vitamins such as vitamin E, and C as well as
carotenoids and avonoids with antioxidant properties. Therefore,
milk with a higher antioxidant capacity will reect greater oxidative stability and provide potentially greater protection for the
consumer from exposure to the oxidative stress that is recognized
as a prominent feature of many acute and chronic diseases (DalleDonne, Rossi, Colombo, Giustarini, & Milzani, 2006; Valko et al.,
2007).
In recent years, considerable interest has focussed on goats and
donkeys milk for their nutritional and biofunctional properties
(Amati et al., 2010; DAlessandro, Martemucci, Jirillo, & Leo, 2010;
Jirillo et al., 2010; Tafaro et al., 2007). Goats milk and derived
dairy products assume importance in the human diet, with
particular relevance in infants for whom goats milk represents an
alternative to cows milk (Hanlein, 2001). From a nutritional point

* Corresponding author. Tel.: 30 26510 07602; fax: 30 26510 07850.

E-mail address: isimos@cc.uoi.gr (Y. Simos).
0958-6946/$ e see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.idairyj.2011.05.007

of view, goats milk is different from that of other species

(Park, 2006). It is characterized by small sized fatty acid globules
(Attaie & Richter, 2000) and a high content of short chain fatty acids
(Alonso, Fontecha, Lozada, Fraga, & Jurez, 1999), which improve fat
digestibility and intestinal absorption (Hachelaf et al., 1993)
compared with cows milk (Chandan, Attaie, & Shahani, 1992).
Moreover, the presence of medium-chain fatty acids (caproic,
caprilic and capric acid) in goats milk has been attributed to
a reduction of cholesterol in human tissues by limiting cholesterol
storage and improving its mobilization (Hanlein, 1992). Goats milk
is thought to have a low allergenic potential compared with cow
milk on the basis of characteristics of aS1-casein (Roncada,
Gaviraghi, Liberatori, Bini, & Greppi, 2002). In a recent study
(Amati et al., 2010), it has been shown that daily use of goats milk
in the diet of immuno-compromised aged patients acts as a downregulator of acute inammation, reducing the exaggerated basal
secretion of interleukin (IL)-8 and IL-6 acute response, and exerting
a moderate down-regulation of IL-1b and tumour necrosis factor
(TNF)-a production. Casein macropeptides from bovine, ovine and
caprine milk exhibit antithrombotic properties similar to the
activity of g-brinogen 400e411 peptide (Manso, Escudero, Alijo, &
Lopez-Fandino, 2002; Qian, Jolles, Migliore-Samour, Schoentgen, &

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Y. Simos et al. / International Dairy Journal 21 (2011) 901e906

Fiat, 1995a). Lactoferrin isolated from sheep presented similar

properties in reducing platelet aggregation as human lactoferrin
(Qian, Jolles, Migliore-Samour, Schoentgen, & Fiat, 1995b). More
interesting is the fact that lactoferrin inhibited platelet aggregation
in concentrations not far from physiological levels.
Donkeys milk is very different from milk of other species
traditionally used for human feeding such as cows, goats and
sheep milks (Alais, 1984), showing a closer similarity to human
milk (Conte, Calabr, & Mons, 2003; Guo et al., 2007). Recent
studies have indicated donkeys milk may be a promising food for
children affected by cows milk protein allergy or multiple food
intolerance (Alessandri & Mari, 2007; Carroccio et al., 2000; Iacono
et al., 1992; Tesse, Paglialunga, Braccio, & Armenio, 2009) and in the
elderly, because of its ability to up-regulate the immune response
(Amati et al., 2010; Tafaro et al., 2007). In particular, the effect of
donkeys milk on immune response resulted in a signicant
increase of IL-8 and IL-6 acute response and in up-regulation of
IL-1b and TNF-a production (Amati et al., 2010).
The objective of this study was to evaluate and compare,
through in vitro, ex vivo and in vivo experiments the antioxidant
activity and inhibition of platelet aggregation capability of goats
and, donkeys milks in comparison with cows milk. Milk from
different goat breeds was also considered.
2. Materials and methods
2.1. Reagents and apparatus
Ammonium dichromate, 3-methylbutanol, a-tocopherol, sulphuric acid and hydrogen peroxide of high purity, adenosine
diphosphate (ADP), platelet-activating factor (PAF), g-linolenic acid
and linoleic acid were purchased from SigmaeAldrich Co (St. Louis,
MO, USA). Total antioxidant capacity (TAC) measurements were
made with a Thermo Scientic MultiSkan Spectrum UV/Vis microplate (Thermo Fischer Scientic Inc. Waltham, MA, USA) and cuvette
spectrophotometer using disposable polysterene square cuvettes of
10 mm optical pathway purchased from Sarstedt Co (Sarstedt AG &
Co. Postfach, Nmbrecht, Germany). Platelet aggregation was performed in a Chrono-log Corporation Model 500-Ca aggregometer
(Chrono-log Corporation, Havertown, PA, USA) using glass cuvettes.
Atomic absorption spectroscopy was performed on a Perkin Elmer
spectrometer, model 560 (Perkin Elmer Waltham, MA, USA).
2.2. Milk source
The study was performed on milk from different species such as
goat, donkey and cow. Commercial, pasteurized, whole (3.5% fat)
cows milk was used as the control. As experimental milk, goats
milk was obtained from different breeds from Greece (Prisca, an
autochthonous breed) and Italy (Ionica, an autochthonous breed;
Saanen, a cosmopolitan breed). Animals of Prisca and Ionica breeds
were reared under extensive conditions on natural pasture in the
area of Epirus (Greece, North West) and Apulia (South Italy),
respectively, while Saanen goats were reared under semi-extensive
system (pasture and integration with concentrate) according to the
common breeding system in the area of Apulia. Donkeys milk was
obtained from a local Italian breed (Martina Franca) reared under
extensive conditions on natural pasture in Apulia. Experimental
milk samples from goats and donkeys were collected in spring,
pasteurized and frozen at
76  C until analysed.
2.3. In vitro experiments
A series of in vitro experiments were performed to evaluate total
antioxidant capacity and the levels of zinc (Zn) and cadmium (Cd)

of milk from different species such as cows (commercial whole,

pasteurized, 3.5% fat cows milk), donkeys and goats. Goats milk
was also tested in relation to different breeds (Prisca, Ionica and
Saanen goats). Estimation of TAC was performed using the Blue
CrO5 assay, according to Charalampidis, Veltsistas, Karkabounas,
and Evangelou (2009) and results are expressed as mM of
a-tocopherol. Zinc and cadmium levels in plasma were measured
by atomic absorption spectroscopy (Perkin Elmer Waltham, MA,
USA). Samples were diluted with four volumes of deionized water
(ddH20) for the zinc measurements. Sensitivity was set at
0.018 mg mL
1 of Zn and 0.025 mg mL
1 of Cd for 1% absorption.
Results are expressed as ppm for Zn and ppb for Cd. All measurements for TAC and atomic spectroscopy were performed in
triplicate.
2.4. In vivo experiments
On the basis of the results of the in vitro experiments performed
in this study, which have shown the highest TAC for goats milk
from Prisca breed, in vivo experiments were undertaken to evaluate
the effects of consumption of milk or vitamin supplementation on
platelet aggregation and plasma antioxidant capacity.
In the present experiments, 25 healthy volunteers (11 male and
14 female), between 23 and 57 years of age (mean age 29  10 y)
were recruited. The volunteers were divided into two groups, corresponding to: Group I (Milk Group, 13 volunteers) and Group II
(Antioxidants Group, 12 volunteers). The volunteers from Group I
consumed 0.6 L day
1 of goats milk from Prisca breed for 40
consecutive days. The volunteers of Group II were supplemented
daily with a mixture of 0.375 g vitamin C in the form of L-ascorbic
acid, and 0.125 g of vitamin E in the form of D-a-tocopherol, for the
same period. Blood collection was performed at the beginning and
at the end of the experiment.
2.4.1. Volunteer blood donors
The volunteers followed a stable normal diet, with respect to
energy value, carbohydrates, lipids, proteins, fruits and vegetables,
according to individual weight and age. The compliance of volunteers to their diet was veried every week with a 24 h recall, in an
interview with a certied dietician and weight measurement. The
volunteers were free of medical problems in their history. Moreover, they did not consume any kind of medication or food
supplements, and did not consume alcoholic drinks during the
experiment. The participation of the volunteers in the study was
without monetary compensation and in agreement with the
human rights legislation from the Declaration of Helsinki (1979).
2.4.2. Preparation of platelets
Blood was taken from the basilica vein of the arm from the
volunteers of both groups by free ow with the aid of an appropriate needle. The blood was placed in test tubes containing citric
acid as anticoagulant agent in the proportion 1 mL of anticoagulant
solution to 9 mL of blood. Centrifugation of the blood samples was
performed at 54  g for 20 min to obtain the plasma rich in platelet
(PRP) fraction. The PRP was placed in a plastic test tube and was
kept in a water bath at 37  C until the termination of the platelet
aggregation tests. The test tubes containing the rest of the blood
were centrifuged again at 645  g for 20 min to isolate the plasma
poor in platelets (PPP) fraction, which was collected in a plastic
tube and used for calibration of the aggregometer.
2.4.3. Platelet aggregation
All assays for platelet aggregation and platelet reactions (shape
changes and release reaction) were conducted on the aggregometer. The assessments were conducted in a cuvette, which

Y. Simos et al. / International Dairy Journal 21 (2011) 901e906

contained 450 mL of PRP and 50 mL of each of two diluted platelet

agonists (ADP and PAF) in ddH2O.
2.5. Ex vivo experiments
The aims of the ex vivo experiments were the evaluation of
activity of milk from different origin (cow, donkey and goat breeds),
at different doses (2.5, 5.0, 10.0 and 20.0 mL) on platelet aggregation.
The experiments were carried out on blood collected from the
basilica vein of the arm of 12 healthy volunteers according to the
criteria described above. The same procedure as described above
was also followed for the preparation of platelet. The control assay
was conducted in a cuvette, which contained 450 mL of PRP and
50 mL of each of two diluted platelet agonists (ADP or PAF) in
ddH2O. Moreover, the experiment assay was also conducted in
a cuvette, containing 450 mL PRP and 50 mL of diluted milk in ddH2O.
Initially, the milk was added into the cuvette, containing 450 mL
PRP, and incubated for a few minutes. After that, each of the two
platelet agonists was added to the cuvette, to observe the
percentage of platelet aggregation. Blood sample analysis was
performed in triplicate for each of the two platelet agonists.
2.6. Statistical analysis
All statistical procedures were performed using SPSS (SPSS 16.0,
SPSS Inc. Chicago, Illinois, USA, 2009). The statistical signicance
between data means was determined by using paired sample t-test.
Data are expressed as mean  SD.
3. Results
3.1. In vitro trials
The in vitro assessments of TAC and levels of Zn and Cd in milk
from the different origins (cow, donkey and goat breeds) are
reported in Table 1. Among the various types of milk, milk of Prisca
goats showed the highest (P < 0.01) antioxidant capacity (66.7 mM
a-tocopherol). This value of TAC was 2 times higher than in Saanen
and Ionica goat breeds (33.6e35.8 mM a-tocopherol, respectively)
and in donkeys milk (31.2 mM a-tocopherol), and 1.5 fold higher
than in cows milk (42.9 mM a-tocopherol).
Analyses of the Cd content showed the highest (p < 0.01) level in
milk of Saanen goats (9.13 ppb) and commercial cows milk
(8.44 ppb), whereas donkeys milk presented the lowest levels
(0.60 ppb). Zinc levels were the lowest in donkeys and Prisca goats
milk (2.3 and 2.6 ppm, respectively) in comparison with the other
milk (range 3.09e3.90 ppm; 0.05 > P < 0.01). Donkeys milk also
had the lowest Cd/Zn ratio (0.15; P < 0.01).

903

Table 2
Plasma total antioxidant capacity (TAC) and platelet aggregation (% platelet aggregation compared to the control) with adenosine diphosphate (ADP) or plateletactivating factor (PAF) in Group I and Group II volunteers.a
Parameter

Group I

Group II

D0

D40

D0

D40

TAC (mM a-tocopherol)

Platelet aggregation (ADP)
Platelet aggregation (PAF)

27.9  3.3a
68.4  7.8
72.3  6.4a

30.3  3.6b
67.4  7.8
66.5  9.9b

30.7  7.7
60.9  4.8
59.3  8.1

31.7  9.6
58.9  8.2
57.4  7.3

a
Group I volunteers consumed 0.6 L goats milk per day for 40 days; Group II
volunteers were orally supplemented with 0.375 g vitamin C and 0.125 g of vitamin
E per day for 40 days. Blood collection was performed at the beginning (D0) and at
the end of the experiment (D40). Data are presented as mean  SD of three
determinations. Different superscripts in row denote signicantly different,
P < 0.05.

goats milk (Group I) for 40 days signicantly increased plasma

antioxidant capacity (P < 0.05). Conversely, at the end of the
supplementation period with vitamin C and vitamin E, the volunteers of Group II showed no change in their plasma antioxidant
capacity (P > 0.05).
The inhibitory effect on platelet aggregation, through either ADP
or PAF, was not statistically signicant after vitamin C and E
supplementation (Group II). In contrast, in Group I, Prisca goats
milk consumption signicantly reduced (P < 0.05) the levels of
platelet aggregation through the PAF pathway.
3.3. Ex vivo trials
Fig. 1 shows the results of ex vivo trials on evaluation of activity
of milk from different origins, according to different doses (2.5, 5.0,
10.0 or 20.0 mL), on platelet aggregation using ADP or PAF agonist.
Inhibition of platelet aggregation was signicantly different with
respect to milk origin. Considering the minimum dose of milk
(2.5 mL), the highest (P < 0.01) inhibition of platelet aggregation
was shown by goats milk of all the breeds evaluated, when ADP as
the platelet agonist was used (67e71%; Fig. 1A). Using PAF as the
platelet aggregation agonist, at the same dose of milk, the stronger
inhibitory capacity was shown by goats milk from Prisca and Ionica
breeds and cows milk (71e73%; P < 0.01; Fig. 1B). The volume that
caused total inhibition of platelet aggregation (100%) was 10 mL for
Prisca goats milk, using either ADP or PAF (Fig. 1). Milk from the
Ionica and Saanen goats and cows also showed more or less
a complete inhibitory effect (96e100%) at a dose of 20 mL. Donkeys
milk did not have any inhibitory effect on ex vivo platelet aggregation (21e27% inhibition of platelet aggregation at 2.5 mL; 33e44%
at 20 mL).
4. Discussion

3.2. In vivo trials

The results of the in vivo trials on the effects of goats milk on
TAC and platelet aggregation are shown in Table 2. Consumption of

In vitro trials on milk from different sources show that the

antioxidant potential of milk from Prisca goats was higher than
milk from Ionica and Saanen goats, cows and donkeys. This positive

Table 1
In vitro total antioxidant capacity (TAC) in plasma and levels of Cd and Zn of milk from different origins.a
Component

Cows milk

Goats milk from:

Prisca

TAC (mM a-tocopherol)

Cd (ppb)
Zn (ppm)
Cd/Zn ratio

42.9
8.44
3.90
2.17






2.10Ca
0.42A
0.24A
0.15Aa

66.7
3.33
2.57
1.29






Donkeys milk
Saanen

2.30A
0.25B
0.17B
0.11C

35.8
9.13
3.59
2.55






Ionica
2.70BCb
0.40A
0.13A
0.13Ab

33.6
3.04
3.09
0.78






3.20B
0.15B
0.49ABa
0.05B

31.2
0.60
2.27
0.15






2.90B
0.06C
0.16Bb
0.02D

a
Data are presented as mean  SD of three determinations. Different superscripts in row differ signicantly; upper case letters show P < 0.01, lower case letters show
P < 0.05.

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Y. Simos et al. / International Dairy Journal 21 (2011) 901e906

Fig. 1. Effects of milk from cow ( ), Prisca goats ( ), Saanen goats ( ), Ionica goats ( ) and donkeys ( ) and in increasing doses on ex vivo percentage of platelet aggregation
compared with the control (control 100%): (A) adenosine diphosphate as platelet agonist; (B) platelet-activating factor as platelet agonist. Blood was collected from 12 healthy
volunteers and trials were performed in triplicate. Data are expressed as means  SD. Different letters indicate the signicant differences either among the doses of the milk within
the same source (A, B, C: P < 0.01; a, b: P < 0.05) or among the milk from different sources within the same dose (D, E, F, G: P < 0.01; d, e: P < 0.05).

effect shown by Prisca goats milk agrees with the increasing trend
of plasma TAC found in in vivo trials after its daily consumption for
40 days, unlike the daily consumption of vitamins C and E. It could
be hypothesized that a period of milk consumption longer than
40 days could have a more signicant effect in terms of antioxidant
capacity. The antioxidant capacity of goats milk might be attributable not only to its composition, that is very rich in antioxidants
as reported by some authors (Chilliard, Ferlay, Rouel, & Lamberet,
2003; Contarini & Avalli, 2001), but probably to the particular
combination of compounds or their greater bioavailability.
Antioxidant capacity of various types of milk has been determined by different methods such as the oxygen radical absorbance
capacity (ORAC) and trolox equivalent antioxidant capacity (TEAC)
assays (Saenz, Elisia, Innis, Friel, & Kitts, 2009; Zulueta et al., 2009).
Zulueta et al. (2009) have provided evidence that the major
contributors of TAC in whole milk are the casein fractions and the

hydrophilic antioxidant compounds, such as vitamin C and uric

acid, in the deproteinised milk. Total casein content is similar in
cows milk and goats milk but their fraction composition differs to
a great extent since the major casein fraction of cows milk is a aS1casein and of goats milk is b1- and b2-caseins (Slacanac et al., 2010).
In our study, milk from Prisca goats, as well as Ionica goats,
showed a higher anti-platelet effect than that of Saanen goats and
of donkeys. It could be attributed to different milk characteristics
due to genotype and/or rearing system and/or diet composition of
the animals. In the present study, Prisca and Ionica goats were
reared under extensive breeding conditions on pasture. The milk
feeding system can have an important role on nutritional quality of
milk, since milk from pasture-fed animals contains high amounts of
polyunsaturated fatty acids, particularly 18:2 and 18:3 (Chilliard
et al., 2003; Palmquist, 1988; Shingeld, Chilliard, Toivonen,
Kairenius, & Givens, 2008). In milk from pasture-fed cows milk,

Y. Simos et al. / International Dairy Journal 21 (2011) 901e906

Schroeder, Gagliostro, Bargo, Delahoy, and Muller (2004) also

reported that fatty acid content is highly unsaturated (average
70e90%), with a large amount of linoleic and linolenic acids.
Pizzoferrato et al. (2007) correlated the degree of antioxidant
protection (DAP) with quality of goat milk. Specically, DAP value
was higher when pasture herbage was dominant in animal feed, as
is likely to have occurred in our study for Prisca and Ionica goats
milk. Moreover we can speculate that the lower response of the
Saanen goats milk in comparison with Prisca and Ionica breeds,
besides the genetic difference, could be linked to the different
feeding system of the animals, constituted by pasture and supplementation of concentrate. In fact, Pizzoferrato et al. (2007) showed
that in grazing goats, the supplementation of feeding with barley,
chickpeas, corn or beans grain, tended to reduce the levels of atocopherol and DAP in milk. Kondyli, Katsiari, and Voutsinas (2007)
have found that goats milk of the native Greek breed reared on
pasture contains a high quantity of vitamins such as vitamin C.
Boosting the human bodys defence mechanism with adequate
amounts of natural antioxidants provided by diet can boost
immunity and reduce the chance of disease. When the body has
insufcient antioxidants, oxidative stress increases and this can
lead to signicant damage and disease (Dalle-Donne et al., 2006).
Many mainstream health and nutrition organizations world-wide
recommend daily consumption of dairy products for optimal
health (Bishop-MacDonald, 2005). In this context, the present
study contributes to identifying some bioactive components of milk
for human health.
5. Conclusions
This study evaluates the biological properties of milk from
different sources such as goat (Prisca, Ionica or Saanen breeds) and
donkey (Martina Franca breed) in comparison with cows milk, in
three experimental models (in vitro, ex vivo and in vivo). The
results showed that the species from which the milk is sourced
affects the biological characteristics of milk in terms of TAC and
anti-platelet effect. Milk from Prisca goats had the highest in vitro
TAC in comparison with the other goat breeds (Ionica and Saanen),
cows milk and donkeys milk. This higher antioxidant capacity of
Prisca goats milk was conrmed in an in vivo trial where participants consumed the milk for 40 days, in comparison with the
consumption of a mixture of vitamin C and E, suggesting a better
bioavailability of antioxidant compounds of milk compared with
vitamin integration in the diet. Donkeys milk had a low in vitro TAC
and did not have any inhibitory effect on ex vivo platelet aggregation. The ex vivo trial showed that milk of Prisca and Ionica goats
had the highest inhibition of platelet aggregation with the
minimum dose of milk, using either ADP or PAF agonists. These
ndings lead us to hypothesize the positive inuence of natural
pasture on total antioxidant capacity and inhibitory properties on
platelet aggregation of goats milk. Further studies are needed to
strengthen the knowledge on factors (feeding, season, etc.,) and
mechanisms involved in the biological properties of goat milk.
Acknowledgements
The research was supported by INTERREG III/A Greece-Italy
(Project Code I 2101030) Paper N. 31.
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