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Dietary plant bioactives for poultry health and productivity
R. J. Wallacea; W. Oleszekb; C. Franzc; I. Hahnc; K. H. C. Baserd; A. Mathee; K. Teichmannf
a Rowett Institute of Nutrition and Health, University of Aberdeen, Aberdeen, AB21 9SB, UK b Institute
of Soil Science and Plant Cultivation, State Research Institute, Pulawy, Poland c University of
Veterinary Medicine, Vienna, Austria d Department of Pharmacognosy, Faculty of Pharmacy, Anadolu
University, Eskisehir, Turkey e Western Hungarian University, Department of Botany, Hungary f
BIOMIN Research Center, Tulln, Austria
Online publication date: 30 September 2010
To cite this Article Wallace, R. J. , Oleszek, W. , Franz, C. , Hahn, I. , Baser, K. H. C. , Mathe, A. and Teichmann, K.(2010)
'Dietary plant bioactives for poultry health and productivity', British Poultry Science, 51: 4, 461 — 487
To link to this Article: DOI: 10.1080/00071668.2010.506908
URL: http://dx.doi.org/10.1080/00071668.2010.506908
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British Poultry Science Volume 51, Number 4 (August 2010), pp. 461
—
487
INVITED REVIEW PAPER
Dietary plant bioactives for poultry health and productivity
R.J. WALLACE, W. OLESZEK
1
, C. FRANZ
2
, I. HAHN
2
, K.H.C. BASER
3
,
A. MATHE
4
AND K. TEICHMANN
5
Rowett Institute of Nutrition and Health, University of Aberdeen, Aberdeen, AB21 9SB, UK,
1
Institute of
Soil Science and Plant Cultivation, State Research Institute, Pulawy, Poland,
2
University of Veterinary
Medicine, Vienna, Austria,
3
Department of Pharmacognosy, Faculty of Pharmacy, Anadolu University,
Eskisehir, Turkey,
4
Western Hungarian University, Department of Botany, Hungary, and
5
BIOMIN
Research Center, Tulln, Austria
Abstract 1. Plants and their biologically active chemical constituents, sometimes called secondary
metabolites or bioactives, present numerous opportunities for the improvement of livestock production
by inclusion in the diet.
2. Many such plant derived materials have well established therapeutic values in man; however, their
potential as feed additives in animal production, particularly of poultry, remains largely unexploited.
3. There is increasing evidence indicating that they can be efficient in controlling diseases, and plant
bioactives may also influence production parameters such as feed efficiency and product quality.
4. It has been reported that they may even replicate some of the effects of antibiotic growth
promoters, which were banned from use in Europe from 2006.
5. This review assesses the status of plant bioactives in poultry production and their mode of action
on avian physiology, particularly in the digestive tract.
INTRODUCTION
Interest in plants, plant extracts and derived
phytochemicals (botanicals) as components of
livestock feedstuffs has increased during the last
decade. Much of the impetus for revisiting the
plant kingdom to look for new, useful additives
that can enhance health and productivity results
from concerns about the safety and sustainability
of antibiotic growth promoters. If transmissible
antibiotic resistance factors result from the use
of growth-promoting antimicrobials (GPA) in
animal production, the efficacy of similar anti-
biotics in therapy for human diseases may be
compromised. Hence, the EU introduced a ban
on GPA in 2006. Other nations may follow. Before
the ban, poultry production had a high depen-
dence on GPA to control intestinal pathogens
such as Escherichia coli,Clostridium perfringens
and coccidial infection. Since then, improved
management has compensated for some of the
production-benefit losses, but not all. Consumer
pressure also plays a part in the move to more
‘‘naturally’’ produced foods (Rickard, 2004). The
increasing demand for organically produced
foods also drives the search for alternative feed
additives (Griggs and Jacob, 2005).
Botanicals should not be considered only as
replacements for GPA, however. They have useful
properties not shared by GPA. Herbs, spices and
their extracts can stimulate feed intake and
endogenous secretions (Wenk, 2003). Many bota-
nicals have antioxidant activities that can improve
the oxidative stability of poultry meat and eggs,
increasing their shelf life. They may stimulate
immunity directly, improving birds’ resistance to
disease. They also have the potential to modify
cholesterol metabolism, leading to a product with
Correspondence to: Professor R.J. Wallace, University of Aberdeen, Rowett Institute of Nutrition and Health, Bucksburn, Aberdeen, AB21 9SB, UK.
E-mail: john.wallace@abdn.ac.uk
Accepted for publication 22nd January 2010.
ISSN 0007–1668(print)/ISSN 1466–1799 (online)/10/040461
—
27 ß2010 British Poultry Science Ltd
DOI: 10.1080/00071668.2010.506908
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healthier implications for human production.
Even reproduction may be improved by increas-
ing semen quality (Durape, 2007).
A final consideration, indeed the most
important of all, is that many plants and phyto-
chemicals have adverse effects on animals when
ingested. Acamovic and Brooker (2005) remind
us: ‘‘The effects depend to a great extent on the
chemistry of the compounds, their concentration
in the diet and the amount consumed, and are
further dependent on the health status of the
animals. Traditionally, most studies of the effects
of these compounds on animals have focused on
their adverse effects and how to alleviate them.
However, recent public concern about the use of
synthetic compounds in animal diets to enhance
performance and health and welfare issues,
coupled with changes in regulations on the use
of synthetic medicaments, has stimulated interest
and research in the use and effects of phytochem-
icals in the diets of farmed animals.
Phytochemicals vary in their chemistry but can
be divided into hydrophilic and hydrophobic
compounds, of which a wide variety of polyphe-
nolic and terpenoid compounds, as well as
alkaloids, carbohydrates and non-protein amino
acids, invoke special interest’’.
The use of botanicals in human and animal
health undoubtedly has potential value
—
many
widely used therapeutic drugs originate from the
plant kingdom
—
but the use of botanicals in
animal production is less well established. It is
important to provide a good description of each
plant, its active phytochemicals and their mole-
cular mode of action against microorganisms or
their interaction with the host. Given the vastness
and diversity of the plant kingdom, variations
between cultivars, variation in applications, and
many other factors, such a complete description
will never be attainable. Nevertheless, it might
reasonably be expected that botanicals in
common use or intended for widespread applica-
tion should have a body of efficacy, safety and
mechanistic information to enable users to assess
and understand the biological activity of the
botanical in question. The aim of this review was
to report on the status of the botanicals field in
poultry in relation to these benchmark criteria.
The review itself was prompted by two main
drivers. One was the EC Framework 7 Specific
Support Action, contract 43077, FEED-SEG,
a consortium whose broad objective is ‘‘to
disseminate state-of-the-art research results in
feed quality topics... (and to)... develop strate-
gies and recommendations for European policies
(e.g. research, health, agriculture)’’. The second
was the publication of an excellent review for
botanicals and ruminants (Rochfort et al., 2008).
The challenge that we as authors of this article
accepted was to attempt to replicate the review of
Rochfort et al. (2008), with poultry rather than
ruminants as the subject group of animals.
Poultry production encompasses broilers, layers
and breeders from different species
—
chicken,
turkey, and duck principally. Much less is known
about the ostrich (Vispo and Karasov 1996), in
spite of its growing commercial importance. This
review focusses on plant bioactives, poultry
production and its underlying science, and does
not repeat the comprehensive sections in the
Rochfort et al. (2008) review on social and
regulatory issues, to which the reader is referred.
THE STATUS OF PLANT BIOACTIVES
AS FEED ADDITIVES
Generally speaking, feed additives are considered
as being applied in the feed by the farmer to
healthy animals not only for nutritional purposes
but also additional functionality on a long-term
basis (possibly along the entire production period
of the respective species), in contrast to veterinary
drugs used only to treat health problems under
control of a veterinarian, applied for a limited
period only. As per definition from Regulation
(EC) No. 1831/2003, ‘‘feed additives are sub-
stances or preparations
—
other than feed material
or premixtures
—
which are intentionally added to
feed or water in order to
—
favourably affect the characteristics of feed, as
e.g. flavouring or antioxidant,
—
affect the characteristics of animal products
regarding microbial load, shelf life or taste,
—
affect the environmental consequences of espe-
cially large-scale livestock production e.g. by
reduction of ammonia excretion or methane
production,
—
favourably influence animal production, perfor-
mance or welfare by affecting the gastrointestinal
microbiota and the digestibility of feeding stuffs, or
—
have a coccidiostatic or histomonostatic effect’’.
Thus, this review, for the most part (as
benefits to productivity are inevitably linked
with the control of disease) concentrates on
plant bioactives as feed additives rather than
therapeutics. Valuable effects on, for example,
fowl typhoid (Waihenya et al., 2002a) would not
normally be covered.
Presently, herbal products are used by the
feed industry predominantly as sensory additives,
flavouring and appetising substances. Although
an understanding of their mode of action would
be a prerequisite for their optimal application
in terms of efficacy, a full understanding of
these aspects in animals is not yet achieved.
For example, aromatic compounds and essential
oils (EO) act along the animal digestive tract
462 R.J. WALLACE ET AL.
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to improve appetite, bacterial modulation,
and are able to induce a number of benefits on
well being (Kamel, 2001). The antimicrobial
properties of EOs and extracts can be dose-
dependently bacteriostatic and/or bactericidal.
In addition, several investigations have shown an
antioxidative effect or changes in digestive
physiology and digestion at weaning (Zabielski
et al., 1999), the microbiology of the gut (Jensen,
1998) and the implementation of test models in
poultry (Hess, 2002). Another complication is
that plant bioactive compounds occur in nature
as complex mixtures rather than as single
compounds, and synergy between individual
components may be an important feature of
their action.
Plant bioactives are often proposed as
possible replacements for AGP. Their efficacy
in achieving the same effects remains open to
question, but an undoubted advantage of plant
bioactives over GPA is that resistance is less likely
to become a problem than with conventional
synthetic compounds.
It must also be remembered that plants
contain many poisonous compounds, including
some of the most toxic known to man. Some
plant extracts may therefore be detrimental for
poultry and by numerous mechanisms may
decrease body weight, feed intake (FI) and feed
conversion ratio (FCR) and digestibility. They
can also influence mortality, muscular conditions
and in some instances can be neurotoxic.
BIOACTIVE COMPOUNDS AND THEIR
EFFECTS ON PRODUCTION
Production efficiency and incidence
of disease
Numerous feeding trials have been performed
with plant extracts, aromatic herbs and EOs
additives, to investigate production parameters
No. of natural
products
With N
1. Alkaloids 12 000
2. Non-protein amino acids 600
3. Amines 100
4. Cyanogenic glycosides 100
5. Glucosinolates 100
Without N
6. Monoterpenes 1 000
7. Sesquiterpenes 3 000
8. Diterpenes 2 000
9. Triterpenes, Saponins, Steroids 4 000
Tetrapenes 350
10. Flavonoids 2 000
11. Polyacetylenes 1 000
12. Polyketides 750
Phenylpropanes 1 000
Figure. Structures, estimated range and numbers of plant secondary metabolites (re-drawn from Acamovic and Brooker (2005), with
permission).
PLANT BIOACTIVES: A REVIEW 463
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Table 1. Performance effects of plant material and plant extracts used as feed additives in poultry nutrition
Performance effect
Plant species/extract Dose Beneficial No effect Detrimental Literature
Aesculus hippocastanum 0
—
10 mg/g body Depression Williams and Olsen (1984)
Muscular incoordination
paralysis
Alfalfa extract 0.06% Thymus and spleen weight FI Abdominal fat weight Dong et al. (2007)
Bursal weight FCR
Immunity
Aloe secundiflora extract
—
Reduced mortality in Newcastle
disease infection, Increase of
interleukin 6
Antibody levels
—
Waihenya et al. (2002a,b)
Artichoke water extract 5% DM Humoral immune response
——
Stoev et al. (2000)
Organ weight
Protection against ochratoxin A
Balanites aegyptiaca
saponins
5
—
250 mg/kg/day Total cholesterol Body weight Nakhla et al. (1992)
Calendula officinalis extract Drinking water Mean weight FCR Immune response Barbour et al. (2004)
Mortality Bursal weight index
Cassia obtusifolia 2% body weight
—
Weight gain FI Hebert and Flory (1983)
Cassia occidentalis
——
Weight Graziano et al. (1983)
Muscular weakness
Citrus extract 10
—
1000 g/t Live weight Metabolisable energy
—
Juin et al. (2003)
FI
Colchinchina momordica 5
—
80 mg/dose Antibody level
——
Rajput et al. (2007)
extract Daily weight gain
EO (thymol, cinnamalde-
hyde, commercial
preparation)
100 ppm
—
FI
—
Lee et al. (2003)
Weight gain
FCR
Liver weight
Ileal digestibility
Fermented wheat germ
extract
—
Suppression of Mycoplasma
gallisepticum infection
Body weight gains
—
Stipkovits et al. (2004)
FCR
Field bean tannin hulls
——
Digestibility Flores et al. (1994)
TMEn
Garlic extract 3.8% garlic Cholesterol level
——
Qureshi et al. (1983)
paste Enzyme suppression
Grape seed extract 2.59
—
5.18% Post mortem meat parameters Weight gain Lau and King (2003)
Hemp seed meal
—
Concentration of palmitic acid
and higher linoleic acids in
eggs
Egg production Silversides and Lefrancois (2005)
FI
464 R.J. WALLACE ET AL.
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Feed efficiency
Various herbs (thyme,
oregano, marjoram,
rosemary, yarrow) and
their EO
10 g/kg Performance Intestinal microflora Endogenous sialic acid
secretion
Cross et al. (2007)
Apparent metabolisable energy
Digestibility
Labiatae extract (sage,
thyme, rosemary)
5000 ppm Apparent faecal digestibility CP digestibility
—
Hernandez et al. (2004)
Ether extract digestibility Weight of organs
Lentinus edodes 0.5
—
4 g/kg Body weight gain Relative weights of organs and GIT
—
Guo et al. (2004b)
Tremella fuciformis FCR
FI
Linseed meal 20% Selenium toxicity Growth rate
—
Jensen and Chang (1976)
Mangifera indica seed
kernel meal
50
—
250 mg/kg meal Body weight FI
—
Odunsi (2005)
Body weight gain Feed efficiency
Organ weights
Myristica fragrance
—— —
Deep sleep in young
chicken
Sherry et al. (1982)
Nepeta cataria 25
—
1000 mg/kg
——
Increased number
if sleeping chicks
Sherry and Hunter (1979)
Oregano, cinnamon and
pepper essential oils
200 ppm
—
FI
—
Hernandez et al. (2004)
FCR
Oregano essential oil 50
—
100 mg/kg
—
Growth Malondialdehyde in tissue Botsoglou et al. (2002)
Plant extracts containing
5% carvacrol, 3% cinna-
maldehyde, 2% capsi-
cum oleoresin
100 mg/kg Villi-related protective activity
——
Jamroz et al. (2006)
Adhesion of E. coli and
C. perfringens
Plant extracts containing
capsaicin, cinnamalde-
hyde and carvacrol
100 mg/kg Breast muscle proportion Ileal digestibility of nutrients
—
Jamroz et al. (2005)
Empty body weight
E. coli and C. perfringens numbers
Lactobacillus spp. number
Lipase activity
Rosemary extract 500
—
1000 mg/kg
—
Lipid oxidation parameters
—
Galobart et al. (2001)
Rye extract
——
Weight gain Day and Thomas (1980)
Saccharum officinarum 500 mg/kg/day Phagocytic activity of peripheral
blood leucocyte
——
Hikosaka et al. (2007)
Antibody response
Immunostimulating activity
(Continued).
PLANT BIOACTIVES: A REVIEW 465
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Table 1. Continued.
Performance effect
Plant species/extract Dose Beneficial No effect Detrimental Literature
Senna occidentalis seeds Extensive axonal damage Neurotoxic Calore et al. (1998)
Silybum marianum fruit
extract
40
—
80 ppm sylimarin Decrease of slaughtering yields Growth rate
—
Schiavone et al. (2007)
Reduction of lipid content in
meat
Hepatoprotection
Synclisia scabrida extracts
—
Apomorphine-induced stereotype
behaviour
——
Sokomba et al. (1986)
Pseudomanas and Staphylococcus
infection
Vicia faba tannin extract 8
—
16 g/kg
——
Mortality Ortiz et al. (1994)
Body weight
FI
FCR
Vicia faba proanthocyani-
din extract
30 g/kg Digestibility of protein Yuste et al. (1992)
Digestive enzyme
Yucca schidigera extract
—
FI Viscosity of proximal ileal content
—
Preston et al. (1999)
0.2% extract Body weight gain Yeo and Kim (1997)
Energy utilisation
Net ammonia production FI
CP, crude protein; DM, dry matter; EO, essential oil; FI, feed intake; FCR, feed conversion ratio; TMEn, true metabolisable energy.
466 R.J. WALLACE ET AL.
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such as feed intake, weight gain and feed
conversion rate (Table 1; see also Windisch
et al., 2008). Comparison of these data has
often been very difficult, however, as different
experiments were performed with different and
widely ranged doses. Some authors reported the
dose in mg per body weight, some in percentage
in the feedstuff, while the others calculated based
on the concentration of active principles. In
many cases FI and FCR have been influenced by
plant extracts. However, in a number of cases FI
and FCR were not changed but the extracts still
had positive effects on body weight, body weight
gain, organ weight and/or energy utilisation.
This results from the strong link between
productivity and health. Plant extracts may
stimulate the immune system (extracts from
alfalfa, artichoke, Saccharum officinarum, Table 1
and elsewhere in this review), suppression
of harmful microorganisms (Pseudomonas,
Staphyloccoccus,E. coli,Eimeria spp., C. perfringens,
Mycoplasma gallisepticum), stimulation of benefi-
cial microbes such as Lactobacillus spp. (extracts
containing capsaicin, cinnamaldehyde and carva-
crol), the regulation of the activity of some
enzymes (e.g. lipase), protection of gut villi and
bacterial adhesion parameters. Plant extracts may
also influence the post-mortem quality of meat,
especially cholesterol concentration, lipids con-
tent, oxidative stability, as well as the quality of
eggs, although sometimes better quality was
accompanied by reduced weight gain (grape
seed extract). An important parameter that can
influence growth performance is the protection
given by plant extracts against some toxins that
can be found in feedstuffs, e.g. ochratoxin A and
selenium.
An extract of sugar cane, which was the
residue after removing glucose, fructose and
sucrose from sugar cane juice was fed at the
dose of 0.5 g/kg/d (El-Abasy et al., 2002;
Yamauchi et al., 2006) to broilers. A higher
body weight gain, gain in body weight/day and
lower feed conversion ratio were observed under
this treatment, but, like many similar studies, the
phytochemical(s) responsible were not identified.
Besides some alterations in intestinal histology
(higher values of villus height, villus area,
epithelial cell area and cell mitosis) promoting
growth and showing immunostimulating effects
were observed. Chinese herbs were shown to be
effective feed additives replacing antibiotics in
Pekin meat duck diets (Wang and Zhou, 2007),
and a similar conclusion was drawn by Jamroz
and Kamel (2002) who observed improvements
in daily gain and feed conversion ratio in poultry
fed on a diet supplemented with plant extracts.
Plant extracts from milk thistle (90 and 180 mg/
kg feed), yarrow (900 and 1800 mg/kg), garlic
(8230 and 16460 mg/kg), oregano, juniper
(450 and 6000 mg/kg) and horseradish (450
and 6000 mg/kg) showed beneficial effects on
male broiler chickens (Lewis et al., 2003). Based
on feed conversion efficiency (FCE), two extracts
e.g. yarrow and garlic were indicated as promis-
ing. Garlic (1 g/kg feed) and thyme (1 g/kg feed)
were also most promising herb feed additive in
the research performed using 5 commercial feeds
supplemented with NorSpiceÕpowders (Demir
et al., 2003). Two additional commercial phyto-
genic feed additives XTRACT
TM
containing
carvacrol (5%), cinnamaldehyde (3%) and
Capsicum oleoresin (2%) as well as SangrovitÕ
containing ground roots of Sanguinaria canaden-
sis rich in the alkaloids sanguinarin and cheler-
ythrin had no effect on chicken growth
performance, nutrient utilisation or threonine
efficiency, but slightly improved daily gain
(þ3.7%) and feed conversion ratio (þ1.7%).
Dietary supplementation of an EO mixture
HerbromixÕ(oregano herb (Origanum onites),
laurel leaf (Laurus nobilis), sage leaf (Salvia
fruticosa), fennel fruit (Foeniculum vulgare),
myrtle leaf (Myrtus communis) and citrus peel
(rich in limonene) to broilers significantly
improved feed conversion rate above that of
the control group (Alcicek et al., 2004; Cabukt
et al., 2006a). In laying hens, cracked-broken egg
rate was decreased with the dietary supplement
of EO (Cabukt et al., 2006b). Supplying Oregano
EO reduced daily feed intake of broilers com-
pared to control animals. Enrichment with EO
significantly improved feed efficiency in broilers
(Halle et al., 2008). Most studies have shown
no significant difference in feed intake caused by
herbal or EO additives, but growth was often
enhanced and FCR rate improved. Since poultry
are known to adjust feed intake strongly accord-
ing to the demand of energy, FCR is therefore a
very sensitive parameter in responses to growth
promoters. Published results are, however, con-
tradictory. Lee et al. (2003a) fed broilers with
200 mg/kg feedingstuff carvacrol or thymol.
Carvacrol reduced feed intake, weight gain and
feed conversion rate, whereas thymol showed no
effect. Addition of oregano herb in quantities of
2
—
20 g/kg feed or oregano oil (100
—
1000 mg/kg
feed) resulted, in contrast, in all cases in better
performance of broiler chicks (Halle et al., 2004),
whilst another trial of the same group
(Westendarp et al., 2006) using carvacrol,
p-cymene and g-terpinene as pure substances
in approximate 50 (carvacrol) or 25 (terpinene,
p-cymene) mg/kg had almost no effect. Recently,
Haselmeyer (2007) studied the effect of thymol in
4 concentrations from 0.1 to 1.0% as a feed
additive in broilers. No significant difference in
performance was obtained over the whole grow-
ing period (35 d). Turkeys fed with 1.25
—
3.75 g/
kg dried oregano leaves showed, in contrast,
PLANT BIOACTIVES: A REVIEW 467
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a clearly improved feed conversion rate
(Bampidis et al., 2005). Adding 60 mg/kg carva-
crol-rich thyme oil to the diet resulted in
significantly higher body weight gain and better
feed efficiency as well as decreased abdominal fat
weight in quails (Denli et al., 2004). A dietary
supplementation of oregano EO (300 mg/kg)
showed a positive effect on performance of
broiler chickens experimentally infected with
Eimeria tenella (Giannenas et al., 2003).
In conclusion, the number of trials on the
effects of plant extracts on performance in
poultry is large. Recently, Windisch et al. (2008)
also evaluated some of the available studies in
broilers, turkeys and quails and concluded that a
majority of the studies showed a reduction in FI
due to the use of dietary plant extracts, a largely
unchanged body weight gain and as a result an
improvement in FCR. However, for each
response parameter (feed intake, body weight
gain and feed conversion ratio) differences in the
quantitative response were found in different
studies. Whether such a general statement is valid
is doubtful, as each plant extract or phytogenic
plant compound will most likely have a different
mode of action and result in different types of
effects on animal performance. A number of
studies have also shown no response or a positive
effect on feed intake and/or body weight gain. In
addition, the experimental conditions in which
the compounds are tested may greatly influence
the outcome of the evaluation, e.g. the nature of
the negative control treatment, experimental
conditions with regard to health status of the
birds and/or challenges imposed to the birds
during evaluation of the feed additives, or the
concentration of the compounds tested.
Moreover, it can be assumed that there will be
a publication bias in this area, meaning that
products or studies showing no or negative
effects have less chance of being published in a
refereed journal.
Product quality
Many plants or plant extracts contain bioactive
compounds that improve the quality of poultry
products, including both meat and eggs. The
main quality indices of interest are organoleptic
properties, storage stability and the ‘‘healthiness’’
of the product for consumption by man.
Although including herbs in the diet might be
expected to influence taste in particular, there
seem to be surprisingly few structured reports on
the influence of phytochemicals on the organo-
leptic qualities of poultry products (Rizza et al.,
2008; Windisch et al., 2008). Thus, the quality
aspects reviewed here will cover predominantly
the effects on stability and healthiness.
Antioxidants
Many plants and phytochemicals, including EO
plants and EO, are known for their antioxidative
properties based mainly on phenolic compounds
in the oil or in other phytochemical fractions.
Some non-phenolic substances may show a
remarkable antioxidative potential. Such sub-
stances contribute to antioxidative benefits in
three respects. Firstly, they may protect feed
components from oxidative damage, substituting
partly the use of -tocopheryl acetate and related
compounds as feed additives or preservatives
respectively. They may also affect oxidative
metabolism in the animal: examples will be
given below. Finally, oxidative stability to a
large extent determines the shelf life of fat,
meat and eggs (Botsoglou et al., 1997; Govaris
et al., 2005), and many plant bioactive feed
additives have been shown to benefit storage
quality.
The dietary supply of thyme oil or thymol
to ageing rats showed a beneficial effect on the
antioxidative enzymes superoxide dismutase and
glutathione peroxidase as well as on polyunsatu-
rated fatty acid composition in various tissues
(Youdim and Deans, 1999). Animals receiving
these supplements had higher enzyme levels and
higher concentrations of polyunsaturated fatty
acids in phospholipids of the brain than the
untreated control (Youdim and Deans, 2000).
Oregano EO added in doses of 50
—
100 mg/kg
to the diet of chickens exerted an antioxidant
effect in the animal tissues (Botsoglou et al.,
2002). Such antioxidant effects would be
expected to improve the health of poultry
livestock as they do in other animals, including
man.
Storage quality is generally linked to the
oxidation of fats. Dietary thyme improved the
oxidative stability of eggs (Botsoglou et al., 1997;
Liu et al., 2009); although thymol is the EO
compound most associated with biological effects
in thyme, other components also appeared to be
involved (Botsoglou et al., 1997). Saffron (Crocus
sativus L.; Botsoglou et al., 2005), oregano
(Radwan et al., 2009), rosemary (Lopez-Bote
et al., 1998; Florou-Paneri et al., 2006; Radwan
et al., 2009), sage (Lopez-Bote et al., 1998),
turmeric (Curcuma longa; Radwan et al., 2009),
tea catechins (Yilmaz, 2006), mulberry leaf,
Japanese honeysuckle and goldthread (Liu et al.,
2009) had similar benefits to the oxidative
stability of eggs. The effects of rosemary were
not seen in another study (Galobart et al., 2001).
Also with rosemary and sage extracts, the
concentration of total cholesterol oxidation
products (COPS) was reduced, and a similar
trend was observed in microsomal fraction
isolates in which the rate of metmyoglobin/
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hydrogen peroxide-catalysed lipid peroxidation
was lower in birds receiving these plant extracts
in comparison with the control fed on basal diet
only (Lopez-Bote et al., 1998). Thus, many plants
can improve the oxidative stability aspect of
product quality, although the phytochemicals
responsible have not been identified.
Lipid metabolism
Fatty acid and cholesterol metabolism in the bird
is influenced by many plants and phytochemicals,
leading to improvements in the fatty acid
composition and particularly cholesterol content
of meat and eggs. Garlic is probably the best
characterised plant to lower the cholesterol
content of poultry meat (Konjufka et al., 1997;
Lim et al., 2006) and eggs (Chowdhury et al.,
2002; Mottaghitalab and Taraz, 2004; Yalcin et al.,
2006, 2007). Other plants and herbs have also
been reported to be beneficial in this respect,
including green tea (Uuganbayar et al., 2005) of
which Chinese green tea was best (Uuganbayar
et al., 2006), and mixed herbs (Poltowicz and
Wezyk, 2001). The mechanism whereby garlic
decreases cholesterol involves lower serum con-
centrations of cholesterol (Horton et al., 1991;
Chowdhury et al., 2002; Mottaghitalab and Taraz,
2004; Lim et al., 2006; Yalcin et al., 2006), which
then presumably limits the cholesterol available
to be taken up into muscle and eggs. The results
of Santoso et al. (2005) suggest that Sauropus
androgynus (Katuk) extract acts in a similar
manner to garlic. Broiler chicks fed on
Codonopsis lanceolata root (a plant used in
Korean cuisine) showed decreased serum levels
of triglyceride, total cholesterol and low density
lipoprotein cholesterol compared to the control
group, and decreased triglycerides and total
cholesterol levels in liver and breast muscle.
The effect appeared to be linked to biliary
cholesterol excretion being increased by 15%.
Whether this is a common mechanism of
product-cholesterol-lowering plants is not yet
clear. The pattern of fatty acids in the abdominal
fat of chicken was also altered by oregano oil
(Wald, 2002), and dietary carvacrol lowered
plasma triglycerides (Lee et al., 2003a).
Yolk colour is also a quality trait that is
influenced by plant additives. Green tea
decreased the yellowness of the yolk
(Uuganbayar et al., 2005), as did mixed herbs
(Poltowicz and Wezyk, 2001), while other dietary
ingredients/additives, including alfalfa concen-
trate, tomato powder and marigold extract
increased the colour intensity of yolk (Karadas
et al., 2006). These natural additives would be
preferred over some synthetic pigments that
have been fed to poultry for many years but
which are now less acceptable to consumers
(Karadas et al., 2006).
BIOACTIVE COMPOUNDS AND THE
GASTROINTESTINAL ENVIRONMENT
Normal flora
Most of the gut microbiological analysis of
poultry used in food production has been done
in the broiler chicken. The two main sites of
microbial activity are the crop and the caecum
(Smith, 1965), although microbe-host interac-
tions elsewhere in the digestive tract may have
important consequences for health (Lan et al.,
2005). Before the advent of molecular commu-
nity profiling techniques, cultivation-based analy-
sis indicated that the anterior part of the tract
(crop, gizzard, small intestine) was dominated by
facultative bacteria, principally Lactobacillus spp.,
while the caecum contained mainly strict anae-
robes (Fuller, 1984). Numbers were high, up to
10
11
per g of digesta. More recently, terminal
restriction fragment length polymorphism (T-
RFLP) analysis, also based on 16S gene sequence
analysis, indicated that the bacterial communities
at different parts of the gut were different, except
when comparing jejunum and duodenum (Torok
et al., 2008). Lu et al. (2003) confirmed this
difference when comparing 16S rRNA gene
libraries from the ileum and caecum. The
former contained nearly 70% Lactobacillus spp.,
while the latter had only 8% Lactobacillus and was
dominated by Clostridiaceae-related species. Fuller
(1984) estimated that there may be more than
200 species in the avian gut. Gong et al. (2002a)
and Zhu et al. (2002) found that many of the 16S
rRNA sequences from caecal clone libraries were
dissimilar to known bacteria. The library
sequences obtained by Zhu et al. contained 40%
related to Sporomusa or enteric bacteria related to
g-proteobacteria, such as E. coli, a result that was
not replicated in the other molecular studies.
Smaller numbers of bacteria colonise the small
intestine, yet they represent a surprisingly diverse
community (Knarreborg et al., 2002; van der
Wielen et al., 2002). A specific community
colonises the caecal mucosa, different from that
inhabiting the lumen (Gong et al., 2002b). All
sequence analysis studies report that there are
large numbers of unknown bacteria present
(Apajalahti et al., 2001; Gong et al., 2002a,b;Lu
et al., 2003; Apajalahti et al., 2004). While some
might assume that these bacteria might be
unculturable (e.g. Apajalahti et al., 2004), there
is no reason to suppose that they will be
functionally different to known gut species and
that they may eventually be cultured.
Both diet and age have a major influence on
the composition of the gut bacterial community.
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The first report of the effect of diet on the
community by molecular techniques was that of
Apajalahti et al., (2001), who used a G þC
profiling method to demonstrate that diet had
a major effect on gut composition. Even a
relatively minor change in diet
—
the supplemen-
tation of a barley diet with glycosidases
—
resulted
in 73% dissimilarity between bacterial commu-
nities in the ileum and 66% in the caecum (Torok
et al., 2008). The changes seemed to occur across
many species, with no individual bacterial species
contributing more than 1 to 5% of the total. Lu
et al. (2008) made the point that the broiler
should be thought of as a young animal whose
mature flora has not yet been achieved. The
caecal and ileal communities were similar up to
14 d, diverging thereafter.
Gut microbiota and productivity
How useful or harmful are the resident gut
bacteria to health and productivity? Some would
consider that the most telling observations about
the role of gut microorganisms in the health and
productivity of poultry are (i) that gnotobiotic
and caecectomised chicken and quail chicks grow
better than their conventional counterparts
(Fuller and Coates, 1983; Furuse and Yokota,
1984, 1985) and (ii) that antibiotics enhance
growth efficiency in broiler production (Graham
et al., 2007). Fuller (1984) concluded that,
although bacterial glycosidases digested polysac-
charides in the feed, there was no evidence of a
net benefit to productivity from this activity.
Indeed, he went so far as to say ‘‘In fact the net
effect of the flora is harmful’’. Vispo and Karasov
(1996), on the other hand, argue that the
retention in evolutionary terms of a caecum
must indicate that an advantage must be con-
ferred by the retention of the structure. Torok
et al. (2008) state ‘‘Gut microbiota positively
influence the host’s gastrointestinal develop-
ment, biochemistry, immunology, physiology,
and nonspecific resistance to infection’’, basing
this assertion on the review by Gordon and Pesti
(1971). The review covered mainly mammalian
species, however, with much less reference to
poultry. Nevertheless, Torok et al. (2008) mana-
ged, by sophisticated analysis of T-RFLP profiles,
to link differences in the gut community compo-
sition with improved performance (apparent
metabolisable energy), which has been a goal of
researchers for many decades.
There are several challenges that pathogens,
both acute and sub-acute, present to poultry
production. C. perfringens, an anaerobic Gram-
positive bacterium known to be a common
pathogen in humans, domestic animals and in
wildlife, is the primary cause of clostridial enteric
disease in poultry production. C. perfringens
associated necrotic enteritis and subclinical dis-
eases are serious threats to poultry health,
causing a spectrum of effects including subclini-
cal infection, mild disease with focal intestinal
necrosis, diarrhoeal illness and liver disease, as
well as the classic form of acute fulminant
necrotising enteritis (Wilson et al., 2005).
Necrotic enteritis is estimated to affect up to
40% of the commercial broiler flocks in the
United States and it is believed to cost the US
poultry industry about 5 USD cents per broiler
(McDevitt et al., 2006). Fuller et al. (1979) found
that the poorer growth of conventional vs. germ-
free birds was due, in part, to Streptococcus
faecium. The mechanism appeared to involve
adhesion to the duodenum (Fuller et al., 1981)
and the deconjugation of bile salts, leading to
malabsorption of lipids (Cole et al., 1981). The
other major intestinal disease suffered by poultry
is coccidiosis, caused mainly by Eimeria spp.
(Kennedy, 2001). The disease is passed from bird
to bird via droppings, which means that the
problem is greatest in intensive units unless
measures are taken to control oocyte numbers.
Immunity
The nutrient content of the diet has a major
effect on immunity in poultry (Kidd, 2004),
without reference to plant bioactives, but there
is nonetheless growing published evidence for
benefits to be obtained by incorporating plants
rich in certain phytochemicals being beneficial
for immune function in poultry (Swiatkiewicz
and Koreleski, 2007). Chinese herbs in particular
seem to be cited as positive for immune effects,
though other plants and extracts have been
reported to be positive. We have not been able
to find a systematic account of the precise
phytochemicals that might be beneficial, so
what follows is inevitably rather disjointed:
there does not appear to be a hypothesis linking
the different plants. Immune function would be
enhanced as a consequence of a more stable
intestinal health favoured by feed additives, or by
animals being less exposed to microbial toxins or
other undesired metabolites, for example ammo-
nia and biogenic amines. Consequently, additives
like aromatic herbs or volatile oils may relieve the
animals from immune defence stress during
critical situations, raising the intestinal availabil-
ity of essential nutrients for absorption and thus,
assist the animal to grow better within its genetic
potential.
Sometimes extracts of plants, not well
characterised, have beneficial effect. Ethanol
extracts of Allium sativum (garlic), Glycyrrhiza
glabra (licorice), Plantago major (plantain) and
Hippophae rhamnoides (sea buckthorn) all had
some beneficial immunological effects on cellular
470 R.J. WALLACE ET AL.
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immunity in laying hens (Dorhoi et al., 2006).
Polysavone, an extract of alfalfa, enhanced
immunity in broilers (Dong et al., 2007). The
phagocytic activity of peripheral blood leucocytes
in chickens orally administered sugar cane
extracts or a polyphenol-rich fraction of the
sugar cane extract (500 mg/kg/day) for 3 con-
secutive days increased significantly, when com-
pared with that of saline-administered control
chickens (Hikosaka et al., 2007). Achyranthan,
a low-molecular-weight Chinese herbal polysac-
charide, showed immunostimulating effects in
both growth assays and in vitro studies (Chen
et al., 2003).
Ligustrum lucidum and Schisandra chinensis
improved antioxidative metabolism and immu-
nity of laying strain male chicks (Ma et al., 2007).
Aniseed (Pimpinella anisum) used at up to 4%
inclusion in laying quail diets provided beneficial
effects on immune responses, although 5%
caused negative effects on feed intake and feed
conversion ratio (Bayram et al., 2007). Similar
effects were found in broiler chicks (Durrani
et al., 2007).
Coccidiosis
Coccidiosis is the most important disease in
poultry production (Cox, 1998) causing annual
costs of more than $3 billion to the worldwide
industry as estimated by Dalloul and Lillehoj
(2006). Mortality, malabsorption of nutrients,
impaired growth rates and rapid and effective
transmission between animals are characteristic
of the disease, which is caused by several species
of Eimeria. Secondary bacterial infections are
frequently observed and may further increase the
severity of the disease. In-feed medication by
anticoccidial drugs has provided good protection
of flocks for decades. Emerging problems with
parasite resistances and concerns about drug
residues however have stimulated the search for
alternatives. Concomitantly with the ban of
antibiotic growth promoters in animal produc-
tion, the European Union (EU) has put to
question the use of coccidiostats from the year
2012 onwards. The decision will have high impact
on poultry production within the EU and is
expected to influence also other regions.
Coccidiosis vaccines are mostly used for
breeder and layer chickens, but hardly at all for
broilers (EC, 2008), which is the most numerous
type of chicken. Six Eimeria species are consid-
ered economically relevant (Holdsworth et al.,
2004), but immunity is highly species-specific and
not all species and relevant strains are included
in most commercial vaccines. To overcome these
limitations, a lot of effort is put into new
strategies for vaccine development (Dalloul and
Lillehoj, 2006; Shirley et al., 2007).
A summary of reported anticoccidial effects
of plants and plant extracts in poultry is given
in Table 2.
Prooxidants
Allen and Fetterer (2002) provided a compre-
hensive review on various feed ingredients and
their influence on coccidiosis. Flaxseed, flaxseed
oil and corn oil, which contain high amounts of
polyunsaturated fatty acids (PUFA), reduced
lesions caused by the chicken parasite Eimeria
tenella, but not lesions caused by Eimeria maxima
(Allen and Fetterer, 2002; Yang et al., 2006).
Artemisinin, a naturally occurring antimalarial
compound, significantly lowered lesions (Allen
and Fetterer 2002) and reduced oocyst output
(Arab et al., 2006) from E. tenella when given at
low levels as a feed additive. The mechanisms of
action of PUFA as well as artemisinin are
assumed to involve induction of oxidative stress
to the parasites. However, there might be
practical difficulties in including sufficient
amounts of PUFA for protection in the diets,
also due to antioxidative ingredients which are
usually included in feed, as studies by Allen et al.
(2000) have shown. Furthermore, this mode of
action seems to be effective against E. tenella,
which is adapted to the specifically anaerobic
conditions of the caeca, but not so much against
other Eimeria species.
Antioxidants
Diets supplemented with g-tocopherol, with the
spice turmeric or curcumin, which all possess
antioxidative properties, reduced small intestinal
lesion scores and improved weight gains during
E. acervulina and E. maxima infections (Allen and
Fetterer, 2002). Antioxidative activity is also
suggested as the mode of action of various
South African plant species investigated by
Naidoo et al. (2008). Tulbaghia violacea showed
improved FCR and lowered oocyst output during
a mixed Eimeria challenge. Green tea reduced
oocyst shedding after an E. maxima infection, but
no beneficial effects on weight gain were
detected (Jang et al., 2007). Wang et al. (2008)
reported beneficial effects of grape seed
proanthocyanidins by counteracting weight loss,
mortality and lesion scores and lowering oxida-
tive stress in intestinal tissues. All these com-
pounds may exert their anticoccidial activity
by protecting infected tissues from oxidative
damage and therefore reducing the severity of
coccidiosis. Similar to compounds causing oxida-
tive stress, the effect of antioxidants seems to
be restricted to certain Eimeria species only,
especially E. acervulina and E. maxima (Allen and
Fetterer, 2002).
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Essential oils
Amelioration of coccidiosis was observed when
supplementing commercial feed additives con-
taining oregano EO (Giannenas et al., 2003;
Batungbacal et al., 2007) or ground aerial parts
of oregano (Giannenas et al., 2004). Both
applications protected significantly from weight
loss or improved feed efficiency and reduced
oocyst output and lesion scores in a coccidiosis
challenge. Improvement of the negative
impact of coccidiosis was also reported for
supplementation with Olympus tea (Sideritis
Table 2. Plants and plant extracts with anticoccidial activity
Plant species/extract Scientific name Activity/Mode of action Literature
Flaxseed meal, flaxseed oil,
n-3 fatty acids
Linum usitatissimum E. tenella (not E. maxima) lesions,
parasitation, development.
Induction of oxidative stress
Allen et al. (1998, 2000), Allen and
Fetterer (2002)
Corn oil Zea mays E. tenella body weight, higher IgA,
lower plasma carotenoids,
Yang et al. (2006)
Artemisia annua dried herb,
Artemisinin, 1,8-Cineol,
Camphor, A. sieberi pet-
roleum ether extract of
aerial parts, A. afra
acetone/water extract
from aerial parts
Artemisia annua,
A. sieberi. A. afra
E. tenella lesions, oocyst output,
E. acervulina oocyst output.
(not E. maxima) Induction of
oxidative stress. Eimeria mix
(Eten, Emax, Eace): FCR. 1,
8-cineol and camphor: weight
gain, lesions
Allen et al. (1997,1998), Allen and
Fetterer (2002), Arab et al.
(2006), Naidoo et al. (2008)
Sophora flavescens root
decoction
Sophora flavescens E. tenella weight gain, mortality,
bloody diarrhoea,
Allen and Fetterer (2002), Youn
and Noh (2001)
Turmeric spice rhizome,
Curcumin
Curcuma longa E. maxima lesions, weight gain.
E. acervulina (not E. tenella)
Antioxidative
Allen et al. (1998), Allen and
Fetterer (2002)
g-Tocopherol e.g. from Linum usi-
tatissimum, var-
ious seed oils
E. maxima lesions, weight gain.
E. acervulina (not E. tenella).
Antioxidative
Allen et al. (2000), Allen and
Fetterer (2002)
Betaine e.g. from sugar beet
(Beta vulgaris ssp.
vulgaris var.
altissima)
E. acervulina (and E. tenella, but
less effective) invasion and
development when used in
combination with salinomycin.
E. maxima weight gain (not
E. tenella,E. acervulina)
Allen et al. (2000), Allen and
Fetterer (2002), Fetterer et al.
(2003), Klasing et al. (2002),
Waldenstedt et al. (1999)
Oregano aerial parts and
essential oil (containing
carvacrol and thymol)
Origanum vulgare L.
ssp. hirtum
Orego-Stim (Meriden): Eimeria
mix (8 species, unknown ratio)
lesions, oocyst output, feed
efficiency. E. tenella weight
gain, FCR, lesions, OPG (exact
inclusion rate unclear!)
Batungbacal et al. (2007),
Giannenis et al. (2003, 2004)
China bark tree extract,
Quinine
Cinchona succirubra E. tenella,E. meleagrimitis Sz
invasion in vitro
Christaki et al. (2004), Fayer
(1971)
Olympus tea Sideritis scardica E. tenella weight gain, diarrhoea,
mortality, lesions, oocysts
output
Florou-Paneri et al. (2004)
Grape seed proanthocyani-
din extract, ethanol/
water extract from
pomace
Vitis vinifera E. tenella weight gain, mortality,
lesion scores. Eimeria mix
(Eten, Emax, Eace): FCR
Naidoo et al. (2008), Wang et al.
(2008)
Sugar cane extract Saccharum offici-
narum L.
E. tenella: body weight gain, oocyst
output, lesions, antibody
response. Small group sizes, no
specification of extract.
El-Abasy et al. (2003)
Wild garlic acetone/water
extract from whole
plant
Tulbaghia violacea Eimeria mix (Eten, Emax, Eace):
FCR, OPG. Marasmine ¼S-
(methylthiomethyl)cysteine
sulfoxide), bis[(methylthio)-
methyl] disulfide, and
derivatives
Naidoo et al. (2008)
Green tea leaves Camellia sinensis E. maxima oocyst output Jang et al. (2007)
Oriental plum, Japanese
plum
Prunus salicina E. acervulina body weight gain,
OPG, IFN-g and IL-15
(mRNAs) of IEL, spleen cell
proliferation. Phenolics,
antioxidants,
Lee et al. (2008)
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scardica; Florou-Paneri et al., 2004). The EO
constituents 1,8-cineole and camphor, from
Artemisia annua protected weight gain and
reduced E. tenella as well as E. acervulina lesions
(Allen and Fetterer, 2002).
Various other plants/products
Youn and Noh (2001) tested 15 therapeutic
plants against an E. tenella challenge and found
a root decoction of Sophora flavescens to be most
active in protecting weight gain and reducing
mortality and bloody diarrhoea. Moreover, a
sugar cane extract had protective effects when
inoculated in the crop of chicken simultaneously
with a challenge. Body weight gain, haemor-
rhages, oocyst output, lesion scores and antibody
response were improved (El-Abasy et al., 2003).
Betaine, an osmoprotectant ubiquitous among
plants, enhanced the activity of anticoccidial
drugs in some cases (Allen and Fetterer 2002;
Fetterer et al., 2003), but failed to do so in others
(Waldenstedt et al., 1999). Apparently, its effect
is restricted to certain Eimeria species only.
Immunomodulation
Immunomodulatory effects are assumed to be
responsible for protection by plum powder
(Prunus salicina) against an E. acervulina chal-
lenge (Lee et al., 2008). Body weight gain, oocyst
shedding, IFN-gand IL-15 levels were signifi-
cantly improved. Furthermore, Guo et al.
(2004a,b) found enhanced cellular and humoral
immune responses of E. tenella-infected chickens
when supplementing a polysaccharide extract
from Astragalus membranaceus, which may
become particularly interesting when used in
conjunction with vaccination.
Future perspectives
In summary, plants and products derived thereof
have clearly shown the potential to alleviate
coccidiosis and reduce its severity in several
studies. Moreover they might play a role in
counteracting subclinical infections and second-
ary bacterial infections associated with the
disease. Most of the active plant materials could
improve some, but not all of the relevant
parameters in coccidiosis and variable effective-
ness against the different Eimeria species was
observed in some cases. To date, no alternative to
anticoccidial drugs is yet known with comparable
efficacy and economy of use in broiler produc-
tion, and a recently published EC report strongly
recommends to maintain the actual status of
so-called ‘‘coccidiostatic drugs’’ as feed additives
within the EU (EC, 2008). Nevertheless, plant
products may have increasing significance in
organic farming, whenever antibiotic-free rearing
of animals is desired, as supporting agent for
vaccination (adjuvants), or in combination with
conventional anticoccidial drugs, especially in the
light of possible bans or reduction of approved
drugs in large economies like the EU. This should
be a great incentive for stimulating research in
the field of alternatives to conventional antic-
occidial drugs in general and especially on the
role of plants and plant products.
Difficulties in comparing research data arise
from the use of different experimental models
and different strains of Eimeria. Parasite strains
are known to possess variable virulence and may
cause variable severity of challenge in different
experiments. An important effort to harmonise
techniques in coccidiosis research and models for
evaluation of drug efficacy against coccidiosis
was taken in the course of the COST 89/820
programme and by Holdsworth et al. (2004).
Guidelines for efficacy testing are also published
by regulative authorities, e.g. the recently pub-
lished EFSA ‘‘guidance for the preparation of
dossiers for coccidiostats and histomonostats’’
(EFSA, 2008). Such guidelines should also be
taken into consideration when alternatives to
anticoccidial drugs are investigated in order
to provide sound and comparable scientific
results.
Necrotic enteritis
Necrotic enteritis (NE) is a disease in poultry
causing high economic costs and seriously
impairs animal welfare. Due to the ban on sub-
therapeutic antibiotic usage, NE has become
increasingly prevalent in the EU. Demands for
safer food have put pressure on the development
of alternative management or dietary strategies
to control this disease. C. perfringens, a Gram-
positive, anaerobic, spore-forming toxigenic bac-
terium is found in soil, dust, faeces, feed and
poultry litter and has been identified as the main
causative agent causing NE in poultry (Branton
et al., 1997; Annett et al., 2002; Dahiya et al., 2006;
McDevitt et al., 2006). C. perfringens is principally
a normal inhabitant of the chicken intestine but
under certain circumstances it can begin to
proliferate rapidly, accompanied by increased
toxin production causing the intestinal mucosal
necrosis characteristic of NE (Branton et al.,
1997; Collier et al., 2003; Dahiya et al., 2005,
2006). However, even high doses of C. perfringens
in the intestinal tract of broiler chickens do not
always lead to the development of NE, as the gut
flora of healthy birds can apparently prevent
its pathogenicity (Fukata et al., 1991). Various
predisposing factors, among them dietary com-
position and incidence of coccidiosis (Williams,
2005), may lead to over-proliferation of
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C. perfringens, and the subsequent progression to
disease is still poorly understood. Host specific
virulence factors like production of -toxin are
assumed to play a role, and recent findings point
towards the importance of the netB gene,
necessary for the production of the respective
toxin (NetB) (Keyburn et al., 2006; Chalmers
et al., 2008; Timbermont et al., 2008). However,
control of C. perfringens seems to be essential and
dietary ingredients have a great influence on the
incidence of NE in broiler chickens.
Reports of the effects of plants and their
extracts on mainly avian C. perfringens are
summarised in Table 3. Dahiya et al. (2006)
reviewed the potential of plant-derived feed
ingredients to control C. perfringens and NE.
Numerous plants and plant products have been
found to possess inherent antimicrobial activity
against clostridia, although mostly their effects
were only determined in vitro. Oregano, black
pepper, cloves and the EO components carvacrol
and eugenol possess antibacterial activity against
clostridia as well as E. coli,Staphylococcus aureus
and Salmonella pullorum. Furthermore, lemon
myrtle (Wilkinson et al., 2003), Artemisia princeps
var. orientalis (Cho et al., 2003), Hypericum
scabrum (Sokmen et al., 1999) and Aristolochia
paucinervis (Gadhi et al., 1999) displayed
in vitro activity against C. perfringens and other
bacteria.
Reports on in vivo investigations are scarce:
according to Dahiya et al. (2006), supplementa-
tion of flaxseed may have benefits by modifica-
tion of intestinal microbial colonisation.
Linolenic acid, the main constituent of flaxseed
fatty acids, may prevent the adhesion of bacteria
to intestinal epithelial cells and mucus, whereas
addition of pectin and guar gum to diets has
reportedly eliminated NE from sick birds.
Specific blends of EO components like thymol,
carvacrol and eugenol (Mitsch et al., 2004) as
well as astaxanthin from the microalgae,
Haematococcus pluvalis, were found to be effective
in controlling C. perfringens colonisation and
proliferation in the gut of broilers (Waldenstedt
et al., 2003). Finally, lupulone from hops, when
administered in drinking water, inhibited
proliferation of artificially inoculated C. perfrin-
gens in the chicken gastrointestinal tract (Siragusa
et al., 2008).
Escherichia coli
Escherichia coli is the most common bacterial
pathogen of poultry and responsible for signifi-
cant losses in the world’s industry. Although our
understanding of pathogenicity has increased in
the past years, the virulence factors (genes) which
lead to disease remain to be fully unravelled (La
Ragione and Woodward 2002). For practical
reasons, E. coli isolated from diseased chicken
are termed avian pathogenic E. coli (APEC).
Colisepticaemia or colibacillosis manifests itself
most commonly as an infection of the respiratory
tract, in rare cases also as enteritis. E. coli are
common inhabitants of poultry intestinal micro-
biota, thus the gastrointestinal tract is seen
as a possible reservoir for infection (Ewers
et al., 2009) and incidence of the disease might
be reduced by keeping intestinal E. coli
numbers low.
Reports of the effects of plants and their
extracts on APEC are summarised in Table 3.
There are numerous studies on in vitro effective-
ness of plant-derived extracts and compounds, as
well as EO against (avian) E. coli (Smith-Palmer
et al., 1998; Penalver et al., 2005b,c,d; Fisher and
Phillips 2006; Horosova et al., 2006; Prakash,
2006; Geidam et al., 2007). EO containing a high
percentage of phenolic components (e.g.
carvacrol and thymol) show higher inhibitory
capacity compared to the oils containing, for
example, the monoterpenic alcohol linalool
(Penalver et al., 2005a). However, literature
supporting actual in vivo activity is scarce. An
alternative strategy to suppress intestinal E. coli
might involve preventing their adhesion to the
intestinal mucosa. This may be achieved by
feeding compounds which increase mucus pro-
duction, thus reducing the possibility of bacterial
adhesion to the intestinal epithelium. A mixture
of cavracrol, cinnamaldehyde and capsaicin
caused the release of large amounts of mucus
on glandular stomach and wall of jejunum in
chickens when incorporated into their diets
(Jamroz et al., 2006). Becker and Galletti (2008)
exploited the ability of E. coli to adhere to
mannose receptors and mannose-containing
analogues to find food and feed components
with gut health-promoting effects. Out of 18
dietary components tested, artichoke and sesame
seed extracts performed well in binding
various E. coli strains. Sesame seed extract was
also most effective in binding chicken Salmonella
isolates.
Antiviral effects
Although a vast range of plants possess antiviral
activity (Jassim and Naji, 2003), they are probably
underexplored and underutilised for this pur-
pose in poultry farming. Actually, the most
important viral diseases are sought to be con-
trolled by vaccination. A polyphenolic extract
from Geranium sanguineum aerial roots and an
extract of the red marine alga Ceramium rubrum
showed excellent in vitro inhibition of human
and chicken influenza A viruses (Serkedjieva
and Hay, 1998). The very scarce animal trials
comprise sulfated Astragalus polysaccharides
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(Huang et al., 2008), Ocimum sanctum and leaf galls
of Ficus racemosa (Kolte et al., 1999), which showed
effects against infectious bursal disease (IBD) and
Aloe secundiflora, which reduced mortality and
severity of clinical signs during a Newcastle
Disease infection (Waihenya et al., 2002b).
Zoonotic infection
Of major concern to consumers are the hazards
presented by zoonotic infection from contami-
nated poultry meat. Campylobacter spp. is the
greatest hazard in terms of numbers of infections
and days lost through illness (Friedman et al.,
Table 3. Plants with activity against Escherichia coli and Clostridium perfringens
Plant species/extract Scientific name Activity/Mode of action Literature
Flaxseed, linolenic acid Linum usitatissimum Prevents adhesion of pathogenic bacteria Dahiya et al. (2006)
Guar gum, pectin Cyamopsis
tetragonolobus
Unknown Dahiya et al. (2006)
Thymol, carvacrol and
eugenol
Inhibit C. perfringens colonisation and
proliferation
Dahiya et al. (2006), Mitsch
et al. (2004)
Turmeric, EO from
rhizome
Curcuma longa Inhibits C. perfringens Dahiya et al. (2006)
Eugenol, EO from clove Syzygium aromaticum Inhibits C. perfringens Dahiya et al. (2006)
Astaxanthin, from red
algae
Haematococcus
pluvalis
Inhibits C. perfringens caecal
colonisation
Waldenstedt et al. (2003)
Lupulone, from hops Humulus lupulus Inhibits intestinal C. perfringens Siragusa et al. (2008)
Lemon myrtle, leaf paste Backhousia citriodora Inhibits C. perfringens (in vitro) Wilkinson et al. (2003)
Japanese mugwort, seco-
tanapartholides
Artemisia princeps
var. orientalis
Inhibits C. perfringens (in vitro) Cho et al. (2003)
Hypericum, acetone
extract from aerial parts
Hypericum scabrum Inhibits C. perfringens (in vitro) Sokmen et al. (1999)
Aristolochia paucinervis,
defatted chloroform
extract of rhizome
Aristolochia
paucinervis
Inhibits C. perfringens (in vitro) Gadhi et al. (1999)
Oregano, EO Origanum vulgare Bactericidial effect Horosova et al. (2006)
Agave, extract Agave picta Inhibits C. perfringens (in vitro) Verastegui et al. (1996)
Paper daisy, petroleum
ether and ethanol
extracts of flowers
Helichrysum sp. Growth inhibition of various Helicobacter
species
Aslan et al. (2007)
Plant extract þ5% carva-
crol, 3% cinnamalde-
hyde, 2% capsicum
oleoresin
Origanum vulgare,
Cinnamomum
cassia, Capsicum
annum
Prevents adhesion of of E. coli Jamroz et al. (2006)
Lemon, EO Citrus limon Growth inhibition by the disc diffusion
method
Fisher and Phillips (2006)
Sweet orange, EO Citrus sinensis Growth inhibition by the disc diffusion
method
Fisher and Phillips (2006)
Bergamont, EO Citrus bergamia Growth inhibition by the disc diffusion
method
Fisher and Phillips (2006)
Shiitake, extract Lentinus edodes Increases the number of desirable bac-
teria in order to inhibit colonisation
of invading pathogens
Guo et al. (2004c)
White jelly, herb polysac-
charide extract
Tremella fuciformes Increases the number of desirable bac-
teria in order to inhibit colonisation
of invading pathogens
Guo et al. (2004c)
Huang Qi, herb polysac-
charide extract
Astragalus
membranacea
Increases the number of desirable bac-
teria in order to inhibit colonisation
of invading pathogens
Guo et al. (2004c)
Spanish origanum, EO Coridothymus
capitatus
Antimicrobial activity Penalver et al. (2005)
Thyme, EO Thymus mastichinia Antimicrobial activity Penalver et al. (2005)
Geranium, EO from steam
distillation
Pelargonium sp. Partly greater efficacy against E.coli than
commercial thyme oil
Penalver et al. (2005)
Guava, aqueous extract Psidium guajava Prevents adhesion of of E. coli Geidam et al. (2005)
Artichoke Cynara cardunculus
var scolymus
Adhesion of E.coli (in vitro) Becker and Galletti (2008)
Sesame seed extract Sesamum indicum Adhesion of E.coli (in vitro) Becker and Galletti (2008)
Palm kernel, extract Aracaceae elais Adhesion of E.coli (in vitro) Becker and Galletti (2008)
Tomato Solanum lycopersicum Adhesion of E.coli (in vitro) Becker and Galletti (2008)
Betel pepper, aqueous
extract
Piper betel Inhibition zone in agar gel plates Prakash (2006)
Senna, aqueous extract Cassia auriculata Inhibition zone in agar gel plates Prakash (2006)
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2000). However, the infection is usually short-
term and self-limiting. Campylobacter jejuni readily
colonise the gastrointestinal tract (GIT) of
poultry, without causing any disease in the host
birds. The principal site of colonisation is the
lower GIT, especially the caeca, large intestine
and cloacae (Beery et al., 1988; Stern et al., 1988).
Campylobacters do not adhere to the intestinal
surface but are highly motile and rapidly track
along intestinal mucus, preferentially within
caecal and cloacal crypts (Beery et al., 1988).
Commercial broiler flocks rarely start shedding
Campylobacter before 2 weeks of age however,
when shedding occurs, Campylobacter is spread
rapidly throughout the flock (Corry and Atabay,
2001; Mead, 2002; Newell and Fearnly, 2003).
Until now, the main approaches evaluated for
handling the Campylobacter problem in practice
include hygienic barriers, diagnostics at the flock
level, competitive exclusion, decontamination
and intervention efforts targeting the lower GIT
(Hariharan et al., 2004). Despite major efforts,
however, there are currently no really successful
strategies for reduction or elimination of C. jejuni
from the food chain. Salmonella infections in man
that result from the consumption of poultry
products are less numerous, but much more
severe. Human infection by two common sero-
vars, S. enteritidis and S. typhimurium usually occurs
via food-borne transmission. Consumption of raw
or undercooked contaminated eggs usually causes
S. enteritidis infection, while S. typhimurium is
transmitted by contaminated chicken meat (Babu
and Raybourne, 2008). Dietary interventions,
including fatty acid modifications, probiotic or
prebiotic treatment have been investigated (Babu
and Raybourne, 2008), but our understanding of
conditions that lead to the proliferation of these
zoonotic bacteria is patchy (Mead, 2004).
Antibiotic growth promoters, now banned
in Europe but still permitted elsewhere, are so
effective that their withdrawal has caused major
difficulties in poultry production (Casewell et al.,
2003). But how do they achieve that growth
promotion? Is it due to the suppression of major
pathogens like C. perfringens? Or sub-pathogenic
species like S. faecium? Or is it due simply to a
decreased bacterial load (Windisch et al., 2008),
or perhaps due to the anti-inflammatory effects
of AGP via the inhibition of production and
excretion of catabolic mediators by intestinal
inflammatory cells (Niewold, 2007)? Finding the
answer to these questions is vital, because with-
out that knowledge it will be difficult to select
phytochemical replacements for AGP. Molecular
ecological analysis described changes in the
microbiota in response to bacitracin-virginiamy-
cin (Lu et al., 2008), but other than a decreased
community diversity in birds receiving the GPA,
it was difficult to explain why production benefits
should occur. Indeed, the decreased numbers of
Lactobacillus contradicted the usual perception of
these being beneficial bacteria, the basis of their
use as probiotics (Fuller, 1989).
SPECIFIC PLANT BIOACTIVES
Acamovic and Brooker (2005) estimated that
plants produced around 5100 different second-
ary compounds (Figure). One of the most
common problems of research performed using
plant extracts in poultry nutrition has been the
poor characterisation of the plant material or
extracts and their standardisation. In many cases,
the identity or concentration of active principle
has been generally unknown. Due to the possible
variation in plant material under different
environmental conditions, harvest time, drying
and storage conditions, repetition of the experi-
ments is generally impossible to identify them.
This is probably why different results are
obtained in independent experiments even
when using the same plant species. Thus, the
development of analytical methods and the
proper standardisation of the material used for
feeding is crucial if the benefit of the knowledge
is to be maximised. Moreover, feeding experi-
ments have often been performed using negative
controls only. To be able to compare data from
different experiments, the commonly accepted
GPA might be recommended as a positive
control. The effects of some of the most
common categories of plant bioactives and their
physiological mode of action are described in
following sections.
Essential oils
EO are steam-volatile or pressed-volatile (e.g.
citrus extracts) extracts of plants, used tradition-
ally by man for many centuries for the pleasant
odour of their essence, their flavour, or their
antiseptic and/or preservative properties.
Although commonly thought of as being derived
from herbs and spices, they are present to some
degree in many plants for their protective role
against bacterial, fungal or insect attack. They
comprise mainly cyclic hydrocarbons (monoter-
penes) and their alcohol, aldehyde or ester
derivatives (Figure). EO appear as feed additives
in the form of the EOs themselves, or as EO-rich
plants, or as pure compounds, sometimes syn-
thetic or ‘‘nature-identical’’.
The number of papers published on the use
of EO and especially those containing the
phenolic compounds carvacrol and thymol has
increased dramatically over the last few years.
The majority report, however, on production
parameters (feed uptake, feed conversion, weight
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gain) only. Comparatively little information is
given on their mode of action, metabolism or
generally on science based functionality due to
the fact that many reports deal with results of
commercial products, avoiding statements on
pharmacological effects or health claims.
EO used as feed additives for broilers
were shown to enhance activities of trypsin, of
amylase in tissue homogenates of pancreas, as
well as the jejunal chyme content (Lee et al.,
2003b; Jang et al., 2004). A mixture of carvacrol,
cinnamaldehyde and capsaicin also stimulated
the intestinal secretion of mucus. Jamroz et al.
(2006) stated that the increased release of large
amounts of mucus and the creation of a thick
layer of mucus on glandular stomach and
jejunum wall in chicks fed with the above mixture
could be responsible for the reduced adherence
of pathogens (E. coli,C. perfringens and others) to
the gut epithelium. This confirms
—
as already
known from human nutrition physiology
(Teuscher, 2003) and phytopharmacology
(Ha
¨nsel and Sticher, 2004)
—
the mode of action
of spices and EO on gut function, namely that it
involves at least partly an irritation of the
exposed tissues and leading to higher secretion
of mucus and enzymes.
In general, antimicrobial activity of EO and
EO compounds, whether bacteriostatic or bacter-
icidal, or against other microorganisms like
fungi, protozoa or food-borne pathogens, is
well documented (Smith-Palmer et al., 1998,
Dorman and Deans, 2000; Chao et al., 2000;
Burt, 2004; Si et al., 2006). Most active in this
respect are the phenolic compounds carvacrol,
thymol and eugenol but also other substances,
including phenylpropane, limonene, geraniol or
citronellal, may be involved (Deans and Ritchie,
1987; Pauli, 1994).
The action of EO compounds as antimicro-
bials occurs via at least two separate mechanisms.
The first is by rapidly depleting the intracellular
ATP pool, through inhibiting ATP synthesis as
a result of their effects on the transmembrane
electrical potential. The leakage of ions such as
potassium and phosphate out of the cell indicates
clearly the membrane damage resulting in
disturbances of the osmotic pressure of the cells
(Ultee et al., 1999; Lambert et al., 2001;
Veldhuizen et al. 2006). Furthermore, changes
in the fatty acid composition of bacterial cell
membranes have been observed at sublethal
doses of several EO compounds (Di Pasqua
et al., 2006). A second growth-inhibitory mechan-
ism is that substances like carvacrol prevent the
synthesis of flagellin, causing bacterial/cells to be
aflagellate and therefore nonmotile. Such cells
are significantly less able to adhere to epithelial
cells, which renders bacteria non-infective (Burt
et al., 2007), a mechanism similar to that known
from acid galacturonides in the diet
(Guggenbichler et al., 2004). The anti-flagellate
activity of EOs obtained from fresh leaves of
Cinnamomum aromaticum,Citrus limon pericarps
and Allium sativum bulbs was investigated in vitro
on Tetratrichomonas gallinarum and Histomonas
meleagridis with positive results (Zenner et al.,
2003).
As EOs comprise a large number of compo-
nents, it is likely that their mode of action
involves several targets in the bacterial cell.
The hydrophobicity of EOs enables them to
partition in the lipids of the cell membrane and
mitochondria, rendering them permeable and
leading to leakage of cell contents. Physical
conditions that improve the action of EOs
include low pH, low temperature and low
oxygen levels. Synergism has been observed
between carvacrol and its precursor p-cymene
and between cinnamaldehyde and eugenol (Burt,
2004). Thus, extrapolating from the effects of
single EO compounds to the effects of mixtures
must be done with caution.
In vitro antimicrobial activities have been
measured with a number of EOs and single
compounds mainly against enteropathogenic
strains of E. coli,Salmonella sp., Cl. perfringens
and others. Using either the broth microdilution
method or the agar diffusion test, EOs with a
higher percentage of phenolic compounds
showed the best inhibitory capacity in terms of
MIC (minimum inhibitory concentration; Jugl-
Chizzola et al., 2005; Penalver et al., 2005; Ben
Arfa et al., 2006). The combination of oregano
EO with fluoroquinolones, doxycycline, lincomy-
cin, and maquindox florfenicol to treat infections
caused by ESBL-producing E. coli were reported
to lower, to a great extent, the effective dose
of these antibiotics and thus minimise the side
effects of antibiotics (Si et al., 2008). Differences
have been observed, however, in the activities of
plant species and plant parts on one side and the
sensitivity of species and strains of the micro-
organisms on the other. This is due to the varying
chemical composition of the used plant material
(chemotype, morpho- and ontogenetic variation),
a factor quite often neglected in microbiological
or animal studies. The in vitro active concentra-
tions exceeded furthermore in general the diet-
ary doses accepted by the animals, which results
in few studies being available so far demonstrat-
ing the efficacy of EO compounds against
specific pathogens in vivo.
Some studies with poultry showed a clear
reduction of C. perfringens in the jejunum and
caecum of broilers fed with a mixture of EO
components (Losa and Koehler, 2001; Mitsch
et al., 2004). The same blend of components as
well as oregano oil or crude drug was effective
against Eimeria ssp. infections in broilers, thus
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reducing the application of coccidiostats
(Giannenas et al., 2003, 2004; Oviedo-Rondon
et al., 2005, 2006). The components of Artemisia
annua, camphor and 1,8-cineole, at 119 mg/kg,
also protected weight gains, and reduced E.
tenella lesion scores. Camphor decreased E.
acervulina lesions (Allen et al., 1997, 1998).
Carvacrol, cinnamaldehyde, oregano oil and
thymol also inhibit C. perfringens spore germina-
tion and outgrowth in ground turkey during
chilling. Cinnamaldehyde was significantly more
effective than the other compounds at a lower
concentration (0.5%) at the most abusive chilling
rate evaluated (Juneja and Friedman, 2007). A
study to test the efficiency of carvacrol, thymol,
trans-cinnamaldehyde and tetrasodium pyropho-
sphate on the radiosensitisation of E. coli and
Salmonella typhi in chicken breast demonstrated
that these active compounds helped reduce
significantly the numbers of E. coli and S. typhi
(Lacroix et al., 2004). A combined administration
of Lactobacillus fermentum and EOs of Origanum
vulgare and Thymus vulgaris decreased the per-
centage of crop, caecum, liver and spleen
colonisation by Salmonella enterica var. dusseldorf
in chicks when compared to the control group
without any treatment (Koscova et al., 2006). In a
study to test the effects of the antibiotic
avilamycin and anise oil supplementation on
broilers’ body weight, including carcass charac-
teristics and organoleptic analysis of meat, it was
concluded that anise oil, at a dose of 400 mg/kg,
can be used as an alternative to antibiotics for
growth promotion in broiler diets (Simsek
et al., 2007).
It is sometimes assumed or implied that
effects of the inclusion of aromatic herbs in the
diet will be caused by the terpenes that comprise
their EO. Cross et al. (2007) demonstrated
that this need not always be true: thyme
and yarrow had different effects on broiler
performance to their corresponding EO.
With oregano, marjoram and rosemary, the
effects were similar.
Two further antimicrobial benefits can the-
oretically be achieved by adding EO to animal
feed: the reduction of feed microbial load and
the improvement of the microbial hygiene of the
carcase (Aksit et al., 2006). The number of
reports in this area is, however, much too limited
to draw conclusions.
Tannins
Tannins comprise a complex mixture of higher
plant, water-soluble polyphenolic compounds of
varying molecular masses that have the ability to
react with proteins, polysaccharides and other
macromolecules. They tend to be considered
antinutritional, because they decrease the
digestibility and metabolisable energy of feeds
through direct interaction with proteins and
carbohydrates from both exogenous and endo-
genous sources. In ruminants, tannins may be
useful in limiting protein degradation in the
rumen, thereby permitting more dietary amino
acids to flow to the abomasum (McSweeney et al.,
2001). In poultry, contrastingly, growth is sup-
pressed by vegetable tannins (Ahmed et al.,
1991). Amino acid absorption is compromised
by tannins, especially of methionine, histidine
and lysine (Mansoori and Acamovic, 2007). High
tannin extracts did not alter the mortality of
chickens, however they reduced the absorption
of minerals such as calcium, magnesium, potas-
sium, sodium and phosphorus from the feed
(Hassan et al., 2003). In another experiment
tannins extracted from Vicia faba seeds increased
mortality, reduced body weight, feed intake and
poorer feed conversion ratio (Ortiz et al., 1994)
as well as decreased the digestibility of protein
and the activity of digestive enzymes (Yuste et al.,
1992). There do not seem to be reports of
beneficial effects of tannins in poultry.
Saponins
Some research has been performed on the
application of plant saponins to poultry produc-
tion, the compounds being recognised as natural
detergents. Extracts from two saponins-rich
plants, Yucca schidigera and Quillaja saponaria
(Cheeke, 2000; Yeo and Kim, 1997; Preston et al.,
1999), had no clear effect on broiler chick
performance. Some effects, like increased food
intake, body weight gain and energy utilisation
were reported in one experiment (Preston et al.,
1999), while in another the feed intake was not
affected when a 0.2% concentration of the
extract was incorporated (Yeo and Kim, 1997).
It should, however, be made clear that the claim
that it is the saponins present in Yucca or Quillaja
extracts that are responsible for their positive
effects has not been justified. These extracts are
simply condensed juice pressed from the trunk,
in which saponins are one of the dominant
groups of compounds present in this matrix.
Polysaccharides are also abundant, and their
influence on nutritional parameters cannot be
neglected. Structurally undefined saponins
(75 mg/kg/day) showed positive effects on
growth and carcase quality (Miah et al., 2004),
while Balanites aegiptica kernel saponins
tended to reduce body weight in chicks
(Nakhala et al., 1992).
Betaine
Although betaine is a generic description of a
type of zwitterionic chemical compound, the
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term used in poultry nutrition refers to a plant
extract or a feed additive containing one parti-
cular betaine, namely trimethyl glycine. This
review covers the effects of betaine only summa-
rily, because a comprehensive review of betaine
and poultry was published very recently (Metzler-
Zebeli et al., 2009). Betaine is an osmoprotectant
present in all plants and particularly abundant in
sugar beet and its byproducts. Benefits from its
use as a feed additive include the prevention of
heat stress and inhibition of Eimeria parasitic
infection, both presumably due to the ionic
nature of the molecule. Its methyl groups are
thought also partly to substitute other methyl
group donors such as methionine and choline.
Both modes of action lead to improved nutrient
digestibility and growth performance.
Other plant bioactives
A large group of phytochemicals that are widely
distributed in plants is phenolics. Among these,
the flavonoids (Figure) are the group which has
been indicated as possibly most beneficial for
poultry performance. The addition to feed of
300 mg/kg of flavonoids (rutin, hesperidine,
quercetin and naringenin) together with manna-
noligosaccharides (MOS) had a significant stimu-
latory effect on feed conversion ratio (Batista
et al., 2007). Additionally there was lower meat
oxidation both after refrigeration and freezing
when birds were fed flavonoids þMOS, which
may be attributed to antioxidant effect of
flavonoids; quercetine and hesperidine are con-
sidered the strongest antioxidants of the flavo-
noid family (Burda and Oleszek, 2001). Extracts
containing isoflavones significantly increased
serum testosterone levels in male chickens and
decreased serum uric acids and abdominal fat
(Zhengkang et al., 2006). Supplementation with
daidzein (3 mg/kg/day) significantly increased
laying rate, average egg weight and egg
cholesterol level in laying hens and ducks
(Wang et al., 1994).
Other phenolics of interest in poultry feed
supplements are catechins and their complexes,
proanthocyanidins, flavolignans, tannins and
phenolic acids. Green tea (Camellia sinensis)
extract containing catechins and their gallates
minimised hyperlipidemia and oxidative stress
induced by corticosterone treatment in broiler
chickens (Eid et al., 2003). Tea also acts as an
antioxidant in meat storage. Silimarin, the poly-
phenolic extract from Silybum marianum and
Cynara cardunculus containing flavolignans,
which are strong antioxidants protecting the
liver from toxins and pollutants by preventing
free radical damage, was fed in broiler chickens
at rates of 40 and 80 mg/kg. The treatment with
silimarin had no effect on growth performance
and had no specific haematoprotective effect,
but slightly decreased slaughter yields. The lipid
content of breast and thigh was decreased and
the resistance of muscles to oxidative stress
increased under this treatment (Schiavone et al.,
2007). Moreover it was shown that silimarin
phytosome can provide protection against the
negative effects of aflatoxin B
1
in broiler chicks
(Tedesco et al., 2004). Similarly, it protects
against pollutants such as carbon monoxide,
pesticides and herbicides, by breaking them
down from potentially lethal substances into
those that are less destructive to the human
body. Polyphenol rich grape pomace (peels and
seeds) added at the rate of 5
—
30 g/kg of diet
reduced the lipid oxidation in meat during
refrigerated storage and increased liver -toco-
pherol concentration (Goni et al., 2007). Grape
seed extract in the rate of 2.59
—
5.28% of the feed
reduced post mortem development of thiobarbi-
turic acid reactive substances in dark poultry
meat but had also detrimental effect on the body
weight gain (Lau et al., 2003).
Extracts from sage, thyme and rosemary
(5000 mg/kg), rich in rosmarinic acid, another
natural antioxidant, had no influence on feed
intake and feed conversion, but from 14 to 21 d
of age broilers grew faster and improved
apparent whole tract and an improved ileal
digestibility of nutrients was observed
(Hernandez et al., 2004).
An alcohol extract of Propolis (honey bee
glue) containing polyphenols used at the rate of
50
—
250 mg/kg diet significantly increased aver-
age weight gain, feed consumption and feed
efficiency in broiler chicks. The mortality rate
determined after 21 d of growth was decreased
as compared to the control diet (Khojasteh and
Shivazad, 2006).
CURRENT RESEARCH PROJECTS
The global trend to move away from in-feed
antibiotics and coccidiostats has strengthened
since 2006, when the use of GPA was banned
within the EU member states. Therefore research
groups and poultry industries worldwide are
searching to develop alternatives. Some have
performed clinical trials with herbal feed
additives.
At present different herbal preparations in
poultry feeding are examined for their antibac-
terial, antiparasitic, antioxidative and/or other
health and performance promoting properties
like feed intake, feed conversion, body weight,
weight gain, growth performance, feed
conversion ratio, gizzard function, gut develop-
ment, nutrient digestibility, digestibility of
organic matter and crude protein, gut microflora
PLANT BIOACTIVES: A REVIEW 479
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or content on metabolisable energy of feed
mixture.
For example at this time in Austria some
companies are working in these fields: Richter
Pharma AG www.richter-pharma.at, Delacon
Phytogenic Feed Additives www.delacon.com,
Indian Herbs GmbH www.indianherbs.at and
Biomin AG www.biomin.at. They are conducting
clinical trials in feeding herbal additives to
different poultry, e g. laying hens, broilers and
turkeys. In Australia, PRATU (Poultry Research
and Teaching Unit, www.poultryhub.org) is
involved in many aspects of poultry science
including nutrition and physiology, health and
welfare, disease, production and environment
and they have funded research projects in all
these sectors. There are also other research
groups all over the world (both from universities,
institutes and companies) as in Germany, United
Kingdom, Poland, Finland, Spain, The
Netherlands, Turkey, China, Taiwan, India,
Pakistan, Ukraine, Lithuania, United States,
Canada, Australia, and Brazil which are doing
research in these fields of activity. Unfortunately
details of these projects are for the most part not
publicly available currently.
CONCLUSIONS
The banning of GPA was intended mainly to
protect the human population from transmissible
antibiotic resistance reaching human pathogens,
rendering them refractory to treatment. The
benefits of the ban extend to less stress on
the environment in general, for example in terms
of loss of microbial diversity in soils fertilised
with manure from animals receiving GPA
(Opalinski et al., 1998). The main downside of
the ban was the problems it presented to
livestock producers, significantly poultry produ-
cers. The examples presented here demonstrate
that there is a strong basis for looking to the
plant kingdom for solutions to the problems, and
indeed for new opportunities to benefit poultry
production.
Although this is a lengthy review, it is by
no means comprehensive. Plants or their
bioactives have production or health benefits
across a wide range of effects other than those
described here, including fertility (Cerolini et al.,
2005), minimising lead concentrations in meat
(Hanafy et al., 1994), and relief of heat
stress (Rajmane and Sonawane, 1997). We hope
that the present review sets a framework for
identifying some plant bioactives that hold
particular promise for future research and
application.
ACKNOWLEDGMENTS
This review forms part of the objectives of the
European Commission-funded project, FEED-SEG
(FOOD-CT-2007-043077). The Rowett Institute of
Nutrition and Health receives funding from the
Scottish Government Rural and Environment
Research and Analysis Directorate (RERAD). Part
of the work (WO) was supported by the IUNG,
project 2.6.We thank Vicki Saint and Mary Mowat
for their work in editing the manuscript and
gathering and collating references, and Alfons
Jansmann for commenting on the manuscript.
REFERENCES
ACAMOVIC,T.&BROOKER, J.D. (2005) Biochemistry of plant
secondary metabolites and their effects in animals.
Proceedings of the Nutrition Society,64: 403–412.
AHMED, A.E., SMITHARD,R.&ELLIS, M. (1991) Activities of
enzymes of the pancreas, and the lumen and mucosa of
the small intestine in growing broiler cockerels fed
on tannin-containing diets. British Journal of Nutrition,
65: 189–197.
AKSIT, M., GOKSOY, E., KOK, F., OZDEMIR,D.&OZDOGAN,M.
(2006) The impacts of organic acid and essential oil
supplementations to diets on the microbiological quality
of chicken carcasses. Archiv fur Geflugelkunde,70: 168–173.
ALCICEK, A., BOZKURT,M.&CABUK, M. (2004) The effect of
a mixture of herbal essential oils, an organic acid or
a probiotic on broiler performance. South African Journal
of Animal Science,34: 217–222.
ALLEN, P.C. & FETTERER, R.H. (2002) Recent advances in
biology and immunobiology of Eimeria species and in
diagnosis and control of infection with these coccidian
parasites of poultry. Clinical Microbiology Reviews,
15: 58–65.
ALLEN, P.C., LYDON,J.&DANFORTH, H.D. (1997) Effects of
components of Artemisia annua on coccidia infections in
chickens. Poultry Science,76: 1156–1163.
ALLEN, P.C., DANFORTH, H.D. & AUGUSTINE, P.C. (1998)
Dietary modulation of avian coccidiosis. International
Journal for Parasitology,28: 1131–1140.
ALLEN, P.C., DANFORTH, H.D. & STITT, P.A. (2000) Effects of
nutritionally balanced and stabilized flaxmeal-based diets
on Eimeria tenella infections in chickens. Poultry Science,
79: 489–492.
ANNETT, C.B., VISTE, J.R., CHIRINO-TREJO,M.&CLASSEN, H.L.
(2002) Necrotic enteritis: effect of barley, wheat and corn
diets on proliferation of Clostridium perfringens type A.
Avian Pathology,31: 599–602.
APAJALAHTI, J.H.A., KETTUNEN, A., BEDFORD, M.R. &
HOLBEN, W.E. (2001) Percent GþC profiling accurately
reveals diet-related differences in the gastrointestinal
microbial community of broiler chickens. Applied and
Environmental Microbiology,67: 5656–5667.
APAJALAHTI, J., KETTUNEN,A.&GRAHAM, H. (2004)
Characteristics of the gastrointestinal microbial commu-
nities, with special reference to the chicken. Worlds Poultry
Science Journal,60: 223–232.
ARAB, H.A., RAHBARI, S., RASSOULI, A., MOSLEMI, M.H. &
KHOSRAVIRAD, F. (2006) Determination of artemisinin in
Artemisia sieberi and anticoccidial effects of the plant
extract in broiler chickens. Tropical Animal Health and
Production,38: 497–503.
BABU, U.S. & RAYBOURNE, R.B. (2008) Impact of dietary
components on chicken immune system and Salmonella
infection. Expert Review of Anti-Infective Therapy,
6: 121–135.
480 R.J. WALLACE ET AL.
Downloaded By: [University of Aberdeen] At: 16:27 22 October 2010
BAMPIDIS, V.A., CHRISTODOULOU, V., FLOUROU-PANERI, P.,
CHRISTAKI, E., CHATZOPOULOU, P.S., TSILIGIANNI,T.&
SPAIS, A.B. (2005) Effect of dietary dried oregano leaves
on growth performance, carcase characteristics and serum
cholesterol of female early maturing turkeys. British Poultry
Science,46: 595–601.
BARBOUR, E.K., SAGHERIAN, V., TALHOUK, S., TALHOUK, R.,
FARRAN, M.T., SLEIMAN, F.T. & HARAKEH, S. (2004)
Evaluation of homeopathy in broiler chickens exposed to
live viral vaccines and administered Calendula officinalis
extract. Medical Science Monitor,10: BR281–BR285.
BATISTA, L.S., GARCIA, E.A., FAITARONE, A.B.G., SHERER, M.R.,
MORI, C., PELICIA,K.&PIZZOLANTE , C.C. (2007) Flavonoids
and mannanoligosaccharides in broiler diets. Brazilian
Journal of Poultry Science,9: 33–37.
BATUNGBACAL, M.R., HILOMEN, G.V., LUIS, E.S., CENTENO, J.R.
&C
ARANDANG, N.F. (2007) Comparative efficacy of
oregano (Origanum vulgare) extract and amprolium in
the control of coccidiosis and their effect on broiler
performance. Philippine Journal of Veterinary Medicine,
44: 91–99.
BAYRAM, I., CETINGUL, I., AKKAYA,B.&UYARLAR, C. (2007)
Effects of aniseed (Pimpinella anisum L.), on egg produc-
tion, quality, cholesterol levels, hatching results and the
antibody values in blood of laying quails (Coturnix coturnix
japonica). Archiva Zootechnica,10: 1–5.
BECKER, P.M. & GALLETTI, S. (2008) Food and feed compo-
nents for gut health-promoting adhesion of E. coli and
Salmonella enterica.Journal of the Science of Food and
Agriculture,88: 2026–2035.
BEERY, J.T., HUGDAHL, M.B. & DOYLE, M.P. (1988)
Colonization of gastrointestinal tracts of chicks by
Campylobacter-Jejuni.Applied and Environmental
Microbiology,54: 2365–2370.
BEN ARFA, A., COMBES, S., PREZIOSI-BELLOY, L., GONTARD,N.&
CHALIER, P. (2006) Antimicrobial activity of carvacrol
related to its chemical structure. Letters in Applied
Microbiology,43: 149–154.
BOTSOGLOU, N.A., YANNAKOPOULOS, A.L., FLETOURIS, D.J.,
TSERVENIGOUSSI, A.S. & FORTOMARIS, P.D. (1997) Effect of
dietary thyme on the oxidative stability of egg yolk. Journal
of Agricultural and Food Chemistry,45: 3711–3716.
BOTSOGLOU, N.A., FLOROU-PANERI, P., CHRISTAKI, E.,
FLETOURIS, D.J. & SPAIS, A.B. (2002) Effect of dietary
oregano essential oil on performance of chickens and on
iron-induced lipid oxidation of breast, thigh and abdom-
inal fat tissues. Br.Poult.Sci.,43: 223–230.
BOTSOGLOU, N.A., FLOROU-PANERI, P., NIKOLAKAKIS, I.,
GIANNENAS, I., DOTAS, V., BOTSOGLOU, E.N. &
AGGELOPOULOS, S. (2005) Effect of dietary saffron (Crocus
sativus L.) on the oxidative stability of egg yolk. British
Poultry Science,46: 701–707.
BRANTON, S.L., LOTT, D., DEATON, J.W., MASLIN, W.R.,
AUSTIN, F.W., POTE, L.M., KEIRS, R.W., LATOUR, M.A. &
DAY, E.J. (1997) The effect of added complex carbohy-
drates or added dietary fiber on necrotic enteritis lesions
in broiler chickens. Poultry Science,76: 24–28.
BURDA,S.&OLESZEK, W. (2001) Antioxidant and antiradical
activities of flavonoids. Journal of Agricultural and Food
Chemistry,49: 2774–2779.
BURT, S. (2004) Essential oils: their antibacterial properties
and potential applications in foods
—
a review. International
Journal of Food Microbiology,94: 223–253.
BURT, S.A., VAN DER ZEE, R., KOETS, A.P., DE GRAAFF, A.M.,
VAN KNAPEN, F., GAASTRA, W., HAAGSMAN, H.P. &
VELDHUIZEN, E.J.A. (2007) Carvacrol induces heat shock
protein 60 and inhibits synthesis of flagellin in
Escherichia coli O157: H7v. Applied and Environmental
Microbiology,73: 4484–4490.
CABUKT, M., BOZKURT, M., ALCICEK, A., AKBAS,Y.&
KUCUKYILMAZ, K. (2006a) Effect of a herbal essential oil
mixture on growth and internal organ weight of broilers
from young and old breeder flocks. South African Journal
of Animal Science,36: 135–141.
CABUKT, M., BOZKURT, M., ALCICEK, A., CATLI, A.U. &
BASER, K.H.C. (2006b) Effect of dietary essential oil
mixture on performance of laying hens in summer
season. South African Journal of Animal Science,36: 215–221.
CALORE, E.E., CAVALIERE, M.J., HARAGUCHI, M., GORNIAK, S.L.,
DAGLI, M.L.Z., RASPANTINI, P.C., CALORE, N.M.P. & WEG,R.
(1998) Toxic peripheral neuropathy of chicks fed Senna
occidentalis seeds. Ecotoxicology and Environmental Safety,
39: 27–30.
CASEWELL, M., FRIIS, C., MARCO, E., MCMULLIN,P.&PHILLIPS,I.
(2003) The European ban on growth-promoting
antibiotics and emerging consequences for human and
animal health. Journal of Antimicrobial Chemotherapy,
52: 159–161.
CEROLINI, S., SURAI, P.F., SPEAKE, B.K. & SPARKS, N.H.C. (2005)
Dietary fish and evening primrose oil with vitamin E
effects on semen variables in cockerels. British Poultry
Science,46: 214–222.
CHALMERS, G., BRUCE, H.L., HUNTER, D.B., PARREIRA, V.R.,
KULKARNI, R.R., JIANG, Y.F., PRESCOTT, J.F. & BOERLIN,P.
(2008) Multilocus sequence typing Analysis of Clostridium
perfringens isolates from necrotic enteritis outbreaks in
broiler chicken populations. Journal of Clinical Microbiology,
46: 3957–3964.
CHAO, S.C., YOUNG, D.G. & OBERG, C.J. (2000) Screening for
inhibitory activity of essential oils on selected bacteria,
fungi and viruses. Journal of Essential Oil Research,
12: 639–649.
CHEEKE, P.R. (2000) Actual and potential applications of
Yucca schidigera and Quillaja saponaria saponins in human
and animal nutrition. Proceedings of the American Society of
Animal Science1999,77: 1–h
—
10-h.
CHEN, H.L., LI, D.F., CHANG, B.Y., GONG, L.M., DAI, J.G. &
YI, G.F. (2003) Effects of Chinese herbal polysaccharides
on the immunity and growth performance of young
broilers. Poultry Science,82: 364–370.
CHO, S.H., NA, Y.E. & AHN, Y.J. (2003) Growth-inhibiting
effects of seco-tanapartholides identified in Artemisia
princeps var. orientalis whole plant on human intestinal
bacteria. Journal of Applied Microbiology,95: 7–12.
CHOWDHURY, S.R., CHOWDHURY, S.D. & SMITH, T.K. (2002)
Effects of dietary garlic on cholesterol metabolism in
laying hens. Poultry Science,81: 1856–1862.
CHRISTAKI, E., FLOROU-PANERI, P., GIANNENAS, I.,
PAPAZAHARIADOU, M., BOTSOGLOU, N.A. & SPAIS, A.B.
(2004) Effect of a mixture of herbal extracts on broiler
chickens infected with Eimeria tenella.Animal Research,
53: 137–144.
COLE, C.B., FULLER,R.&COATES, M.E. (1981) Microbial
activity in the alimentary tract of birds, in: SASAKI, S.,
OZAWA,A.&HASHIMOTO, K. (Eds) Recent Advances in
Germfree Research, pp. 365
—
367 (Tokyo, Tokai University
Press).
COLLIER, C.T., VAN DER KLIS, J.D., DEPLANCKE, B.,
ANDERSON, D.B. & GASKINS, H.R. (2003) Effects of tylosin
on bacterial mucolysis, Clostridium perfringens colonization,
and intestinal barrier function in a chick model of necrotic
enteritis. Antimicrobial Agents and Chemotherapy,
47: 3311–3317.
CORRY, J.E.L. & ATABAY, H.I. (2001) Poultry as a source of
Campylobacter and related organisms. Journal of Applied
Microbiology,90: 96S–114S.
COX, F.E.G. (1998) Control of coccidiosis: lessons from
other sporozoa. International Journal for Parasitology,
28: 165–179.
CROSS, D.E., MCDEVITT, R.M., HILLMAN,K.&ACAMOVIC,T.
(2007) The effect of herbs and their associated essential
oils on performance, dietary digestibility and gut
PLANT BIOACTIVES: A REVIEW 481
Downloaded By: [University of Aberdeen] At: 16:27 22 October 2010
microflora in chickens from 7 to 28 days of age. British
Poultry Science,48: 496–506.
DAHIYA, J.P., HOEHLER, D., WILKIE, D.C., VAN KESSEL, A.G. &
DREW, M.D. (2005) Effect of dietary glycine on intestinal
Clostridium perfringens populations and a-toxin production
in broiler chickens. Poultry Science,84: 94.
DAHIYA, J.P., WILKIE, D.C., VAN KESSEL, A.G. & DREW, M.D.
(2006) Potential strategies for controlling necrotic enter-
itis in broiler chickens in post-antibiotic era. Animal Feed
Science and Technology,129: 60–88.
DALLOUL, R.A. & LILLEHOJ, H.S. (2006) Poultry
coccidiosis: recent advancements in control measures
and vaccine development. Expert Review of Vaccines,
5: 143–163.
DAY, R.M. & THOMAS, O.P. (1980) Growth depression
of chicks fed a crude rye extract containing pectic
substances. Poultry Science,59: 2754–2759.
DEANS, S.G. & RITCHIE, G. (1987) Antibacterial properties
of plant essential oils. International Journal of Food
Microbiology,5: 165–180.
DEMIR, E., SARICA, S., O
¨ZCAN, M.A. & SUIC¸ MEZ, M. (2003) The
use of natural feed additives as alternatives for an
antibiotic growth promoter in broiler diets. British
Poultry Science,44: 44–45.
DENLI, M., OKAN,F.&ULUOCAK, A.N. (2004) Effect of dietary
supplementation of herb essential oils on the growth
performance, carcass and intestinal characteristics of quail
(Coturnix coturnix japonica). South African Journal of Animal
Science,34: 174–179.
DIPASQUA, R., HOSKINS, N., BETTS,G.&MAURIELLO, G. (2006)
Changes in membrane fatty acids composition of micro-
bial cells induced by addiction of thymol, carvacrol,
limonene, cinnamaldehyde, and eugenol in the growing
media. Journal of Agricultural and Food Chemistry,
54: 2745–2749.
DONG, X.F., GAO, W.W., TONG, J.M., JIA, H.Q., SA, R.N. &
ZHANG, Q. (2007) Effect of polysavone (alfalfa extract) on
abdominal fat deposition and immunity in broiler chick-
ens. Poultry Science,86: 1955–1959.
DORHOI, A., DOBREAN, V., ZAHAN,M.&VIRAG, P. (2006)
Modulatory effects of several herbal extracts on avian
peripheral blood cell immune responses. Phytotherapy
Research,20: 352–358.
DORMAN, H.J.D. & DEANS, S.G. (2000) Antimicrobial agents
from plants: antibacterial activity of plant volatile oils.
Journal of Applied Microbiology,88: 308–316.
DURAPE, N.M. (2007) Phytochemicals improve semen quality
and fertility. World Poultry,23: 18–20.
DURRANI, F., SULTAN, A., SAJJAD, A., CHAND, N., KHATTAK,F.&
DURRANI, Z. (2007) Efficacy of aniseed extract as immune
stimulant and growth promoter in broiler chicks. Pakistan
Journal of Biological Sciences, 10.
EID, Y.Z., OHTSUKA,A.&HAYASHI, K. (2003) Tea polyphenols
reduce glucocorticoid-induced growth inhibition and
oxidative stress in broiler chickens. British Poultry Science,
44: 127–132.
EL-ABASY, M., MOTOBU, M., SHIMURA, K., NA, K.J., KANG, C.B.,
KOGE, K., ONODERA,T.&HIROTA, Y. (2002)
Immunostimulating and growth-promoting effects of
sugar cane extract (SCE) in chickens. Journal of Veterinary
Medical Science,64: 1061–1063.
EL-ABASY, M., MOTOBU, M., NA, K.J., SHIMURA, K.,
NAKAMURA, K., KOGE, K., ONODERA,T.&HIROTA,Y.
(2003) Protective effects of sugar cane extracts (SCE) on
Eimeria tenella infection in chickens. Journal of Veterinary
Medical Science,65: 865–871.
EUROPEAN COMMISSION (EC) (2008) Report to the European
Parliament and the Council on the use of coccidiostats and
histomonostats as feed additives (COM (2008) 233)
Pursant to Article 11 of Regulation 1831/2003. 2008.
Ref Type: Report.
EUROPEAN FOOD SAFETY AUTHORITY (EFSA) (2008) Guidance
for the preparation of dossiers for coccidiostats and
histomonostats. The EFSA Journal,777: 1–11.
EWERS, C., ANTAO, E.M., DIEHL, I., PHILIPP, H.C. &
WIELER, L.H. (2009) Intestine and environment of the
chicken as reservoirs for extraintestinal pathogenic
Escherichia coli strains with zoonotic potential. Applied
and Environmental Microbiology,75: 184–192.
FAYER, R. (1971) Quinine inhibition of host cell penetration
by Eimerian sporozoites in-vitro.Journal of Parasitology,
57: 901–905.
FETTERER, R.H., AUGUSTINE, P.C., ALLEN, P.C. & BARFIELD, R.C.
(2003) The effect of dietary betaine on intestinal and
plasma levels of betaine in uninfected and coccidia-
infected broiler chicks. Parasitology Research,90: 343–348.
FISHER,K.&PHILLIPS, C.A. (2006) The effect of lemon, orange
and bergamot essential oils and their components on the
survival of Campylobacter jejuni,Escherichia coli O157,
Listeria monocytogenes,Bacillus cereus and Staphylococcus
aureus in vitro and in food systems. Journal of Applied
Microbiology,101: 1232–1240.
FLORES, M.P., CASTANON, J.I.R. & MCNAB, J.M. (1994) Effect of
tannins on starch digestibility and TMEn of triticale and
semipurified starches from triticale and field beans. British
Poultry Science,35: 281–286.
FLOROU-PANERI, P., CHRISTAKI, E., GIANNENAS, I.A.,
PAPAZAHARIADOU, M., BOTSOGLOU, N.A. & SPAIS, A.B.
(2004) Effect of dietary Olympus tea (Sideritis scardica)
supplementation on performance of chickens challenged
with Eimeria tenella.Journal of Animal and Feed Sciences,
13: 301–311.
FLOROU-PANERI, P., DOTAS, D., MITSOPOULOS, I., DOTAS, V.,
BOTSOGLOU, E., NIKOLAKAKIS,I.&BOTSOGLOU, N. (2006)
Effect of feeding rosemary and -tocopheryl acetate on
hen performance and egg quality. Journal of Poultry Science,
43: 143–149.
FRIEDMAN, C.R., NEIMANN, J., WEGENER, H.C. & TAUXE, R.V.
(2000) Epidemiology of Campylobacter jejuni infections in
the United States and other industrialized nations, in:
NACHAMKIN,I.&BLASER, M.J. (Eds) Campylobacter, 2nd ed.,
pp. 139
—
154 (Washington, DC, ASM Press).
FUKATA, T., HADATE, Y., BABA,E.&ARAKAWA, A. (1991)
Influence of bacteria on Clostridium perfringens infections
in young chickens. Avian Diseases,35: 224–227.
FULLER, R. (1984) Microbial activity in the alimentary tract
of birds. Proceedings of the Nutrition Society,43: 55–61.
FULLER, R. (1989) Probiotics in man and animals. Journal
of Applied Bacteriology,66: 365–378.
FULLER,R.&COATES, M.E. (1983) Influence of the intestinal
microflora on nutrition, in: FREEMAN, B.M. (Ed.) Physiology
and Biochemistry of the Domestic Fowl, pp. 51
—
61 (London,
Academic Press).
FULLER, R., COATES, M.E. & HARRISON, G.F. (1979) Influence
of specific bacteria and a filterable agent on the growth
of gnotobiotic chicks. Journal of Applied Bacteriology,
46: 335–342.
FULLER, R., HOUGHTON, S.B. & BROOKER, B.E. (1981)
Attachment of Streptococcus faecium to the duodenal
epithelium of the chicken and its importance in coloniza-
tion of the small intestine. Applied and Environmental
Microbiology,41: 1433–1441.
FURUSE,M.&YOKOTA, H. (1984) Protein and energy-
utilization in germ-free and conventional chicks given
diets containnig different levels of dietary-protein. British
Journal of Nutrition,51: 255–264.
FURUSE,M.&YOKOTA, H. (1985) Effect of the gut microflora
on chick growth and utilization of protein and energy at
different concentrations of dietary-protein. British Poultry
Science,26: 97–104.
GADHI, C.A., WEBER, M., MORY, F., BENHARREF, A., LION, C.,
JANA,M.&LOZNIEWSKI, A. (1999) Antibacterial activity of
482 R.J. WALLACE ET AL.
Downloaded By: [University of Aberdeen] At: 16:27 22 October 2010
Aristolochia paucinervis Pomel. Journal of Ethnopharmacology,
67: 87–92.
GALOBART, J., BARROETA, A.C., BAUCELLS, M.D., CODONY,R.&
TERNES, W. (2001) Effect of dietary supplementation with
rosemary extract and alpha-tocopheryl acetate on lipid
oxidation in eggs enriched with omega 3-fatty acids.
Poultry Science,80: 460–467.
GEIDAM, Y.A., USMAN, H., ABUBAKAR,M.&IBRAHIM, B. (2007)
Effects of aqueous leaf extracts of Psidium guajava on
bacteria isolated from the navel of day-old chicks. Research
Journal of Microbiology,2: 960–965.
GIANNENAS, I., FLOROU-PANERI, P., PAPAZAHARIADOU, M.,
CHRISTAKI, E., BOTSOGLOU, N.A. & SPAIS, A.B. (2003)
Effect of dietary supplementation with oregano essential
oil on performance of broilers after experimental infec-
tion with Eimeria tenella.Archives of Animal Nutrition-Archiv
fur Tierernahrung,57: 99–106.
GIANNENAS, I.A., FLOROU-PANERI, P., PAPAZAHARIADOU, M.,
BOTSOGLOU, N.A., CHRISTAKI,E.&SPAIS, A.B. (2004)
Effect of diet supplementation with ground oregano on
performance of broiler chickens challenged with Eimeria
tenella.Archiv fur Geflugelkunde,68: 247–252.
GIANNENAS, I.A., FLOROU-PANERI, P., BOTSOGLOU, N.A.,
CHRISTAKI,E.&SPAIS, A.B. (2005) Effect of supple-
menting feed with oregano and/or alpha-tocopheryl
acetate on growth of broiler chickens and oxidative
stability of meat. Journal of Animal and Feed Sciences,
14: 521–535.
GONG, J.H., FORSTER, R.J., YU, H., CHAMBERS, J.R.,
SABOUR, P.M., WHEATCROFT,R.&CHEN, S. (2002a)
Diversity and phylogenetic analysis of bacteria in the
mucosa of chicken ceca and comparison with bacteria in
the cecal lumen. FEMS Microbiology Letters,208: 1–7.
GONG, J.H., FORSTER, R.J., YU, H., CHAMBERS, J.R.,
WHEATCROFT, R., SABOUR, P.M. & CHEN, S. (2002b)
Molecular analysis of bacterial populations in the ileum
of broiler chickens and comparison with bacteria in the
cecum. FEMS Microbiology Ecology,41: 171–179.
GONI, I., BRENES, A., CENTENO, C., VIVEROS, A., SAURA-
CALIXTO, F., REBOLE, A., ARIJA,I.&ESTEVEZ, R. (2007)
Effect of dietary grape pomace and vitamin E on growth
performance, nutrient digestibility, and susceptibility to
meat lipid oxidation in chickens. Poultry Science,
86: 508–516.
GORDON, H.A. & PESTI, L. (1971) The gnotobiotic animal as
a tool in the study of host microbial relationships.
Bacteriological reviews,35: 390–429.
GOVARIS, A., BOTSOGLOU, D., FLOROU-PANERI, P., MOULAS,A.&
PAPAGEORGIOU, G. (2005) Dietary supplementation of
oregano essential oil and alpha-tocopheryl acetate on
microbial growth and lipid oxidation of turkey breast
fillets during storage. International Journal of Poultry Science,
4: 969–975.
GRAHAM, J.P., BOLAND, J.J. & SILBERGELD, E. (2007)
Growth promoting antibiotics in food animal
production: an economic analysis. Public Health Reports,
122: 79–87.
GRAZIANO, M.J., FLORY, W., SEGER, C.L. & HEBERT, C.D. (1983)
Effects of a Cassia occidentalis extract in the domestic
chicken (Gallus domesticus). American Journal of Veterinary
Research,44: 1238–1244.
GRIGGS, J.P. & JACOB, J.P. (2005) Alternatives to antibiotics
for organic poultry production. Journal of Applied Poultry
Research,14: 750–756.
GUGGENBICHLER, J.P., FOLLRICH, B., FRANZ,C.&JURENITSCH,J.
(2004) Einsatz von Antibiotika in der Nutztierhaltung
—
Ersatz durch saure Oligogalakturonide. Antibiotika
Monitor,20: 93–101.
GUO, F.C., KWAKKEL, R.P., WILLIAMS, B.A., PARMENTIER, H.K.,
LI, W.K., YANG, Z.Q. & VERSTEGEN, M.W.A. (2004a) Effects
of mushroom and herb polysaccharides on cellular and
humoral immune responses of Eimeria tenella infected
chickens. Poultry Science,83: 1124–1132.
GUO, F.C., KWAKKEL, R.P., WILLIAMS, B.A., LI, W.K., LI, H.S.,
LUO, J.Y., LI, X.P., WEI, Y.X., YAN, Z.T. &
VERSTEGEN, M.W.A. (2004b) Effects of mushroom and
herb polysaccharides, as alternatives for an antibiotic, on
growth performance of broilers. British Poultry Science,
45: 684–694.
GUO, F.C., WILLIAMS, B.A., KWAKKEL, R.P., LI, H.S., LI, X.P.,
LUO, J.Y., LI, W.K. & VERSTEGEN, M.W.A. (2004c) Effects of
mushroom and herb polysaccharides, as alternatives for
an antibiotic, on the cecal microbial ecosystem in broiler
chickens. Poultry Science,83: 175–182.
GUO, F.C., KWAKKEL, R.P., WILLIAMS, B.A., SUO, X., LI, W.K. &
VERSTEGEN, M.W.A. (2005) Coccidiosis immunization:
effects of mushroom and herb polysaccharides on
immune responses of chickens infected with Eimeria
tenella.Avian Diseases,49: 70–73.
HALLE, I., THOMANN, R., BAUERMANN, U., HENNING,M.&
KOHLER, P. (2004) Effects of a graded supplementation
of herbs and essential oils in broiler feed on growth
and carcass traits. Landbauforschung Volkenrode,
54: 219–229.
HALLE, I., THOMANN,R.&BAUERMANN, U. (2008) Effect of
a graded supplementation of savory in broiler feed on
growth and carcass traits. Archiv fur Geflugelkunde,
72: 129–135.
HANAFY, M.S.M., SHALABY, S.M., ELFOULY, M.A.A.,
ELAZIZ, M.I.A. & SOLIMAN, F.A. (1994) Effect of garlic on
lead contents in chicken tissues. Deutsche Tierarztliche
Wochenschrift,101: 157–158.
HANSEL,R.&STICHER, O. (2004) Pharmakognosie
Phytopharmazie (New York, Springer Berlin).
HARIHARAN, H., MURPHY, G.A. & KEMPF, I. (2004)
Campylobacter jejuni: public health hazards and potential
control methods in poultry: a review. Veterinarni Medicina,
49: 441–446.
HASELMEYER, A. (2007) Wirkung von Thymian als Futterzusatz
beim Broiler. DVM Thesis Vet.-med. Univ. Vienna. DVM
Thesis Vet.-med.University Vienna.
HASSAN, I.A.G., ELZUBEIR, E.A. & ELTINAY, A.H. (2003)
Growth and apparent absorption of minerals in broiler
chicks fed diets with low or high tannin contents. Tropical
Animal Health and Production,35: 189–196.
HEBERT, C.D. & FLORY, W. (1983) Determination of the oral
toxicity of Cassia obtusifolia seeds in chickens. Veterinary
and Human Toxicology,25: 164–166.
HERNANDEZ, F., MADRID, J., GARCIA, V., ORENGO,J.&
MEGIAS, M.D. (2004) Influence of two plant extracts on
broilers performance, digestibility, and digestive organ
size. Poultry Science,83: 169–174.
HESS, M. (2002) In-vitro tests of functional plant products against
pathogens of poultry. Lecture, 1st Europ. Sympos. Biocative
Secondary Plant Products in Veterinary Medicine, VUW
Vienna/A, in: In-vitro tests of functional plant products
against pathogens of poultry. Lecture, 1st Europ. Sympos.
Biocative Secondary Plant Products in Veterinary
Medicine, VUW Vienna/A.
HIKOSAKA, K., ELABASY, M., KOYAMA, Y., MOTOBU, M.,
KOGE, K., ISOBE, T., KANG, C.B., HAYASHIDANI, H.,
ONODERA, T., WANG, P.C., MATSUMURA,M.&HIROTA,Y.
(2007) Immunostimulating effects of the polyphenol-rich
fraction of sugar cane (Saccharum officinarum L.) extract in
chickens. Phytotherapy Research,21: 120–125.
HOLDSWORTH, P.A., CONWAY, D.P., MCKENZIE, M.E.,
DAYTON, A.D., CHAPMAN, H.D., MATHIS, G.F., SKINNER, J.T.,
MUNDT, H.C. & WILLIAMS, R.B. (2004) World Association
for the Advancement of Veterinary Parasitology (WAAVP)
guidelines for evaluating the efficacy of anticoccidial drugs
in chickens and turkeys. Veterinary Parasitology,
121: 189–212.
PLANT BIOACTIVES: A REVIEW 483
Downloaded By: [University of Aberdeen] At: 16:27 22 October 2010
HOROSOVA, K., BUJNAKOVA,D.&KMET, V. (2006) Effect of
oregano essential oil on chicken lactobacilli and E. coli.
Folia Microbiologica,51: 278–280.
HORTON, G.M.J., FENNELL, M.J. & PRASAD, B.M. (1991) Effect
of dietary garlic (Allium sativum) on performance carcass
composition and blood-chemistry changes in broiler
chickens. Canadian Journal of Animal Science,71: 939–942.
HUANG, X.Y., WANG, D.Y., HU, Y.H., LU, Y., GUO, Z.H.,
KONG, X.F. & SUN, J.F. (2008) Effect of sulfated astragalus
polysaccharide on cellular infectivity of infectious bursal
disease virus. International Journal of Biological
Macromolecules,42: 166–171.
JAMROZ,D.&KAMEL, C. (2002) Plant extracts enhance broiler
performance. Journal of Animal Science,80:4.
JAMROZ, D., WERTELECKI, T., HOUSZKA,M.&KAMEL, C. (2006)
Influence of diet type on the inclusion of plant origin
active substances on morphological and histochemical
characteristics of the stomach and jejunum walls in
chicken. Journal of Animal Physiology and Animal
Nutrition,90: 255–268.
JAMROZ, D., WILICZKIEWICZ, A., WERTELECKI, T., ORDA,J.&
SKORUPINSKA, J. (2005) Use of active substances of plant
origin in chicken diets based on maize and locally grown
cereals. British Poultry Science,46: 485–493.
JANG, I.S., KO, Y.H., YANG, H.Y., HA, J.S., KIM, J.Y., KIM, J.Y.,
KANG, S.Y., YOO, D.H., NAM, D.S., KIM, D.H. & LEE, C.Y.
(2004) Influence of essential oil components on growth
performance and the functional activity of the pancreas
and small intestine in broiler chickens. Asian-Australasian
Journal of Animal Sciences,17: 394–400.
JANG, S.I., JUN, M.H., LILLEHOJ, H.S., DALLOUL, R.A.,
KONG, I.K., KIM,S.&MIN, W.G. (2007) Anticoccidial
effect of green tea-based diets against Eimeria maxima.
Veterinary Parasitology,144: 172–175.
JASSIM, S.A.A. & NAJI, M.A. (2003) Novel antiviral agents:
a medicinal plant perspective. Journal of Applied
Microbiology,95: 412–427.
JENSEN, B.B. (1998) The impact of feed additives on the
microbial ecology of the gut in young pigs. Journal of
Animal and Feed Sciences,7: 45–64.
JENSEN, L.S. & CHANG, C.H. (1976) Fractionation studies on a
factor in linseed meal protecting against selenosis in
chicks. Poultry Science,55: 594–599.
JUGL-CHIZZOLA, M., SPERGSER, J., SCHILCHER, F., NOVAK, J.,
BUCHER, A., GABLER, C., HAGMULLER,W.&ZITTERL-
EGLSEER, K. (2005) Effects of Thymus vulgaris L. as feed
additive in piglets and against haemolytic E-coli in vitro.
Berliner und MunchenerTtierarztliche Wochenschrift,
118: 495–501.
JUIN, H., ELGAARD,T.&CHICOTEAU, P. (2003) Effect of a citrus
extract (NOR-SPICE AB) on broiler performances. British
Poultry Science,44: 810–811.
JUNEJA, V.K. & FRIEDMAN, M. (2007) Carvacrol, cinnamal-
dehyde, oregano oil, and thymol inhibit Clostridium
perfringens spore germination and outgrowth in ground
turkey during chilling. Journal of Food Protection,
70: 218–222.
KAMEL, C. (2001) Tracing modes of action and roles of plant
extracts in non-ruminants, in: GARNSWORTHY, P.C. &
WISEMAN, J. (Eds) Recent Advances in Animal Nutrition,
pp. 135
—
149 (Nottingham, Nottingham University Press).
KARADAS, F., GRAMMENIDIS, E., SURAI, P.F., ACAMOVIC,T.&
SPARKS, C. (2006) Effects of carotenoids from lucerne,
marigold and tomato on egg yolk pigmentation and
carotenoid composition. British Poultry Science,
47: 561–566.
KENNEDY, M.J. (2001) Coccidiosis in Chickens, pp. 655
—
35
(Alberta Agriculture, Food and Rural Development).
KEYBURN, A.L., SHEEDY, S.A., FORD, M.E., WILLIAMSON, M.M.,
AWAD, M.M., ROOD, J.I. & MOORE, R.J. (2006) Alpha-toxin of
Clostridium perfringens is not an essential virulence factor in
necrotic enteritis in chickens. Infection and Immunity,
74: 6496–6500.
KHOJASTEH SHALMANY,S.&SHIVAZAD, M. (2006) The effect of
diet propolis supplementation on ross broiler chicks
performance. International Journal of Poultry Science,
5: 84–88.
KIDD, M.T. (2004) Nutritional modulation of immune
function in broilers. Poultry Science,83: 650–657.
KLASING, K.C., ADLER, K.L., REMUS, J.C. & CALVERT, C.C.
(2002) Dietary betaine increases intraepithelial lympho-
cytes in the duodenum of coccidia-infected chicks and
increases functional properties of phagocytes. Journal of
Nutrition,132: 2274–2282.
KNARREBORG, A., SIMON, M.A., ENGBERG, R.M., JENSEN, B.B. &
TANNOCK, G.W. (2002) Effects of dietary fat source and
subtherapeutic levels of antibiotic on the bacterial com-
munity in the ileum of broiler chickens at various ages.
Applied and Environmental Microbiology,68: 5918–5924.
KOLTE, A.Y., SADEKAR, R.D., BARMASE, B.S., DESAI, V.F. &
KOLTE, B.R. (1999) Immunomodulating effect of dry
powder of Ocimum sanctum and leaf gall of Ficus racemosa
leaves in broilers naturally infected with IBD virus. Indian
Veterinary Journal,76: 84–86.
KONJUFCA, V.H., PESTI, G.M. & BAKALLI, R.I. (1997)
Modulation of cholesterol levels in broiler meat by dietary
garlic and copper. Poultry Science,76: 1264–1271.
KOSCOVA, J., NEMCOVA, R., GANCARCIKOVA, S., JONECOVA, Z.,
SCIRANKOVA, L., BOMBA,A.&BULECA, V. (2006) Effect of
two plant extracts and Lactobacillus fermentum on coloniza-
tion of gastrointestinal tract by Salmonella enterica var.
Dusseldorf in chicks. Biologia,61: 775–778.
LARAGIONE, R.M. & WOODWARD, M.J. (2002) Virulence factors
of Escherichia coli serotypes associated with avian colisepti-
caemia. Research in Veterinary Science,73: 27–35.
LACROIX,M.&CHIASSON, F. (2004) The influence of MAP
condition and active compounds on the radiosensitization
of Escherichia coli and Salmonella typhi present in chicken
breast. Radiation Physics and Chemistry,71: 69–72.
LAMBERT, R.J.W., SKANDAMIS, P.N., COOTE, P.J. &
NYCHAS, G.J.E. (2001) A study of the minimum inhibitory
concentration and mode of action of oregano essential oil,
thymol and carvacrol. Journal of Applied Microbiology,
91: 453–462.
LAN, Y., VERSTEGEN, M.W.A., TAMMINGA,S.&WILLIAMS, B.A.
(2005) The role of the commensal gut microbial commu-
nity in broiler chickens. Worlds Poultry Science Journal,
61: 95–104.
LAU, D.W. & KING, A.J. (2003) Pre- and post-mortem use of
grape seed extract in dark poultry meat to inhibit
development of thiobarbituric acid reactive substances.
Journal of Agricultural and Food Chemistry,51: 1602–1607.
LEE, K.W., EVERTS, H., KAPPERT, H.J., YEOM, K.H. &
BEYNEN, A.C. (2003a) Dietary carvacrol lowers body
weight gain but improves feed conversion in female
broiler chickens. Journal of Applied Poultry Research,
12: 394–399.
LEE, K.W., EVERTS, H., KAPPERT, H.J., FREHNER, M., LOSA,R.&
BEYNEN, A.C. (2003b) Effects of dietary essential oil
components on growth performance, digestive enzymes
and lipid metabolism in female broiler chickens. British
Poultry Science,44: 450–457.
LEWIS, M.R., ROSE, S.P., MACKENZIE, A.M. & TUCKER, L.A.
(2003) Effects of dietary inclusion of plant extracts on the
growth performance of male broiler chickens. British
Poultry Science,44: S43–S44.
LIM, K.S., YOU, S.J., AN, B.K. & KANG, C.W. (2006) Effects of
dietary garlic powder and copper on cholesterol content
and quality characteristics of chicken eggs. Asian-
Australasian Journal of Animal Sciences,19: 582–586.
LIU, X. D., JANG, A., LEE, B.D., LEE, S. K., LEE,M.&JO,C.
(2009) Effect of dietary inclusion of medicinal herb extract
484 R.J. WALLACE ET AL.
Downloaded By: [University of Aberdeen] At: 16:27 22 October 2010
mix in poultry ration on the physico-chemical quality and
oxidative stability of eggs. Asian-Australian Journal of
Animal Sciences,22: 421–427.
LOPEZ-BOTE, C.J., GRAY, J.I., GOMAA, E.A. & FLEGAL, C.J. (1998)
Effect of dietary administration of oil extracts from
rosemary and sage on lipid oxidation in broiler meat.
British Poultry Science,39: 235–240.
LOSA,R.&KOEHLER, B. (2001) Prevention of colonisation
of Clostridium perfringens in broilers intestine by
essential oils, in: Proceedings of 13th Symposium on
Poultry Nutrition, Blankenberge, Belgium, 133
—
134.
LU, J.R., IDRIS, U., HARMON, B., HOFACRE, C., MAURER, J.J.
&L
EE, M.D. (2003) Diversity and succession of the
intestinal bacterial community of the maturing broiler
chicken. Applied and Environmental Microbiology,
69: 6816–6824.
LU, J., HOFACRE, C., SMITH,F.&LEE, M.D. (2008) Effects
of feed additives on the development on the ileal
bacterial community of the broiler chicken. Animal,
2: 669–676.
MA, D., LIU, Y.Q., LIU, S.W., LI, Q.D. & SHAN, A. (2007)
Influence of Ligustrum lucidum and Schisandra chinensis
fruits on antioxidative metabolism and immunological
parameters of layer chicks. Asian-Australasian Journal of
Animal Sciences,20: 1438–1443.
MANSOORI,B.&ACAMOVIC, T. (2007) The effect of tannic acid
on the excretion of endogenous methionine, histidine and
lysine with broilers. Animal Feed Science and Technology,
134: 198–210.
MCDEVITT, R.M., BROOKER, J.D., ACAMOVIC,T.&
SPARKS, N.H.C. (2006) Necrotic enteritis; a continuing
challenge for the poultry industry. Worlds Poultry Science
Journal,62: 221–247.
MCSWEENEY, C.S., PALMER, B., MCNEILL, D.M. & KRAUSE, D.O.
(2001) Microbial interactions with tannins: nutritional
consequences for ruminants. Anim. Feed Sci. Technol.,
16: 83–93.
MEAD, G.C. (2002) Factors affecting intestinal colonisation of
poultry by campylobacter and role of microflora in
control. Worlds Poultry Science Journal,58: 169–178.
MEAD, G.C. (2004) Current trends in the microbiological
safety of poultry meat. Worlds Poultry Science Journal,
60: 112–118.
METZLER-ZEBELI, B.U., EKLUND,M.&MOSENTHIN, R. (2009)
Impact Of osmoregulatory and methyl donor funtions of
betaine on intestinal health and performance in poultry.
World’s Poultry Sci. J.,65: 419–441.
MIAH, M.Y., RAHMAN, M.S., ISLAM, M.K. & MONIR, M.M. (2004)
Effects of saponin and L-carnitine on the performance and
reproductive fitness of male broiler. International Journal of
Poultry Science,3: 530–533.
MITSCH, P., ZITTERL-EGLSEER, K., KOHLER, B., GABLER, C.,
LOSA,R.&ZIMPERNIK, I. (2004) The effect of two different
blends of essential oil components on the proliferation of
Clostridium perfringens in the intestines of broiler chickens.
Poultry Science,83: 669–675.
MOTTAGHITALAB,M.&TARAZ, Z. (2004) Garlic powder as
blood serum and egg yolk cholesterol lowering agent.
Journal of Poultry Science,41: 50–57.
NAIDOO, V., MCGAW, L.J., BISSCHOP, S.P.R., DUNCAN,N.&
ELOFF, J.N. (2008) The value of plant extracts with
antioxidant activity in attenuating coccidiosis in broiler
chickens. Veterinary Parasitology,153: 214–219.
NAKHLA, H.B., MOHAMMED, O.S.A., ABUALFUTUH, I.M. &
ADAMS, S.E.I. (1992) Effects on chicks of balanites
Aegyptiaca kernel saponin given by different routes of
administration. Veterinary and Human Toxicology,
34: 224–226.
NEWELL, D.G. & FEARNLEY, C. (2003) Sources of
Campylobacter colonization in broiler chickens. Applied
and Environmental Microbiology,69: 4343–4351.
NIEWOLD, T.A. (2007) The nonantibiotic anti-inflammatory
effect of antimicrobial growth promoters, the real mode of
action? A hypothesis. Poultry Science,86: 605–609.
ODUNSI, A.A. (2005) Response of laying hens and growing
broilers to the dietary inclusion of mango (Mangifera
indica L.) seed kernel meal. Tropical Animal Health and
Production,37: 139–150.
OPALINSKI, K.W., DMOWSKA, E., MAKULEC, G., MIERZEJEWSKA, E.,
PETROV, P., PIERZYNOWSKI, S.G. & WOJEWODA, D. (1998) The
reverse of the medal: feed additives in the environment.
Journal of Animal and Feed Sciences,7: 35–43.
ORTIZ, L.T., ALZUETA, C., TREVINO,J.&CASTANO, M. (1994)
Effects of Faba bean tannins on the growth and
histological structure of the intestinal-tract and liver of
chicks and rats. British Poultry Science,35: 743–754.
OVIEDO-RONDON, E.O., CLEMENTE-HERNANDEZ, S., WILLIAMS,P.
&L
OSA, R. (2005) Responses of coccidia-vaccinated
broilers to essential oil blends supplementation up to
forty-nine days of age. Journal of Applied Poultry Research,
14: 657–664.
OVIEDO-RONDON, E.O., HUME, M.E., HERNANDEZ,C.&
CLEMENTE-HERNANDEZ, S. (2006) Intestinal microbial ecol-
ogy of broilers vaccinated and challenged with mixed
Eimeria species, and supplemented with essential oil
blends. Poultry Science,85: 854–860.
PAULI, G.H. (1994) Issues concerning regulatory approval of
macroingredients in food. Abstracts of Papers of the American
Chemical Society,207: 45–AGFD.
PENALVER, P., HUERTA, B., BORGE, C., ASTORGA, R., ROMERO,R.
&P
EREA, A. (2005) Antimicrobial activity of five essential
oils against origin strains of the Enterobacteriaceae family.
APMIS,113: 1–6.
POLTOWICZ,K.&WEZYK, S. (2001) Effect of herb supplemen-
tation in the feeding of laying hens on their
productivity and egg quality. Roczniki Naukowe
Zootechniki,28: 215–225.
PRAKASH, S.K. (2006) Effects of herbal extracts
towards microbicidal activity against pathogenic
Escherichia coli in poultry. International Journal of Poultry
Science,5: 259–261.
PRESTON, C.M., MCCRACKEN, K.J. & BEDFORD, M.R. (1999)
Effects of Yucca schidigera extract, Saccharomyces boulardii
and enzyme supplementation of wheat-based diets on
broiler performance and diet metabolisability. British
Poultry Science,40: S39–S40.
QURESHI, A.A., ABUIRMEILEH, N., DIN, Z.Z., AHMAD, Y.,
BURGER, W.C. & ELSON, C.E. (1983) Suppression of
cholesterogenesis and reduction of LDL cholesterol by
dietary ginseng and its fractions in chicken liver.
Atherosclerosis,48: 81–94.
RADWAN, N.L., HASSAN, R.A., QUOTA, E.M. & FAYEK, H.M.
(2009) Effect of natural antioxidant on oxidative stability
of egg and productive and reproductive performance
of laying hens. International Journal of Poultry Science,
7: 134–150.
RAJMANE, B.V. & SONAWANE, A.S. (1997) Effective use of
herbal preparation (stresroak) as an antistress on perfor-
mance of broilers in hot climate. Biotehnologija u Stocarstvu,
13: 215–218.
RAJPUT, Z.I., XIAO, C.W., HU, S.H., ARIJO, A.G. &
SOOMRO, N.M. (2007) Improvement of the efficacy of
influenza vaccination (H5N1) in chicken by using extract
of Cochinchina momordica seed (ECMS). Journal of Zhejiang
University Science B.,8: 331–337.
RICKARD, M.D. (2004) The use of animals in research:
counting the costs and the benefits. Australian Journal of
Experimental Agriculture,44: 1079–1083.
RIZZA, P.V., MENTEN, J.F.M., RACANICCI, A.M.C. & SANTAROSA,J.
(2008) Foundation and perspectives of the use of plant
extracts as performance enhancers in broilers. Brazilian
Journal of Poultry Science,10: 195–204.
PLANT BIOACTIVES: A REVIEW 485
Downloaded By: [University of Aberdeen] At: 16:27 22 October 2010
ROCHFORT, S., PARKER, A.J. & DUNSHEA, F.R. (2008) Plant
bioactives for ruminant health and productivity.
Phytochemistry,69: 299–322.
SANTOSO, U., SETIANTO,J.&SUTEKY, T. (2005) Effect of
Sauropus androgynus (Katuk) extract on egg production
and lipid metabolism in layers. Asian-Australasian Journal of
Animal Sciences,18: 364–369.
SCHIAVONE, A., RIGHI, F., QUARANTELLI, A., BRUNI, R.,
SERVENTI,P.&FUSARI, A. (2007) Use of Silybum marianum
fruit extract in broiler chicken nutrition: influence on
performance and meat quality. Journal of Animal Physiology
and Animal Nutrition,91: 256–262.
SERKEDJIEVA,J.&HAY, A.J. (1998) In vitro anti-influenza virus
activity of a plant preparation from Geranium sanguineum
L. Antiviral Research,37: 121–130.
SHERRY, C.J. & HUNTER, P.S. (1979) Effect of an ethanol
extract of catnip (Nepeta cataria) on the behavior of the
young chick. Experientia,35: 237–238.
SHERRY, C.J., RAY, L.E. & HERRON, R.E. (1982) The
pharmacological effects of ligroin extract of
nutmeg (Myristica fragrans). Journal of Ethnopharmacology,
6: 61–66.
SHIRLEY, M.W., SMITH, A.L. & BLAKE, D.P. (2007) Challenges
in the successful control of the avian coccidia. Vaccine,
25: 5540–5547.
SI, W., GONG, J., TSAO, R., ZHOU, T., YU, H., POPPE, C.,
JOHNSON,R.&DU, Z. (2006) Antimicrobial activity of
essential oils and structurally related synthetic food
additives towards selected pathogenic and beneficial gut
bacteria. Journal of Applied Microbiology,100: 296–305.
SI, H.B., HU, J.Q., LIU, Z.C. & ZENG, Z.L. (2008) Antibacterial
effect of oregano essential oil alone and in combination
with antibiotics against extended-spectrum beta-lactamase-
producing Escherichia coli.Fems Immunology and Medical
Microbiology,53: 190–194.
SILVERSIDES, F.G. & LEFRANCOIS, M.R. (2005) The effect of
feeding hemp seed meal to laying hens. British Poultry
Science,46: 231–235.
SIMSEK, U.G., CIFTCI, M., DALKILIC, B., GULER,T.&ERTAS, O.N.
(2007) The effects of dietary antibiotic and anise oil
supplementation on body weight, carcass characteristics
and organoleptic analysis of meat in broilers. Revue de
Medecine Veterinaire,158: 514–518.
SIRAGUSA, G.R., HAAS, G.J., MATTHEWS, P.D., SMITH, R.J.,
BUHR, R.J., DALE, N.M. & WISE, M.G. (2008)
Antimicrobial activity of lupulone against Clostridium
perfringens in the chicken intestinal tract jejunum and
caecum. Journal of Antimicrobial Chemotherapy,61: 853–858.
SMITH-PALMER, A., STEWART,J.&FYFE, L. (1998) Antimicrobial
properties of plant essential oils and essences against five
important food-borne pathogens. Letters in Applied
Microbiology,26: 118–122.
SMITH, H.W. (1965) Development of flora of alimentary tract
in young animals. Journal of Pathology and Bacteriology,
90: 495–513.
SOKMEN, A., JONES, B.M. & ERTURK, M. (1999) The in vitro
antibacterial activity of Turkish medicinal plants. Journal
of Ethnopharmacology,67: 79–86.
SOKOMBA, E., WAMBEBE, C., CHOWDHURY, B.K., IRIAH, J.,
OGBEIDE, O.N. & ORKOR, D. (1986) Preliminary phyto-
chemical, pharmacological and antibacterial studies of the
alkaloidal extracts of the leaves of Synclisia scabrida Miers.
Journal of Ethnopharmacology,18: 173–185.
STERN, N.J., BAILEY, J.S., BLANKENSHIP, L.C., COX, N.A. &
MCHAN, F. (1988) Colonization characteristics of
Campylobacter jejuni in chick ceca. Avian Diseases,
32: 330–334.
STIPKOVITS, L., LAPIS, K., HIDVEGI, M., KOSA, E., GLAVITS,R.&
RESETAR, A. (2004) Testing the efficacy of fermented wheat
germ extract against Mycoplasma gallisepticum infection of
chickens. Poultry Science,83: 1844–1848.
STOEV, S.D., ANGUELOV, G., IVANOV,I.&PAVLOV, D. (2000)
Influence of ochratoxin A and an extract of artichoke
on the vaccinal immunity and health in broiler chicks.
Experimental and Toxicologic Pathology,52: 43–55.
SWIATKIEWICZ,S.&KORELESKI, J. (2007) Feed additives
enhancing immune responses in poultry. Medycyna
Weterynaryjna, 63.
TEDESCO, D., STEIDLER, S., GALLETTI, S., TAMENI, M.,
SONZOGNI,O.&RAVAROTTO, L. (2004) Efficacy of sily-
marin-phospholipid complex in reducing the toxicity
of aflatoxin B-1 in broiler chicks. Poultry Science,
83: 1839–1843.
TEUSCHER, E. (2003) Biogene Arzneimittel Wiss. Verl.-Ges.
Stuttgart.
TIMBERMONT, L., LANGKRIET, A., GHOLAMIANDEHKORDI, A.R.,
PASMANS, F., MARTEL, A., HAESEBROUCK, F., DUCATELLE,R.&
VAN, I.F. (2008) Origin of Clostridium perfringens isolates-
determines the ability to induce necrotic eneritis in
broilers. Comp.Immunol.Microbiol.Infect.Dis.
TOROK, V.A., OPHEL-KELLER, K., LOO,M.&HUGHES , R.J.
(2008) Application of methods for identifying broiler
chicken gut bacterial species linked with increased
energy metabolism. Applied and Environmental
Microbiology,74: 783–791.
ULTEE, A., KETS, E.P.W. & SMID, E.J. (1999) Mechanisms of
action of carvacrol on the food-borne pathogen Bacillus
cereus. Applied and Environmental Microbiology,
65: 4606–4610.
UUGANBAYAR, D., BAE, I.H., CHOI, K.S., SHIN, I.S., FIRMAN, J.D.
&Y
ANG, C.J. (2005) Effects of green tea powder on laying
performance and egg quality in laying hens. Asian-
Australasian Journal of Animal Sciences,18: 1769–1774.
UUGANBAYAR, D., SHIN, I.S. & YANG, C.J. (2006) Comparative
performance of hens fed diets containing Korean,
Japanese and Chinese green tea. Asian-Australasian
Journal of Animal Sciences,19: 1190–1196.
VAN DER WIELEN, P.W.J.J., KEUZENKAMP, D.A., LIPMAN, L.J.A.,
VAN KNAPEN,F.&BIESTERVELD, S. (2002) Spatial and
temporal variation of the intestinal bacterial community
in commercially raised broiler chickens during growth.
Microbial Ecology,44: 286–293.
VELDHUIZEN, E.J.A., TJEERDSMA-VAN BOKHOVEN, J.L.M.,
ZWEIJTZER, C., BURT, S.A. & HAAGSMAN, H.P. (2006)
Structural requirements for the antimicrobial activity
of carvacrol. Journal of Agricultural and Food Chemistry,
54: 1874–1879.
VISPO,C.&KARASOV, W.H. (1996) The interaction of avian
gut microbes and their host: an elusive symbiosis, in:
MACKIE, R.I. & WHITE, B.A. (Eds) 1st edn, pp. 116
—
155
(New York, Chapman & Hall).
WAIHENYA, R.K., MTAMBO, M.M.A., NKWENGULILA,G.&
MINGA, U.M. (2002a) Efficacy of crude extract of Aloe
secundiflora against Salmonella gallinarum in experimentally
infected free-range chickens in Tanzania. Journal of
Ethnopharmacology,97: 317–323.
WAIHENYA, R.K., MTAMBO, M.M.A. & NKWENGULILA, H. (2002b)
Evaluation of the efficacy of the crude extract of Aloe
secundiflora in chickens experimentally infected with
Newcastle disease virus. Journal of Ethnopharmacology,
79: 299–304.
WALD, C. (2002) Untersuchungen zur Wirksamkeit a¨therischer
O
¨le im Futter von Aufzuchtferkeln und Broilern. PhD Thesis.
Univ. Halle-Wittenberg, Germany.
WALDENSTEDT, L., ELWINGER, K., THEBO,P.&UGGLA, A. (1999)
Effect of betaine supplement on broiler performance
during an experimental coccidial infection. Poultry Science,
78: 182–189.
WALDENSTEDT, L., INBORR, J., HANSSON,I.&ELWINGER,K.
(2003) Effects of astaxanthin-rich algal meal (Haematococcus
pluvalis) on growth performance, caecal campylobacter
and clostridial counts and tissue astaxanthin concentration
486 R.J. WALLACE ET AL.
Downloaded By: [University of Aberdeen] At: 16:27 22 October 2010
of broiler chickens. Animal Feed Science and Technology,
108: 119–132.
WANG,J.&ZHOU, H. (2007) Comparison of the effects of
Chinese herbs, probiotics and prebiotics with those of
antibiotics in diets on the performance of meat ducks.
Journal of Animal and Feed Sciences,16: 96–103.
WANG, G.J., HAN, Z.K., CHEN,J.&CHEN, W.H. (1994) Effect of
daidzein on muscle growth in broilers and mechanism
involved. Science Technology in Animal Husbandry Veterinary
Medicine Guang Dong,19: 4–6.
WANG, M.L., SUO, X., GU, J.H., ZHANG, W.W., FANG,Q.&
WANG, X. (2008) Influence of grape seed proanthocyani-
din extract in broiler chickens: effect on chicken cocci-
diosis and antioxidant status. Poultry Science,
87: 2273–2280.
WENK, C. (2003) Herbs and botanicals as feed additives in
monogastric animals. Asian-Australasian Journal of Animal
Sciences,16: 282–289.
WESTENDARP, H., KLAUS, P., HALLE, I., MORLEIN, D.,
HENNING,M.&KOHLER, P. (2006) Effect of carvacrol,
gamma-terpinene and p-cymene-7-ol in broiler feed on
growth traits and N-metabolism. Landbauforschung
Volkenrode,56: 149–157.
WILKINSON, J.M., HIPWELL, M., RYAN,T.&CAVANAGH, H.M.A.
(2003) Bioactivity of Backhousia citriodora: antibacterial
and antifungal activity. Journal of Agricultural and Food
Chemistry,51: 76–81.
WILLIAMS, R.B. (2005) Intercurrent coccidiosis and necrotic
enteritis of chickens: rational, integrated disease manage-
ment by maintenance of gut integrity. Avian Pathology,
34: 159–180.
WILLIAMS, M.C. & OLSEN, J.D. (1984) Toxicity of Seeds of
3 Aesculus Spp to Chicks and Hamsters. American Journal
of Veterinary Research,45: 539–542.
WILSON, J., TICE, G., BRASH, M.L. & STHILAIRE, S. (2005)
Manifestations of Clostridium perfringens and related
bacterial enteritides in broiler chickens. Worlds Poultry
Science Journal,61: 435–449.
WINDISCH, W., SCHEDLE, K., PLITZNER,C.&KROISMAYR,A.
(2008) Use of phytogenic products as feed additives for
swine and poultry. Journal of Animal Science,
86: E140–E148.
YALCIN, S., ONBASILAR, I., REISLI,Z.&YALCIN, S. (2006) Effect
of garlic powder on the performance, egg traits and blood
parameters of laying hens. Journal of the Science of Food and
Agriculture,86: 1336–1339.
YALCIN, S., ONBASILAR, I., SEHU,A.&YALCIN, S. (2007) The
effects of dietary garlic powder on the performance, egg
traits and blood serum cholesterol of laying quails. Asian-
Australasian Journal of Animal Sciences,20: 944–947.
YAMAUCHI, K., BUWJOOM, T., KOGE,K.&EBASHI, T. (2006)
Histological alterations of the intestinal villi and epithelial
cells in chickens fed dietary sugar cane extract. British
Poultry Science,47: 544–553.
YANG, X.J., GUO, Y.M., WANG,Z.&NIE, W. (2006) Fatty acids
and coccidiosis: effects of dietary supplementation with
different oils on coccidiosis in chickens. Avian Pathology,
35: 373–378.
YEO,J.&KIM, K.I. (1997) Effect of feeding diets containing
an antibiotic, a probiotic, or yucca extract on growth and
intestinal urease activity in broiler chicks. Poultry Science,
76: 381–385.
YILMAZ, Y. (2006) Novel uses of catechins in foods. Trends in
Food Science & Technology,17: 64–71.
YOUDIM, K.A. & DEANS, S.G. (1999) Beneficial effects of
thyme oil on age related changes in phospholipid C20
and C22 polyunsaturated fatty acid composition of
various rat tissues. Biochimica et Biophysica Acta,
1438: 140–146.
YOUDIM, K.A. & DEANS, S.G. (2000) Effect of thyme oil and
thymol dietary supplementation on the antioxidant status
and fatty acid composition of the ageing rat brain. British
Journal of Nutrition,83: 87–93.
YOUN, H.J. & NOH, J.W. (2001) Screening of the anticoccidial
effects of herb extracts against Eimeria tenella.Veterinary
Parasitology,96: 257–263.
YUSTE, P., LONGSTAFF,M.&MCCORQUODALE, C. (1992) The
effect of proanthocyanidin-rich hulls and proanthocyani-
din extracts from bean (Vicia faba L) hulls on nutrient
digestibility and digestive enzyme-activities in young
chicks. British Journal of Nutrition,67: 57–65.
ZABIELSKI, R., LEHUEROU-LURON,I.&GUILLOTEAU, P. (1999)
Development of gastrointestinal and pancreatic functions
in mammalians (mainly bovine and porcine species):
influence of age and ingested food. Reproduction
Nutrition Development,39: 5–26.
ZENNER, L., CALLAIT, M.P., GRANIER,C.&CHAUVE, C. (2003)
In vitro effect of essential oils from Cinnamomum
aromaticum, Citrus limon and Allium sativum on two
intestinal flagellates of poultry, Tetratrichomonas gallinarum
and Histomonas meleagridis.Parasite,10: 153–157.
ZHENGKANG, H., WANG, G., YAO,W.&ZHU, W.Y. (2006)
Isoflavonic phytoestrogens
—
new prebiotics for farm
animals: a review on research in China. Current Issues in
Intestinal Microbiology,7: 53–60.
ZHU, X.Y., ZHONG, T.Y., PANDYA,Y.&JOERGER, R.D. (2002)
16S rRNA-based analysis of microbiota from the cecum of
broiler chickens. Applied and Environmental Microbiology,
68: 124–137.
PLANT BIOACTIVES: A REVIEW 487
Downloaded By: [University of Aberdeen] At: 16:27 22 October 2010
