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Options for Integrated Strategies for the Control of Avian Coccidiosis

Authors:
  • Shandong Vocational Animal Sciences and Veterinary College, Weifang, China

Abstract

Avian coccidiosis is one of the serious infectious diseases of poultry caused by different species of genus Eimeria. Though some anticoccidial vaccines are in the market with controversial efficacy, farmers mainly rely on the prophylactic and therapeutic use of chemicals for the control of avian coccidiosis. Frequent use of anticoccidial drugs, however, has resulted in the development of resistance in the Eimerian species. Increasing awareness about public health hazards associated with drug residues in food chain has also added to the constraints in using the synthetic drugs for treatment and control of diseases in animals. Therefore, there is a renewed interest in using alternatives for safe, effective and economical control of avian coccidiosis. Some of the alternatives focused in the current review include acids, vitamins, probiotics, mushrooms, amino acids, nonsteroidal anti-inflammatory agents, natural feed additives, essential oils and botanicals having anticoccidial properties. This review may, in given situations, be helpful in planning integrated control strategies for avian coccidosis. © 2012 Friends Science Publishers
INTERNATIONAL JOURNAL OF AGRICULTURE & BIOLOGY
ISSN Print: 1560–8530; ISSN Online: 1814–9596
12–317/ZIP/2012/14–6–1014–1020
http://www.fspublishers.org
Review Article
To cite this paper: Abbas, R.Z., Z. Iqbal, A. Khan, Z.U.D. Sindhu, J.A. Khan, M.N. Khan and A. Raza, 2012. Options for integrated strategies for the control
of avian coccidiosis. Int. J. Agric. Biol., 14: 10141020
Options for Integrated Strategies for the Control of Avian
Coccidiosis
RAO ZAHID ABBAS
1
, ZAFAR IQBAL, AHRAR KHAN†, ZIA-U-DIN SINDHU
1
, JUNAID ALI KHAN‡, MUHAMMAD
NISAR KHAN AND ALI RAZA
Department of Parasitology, University of Agriculture, Faisalabad-038040-Pakistan
Deprtment of Pathology, University of Agriculture, Faisalabad-038040-Pakistan
Department of Physiology and Pharmacology, University of Agriculture, Faisalabad-038040-Pakistan
Corresponding author’s e-mail: raouaf@hotmail.com
ABSTRACT
Avian coccidiosis is one of the serious infectious diseases of poultry caused by different species of genus Eimeria. Though
some anticoccidial vaccines are in the market with controversial efficacy, farmers mainly rely on the prophylactic and
therapeutic use of chemicals for the control of avian coccidiosis. Frequent use of anticoccidial drugs, however, has resulted in
the development of resistance in the Eimerian species. Increasing awareness about public health hazards associated with drug
residues in food chain has also added to the constraints in using the synthetic drugs for treatment and control of diseases in
animals. Therefore, there is a renewed interest in using alternatives for safe, effective and economical control of avian
coccidiosis. Some of the alternatives focused in the current review include acids, vitamins, probiotics, mushrooms, amino
acids, nonsteroidal anti-inflammatory agents, natural feed additives, essential oils and botanicals having anticoccidial
properties. This review may, in given situations, be helpful in planning integrated control strategies for avian coccidosis. ©
2012 Friends Science Publishers
Key Words: Anticoccidials; Alternatives; Poultry; Coccidia (or Eimeria); Coccidiosis; Drug resistance
INTRODUCTION
Commercial poultry farming is expanding day by day
and contributing in the provision of affordable and high
quality proteins (Ahmad et al., 2010; Ghafoor et al., 2010).
However, this sector is still confronted with many enteric
diseases like coccidiosis which are hindering its progress
(Saima et al., 2010; Hafez, 2011).
Avian coccidiosis in an intestinal protozoan disease
caused by various species belonging to genus Eimeria.
According to a recent estimate (Chapman, 2009), the United
States poultry industry costs about US$127 million annual
losses just because of coccidiosis and proportionally similar
losses may be faced by the poultry producers in various
parts of the world. Thus, in commercial poultry systems,
coccidiosis is thought to be the one of the most expensive
infectious diseases. Thus far, chemoprophylaxis and
anticoccidial feed additives have controlled the disease but
situation has been complicated by the emergence of drug
resistant strains against commonly used drugs (Abbas et al.,
2008; Abbas et al., 2011a).
Vaccination by using live coccidial oocysts has been
another effective approach for coccidiosis control (Shirley
& Lillehoj, 2012), but, in poorly managed production
systems particularly in case of broiler birds, live vaccines
may result in the onset of severe reactions ultimately
affecting the performance and production of flocks
(Chapman, 2000). As a result of this drawback of live
vaccines, attenuated vaccines, having reduced
pathogenicity, have been developed, but these are expensive
to produce. The other draw back of using vaccines is
diversity of Eimeria strains in different geographical
distributions. Therefore, vaccine strain, effective in one
geographical area may not be effective in the other area.
Because of development of drug resistance and
pathogenicity associated problems with live vaccines,
poultry producers all over the world are moving towards
alternative control of avian coccidiosis. Cost effective
alternative strategies are being sought for more effective and
safer control of avian coccidiosis (Abbas et al., 2011b,
2011c; Abbas et al., 2012; Arczewska-Wlosek &
Swiatkiewicz, 2012; Zaman et al., 2012) which are
discussed in the following sections.
Acids: Acids are known to have antibacterial, antifungal,
and antiprotozoal activity particularly at low pH. Many
acids like formic acid, butyric acid, anacardic acid, acetic
acid and hydrochloric acid are found effective in controlling
avian coccidiosis (Shobha & Ravindranath, 1991; Garcia et
al., 2007; Abbas et al., 2011b, c). In an experimental study,
Garcia et al. (2007) found formic acid to have positive
INTEGRATED STRATEGIES FOR THE CONTROL OF AVIAN COCCIDIOSIS / Int. J. Agric. Biol., Vol. 14, No. 6, 2012
1015
effects like increase in height of villus, depth of crypt and
surface area of villus in broiler chickens experimentally
challenged with E. tenella. The broiler growth performance
and immune response were determined by using different
doses of liquid dl-2-hydroxy-4-methylthio butanoic acid
(LMA). In an arrangement of LMA with 4 graded levels
140%, 120%, 100% and 80% of methionine, broiler
requirements were suggested by Chinese feeding standards
for chickens; humoral immunity, cellular immunity and
growth performance were determined. It was observed
(Zhang & Guo, 2008) that in broiler chickens, methionine
deficiency led to decrease in feed utilization; humoral and
nonspecific immuno-competence were also decreased.
However, use of LMA for methionine deficiency corrected
these problems.
Organic acids like acetic acid have also been reported
to have antimicrobial and anticoccidial effects (Chaveerach
et al., 2004; Van Immerseel et al., 2004; Abbas et al.,
2011b). Acetic acid is a weak organic acid which gives
vinegar and is a partially dissociated acid in an aqueous
solution. Only a few reports are available regarding the
protective effects of acetic acid against avian coccidiosis
(Abbas et al., 2011b). Organic acids showed promise in
altering bacterial activities and cecal environment in
chicken. Furthermore, a number of reports (Manickam et
al., 1994; Runho et al., 1997; Yeo & Kim, 1997; Gunes et
al., 2001; Abbas et al., 2011b) also showed the positive
effects of organic acids on performance parameters such as
weight gains and feed consumption. Recently, Abbas et al.
(2011b) has shown the anticoccidial effect of acetic acid
both in terms of improved performance (weight gain and
feed consumption ratio) and pathological parameters (lesion
scores, oocyst scores & mortality).
Some strong acids like hydrochloric acid, in low
concentrations, are also being used for the control and
treatment of avian coccidiosis (Abbas et al., 2011c).
Furthermore, the acids when used at low concentrations also
result in better performance by improving the solubility of
the feed ingredients, digestion and absorption of nutrients
but higher concentrations result in negative impact on
weight gains and feed intake (Owings et al., 1990; Adams,
1999; Vesteggh, 1999).
Anacardic acid shows antimicrobial (Himejima &
Kubo, 1991) and antitumor (Kubo et al., 1993) activities in
addition to having effective molluscicidal (Kubo et al.,
1986) effects. The feed supplementation with 0.4% cashew
nut shell oil and 0.2% anacardic acid was found to be
effective in controlling coccidial infection. Furthermore, it
was also reported that anacardic acids with four
concentrations C
15:3
, C
15:2
, C
15:1
or C
15:0
showed uncoupling
effects of alkyl side chains (similar to the classical
uncoupler 2,4-dinitrophenol) on the ADP/O ratio, state 4
and respiratory control ratio in succinate-oxidizing rat liver
mitochondria (Toyomizu et al., 2000). Considering that
proton electrochemical potential mediats the oxidative
phosphorylation, as chemiosmotic hypothesis described, in
mitochondria anacardic acids could act as ionophores and/or
as protonophores (Toyomizu et al., 2003). Anacardic acids
administration has dual effect as anticoccidial and/or anti-
inflammatory drugs due to its possible protonophores/
ionophore properties.
So far, the exact anticoccidial mode of action of acids
is not fully understood but it is thought that after entering
into the microbial cell, the acids ionize to release H
+
ions,
resulting in a decrease of intracellular pH. This influences
microbial metabolism, inhibiting the action of important
microbial enzymes and forces the cell to use energy to
export the excess of protons H
+
, ultimately resulting death
by starvation. In the same matter, the protons H
+
can
denature acid sensitive proteins and DNA of the microbial
cell (Russell & Diez-Gonzalez, 1998).
Vitamins: Vitamins play a significant role in the
development of chicken immune system and thus enabling
them to fight against various stresses (Khan et al., 2010;
Ajakaiye et al., 2011). Essential nutrients such as vitamins
may affect both humoral and cell-mediated immune
responses. Vitamin A differentiates the epithelial cells,
which is highly essential for maintaining the integrity of
mucosal surface of intestine (Chew & Park, 2004).
Deficiency of vitamin A increases the chances of enteric
diseases like coccidiosis and it also impaires the local
immune defences within the gut lymphoid tissues of broiler
chickens (Dalloul et al., 2002). Due to this effect, there was
a significant reduction in intraepithelial lymphocyte
subpopulations, mainly CD4+ T cells. The alteration in
intraepithelial lymphocyte subpopulation leads to lower the
ability of resistance against E. acervulina. Furthermore, it
was reported (Dalloul et al., 2002) that the deficiency of
vitamin A also affects the systemic immune system by
reducing the ability of splenic T lymphocytes to respond to
in vitro mitogen stimulation, which resulted in lower IFN-
gamma secretion. In fact dietary vitamin A levels can affect
gut immunity in broiler chickens, and its deficiency may
lead to immunosuppression at those sites that make the birds
more susceptible to coccidiosis.
Probiotics: Probiotics are ‘live microorganisms, which
when administrated in adequate amounts confer a health
benefit on the host’ (FAO, 2002). In poultry production,
probiotics are identified for their ability to reinstate the
intestinal microflora after being disrupted by antibiotic
treatment or enteric infections (Line et al., 1998; Pascual et
al., 1999). In addition, they are also known for their capacity
to enhance the immune system and used against allergies
and other immune diseases (Dalloul et al., 2003a, b; Kabir
et al., 2004; Koenen et al., 2004).
Recently, Lee et al. (2007a) reported the increased
resistance of birds against coccidiosis and a partial
protection against growth retardation with a Pediococcus-
based commercial probiotic (MitoGrow®). In another study,
Pediococcus and Saccharomyces-based probiotic
(MitoMax®) given to birds challenged with 5000 oocysts of
either E. acervulina or E. tenella, less oocyst shedding and a
ABBAS et al. / Int. J. Agric. Biol., Vol. 14, No. 6, 2012
1016
better antibody response was found in probiotic fed birds
compared to non-probiotic controls. These results suggest
that MitoMax® when included in the diet, may improve the
resistance against coccidiosis by enhancing the humoral
immune response in birds (Lee et al., 2007b). Furthermore,
Lactobacillus-based probiotic has optimistic influence on
cellular immunity (Dalloul et al., 2005).
Mushrooms: Mushrooms contain antibacterial and
antioxidant properties, thus, having the health-supporting
benets. Recently, Willis et al. (2007) conducted an
experiment to determine the health and growth of broiler
chicken by using the combination of probiotics (PrimaLac)
and extract of Shiitake mushroom (Lentinus edodes). The
results indicated that this combination was not effective for
weight gain but showed positive effect on health
enhancement. Furthermore, Guo et al. (2004, 2005)
explored the immunoprotective effects of polysaccharide
extracts of two mushrooms, Tremella fuciformis and
Lentinus edodes, with an herb Astragalus membranaceus in
the chickens infected with E. tenella. Both Lentinus edodes
and Astragalus membranaceus fed groups showed lower
cecal oocyst output. Likewise, it has been reported (Dalloul
et al., 2006) that a mushroom lectin (FFrL) extracted from
Fomitella fraxinea has the immuno-potentiating effect on
cell-mediated immunity and subsequent protection against
coccidiosis. As mushrooms have immunomodulatory
activity, they can be used as effective growth promoting and
immunostimulating agents in poultry.
Nonsteroidal anti-inflammatory drugs: The use of
nonsteroidal anti-inflammatory drugs may be another
effective approach for the control and treatment of avian
coccidiosis but so far a very limited work has been done on
this aspect. Ibuprofen is a nonsteroidal anti-inflammatory
drug which inhibits the biosynthesis of prostaglandins with
pro-inflammatory and immunosuppressive properties and is
therefore proposed as a candidate molecule for the treatment
of coccidiosis in broiler chickens (Vermeulen et al., 2004).
A number of trials were performed to find out the
anticoccidial activity of Ibuprofen. In all experiments,
Ibuprofen was administered via drinking water and it was
found that coccidial lesion scores and oocyst shedding were
reduced when Ibuprofen was provided at a dose of 100
mg/kg body weight. However, at this dose, Ibuprofen did
not show any significant effect on the degree of sporulation
and infectivity of E. acervulina oocysts.
Natural feed stuffs: The use of natural feed additives has
also been reported to provide protection against coccidiosis.
Among natural products, fat rich diets such as fish oils,
flaxseed and its oil, when fed to chickens from first day of
age, are effective to control caecal coccidiosis (Allen et al.,
1996a). Fat diets are a rich source of n-3 fatty acids (n-3
FA). Allen et al. (1996b) showed that n-3 FA rich diets (fish
oil & flaxseed oil diets) significantly reduced the
development of both sexual and asexual stages of E. tenella,
characterized by cytoplasmic vacuolization,
chromatin
condensation within the nucleus, and lack of
parasitophorous
vacuole delineation (Danforth et al., 1997).
Later, these findings were confirmed by the same effect of
n-3 FA diets on other parasites (Allen et al., 1998). These
diets (n-3 FA diets) are detrimental for the development of
parasite because of inducing oxidative
stress (due to the high
concentration of easily oxidized double
bonds). Therefore,
the anticoccidial effect of n-3 FA against caecal coccidiosis
(E. tenalla) is directly related to the concentrations
of double
bonds in n-3 FA ethyl esters
(Allen & Danforth, 1998).
However, n-3 FA diets are particularly effective against E.
tenella because the developmental stages, sporulated
oocysts and sporozoites, of this Eimeria spp. are deficient in
superoxide dismutase enzyme, which would
protect them
from reactive oxygen damage. Allen et al. (2000) further
supported the oxidative-stress hypothesis and observed that
the antioxidant-stabilized diets supplemented with up
to
10% flaxseed could not protect against E. tenella. Sources
of fats, such as n-3 FA, can be used in combination of
anticoccidial drugs or vaccines for the effective control of E.
tenella. But further research is needed to explore the
knowledge about the missing information about their mode
of action and immunomodulatory effects.
Glycine betaine or betaine is extensively originated in
nature and has been in use as anticoccidial agent in broiler
chickens (Boch et al., 1994). The cells are protected from
osmotic stress by betain accumulation and permit them to
carry on activities of regular metabolism, in situations that
would generally deactivate the cell (Petronini et al., 1992;
Ko et al., 1994). In avian species coccidia is related with an
enteric disease, and ionic and osmotic disorders are
associated with this disease (Virtanen, 1995). These
disorders may be worsened by using ionophorous
anticoccidial drugs (Virtanen, 1995). Betaine, because of its
osmoprotectant effects against osmotic stress, stabilizes cell
membranes and thus enabling the maintenance of osmotic
pressure in cells and ultimately maintain and ensure normal
metabolic activity (Ko et al., 1994). Because of this
osmoprotection, a number of studies (Augustine et al.,
1997; Allen et al., 1998; Fetter et al., 2003) have been
conducted to find out protection against avian coccidiosis.
Betain showed not only intestinal protection against
coccidiosis but also showed improved weight gains.
However, to get maximum protection, authors suggested to
use betain in combination with anticoccidial drugs.
Essential oils: Essential oils (EOs) are the combination of
fragrant, volatile compounds, named after the aromatic
characteristics of plant materials from which they are
isolated (Oyen & Dung, 1999). EOs have been reported to
have immunomodulatory effects that play a vital role in
treating infectious diseases, especially when these oils have
no adverse effect on the host (Awaad et al., 2010). Most of
the EOs inhibit nitric oxide production in macrophages (de
Oliveira Mendes et al., 2003). Nitric oxide is a potent
intracellular parasite killing mechanism in macrophages and
it is well known fact that macrophages are pivotal in the
innate immune response (Dogdan, 2001). Oregano EOs
INTEGRATED STRATEGIES FOR THE CONTROL OF AVIAN COCCIDIOSIS / Int. J. Agric. Biol., Vol. 14, No. 6, 2012
1017
have shown an antioccidial effect both in terms of better
production (weight gain & feed conversion ratio) and
reduced pathogenic effects (mortality, lesion scores, oocyst
excretion) against experimentally induced E. tenella
infection in broiler chickens (Giannesnas et al., 2003). But,
this anticoccidial effect was lower as compared to
commercial anticoccidial drug ‘laslalocid’. However, in
another study (da Silva et al., 2009), the anticoccidial effect
of Oregano EOs was similar to anticoccidial effect exerted
by ionophores antibiotics. Later, Oregano EOs were used in
combination with some other plants EOs and extracts. This
combined use of Oregano EOs increased the spectrum of
their activity against both bacteria and Eimeria species
(Bona et al., 2012). The effect of EOs on improvement in
feed effeciency and ultimately better weight gains could be
attributed to their positive effects on nutrient digestibility
(Hernandez et al., 2004; Jamroz et al., 2005).
The carvacrol and thymol compounds, the primary
components of Oregano EOs, are thought to impart
anticoccidial activity by maintaining the intestinal integrity
(Greathead & Kamel, 2006; da Silva et al., 2009).
Prebiotics: Prebiotic is a non digestible food ingredient that
beneficially affects the host by selectively stimulating the
growth and/or activity of one or a limited number of
bacteria in colon, and thus improves host health (Gibson &
Roberfroid, 1995). The positive influence of prebiotics on
the intestinal flora has been confirmed by a number of
studies (Van Loo et al., 1999). Mannanoligosaccharides
(MOS), derived from the cell wall of the yeast
Saccharomyces cerevisae, are widely used as prebiotics to
promote gastrointestinal health and performance. Mode of
action of MOS is thought to block the binding of pathogens
to mannan receptors on the mucosal surface and stimulate
the immune response (Spring et al., 2000). In poultry, MOS
enhance the development of Bifidobacteria spp. and
Lactobacillus spp. in the intestinal tract of young chickens
and suppress the number of enterobacteriacea members
(Fernandez et al., 2002). Dietary MOS (1 g/kg feed) were
found effective against, artificially induced, light infection
of E. tenella (Elmusharaf et al., 2006). Later on, it was also
observed that a dietary supplementation of MOS, at a
concentration of 10 g/kg feed, reduced the oocyst excretion
and diminished the severity of lesions caused by E.
acervulina. But this anticoccidial effect was also observed
against light infection induced by subclinical doses of
sporulated oocysts (Elmusharaf et al., 2007). However,
further research is required to validate whether MOS has
anticoccidial activity when used at higher concentrations in
feed in combination with higher challenge doses.
Botanicals: Recently, research on botanicals is getting great
attention for the control and treatment of enteric diseases
caused by both microbes and parasites (Alawa et al., 2010;
Jung et al., 2011; Badar et al., 2011). Several poultry
scientists all over the world are also actively engaged in
research into the use of plants and plant derived products to
fight and reduce the heavy economic losses in poultry
industry caused by coccidiosis. Recently, Abbas et al.
(2012) has provided an excellent review on the anticoccidial
effects of various botanicals, herbal complexes and
commercially available botanical products, against avian
coccidiosis, along with their doses, active compounds, and
mechanism of action. A number of botanicals were
discussed but the candidate plants with anticoccidial
properties include Aloe spps. (Marizvikuru et al., 2006; Yim
et al., 2011), Artemisia spp. (Allen et al., 1998; Arab et al.,
2006; Brisibe et al., 2008; de Almeida et al., 2012),
Azadirachta indica (Tipu et al., 2002; Abbas et al., 2006;
Biu et al., 2006; Toulah et al., 2010), Beta vulgaris (Ko et
al., 1994; Augustine et al., 1997; Kettunen et al., 2001;
Klasing et al., 2002), Camellia sinensis (Jang et al., 2007);
Curcuma longa (Allen et al., 1998; Abbas et al., 2010;
Khalafalla et al., 2011), Echinacea purpure (Allen, 2003),
Origanum vulgare (Giannesnas et al., 2003), Saccharum
officinarum (El-Abasy et al., 2003), Triticum aestivum
(Allen et al., 1998) and Yucca schidigera (Alfaro et al.,
2007). Most recently an herbal complex containing Allium
sativum, Salvia officinalis, Echinacea purpurea, Thymus
vulgaris and Origanum vulgare has also been found
effective against many species of Eimeria, in broiler
chickens, in terms of reducing oocyst output (Arczewska-
Wlosek & Swiatkiewicz, 2012).
Most of the above mentioned plants have been
reported to have antioxidant compounds like saponins,
flavonoids, papaine, n-3 fatty acids, vernoside and tannins,
and therefore may be lethal to the parasites by inducing
oxidative stress.
Integrated coccidiosis control program: It is clear from
the scientific literature that rapidly increasing problem of
drug resistance and treatment failure will give rise to use
of alternative control strategies in an integrated avian
coccidiosis control program in future. Integrated control
refers to the intelligent use of alternative control methods
like; use of botanicals, vaccine, pre- and pro-biotics and
immunemodulatory compounds in order to minimize the
use of chemical compounds. In case of avian coccidiosis,
alternation of drugs has been practiced with vaccines for
many years. The suggestion that vaccination be combined
with chemotherapy is not new, but efforts have not been
made to develop an integrated control program by
adopting other alternatives as well. Plant, bacterial, and
other substances claimed to alleviate coccidiosis either
directly or indirectly by improving health and immune
status have been evaluated individually. So far, there is no
data available on integration of these strategies into one
coccidiosis control program. The future research in the
area of botanicals and alternative control strategies should
be focused on integration of already proven alternatives
into an effective control program so that farmer could
control coccidiosis in an effective manner with minimal
use of drugs.
ABBAS et al. / Int. J. Agric. Biol., Vol. 14, No. 6, 2012
1018
CONCLUSION
In the face of development of drug resistance almost all
over the world and drug residues in food, there is an urgent
need to take a shift towards alternative ways for the effective
and long term control of avian coccidiosis. Using
alternatives, mentioned in this review, provide a novel
approach for controlling wide spread drug resistant Eimeria
strains in intensive poultry production systems. Most of the
alternates enhance the immunity of the birds and thus could
play a vital role to minimize or eliminate the burden of
anticoccidial chemotherapeutic agents in poultry production.
Integration of the alternates proposed above for the treatment
and control of avian coccidioisis may be one of the viable
options. However, there is need of large scale experimental
trials to establish the efficacy of alternative agents because
most of these studies lack the sufficient replication, proper
experimental designing and appropriate controls.
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(Received 23 June 2012; Accepted 01 October 2012)
... These findings supported those of Farag and Alagawany [33]. The ability of the employed APS to reduce the infectivity of the subjected oocysts has repeatedly been highlighted by several writers, including Shahrajabian et al. [39] and Abbas et al. [39], as a sure sign of the effectiveness of therapy and control of the coccidiosis disease. APS, Astragalus polysaccharides. ...
... These findings supported those of Farag and Alagawany [33]. The ability of the employed APS to reduce the infectivity of the subjected oocysts has repeatedly been highlighted by several writers, including Shahrajabian et al. [39] and Abbas et al. [39], as a sure sign of the effectiveness of therapy and control of the coccidiosis disease. APS, Astragalus polysaccharides. ...
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... The essential oils of different botanicals such as Trachyspermum ammi, Origanum vulgare and many others are known for their immunomodulatory effects against parasites by stimulation of mucosal immunity and also known to enhance cellular and humoral immunity against coccidiosis. They are involved in immune stimulation, enhancement by macrophage activity and enhancing antibodies level in infected birds (Abbas et al. 2012a(Abbas et al. , 2012b(Abbas et al. , 2017. ...
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