INTERNATIONAL JOURNAL OF AGRICULTURE & BIOLOGY
ISSN Print: 1560–8530; ISSN Online: 1814–9596
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: 1014‒1020
Options for Integrated Strategies for the Control of Avian
RAO ZAHID ABBAS
, ZAFAR IQBAL, AHRAR KHAN†, ZIA-U-DIN SINDHU
, 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: email@example.com
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
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
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
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
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/
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
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
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
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
beneﬁts. 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,
condensation within the nucleus, and lack of
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
the anticoccidial effect of n-3 FA against caecal coccidiosis
(E. tenalla) is directly related to the concentrations
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
from reactive oxygen damage. Allen et al. (2000) further
supported the oxidative-stress hypothesis and observed that
the antioxidant-stabilized diets supplemented with up
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
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
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
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.
Abbas, R.Z., Z. Iqbal, M.S. Akhtar, M.N. Khan, A. Jabbar and Z. Sandhu,
2006. Anticoccidial screening of Azadirachta indica (Neem) in
broilers. Pharmacol. Online., 3: 365–371
Abbas, R.Z., Z. Iqbal, Z.D. Sindhu, M.N. Khan and M. Arshad, 2008.
Identification of cross resistance and multiple resistance in Eimeria
tenella field isolates to commonly used anticoccidials in Pakistan. J.
Appl. Poult. Res., 17: 361–368
Abbas, R.Z., Z. Iqbal, M.N. Khan, M.A. Zafar and M.A. Zia, 2010.
Anticoccidial activity of Curcuma longa L. in Broiler Chickens.
Brazil Arch. Biol. Technol., 53: 63–67
Abbas, R.Z., Z. Iqbal, D. Blake, M.N. Khan and M.K. Saleemi, 2011a.
Anticoccidial drug resistance in fowl coccidia: the state of play
revisited. World's Poult. Sci. J., 67: 337–350
Abbas, R.Z., S.H. Munawar, Z. Manzoor, Z. Iqbal, M.N. Khan, M.K.
Saleemi, M.Z. Zia and A. Yousaf, 2011b. Anticoccidial effects of
acetic acid on performance and pathogenic parameters in broiler
chickens challenged with Eimeria tenella. Pes. Vet. Brasil., 31: 99–
Abbas, R.Z., Z. Manzoor, S.H. Munawar, Z. Iqbal, M.N. Khan, M.K.
Saleemi, M.Z. Zia and A. Yousaf, 2011c. Anticoccidial activity of
hydrochloric acid (HCl) against Eimeria tenella in broiler chickens.
Pes. Vet. Brasil., 31: 425–429
Abbas, R.Z., D. Colwell and J. Gilleard, 2012. Botanicals: an alternative
approach for the control of avian coccidiosis. Worlds Poult. Sci. J.,
Adams, C., 1999. Poultry and dietary acids. Anim. Feed, 20: 14–19
Ahmad, F., Ahsan-ul-Haq, M. Ashraf, G. Abbas and M.Z. Siddiqui, 2011.
Effect of Different Light Intensities on the Production Performance
of Broiler Chickens. Pakistan Vet. J., 31: 203–206
Ajakaiye, J.J., M. Cuesta-Mazorra and J.R. Garcia-Diaz, 2011. Vitamins C
and E can alleviate adverse effects of heat stress on live weight and
some egg quality profiles of layer hens. Pakistan Vet. J., 31: 45–49
Alawa, C.B.I., A.M. Adamu, J.O. Gefu, O.J. Ajanusi, P.A. Abdu and N.P.
Chiezey, 2010. In vivo Efficacy of Vernonia amygdalina
(Compositae) Against Natural Helminth Infection in Bunaji (Bos
indicus) Calves. Pakistan Vet. J., 30: 215–218
Alfaro, D.M., A.V.F. Silva, S.A. Borges, F.A. Maiorka, S. Vargas and E.
Santin, 2007. Use of Yucca schidigera extract in broiler diets and its
effects on performance results obtained with different coccidiosis
control methods. J. Appl. Poult. Res., 16: 248–254
Allen, P.C, H.D. Danforth and O.A. Levander, 1996a. Diets high in n-3
fatty acids reduces caecal lesion scores in broiler chickens infected
Eimeria tenella. Poult. Sci., 75: 179–185
Allen, P.C., H.D. Danforth and P.A. Stitt, 2000. Effects of nutritionally
balanced and stabilized flaxmeal-based diets on Eimeria tenella
infections in chickens. Poult. Sci., 79: 489–492
Allen, P.C., H.D. Danforth, V.L. Morris and O.A. Levander, 1996b.
Association of lowered plasma carotenoids with protection against
cecal coccidiosis by diets high in n-3 fatty acids. Poult. Sci., 75: 966–
Allen, P.C. and H.D. Danforth, 1998. Effects of dietary supplementation
with n-3 fatty acid ethyl esters on coccidiosis in chickens. Poult. Sci.,
Allen, P.C., H.D. Danforth and P.C. Augustine, 1998. Dietary modulation
of avian coccidiosis. Int. J. Parasitol., 28: 1131–1140
Allen, P.C., 2003. Dietary supplementation with Echinacea and
development of immunity to challenge infection with coccidia.
Parasitol. Res., 91: 74–78
Arab, H.A., S. Rahbari, A. Rassouli, M.H. Moslemi and F. Khosravirad,
2006. Determination of artemisinin in Artemisia sieberi and
anticoccidial effects of the plant extract in broiler chicken. Trop.
Anim. Health Prod., 38: 497–503
Arczewska-Wlosek, A. and S. Swiatkiewicz, 2012. The effect of a dietary
herbal extract blend on the performance of broilers challenged with
Eimeria oocysts. J. Anim. Feed Sci., 21: 133–142
Augustine, P.C., J.L. McNaughton, E. Virtanen and L. Rosi, 1997. Effect of
betaine on the growth performance of chicks inoculated with mixed
cultures of avian Eimeria species and on invasion and development
of Eimeria tenella and Eimeria acervulina in-vitro and in-vivo.
Poult. Sci., 76: 802–809
Awaad, M.H.H., G.A. Abdel-Alim, K.S.S. Sayed Kawkab, A. Ahmed, A.A.
Nada, A.S.Z. Metwalli and A.N. Alkhalaf, 2010. Immunostimulant
effects of essential oils of peppermint and eucalyptus in chickens.
Pakistan Vet. J., 30: 61–66
Badar, N., Z. Iqbal, M.N. Khan and M.S. Akhtar, 2011. In Vitro and In
Vivo Anthelmintic Activity of Acacia nilotica (L.) Willd. Ex Delile
Bark and Leaves. Pakistan Vet. J., 31: 185–191
Biu, A.A., S.D. Yusuf and J.S. Rabo, 2006. Use of neem (Azadirachta
indica) aqueous extract as a treatment for poultry coccidiosis in
Borno State, Nigeria. African Scientist, 7: 147–153
Boch, J., B. Kempf and E. Bremer, 1994. Osmoregulation in Bacillus
subtilis: Synthesis of the osmoprotectant glycine betaine from
exogenously provided choline. J. Bacteriol., 176: 5364–5371
Bona, T.D.M.M., L. Pickler, L.B. Miglino, L.N. Kuritza, S.P. Vasconcelos
and E. Santin, 2012. Oregano, rosemery, cinnamon essential oil and
pepper extract to control Salmonella, Eimeria and Clostridium in
broiler chickens Source: Pesq. Vet. Brasil., 32: 411–418
Brisibe, E.A., E.U. Umoren, P.U. OWAI and F. Brisibe, 2008. Dietary
inclusion of dried Artemisia annua leaves for management of
coccidiosis and growth enhancement in chickens. African J.
Biotechnol., 7: 4083–4092
Chapman, H.D., 2000. Practical use of vaccines for the control of
coccidiosis in the chicken. World's Poult. Sci. J., 56: 7–20
Chapman, H.D., 2009. A landmark contribution to poultry science –
prophylactic control of coccidiosis in poultry. Poult. Sci., 88: 813–815
Chaveerach, P., L.J.A. Lipman and F. van Knapen, 2004. Antagonistic
activities of several bacteria on in vitro growth of 10 strains of
campylobacter jejuni/coli. Int. J. Food Microbiol., 90: 43–50
Chew, B.P. and J.S. Park, 2004. Carotenoid action on the immune response.
J. Nutrition, 134: 257–261
da Silva, M.A., B.M. de Sousa Pessotti, S.F. Zanini, G.L. Colnago, M.R.A.
Rodrigues, L. de Carvalho Nunes, M.S. Zanini and I.V.F. Martins,
2009. Intestinal mucosa structure of broiler chickens infected
experimentally with Eimeria tenella and treated with essential oil of
oregano. Ciência Rural, Santa Maria, 39: 1471–1477
Dalloul, R.A., H.S. Lillehoj, J.S. Lee, S.H. Lee and K.S. Chung, 2006.
Immunopotentiating effect of a Fomitella fraxinea-derived lectin on
chicken immunity and resistance to coccidiosis. Poult. Sci., 85: 446–
Dalloul, R.A., H.S. Lillehoj, N.M. Tamim, T.A. Shellem and J.A. Doerr,
2005. Induction of local protective immunity to Eimeria acervulina
by a Lactobacillus-based probiotic. Comparative Immunology,
Microbiol. Infec. Dis., 28: 351–361
INTEGRATED STRATEGIES FOR THE CONTROL OF AVIAN COCCIDIOSIS / Int. J. Agric. Biol., Vol. 14, No. 6, 2012
Dalloul, R.A., H.S. Lillehoj, T.A. Shellem and J.A. Doerr, 2002. Effect of
vitamin A deficiency on host intestinal immune response to Eimeria
acervulina in broiler chickens. Poult. Sci., 81: 1509–1515
Dalloul, R.A., H.S. Lillehoj, T.A. Shellum and J.A. Doerr, 2003a. Intestinal
immunomodulation by vitamin A deficiency and lactobacillus-based
probiotic in Eimeria acervulina infected broiler chickens. Avian Dis.,
Dalloul, R.A., H.S. Lillehoj, T.A. Shellum and J.A. Doerr, 2003b. Enhanced
mucosal immunity against Eimeria acervulina in broilers fed a
Lactobacillus-based probiotic. Poult. Sci., 82: 62–66
Danforth, H.D., P.C. Allen and O.A. Levander, 1997. The effect of high n-
3 fatty acid diets on the ultrastructural development of E. tenella.
Parasitol. Res., 83: 440–444
de Almeida, G.F., K. Horsted, S.M. Thamsborg, N.C. Kyvsgaard, J.F.S.
Ferreira and J.E. Hermansen, 2012. Use of Artemisia annua as a
natural coccidiostat in free-range broilers and its effects on
infection dynamics and performance Source. Vet. Parasitol., 186:
de Oliveira Mendes, S.T., A.P. Ribeiro Sobrinho, A.T. de Carvalho, M.I. de
Souza Côrtes and L.Q. Vieira 2003. In vitro evaluation of the
cytotoxicity of two root canal sealers on macrophage activity. J.
Endod., 29: 95–99
Dogdan, C., 2001. Nitric oxide and the immune response. Nat. Immunol., 2:
El-Abasy, M., M. Motobu, K.J. NA, K. Shimura, K. Nakamura, K. Koge,
T. Onodera and Y. Hirota, 2003. Protective effects of sugar cane
extracts (SCE) on Eimeria tenella infection in chickens. J. Vet. Med.
Sci., 65: 865–871
Elmusharaf, M.A., V. Bautista, L. Nollet and A.C. Beynen, 2006. Effect of
a mannanoligosaccharide preparation on Eimeria tenella infection in
broiler chickens. Int. J. Poult. Sci., 5: 583–588
Elmusharaf, M.A., H.W. Peek, L. Nollet and A.C. Beynen, 2007. The effect
of and in-feed mannaoligosaccharide preparation (MOS) on a
coccidiosis infection in broilers. Anim. Feed Sci. Technol., 134: 347–
Fernandez, F., M. Hinton and B. VanGils, 2002. Dietary
mannanoligosaccharide and their effect on chicken caecal microflora
in relation to Salmonella enteritidis colonization. Avian Pathol., 31:
Fetter, R., H. Augustine, P.C. Allen and R.C. Barfield, 2003. The effects
of dietary betaine on intestinal and plama levels of betaine in
unifected and coccidia-infected broiler chicks. Parasitol. Res., 90:
Food and Agriculture Organization of the United Nations (FAO). 2002.
Guidelines for the Evaluation of Probiotics in Food.
Garcia, V., P. Catala-Gregori, F. Hernandez, M.D. Megias and J. Madrid,
2007. Effect of formic acid and plant extracts on growth, nutrient
digestibility, intestine mucosa, morphology, and meat yield of
broilers. J. Appl. Poult. Res., 16: 555–562
Ghafoor, A., H. Badar, N. Hussain and N. Tariq, 2010. An empirical
estimation of the factors affecting demand and supply of poultry
meat. Pakistan Vet. J., 30: 172–174
Gibson, G.R. and M. Roberfroid, 1995. Dietary modulation of the human
colonic microbiota: introducing the concept of prebiotics. J. Nut.,
Giannesnas, P.M., M. Florou-Paneri, E. Papazahariadou, E. Christaki, N.A.
Botsoglou and A.B. Spais, 2003. Effect of dietary supplementation
with oregano essential oil on performance of broilers after
experimental infection with Eimeria tenella. Arch. Anim. Nut., 57:
Greathead, H. and C. Kamel, 2006. Encapsulated plant extracts to fight
coccidiosis. Feed Mix., 14: 18–21
Gunes, H., H. Cerit and A. Altinel, 2001. Etlik piliçlerin verim özellikleri
üzerine pre-probiotigin (Fermacto-500) etkisi. 1
Univ. Vet. Fak.
Derg., 27: 217–229
Guo, F.C., R.P. Kwakkel, B.A. Williams, H.K. Parmentier, J. Liwk, Z.Q.
Yang and M.W.A. Verstegen, 2004. Effects of mushroom and herb
polysaccharides on cellular and humoral immune responses of
Eimeria tenella infected chickens. Poult. Sci., 83: 1124–1132
Guo, F.C., R.P. Kwakkel, B.A. Williams, X. Suo, W.K. Li and M.W.
Verstegen, 2005. Coccidiosis immunization: Effects of mushroom
and herb polysaccharides on immune responses of chickens infected
with Eimeria tenella. Avian Dis., 49: 70–73
Hafez, H.M., 2011. Enteric Diseases of Poultry with Special Attention to
Clostridium perfringens. Pakistan Vet. J., 31: 175–184
Hernandez, F., J. Madrid, V. Garcia, J. Orengo and M.D. Megias, 2004.
Influence of two plant extracts on broiler performance, digestibility,
and digestive organ size. Poult. Sci., 83: 169–174
Himejima, M. and I. Kubo, 1991. Antibacterial agents from the cashew
Anacardium occidentales (Anacardiaceae) nut shell oil. J. Agic.
Food Chem., 39: 418–421
Jamroz, D., A. Wiliczkiewicz, T. Werteleck, J. Orda and J. Sukorupinska,
2005. Use of active substances of plant origin in chicken diets based
maize and locally grown cereals. British Poult. Sci., 46:
Jang, S.I., J. Moo-Hyung, S. Hyun, H.S. Lillehoj, A. Rami, R.A. Dalloul, K.
Il-Keun, K. Suk and M. Wongi, 2007. Anticoccidial effect of green
tea-based diets against Eimeria maxima. Vet. Parasitol., 144: 172–
Jung, W., C. Chun-Nam, L. Yeo-Eun, Y. Chang-Yeol, P. Eun-Kee, K. Suk
and L. Hu-Jang, 2011. Anti-diarrheal effects of a combination of
korean traditional herbal extracts and dioctahedral smectite on piglet
diarrhea caused by Escherichia coli and Salmonella typhimurium.
Pakistan Vet. J., 31: 336–340
Kabir, S.M.L., M.M. Rahman, M.B. Rahman, M.M. Rahman and S.U.
Ahmed, 2004. The dynamics of probiotics on growth performance
and immune response in broilers. Int. J. Poult. Sci., 3: 361–364
Kettunen, H., K. Tiihonen, S. Peuranen, M.T. Saarinen and J.C. Remus,
2001. Dietary betaine accumulates in the liver and intestinal
epithelium structure in healthy and coccidian infected broiler
chickens. Comp. Biochem. Physiol., 130: 759–769
Khalafalla, R.E. U. Muller, M. Shahiduzzaman, V. Dyachenko, A.Y.
Desouky, G. Alber and A. Daugschies, 2011. Effects of curcumin
(diferuloylmethane) on Eimeria tenella sporozoites in vitro.
Parasitol. Res., 108: 879–886
Khan, W.A., M.Z. Khan, A. Khan and I. Hussain, 2010. Pathological effects
of aflatoxin and their amelioration by vitamin E in White Leghorn
layers. Pakistan Vet. J., 30: 155–162
Klasing, K.C., K.L. Adler, J.C. Remus and C.C. Calvert, 2002. Dietary
betaine increases intraepithelial lymphocytes in the duodenum of
coccidial-infected chicks and increases functional properties of
phagocytes. J. Nut., 132: 2274–2282
Ko, R., L.T. Smith and G.M. Smith, 1994. Glycine betaine confers
enhanced osmotolerance and cryotolerance on Listeria
monocytogenes. J. Bacteriol., 176: 426–431
Koenen, M.E., J. Kramer, R. van der Hulst, L. Heres, S.H.M. Jeurissen and
W.J.A. Boersma, 2004. Immunomodulation by probiotic lactobacilli
in layer and meat-type chickens. British Poult. Sci., 45: 355–366
Kubo, I., M. Ochi, P.C. Vieira and S. Komatsu, 1993. Antitumor agents
from the cashew (Anacardium occidentale) apple juice. J. Agricult.
Food Chem., 41: 1021–1015
Kubo, I., S. Komatsu and M. Ochi, 1986. Molluscicides from the cashew
Anacardium occidentale and their large-scale isolation. J. Agric.
Food Chem., 34: 970–973
Lee, S.H., H.S. Lillehoj, R.A. Dalloul, D.W. Park, Y.H. Hong and J.J. Lin,
2007a. Influence of Pediococcus-based probiotic on coccidiosis in
broiler chickens. Poult. Sci., 86: 63–66
Lee, S.H., H.S. Lillehoj, D.W. Park, Y.H. Hong and J.J. Lin, (2007b).
Effects of Pediococcus-based probiotic (MitoMax®) on coccidiosis
in broiler chickens. Comp. Immunol. Microbiol. Inf. Dis., 30: 261
Line, E.J., S.J. Bailey, N.A. Cox, N.J. Stern and T. Tompkins, 1998. Effect
of yeast-supplemented feed on Salmonella and Campylobacter
populations in broilers. Poult. Sci., 77: 405–410
Manickam, R., K. Viswanathan and M. Mohan, 1994. Effect of probiotics
in broiler performance. Indian Vet. J
., 71: 737–739
Marizvikuru, M., B. Evison, C. Michael and E.H. Tinyiko, 2006. The in
vitro studies on the effect of Aloe vera ((L.) Webb. & Berth.) and
Aloe spicata (L.f.) on the control of coccidiosis in chickens. Int. J.
Appl. Res. Vet. Med., 4: 128–133
ABBAS et al. / Int. J. Agric. Biol., Vol. 14, No. 6, 2012
Owings, W.J., D.L. Reynolds, R.J. Hasiak and P.R. Ferket, 1990. Influence
of dietary supplementation with Streptococcus faecium M-74 on
broiler body weight feed conversion; carcass characteristics and
intestinal microbial colonisation. Poult. Sci., 69: 1257–1264
Oyen, L.P.A. and N.X. Dung, 1999. In: Oyen, L.P.A. and N.X. Dung (eds.),
Essential Oil Plants. Backhuys Publishers, Leiden
Pascual, M., M. Hugas, J.I. Badiola, J.M. Monfort and M. Garriga, 1999.
Lactobacillus salivarius CTC2197 prevents Salmonella enteritidis
colonization in chickens. Appl. Environ. Microbiol., 65: 4981–4986
Petronini, P.G., E.M. DeAngelis, P. Borghetti and A.F. Borghetti, 1992.
Modulation by betaine of cellular responses to osmotic stress. J.
Biochem., 282: 69–73
Runho, R.C., N.K. Sakomura, S. Kuana, D. Banzatto, O.M. Junqueira and
J.H. Stringhini, 1997. Use of an organic acid (fumaric acid) in broiler
rations. Revta Bras. Zootec., 26: 1183–1191
Russell, J.B. and F. Diaz-Gonzales, 1998. The effects of fermentation acids
on bacterial growth. Adv. Microbiol. Physiol., 39: 205–234
Saima, M.Z.U.K., M.A. Jabbar, A. Mehmud, M.M. Abbas and A. Mahmood,
2010. Effect of lysine supplementation in low protein diets on the
performance of growing broilers. Pakistan Vet. J., 30: 17–20
Shirley, M.W. and H.S. Lillehoj, 2012. The long view: a selective review of
40 years of coccidiosis research. Avian Pathol., 41: 111–121
Shobha, S.V. and B. Ravindranath, 1991. Supercritical carbon dioxide and
solvent extraction of the phenolic lipids of cashew nut (Anacardium
occidentale) shells. J. Agric. Food Chem., 39: 2214–2217
Spring, P., C. Wenk, K.A. Dawson and K.E. Newman, 2000. The effects of
dietary mannanoligosaccharides on the cecal parameters and
concentration of enteric bacteria in the caecal of salmonella-
challenged broiler chicks. Poult. Sci., 79: 205–211
Tipu, M.A., T.N. Pasha and Z. Ali, 2002. Comperative efficacy of
salinomycin sodium and Neem fruit (Azadirachta indica) as feed
additives anticoccidials in broilers. Int. J. Poult. Sci., 1: 91–93
Toulah, F.H., H.A. Ismeel and S. Khan, 2010. Effect of treatment with
Neem (Azadirachta indica) compared with Baycox drug on the
caecum of chicken experimentally infected with Eimeria tenella. J.
Egypt Soc. Parasitol., 40: 93–106
Toyomizu, M., K. Okamoto, T. Ishibashi, Z. Chen and T. Nakatsu, 2000.
Uncoupling effect of anacardic acids form cashew nut shell oil on
oxidative phosphorylation of rat liver mitochondria. Life Sci., 66:
Toyomizu, M., Y. Nakai, T. Nakatsu and Y. Akiba, 2003. Inhibitory effect
of dietary anacardic acid supplementation on cecal lesion formation
following chicken coccidial infection. Anim. Sci. J., 74: 105–109
Van Immerseel, F., J. de Buck, F. Boyen, L. Bohez, F. Pasmans, J. Volf, M.
Sevcik, I. Rychlik, F. Haesebrouck and R. Ducatelle, 2004. Medium-
chain fatty acids decrease colonization and invasion through hilA
suppression shortly after infection of chickens with Salmonella
enterica serovar Enteritidis. Appl. Environ. Microbiol
., 70: 3582–
Van Loo, J., J. Cummings, N. Delzenne, H. Englyst, A. Franck, M.
Hopkins, N. Kok, G. Macfarlane, D. Newton, M. Quigley, M.
Roberfroid, T. van Vliet and E. van den Heuvel, 1999. Functional
food properties of non-digestible oligosaccharides; a consensus
report from the ENDO project (DGXII AIRII-CT94-1095). British J.
Nut., 2: 121–132
Vermeulen, B., H.W. Peek, J.P. Remon and W.J. Landman, 2004. Effect of
ibuprofen on coccidiosis in broiler chickens. Avian Dis., 48: 68–76
Vesteggh, H.A.J. 1999. Lactic acid has positive effect on broiler
performance. World Poult., 8: 16–17
Virtanen, E., 1995. Piecing together the betaine puzzle. Feed Mix., 3: 12–17
Willis, W.L., O.S. Isikhuemhen and S.A. Ibrahim, 2007. Performance
assessment of broiler chickens given mushroom extract alone or in
combination with probiotics. Poult. Sci., 86: 1856–1860
Yeo, J. and K. Kim, 1997. Effect of feeding diets containing an antibiotic, a
probiotic or yucca extract on growth and intestinal urease activity in
broiler chicks. Poult. Sci., 76: 381–385
Yim, D., S.S. Kang, D.W. Kim, S.H. Kim, H.S. Lillehoj and W. Min, 2011.
Protective effects of Aloe vera-based diets in Eimeria maxima-
infected broiler chickens. Exp. Parasitol., 127: 322–325
Zaman, M.A., Z. Iqbal, R.Z. Abbas and M.N. Khan, 2011. Anticoccidial
activity of herbal complex in broiler chickens challenged with
Eimeria tenella. Parasitol., 139: 237–243
Zhang, L.B. and Y.M. Guo, 2008. Effects of liquid DL-2-hydroxy-4-
methylthio butanoic acid on growth performance and immune
responses in broiler chickens. Poult. Sci., 87: 1370–1376
(Received 23 June 2012; Accepted 01 October 2012)