Coccidiosis in poultry: review on diagnosis, control,

prevention and interaction with overall gut health

M. DE GUSSEM
1
Alpharma Animal Health, Laarstraat 16, B-2610 Wilrijk, Belgium
Corresponding author: [email protected]
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Coccidiosis in poultry is still considered as one of the main diseases affecting performance of poultry
reared under intensive production systems. Although a lot of research efforts have been allocated towards
molecular techniques, and a lot of progress has been noted in this field, practical use of these techniques
are not available today, except in the field of diagnostics, where several polymerase chain reaction (PCR)
tests for chicken Eimeria spp. are available today albeit not yet commonly used. On the other hand, with
currently available diagnostic methods such as oocyst counts and lesion scoring, an interpretation of the
impact of (subclinical) coccidiosis is not easy. Another problem difficult to address with currently
available tools, is the interpretation of the efficacy of an anticoccidial program. Anticoccidial sensitivity
testing is the only reproducible method available today, but interpretation is far from easy. The result of all
this is that, although coccidiosis is not, by some, perceived as a major problem in poultry production,
economical impact of coccidiosis is most probably underestimated and optimisation of anticoccidial
programmes might be advantageous to the broiler industry. In addition to this, a link between subclinical
coccidiosis and bacterial enteritis complicates choosing the right tools and strategy for poultry producers.
Implementing sound shuttle and rotation programs can be part of the answer in order to not only control
clinical, but also subclinical coccidiosis.
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Keywords: Eimeria, diagnosis, prevention, anticoccidials, vaccination, resistance, chicken
Introduction

Coccidiosis is a disease that is caused by protozoan parasites of the genus Eimeria, developing within
the intestine of most domestic and wild animals and birds. Seven species of Eimeria (E. acervulina, E.
brunetti, E. maxima, E. mitis, E. necatrix, E. praecox and E. tenella) are recognized as infecting chickens.
Although coccidiosis is a disease known for many years, it is still considered as the most economical
important parasitic condition affecting poultry production worldwide. Based on a compartmentalized
model (Williams, 1999), cost of coccidiosis in poultry in Sweden was estimated to be 0.023 per kg live
weight (Waldenstedt, 2004). Extrapolated to assess the worldwide impact of coccidiosis, and assuming 50
billion broilers of 2 kg live weight annually produced (Srensen et al., 2006) this cost is probably more
than 2.3 billion . Noteworthy in this aspect is that the Swedish poultry production is at high standards and
therefore coccidiosis is, within the Swedish poultry industry, not considered to be an important issue. Very
important is the finding that almost 70 percent of this estimated cost is due to subclinical coccidiosis, by
impact on weight gain and feed conversion rate. One of the reasons for these remarkable findings is
probably the difficult diagnosis of subclinical coccidiosis, which prevents the industry to evaluate the best
possible strategies for control of coccidiosis.
For the control of coccidiosis in chickens and turkeys, a number of preventive medications have been
approved for use world-wide, but reduced sensitivity and resistance are increasingly important as no new
anticoccidial compounds are known to be under development. Also live attenuated and non-attenuated
vaccines are available, but next to cost reasons, the fact that live vaccines need host cells to replicate and
to instigate an active immunity, cause them to result in subclinical coccidiosis and this is a disadvantage.
This is associated with a diminution of performance and, in the absence of growth promoters, even
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attenuated vaccines are considered by many poultry producers to be associated with a higher incidence of
bacterial enteritis. In spite of this, live vaccines are significant and important tools in the anticoccidial
arsenal, as will be explained in this paper. New approaches such as vaccination of breeders with the goal
of confer of protective maternal antibodies and recombinant vaccines are not popular in practice or not yet
available. Molecular techniques such as polymerase chain reaction (PCR) methods are becoming
increasingly important, but no quantitative method is available on a cost effective and large scale basis.
Fundamental research on coccidiosis today is mainly focused on improving molecular techniques that
might result in improved diagnostics or the development of recombinant vaccines; but hitherto molecular
techniques have not solved many practical questions on what kind of prevention is adequate for a certain
poultry production unit. So, although significant and promising steps have been made in describing the
biology, diagnosis, epidemiology and prevention of coccidiosis, a number of issues important to the
industry are not sufficiently addressed today.
The purpose of this review is to provide a brief overview and interpretation of the, for the poultry industry,
most practically relevant insights on diagnosis, control, prevention and the impact of coccidiosis on the
overall gut health of chicken.
Diagnosis and drug sensitivity testing
As indicated, next to the fact Eimeria are very effective parasites, one of the main reasons coccidiosis
is still a major problem, is the difficult diagnosis. The classical parasitological methods of diagnosis are
labor intensive and therefore costly. Oocyst per gram (OPG) counts in faeces or litter have a poor relation
with the impact of the parasite on the performance of a flock. Identification of different species based on
morphology of oocysts is very challenging and requires expertise. Lesion scoring is an interpretation
based on macroscopic visible lesions caused by Eimeria, usually following a scoring system from zero to
four (Johnson and Reid, 1970). The individual scores for all the species are usually compiled for a certain
number of birds (e.g. six) per flock resulting in a Total Mean Lesion Score (TMLS). The method is
extremely labor intensive, sometimes subjective and only reliable when performed by skilled people. The
correlation between lesion scores and performance is believed to be stronger than with OPG but still there
is a difficult appreciation of the level of lesions towards impact on performance, especially at subclinical
levels. A limitation is for instance the fact that E. mitis, although quite pathogenic, does not cause typical
lesions and is mostly disregarded when using this method. Lesion scoring still remains the most frequently
applied diagnostic method today. The seven species of Eimeria infecting chickens are considered not
equally important. Generally, it is agreed upon that from the species recognized in broiler chickens, the
most pathogenic are E. acervulina, E. maxima and E. tenella. The latter is, amongst broiler farmers, the
best known. It infects the caeca and because of its deep development in the mucosa and subsequent wide-
spread damage with distinct gross lesions and loss of blood in the faeces, it is easily recognized also by
farmers. On the other hand, when performing field necropsies on a larger scale, E. tenella appears to be
the least prevalent of the three species mentioned. Also, the damage is being limited to the caeca, relative
less important parts of the gut with regard to digestion and absorption, thus effects on growth and feed
conversion rate. Diagnosis of clinical disease caused by E. tenella is quite easy and action (therapy on the
short term, change of preventive means on the long term) can be swift. These facts make its impact on the
productivity of the broiler industry is relatively limited compared to the other species, although many
broiler farmers associate coccidiosis only with caecal coccidiosis. This is a good example of perception
not being in accordance with the facts. E. acervulina and E. maxima, both much more prevalent, are less
perceived to be related with clinical coccidiosis in the field. E. acervulina is causing white lesions in
duodenum and in heavier infections also more caudal, interfering even with the ability for E. maxima to
develop (Mathis, 2005). E. maxima causes petechiae in the midgut. To assess the level of damage caused
by these two species, lesion scoring can be performed. An important debate is still ongoing on what levels
are to be considered clinical (and requiring treatment) and what levels are subclinical. Some consider
lesions higher than 1.5 per species as indicative for clinical disease, and levels below as subclinical, not
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requiring treatment. E. praecox and E. mitis are not scored for and are completely disregarded using the
lesion scoring method, although both species are shown to be able to cause losses through an increased
feed conversion rate and in the latter case even morbidity (Gore and Long, 1982; Fitz-Coy and Edgar,
1992; Williams, 1998). Moreover, it has been demonstrated there can be a poor relation between
macroscopic and microscopic lesions, emphasizing using macroscopic lesion scoring alone is not suitable
to detect all economical relevant coccidiosis infections (Idris et al, 1997). It is frequently disregarded that
all macroscopic, but also microscopic lesions, in fact any infection of coccidia, requires an invasion and
thus destruction of host cells. This is both true when the parasitical life cycle can complete, but even so
when an intervention of the immune system occurs. In the latter case not only host cells are destroyed, but
also the activation of the immune system requires use of nutrients that cannot be addressed to the
conversion of nutrients into meat, the ultimate goal of broiler production. As a consequence it is important
to understand that any level of coccidiosis is causing a real, but difficult to quantify, loss in performance.
As coccidiosis is a disease that cannot currently be eradicated, the objective of coccidiosis prevention is
finding the economical optimal balance between costs of diagnosis, prevention, treatment and
development of host immunity while trying to keep the subclinical loss as low as possible. It is clear that
producers achieving a better balance will have a competitive advantage over other producers.
Necropsy sessions are performed in cooperation with the pharmaceutical industry in a number of
countries. Basically, such systems consist of a planned, organized and benchmarked assessment of the
lesion scores and gut health on poultry complex (group of farms on the same anticoccidial program) basis.
A number of times per year and always at the same laboratory, preferably the same, well-trained
specialists assess a significant number of poultry houses, thus improving the reproducibility compared to a
field lesion scoring session. This methodology is suitable for assessing the overall efficacy of the
anticoccidial program, including reduced sensitivity and resistance of drugs in use. In order to make firmer
conclusions, session data are compared with historical data.
A nice overview of advances in diagnosis of coccidiosis and analysis in genetic variation in Eimeria is
given by Morris and Gasser (2006). This review covers both biochemical and molecular methods such as
multilocus enzyme electrophoresis, southern blot analysis, pulsed-field gel electrophoresis and several
PCR techniques. These techniques are a major addition for scientific research and more practical
applications such as establishing vaccine quality control, but unfortunately, the lack of a rapid, low-cost
and especially quantitative test is preventing their broad scale use. The main application of these
techniques for field diagnosticians today is the possibility of defining presence of species currently
disregarded such as E. praecox and E. mitis. Still, the lack of the quantitative aspect of the techniques is
preventing an accurate appreciation of different coccidial species certainly with the widespread use of
ionophores that also allow some multiplication of sensitive parasites.
A very innovative technique can be found on a website (Gruber et al., 2007) and is called Coccimorph.
This is a computational approach for parasite diagnosis, in this case Eimeria spp. from chicken and rabbit.
Images from sporulated oocysts from a confirmed species were assessed on different features: curvature
characterization, size and symmetry and internal structure characterization. Users can upload their digital
images from unidentified oocysts and have the program identify the species concerned. This is very
accessible and the low cost is a major advantage. A disadvantage is only sporulated oocysts can be
identified, which limits the use of this technique to litter sample identification only.
Anticoccidial sensitivity testing (AST) is a well-known technique to try to assess resistance of a certain
coccidial isolate to different anticoccidial drugs (McDougald, 1987; Chapman, 1998; Naciri et al., 2003;
Peek and Landman, 2003). Although a valid method for a certain isolate, this technique is not routinely
used. The main reasons are the long duration and very high cost associated with the complicated, in vivo
character of the test. The short period of testing (usually about six days) without allowing the initially
naive birds to recover from an artificially high infective dose makes interpretation of the results not easy.
One way to decrease the cost is using strains originating from different houses in one AST. In this way, a
worst case result for the different strains may give good information on what anticoccidials could be
effectively used on a big portion of farms part of a broiler complex. By meta-analysing AST results from
strains with a known drug history, a better knowledge can be obtained on how fast resistance is induced,
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how long it remains established in a certain coccidial population and on whether there is cross-resistance
amongst drugs.
Prevention and control of coccidiosis
There are basically two means of prevention of coccidiosis: chemoprophylaxis and vaccination.
Chemoprophylaxis using so-called anticoccidial products (ACP) or anticoccidials in the ration is by far the
most popular: it is estimated that 95% of the broilers produced (Chapman, 2005) receive anticoccidials.
Sometimes the term coccidiostats are used with regard to ACP but in reality most of the ACP currently
on the market are coccidiocidal and not just static.
Generally two groups of anticoccidials are considered, ionophorous antibiotics or ionophores and
synthetically produced drugs, also denominated as chemicals. Chemicals were the first type of drugs
being used in treatment and later on in prevention of coccidiosis. In 1948, sulphaquinoxaline was the first
drug administered in the feed continuously and at lower doses (Chapman, 2003, McDougald, 2003). Other
chemicals followed in the years after, allowing the poultry industry to expand and upscale production.
Most of the initially marketed chemicals have disappeared from the market. The main reason for this is the
rapid selection for resistance in coccidia when these chemicals were used, requiring their judicious use,
switching to another drug before resistance has built up. This limits the commercial potential which, in
combination with increasingly high costs associated with registration of anticoccidials, explains the short
life-cycles of some chemicals. There are a couple of chemicals that are marketed today, such as
amprolium, nicarbazin, robenidin, diclazuril, zoalene, decoquinate, halofuginone. The fact that they are
still being marketed is a demonstration of their value to the poultry industry and thus an indication of the
more limited potential for resistance build-up compared to the ones which disappeared. The resistance
status of chemicals can be assessed using ASTs (McDougald et al., 1987; Peek and Landman, 2003;
Naciri et al., 2004). If coccidiocidal, chemicals can and are in practice often used in order to reduce the
infection pressure of coccidiosis (De Gussem, 2005), in a so-called clean-up program. Clean-up programs
and consequent reduced (subclinical) infection pressure is expected to have a positive impact on
performance. To achieve this, chemicals are preferably used during a complete grow-out, a so-called full
program. Some producers do not, in order to limit risk for resistance, use chemicals in full program, but
switch from one chemical to another in the same grow-out, in a so called shuttle program. Switching after
a certain grow-out from one anticoccidial to another or to a shuttle program is called rotation (Chapman,
2005). However, most popular ACPs are carboxylic true ionophores. The main reason for their popularity
is the relatively limited risk for complete resistance to these products, at least compared to the risk for
resistance towards chemicals. Indeed, after introduction of the first ionophore on the market, monensin, in
the 1970s it is remarkable to see that these drugs are still predominant in the prevention of coccidiosis.
An explanation for this slow acquisition of resistance to ionophores is the fact that they allow for some
leakage of sensitive oocysts. This leads to a less stringent resistance selection than with chemicals. The
mode of action of the different ionophores is similar: they facilitate cation transport across the parasitic
cell membrane. This causes ionic gradient and content modifications (Gumila et al., 1996) with parasite
cell death as a final consequence. Based on their cation selectivity, transport rate capacitity and structure,
three classes of ionophores can be discriminated (Presmann, 1976; Westley, 1982), monovalent,
monovalent glycoside and divalent ionophores. The ones registered and marketed worldwide are the
monovalent ionophores monensin, salinomycin, narasin, the monovalent glycosides maduramicin and
semduramicin and the divalent ionophore lasalocid. One of the main debates still ongoing amongst
coccidiologists is the ability for acquiring resistance to one drug by the use of another drug, the so-called
cross resistance (Chapman, 2007). Evidence of incomplete cross resistance within a certain ionophore
class is illustrated by the fact that, after years of use of the monovalent ionophore monensin, resistance to
narasin in United States was encountered before the product was commercially launched (Weppelman et
al., 1977). Several papers indicate this cross resistance is less obvious between products of different
classes, for instance between maduramicin and monovalent ionophores or between lasalocid and
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monovalent ionophores (McDougald, 1987; Bedrnik et al., 1989; Marien et al, 2007). The debate is of
particular importance when defining rotation programs: stricto sensu rotating between one monovalent
drug to another can be considered rotation, but taken into account the above described incomplete cross
resistance within a class of ionophores, the relevance of this type of rotation could be questioned.
Therefore, relevant or true rotation for anticoccidials could be suggested to be between classes of
ionophores or chemicals. Some producers do not use rotation programs, although a majority of producers
has accepted this principle as valuable in order to maintain and safeguard the efficacy of anticoccidials.
Chapman (2005) pointed out that one of the reasons producers can afford limited rotation, thus working
with not fully effective drugs, is the importance of immunity towards coccidiosis. This might be true when
drugs are used to prevent clinical coccidiosis, but to control subclinical coccidiosis this is probably an
inadequate strategy. As solid flock immunity is achieved, in built up litter conditions, only at 6 to 7 weeks
of age (Chapman, 1999), subclinical levels will cause economical damage. Logically deducting, a more
efficient anticoccidial will cause lower levels of subclinical coccidiosis, thus less economical damage.
Subclinical damage is therefore considered by some coccidiologists today to be the most important reason
for rotation programs.
Live vaccination, as indicated higher, is today less applied in broiler production. Two types of vaccines
are discriminated, attenuated and virulent (Chapman et al., 2002). Attenuated vaccines lack a part of the
life cycle (less asexual reproductive cycles) of the original strain they were derived from, and as a
consequence have a lower reproductive and pathogenic potential. This is a major advantage towards
performance of virulent coccidial vaccines, but because of the lower reproductive potential of attenuated
vaccines, production costs are significantly higher. Another discrimination to be made are vaccines
consisting of anticoccidial-sensitive strains and others made of more or less resistant strains. The main
advantage of the live ACP sensitive vaccines is their ability to alter the level of resistance in a certain
coccidial population. There are several reports on this very interesting feature of vaccines (Mathis, 2003;
Chapman and McFarland, 2004; Mathis and Broussard, 2006; Peek and Landman, 2006), still many
questions remain on how many consecutive grow-outs should be applied to overcome or prevent
resistance to the different anticoccidials marketed. Also the stability of this resensitized populations are
not well known. Still, the approach of live vaccination to optimize the efficacy of anticoccidials is very
important and next to simple resting (Chapman and McFarland, 2003) of anticoccidials the only method
known to help reducing the portion of resistant parasites in a given coccidial population.
For the design of anticoccidial programs, above aspects of resistance and restoration of sensitivity may be
used to optimize rotation and shuttle programs. A first consideration is on the definition of shuttle and
rotation programs. Strictly spoken, changing from one drug to another is enough to talk about shuttle or
rotation, but in view of the cross resistance described, a more narrow definition would suggest rotation
and shuttle to be more valid if switching from one class of drug to another. Indeed, no proof exists that a
shuttle between two monovalent ionophores will slow down resistance development; therefore no
indication exists to perform this type of shuttles. Another consideration is on giving a simple rest to
anticoccidials: as proven by Chapman and McFarland (2003), resting monovalent ionophores is
advantageous to the efficacy of a coccidial population towards the ionophore previously used, but cross
resistance might invalidate this rest. Therefore, in order to substantially control coccidiosis, and also
subclinical losses, prudent use of anticoccidials might include consolidation of ionophores from the same
class in the same shuttle or to simply use full programs, and after this use of a class, rotating away, ideally
to chemicals or vaccines. For practical reasons, also another class of ionophores can be considered for a
next phase in a rotation program. Still a lot of research is needed to better validate these seemingly
obvious ideas.

Interaction of coccidiosis with microbial intestinal flora

Over the last years, interesting research models have been developed to study impaired gut health in
the absence of growth promoters. Indeed, one of the main concerns for poultry integrations is the vast
majority of flocks suffering from several degrees of gut disorders (Van Immerseel, 2004). These disorders
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are poorly defined, variable in etiology, severity and appearance. Nomenclature is very diverse but some
popular terms to describe this condition of impaired gut health are dysbacteriosis, bacterial enteritis (BE),
small intestinal bacterial overgrowth, clostridiosis and wet litter.
Signs during necropsy associated with the conditions described are
thin, fragile, often translucent intestinal walls,
ballooning of the gut,
hyperaemia of the mesenteric blood vessels and blood vessels on the serosal side of the intestine,
flaccid gut edges after incision, lack of tonus
watery or foamy contents,
poorly digested feed particles at the end of the gastro-intestinal tract (GIT)
multi-coloured oily aspect of the gut contents in contact with the mucosa
During a visit in a typical affected poultry house, following are frequently encountered signs:
wet litter, initially in patches under drinking or feeding lines where condensation is typical, in
more severe cases wet litter is generalized
greasy aspect of the wet litter
droppings with greasy and poorly digested feed particles are common
Initially and typically feed consumption is stalling, while water consumption shows daily
increase following standards for the breed concerned, causing an increased water:feed ratio
(WFR). During a typical episode of bacterial enteritis the WFR is exceeding 2 in normal ambient
conditions. In a later phase, also water consumption is stalling.
Because of wet litter, birds have dirty feathers
Feeding and drinking activity is reduced
Because in affected animals, Clostridium perfringens (Cp) has been isolated in much larger numbers and
more proximal in the GIT than in healthy birds, BE is often associated with NE, a condition also
associated with Cp. Three predisposing factors are associated with BE: feed factors known to cause BE,
(subclinical) coccidiosis and management. Most of the research models combine two of these
predisposing factors namely (i) feed known to instigate BE and (ii) subclinical coccidiosis. Models usually
combine the instigating feed components with a consequent coccidial challenge sometimes with an
additional Cp challenge to exacerbate BE. Some researchers claim models to be as efficient without the
additional Cp challenge. Clostridium perfringens is a very common and very abundant bacterial species in
the caeca, even in normal conditions and it is assumed that Cp is able to relocate to more proximal
locations in the gut whenever the conditions are appropriate: availability of nutrients for Cp. It is however
not clear yet whether Cp is the cause or rather a consequence or indicator of BE: a lack of knowledge of
the exact pathogenesis of the condition exists, or even, a lack of knowledge of the several possible
pathogeneses that can lead, to a similar outcome described as BE. The well-known impairment of
digestive function caused by coccidia is therefore probably a main factor in conditioning the guts for Cp to
grow. In several models, attenuated Eimeria strains are used, indicating that subclinical coccidiosis is
sufficient as a predisposing factor. Still, other factors impairing digestion and absorption of nutrients, such
as enzymatic dysfunction, viral infections or mycotoxins are likely to be equally effective as a
predisposing factor, although in practical conditions and with current knowledge, subclinical coccidiosis is
believed by many to be the most important one. As a consequence, the last commonly recognized
predisposing factor, poor management, is probably not so important in inducing the disease but more
important in defining the degree of severity of BE and the subsequent impact on the zootechnical
performance of a flock.
A very important debate is ongoing in the role that ACP have in prevention of BE. A publication on
reduction of Cp counts in the intestinal tract (Elwinger et al., 1998)of birds medicated with narasin, a
monovalent ionophore, strongly suggest the positive impact of ionophore compounds on reducing the
impact of BE. This reduction of Cp counts is a consequence of the well known antibacterial activity of
ionophorous compounds. Minimal inhibitory concentrations (MIC) for the different ionophores are to be
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found in several publications. However, as it is not proven that Cp is the main etiologic agent of BE or
rather an opportunistic bacterium, no conclusions can be made whether ionophores have a direct
preventive effect on BE. Maybe they simply reduce the effects of one of the consequences of BE, Cp
proliferation. This discussion might seem not so relevant at first sight, but in practice one of the main
drivers on the choice of ACP in anticoccidial programs is this presumed effect on BE. A few questions
remain unanswered in rightfully assessing the role of ionophores in prevention of BE:
1. All over the world, the vast majority of anticoccidial programs consist of ionophores. As indicated
by the large number of antibiotic treatments through drinking water, BE is still considered one of
the main problems in poultry production. What would be the number of antibiotic treatments if
ACP were used that have anticoccidial activity, equivalent to ionophore efficacy, but not the
antibacterial activity? Maybe the number of treatments would be higher in absence of the
antibacterial activity exerted by the ionophores, but yet there is neither clear evidence nor
numbers.
2. As (subclinical) coccidial infections are known to be a predisposing factor of BE, what would be
the number of treatments if an ACP existed that had no antibacterial activity but was able to very
effectively suppress coccidial infections? Some of the chemicals would apply to this category of
ACP.
3. Even if assuming Cp is a cause and not a consequence of BE, are the differences in Cp MIC for
the different ionophores relevant? As all ionophores are used at concentrations in the gut that
approach or largely exceed Cp MIC, there is no inference or even an indication that this is a valid
hypothesis.
4. Is, when using the same ionophores because of the (maybe perceived) important role in prevention
of BE, there a risk of installing a vicious circle through overuse of ionophores, reduced
anticoccidial sensitivity (not resistance), higher coccidial challenge thus a more prominent role of
coccidiosis as predisposing factor for BE?
Conclusion
Although coccidiosis has been the subject of a lot of research over the last decades, a number of very
significant questions remain unanswered. As poultry production is subject to continuous changes, also the
problems related to coccidiosis change over the years. A lot is to be expected from recent progress made
with molecular techniques, but practical applications of these techniques are scarce today. The industry
has to rely on established techniques in order to diagnose coccidiosis, and these techniques still bring
added value if used in a correct way. The assessment of efficacy of different ACP is important in order to
optimize anticoccidial programs, not only to limit cases of clinical coccidiosis, but mainly to reduce the
impact of subclinical coccidiosis, estimated to be a lot more costly to the poultry industry. An important
debate is ongoing on how rotation programs can be made as efficient as possible. Live vaccines could
have an interesting role to boost the efficacy of ACP. As bacterial enteritis is today one of the most
important problems affecting the performance of the poultry industry, the role of coccidiosis in this multi-
factorial condition is to be carefully assessed. Anticoccidials could have a beneficial effects by reducing
the impact of BE, but if these effects are due to direct antibacterial, or indirect by the effects on coccidia,
remains to be further investigated.
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