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Avian Pathology
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Ascites syndrome in broilers: physiological and

nutritional perspectives
a

A. Baghbanzadeh & E. Decuypere

Section of Physiology, Department of Basic Sciences, Faculty of Veterinary Medicine ,

University of Tehran , PO Box 14155-6453, Tehran, Iran
b

Laboratory for Physiology and Immunology of Domestic Animals, Department of Animal

Production, Faculty of Agricultural and Applied Biological Sciences , K.U. Leuven ,
Kardinaal Mercierlaan 92, B-3001, Leuven, Belgium
Published online: 08 Apr 2008.

To cite this article: A. Baghbanzadeh & E. Decuypere (2008) Ascites syndrome in broilers: physiological and nutritional
perspectives, Avian Pathology, 37:2, 117-126, DOI: 10.1080/03079450801902062
To link to this article: http://dx.doi.org/10.1080/03079450801902062

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Avian Pathology (April 2008) 37(2), 117126

REVIEW ARTICLE

Ascites syndrome in broilers: physiological and nutritional

perspectives
A. Baghbanzadeh1* and E. Decuypere2
1

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Section of Physiology, Department of Basic Sciences, Faculty of Veterinary Medicine, University of Tehran, PO Box
14155-6453, Tehran, Iran, and 2Laboratory for Physiology and Immunology of Domestic Animals, Department of Animal
Production, Faculty of Agricultural and Applied Biological Sciences, K.U. Leuven, Kardinaal Mercierlaan 92, B-3001
Leuven, Belgium

Broiler chickens are intensively selected for productive traits. The management of these highly productive
animals must be optimal to allow their full genetic potential to be expressed. If this is not done, inefficient
production and several metabolic diseases such as ascites become apparent. The causes of the ascites are
multifactorial but diet and, particularly, interactions between diet, other environmental and genetic factors
play an important role. The relatively high heritability estimates for ascites-related traits and the significance
of maternal genetic effects for most of the traits indicate that direct and maternal genetic effects play an
important role in development of the ascites syndrome. An imbalance between oxygen supply and the
oxygen required to sustain rapid growth rates and high food efficiencies causes ascites in broiler chickens.
Because of the relationship to oxygen demand, ascites is affected and/or precipitated by factors such as
growth rate, altitude (hypoxia) and environmental temperature. As the high metabolic rate (fast growth) is a
major factor contributing to the susceptibility of broilers to ascites, early-age feed or nutrient restriction
(qualitative or quantitative) or light restriction in order to slow down the growth rate seem practically viable
methods, since final body weight is not compromised. Manipulation of the diet composition and/or feed
allocation system can have a major effect on the incidence of ascites. Optimization of the house temperature
and ventilation in cold weather seem helpful practices to decrease ascites incidence.

Introduction
The modern chicken (Gallus gallus domesticus) has been
intensely selected for higher growth rates and so
indirectly for a high rate of protein synthesis, which
requires more oxygen (Decuypere et al., 2005), increased
feed conversion (Decuypere et al., 2000; Pakdel et al.,
2002), egg production (Decuypere et al., 2000) or meat
yield and breast percentage (Hoving-Bolink et al., 2000).
Modern strains of broilers are able to achieve market
weight in 60% less time than broilers of 40 years ago.
Nevertheless, the pulmonary and cardiac capacity of
modern broilers is very similar to the old broiler strains,
which forces their cardiopulmonary system to work very
close to its physiological limit (Lorenzoni et al., 2006).
The lung capacity does not always meet the oxygen
demands necessary for rapid growth. This results in
impaired ability to regulate the energy balance under
extreme conditions, such as low ambient temperature or
high altitude (Luger et al., 2003). If the lung of the
chicken grows less rapidly than the rest of the body,
hypoxia and ascites could result (Julian, 2000). Recent
data suggest that ascites is not caused by an increased
oxygen requirement of fast growth rate per se at low
altitude, but by an impaired oxygen supply to sustain fast
growth rate (Decuypere et al., 2005). Ascites (pulmonary

hypertension syndrome, or water belly) is a metabolic

disorder, characterized by hypoxaemia, increased workload of the cardiopulmonary system, central venous
congestion (Luger et al., 2003), an excessive accumulation of fluid in body coelomic cavities (Olkowski et al.,
1999), hypertrophy of the right ventricle and a flaccid
heart (Riddell, 1991), and finally death (Luger et al.,
2003). A high incidence of ascites can occur when
broilers are reared at altitudes high enough to substantially reduce the partial pressure of oxygen (Owen et al.,
1990; Wideman et al., 2003). Studies showed a high
incidence of subclinical heart disease in fast-growing
broilers, with many developing clinical signs of chronic
heart failure and ascites. Recently, a novel observation
was reported where sudden death in broilers was
associated with rupture of the right atrium (Olkowski
et al., 2007). Although the incidence of this metabolic
disorder in well-managed flocks is very low, it causes
important economic losses to the poultry breeding
industry*an estimated 4.7% of the broilers worldwide
have the disease (Maxwell & Robertson, 1997). It is
estimated that 5% of broilers and 20% of roaster birds
die of ascites (Balog, 2003); considering that an estimated 40 billion broilers are produced annually around

*To whom correspondence should be addressed. Tel: 98 21 61117081. Fax: 98 21 66422045. E-mail: abaghban@ut.ac.ir
Received 4 October 2007
ISSN 0307-9457 (print)/ISSN 1465-3338 (online)/08/20117-10 # 2008 Houghton Trust Ltd
DOI: 10.1080/03079450801902062

118 A. Baghbanzadeh and E. Decuypere

the world, it is evident that the economic losses due to

ascites are significant. Genetic, physiological, environmental, and management factors all seem to interact to
produce a cascade of events that culminate in ascites
syndrome.

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Aetiology of the Ascites Syndrome

Despite the intensive investigation of the syndrome for
many years, the primary cause of ascites is unclear
(Crespo & Shivaprasad, 2003). The physiology of this
syndrome (see Figure 1) has been extensively studied
(Julian, 1993, 2000; Scheele, 1996; Hassanzadeh et al.,
1997; Decuypere et al., 2000; Wideman, 2000). Ascites
syndrome, first reported in flocks of broiler chickens
reared at high altitudes in Bolivia (Hall & Machicao,
1968), may result from one or more of four physiological
changes that cause an increased production and/or
decreased removal of peritoneal lymph (Balog, 2003).
Obstruction of lymph drainage, decreased plasma oncotic pressure, fluid leakage secondary to increased vascular permeability, and, last but not least, increased
portal pressure secondary to right ventricular failure or
liver damage may all result in ascites (Julian, 2005).
Neoplasia, most frequently, oviduct carcinomas and,
alternatively, right ventricular failure with valvular
insufficiency, in which high venous pressure in the vena
cava interferes with lymph return, may bring about
blockage of lymph and, subsequently, ascites (Balog,
2003). Since plasma proteins, especially albumin, are
mainly responsible for blood oncotic pressure, some
researchers (Wise & Evans, 1975; Bowes et al., 1989)
explained decreased plasma proteins in ascites-sensitive
broilers or those with ascites. Decreased plasma protein
could be a result of loss of high-protein lymph from the
liver or a stop-eating process due to right ventricular
hypertrophy. Vascular damage and subsequent leakage
of fluid and proteins through the vascular epithelium can
be caused by viral and/or bacterial infections, chemical
toxins, chlorinated hydrocarbons and some phenolic
compounds, coal-tar derivatives, dioxin, and pentacholorophenol (Balog, 2003). Increased vascular hydraulic
pressure could be a result of hepatic pathologies, right
atrioventricular valve pathologies, pulmonary hypertension and miscellaneous cardiac pathologies (Currie,
1999).

and do not expand like the (alveolar) lungs of mammals

(Balog, 2003). In other words, the avian respiratory
system possesses rigid lungs of fixed volume (Fedde,
1984), which do not expand or contract with each breath
as mammalian lungs do. The blood and air capillaries
form a network that allows the small blood capillaries of
the lung to dilate only very little to accommodate
increased blood flow (Julian, 1998).
Pressure, generated by cardiac contraction, drives
blood flow around the circulation. Poiseuilles law relates
volume flow (Q) to the pressure drop (P1  P2) along a
tube of radius (r) and length (L) during steady flow as
follows:

Q  (P1 P2 )

pr4
8mL

(p is blood viscosity)

Vascular resistance (R) will be calculated as:

R

P1  P2
Q

It is obvious that a slight change in a vessel radius has

major effects on flow and, consequently, on resistance
characteristics.
On the other hand, the FrankStarling law of the
heart describes an increase in contractility of the
myocardium due to an elevated preload. In terms of
the right ventricle, preload is determined by cardiac
venous return. This mechanism increases cardiac output
by elevating the stroke volume. If pulmonary vascular
resistance increases, the afterload increases, leading to a
pressure overload in the right ventricle. The classical
response to this stimulus is ventricular hypertrophy, one
of the common lesions in ascitic birds. One important
consequence of ventricular hypertrophy is distortion of
atrio-ventricular valves, which also become thicker, leaky
and less efficient (see below, Avian Heart Valves
Anatomy) and the production of regurgitant flow from
the ventricle to the atrium during ventricular systole.
The ventricle is then subjected to volume overload and
the resultant haemodynamic pressure imbalance generates ascites (Currie, 1999).

Pulmonary Hypertension
Pulmonary hypertension is the result of processes taking
place in both respiratory and cardiovascular systems.
The architecture of the modern broilers*small stature,
the large, heavy breast mass, the pressure from abdominal contents on air sacs, and the small lung volume*
may all be involved in the increased incidence of ascites
syndrome (Julian, 1998; Balog, 2003). Theoretically, the
unique anatomy of the avian respiratory system results
in a model of gas exchange that is more efficient than the
mammalian model (Piiper & Scheid, 1975), and for a
given level of ventilation to the gas-exchange surfaces,
cardiac output, and lung diffusing capacity, arterial O2
loading and CO2 elimination are predicted to be better in
a parabronchial lung, compared with an alveolar lung
with the same inspired gases and metabolic demands
(Powell, 2000). But the rigid (parabronchial) lungs of
birds conform closely to the contour of the body cavity

Avian Heart Valves Anatomy

Blood entering the left ventricle from the left atrium on
atrial systole passes through an orifice guarded by a
membranous atrioventricular valve, similar in general
structure to a mammalian atrioventricular valve, except
that it is tricuspid. Blood passing from the right atrium
to the right ventricle enters through an orifice guarded
by an atrioventricular valve that is structurally unique to
birds. In pronounced contrast to the fibrous structure
characteristic of the mammalian tricuspid valve, in birds
the right atrioventricular valve consists of a single spiral
flap of myocardium attached obliquely to the free wall of
the right ventricle, so it is capable of becoming thicker
and leaky, as a consequence of ventricular hypertrophy.
The outflow valves from the right and left ventricles are,
at first glance, more conventional (mammalian) in
nature (Smith et al., 2000).

Ascites in broilers

Cold
Moderate heat
Activity
Hyperthyroidism
Elevated muscle mass
Over-eating

High altitude
(decreased pO2)

Increased basal metabolic rate

Increased requirement for oxygen at tissue level

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Factors that increase the oxygen requirement

of the bird
Factors that reduce oxygen pick-up
Factors that reduce O2 transfer in lungs
Factors that reduce blood O2 carrying capacity
Factors that reduce O2 release in tissues
Reduced pulmonary vasculature capacity
Polycythemia
Increased blood viscosity
Reduced erythrocyte deformability
Pathological narrowing of lung capillaries
Embolic blockage of pulmonary circulation

Physiological hypoxia

Increased synthesis of erythropoietin

Increased blood flow

Increased haematocrit

Increased stroke volume

Increased cardiac output

Increased heart rate

Any agent that induces hypervolemia
(e.g. excess Na+)

Elevated vasculature pressure in the lung & pulmonary arteries

Pressure overload on the right ventricular muscle wall

Right ventricular hypertrophy

Increased pressure
in
the pulmonary arteries, arterioles & capillaries

Some broilers develop lung

oedema and die at this stage.

Right atrioventricular valve insufficiency

Ventricular volume overload

Dilation & right ventricular failure

Oedema due to increased blood pressure in the veins,

liver and abdominal vessels, particularly the fenestrated
sinusoids of the liver into the peritoneal spaces

Ascites

Figure 1. Physiological and pathophysiological factors affecting ascites syndrome.

119

120 A. Baghbanzadeh and E. Decuypere

Ascites Symptoms
Ascites symptoms in broiler chickens include generalized
oedema, fluid accumulation in the pericardium, hydropericardium (pericardial effusion) (Olkowski et al.,
2003), in the abdominal cavity (Balog et al., 2003),
epicardial fibrosis, lung oedema, enlarged, flaccid heart
(Balog et al., 2003), hypertrophy and dilation of the
heart, especially the right ventricle (Decuypere et al.,
2000), variable liver changes, hypoxaemia, pale comb
and higher blood haematocrit (Luger et al., 2003). These
symptoms indicate that a large number of organs
(including the heart, lung, liver, etc.) are involved in
the disease.

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Erythropoiesis and Ascites

Chickens have a thicker respiratory membrane than
other birds, and broilers have a thicker respiratory
membrane than Leghorn-type fowl, so the ability of
broilers to move oxygen into haemoglobin may not be as
good as in other birds. Research on oxygen haemoglobin
saturation in meat-type chickens indicates that fastgrowing broilers have a lower oxygen saturation than
slow-growing broilers. These results suggest that some
meat-type chickens are not fully oxygenating their
haemoglobin even at low altitude. This may be the result
of increased blood flow rate through the lung capillary
bed of the lung, which does not allow time for
haemoglobin to pick up a full load of oxygen (Julian,
2000). In ascites, where metabolic burdening imposes on
the broilers difficulties in fulfilling tissue demands for
oxygen, birds exhibit a decrease in blood oxygen
saturation and high haematocrit values. Elevation in
haematocrit can be caused by diminished plasma
volume, as a result of fluid exudation out of the blood
system to the abdominal cavity, or enhanced erythropoiesis. The development of mature peripheral red blood
cells from pluripotent stem cells in the bone marrow is a
complex process, regulated by erythropoietin, corticosterone, triiodothyronine and growth factors. Recent
studies have revealed an increase in haematocrit, with
no significant change in plasma volume. It has also been
concluded that continually increased corticosterone
concentrations, as an inducer of erthropoiesis proliferation and differentiation arrest, in ascitic chickens,
resulted in increased production of red blood cells
(partially immature) with decreased haemoglobin content, which might have contributed to enhanced development of hypoxaemia and to aggravation of the
syndrome (Luger et al., 2003). Although increased
haematocrit values should be a positive aid to alleviate
hypoxaemia, birds dying of ascites all show high
haematocrit levels that increase blood viscosity and
augment the inability of the failing right ventricle to
pump blood through the vasoconstricted pulmonary
blood vessels (Shlosberg et al., 1998)

Genetics and Ascites

Poultry breeders have been selecting very successfully on
growth-related traits of broilers over the past few
decades. Recently, the breeding industry has taken up
new challenges and efforts are being directed to produce
stock adaptable to a wide range of environments and to
decrease the incidence of metabolic and physiological

disorders, of which ascites syndrome is an example

(Pakdel et al., 2004).
Genetically, the modern broiler, especially male broilers, seems to be more prone to develop ascites. This is
probably due to extreme selection for either the growth
rate or the feed conversion ratio, which puts high
demands on the metabolic processes and on the oxygen
demand (Decuypere et al., 2000), and oxygen requirement is affected by genetic factors other than growth
rate. Birds selected both for low food conversion ratio
(FCR) with low rates of heat production that were
stimulated to a higher heat production by a low ambient
temperature had difficulties in adapting to environmental changes. It has also been shown that the highest
incidence of ascites occurs in broilers that combined low
FCR with fast growth rate, whereas in broilers with
either slower growth or higher FCR, the incidence of
ascites was much lower. A low FCR in fast-growing
birds was attributed to low values of heat production.
Moreover, birds selected for a combination of both fast
growth and low FCR had low pO2 and high pCO2 in
venous blood at low ambient temperature compared
with the slower growing birds (Decuypere et al., 2005).
There are a few reports about genetic parameters for
ascites-related traits. Lubritz et al. (1995) demonstrated
favourable heritabilities for fluid accumulation in the
abdominal cavity and the ratio of right ventricular
weight to the total ventricle weight. They suggested
that selection based on these traits, which were measured
under cold conditions, would be effective to reduce the
incidence of ascites. Shlosberg et al. (1996) evaluated the
suitability of haematocrit value to select against ascites.
Maxwell et al. (1998) indicated that, in the presence of
ascites, troponin T, an indicator of heart muscle damage,
was heritable. Moghadam et al. (2001) showed that the
heart defect (i.e. including pulmonary hypertension,
right ventricular failure and fluid accumulation in the
peritoneal cavity) as a trait related to ascites was
heritable and had a positive genetic correlation with
body weight. de Greef et al. (2001) demonstrated that the
genetic parameters of ascites related traits within
the same physical environment varied considerably
with the severity of the disease. Therefore, the choice
of selection criteria is complicated. Ascites traits, including the haematocrit value and the ratio of the right
ventricular weight to the total ventricular weight, have
been used as indirect criteria in selection for reduced
incidence of ascites in broilers (Shlosberg et al., 1996;
Wideman et al., 1997; Scheele et al., 2003; Pakdel et al.,
2005). The current methodology for estimating parameters for ascites indicator traits does not account for
the differences between healthy and diseased birds.
However, methods are available to distinguish between
healthy and diseased animals. For example, in the case of
mastitis in dairy cows, the parameter estimations were
improved by dividing the heterogeneous populations
into two more homogeneous distributions, healthy and
diseased. With these improved estimates, a better alternative for selection against susceptibility to mastitis was
provided (Detilleux & Leroy, 2000). Mixture models
have been widely used to separate heterogeneous populations into more homogeneous distributions (McLachlan & Khrishnan, 1997). The mixture model can be
used for situations in which it is unknown how to classify
individuals between distributions. This is the case when
analysing ascites traits, because there are no clear criteria

Ascites in broilers

to distinguish between healthy and diseased birds (de

Greef et al., 2001). Using mixture models, birds can be
assigned to different distributions via probabilities
estimated from trait observations (Detilleux & Leroy,
2000). For ascites traits, a mixture model in its simplest
form may be used to assign observations to two
components; that is, ascitic and non-ascitic. The identification and culling of birds could then be based on the
probability of putative ascites, given ascites indicator
traits, rather than on crude ascites traits (Zerehdaran
et al., 2006).

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Nutrition and Ascites

The broiler growth rate has been found to have a direct
relationship with susceptibility to ascites (Camacho
et al., 2004). Manipulation of the diet composition
and/or feed allocation system can have a major effect
on the incidence of ascites. In most instances, such
changes to the feeding programme influence ascites via
their effect on growth rate. Major nutritional factors
including high nutrient density rations, high feed intake
and feed form are known to influence the occurrence of
ascites in broilers (Balog et al., 2000; Coello et al., 2000;
Bo lu kbasi et al., 2004; Ozkan et al., 2006).
Managing the Growth Rate
Although the growth rate can influence metabolic
diseases during the entire period of broiler production,
research has shown that the early period is particularly
important (Camacho et al., 2004). A reduced growth
rate from 3 to 14 days of age not only benefits bird
health during that period but also later when the growth
rate is as fast or faster than birds that have not
experienced slower early growth. These suggest that
early days of production represents an important developmental period in poultry meat stocks. Recently,
management strategies have been investigated to alter
the growth curve of meat stocks with the objective of
reducing the incidence of metabolic diseases while
maintaining competitive production traits. Methods
have included quantitative and qualitative feed restriction, altered feed form, and environmental management.
Feed restriction. Feed restriction techniques have ranged
from very severe (maintenance only) to milder forms,
which involve daily feed restriction or skipping feeding 1
or 2 days a week. Feed restriction has proven successful
in reducing metabolic disease such as ascites, but the
degree of restriction required to control health problems
needs to be balanced with the time required to reach
market weight and other effects on bird productivity.
Feed restriction reduces growth at a critical time in a
broiler chicks lifecycle when it is the most susceptible to
metabolic disease due to its high oxygen demands (Balog
et al., 2000; Coello et al., 2000; Ozkan et al., 2006).
Despite some of the advantages of feed restriction as a
treatment to reduce ascites, adverse secondary effects
might result due to lower consumption of anticoccidial
products fed to control coccidiosis. Another important
problem resulting from feed restriction programmes is
poor pigmentation, which is directly related to the
quantity of xanthophylls consumed. Pigmentation is
very important because it is perceived as a measure of
quality in the marketplace (Camacho-Fernandez et al.,

121

2002). Feed restriction can reduce the availability of

nutrients and pigmentation precursors, which may have
a direct effect on weight gain, muscle mass, and the
profitcost relationship. These effects could be more
pronounced if the restriction programme was not correct
(Camacho-Fernandez et al., 2002).
Nutrient density. Reducing the concentration of nutrients
in a diet can reduce the growth rate, with the effects most
pronounced from 0 to 21 days of age, during the time
when birds cannot totally adapt intake to lower feed
nutrient content. If diets remained balanced to energy
content, the effect of nutrient density on growth rate is
relatively small unless the decrease in density is very
large. However, even moderately lower nutrient density
reduces mortality due to ascites (Camacho-Fernandez
et al., 2002).
Diet form. Most meat birds are fed crumbled or pelleted
diets to achieve maximum growth and feed efficiency.
Feeding mash reduces growth rate (1 to 2 days to
market) and reduces mortality and condemnations due
to metabolic disease. However, this type of programme
may not be economically acceptable in all areas and has
been demonstrated to increase the incidence of pendulous crops. Broilers that consume pellet feed have
frequently been shown to have higher incidences of
ascites than broilers that consume the same diet in mash
form (Bolu kbasi et al., 2005).
Omega-3 fatty acid sources (flax and fish oils). It has
been found that decreased deformity of the erythrocytes,
as measured by the filtration index, can increase the
amount of ascites in broiler chickens (Mirsalimi &
Julian, 1991; Mirsalimi et al., 1993). The deformity of
erythrocytes is reduced by hypoxaemia. Studies with
humans have demonstrated that erythrocyte deformity
can be increased by dietary supplementation of omega-3
(n-3) fatty acids from fish oils (Berlin et al., 1992).
Archer et al. (1989) found that supplementation with fish
oil reduces blood viscosity and right ventricular hypertrophy in rats. However, other studies (Hulan et al.,
1989) reported a reduction in the growth rate of birds fed
red fish meal as a source of omega-3 fatty acids. This is
important, because the incidence of ascites can be
reduced by slowing the growth rate of broilers (Julian,
1993). The increased content of unsaturated fatty acids
probably increases the fluidity of the erythrocyte membrane and alters membrane function to increase the
deformability of the erythrocytes and potentially help
reduce the incidence of ascites. This could explain the
reduction in whole blood viscosity under hypobaric
conditions with feeding of flax oil. These factors together
would decrease the resistance to blood flow and improve
the movement of the erythrocytes through the capillaries,
thus improving oxygen transport and decreasing ascites
(Walton et al., 1999).
L-Carnitine. It is generally accepted that endogenous Lcarnitine synthesis together with its dietary intake should
be sufficient for normal function. However, in cases of
increased metabolic rate (in fasting-growth broilers),
when energy demands are elevated, the availability of
L-carnitine may become a limiting factor for fat oxidation. In these circumstances, additional exogenous lcarnitine might prove beneficial. It is hypothesized that

122 A. Baghbanzadeh and E. Decuypere

chickens are more resistant to

the development of ascites due to an improved cardiac
output. Furthermore, there is evidence that free radicals
may be involved in the development of ascites (Bottje &
Wideman, 1995). As L-carnitine (ester) is known to have
free radical scavenging properties (Packer et al., 1991),
this might also contribute to a beneficial effect of
L-carnitine on ascites incidence. This hypothesis is
currently under investigation (Buyse et al., 2001).

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L-carnitine-supplemented

Hatchery and Ascites

Antioxidants. The elevated production of reactive oxygen

in broilers prone to ascites may potentiate the development of the disease or aggravate the disease as it occurs
(Enkvetchakul et al., 1993). For chickens, the first line of
defence against reactive oxygen is endogenous antioxidants such as tocopherols, glutathione, uric acid, and
ascorbic acid. The levels of glutathione and a-tocopherol
and g-tocopherol are decreased in the mitochondria of
an ascitic broiler, suggesting reactive oxygen is produced
at the primary site of energy transduction (Cawthorn et
al., 2001). Ascorbic acid and glutathione concentrations
are reduced in both the liver and lung of broilers that
have been reared in ascites-promoting conditions, signifying their utilization against reactive oxygen production in these tissues. In contrast to other endogenous
antioxidants, uric acid is increased in the liver and lung
(Enkvetchakul et al., 1993). This probably results from
an increased net catabolism of adenosine triphosphate
that occurs with the stimulation of anaerobic glycolysis,
increasing the flow of substrates through the purine
degradation pathway (Stinefelt, 2003). Therefore, the
change in the antioxidant status of the broiler during
ascites progression is observed in conjunction with
increased markers of reactive oxygen-mediated tissue
injury, indicating a state of oxidative stress during
ascites. Researchers have attempted to alleviate the onset
of ascites by increasing the antioxidant status of the
broiler before exposure to ascites-promoting conditions.
Broilers that received a vitamin E implant that released a
total of 15 mg a-tocopherol from 0 to 3 weeks of age
immediately before exposure to ascites had significantly
reduced ascites-induced mortality than placebo-treated
broilers (Bottje et al., 1995). Liver and lung concentrations of a-tocopherol in healthy vitamin-E-treated birds
were increased, providing the bird with additional
protection from reactive oxygen. Healthy vitamin-Etreated birds had plasma lipid peroxide values lower
than placebo-treated birds in the same conditions,
indicating the enhanced protection that vitamin E
provides against lipid peroxidation. The vitamin E
implant reduced ascites-induced mortality, probably by
providing an enhanced antioxidant defence against the
reactive species production that otherwise causes tissue
damage and promotes ascites progression. In contrast to
the results obtained with vitamin E implants, supplementing broiler diets with vitamin E did not reduce
ascites-induced mortality (Bottje et al., 1997; VillarPatino et al., 2002). Vitamin C supplemented in broiler
feed at 400 mg/kg feed reduces lipid peroxidation in
cardiac tissue as well but does not affect ascites-induced
mortality. The effect of manipulating other important
antioxidants, such as uric acid, flavenoids, or carotenoids, has not been investigated (Stinefelt, 2003).

Oxygen requirement is the most critical trigger of ascites

in broilers (Julian, 2000). High metabolic demands
together with decreased availability of oxygen may lead
to hypoxaemia and ascites (Wideman, 2001). Ascites
susceptibility is particularly pronounced during the
period of rapid juvenile growth when the metabolic
rate is very high (Decuypere et al., 2000). Although the
peak incidence of ascites occurs in the fifth or sixth week
of the growing period, the aetiology of the disease may
be initiated much earlier, even during the embryonic
stage (Coleman & Coleman, 1991). Embryonic growth
can be estimated by egg weight and oxygen consumption
at certain stages of development. Rapid growth increases
the oxygen requirement, cardiac output, and blood flow,
and may result in increased pulmonary arterial pressure
primarily by increasing the metabolic demand for oxygen
(Julian, 2000; Wideman & Tackett, 2000). Chicken
embryos grow rapidly over the last 7 days of incubation,
resulting in a 60% increase in the oxygen consumption
during the interval between the start of pulmonary
breathing and hatching (Decuypere et al., 2000; Sahan
et al., 2006). Therefore hypoxia, known to be involved in
the occurrence of the ascites syndrome, could arise in the
chick embryo during the interval between internal
pipping and hatching (Dewil et al., 1996). In fact, Dewil
et al., (1996) reported hypoxic conditions in the late
embryonic phase. Oxygen supplementation from 18 to 21
days of incubation could be used as an effective means of
improving hatchability of broiler eggs. Oxygen supplementation during incubation could also increase the
embryonic growth rate and 1-day-old chick weight
(Sahan et al., 2006). The findings of Chineme et al.
(1995) indicated that the length and/or severity of
prenatal hypoxia may influence postnatal characteristics
related to ascites. Eggs incubated in an environment with
a relatively high concentration of carbon dioxide
hatched earlier than in an environment with normal
amounts (Buys et al., 1998a; Hassanzadeh et al., 2002).
The chickens incubated in the environment with increased concentration of carbon dioxide showed a lower
incidence of ascites during the growing period because
high concentrations of carbon dioxide in the incubation
environment might decrease the length of time the
embryo experiences hypoxia (Buys et al., 1998a; Hassanzadeh et al., 2002). Rouwet et al. (2002) demonstrated that chronic hypoxia during embryonic
development induces structural and functional cardiovascular abnormalities (e.g. left ventricular dysfunction)
in the near-term chick embryos. These abnormalities
may be responsible for the increased mortality of
embryos incubated under high altitude. It is hypothesized that developmental changes induced by environmental or incubation conditions may play a role in the
genotype and environment interaction in ascites susceptibility (Decuypere, 2002). Eggs incubated in an environment with a high concentration of carbon dioxide
hatched earlier than those in an environment with
normal carbon dioxide levels (Buys et al., 1998a;
Hassanzadeh et al., 2002). Moreover, the chickens
incubated in the environment with increased concentrations of carbon dioxide showed a lower incidence of
ascites during the growing period. Different degrees of
ventilation during incubation may therefore interact
with genotype and egg shell characteristics (which

Ascites in broilers

determine gaseous exchange) to affect the total incubation time and, thereby, influence the susceptibility to
ascites and related physiological responses in later
postnatal life (Chineme et al., 1995).

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pH and Ascites
Ascites is ultimately caused by an imbalance between the
oxygen supply to the body tissues and the oxygen
requirement of the tissues (Julian, 1993). Poor tissue
oxygenation can be caused by an increased oxygen
requirement of the tissues due to increased metabolism
from rapid growth (Peacock et al., 1989) or in response
to cold temperature; by a decreased availability of
oxygen in the environment due to high altitude (hypobaric conditions) or poor ventilation; or by low oxygen
content of the blood because of low haemoglobin
oxygen affinity or decreased blood oxygen capacity of
haemoglobins or low oxygen exchange in the lung
(Julian, 1993). Ascites can be reduced by decreasing
the oxygen requirements of the bird (such as by reducing
growth rate and avoiding cold) or increasing oxygen
delivery to the tissues.
In mammals, acidosis causes vasoconstriction, while
alkalosis causes vasodilation, which affects pulmonary
arterial pressure and pulmonary hypertension. The
blood pH also affects the affinity of haemoglobin for
oxygen in the lung and release of oxygen to the tissues
(the Bohr effect). A decrease in blood pH lowers the
oxygen affinity of haemoglobin, which encourages
release in the tissues, while increased blood pH increases
oxygen affinity to increase haemoglobin saturation in the
lung (Issacks et al., 1986). The feeding of excess chloride
or sulphate has been shown to depress blood pH and
bicarbonate levels in chickens (Ruiz-Lopez & Austic,
1993), while feeding bicarbonate would be expected to
increase blood pH. It has been suggested that broiler
chickens that have a high metabolic rate may be in a state
of metabolic acidosis when they are on full feed (Julian,
1993). Several workers have shown that fast-growing
birds have lower blood oxygen concentration than slowgrowing birds; likewise, birds on full feed have lower
blood oxygen than food-deprived birds (Fedde et al.,
1998; Julian & Mirsalimi, 1992; Reeves et al., 1991).
Feeding low chloride/high bicarbonate diets results in a
decrease in pulmonary hypertension. Conversely, feeding
diets with high chloride content tends to increase the
incidence of ascites. Increased blood pH would increase
oxygen haemoglobin affinity, which is low in fully fed
broilers, probably because of metabolic acidosis. It has
been demonstrated that decreased blood pH results in
increased pulmonary arterial pressure in mammals and
this may also be true in birds. Increased blood pH can
improve the loading of oxygen by haemoglobin in the
lung due to the Bohr effect. It therefore appears that
supplementing broilers with bicarbonate may be beneficial in fast-growing birds with very high oxygen
requirements and high production of carbon dioxide,
as long as the decreased pH normally present in the
muscles that facilitates oxygen unloading is not affected.
Further work is needed to establish the mode of action
of bicarbonate and increasing the cation/anion ratio in
the diet on arterial blood oxygen saturation (Squires &
Julian, 2001).

123

Environmental/Management Factors and Ascites

Altitude. The most obvious environmental factor to play
a role in ascites development in broilers is high altitude.
The effect of high altitude (either natural or simulated) is
a decrease in the partial pressure of oxygen. When birds
are exposed to low atmospheric oxygen levels (high
altitude), pulmonary blood vessels constrict and pulmonary vascular resistance increases (Wideman, 1997).
This immediate increase in pulmonary arterial pressure
can, over time, cause right ventricular hypertrophy and
eventually result in ascites syndrome (Wideman et al.,
1998).
Cold temperature. The second most studied environmental cause of pulmonary hypertension and ascites is
temperature. The strong correlation between cold temperature and cardiac hypertrophy/ascites has been recognized for several decades. Cold temperatures increase
ascites by increasing both metabolic oxygen requirements and by increasing pulmonary hypertension (Julian
et al., 1989; Stolz et al., 1992). Wideman & Tackett
(2000) attributed this increase in pulmonary arterial
pressure to a cold-induced increase in cardiac output, as
opposed to being caused by hypoxaemic pulmonary
vasoconstriction. The effect of the timing of a cold stress
on ascites development in broilers indicates that exposure to cold temperatures during brooding has a lasting
effect on ascites incidence (Julian, 2000; Groves, 2002).
The consensus appears to be that cold stress during the
first 2 weeks of life affects the birds metabolic rate for
several weeks and increases their susceptibility to ascites.
Groves (2002) further reported that the duration of the
cold stress is more critical than the minimum temperature reached. He also indicated that exposure to
suboptimal temperatures lead to ascites mortalities
about 2 weeks later and that, after 3 weeks of age,
temperature stress becomes less critical. Interestingly,
ascites was reported to develop 2 weeks after placement
of young birds in a hypobaric chamber and, conversely,
birds stopped developing ascites 2 weeks after removal
from the simulated high altitude (Balog et al., 2001).
Lighting. Broilers are usually grown on a near-continuous lighting schedule so that feed consumption and
growth rate can be maximized. Early studies in photoperiod manipulation reported a decreased growth rate
for broilers raised with a step-down lighting programme
(Classen et al., 1991). It was hypothesized that limiting
the number of hours of light will slow growth slightly
and will reduce activity that requires additional oxygen,
and may actually improve feed efficiency (Julian,
1990a,b). Subsequent studies on the effect of longer
dark periods or intermittent lighting indicated that,
similar to feed restriction, photoperiod manipulations
can decrease the incidence of ascites syndrome (Julian,
1990b, 2000; Hassanzadeh et al., 2000).
Air quality and ventilation. It has been suggested that
poor ventilation could cause low environmental oxygen
or high toxic fumes (carbon monoxide, carbon dioxide
or ammonia), which may have detrimental effects on the
respiratory or cardiovascular systems of birds and
promote ascites development (Wideman, 1998). It also
has been suggested that environmental dust could affect
oxygen transfer in the lung and increase the ascites

124 A. Baghbanzadeh and E. Decuypere

incidence. The hypothetical effects of air quality and

ventilation have been difficult to prove. Although birds
exposed to poorly ventilated conditions have been
reported to develop greater numbers of cartilaginous
and osseous nodules in their lungs and birds with ascites
syndrome have higher numbers of these nodules (Balog,
2003), the causal effect of low ventilation on ascites is
still unproven. In addition, there are a number of reports
of air quality and ventilation not affecting ascites
development (Julian & Wilson, 1992; Julian, 1993,
1995, 2000; McGovern et al., 1999, 2000).

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Conclusions
Ascites, like several other metabolic disorders, is a
multifactorial syndrome, caused by interactions among
environmental, physiological and genetic factors. Forced
selection to achieve faster growing chickens has made the
farmers enjoy the better phenotypical traits resulting
from improved genetic potential; but, due to some
anatomical and physiological limitations, the same
improved potential could have adverse effects on bird
health. Impaired oxygen supply to sustain a continuous
fast growth rate causes may increase the risk for a higher
incidence of ascites syndrome. Selection for breast meat
yield, due to market demand, may impose more threat to
the bird since chickens with a higher percentage of breast
muscle have a lower capillary density (Hoving-Bolink
et al., 2000). The impaired oxygen supply will stimulate
the development of many compensatory mechanisms in
cardiopulmonary systems which, in turn, brings about
ascites syndrome such as hypertension, ventricular
hypertrophy, erythropoietic responses, and so on.
Management practices to limit growth rate, such as
feed restriction, nutrient density and diet form have been
applied. These practices indirectly reduce the need for
oxygen to partly compensate the physiological limitations; on the other hand, efforts have been made to
normalize red blood cell structure and function, and free
radicals scavenged.
In recent years special attention has also been paid to
the factors inside the incubator that may influence
normal epigenesis, predisposing the chicks hatched to
ascites syndrome.

References
Archer, S.L., Johnson, G.J., Gebhard, R.L., Castlemen, W.L., Levine,
A.S., Westcott, J.Y., Voelkel, N.F., Nelson, D.P. & Weir, E.K. (1989).
Effect of dietary fish oil on lung lipid profile and hypoxic pulmonary
hypertension. Journal of Applied Physiology, 66, 16621673.
Balog, J.M. (2003). Ascites syndrome (pulmonary hypertension syndrome) in broiler chickens: are we seeing the light at the end of the
tunnel? Avian and Poultry Biology Reviews, 14(3), 99126.
Balog, M.J., Anthony, N.B., Cooper, M.A., Kidd, B.D., Huff, G.R.,
Huff, W.E. & Rath, N.C. (2000). Ascites syndrome and related
pathologies in feed restricted broilers raised in a hypobaric chamber.
Poultry Science, 79, 318323.
Balog, M.J., Anthony, N.B., Cooper, M.A., Kidd, B.D., Huff, G.R.,
Huff, W.E., Rath, N.C. & Kirby, Y.K. (2001). Effect of timing of
hypobaric exposure on the incidence of ascites syndrome in broilers.
Poultry Science, 80(suppl 1), 262.
Balog, J.M., Kidd, B.D., Huff, G.R., Huff, W.E., Rath, N.C. &
Anthony, N.B. (2003). Effect of cold stress on broilers selected for
resistance or susceptibility to ascites syndrome. Poultry Science, 82,
13831387.

Berlin, E., Bhathena, S.J., Judd, J.T., Nair, P.P., Peters, R.C., Bhagavan,
H.N., Ballard-barbash, R. & Taylor, P.R. (1992). Effects of omega-3
fatty acid and vitamin E supplementation on erythrocyte membrane
fluidity, tocopherols, insulin binding and lipid composition in men.
Journal of Nutrition and Biochemistry, 3, 392400.
Bolukbasi, C., Guzel, M. & Aktas, M.S. (2004). The Effect of early feed
restriction on ascites induced by cold temperatures and growth
performance in broilers. Journal of Applied Animal Research, 26, 89
92.
Bolukbasi, S.C., Aktas, M.S. & Guzel, M. (2005). The effect of feed
regimen on ascites induced by cold temperatures and growth
performance in male broilers. International Journal of Poultry Science,
4(5), 326329.
Bottje, W.G. & Wideman, R.F. (1995). Potential role of free radicals in
the etiology of pulmonary hypertension syndrome. Poultry and Avian
Biological Reviews, 6, 211231.
Bottje, W., Enkvetchakul, B., Moore, R. & McNew, R. (1955). Effect of
a-tocopherol on antioxidants, lipid peroxidation, and the incidence of
pulmonary hypertension syndrome (ascites) in broilers. Poultry
Science, 74, 13561369.
Bottje, W, Erf, G., Bersi, T., Wang, S., Barnes, D. & Beers, K. (1997).
Effect of dietary DL-a-tocopherol on tissue and a- and g-tocopherol
and pulmonary hypertension syndrome (ascites) in broilers. Poultry
Science, 75, 15071512.
Bowes, V.A., Julian, R.J. & Stirtzinger, T. (1989). Comparison of serum
biochemical profiles of male broilers with female broilers and white
leghorn chickens. Canadian Journal of Veterinary Research, 53, 711.
Buys, N., Buyse, J., Hassanzadeh-Ladmakhi, M. & Decuypere, E.
(1998a). Intermittent lighting reduces the incidence of ascites in
broilers: An interaction with protein content of feed on performance
and the endocrine system. Poultry Science, 77, 5461.
Buys, N., Dewil, E., Gonzales, E. & Decuypere, E. (1998b). Different
CO2 levels during incubation interact with hatching time and ascites
susceptibility in two broiler lines selected for different growth rate.
Avian Pathology, 27, 605612.
Buyse, J., Janssens, G.P.J. & Decuypere, E. (2001). The effects of dietary
L-carnitine supplementation on the performance, organ weights and
circulating hormone and metabolite concentrations of broiler chickens reared under a normal or low temperature schedule. British
Poultry Science, 42, 230241.
Camacho, M.A., Suarez, M.E., Herrera, J.G., Cuca, J.M. & GarciaBojalil, C.M. (2004). Effect of age of feed restriction and microelement supplementation to control ascites on production and carcass
characteristics of broilers. Poultry Science, 83, 526532.
Camacho-Fernandez, D., Lopez, C., Avila, E. & Arce, J. (2002).
Evaluation of different dietary treatments to reduce the ascites
syndrome and their effect on corporal characteristics in broiler
chickens. Journal of Applied Poultry Research, 11, 164174.
Cawthorn, D., Beers, K. & Bottje, W.G. (2001). Electron transport chain
defect and inefficient respiration may underlie pulmonary hypertension syndrome (ascites)-associated mitochondrial dysfunction in
broilers. Poultry Science, 80, 474484.
Chineme, C.N., Buyse, J., Hassanzadeh-Ladmakhi, M., Albers,
G.A.A. & Decuypere, E. (1995). Interaction of genotype, egg-shell
conductance and dietary T3 supplementation in the development of
heart-failure syndrome and ascites in broiler-chicken. Archiv fur
Geflu
gelkunde. 59, 129134.
Classen, H.L., Riddell, C. & Robinson, F.E. (1991). Effects of
increasing photoperiod length on performance and health of broiler
chickens. British Poultry Science, 32, 2129.
Coello, C.L., Arce, M.J. & Avila, G.E. (2000). Management techniques
to reduce incidence of ascites and SDS. Proceeding of the XXI
Worlds Poultry Science Association Congress, WPSA, Montreal,
Quebec, Canada.
Coleman, M.A. & Coleman, G. E. (1991). Ascites control through
proper hatchery management. Misset World Poultry, 7, 3335.
Crespo, R. & Shivaprasad, H.L. (2003). Diseases of Poultry 11th edn
(pp. 10721075). Ames: Iowa State Press.
Currie, R.J.W. (1999). Ascites in poultry: recent investigations. Avian
Pathology, 28, 313326.
Decuypere, E. (2002). Ascites as a multifactorial syndrome of broiler
chickens: considerations from a developmental and selection view-

Downloaded by [61.2.96.27] at 01:06 12 February 2015

Ascites in broilers
point. Proceedings of the 2nd Symposium of the World Poultry
Science Association of the Iran Branch (pp. 119136). Tehran, Iran.
Decuypere, E., Buyse, J. & Buys, N. (2000). Ascites in broiler chickens:
exogenous and endogenous structural and functional causal factors.
Worlds Poultry Science Journal, 56, 367376.
Decuypere, E., Hassanzadeh, M. & Buys, N. (2005). Further insights
into the susceptibility of broilers to ascites. Veterinary Journal, 169,
319320.
de Greef, K.H., Janss, L.L.G., Vereiken, A.L.J., Pit, R. & Gerritsen,
C.L.M. (2001). Disease-induced variability of genetic correlations:
ascites in broilers as a case study. Journal of Animal Science, 79, 1723
1733.
Detilleux, J. & Leroy, P.L. (2000). Application of a mixed normal
mixture model for the estimation of mastitis-related parameters.
Journal of Dairy Science. 83, 23412349.
Dewil, E., Buys, N., Albers, G.A.A. & Decuypere, E. (1996). Different
characteristics in chick embryos of two broiler lines differing in
susceptibility to ascites. British Poultry Science, 37, 10031013.
Enkvetchakul, B., Bottje, W., Anthony, N., Moore, R. & Huff, W.
(1993). Compromised antioxidant status associated with ascites in
broilers. Poultry Science, 72, 22722280.
Fedde, M.R. (1984). Respiration in birds. In M. Swenson (Ed.), Dukes
Physiology of Domestic Animals 10th edn. (pp. 255261), Cornell
University Press San Diego, CA, USA.
Fedde, M.R., Weigle, G. E. & Wideman, R. F. (1998). Influence of feed
deprivation on ventilation and gas exchange in broilers: relationship
to pulmonary hypertension syndrome. Poultry Science, 77, 1704
1710.
Groves, P.J. (2002). Environmental determinants of broiler ascites
syndrome. Proceedings of the Australian Poultry Science Symposium
Vol. 14 (pp. 8388). Sydney, Australia.
Hall, S.A. & Machicao, N. (1968). Myocarditis in broiler chickens
reared at high altitude. Avian Diseases, 12, 7584.
Hassanzadeh, M., Buys, N., Dewil, E., Rahimi, G. & Decuypere, E.
(1997). The prophylactic effect of vitamin C supplementation on
broiler ascites incidence and plasma thyroid hormone concentration.
Avian Pathology, 26, 3344.
Hassanzadeh, M., Bozorgmerifard, M.H., Akbari, A.R., Buyse, J. &
Decuypere, E. (2000). Effect of intermittent lighting schedules during
the natural scotoperiod on T3-induced ascites in broiler chickens.
Avian Pathology, 29, 433439.
Hassanzadeh, M., Buyse, J. & Decuypere, E. (2002). Further evidence
for the involvement of cardiac a-adrenergic receptors in right
ventricle hypertrophy and ascites in broiler chickens. Avian Pathology,
31, 177181.
Hoving-Bolink, A.H., Kranen, R.W., Klont, R.E., Gerritsen, C.L.M. &
de Greef, K.H. (2000). Fibre area and capillary supply in broiler
breast muscle in relation to productivity and ascites. Meat Science,
56, 397402.
Hulan, H.W., Ackman, R.G., Ratnayake, W.M.N. & Proudfoot, F.G.
(1989). Omega-3 fatty acid levels and general performance of
commercial broilers fed practical levels of red fish meal. Poultry
Science, 68, 153162.
Issacks, R., Goldman, P. & Kim, C. (1986). Studies on avian erythrocyte
metabolism XIV. Effect of CO2 and pH on P50 in the chicken.
American Journal of Physiology, R260, 250, R266.
Julian, R.J. (1988). Pulmonary hypertension as a cause of right
ventricular failure and ascites in broilers. Zootechnica International,
11, 5862.
Julian, R.J. (1989). Lung volume of meat-type chickens. Avian Disease,
33, 174176.
Julian, R.J. (1998). Rapid growth problems: ascites and skeletal
deformities in broilers, Poultry Science, 77, 17731780.
Julian, R.J. (1990a). Cardiovascular diseases. In F.T.W. Jordan (Ed.),
Poultry Diseases, 3rd edn (pp. 330353). London: Bailliere Tindall.
Julian, R.J. (1990b). Pulmonary hypertension: a cause of right heart
failure, ascites in meat-type chickens. Feedstuffs, 78, 1922.
Julian, R.J. (1993). Ascites in poultry. Avian Pathology, 22, 419454.
Julian, R.J. (1995). Suggestions for reducing ascites in meat-type
chickens. Proceedings of the 44th Western Poultry Disease Conference
(pp. 1920), Sacramento, CA, USA.

125

Julian, R.J. (2000). Physiological management and environmental

triggers of the ascites syndrome: a review. Avian Pathology, 29,
519527.
Julian, R.J. (2005). Production and growth related disorders and other
metabolic diseases of poultry*A review. The Veterinary Journal, 169,
350369.
Julian, R.J. & Mirsalimi, S.M. (1992). Blood oxygen concentration of
fast growing and slow growing broiler chickens, and chickens with
ascites from right ventricular failure. Avian Diseases, 36, 730732.
Julian, R.J. & Wilson, B. (1992). Pen oxygen concentration and
pulmonary hypertension-induced right ventricular failure and ascites
in meat-type chickens at low altitude. Avian Disease, 36, 733735.
Lorenzoni, A.G. & Ruiz-Feria., C.A. (2006). Effects of vitamin E and
L-arginine on cardiopulmonary function and acites parameters in
broiler chickens reared under subnormal temperatures. Poultry
Science, 85, 22412250.
Lubritz, D., Smith, J. & McPherson, B. (1995). Heritability of ascites
and the ratio of right to total ventricle weight in broiler breeder male
lines. Poultry Science, 74, 12371241.
Luger, D., Shinder, D., Wolfenson, D. & Yahav, S. (2003). Erythropoiesis regulation during the development of ascites syndrome in broiler
chickens: A possible role of corticosterone on egg production. Journal
of Animal Science, 81, 784790.
McGovern, R.H., Feddes, J.J.R, Robinson, F.E. & Hanson, J.A. (1999).
Growth performance, carcass characteristics, and the incidence of
ascites in broilers in response to feed restriction and litter oiling.
Poultry Science, 78, 522528.
McGovern, R.H., Feddes, J.J.R., Robinson, F.E. & Hanson, J.A. (2000).
Growth, carcass characteristics, and incidence of ascites in broilers
exposed to environmental fluctuations and oiled litter. Poultry
Science, 79, 324330.
McLachlan, G.J. & Krishnan, T. (1997). The EM algorithm and
extensions. Wiley, New York, NY, USA.
Maxwell, M.H. & Robertson, G.W. (1997). World broiler ascites survey
1996. Poultry International, 36, 1630.
Maxwell, M.H., Robertson, G.W., Bautista Ortega, J. & Hocking, P.M.
(1998). A preliminary estimate of the heritability of plasma troponin
T in broiler chickens. British Poultry Science, 39, 1619.
Mirsalimi, S.M. & Julian, R.J. (1991). Reduced erythrocyte deformability as a possible contributing factor to pulmonary hypertension
and ascites in broiler chickens. Avian Diseases, 35, 374379.
Mirsalimi, S.M., Julian, R.J. & Squires, E.J. (1993). Effect of hypobaric
hypoxia on slow and fast growing chickens fed diets with high and
low protein levels. Avian Diseases, 37, 660667.
Moghadam, H.K., McMillan, I., Chambers, J.R. & Julian, R.J. (2001).
Estimation of genetic parameters for ascites syndrome in broiler
chickens. Poultry Science, 80, 844848.
Olkowski, A.A., Krover, D., Rathgeber, B. & Classen, H. L. (1999).
Cardiac index, oxygen delivery, and tissue oxygen extraction in slow
and fast growing chickens, and in chickens with heart failure and
ascites: a comparative study. Avian Pathology, 28, 137146.
Olkowski, A.A., Wajnarowicz, C., Rathgeber, B.M., Abbott, J.A. &
Classen, H.L. (2003). Lesions of pericardium and their significance in
the aetiology of heart failure in broiler chickens. Research in
Veterinary Science, 74, 203211.
Olkowski, A.A., Nain, S., Wajnarowicz, C., Laarveld, B., Alcorn, J. &
Ling, B.B. (2007). Comparative study of myocardial high energy
phosphate substrate content in slow and fast growing chicken and in
chickens with heart failure and ascites. Comparative Biochemistry
and Physiology, Part A: Molecular & Integrative Physiology (148) 1,
230238.
Owen, R.L., Wideman, R.F., Hattel, A.L. & Cowen, B.S. (1990). Use of
a hypobaric chamber as a model system for investigating ascites in
broilers. Avian Diseases, 34, 754758.
Ozkan, S., Plavnik, I. & Yahav, S. (2006). Effects of early feed restriction
on performance and ascites development in broiler chickens subsequently raised at low ambient temperature. Journal of Applied Poultry
Research, 15, 919.
Packer, L., Valenza, M., Serbinosa, E., Starke-Reed, P., Frost, K. &
Kagan, V. (1991). Free radical scavenging is involved in the protective
effects of L-propionyl-carnitine against ischemia reperfusion injury
of the heart. Archive Biochemistry Biophysics, 288, 533537.

Downloaded by [61.2.96.27] at 01:06 12 February 2015

126 A. Baghbanzadeh and E. Decuypere

Pakdel, A., Van-Arendonk, J.A.M., Vereijken, A.L.J. & Bovenhuis, H.
(2002). Direct and maternal genetic effects for ascites-related traits in
broilers. Poultry Science, 81, 12731279.
Pakdel, A., Rabie, T., Veenendaal, T., Crooijmans, R.P.M.A., Groenen,
M.A.M., Vereijken, A.L.J., Van Arendonk, J.A.M. & Bovenhuis, H.
(2004). Genetic analysis of ascites-related traits in broilers. Doctoral
thesis, Animal Breeding and Genetics Group, Department of Animal
Sciences, Wageningen University, The Netherlands, p. 144.
Pakdel, A., Bijma, P., Ducro, B.J. & Bovenhuis, H. (2005). Selection
strategies for body weight and reduced ascites susceptibility in
broilers. Poultry Science, 84, 528535.
Peacock, A.J., Pickett, I.C., Morris, K. & Reeves, J.T. (1989). The
relationship between rapid growth and pulmonary hemodynamics in
the fast-growing broiler chicken. American Review of Respiratory
Diseases, 139, 15241530.
Piiper, J. & Scheid, P. (1975). Gas transport efficacy of gills, lungs and
skin: theory and experimental data. Respiratory Physiology, 23, 209
221.
Powell, F.L. (2000). Respiration. In: G.C. Whittow (Ed.), Sturkies
Avian Physiology 5th edn (pp. 233264). Academic Press San Diego,
CA, USA.
Reeves, J.T., Ballam, G., Hofmeister, S., Picket, C., Morris, K. &
Peacock, A. (1991). Improved arterial oxygenation with feed restriction in rapidly growing broiler chickens. Comparative Biochemistry
and Physiology, Part A, Physiology, 99, 3, 481485.
Riddell, C. (1991). Developmental, metabolic, and miscellaneous
disorders. In B.W. Calnek, H.J. Barnes, C.W. Beard, W.M. Reid &
H.W. Yoder, Jr. (Eds.), Diseases of Poultry 9th edn (pp. 839841).
Ames: Iowa State University.
Rouwet, E.V., Tintu, A.N., Schellings, M.V.M., Van Bilsen, M.,
Lutgens, E., Hofstra, L., Slaaf, D.W., Ramsay, G. & Le Noble,
F.A.C. (2002). Hypoxia induces aortic hypertrophic growth, left
ventricular dysfunction and sympathetic hyper innervation of peripheral arteries in the chick embryo. Circulation, 105, 27912796.
Ruiz-Lopez, B. & Austic, R.E. (1993). The effect of selected minerals on
the acidbase balance of growing chicks. Poultry Science, 72, 1054
1062.
Sahan, U., Ipek, A., Altan, O. & Yilmaz-Dikmen, B. (2006). Effects of
oxygen supplementation during the last stage of incubation on broiler
performance, ascites susceptibility and some physiological traits.
Animal Research, 55, 145152.
Scheele, C.W. (1996). Ascites in chickens, Thesis, Landbouwuniversiteit,
Wageningen, The Netherlands.
Scheele, C.W., Van Der Klis, J.D., Kwakernaak, C., Buys, N. &
Decuypere, E. (2003). Hematological characteristics predicting
susceptibility for ascites. 2. High haematocrit values in juvenile
chickens. British Poultry Science, 44, 484489.
Shlosberg, A., Bellaiche, M., Zeitlin, G., Yaacobi, M. & Cahaner, A.
(1996). Hematocrit values and mortality from ascites in cold stressed
broilers from parents selected by hematocrit. Poultry Science, 75,
15.
Shlosberg, A., Belaiche, M., Berman, E., Perk, S., Deeb, N., Neumark,
E. & Cahaner, A. (1998). Relationship between broiler chicken
hematocrit-selected parents and their progeny with regard to
hematocrit, mortality from ascites and body weight. Research in
Veterinary Science, 64, 105109.

Smith, F.M., West, N.H. & Jones, D.R. (2000). The cardiovascular
system. In G.C. Whittow (Ed.), Sturkies Avian Physiology 5th edn
(pp. 141231). Academic Press.
Squires, E.J. & Julian, R.J. (2001). The effect of dietary chloride and
bicarbonate on blood pH, haematological variables, pulmonary
hypertension and ascites in broiler chickens. British Poultry Science,
42, 207212.
Stinefelt, B.M. (2003). Uric acid as an antioxidant and the effect of
changes in plasma uric acid concentrations on broiler susceptibility
to ascites, MSc Thesis, Davis College of Agriculture, Forestry, and
Consumer Sciences At West Virginia University, WV, USA.
Stolz, J.L., Rosenbaum, L.M., Jeong, D. & Odom, T.W. (1992). Ascites
syndrome, mortality and cardiological responses of broiler chickens
subjected to cold exposure. Poultry Science, 71(Suppl 1), 4.
Villar-Patino, G., Diaz-Cruz, A., Avila-Gonzalez, E., Guinzberg, R.,
Pablos, J.L. & Pina, E. (2002). Effects of dietary supplementation
with vitamin C or vitamin E on cardiac lipid peroxidation and
growth performance in broilers at risk of developing ascites
syndrome. American Journal of Veterinary Research. 63, 5, 673676.
Walton, J-P., Bond, J.M., Julian, R.J. & Squires, E.J. (1999). Effect of
dietary flax oil and hypobaric hypoxia on pulmonary hypertension
and haematological variables in broiler chickens. British Poultry
Science, 40, 385391.
Wideman, R.F. (1997). Understanding pulmonary hypertension syndrome (ascites). Hubbard Farms Technical Report (pp. 16), Walpole,
NH, USA.
Wideman, R.F. (1998). Causes and control of ascites in broilers.
National Meeting on Poultry Proceeding, 33, 5685.
Wideman, R.F. (2000). Cardio-pulmonary hemodynamics and ascites in
broiler chickens. Avian and Poultry Biology Review, 11, 2143.
Wideman, R.F. (2001). Pathophysiology of heart/lung disorders:
pulmonary hypertension syndrome in broiler chickens. World Poultry
Science Journal, 57, 289307.
Wideman, R.F. & Tackett, C. (2000). Cardiopulmonary function in
broilers reared at warm or cold temperatures: effect of acute
inhalation of 100% oxygen. Poultry Science, 79, 257264.
Wideman, R.F., Kirby, Y.K., Owen, R.L. & French, H. (1997). Chronic
unilateral occlusion of an extrapulmonary primary bronchus induces
pulmonary hypertension syndrome (ascites) in male and female
broilers. Poultry Science, 76, 400404.
Wideman, R.F., Wing, T., Kirby, Y.K., Forman, M.F., Marson, N.,
Tackett, C.D. & Ruiz-Feria, C.A. (1998). Evaluation of minimally
invasive indices for predicting ascites susceptibility in three successive
hatches of broilers exposed to cool temperatures. Poultry Science, 77,
15651573.
Wideman, R.F., Hooge, D.M. & Cummings, K.R. (2003). Dietary
sodium bicarbonate, cool temperatures, and feed withdrawal: impact
on arterial and venous blood-gas values in broilers. Poultry Science,
82, 560570.
Wise, D.R. & Evans, E.T.R. (1975). Turkey syndrome 65, oedema
syndrome and mycoplasma meleagridis. Research in Veterinary
Science, 18, 190192.
Zerehdaran, S., Van Grevehof, E.M., Van Der Waaij, E.H. &
Bovenhuis, H. (2006). A Bivariate mixture model analysis of body
weight and ascites traits in broilers. Poultry Science, 85, 3238.