Professional Documents
Culture Documents
Ascites Syndrome in Broilers Physiological and Nutritional Perspectives
Ascites Syndrome in Broilers Physiological and Nutritional Perspectives
Ascites Syndrome in Broilers Physiological and Nutritional Perspectives
REVIEW ARTICLE
Ascites syndrome in broilers: physiological and nutritional
perspectives
A. Baghbanzadeh1* and E. Decuypere2
1
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 hypertension syndrome, or ‘‘water belly’’) is a metabolic
intensely selected for higher growth rates and so disorder, characterized by hypoxaemia, increased work-
indirectly for a high rate of protein synthesis, which load of the cardiopulmonary system, central venous
requires more oxygen (Decuypere et al., 2005), increased congestion (Luger et al., 2003), an excessive accumula-
feed conversion (Decuypere et al., 2000; Pakdel et al., tion of fluid in body coelomic cavities (Olkowski et al.,
2002), egg production (Decuypere et al., 2000) or meat 1999), hypertrophy of the right ventricle and a flaccid
yield and breast percentage (Hoving-Bolink et al., 2000). heart (Riddell, 1991), and finally death (Luger et al.,
Modern strains of broilers are able to achieve market 2003). A high incidence of ascites can occur when
weight in 60% less time than broilers of 40 years ago. broilers are reared at altitudes high enough to substan-
Nevertheless, the pulmonary and cardiac capacity of tially reduce the partial pressure of oxygen (Owen et al.,
modern broilers is very similar to the old broiler strains, 1990; Wideman et al., 2003). Studies showed a high
which forces their cardiopulmonary system to work very incidence of subclinical heart disease in fast-growing
close to its physiological limit (Lorenzoni et al., 2006). broilers, with many developing clinical signs of chronic
The lung capacity does not always meet the oxygen heart failure and ascites. Recently, a novel observation
demands necessary for rapid growth. This results in was reported where sudden death in broilers was
impaired ability to regulate the energy balance under associated with rupture of the right atrium (Olkowski
extreme conditions, such as low ambient temperature or et al., 2007). Although the incidence of this metabolic
high altitude (Luger et al., 2003). If the lung of the disorder in well-managed flocks is very low, it causes
chicken grows less rapidly than the rest of the body, important economic losses to the poultry breeding
hypoxia and ascites could result (Julian, 2000). Recent industry*an estimated 4.7% of the broilers worldwide
data suggest that ascites is not caused by an increased have the disease (Maxwell & Robertson, 1997). It is
oxygen requirement of fast growth rate per se at low estimated that 5% of broilers and 20% of roaster birds
altitude, but by an impaired oxygen supply to sustain fast die of ascites (Balog, 2003); considering that an esti-
growth rate (Decuypere et al., 2005). Ascites (pulmonary mated 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 and do not expand like the (alveolar) lungs of mammals
ascites are significant. Genetic, physiological, environ- (Balog, 2003). In other words, the avian respiratory
mental, and management factors all seem to interact to system possesses rigid lungs of fixed volume (Fedde,
produce a cascade of events that culminate in ascites 1984), which do not expand or contract with each breath
syndrome. 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
Aetiology of the Ascites Syndrome increased blood flow (Julian, 1998).
Despite the intensive investigation of the syndrome for Pressure, generated by cardiac contraction, drives
many years, the primary cause of ascites is unclear blood flow around the circulation. Poiseuille’s law relates
(Crespo & Shivaprasad, 2003). The physiology of this volume flow (Q) to the pressure drop (P1 P2) along a
syndrome (see Figure 1) has been extensively studied tube of radius (r) and length (L) during steady flow as
(Julian, 1993, 2000; Scheele, 1996; Hassanzadeh et al., follows:
1997; Decuypere et al., 2000; Wideman, 2000). Ascites
syndrome, first reported in flocks of broiler chickens pr4
reared at high altitudes in Bolivia (Hall & Machicao, Q (P1 P2 ) (p is blood viscosity)
8mL
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). Vascular resistance (R) will be calculated as:
Obstruction of lymph drainage, decreased plasma onco-
tic pressure, fluid leakage secondary to increased vas-
cular permeability, and, last but not least, increased P1 P2
R
portal pressure secondary to right ventricular failure or Q
liver damage may all result in ascites (Julian, 2005).
Neoplasia, most frequently, oviduct carcinomas and,
alternatively, right ventricular failure with valvular It is obvious that a slight change in a vessel radius has
insufficiency, in which high venous pressure in the vena major effects on flow and, consequently, on resistance
cava interferes with lymph return, may bring about characteristics.
blockage of lymph and, subsequently, ascites (Balog, On the other hand, the FrankStarling law of the
2003). Since plasma proteins, especially albumin, are heart describes an increase in contractility of the
mainly responsible for blood oncotic pressure, some myocardium due to an elevated preload. In terms of
researchers (Wise & Evans, 1975; Bowes et al., 1989) the right ventricle, preload is determined by cardiac
explained decreased plasma proteins in ascites-sensitive venous return. This mechanism increases cardiac output
broilers or those with ascites. Decreased plasma protein by elevating the stroke volume. If pulmonary vascular
could be a result of loss of high-protein lymph from the resistance increases, the afterload increases, leading to a
liver or a stop-eating process due to right ventricular pressure overload in the right ventricle. The classical
hypertrophy. Vascular damage and subsequent leakage response to this stimulus is ventricular hypertrophy, one
of fluid and proteins through the vascular epithelium can of the common lesions in ascitic birds. One important
be caused by viral and/or bacterial infections, chemical consequence of ventricular hypertrophy is distortion of
toxins, chlorinated hydrocarbons and some phenolic atrio-ventricular valves, which also become thicker, leaky
compounds, coal-tar derivatives, dioxin, and pentacho- and less efficient (see below, Avian Heart Valves
lorophenol (Balog, 2003). Increased vascular hydraulic Anatomy) and the production of regurgitant flow from
pressure could be a result of hepatic pathologies, right the ventricle to the atrium during ventricular systole.
atrioventricular valve pathologies, pulmonary hyperten- The ventricle is then subjected to volume overload and
sion and miscellaneous cardiac pathologies (Currie, the resultant haemodynamic pressure imbalance gener-
1999). ates ascites (Currie, 1999).
Pulmonary Hypertension
Avian Heart Valves Anatomy
Pulmonary hypertension is the result of processes taking
place in both respiratory and cardiovascular systems. Blood entering the left ventricle from the left atrium on
The architecture of the modern broilers*small stature, atrial systole passes through an orifice guarded by a
the large, heavy breast mass, the pressure from abdom- membranous atrioventricular valve, similar in general
inal contents on air sacs, and the small lung volume* structure to a mammalian atrioventricular valve, except
may all be involved in the increased incidence of ascites that it is tricuspid. Blood passing from the right atrium
syndrome (Julian, 1998; Balog, 2003). Theoretically, the to the right ventricle enters through an orifice guarded
unique anatomy of the avian respiratory system results by an atrioventricular valve that is structurally unique to
in a model of gas exchange that is more efficient than the birds. In pronounced contrast to the fibrous structure
mammalian model (Piiper & Scheid, 1975), and for a characteristic of the mammalian tricuspid valve, in birds
given level of ventilation to the gas-exchange surfaces, the right atrioventricular valve consists of a single spiral
cardiac output, and lung diffusing capacity, arterial O2 flap of myocardium attached obliquely to the free wall of
loading and CO2 elimination are predicted to be better in the right ventricle, so it is capable of becoming thicker
a parabronchial lung, compared with an alveolar lung and leaky, as a consequence of ventricular hypertrophy.
with the same inspired gases and metabolic demands The outflow valves from the right and left ventricles are,
(Powell, 2000). But the rigid (parabronchial) lungs of at first glance, more conventional (mammalian) in
birds conform closely to the contour of the body cavity nature (Smith et al., 2000).
Ascites in broilers 119
Cold
Moderate heat
Activity
High altitude Hyperthyroidism
(decreased pO2) Elevated muscle mass
Over-eating
Increased pressure
Some broilers develop lung
in
oedema and die at this stage.
the pulmonary arteries, arterioles & capillaries
Ascites
to distinguish between healthy and diseased birds (de 2002). Feed restriction can reduce the availability of
Greef et al., 2001). Using mixture models, birds can be nutrients and pigmentation precursors, which may have
assigned to different distributions via probabilities a direct effect on weight gain, muscle mass, and the
estimated from trait observations (Detilleux & Leroy, profitcost relationship. These effects could be more
2000). For ascites traits, a mixture model in its simplest pronounced if the restriction programme was not correct
form may be used to assign observations to two (Camacho-Fernandez et al., 2002).
components; that is, ascitic and non-ascitic. The identi-
fication and culling of birds could then be based on the Nutrient density. Reducing the concentration of nutrients
probability of putative ascites, given ascites indicator in a diet can reduce the growth rate, with the effects most
traits, rather than on crude ascites traits (Zerehdaran pronounced from 0 to 21 days of age, during the time
et al., 2006). 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
Nutrition and Ascites
relatively small unless the decrease in density is very
The broiler growth rate has been found to have a direct large. However, even moderately lower nutrient density
relationship with susceptibility to ascites (Camacho reduces mortality due to ascites (Camacho-Fernandez
et al., 2004). Manipulation of the diet composition et al., 2002).
and/or feed allocation system can have a major effect
on the incidence of ascites. In most instances, such Diet form. Most meat birds are fed crumbled or pelleted
changes to the feeding programme influence ascites via diets to achieve maximum growth and feed efficiency.
their effect on growth rate. Major nutritional factors Feeding mash reduces growth rate (1 to 2 days to
including high nutrient density rations, high feed intake market) and reduces mortality and condemnations due
and feed form are known to influence the occurrence of to metabolic disease. However, this type of programme
ascites in broilers (Balog et al., 2000; Coello et al., 2000; may not be economically acceptable in all areas and has
Bölükbasi et al., 2004; Ozkan et al., 2006). been demonstrated to increase the incidence of pendu-
lous crops. Broilers that consume pellet feed have
frequently been shown to have higher incidences of
Managing the Growth Rate ascites than broilers that consume the same diet in mash
Although the growth rate can influence metabolic form (Bölükbasi et al., 2005).
diseases during the entire period of broiler production,
research has shown that the early period is particularly Omega-3 fatty acid sources (flax and fish oils). It has
important (Camacho et al., 2004). A reduced growth been found that decreased deformity of the erythrocytes,
rate from 3 to 14 days of age not only benefits bird as measured by the filtration index, can increase the
health during that period but also later when the growth amount of ascites in broiler chickens (Mirsalimi &
rate is as fast or faster than birds that have not Julian, 1991; Mirsalimi et al., 1993). The deformity of
experienced slower early growth. These suggest that erythrocytes is reduced by hypoxaemia. Studies with
early days of production represents an important devel- humans have demonstrated that erythrocyte deformity
opmental period in poultry meat stocks. Recently, can be increased by dietary supplementation of omega-3
management strategies have been investigated to alter (n-3) fatty acids from fish oils (Berlin et al., 1992).
the growth curve of meat stocks with the objective of Archer et al. (1989) found that supplementation with fish
reducing the incidence of metabolic diseases while oil reduces blood viscosity and right ventricular hyper-
maintaining competitive production traits. Methods trophy in rats. However, other studies (Hulan et al.,
have included quantitative and qualitative feed restric- 1989) reported a reduction in the growth rate of birds fed
tion, altered feed form, and environmental management. red fish meal as a source of omega-3 fatty acids. This is
important, because the incidence of ascites can be
Feed restriction. Feed restriction techniques have ranged reduced by slowing the growth rate of broilers (Julian,
from very severe (maintenance only) to milder forms, 1993). The increased content of unsaturated fatty acids
which involve daily feed restriction or skipping feeding 1 probably increases the fluidity of the erythrocyte mem-
or 2 days a week. Feed restriction has proven successful brane and alters membrane function to increase the
in reducing metabolic disease such as ascites, but the deformability of the erythrocytes and potentially help
degree of restriction required to control health problems reduce the incidence of ascites. This could explain the
needs to be balanced with the time required to reach reduction in whole blood viscosity under hypobaric
market weight and other effects on bird productivity. conditions with feeding of flax oil. These factors together
Feed restriction reduces growth at a critical time in a would decrease the resistance to blood flow and improve
broiler chick’s lifecycle when it is the most susceptible to the movement of the erythrocytes through the capillaries,
metabolic disease due to its high oxygen demands (Balog thus improving oxygen transport and decreasing ascites
et al., 2000; Coello et al., 2000; Ozkan et al., 2006). (Walton et al., 1999).
Despite some of the advantages of feed restriction as a
treatment to reduce ascites, adverse secondary effects L-Carnitine. It is generally accepted that endogenous L-
might result due to lower consumption of anticoccidial carnitine synthesis together with its dietary intake should
products fed to control coccidiosis. Another important be sufficient for normal function. However, in cases of
problem resulting from feed restriction programmes is increased metabolic rate (in fasting-growth broilers),
poor pigmentation, which is directly related to the when energy demands are elevated, the availability of
quantity of xanthophylls consumed. Pigmentation is L-carnitine may become a limiting factor for fat oxida-
very important because it is perceived as a measure of tion. In these circumstances, additional exogenous l-
quality in the marketplace (Camacho-Fernandez et al., carnitine might prove beneficial. It is hypothesized that
122 A. Baghbanzadeh and E. Decuypere
determine gaseous exchange) to affect the total incuba- Environmental/Management Factors and Ascites
tion time and, thereby, influence the susceptibility to
Altitude. The most obvious environmental factor to play
ascites and related physiological responses in later
a role in ascites development in broilers is high altitude.
postnatal life (Chineme et al., 1995).
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
pH and Ascites altitude), pulmonary blood vessels constrict and pul-
monary vascular resistance increases (Wideman, 1997).
Ascites is ultimately caused by an imbalance between the This immediate increase in pulmonary arterial pressure
oxygen supply to the body tissues and the oxygen can, over time, cause right ventricular hypertrophy and
requirement of the tissues (Julian, 1993). Poor tissue eventually result in ascites syndrome (Wideman et al.,
oxygenation can be caused by an increased oxygen 1998).
requirement of the tissues due to increased metabolism
from rapid growth (Peacock et al., 1989) or in response Cold temperature. The second most studied environ-
to cold temperature; by a decreased availability of mental cause of pulmonary hypertension and ascites is
oxygen in the environment due to high altitude (hypo- temperature. The strong correlation between cold tem-
baric conditions) or poor ventilation; or by low oxygen perature and cardiac hypertrophy/ascites has been re-
content of the blood because of low haemoglobin cognized for several decades. Cold temperatures increase
oxygen affinity or decreased blood oxygen capacity of ascites by increasing both metabolic oxygen require-
haemoglobins or low oxygen exchange in the lung ments and by increasing pulmonary hypertension (Julian
(Julian, 1993). Ascites can be reduced by decreasing et al., 1989; Stolz et al., 1992). Wideman & Tackett
the oxygen requirements of the bird (such as by reducing (2000) attributed this increase in pulmonary arterial
growth rate and avoiding cold) or increasing oxygen pressure to a cold-induced increase in cardiac output, as
delivery to the tissues. opposed to being caused by hypoxaemic pulmonary
In mammals, acidosis causes vasoconstriction, while vasoconstriction. The effect of the timing of a cold stress
alkalosis causes vasodilation, which affects pulmonary on ascites development in broilers indicates that expo-
arterial pressure and pulmonary hypertension. The sure to cold temperatures during brooding has a lasting
blood pH also affects the affinity of haemoglobin for effect on ascites incidence (Julian, 2000; Groves, 2002).
oxygen in the lung and release of oxygen to the tissues The consensus appears to be that cold stress during the
(the Bohr effect). A decrease in blood pH lowers the first 2 weeks of life affects the bird’s metabolic rate for
oxygen affinity of haemoglobin, which encourages several weeks and increases their susceptibility to ascites.
release in the tissues, while increased blood pH increases Groves (2002) further reported that the duration of the
oxygen affinity to increase haemoglobin saturation in the cold stress is more critical than the minimum tempera-
lung (Issacks et al., 1986). The feeding of excess chloride ture reached. He also indicated that exposure to
or sulphate has been shown to depress blood pH and suboptimal temperatures lead to ascites mortalities
bicarbonate levels in chickens (Ruiz-Lopez & Austic, about 2 weeks later and that, after 3 weeks of age,
1993), while feeding bicarbonate would be expected to temperature stress becomes less critical. Interestingly,
increase blood pH. It has been suggested that broiler ascites was reported to develop 2 weeks after placement
chickens that have a high metabolic rate may be in a state of young birds in a hypobaric chamber and, conversely,
of metabolic acidosis when they are on full feed (Julian, birds stopped developing ascites 2 weeks after removal
1993). Several workers have shown that fast-growing from the simulated high altitude (Balog et al., 2001).
birds have lower blood oxygen concentration than slow-
growing birds; likewise, birds on full feed have lower Lighting. Broilers are usually grown on a near-contin-
blood oxygen than food-deprived birds (Fedde et al., uous lighting schedule so that feed consumption and
1998; Julian & Mirsalimi, 1992; Reeves et al., 1991). growth rate can be maximized. Early studies in photo-
Feeding low chloride/high bicarbonate diets results in a period manipulation reported a decreased growth rate
decrease in pulmonary hypertension. Conversely, feeding for broilers raised with a step-down lighting programme
diets with high chloride content tends to increase the (Classen et al., 1991). It was hypothesized that limiting
incidence of ascites. Increased blood pH would increase the number of hours of light will slow growth slightly
oxygen haemoglobin affinity, which is low in fully fed and will reduce activity that requires additional oxygen,
broilers, probably because of metabolic acidosis. It has and may actually improve feed efficiency (Julian,
been demonstrated that decreased blood pH results in 1990a,b). Subsequent studies on the effect of longer
increased pulmonary arterial pressure in mammals and dark periods or intermittent lighting indicated that,
this may also be true in birds. Increased blood pH can similar to feed restriction, photoperiod manipulations
improve the loading of oxygen by haemoglobin in the can decrease the incidence of ascites syndrome (Julian,
lung due to the Bohr effect. It therefore appears that 1990b, 2000; Hassanzadeh et al., 2000).
supplementing broilers with bicarbonate may be bene-
ficial in fast-growing birds with very high oxygen Air quality and ventilation. It has been suggested that
requirements and high production of carbon dioxide, poor ventilation could cause low environmental oxygen
as long as the decreased pH normally present in the or high toxic fumes (carbon monoxide, carbon dioxide
muscles that facilitates oxygen unloading is not affected. or ammonia), which may have detrimental effects on the
Further work is needed to establish the mode of action respiratory or cardiovascular systems of birds and
of bicarbonate and increasing the cation/anion ratio in promote ascites development (Wideman, 1998). It also
the diet on arterial blood oxygen saturation (Squires & has been suggested that environmental dust could affect
Julian, 2001). oxygen transfer in the lung and increase the ascites
124 A. Baghbanzadeh and E. Decuypere
incidence. The hypothetical effects of air quality and Berlin, E., Bhathena, S.J., Judd, J.T., Nair, P.P., Peters, R.C., Bhagavan,
ventilation have been difficult to prove. Although birds H.N., Ballard-barbash, R. & Taylor, P.R. (1992). Effects of omega-3
fatty acid and vitamin E supplementation on erythrocyte membrane
exposed to poorly ventilated conditions have been
fluidity, tocopherols, insulin binding and lipid composition in men.
reported to develop greater numbers of cartilaginous
Journal of Nutrition and Biochemistry, 3, 392400.
and osseous nodules in their lungs and birds with ascites Bölükbasi, C., Güzel, M. & Aktas, M.S. (2004). The Effect of early feed
syndrome have higher numbers of these nodules (Balog, restriction on ascites induced by cold temperatures and growth
2003), the causal effect of low ventilation on ascites is performance in broilers. Journal of Applied Animal Research, 26, 89
still unproven. In addition, there are a number of reports 92.
of air quality and ventilation not affecting ascites Bölükbasi, S.C., Aktas, M.S. & Güzel, M. (2005). The effect of feed
development (Julian & Wilson, 1992; Julian, 1993, regimen on ascites induced by cold temperatures and growth
1995, 2000; McGovern et al., 1999, 2000). 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
Conclusions
Biological Reviews, 6, 211231.
Ascites, like several other metabolic disorders, is a Bottje, W., Enkvetchakul, B., Moore, R. & McNew, R. (1955). Effect of
multifactorial syndrome, caused by interactions among a-tocopherol on antioxidants, lipid peroxidation, and the incidence of
environmental, physiological and genetic factors. Forced pulmonary hypertension syndrome (ascites) in broilers. Poultry
selection to achieve faster growing chickens has made the Science, 74, 13561369.
Bottje, W, Erf, G., Bersi, T., Wang, S., Barnes, D. & Beers, K. (1997).
farmers enjoy the better phenotypical traits resulting
Effect of dietary DL-a-tocopherol on tissue and a- and g-tocopherol
from improved genetic potential; but, due to some
and pulmonary hypertension syndrome (ascites) in broilers. Poultry
anatomical and physiological limitations, the same Science, 75, 15071512.
improved potential could have adverse effects on bird Bowes, V.A., Julian, R.J. & Stirtzinger, T. (1989). Comparison of serum
health. Impaired oxygen supply to sustain a continuous biochemical profiles of male broilers with female broilers and white
fast growth rate causes may increase the risk for a higher leghorn chickens. Canadian Journal of Veterinary Research, 53, 711.
incidence of ascites syndrome. Selection for breast meat Buys, N., Buyse, J., Hassanzadeh-Ladmakhi, M. & Decuypere, E.
yield, due to market demand, may impose more threat to (1998a). Intermittent lighting reduces the incidence of ascites in
the bird since chickens with a higher percentage of breast broilers: An interaction with protein content of feed on performance
muscle have a lower capillary density (Hoving-Bolink and the endocrine system. Poultry Science, 77, 5461.
et al., 2000). The impaired oxygen supply will stimulate Buys, N., Dewil, E., Gonzales, E. & Decuypere, E. (1998b). Different
the development of many compensatory mechanisms in CO2 levels during incubation interact with hatching time and ascites
susceptibility in two broiler lines selected for different growth rate.
cardiopulmonary systems which, in turn, brings about
Avian Pathology, 27, 605612.
ascites syndrome such as hypertension, ventricular
Buyse, J., Janssens, G.P.J. & Decuypere, E. (2001). The effects of dietary
hypertrophy, erythropoietic responses, and so on. L-carnitine supplementation on the performance, organ weights and
Management practices to limit growth rate, such as circulating hormone and metabolite concentrations of broiler chick-
feed restriction, nutrient density and diet form have been ens reared under a normal or low temperature schedule. British
applied. These practices indirectly reduce the need for Poultry Science, 42, 230241.
oxygen to partly compensate the physiological limita- Camacho, M.A., Suarez, M.E., Herrera, J.G., Cuca, J.M. & Garcia-
tions; on the other hand, efforts have been made to Bojalil, C.M. (2004). Effect of age of feed restriction and microele-
normalize red blood cell structure and function, and free ment supplementation to control ascites on production and carcass
radicals scavenged. characteristics of broilers. Poultry Science, 83, 526532.
In recent years special attention has also been paid to Camacho-Fernandez, D., Lopez, C., Avila, E. & Arce, J. (2002).
the factors inside the incubator that may influence Evaluation of different dietary treatments to reduce the ascites
normal epigenesis, predisposing the chicks hatched to syndrome and their effect on corporal characteristics in broiler
chickens. Journal of Applied Poultry Research, 11, 164174.
ascites syndrome.
Cawthorn, D., Beers, K. & Bottje, W.G. (2001). Electron transport chain
defect and inefficient respiration may underlie pulmonary hyperten-
sion syndrome (ascites)-associated mitochondrial dysfunction in
References broilers. Poultry Science, 80, 474484.
Chineme, C.N., Buyse, J., Hassanzadeh-Ladmakhi, M., Albers,
Archer, S.L., Johnson, G.J., Gebhard, R.L., Castlemen, W.L., Levine, G.A.A. & Decuypere, E. (1995). Interaction of genotype, egg-shell
A.S., Westcott, J.Y., Voelkel, N.F., Nelson, D.P. & Weir, E.K. (1989). conductance and dietary T3 supplementation in the development of
Effect of dietary fish oil on lung lipid profile and hypoxic pulmonary heart-failure syndrome and ascites in broiler-chicken. Archiv fur
hypertension. Journal of Applied Physiology, 66, 16621673. Geflügelkunde. 59, 129134.
Balog, J.M. (2003). Ascites syndrome (pulmonary hypertension syn- Classen, H.L., Riddell, C. & Robinson, F.E. (1991). Effects of
drome) in broiler chickens: are we seeing the light at the end of the increasing photoperiod length on performance and health of broiler
tunnel? Avian and Poultry Biology Reviews, 14(3), 99126. chickens. British Poultry Science, 32, 2129.
Balog, M.J., Anthony, N.B., Cooper, M.A., Kidd, B.D., Huff, G.R., Coello, C.L., Arce, M.J. & Avila, G.E. (2000). Management techniques
Huff, W.E. & Rath, N.C. (2000). Ascites syndrome and related to reduce incidence of ascites and SDS. Proceeding of the XXI
pathologies in feed restricted broilers raised in a hypobaric chamber. World’s Poultry Science Association Congress, WPSA, Montreal,
Poultry Science, 79, 318323. Quebec, Canada.
Balog, M.J., Anthony, N.B., Cooper, M.A., Kidd, B.D., Huff, G.R., Coleman, M.A. & Coleman, G. E. (1991). Ascites control through
Huff, W.E., Rath, N.C. & Kirby, Y.K. (2001). Effect of timing of proper hatchery management. Misset World Poultry, 7, 3335.
hypobaric exposure on the incidence of ascites syndrome in broilers. Crespo, R. & Shivaprasad, H.L. (2003). Diseases of Poultry 11th edn
Poultry Science, 80(suppl 1), 262. (pp. 10721075). Ames: Iowa State Press.
Balog, J.M., Kidd, B.D., Huff, G.R., Huff, W.E., Rath, N.C. & Currie, R.J.W. (1999). Ascites in poultry: recent investigations. Avian
Anthony, N.B. (2003). Effect of cold stress on broilers selected for Pathology, 28, 313326.
resistance or susceptibility to ascites syndrome. Poultry Science, 82, Decuypere, E. (2002). Ascites as a multifactorial syndrome of broiler
13831387. chickens: considerations from a developmental and selection view-
Ascites in broilers 125
point. ‘Proceedings of the 2nd Symposium of the World Poultry Julian, R.J. (2000). Physiological management and environmental
Science Association of the Iran Branch (pp. 119136). Tehran, Iran. triggers of the ascites syndrome: a review. Avian Pathology, 29,
Decuypere, E., Buyse, J. & Buys, N. (2000). Ascites in broiler chickens: 519527.
exogenous and endogenous structural and functional causal factors. Julian, R.J. (2005). Production and growth related disorders and other
Worlds Poultry Science Journal, 56, 367376. metabolic diseases of poultry*A review. The Veterinary Journal, 169,
Decuypere, E., Hassanzadeh, M. & Buys, N. (2005). Further insights 350369.
into the susceptibility of broilers to ascites. Veterinary Journal, 169, Julian, R.J. & Mirsalimi, S.M. (1992). Blood oxygen concentration of
319320. fast growing and slow growing broiler chickens, and chickens with
de Greef, K.H., Janss, L.L.G., Vereiken, A.L.J., Pit, R. & Gerritsen, ascites from right ventricular failure. Avian Diseases, 36, 730732.
C.L.M. (2001). Disease-induced variability of genetic correlations: Julian, R.J. & Wilson, B. (1992). Pen oxygen concentration and
ascites in broilers as a case study. Journal of Animal Science, 79, 1723 pulmonary hypertension-induced right ventricular failure and ascites
1733. in meat-type chickens at low altitude. Avian Disease, 36, 733735.
Detilleux, J. & Leroy, P.L. (2000). Application of a mixed normal Lorenzoni, A.G. & Ruiz-Feria., C.A. (2006). Effects of vitamin E and
mixture model for the estimation of mastitis-related parameters. L-arginine on cardiopulmonary function and acites parameters in
Journal of Dairy Science. 83, 23412349. broiler chickens reared under subnormal temperatures. Poultry
Dewil, E., Buys, N., Albers, G.A.A. & Decuypere, E. (1996). Different Science, 85, 22412250.
characteristics in chick embryos of two broiler lines differing in Lubritz, D., Smith, J. & McPherson, B. (1995). Heritability of ascites
susceptibility to ascites. British Poultry Science, 37, 10031013. and the ratio of right to total ventricle weight in broiler breeder male
Enkvetchakul, B., Bottje, W., Anthony, N., Moore, R. & Huff, W. lines. Poultry Science, 74, 12371241.
(1993). Compromised antioxidant status associated with ascites in Luger, D., Shinder, D., Wolfenson, D. & Yahav, S. (2003). Erythropoi-
broilers. Poultry Science, 72, 22722280. esis regulation during the development of ascites syndrome in broiler
Fedde, M.R. (1984). Respiration in birds. In M. Swenson (Ed.), Dukes chickens: A possible role of corticosterone on egg production. Journal
Physiology of Domestic Animals 10th edn. (pp. 255261), Cornell of Animal Science, 81, 784790.
McGovern, R.H., Feddes, J.J.R, Robinson, F.E. & Hanson, J.A. (1999).
University Press San Diego, CA, USA.
Fedde, M.R., Weigle, G. E. & Wideman, R. F. (1998). Influence of feed Growth performance, carcass characteristics, and the incidence of
deprivation on ventilation and gas exchange in broilers: relationship ascites in broilers in response to feed restriction and litter oiling.
Poultry Science, 78, 522528.
to pulmonary hypertension syndrome. Poultry Science, 77, 1704
McGovern, R.H., Feddes, J.J.R., Robinson, F.E. & Hanson, J.A. (2000).
1710.
Growth, carcass characteristics, and incidence of ascites in broilers
Groves, P.J. (2002). Environmental determinants of broiler ascites
exposed to environmental fluctuations and oiled litter. Poultry
syndrome. Proceedings of the Australian Poultry Science Symposium
Science, 79, 324330.
Vol. 14 (pp. 8388). Sydney, Australia.
McLachlan, G.J. & Krishnan, T. (1997). The EM algorithm and
Hall, S.A. & Machicao, N. (1968). Myocarditis in broiler chickens
extensions. Wiley, New York, NY, USA.
reared at high altitude. Avian Diseases, 12, 7584.
Maxwell, M.H. & Robertson, G.W. (1997). World broiler ascites survey
Hassanzadeh, M., Buys, N., Dewil, E., Rahimi, G. & Decuypere, E.
1996. Poultry International, 36, 1630.
(1997). The prophylactic effect of vitamin C supplementation on
Maxwell, M.H., Robertson, G.W., Bautista Ortega, J. & Hocking, P.M.
broiler ascites incidence and plasma thyroid hormone concentration.
(1998). A preliminary estimate of the heritability of plasma troponin
Avian Pathology, 26, 3344.
T in broiler chickens. British Poultry Science, 39, 1619.
Hassanzadeh, M., Bozorgmerifard, M.H., Akbari, A.R., Buyse, J. &
Mirsalimi, S.M. & Julian, R.J. (1991). Reduced erythrocyte deform-
Decuypere, E. (2000). Effect of intermittent lighting schedules during
ability as a possible contributing factor to pulmonary hypertension
the natural scotoperiod on T3-induced ascites in broiler chickens.
and ascites in broiler chickens. Avian Diseases, 35, 374379.
Avian Pathology, 29, 433439. Mirsalimi, S.M., Julian, R.J. & Squires, E.J. (1993). Effect of hypobaric
Hassanzadeh, M., Buyse, J. & Decuypere, E. (2002). Further evidence hypoxia on slow and fast growing chickens fed diets with high and
for the involvement of cardiac a-adrenergic receptors in right low protein levels. Avian Diseases, 37, 660667.
ventricle hypertrophy and ascites in broiler chickens. Avian Pathology, Moghadam, H.K., McMillan, I., Chambers, J.R. & Julian, R.J. (2001).
31, 177181. Estimation of genetic parameters for ascites syndrome in broiler
Hoving-Bolink, A.H., Kranen, R.W., Klont, R.E., Gerritsen, C.L.M. & chickens. Poultry Science, 80, 844848.
de Greef, K.H. (2000). Fibre area and capillary supply in broiler Olkowski, A.A., Krover, D., Rathgeber, B. & Classen, H. L. (1999).
breast muscle in relation to productivity and ascites. Meat Science, Cardiac index, oxygen delivery, and tissue oxygen extraction in slow
56, 397402. and fast growing chickens, and in chickens with heart failure and
Hulan, H.W., Ackman, R.G., Ratnayake, W.M.N. & Proudfoot, F.G. ascites: a comparative study. Avian Pathology, 28, 137146.
(1989). Omega-3 fatty acid levels and general performance of Olkowski, A.A., Wajnarowicz, C., Rathgeber, B.M., Abbott, J.A. &
commercial broilers fed practical levels of red fish meal. Poultry Classen, H.L. (2003). Lesions of pericardium and their significance in
Science, 68, 153162. the aetiology of heart failure in broiler chickens. Research in
Issacks, R., Goldman, P. & Kim, C. (1986). Studies on avian erythrocyte Veterinary Science, 74, 203211.
metabolism XIV. Effect of CO2 and pH on P50 in the chicken. Olkowski, A.A., Nain, S., Wajnarowicz, C., Laarveld, B., Alcorn, J. &
American Journal of Physiology, R260, 250, R266. Ling, B.B. (2007). Comparative study of myocardial high energy
Julian, R.J. (1988). Pulmonary hypertension as a cause of right phosphate substrate content in slow and fast growing chicken and in
ventricular failure and ascites in broilers. Zootechnica International, chickens with heart failure and ascites. Comparative Biochemistry
11, 5862. and Physiology, Part A: Molecular & Integrative Physiology (148) 1,
Julian, R.J. (1989). Lung volume of meat-type chickens. Avian Disease, 230238.
33, 174176. Owen, R.L., Wideman, R.F., Hattel, A.L. & Cowen, B.S. (1990). Use of
Julian, R.J. (1998). Rapid growth problems: ascites and skeletal a hypobaric chamber as a model system for investigating ascites in
deformities in broilers, Poultry Science, 77, 17731780. broilers. Avian Diseases, 34, 754758.
Julian, R.J. (1990a). Cardiovascular diseases. In F.T.W. Jordan (Ed.), Ozkan, S., Plavnik, I. & Yahav, S. (2006). Effects of early feed restriction
Poultry Diseases, 3rd edn (pp. 330353). London: Bailliere Tindall. on performance and ascites development in broiler chickens subse-
Julian, R.J. (1990b). Pulmonary hypertension: a cause of right heart quently raised at low ambient temperature. Journal of Applied Poultry
failure, ascites in meat-type chickens. Feedstuffs, 78, 1922. Research, 15, 919.
Julian, R.J. (1993). Ascites in poultry. Avian Pathology, 22, 419454. Packer, L., Valenza, M., Serbinosa, E., Starke-Reed, P., Frost, K. &
Julian, R.J. (1995). Suggestions for reducing ascites in meat-type Kagan, V. (1991). Free radical scavenging is involved in the protective
chickens. Proceedings of the 44th Western Poultry Disease Conference effects of L-propionyl-carnitine against ischemia reperfusion injury
(pp. 1920), Sacramento, CA, USA. of the heart. Archive Biochemistry Biophysics, 288, 533537.
126 A. Baghbanzadeh and E. Decuypere
Pakdel, A., Van-Arendonk, J.A.M., Vereijken, A.L.J. & Bovenhuis, H. Smith, F.M., West, N.H. & Jones, D.R. (2000). The cardiovascular
(2002). Direct and maternal genetic effects for ascites-related traits in system. In G.C. Whittow (Ed.), Sturkie’s Avian Physiology 5th edn
broilers. Poultry Science, 81, 12731279. (pp. 141231). Academic Press.
Pakdel, A., Rabie, T., Veenendaal, T., Crooijmans, R.P.M.A., Groenen, Squires, E.J. & Julian, R.J. (2001). The effect of dietary chloride and
M.A.M., Vereijken, A.L.J., Van Arendonk, J.A.M. & Bovenhuis, H. bicarbonate on blood pH, haematological variables, pulmonary
(2004). Genetic analysis of ascites-related traits in broilers. Doctoral hypertension and ascites in broiler chickens. British Poultry Science,
thesis, Animal Breeding and Genetics Group, Department of Animal 42, 207212.
Sciences, Wageningen University, The Netherlands, p. 144. Stinefelt, B.M. (2003). Uric acid as an antioxidant and the effect of
Pakdel, A., Bijma, P., Ducro, B.J. & Bovenhuis, H. (2005). Selection changes in plasma uric acid concentrations on broiler susceptibility
strategies for body weight and reduced ascites susceptibility in to ascites, MSc Thesis, Davis College of Agriculture, Forestry, and
broilers. Poultry Science, 84, 528535. Consumer Sciences At West Virginia University, WV, USA.
Peacock, A.J., Pickett, I.C., Morris, K. & Reeves, J.T. (1989). The Stolz, J.L., Rosenbaum, L.M., Jeong, D. & Odom, T.W. (1992). Ascites
relationship between rapid growth and pulmonary hemodynamics in syndrome, mortality and cardiological responses of broiler chickens
the fast-growing broiler chicken. American Review of Respiratory subjected to cold exposure. Poultry Science, 71(Suppl 1), 4.
Diseases, 139, 15241530. Villar-Patino, G., Diaz-Cruz, A., Avila-Gonzalez, E., Guinzberg, R.,
Piiper, J. & Scheid, P. (1975). Gas transport efficacy of gills, lungs and Pablos, J.L. & Pina, E. (2002). Effects of dietary supplementation
skin: theory and experimental data. Respiratory Physiology, 23, 209 with vitamin C or vitamin E on cardiac lipid peroxidation and
221. growth performance in broilers at risk of developing ascites
Powell, F.L. (2000). Respiration. In: G.C. Whittow (Ed.), Sturkie’s syndrome. American Journal of Veterinary Research. 63, 5, 673676.
Avian Physiology 5th edn (pp. 233264). Academic Press San Diego, Walton, J-P., Bond, J.M., Julian, R.J. & Squires, E.J. (1999). Effect of
CA, USA.
dietary flax oil and hypobaric hypoxia on pulmonary hypertension
Reeves, J.T., Ballam, G., Hofmeister, S., Picket, C., Morris, K. &
and haematological variables in broiler chickens. British Poultry
Peacock, A. (1991). Improved arterial oxygenation with feed restric-
Science, 40, 385391.
tion in rapidly growing broiler chickens. Comparative Biochemistry
Wideman, R.F. (1997). Understanding pulmonary hypertension syn-
and Physiology, Part A, Physiology, 99, 3, 481485.
drome (ascites). Hubbard Farms Technical Report (pp. 16), Walpole,
Riddell, C. (1991). Developmental, metabolic, and miscellaneous
NH, USA.
disorders. In B.W. Calnek, H.J. Barnes, C.W. Beard, W.M. Reid &
Wideman, R.F. (1998). Causes and control of ascites in broilers.
H.W. Yoder, Jr. (Eds.), Diseases of Poultry 9th edn (pp. 839841).
National Meeting on Poultry Proceeding, 33, 5685.
Ames: Iowa State University.
Wideman, R.F. (2000). Cardio-pulmonary hemodynamics and ascites in
Rouwet, E.V., Tintu, A.N., Schellings, M.V.M., Van Bilsen, M.,
broiler chickens. Avian and Poultry Biology Review, 11, 2143.
Lutgens, E., Hofstra, L., Slaaf, D.W., Ramsay, G. & Le Noble,
Wideman, R.F. (2001). Pathophysiology of heart/lung disorders:
F.A.C. (2002). Hypoxia induces aortic hypertrophic growth, left
pulmonary hypertension syndrome in broiler chickens. World Poultry
ventricular dysfunction and sympathetic hyper innervation of per-
Science Journal, 57, 289307.
ipheral arteries in the chick embryo. Circulation, 105, 27912796.
Wideman, R.F. & Tackett, C. (2000). Cardiopulmonary function in
Ruiz-Lopez, B. & Austic, R.E. (1993). The effect of selected minerals on
broilers reared at warm or cold temperatures: effect of acute
the acidbase balance of growing chicks. Poultry Science, 72, 1054
1062. inhalation of 100% oxygen. Poultry Science, 79, 257264.
Sahan, U., Ipek, A., Altan, O. & Yilmaz-Dikmen, B. (2006). Effects of Wideman, R.F., Kirby, Y.K., Owen, R.L. & French, H. (1997). Chronic
oxygen supplementation during the last stage of incubation on broiler unilateral occlusion of an extrapulmonary primary bronchus induces
performance, ascites susceptibility and some physiological traits. pulmonary hypertension syndrome (ascites) in male and female
Animal Research, 55, 145152. broilers. Poultry Science, 76, 400404.
Scheele, C.W. (1996). Ascites in chickens, Thesis, Landbouwuniversiteit, Wideman, R.F., Wing, T., Kirby, Y.K., Forman, M.F., Marson, N.,
Wageningen, The Netherlands. Tackett, C.D. & Ruiz-Feria, C.A. (1998). Evaluation of minimally
Scheele, C.W., Van Der Klis, J.D., Kwakernaak, C., Buys, N. & invasive indices for predicting ascites susceptibility in three successive
Decuypere, E. (2003). Hematological characteristics predicting hatches of broilers exposed to cool temperatures. Poultry Science, 77,
susceptibility for ascites. 2. High haematocrit values in juvenile 15651573.
chickens. British Poultry Science, 44, 484489. Wideman, R.F., Hooge, D.M. & Cummings, K.R. (2003). Dietary
Shlosberg, A., Bellaiche, M., Zeitlin, G., Yaacobi, M. & Cahaner, A. sodium bicarbonate, cool temperatures, and feed withdrawal: impact
(1996). Hematocrit values and mortality from ascites in cold stressed on arterial and venous blood-gas values in broilers. Poultry Science,
broilers from parents selected by hematocrit. Poultry Science, 75, 82, 560570.
15. Wise, D.R. & Evans, E.T.R. (1975). Turkey syndrome 65, oedema
Shlosberg, A., Belaiche, M., Berman, E., Perk, S., Deeb, N., Neumark, syndrome and mycoplasma meleagridis. Research in Veterinary
E. & Cahaner, A. (1998). Relationship between broiler chicken Science, 18, 190192.
hematocrit-selected parents and their progeny with regard to Zerehdaran, S., Van Grevehof, E.M., Van Der Waaij, E.H. &
hematocrit, mortality from ascites and body weight. Research in Bovenhuis, H. (2006). A Bivariate mixture model analysis of body
Veterinary Science, 64, 105109. weight and ascites traits in broilers. Poultry Science, 85, 3238.