Ascites Syndrome in Broiler Chickens

13 Pages·2014·0.23 MB·English

http://www.jstage.jst.go.jp/browse/jpsa
doi:10.2141/jpsa.0130063
CopyrightⒸ2014,JapanPoultryScienceAssociation.
≪Review≫
Ascites Syndrome in Broiler Chickens: A Review on the Aspect of
Endogenous and Exogenous Factors Interactions
Mohammad Hassanzadeh1, Johan Buyse2, Tohid Toloei1 and Eddy Decuypere2
1DepartmentofPoultryDiseases,FacultyofVeterinaryMedicineUniversityofTehran,P.O.Box14155-6453,Tehran,Iran
2DepartmentofBiosystems,K.U.Leuven.KasteelparkArenberg30,B-3001Leuven,Belgium
Increasing susceptibility of broiler chickens to ascites syndrome has coincided with a continuing genetic and
nutritionalimprovementintheirfeedefficiencyandgrowthrate. Imbalancebetweenoxygensupplyandtheoxygen
requiredtosustainrapidgrowthratesandhighfoodefficienciesisbelievedtobetheprimarycauseofascites. This
imbalance is caused by exogenous and/or endogenous factors.
Selection in fast growth broilers, have also resulted in the development of birds with changed anatomical,
physiological,metabolicandhematologicalparametersincludingthyroidhormoneactivity,partialpressureofO2and
carbondioxideinvenousblood,cardiacβ-adrenergicreceptorsandhematocritlevelsthatcoincidewithsusceptibility
toascitesinbroilerchickens. Observationstodatehaveindicatedthatthestructuralorendocrinechangesareoften
linkedwithascitessusceptibilityandmaybeinfluencedduringtheearlystagesofdevelopment,embryogenesisand
incubation. Inthisreview,particularattentionispaidtotheinteractionsbetweenendogenousandexogenousfactors
aspredisposingfactorsfordevelopmentofascitessyndrome. Additionally,preventivemanagementprocedureslike
differentlightingschedules,feedrestrictionprotocolsandsupplementationoffeedwithantioxidantswhichreducethe
incidence of ascites in broiler chickens are highlighted.
Key words: ascites, broilers, endogenous, exogenous, hypothyroidism
J. Poult. Sci., 51: 229-241, 2014
nolongerrestrictedtobirdsthatarekeptathighaltitudes,as
Introduction
wasinitiallyreportedbyCuevaetal. (1974). However,itis
Ascites is an important metabolic disorder in broiler now found in flocks that are kept at sea level as well
industry. It is a major noninfectious cause of death among (Decuypereetal., 2000;Hassanzadehetal., 1997a,b, 2000,
broilers and can account for over 25% of broiler losses 2001, 2012;Balog, 2003;Scheeleetal., 2005;Al-Mesriand
(MaxwellandRobertson, 1997;Balog, 2003). Ascitesisthe Hassanzadeh, 2010).
result of malfunctioning heart and circulatory system and is Modern strains of broilers are able to achieve market
caused by an imbalance between oxygen supply and the weight in 60% less time than broilers of 40 years ago
oxygenrequiredtosustainrapidgrowthratesandhighfood (Baghbanzadeh and Decuypere, 2008). While, both heart
efficiencies in broiler chickens (Decuypere et al., 2000). and lung percentages of broiler chickens are tended to be
Thegeneticbackgroundinvolvedinthissyndromehasbeen significantly lower in the modern strain at most of the
linkedtoalteredmetabolicneedsofrapidlygrowingbroilers slaughter ages (Havenstein et al., 2003). Havenstein et al.
becauselinesselectedforveryhighgrowthcapacityandlow (1994, 2003) investigated on the relative contributions of
feed conversion are more sensitive to ascites than slower- genetics and nutrition to changes carcass characteristics of
growing broilers (Chimene et al., 1995; Decuypere et al., broiler chickens. Authors reported that modern diet (e.g.
2000;Balog, 2003;DeSmitetal., 2005;Hassanzadehetal., pelletedandcrumblesinsteadofmash)reducedlungssizeas
2010). Ascites is a multifactorial problem mediated by a percentage of body weight in comparison to the diet that
environmental,nutritionalandgeneticfactors(Decuypereet was used 40 years ago. Again, their data suggest that both
al., 2000; Balog, 2003; Julian, 2005). Ascites syndrome is heartandlungsizeasapercentageoflivebodyweighthave
been decreased with genetic selection for increased growth
Received:April15,2013,Accepted:November6,2013
rate. This, along with the rapid increase in body fat at the
ReleasedOnlineAdvancePublication:December25,2013
lateragesonthemoderndietmaybecontributingfactorsto
Correspondence: M. Hassanzadeh, Department of Poultry Diseases,
the increased incidence of late mortality e.g. ascites, in the
Faculty of Veterinary Medicine University of Tehran, P.O.Box 14155-
6453,Tehran,Iran.(E-mail:[email protected]) modern strain (Havenstein et al., 2003). They concluded
230 JournalofPoultryScience,51(3)
that relative size of the heart and lungs may be contributing decrease in the partial pressure of the oxygen. When birds
factors to the ability of modern broilers to service the are exposed to low atmospheric oxygen levels, pulmonary
respiratory demands of their bodies. Nevertheless, the blood vessels constrict, restrict blood-flow to the lung and
pulmonary and cardiac capacity of modern broilers is very increase the work-load on the right ventricle (Julian, 1993).
similar to the old broiler strains which force their cardio- This immediate increase in pulmonary arterial pressure can,
pulmonary system to work very close to its physiological overtime,causerightventricularhypertrophyandeventually
limit (Lorenzoni et al., 2006). The lung capacity does not result in ascites syndrome (Wideman et al., 1998). Addi-
alwaysmeettheoxygendemandsnecessaryforrapidgrowth. tionally, hypoxemia also leads to increase blood viscocity
Thisresultsinimpairedabilitytoregulatetheenergybalance andresultsinanincreaseinresistancetobloodflowthrough
underextremeconditionssuchaslowambienttemperatureor the pulmonary blood vessels (Julian, 1993; Maxwell and
high altitude (Luger et al., 2003; Hassanzadeh et al., 2003, Robertson, 1997).
2004, 2005a,b, 2008;Ozkanetal., 2010). Ifthelungofthe Powell(2000)suggestedthattheincreasedgrowthratein
chickengrowslessrapidlythantherestofthebody,hypoxia modernfast-growingbroilerchickensat sea level requiresa
and ascites could result (Hassanzadeh et al., 2005b). highermetabolicratetherefore,anincreaseincardiacoutput
Decuypereetal. (2000, 2005)suggestedthatatlowaltitude, causes pulmonary hypertension and ascites. According to
ascites is not only caused by an increased oxygen require- experimental results, hypercapnia (high CO2 in the blood)
ment in fast growth rate chickens, but also by an impaired plays important role in activating of vasoconstriction and
oxygen supply to sustain growth rate. highbloodpressureinbroilerchickenssusceptibletoascites
Changes in hematocrit values, partial pressure of oxygen at sea level (Buys et al., 1999; Decuypere et al., 2000;
(pO ) and carbon dioxide (pCO ) and endocrine function Scheele et al., 2003, 2005, Hassanzadeh et al., 2010, Al-
2 2
such as thyroid hormone activity are important regulatory MesriandHassanzadehetal., 2010). Inadditiontocardiac
mechanisms of the metabolic rate during the embryonic insufficiency, the occurrence of ascites in chickens at sea
development and growing period (Buyse et al., 1996; Buys levelcanalsobecausedbymalfunctionsofthecardiopulmo-
et al., 1998; Decuypere et al., 2000, 2005; Luger et al., narysystemwhichcausedisturbancesinthetensionofblood
2001, 2003; Teshfam et al., 2005; Arab et al., 2006; gases (Fig. 1).
Hassanzadeh et al., 2002, 2004, 2005a, b, 2008, 2010, Although ascites is conventionally associated with the
2012;Bahadoranetal., 2010). Theroleofthyroidhormone rapid growth rate of broilers, high metabolic rates and high
intheregulationofmetabolismcouldbecomemoreapparent oxygen requirements (Hassanzadeh, 1997; Hassanzadeh et
in different genotypes of chickens (Scheele et al., 1992; al., 1997a, b, Julian, 1993, 2005; Balog, 2003), recent data
Scheele, 1996; Decuypere et al., 2000; Luger et al., 2001; indicated that ascites is not always caused by an increased
Malan et al., 2003; Hassanzadeh et al., 2004, 2010) and oxygenrequirementoffastgrowthrateperseatlowaltitude,
under environmental conditions such as at low ambient butbyanimpairedoxygensupplytosustainthefastgrowth
temperature (Scheele et al.,1992; Hassanzadeh et al., 2003, rate (Decuypere et al., 2000, 2005; Scheele et al., 2005;
2005a, 2010),differentlightingprograms(Buyseetal.,1994; Malanetal., 2003;Hassanzadehetal., 2010). Decuypereet
Buys et al.,1998; Hassanzadeh et al., 2000, 2003, 2005a, al. (2000) mentioned that thyroid function is an important
2012) and even at high altitudes (Hassanzadeh et al., 2002, regulatory mechanism of the metabolic rate, it is plausible
2003, 2004, 2005a, b, 2008). that early selection for feed conversion (FCR) could have
Itisobviousthatgeneticselectionforalineofbroilersthat resultedinfunctionalofhypothyroidism,asascitessensitive
is resistant to ascites would be a permanent solution to the birds are believed to be limited in their thyroxin (T4)
problem of ascites. For a short-term solution, there is no production (Scheele et al., 1992; Scheele, 1996). Insuf-
single treatment or preventive system for control of the ficient thyroid hormone activity to regulate metabolism,
ascites. Theconditionisoftenrelatedtofastgrowthrateand related to genetic background, will therefore become es-
metabolic activity of birds, and management techniques to peciallyapparentatlowambienttemperature(Scheeleetal.,
reduce early growth rate offer the best short-term preventa- 1992). Recent results (Buys et al., 1999; Decuypere et al.,
tive scenario (Buyse et al., 1996; Buys et al., 1998; Balog, 2000; Scheele et al., 1992, 2005; Luger et al., 2001;
2003; Hassanzadeh et al., 2000, 2003, 2005a, 2012). Hassanzadehetal., 2010)confirmedthoseoftheScheeleet
In this review, particular attention is paid to the en- al. (1992) and indicated that hypothyroidism, observed in
dogenous and environmental factors that interact with other linescombiningafavourableFCRandfastgrowth,playsan
predisposing factors for development of the ascites. important part in the reduction of oxygen consumption that
Furthermore,someofthepreventivemanagementprocedures lead to anoxia, heart failure and ascites.
that reduce the incidence of ascites in broiler chickens such Birds that were selected for combination of fast growth
as different lighting schedules, feed restriction and antioxi- and high feed efficiency had a low O and a high CO
2 2
dant supplementation are also reviewed. tensions in venous blood at a low ambient temperature
compared with the slower-growing birds (Scheele et al.,
Factors Involvement for Development of Ascites
2005;Decuypereetal., 2005;Hassanzadehetal., 2010;Al-
a. Interaction between endogenous and exogenous factors Mesri and Hassanzadeh, 2010). Authors argued that a
Theeffectofhighaltitude,eithernaturalorsimulated,isa thyroidhormone insufficiencywasone ofthecausal factors
Hassanzadehetal.:AscitesSyndromeinBroilers:AReview 231
Fig.1. Flowchartofthedevelopmentofascitessyndromeinbroilerchickens.
ofincreasedfeedefficiencyandwasresponsibleforimpaired Therelationshipbetweenactivityofthyroidhormoneand
O supply when trying to sustain a fast growth rate. This anatomicalparameterswasdiscussedinthestudyofMalanet
2
maydevelopamismatchbetweenthedeliveryofO andO al. (2003). They demonstrated that a deficiency in thyroid
2 2
demands, resulting in anoxia, hypoxemia and hypoxia hormone could impair lung development and may increase
(Decuypere et al., 2000). It will occur in particular under the risk of ascites in chickens with rapid growth. This was
circumstances where the O requirements of birds are in- confirmedbytherecentreportsofHassanzadehetal. (2004,
2
creasedsuchasinacoldenvironment,andmayleadtoheart 2005b, 2008) who documented a direct correlation between
failure and ascites (Decuypere et al., 2000; Malan et al., the heart and lung development of post-hatch broiler
2003; Bahadoran and Hassanzadeh, 2010; Hassanzadeh et chickens with the embryonic thyroid hormone activity.
al., 2004, 2008, 2010, 2012). These data showed that post-hatched chickens had lower
232 JournalofPoultryScience,51(3)
heart and lungs weights in relation to their body size when suggest that some meat-type chickens are not fully
plasma thyroid hormone levels were observed lower during oxygenating their haemoglobin even at low altitude (Julian,
the embryonic development. Consequently, such chickens 1993, 2005). Thismaybetheresultofincreasedbloodflow
withlowerlungcapacityhadahighersusceptibilitytoascites rate through the lung capillary bed of the lung, which does
when exposed to low temperatures and chronic hypoxia at not allow time for haemoglobin to pick up a full load of
high altitude (Hassanzadeh et al., 2008). oxygen(Wideman&Kirby, 1995). Whilethebreastmuscle
Toserveasapredictorofbroilerssusceptibilitytoascites, development hinders respiration, as does intra-abdominal
a potential indicator should differ significantly between pressure from the internal organs or body fat (Jones, 1995).
ascites-susceptible versus ascites-resistant individuals when PreviousresultofJulian(1989)hasindicatedthatcardiopul-
theyarerearedtogetherunderstandardconditionsatanearly monary parameters are extremely unfavorable to broiler
age. Hematocrit was found to be one of the most reliable chickens and suggested that a reduction in the area of gas
indicators for detection of ascites (Maxwell et al., 1992; exchange in broilers therefore causes a higher susceptibility
Shlosberg et al., 1996; Wideman et al., 1998). Broilers to pulmonary hypertension and ascites. Vidyadaran et al.
developingasciteswerecharacterizedbylowerheartrateas (1987) showed that the respiratory system of the adult
well (Olkowski et al., 2005; Wideman et al., 1998) and domesticfowlwasfarlesswell-adaptedanatomicallyforgas
higher right ventricle weight to total ventricle weight ratio exchange compared to that of non-galliform species.
(WidemanandKirby, 1995,Druyanetal., 2007). However, Hassanzadehetal. (2005b, 2008)reportedacausalrelation-
in all these studies, differences were found only between shipbetweentheanatomicalparametersofcardiopulmonary
broilers that had already developed some degree of ascites systemswiththesusceptibilitytoascitesinbroilerchickens.
when compared to their healthy counterparts. Thus, these In these studies the anatomical parameters of cardiopulmo-
differences were most probably secondary to the manifesta- narysystemsweredecreasedwithageinthebroilerchickens
tions of ascites (Druyan et al., 2009), hence, can serve as when this parameter was expressed as a percentage of body
diagnostic tools but not for early prediction. Such an weight. Additionally, such parameters were extremely un-
indicatorisessentialforindirectphenotypicselectionagainst favorableinbroilerchickenscomparedtothoseoflayerand
ascites susceptibility, therefore, all birds should be healthy. native chickens and suggested a reduction in the gas
Reevesetal. (1991)noticedthatascites-susceptiblechickens exchangeareainbroilersandthereforeahighersusceptibility
suffer from relative hypoventilation at an early age, which to pulmonary hypertension and ascites (Hassanzadeh et al.,
may cause an elevated partial pressure of CO2 in blood. 2005b, 2008).
Later studies by Scheele (1996), Buys et al. (1999), Recently, we observed a correlation between insufficien-
Olkowski et al. (1999), Scheele et al. (2003, 2005), ciesofthecardiopulmonarysystemwithariseinpCO anda
2
Hassanzadeh et al. (2010), Al-Mesri and Hassanzadeh, decline in pO in the venous blood of birds and the
2
(2010) and Van As. et al. (2010) confirmed these findings. development of ascites syndrome (Al-Mesri and
TheyreportedthatthehighpartialpressureofCO2invenous Hassanzadeh, 2010). Indeed,alargefallwasobservedinthe
bloodof2-week-oldbroilerchickenscouldbeasapotential volumeofthethoraciccavities,bothbeforeandafterremoval
indicatorforascitessusceptibilityatlaterage. However,the of the heart and lung tissues, in the fast-growing compared
resultsofDruyanetal. (2009)suggestedthathighheartrate, with those of the slow-growing broiler chickens. Such
measured by oximeter at 1 wk of age, may serve as an phenomenon was accompanied by a significant increase of
additionaloralternativecriterionforselectionagainstascites the pCO and a decrease of the pO tensions in the venous
2 2
susceptibility. blood of rapid-growing compared with those of the slow-
Anatomy and physiology of the avian respiratory and growing broiler chickens.
cardiovascular systems are important in the susceptibility to b. Mediators contributed to pulmonary arterial hypertension
pulmonaryhypertensionsyndromeandascites(Julian, 1989; Anythingthatincreasesthepulmonaryvascularresistance
Decuypere et al., 2000; Hassanzadeh et al., 2005b, 2008). and/or increases cardiac output can initiate or accelerate the
Decuypere et al. (2000) indicated that alteration in the pathophysiologicalprogressionleadingtopulmonaryarterial
proportional growth as a result of indirect selection for hypertension and ascites in broiler chickens (Julian, 1993,
greater muscularity may have had the effect of producing 2005;BaghbanzadehandDecuypere, 2008;Widemanetal.,
birds with a relatively small respiratory and cardiovascular 2013; ). Mediators, like catecholamines (Lefkowitz et al.,
system. Authors argued that if development of the ascites 1984; Hassanzadeh et al., 1997a, 2001, 2002), endothelin-1
syndrome is a consequence of structural or morphological/ (Villamor et al., 2002; Odom et al., 2004), methylglyoxal
histological alterations, this must result in observable (KhajaliandFahimi, 2010;KhajaliandWideman, 2011)and
physiological changes. Modern broiler chickens have serotonin (Chapman and Wideman, 2002; Kluess et al.,
thickerrespiratorymembranethanLeghorn-typefowl,sothe 2012) play a major role in accelerating of pulmonary
abilityofbroilerchickenstomoveoxygenintohaemoglobin hypertension that may lead to ascites in broiler chickens
maynotbeasgoodasinLeghorn-typebirds(Julian, 1993). (Hassanzadeh et al., 1997a, b; Wideman et al., 2013).
Research on oxygen haemoglobin saturation in meat-type Catecholamines such as epinephrine and norepinephrine
chickens indicates that fast-growing broilers have a lower regulate physiological events by binding to α- and β-
oxygensaturationthanslow-growingbroilers. Theseresults adrenergic receptors on the surface of target cells. Nor-
Hassanzadehetal.:AscitesSyndromeinBroilers:AReview 233
epinephrine released by sympathetic nerve terminals and chick embryos incubated at high CO levels downregulated
2
epinephrine released into the circulation by the adrenal the expression of myocardial β-adrenergic receptors.
glandsinresponsetostress,maycontributetotheincreasein Authorsarguedthatthedecreaseinreceptordensityreflectsa
pulmonary vascular resistance during exposure to hypoxia regulatory phenomenon and is not due merely to right
and cool temperatures (Lin and Sturkie, 1968; Wideman, ventricular hypertrophy (Mardon et al., 1998). These data
1999). Lefkowitz et al. (1984) and Cohen et al. (1984) pointtotheinvolvementofcatecholaminestogetherwithβ-
reported that the constriction of smooth muscles of the adrenergicreceptorsinthesyndromeofpulmonaryhyperten-
vascular system was a consequence of an adrenergic stimu- sion in broiler chickens. In particular, the observation of a
lation due to catecholamine hormones. So, intravenously differential β-adrenergic receptor density in the cardiac
administered epinephrine elicits immediate pulmonary muscle of ascites-sensitive birds may be linked with the
vasoconstriction accompanied by pulmonary hypertension slight degree of hypothyroidism that is found in these
(Wideman, 1999;Villamoretal., 2002;LorenzoniandRuiz- broilers. Also it points to a possible cardiogenic origin for
Feria, 2006; Ruiz-Feria, 2009; Bautista-Ortega and Ruiz- the susceptibility to ascites on a genetic basis that was
Feria, 2010). already discussed in previous section of this review.
β-adrenergic receptors are found on the various organs Intimatelyendothelin-1isinvolvedinthepathogenesisof
such as heart tissue, the blood vessels, smooth and skeletal pulmonary arterial hypertension in mammals and broiler
muscles,howevercardiacmusclecontainspredominantlyβ1 chickens (Wideman et al., 2013). In broilers, endothelin-1
subtypes of the adrenergic receptor. In cardiac tissue elicitsdose-dependentconstrictionofpulmonaryarteriesthat
epinephrine and norepinephrine appear to be about equally can be modulated by nitric oxide (Martinez-Lemus et al.,
potent to regulate physiological events by binding to β- 2003; Villamor et al., 2002; Odom et al., 2004). Repeated
receptors (Stiles et al., 1984). Investigations in human and intravenous injections of endothelin-1 triggered pulmonary
other mammals have confirmed that β-adrenergic receptors arterialhypertensioninbroilerchickens(Zhouetal., 2008).
play an important role in regulation of cardiovascular Gomez et al. (2007) reported that the lungs of broilers with
performance like tachycardia. These receptors are dynami- pulmonary hypertension expressed higher levels of
cally regulated by a wide variety of pathological and endothelin-1 mRNA compared with lungs from the nonhy-
physiologicalconditions. Thephysiologicallevelsofthyroid pertensive broilers. In addition, cardiac expression of
hormonehavebeensuggestedtobeanimportantmodulator endothelin-1 mRNA was higher in the right but not in left
of the normal maturation of the β-adrenergic system in ventricle of broilers compared with those of egg-laying
developing rat ventricular myocardium (Novotny et al., chickens,andbroilershadhigherserumlevelsofendothelin-
1999). In mammals, hypoxia regulates the density of β- 1 than those of layers (Hassanpour et al., 2010). Cumula-
adrenergicreceptors. Inbroilerchickens,Hassanzadehetal. tively these observations reflect a consistent association
(1997a)foundthatthedensityofβ-adrenergicreceptorswas between excessive endothelin-1 production and pulmonary
higherincardiaccellsofascites-sensitivebirdscomparedto hypertension (Wideman et al., 2013).
those of the chickens that were ascites-resistant. Moreover, Methylglyoxal is formed from carbohydrates, fatty acids
thecapacityofβ-adrenoreceptorswasloweredinthecardiac and proteins. It has been shown to damage the vascular
cells of birds with right ventricular hypertrophy and heart endothelium and implicated in vascular remodeling and
failure compared with those of healthy birds (Hassanzadeh systemic arterial vasoconstriction and hypertension in
et al., 2001). In the other investigation, the density of mammals. Recently,reportsinbroilerchickensindicatethat
myocardial β-adrenergic receptors in non-hypertrophied intravenous and intramuscular injections of Methylglyoxal
ventricles of high-altitude hypoxic birds was significantly both rapidly elicited pulmonary vasoconstriction and pul-
reduced compared with the low-altitude normoxic birds monary hypertension (Khajali and Wideman, 2011), which
(Hassanzadeh et al., 2002). potentially may reveal a mechanistic link between full-
Hypoxia is a potent stimulus to release of catecholamine feeding,oxidativestress,endothelialdamage,andtheascites
from sympathetic system and the adrenal medulla into syndrome (Khajali and Fahimi, 2010).
circulation(Cheung, 1989). Accordingtopreviousworksin Serotoninisanextremelypotentpulmonaryvasoconstric-
mammals, increasing activity of the sympathetic nervous tor that triggers pulmonary hypertension by activating
systemincompensationforthereducedcardiacoutputseems receptorsexpressedonpulmonaryarterysmoothmusclecells
to be a mechanism of the organism to help the failing heart (Chapman and Wideman, 2002, Kluess et al., 2012). In
(Velarde et al., 1996; Browne et al., 1997). Such phe- broiler chickens, plasma serotonin levels normally are quite
nomenon could be characterization of β-adrenergic receptor low, however serotonin can be released from activated
in heart failure and even in high-altitude hypoxic birds thrombocytes and from pulmonary neuroendocrine cells or
(Hassanzadehetal., 2001, 2002). Itseemsthedownregula- serotonergic nerves (Chapman et al., 2008). Kluess et al.
tionofβ-receptorsinthesebirdscouldbeduetochronically (2012)pointedthatbroilersfeddietssupplementedwithhigh
increased receptor occupancy as a result of elevated con- levelsoftryptophan,anessentialaminoacidandprecursorof
centrationofcirculatingandneuralreleasedcatecolaminesas serotonin, developed higher pulmonary arterial pressures
hasalreadybeenreportedinmammals(Voelkeletal., 1981; thanthoseofbroilersfeddietscontainingadequatelevelsof
Maderetal., 1991). Hassanzadehetal. (2002)reportedthat tryptophan. ChapmanandWideman, (2002)mentionedthat
234 JournalofPoultryScience,51(3)
serotoninclearlyplaysakeyroleinincreasingthebasaltone The severity of embryonic hypoxia may be related to the
(partial state of contracture) of the pulmonary resistance porosity and structure of the egg shell and hence, to the
vessels, and potentially can act as a dominant pulmonary partial pressures of O and CO in the egg and air chamber,
2 2
vasoconstrictorinbroilerchickens. Itappearsthatsuscepti- especiallyduringthelastdaysofincubation(DeSmitetal.,
bility to pulmonary tension in broilers may involve in 2006). Sadler et al. (1954) explained that the beneficial
excessive serotonin biosynthesis, inhibited uptake or en- effects of CO were the result of the reduction of pH of the
2
hanced release of serotonin by thrombocytes, enhanced albumen,whichmighthaveretardedtheapparentbreakdown
receptor-mediatedvasoconstrictiveresponsivenesstoseroto- of the chalaziferous membrane and the thick layer of
nin, or altered internalization of serotonin by a specific albumen, leading to reduce the length of incubation. Al-
transporter associated with vascular remodeling (Wideman ternatively,itcouldberelatedtothedurationofthehypoxic
and Hamal, 2011). period and, therefore, to the pipping and hatching time.
c. Hatching parameters and ascites susceptibility Blacker et al. (2004) provided evidence for the role of
Until some years ago, a large part of commercial in- hypoxia during the embryonic development regarding the
cubations was performed using the multistage system. controlofpulmonarysurfactant. Theauthorssuggestedthat
Today, the incubation of broiler eggs has become a highly the avian pulmonary surfactant system exhibits a high level
controlled process, during which the temperature, humidity, ofplasticitywithintheearlystagesofsurfactantmaturation.
O , and CO concentrations create the optimal environment A possible explanation for these observations is an inter-
2 2
for embryonic development. The composition of the am- actionbetweenenvironmentalandendogenousphysiological
bient gaseous environment in the incubator plays an im- factors,suchascorticosteroneandthyroidhormones,during
portant role during embryonic development, and by mani- the critical developmental period of chick embryos
pulating the incubation conditions, the developmental (Hassanzadeh et al., 2004, Blacker et al., 2004). These
trajectoriesofthe chickembryohasbeeninfluenced(Dewil interactions could exploit developmental plasticity, which
et al., 1996; Hassanzadeh et al., 2002, 2004, 2005b, 2008; result in the physiological heterokairy of the surfactant
De Smit et al., 2005, 2006). The peak mortality due to system by altering both the rate and onset of production of
ascites occurs at the end of the growth period, but it is now surfactant lipids and the earlier commencement of air
thought that the etiology of this disease might be existed breathing. These observations indicate that hypoxic condi-
during embryonic development (Coleman and Coleman, tions occuring in the embryonic period can alter the de-
1991). As the chick embryo consumes 60% more O velopmental trajectories of some endogenous parameters in
2
between the start of pulmonary breathing and hatching prenatal and postnatal chicks. The development of these
comparedtoearlierstages,itispossiblethatashortageofO important parameters is favorable to the formation of an
2
occurs during this stage. Decuypere et al. (2000) reported increased gas exchange area and results in the lower sus-
thatahighCO concentrationintheairchamberisatrigger ceptibility of birds to pulmonary hypertension.
2
for hatching. The findings of Chineme et al. (1995) Hypoxic conditions during embryonic development may
indicated that the length and/or severity of prenatal hypoxia initiate structural changes in cardiovascular and pulmonary
may influence postnatal characteristics that were related to systems, as was observed in our recent study of chickens at
ascites. Further studies (Buys et al., 1998; Hassanzadeh et high altitude (Hassanzadeh et al., 2005b, 2008). In these
al., 2002; De Smit et al., 2006) showed that increased CO studies, day-old high altitude-hatched chicks had a signifi-
2
concentrationsintheincubatorbynon-ventilationduringthe cantly higher proportion of their heart (1.23±0.08 versus
first10dorthelast7dofincubationincreasedtheperform- 0.87±0.07) and lung weights (2.02±0.07 versus 1.23±
anceofthechickembryoandevenhadbeneficialeffectson 0.13) to body weight compared to that of low altitude-
post-hatch growth and ascites susceptibility. In these hatchedchicks,whilenosignificantdifferencewasfoundat
studies,itwasshownthateggsincubatedinanenvironment the age of slaughter. This coincided with a reduced in-
withahighconcentrationofCO duringthelastweek(Buys cidence of ascites and right ventricular hypertrophy in high
2
etal., 1998;Hassanzadehetal., 2002)and/orthefirst10dof altitude-hatched birds than those of low altitude-hatched
theirincubations(DeSmitetal., 2006)werehatchedearlier birds (Hassanzadeh et al., 2004, 2008). Additionally,
than in an environment with normal CO levels. Further- changes in anatomical parameters of high altitude chicks
2
more, embryos that were incubated at high altitude, 2000m were also accompanied with increased levels of thyroid
above sea level, for first 10 d of incubation had an earlier hormone and corticosterone of their embryos. These early
hatching time than those incubated at low altitude stages of development may be decisive in determining the
(Bahadoranetal., 2010). Inthisstudy,thosechickenswhich subsequent adaptive capacity to cope with unfavorable
hatched earlier showed a lower incidence of ascites during environmental conditions after hatching (Buys et al., 1999;
the growing period, because high concentrations of CO in Hassanzadeh et al., 2004, 2008).
2
the incubation environment might actually decrease the Inadditiontotheenvironmentalincubationconditionse.g.
lengthoftimeandtheembryoexperienceshypoxia(Buyset high CO levels or altitude, the genetic background of the
2
al., 1998; Hassanzadeh et al., 2002, 2004; De Smit et al., chickalsoinfluencestheembryonicdevelopmentalpathway.
2006). Chickens selected for various post-hatch characteristics also
Several explanations have been published for the events. differ with regards to their embryonic developmental tra-
Hassanzadehetal.:AscitesSyndromeinBroilers:AReview 235
jectories (Decuypere et al., 2000). In comparative studies, coincided with a temporary reduction in the growth rate at
broilersfromlinesthatdifferedintheirascitessusceptibility young ages, with a concomitant reduction of metabolic
(Dewiletal., 1996;Buysetal., 1998;DeSmitetal., 2005, indicators.
2006) showed also difference in their certain embryonic Recently,Hassanzadehetal. (2012)appliedacomparative
characteristics. Therefore, chicks of ascites-sensitive lines study on the beneficial effects of four different dark-light
hatched later, had lower thyroid hormone concentrations, a schedules on the incidence of ascites and metabolic pa-
lower pCO and a higher pO in the air cell during the late rameters in fast growing broiler chickens. In this study the
2 2
stages of embryonic development. rate of ascites mortality was declined when the duration of
daily dark period was increased. The reduction of ascites
Management Techniques for Control of Ascites
mortality was accompanied with declined pCO2 tension in
a. Lighting venous blood of dark-exposed chickens, strengthening the
It is a common practice to raise broiler chickens in con- view that a lower metabolic rate and hence a decrease in
tinuous or near continuous illumination and/or is recom- oxygen requirement had a beneficial effect on the incidence
mended that a short dark period should be included to of ascites (Classen et al., 1991; Buyse et al., 1994; Buys et
accustombirdstodarknessandtominimizepanicincaseof al., 1998; Hassanzadeh et al., 2000, 2003, 2005a, 2012).
power failure (Buyse et al., 1996). There is interest in b. Feed restriction
discontinuous lighting patterns such as an increasing photo- Early growth restriction is still an important management
periodlightingsystem(Classenetal., 1991;Hassanzadehet tool to reduce the incidence of ascites until an effective
al., 2003)and/orintermittentlightingschedules(Buysetal., selectionprogramisdevelopedandimplementedbypoultry
1998;Hassanzadehetal., 2000, 2005a)forbroilersbecause breeder companies in the future. Growth restriction can be
these alternative lighting programs could improve broiler achievedbychangesinfeedingregimes(Balog, 2003). The
performance and reduce the occurrence of metabolic dis- hypoxia related to a high metabolic rate can be partially
orders like sudden death and ascites syndromes (Julian, prevented by limiting energy intake via feed restriction in
2005). broilers (Julian, 2005; Balog, 2003). Feed restriction
Buyseetal. (1994)pointedoutheatproductionandhence reducesgrowthatacriticaltimeinabroilerchick’slifecycle
oxygenrequirementsperkilogramofmetabolicbodyweight whenitisthemostsusceptibletometabolicdiseaseduetoits
in chickens following a normal growth trajectory at about 2 high oxygen demands (Balog et al., 2000; Ozkan et al.,
to 3 weeks of age which is indicative of an amplified 2006, 2010). However, use of this management technique
metabolic demand. This metabolic demand predisposes dependsonbodyweightofchickenatcertainslaughterages,
chickenstodevelopmentofascites. Itwashypothesizedthat which is associated with compensatory weight gain,
limitingthenumberofhoursoflightwouldslowthegrowth improvementsincarcassyield,feedpricesandtheincidence
rateslightly,especiallyattheearlierage, andreduceactivity ofascites(Balog, 2003). Therehavebeenconflictingresults
that requires additional oxygen which may improve feed in catch-up growth and yield data, illustrating the severity
efficiency (Julian, 1993, 2005). and duration of the growth restriction (Julian, 2005). The
Imposing intermittent lighting schedules (1L: 3D) during distinct advantage of feed restriction is the decrease in
the24hday(Buysetal., 1998)orduringthe12hofnatural mortality (Shlosberg et al., 1991; Balog, 2003). Feed
scotoperiod, from 8 pm to 8 am (Hassanzadeh et al., 2000) restriction (by reducing ad libitum intake) reduced the
significantlyreducedtheincidenceofrightventricularfailure incidence of ascites without compromising body weight
andascitesinbroilerchickens. Inbothstudies,thechangeof (Albers et al., 1990; Balog, 2003). Skip-one or two-days a
continuous lighting (CL) to intermittent lighting (IL) at an week feed restriction programs during the early growth
early age was followed by initial growth depression as period effectively reduced the number of chickens that
described earlier (Buyse et al., 1994, 1996). However, this developed ascites (Julian, 2005; Baghbanzadeh and
depression was followed by a period of compensatory Decuypere, 2008). Experimentally it has been shown that
growth, so that the birds reared in IL were reached to the other factors like age at initiation of restriction, duration of
samefinalbodyweightbysixweeks(Buysetal., 1998)and restriction and its severity, determine to a large extent the
seven weeks of age (Hassanzadeh et al., 2000). The same ability of the chickens to manifest compensatory growth to
results were found when the intermittent lighting schedule theirfullpotential(Julian, 2005). Feedrestrictionshouldnot
(1L:3D):repeatedsixtimesdailyfromthreeto42days,oran bestartedtoolate,fortoolongandnottooseverearegimen
increasing photoperiod schedule: 4 to 14 days, 6L:18D; 15 shouldbeusedotherwise,catch-upgrowthisnotmanifested
to21days, 10L:14D; 22to28days, 14L:10D; 29to35days, fully (Julian, 2005). Feed restriction can reduce the avail-
18L:6D; 36 to 42 days, 23L:1D, were used at high altitude ability of nutrients and pigmentation precursors, which may
to reduce the incidence of ascites in broiler chickens have a direct effect on weight gain, muscle mass, and the
(Hassanzadeh et al., 2003, 2005a). The beneficial effect of profit cost relationship. These effects could be more
intermittent lighting on the incidence of ascites was more pronounced if the restriction program was not performed
pronounced when IL was only applied from day 3 to 14 correctly (Camacho-Fernandez et al., 2002).
and/orfromday10to21ofage(Hassanzadehetal., 2005a). c. Antioxidants
In these studies, the reduction of ascites mortality also was Amajorcellularsourceofoxidativestressincellsoccurs
236 JournalofPoultryScience,51(3)
within mitochondria due to incomplete reduction of oxygen VitaminC,asawater-solublevitamin,canbesynthesized
toreactiveoxygenspecies(ROS) (e.g.,superoxide) (Chance atasufficientratetomeettheneedsundernormalconditions
et al., 1979). Antioxidants play a major role in protecting ofpoultry. DietaryvitaminChasbeenreportedtoimprove
cellsfromtheactionsofROSbyreducingchemicalradicals resistance to a variety of stressors, including environmental
and disrupting the process of lipid peroxidation (Yu, 1994). and pathological factors. Vitamin C is also an antioxidant
The low levels of antioxidants in birds with pulmonary that can react directly with aqueous free radicals, such as
hypertension syndrome (PHS) could therefore lead to an hydroxylradicals,bydonatingoneelectronandsoreducing
inability to control lipid peroxidation (Bottje et al., 1995). their reactivity (Yu, 1994; Bottje and Wideman, 1995,
The production of free radicals is enhanced by systemic Hassanzadeh et al., 1997b). Moreover, vitamin C has been
hypoxia, inflammation and thyroid hormones (Bottje and showntofunctioninrestoringtheantioxidantcapabilitiesof
Wideman, 1995) which cause tissue damage through the oxidized vitamin E or by converting the tocopherol radical
lipid peroxidation of cell membranes and consequently backtoitsreducedstate. Thissuggeststhatamajorroleof
increased membrane permeability (Maxwell and Robertson, vitamin C is to recycle the vitamin E radical (Bottje and
1997). Wideman, 1995).
L-Arginineisanessentialaminoacidinthechickenandit Supplemental Arginine improved the pulmonary vascular
has been suggested that the dietary inclusion levels rec- performance and pulmonary vasodilation of hypoxic broiler
ommendedformaximalgrowthratedonotcorrespondwith chickens and its effects were further improved by the
those required for maximal nitric oxide (NO) production addition of the antioxidant vitamins E and C (Ruiz-Feria,
(Dietert and Austic, 1994). L-Arginine is the substrate of 2009). The authors are making reference to that Arginine
endothelialNOsynthase(eNOS),anenzymethatsynthesizes andantioxidantvitaminsmayhaveplayedcomplementaryor
NO, a potent vasodilator (Dudzinski and Michel, 2007) and synergistic roles to increase NO bioavailability and reduce
antimitogenic (Tan et al., 2005). Basal levels of endo- oxidative stress damage, thus improving cardiopulmonary
thelium-derived NO signal the pulmonary artery smooth performance.
musclecellstorelax,thusmaintainingvasculartone(Govers Dried turmeric rhizome powder used as a spice, food
andRabelink, 2001). SupplementaionofArginineimproves preservative, and a coloring agent, is a rich source of bene-
cardiovascular performance in birds exposed to cold ficial phenolic compounds: the curcuminoids (Srinivasan,
environments (Ruiz-Feria, 2009) and has been reported to 1953). Three main curcuminoids, curcumin, demethoxy-
reduce PHS in broiler chickens (Wideman et al., 1995; Tan curcumin and bisdemethoxycurcumin (Balasubramanyam et
et al., 2005), although the results have not been consistent. al., 2003) have been isolated from turmeric. They have
The superoxide anion causes a loss of NO bioavailability strongantioxidantactivity(Asaietal., 1999). Manystudies
byshorteningitshalf-lifeandtherebyreducingpotentialfor have shown the capacity of curcumin, the most active
endothelial vasodilation (Lopez-Lopez et al., 2001). component of turmeric, to prevent lipid peroxidation, a key
Furthermore, the reaction of the superoxide anion with NO process in the onset and progression of many diseases
leads to the production of peroxynitrite, a potent oxidant (Venkatesan, 1998). Moreover, antioxidant properties of
agent that is responsible for direct tissue damage by turmeric include protection of haemoglobin from oxidation,
oxidation, peroxidation and nitration of lipids, proteins, and inhibitionn of the generation of ROS, H2O2 and nitrite
DNA(BottjeandWideman, 1995;Julian, 2005). Excessive radicals by activated macrophages, the reduction of ROS
production of free radicals could cause damage to the production in vivo, inhibition of H2O2-induced damage in
pulmonaryvascularendothelium,destructionofthecellsand human keratinocytes and fibroblasts (Chattopadhyay et al.
therefore, a reduction in the amount of eNOS. 2004). Recently,Daneshyaretal. (2012)reportedinclusion
Vitamin E is known to be a powerful lipid-soluble anti- of 5.0g/kg Curcoma longa rhizome (turmeric rhizome)
oxidant that scavenges lipid radicals. It has the ability to powder,asastrongantioxidant,reducedserummalondialde-
reactwithfattyacidperoxylradicals,whicharetheprimary hyde content and the mortality rate of ascites in broiler
products of lipid peroxidation and intercepts the chain chickens. They argued that turmeric rhizome was also
reaction, preventing further free radical reactions. During sufficienttoincreasethebloodO2saturationandbicarbonate
theantioxidantreaction,tocopherolisconvertedintoastable concentration of T3-suplemented chickens which could be
freeradical(BottjeandWideman, 1995). Therefore,vitamin related to the lowering of ascites incidence.
E could help reduce level of oxidative stress in lung blood It has been found that decreased deformity of the
vesselsandreduceendothelialdamage. Ithasbeenreported erythrocytes can increase incidence of ascites in broiler
thatbirdsthatdevelopasciteshavelowlevelsof-tocopherol chickens (Mirsalimi et al., 1993). The deformity of eryth-
in their lungs and livers, which provide evidence that a rocytes is reduced by hypoxaemia. Studies in human have
compromisedantioxidantstatusisinvolvedintheetiologyof demonstratedthaterythrocytedeformitycanbeincreasedby
pulmonary hypertension syndrome (Enkvetchakul et al., dietary supplementation of omega-3 (n-3) fatty acids from
1993). Supplementation of tocopherol in the diet (Villar- fishoils(Berlinetal., 1992). Archeretal. (1989)foundthat
Patino et al., 2002) and tocopherol as an implant (Bottje et supplementation with fish oil reduces blood viscosity and
al., 1995)havebeenusedtoimprovebodyantioxidantstatus rightventricularhypertrophyinrats. However,otherstudies
and prevent ascites incidence in broiler chickens. (Hulan et al., 1989) reported a reduction in growth rate of
Hassanzadehetal.:AscitesSyndromeinBroilers:AReview 237
birds fed red fish meal as a source of omega-3 fatty acids. tially important in reflecting endogenous versus exogenous
This is important, because the incidence of ascites can be interactions with regards to susceptibility to ascites. The
reducedbyslowingthegrowthrateofbroilers(Julian, 1993). structuralorendocrinechangesthatareoftenlinkedwiththis
The increased content of unsaturated fatty acids probably susceptibility may be influenced in the early stages of
increasesthefluidityoftheerythrocytemembraneandalters development and even during embryogenesis (Dewil et al.,
membrane function to increase the deformability of the 1996; Buys et al., 1998; Hassanzadeh et al., 2002, 2004,
erythrocyteswithapotentialhelptoreducetheincidenceof 2005a, b, 2008; De Smit et al., 2005, 2006). Therefore, it
ascites (Walton et al., 1999; Baghbanzadeh and Decuypere, has been hypothesized that developmental changes that are
2008). This could explain the reduction in whole blood induced by incubation conditions are another instance for
viscosityunderhypobaricconditionswithfeedingofflaxoil. interactions between endogen and environmental factors in
Thesefactorstogetherwoulddecreasetheresistancetoblood ascitessusceptibility,whichfurthercomplicatestheetiology
flowandimprovethemovementoftheerythrocytesthrough of this important syndrome.
the capillaries, thus improving oxygen transport and de-
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