Avian Pathology

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Ascites in poultry

Richard J. Julian

To cite this article: Richard J. Julian (1993) Ascites in poultry, Avian Pathology, 22:3, 419-454,
DOI: 10.1080/03079459308418934

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Avian Pathology (1993) 22, 419-454

REVIEW ARTICLE

Ascites in poultry

RICHARD J. JULIAN

Department of Pathology, Ontario Veterinary College, University of Guelph,

Canada, NIG 2W1

SUMMARY
Research on ascites occurring in meat-type chickens reared at moderate and low
altitude has shown that the pathogenesis is similar to that of the high altitude disease.
Pulmonary hypertension (PH) caused by increased blood flow or increased resis-
tance to flow in the lung results in right ventricular hypertrophy (RVH), valvular
insufficiency, increased venous pressure and ascites. The structure of the avian heart,
with its thin-walled right ventricle and muscular right atrioventricular valve, allows
PH to induce heart failure quickly. The sudden increase in pulmonary hypertension
syndrome (PHS) in meat-type chickens in the 1980s was associated with a rapid
increase in growth rate and feed conversion. This was a result of a combination of
genetic selection for fast-growing, heavy broilers with low feed conversion and a
more dense, high caloric, pelleted food that supplied all the nutrients required for
rapid growth and encouraged a high nutrient intake. PHS in meat-type chickens is
usually primary pulmonary hypertension, that is, PH that occurs without evidence of
prior heart or lung disease that could account for the increase in blood flow or
resistance to flow that results in the increased pressure in the pulmonary arteries.
The lungs of birds are firm and fixed in the thoracic cavity and they do not expand
to draw air into the lung. The blood and air capillaries form a rigid network that
allows only minimal expansion of the blood capillaries when more blood flow is
required. Air is moved through the lung by abdominal movement which draws air in
and out of the air sacs. The anatomy and physiology of the avian respiratory system
are important in the susceptibility of meat-type chickens to PHS. The small stature
of the modern meat-type chicken, the large, heavy breast mass, the pressure from
abdominal contents on air sacs, and the small lung volume compared to body
weight, may all be involved in the increased incidence of PHS. There is limited space
for blood flow in the avian lung. Factors that increase blood flow or increase
resistance to flow are additive. Increased blood viscosity caused by the polycythaemia
of hypoxia, or increased erythrocyte rigidity of high Na + , are more likely to produce
PH in fast-growing than in slow-growing birds. Increased flow due to cold exposure
is also additive. Ascites caused by PH is a production-related disease at low altitude.
It can be prevented easily by restricting growth rate. It is possible that some
meat-type chickens of the phenotype we have created have reached the limit of blood
flow through their lungs and that future improvements in growth rate will only be
possible if the lung and abdominal cavity capacities are enlarged.

Received 23 November 1992; Accepted 23 November 1992.

419
420 R. J. JULIAN

INTRODUCTION
For many years, ascites has been a major cause of illness and death in meat-type
chickens reared at high altitude (above 3,500 m). Research has shown that the
accumulation of fluid in the peritoneal cavities is the result of increased intravas-
cular pressure in the portal system of the liver and capillaries of the organs in the
abdominal cavity. This portal hypertension arises from right ventricular valvular
insufficiency resulting from right ventricular hypertrophy (RVH), which is a
response to pulmonary hypertension (PH).
An increase in the 1960s in ascites in broiler chickens reared at low altitude was
associated with contamination of dietary fat by dioxin. The terms "chick oedema
factor" and "toxic fat syndrome" were used to describe this condition. The
incidence of ascites at moderate and low altitude increased again in the 1970s and
there was a marked increase in the 1980s. The incidence at high altitude also
continued to increase. These increases in ascites led to many reports describing
the lesions and discussing the possible causes of so-called "waterbelly" or ascites
syndrome (AS). Research on AS has been increasing over the past 10 years and
is now carried out in many parts of the world.

DEFINITION
Ascites is an increase in the amount of lymph normally found in the peritoneal
spaces. If there is increased protein in the lymph or oedema fluid, it may contain
clumps or strands of fibrin. Since liver oedema is high protein lymph (Julian,
1985a), fluid accumulating in the hepato-peritoneal spaces frequently contains
fibrin. Fibrin in other spaces suggests vascular damage. Birds have eight coelomic
cavities (King & McLelland, 1984). Depending on the cause of the ascites the
greatest quantity of fluid is usually found in the ventral hepato-peritoneal spaces,
in the cardiac coelomic space (pericardial sac) and in the intestinal peritoneal
space. Fluid may also be found in the right dorsal hepato-peritoneal space. Fluid
has not been reported in the left dorsal hepato-peritoneal space. Very small
amounts of fluid may be found in the coelomic spaces surrounding the lung,
particularly in birds with lung oedema, but these are narrow spaces and tend not
to become distended Qulian, 1987a, 1990a; Bezuidenhout, 1988). The normal
amount of fluid in the coelomic cavities is not recorded but, except for the
pericardial sac, any visible accumulation is likely to be abnormal. Normal meat-
type chickens frequently have 1 to 3 ml of fluid in the pericardial sac at 6 to 8
weeks of age but any quantity over 4 ml is likely to be abnormal Qulian,
unpublished).

CAUSES OF ASCITES
Ascites is not a disease, it is a sign or lesion that may result from one or more of
four physiological changes that cause an increased production or decreased
removal of peritoneal lymph Qulian, 1990a).
 ASCITES IN POULTRY 421

Ascites associated with obstruction of lymph drainage

Blockage of the thoracic duct or other lymphatics by neoplasia is the main cause
of obstruction in mammals (Julian, 1985a). Implantation of an oviduct adenocar-
cinoma into the intestinal peritoneal space (Kajigaya et al, 1987; Anjum et al,
1989b) frequently results in fluid accumulation in older hens. Increased venous
pressure at the outlet of the thoracic duct may impair lymph drainage (Julian,
1985a). Broiler chickens with right ventricular failure (RVF) from PH develop
ascites very rapidly, possibly because of interference with lymph return by high
vejious pressure where the thoracic duct opens into the vena cava Qulian et al,
1989b).

Ascites associated with decreased plasma oncotic pressure

Compared with mammals, birds have low concentrations of plasma protein. It is
lower in newly hatched birds and is directly related to dietary protein Qulian,
unpublished). Plasma protein and plasma albumin are lower in young broilers
than in Leghorns on the same diet (Bowes et al, 1989). Except for the ascites of
cachexia there are no specific examples, in birds, of ascites caused by alterations
in oncotic (similar to osmotic but includes colloidal effect) pressure. Ascites may
be the result of low plasma albumin (Wise & Evans, 1975) but the description of
the heart in their report suggests an alternative pathogenesis. The loss of high
protein lymph from the liver in ascites may lower plasma protein and increase the
outflow of lymph (Julian, 1985a). Broilers with ascites from RVF have lower
plasma protein than normal broilers (Cardenas et al., 1985). Inappetence caused
by RVF may also result in lowered plasma protein and oncotic pressure.

Ascites associated with increased vascular permeability

Endothelial injury increases vascular permeability and allows fluid and plasma
protein to escape (Julian 1985a). This changes the oncotic balance and draws
fluid into the area. Free radicals damage endothelium as do a variety of bacterial
and chemical toxins Qulian, 1990a) and viral infections (Cheema et al, 1989;
Anjum, 1990). Endothelial damage may result in the accumulation of a small
quantity of fluid in affected tissues or peritoneal spaces as occurs in transudative
diathesis (Thompson & Smith, 1953; Cheville, 1966). Endothelial damage has
been suggested as the cause of the fluid leakage in ascites caused by some
phenolic compounds and coal-tar derivatives (creolin, carbolineum, etc.), dioxin
(toxic fat syndrome) (Bressler et al, 1951; Flick et al, 1973; Lekkas et al, 1986;
Julian, 1991), pentachlorophenol (Prescott et al, 1982) and chlorinated hydro-
carbons (McCune et al, 1962). When large quantities of fluid are found in the
coelomic spaces in the toxic fat syndrome (dioxin toxicity) or viral myocarditis
such as Angara disease (Anjum et al., 1989a), both endothelial damage and
increased hydraulic pressure from myocardial or liver damage are probably
involved (Allen, 1964; Julian, 1991). It is also possible that dioxin toxicity
422 R. J. JULIAN

increases tissue oxygen requirement, as do the polychlorinated biphenols (Hatch,

1988), and causes ascites by PH-induced RVF Julian, 1990a).

Ascites associated with increased hydraulic pressure in the blood vascular

system
The term hydraulic is used to describe changes that occur as the result of liquid
in motion. Increased fluid pressure in the capillary bed and sinusoids of the liver
or other permeable parts of the vascular system is the most important cause of
fluid accumulation in tissue and peritoneal spaces (Julian, 1990a). Intravascular
pressure can rise because of increased blood-flow or increased resistance to flow,
but interference with venous return is the common cause. The sinusoidal system
of the liver is fenestrated allowing high protein lymph to escape more easily. Since
the liver is closely associated with the peritoneal spaces, liver oedema results in
ascites. Fibrin clots are frequently present at necropsy (Julian, 1987a). Liver
fibrosis obstructing efferent hepatic vessels and increasing sinusoidal pressure is
the most common cause of ascites in humans. RVF with increased venous
pressure is the most common cause in animals and birds (Julian, 1990a). Since
early RVF results in oedema, swelling and mild nodular change in the liver, and
chronic RVF results in liver atrophy and fibrosis, it is important that both the
heart and liver are examined to determine the pathogenesis of ascites caused by
increased hydraulic pressure (Julian & Goryo, 1990).

Liver damage causing increased hydraulic pressure and ascites

Liver fibrosis, following repeated or severe episodes of hepatocyte necrosis, is the
usual cause of efferent hepatic vessel obstruction. Tumours, granulomas, para-
sites (Julian, 1985a) or any chronic or severe damage that obstructs venous
return, can produce this form of ascites. Toxins, infectious agents, biliary obstruc-
tion causing cholangiohepatitis, and amyloidosis are the most frequent.
Of the toxic material reported to cause liver fibrosis and ascites in poultry, only
pyrrolizidine alkaloids, such as Crotalaria poisoning and heliotropin (Thomas,
1934; Pass, 1982; Williams & Molyneux, 1987; Julian, 1991), and mycotoxins
(Asplin & Carnaghan, 1961; Dutton & Westlake, 1982; Wyatt, 1985; Hoerr,
1991), have received widespread attention. Mexican poppy also causes oedema
disease in chickens (Norton & O'Rourke, 1980). Experimental coal-tar poisoning
caused liver damage and ascites in ducks (Carlton, 1966). Hepatic amyloidosis
causes obstruction of venous return, resulting in ascites in ducks and other
waterfowl. Amyloidosis occurs frequently in young, meat-type duckling and
breeding flocks, in wild waterfowl in captivity, and in association with chronic
disease (Julian, 1988). The reason waterfowl are so susceptible to amyloid
retention in the liver and other organs is not known.
Cholangiohepatitis caused by biliary obstruction as the result of Clostridium
perfringens or other infection in the biliary system is frequently seen in broiler
chickens, at processing, in countries where necrotic enteritis occurs. In most cases
 ASCITES IN POULTRY 423

affected broilers have not shown clinical illness and they are of normal size and
body condition although jaundice may be present. The liver of affected broilers is
uniformly enlarged, up to four times normal, firm to hard, smooth and brown,
light tan or yellow with multiple small white foci scattered on the surface and
throughout the parenchyma (Randall et al, 1983; Julian, 1985b; Hutchinson &
Riddell, 1990; Randall, 1991). Hutchinson and Riddell (1990) compared broilers
with ascites to those with cholangiohepatitis at processing and pointed out that
the heart is normal in cholangiohepatitis. Some broilers with cholangiohepatitis at
processing also have ascites and occasionally broilers submitted for necropsy have
ascites caused by cholangiohepatitis. These broilers do not have RVF. The ascites
is the result of liver damage (Randall, 1991). Liver damage causing interference
with venous return and portal hypertension is reported to result in pulmonary
hypertension in rats and humans. Although the mechanism is not understood
(Rabinovitch, 1991) it may be induced by chemical mediators (endothelin)
inducing vasoconstriction in the lung (Lerman et al, 1991). Pulmonary hyperten-
sion can also be induced in rats by monocrotaline, (an hepatotoxin in poultry) the
active ingredient in Crotalaria poisoning and other toxic plants (Heath et al,
1975; Guzowski & Salgado, 1987). Toxic metabolites of monocrotaline causes
pulmonary vascular disease resulting in cor pulmonale (Rabinovitch, 1991; Ye &
Rabinovitch, 1991).

Valvular insufficiency and right ventricular failure causing increased hydraulic pressure
and ascites
Heart disease resulting in increased venous pressure can be divided into: primary
right heart or valvular disease, and right ventricular failure secondary to increased
pulmonary arterial pressure (pulmonary hypertension). Primary heart and valvular
diseases. These include three types—congenital heart diseases, right atrioventricu-
lar valve lesions and degenerative cardiomyopathies.
Congenital heart diseases such as intra-atrial and intraventricular septal defects
which result in left to right shunts, cause heart failure by the same mechanism as
PH. Congenital heart defects result in a low incidence of ascites in broiler chicks
usually within the first 2 weeks (Hemsley, 1965; Siller & Hemsley, 1966; Jackson
et al, 1972; Julian & Wilson, 1986; Julian, 1990a).
Right atrioventricular valve lesions, most frequently include valvular endocarditis
(Julian, 1990a; Randall & Pearson, 1991), which may occur secondary to
staphylococcal bacteraemia or other infection. Ascites caused by increased venous
pressure from valvular insufficiency because of right atrioventricular valvular
endocarditis occurs sporadically in broiler chickens, and in one survey of mortal-
ity in England caused 4.5% of the ascites cases (Julian, unpublished).
Endocardiosis of the right atrioventricular valve has been reported in normal birds
(Siller & Hemsley, 1966) and in ascites from RVF (Guarda et al, 1990) but in
these cases it was probably secondary to right ventricular dilation and hypertrophy
and was not the cause of valvular insufficiency.
Degenerative and dilatory cardiomyopathies, these include spontaneous turkey
424 R. J. JULIAN

cardiomyopathy (STC, cardiohepatic syndrome, round-heart disease), fura-

zolidone-induced cardiomyopathy, and other toxic, autoimmune, nutritional, and
infectious cardiomyopathies, which result in ascites when the right ventricle is
affected and RVF occurs (Wilson & Siller, 1954; Czarnecki, 1984; Julian, 1990a;
Julian et al, 1992d). In this pathogenic mechanism of ascites, RVF is secondary
to degenerative change in the muscle of the right ventricular wall and there is no
evidence that PH is involved (Webb & VanVleet, 1971; Reed & VanVleet, 1988).
Left ventricular dilation is frequently present as well. The myocardial changes are
primary and the other lesions described in ascites caused by myocardial degener-
ation result from passive congestion from increased venous pressure, following
RVF. Except for STC and more recently Angara disease, naturally occurring
degenerative or inflammatory lesions of the myocardium causing ascites are rare
in birds. STC was first described by Magwood & Bray (1962). It has become
much more prominent recently and frequently causes 3-6% mortality in commer-
cial turkey flocks. There is evidence that STC is the result of cardiac muscle
hypoxia in the late embryo or young poult (Mirsalimi et al, 1990; Julian et al,
1992d) caused by reduced egg shell porosity or low environmental oxygen, and
the high oxygen requirement of rapidly developing myocardial fibres (Julian,
1990a; Frame, 1991). The increased oxygen requirement associated with rapid
growth, cold, or excessive heat, may also be involved (Julian et al, 1992d).
Hydropericardium and ascites from heart lesions associated with vitamin E-se-
lenium responsive disease (nutritional muscular dystrophy) from free radical
damage, has been described in turkey poults and waterfowl (Wilson et al, 1988;
Austic & Scott, 1991). Furazolidone-induced cardiomyopathy has been used as a
model of dilated cardiomyopathy and has been studied extensively (Staley et al,
1978; Ferron & van Stratum, 1982; Mirsalimi et al, 1990; Julian, 1991). Field
and experimental cases of furazolidone-induced cardiomyopathy and ascites have
also been reported in ducks (Klimes & Kruza, 1962; VanVleet & Ferrans, 1983)
and chickens (Orr et al, 1986; Reed et al, 1987). Chickens, ducks and turkeys
fed high levels of rapeseed oil developed ascites apparently secondary to heart
muscle damage (Hulan et al, 1984; Ratanasethkul et al, 1976). Monensin
toxicity may result in ascites, as may other drug and chemical-induced cardiomy-
opathies Qulian, 1990a).
Until recently, myocarditis caused by infectious agents was not thought to be
an important cause of RV damage and ascites. In 1987, Angara disease (hy-
dropericardium syndrome) occurred in Pakistan (Qureshi, 1988, 1989; Anjum et
al, 1989a; Jaffery, 1989; Niazi et al, 1989). Adenovirus has been isolated from
affected broilers and is thought to cause the myocardial damage that results in
ascites (Afzal & Ahmad, 1990; Anjum, 1990; Afzal et al, 1991). A similar disease
has been reported from Iraq (Abdul-Aziz & Al-Attar, 1991). There have been
previous reports from North America of adenovirus infection causing myocarditis
(Cowen et al, 1988; Cowen 1991). Other viruses have also been reported to
cause myocarditis and ascites (Spradbrow & Bains, 1974; Reed & Winterfield,
1985; Gilka & Spencer, 1990). When hydropericardium is the most prominent
lesion as it is in the toxic fat syndrome and Angara disease, myocardial vascula-
 ASCITES IN POULTRY 425

ture damage has probably occurred and a combination of endothelial leakage and
increased hydraulic pressure from RVF may be involved in the fluid accumula-
tion.
There is some evidence that the cardiomyopathy associated with dietary potas-
sium deficiency and sudden death (Hopkinson, 1991) is PH-induced since there
is hypertrophy of the right ventricular wall (Pass, 1983).
Many general articles have been written on ascites or the ascites syndrome
describing the incidence, lesions and various causes of ascites (Neumann et al,
1975; Bergmann et al, 1979; Estudillo-Lopez, 1980; Lopez-Coello et al, 1982;
Agudelo, 1983; Ashfaque et al, 1983; Huchzermeyer, 1984, 1985; Wideman,
1984, 1988; Da Silva, 1985; Rivera, 1985; Pozos et al, 1986; Hernandez, 1987;
Odom et al, 1987; Riddell, 1987; Hoerr, 1988, 1989; Wilson et al, 1988; Canese
et al, 1989; Cowen, 1989; Gallazzi, 1989; Maxwell, 1990a).
The second category of heart disease resulting in increased venous pressure is
that associated with ascites caused by PH-induced RVF. This results in the
pulmonary hypertension syndrome (PHS), to which the remainder of this review
is devoted.

PULMONARY HYPERTENSION SYNDROME

Ascites caused by valvular insufficiency and RVF following right ventricular
hypertrophy and dilation from PH in poultry at high altitude has been recognized
for many years (Altland, 1961; Burton & Smith, 1967, 1968; Olander et al, 1967;
Burton et al, 1968, 1972; Esquerre et al, 1968; Hall & Machicao, 1968; Cueva
et al, 1970, 1974; Pizarro et al, 1970; Abati & Mcgrath, 1973; Hung et al, 1973;
Ayon et al, 1979a, 1979b; Hernandez, 1979; Sillau et al, 1980; Villaseftor &
Rivera-Cruz, 1980; Marin, 1981; Useche et al, 1981; Ploog, 1982; Huchzer-
meyer, 1984, 1985; Tellez et al, 1986).
The incidence of PHS in broilers raised at moderate and high altitude increased
dramatically in the 1980s (Da Silva, 1985; DuPreez, 1985; Huchzermeyer, 1985;
Lopez-Coello, 1985; Lopez-Coello et al, 1985a; 1985b; 1986, 1987, 1989;
Acosta-Jacome, 1986; Huchzermeyer & de Ruyck, 1986; Hernandez, 1987;
Alvarado & Gonzales, 1989). Some researchers were not convinced that the
increase in ascites at moderate altitude was associated with reduced oxygen
tension and suggested that nutrients, mycotoxins or environmental contaminants
were involved (Estudillo-Lopez, 1980; Lopez-Coello et al, 1982; Machorro &
Paasch-Martinez, 1985; Rivera, 1985).
Many researchers say that PH-induced RVF at high altitude is caused by
hypoxaemia-induced arteriolar vasoconstriction restricting blood-flow to the lung
and increasing the work-load on the RV, as appears to be the case in mammals.
Julian (1987b) however, on the basis of the work of Powell & Mazzona (1983)
and Powell et al. (1985), suggested that arteriolar vasoconstriction may not be the
cause of increased pulmonary pressure in broilers at high altitude and that the
blood capillaries of the lung are the resistance vessels in birds (i.e. that insufficient
capillary capacity may be the limiting factor for increased blood-flow through the
426 R. J. JULIAN

pulmonary circulation of broilers). Although there is a higher percentage of total

blood volume in the capillary bed of birds than in mammals, the small capillaries
of birds can expand only very little to allow for increased flow or to improve the
flow of more viscid blood or less deformable RBCs through the capillaries.
Increased blood-flow because of rapid growth and the increased blood viscosity
caused by polycythaemia because of hypoxia-induced hypoxaemia, may be the
main reasons for the dramatic increase of PHS in hypoxia-induced PH in broiler
chickens.
Ascites also became very prevalent in the 1980s in fast-growing meat-type
chickens reared at low altitude (Swire, 1980; Buys & Barnes, 1981; MacLachan
& Johnston, 1981; Agudelo, 1983; Juranova et al, 1983; Julian, 1983b; Morgan-
roth et al, 1984; Power et al, 1984; van Blerk, 1985; DuPreez, 1985; Reece et al,
1985; Riddell, 1985a, 1985b; Maxwell et al, 1986a; Fitz-Coy & Hartner-Dennis,
1988; Frankenhuis, 1988; Nixon, 1988; Wideman, 1988; Baptista & Falcao,
1989; Gallazzi, 1989; Albers & Frankenhuis, 1990; Kiran, 1990; Quessy, 1991).

Clinical signs and pathological lesion described in PH-induced ascites

The literature on ascites caused by PH-induced RVF has focused on the clinical
and pathological changes caused by RVF rather than on the physiology and
pathogenesis of the disorder, as if ascites were a disease rather than a lesion. All
the clinical signs in PHS, except lung oedema and hypoxia resulting from PH,
and all the pathological lesions, except some of those found in the heart and lung,
are the result of increased venous pressure from the RVF (Wilson et al, 1988).
The signs and macroscopic and microscopic lesions described are identical to
those found in valvular insufficiency or RVF from any cause. They are also similar
to the earlier descriptions of ascites caused by PH at high altitude and by high
dietary Na + (Krakower & Heino, 1947; Eleazer & Bierer, 1964; Olander et al,
1967; Hall & Machicao, 1968; Mohanty & West, 1969; Cueva et al, 1974;
Swayne et al, 1986). Most of the reported differences in haematology and
biochemistry between normal and ascitic birds are also the result of, rather than
the cause of, RVF.

Clinical signs
Affected broilers have cyanosis of the skin of the head and body. Veins are dilated
and prominent. The comb and wattles may be shrunken. The abdomen is dilated
with fluid in chickens that have been affected for several days or more. These
broilers have an increased respiration rate and reduced exercise tolerance. They
may die from hypoxia when handled. Broilers with lung oedema from PH also
have an increased respiratory rate and are cyanotic. They may die from hypoxia
before ascites develops. Recently affected chickens are of normal size but growth
stops when RVF develops and those that survive are smaller than their pen mates
(Hernandez, 1979; Lopez-Coello et al, 1982, 1985a,b 1986, Wideman, 1984,
1988; Julian, 1987a, 1990b; Maxwell, 1990a; Fraser, 1991).
 ASCITES IN POULTRY 427

Haematology and biochemistry

There is a marked increase in blood volume in RVF (Burton & Smith, 1972; Cai
et al, 1984; Julian & Mirsalimi, unpublished). This may be because chickens in
RVF have marked dilation of veins and lymphatics and reduced blood-flow to the
left ventricle. The resulting low systemic pressure would stimulate fluid retention
by the kidney and increases blood volume. The increase in red blood cells (RBCs)
also increases blood volume. Broilers with ascites from RVF have low blood
protein, mainly from reduced albumin (Cardenas et al, 1985). There are only
minor changes in electrolytes, but enzymes that reflect tissue damage or hypoxia
from chronic passive congestion are elevated (Jaeger & McGrath, 1974;
Rodriguez-Velez & Rosiles-Martinez, 1988; Maxwell et al, 1990). The most
significant changes are in the RBC profile. There is an increase in RBC numbers,
haematocrit, mean cell volume and haemoglobin (Cardenas et al, 1985; de
Sandino & Hernandez, 1985; Maxwell et al, 1986a, 1987, 1990; Hernandez,
1987; Niazi et al, 1989; Odom et al, 1989; Maxwell, 1990a; Witzel et al, 1990).
Hypoxaemia from high altitude or rickets-induced hypoxia causes similar haema-
tological and biochemical changes (Burton et al, 1971; Julian et al, 1986;
Maxwell, 1990a; Maxwell et al, 1990; Yersin et al, 1992) although some broilers
from these studies may have been in RVF when they were sampled. Broilers in
RVF have been shown to be hypoxaemic although it is not clear why (Julian &
Mirsalimi, 1992). Hypoxaemia causes an increase in RBCs. Since there is plasma
expansion in RVF the increased haematocrit indicates a marked increase in total
RBCs, many of which are young, large cells. Changes in leukocyte values appear
to be a response to disease and stress with increased granulocytes and decreased
lymphocytes (Maxwell et al, 1986a).

Pathological lesions
At necropsy the skin and tissues are congested and may be red or quite dark. The
veins are dilated with blood and are prominent, particularly in the skin and on the
heart and intestine. There is a large or small quantity of clear, yellow, fluid with
clots of fibrin in the peritoneal cavities. The liver may be swollen and congested
or firm and irregular with oedema and have fibrin adherent to the surface. It may
be nodular or shrunken, it may be white with oedema under the capsule and have
a thickened capsule. There is a mild to marked hydropericardium and occasion-
ally there is epicarditis with the pericardium adherent. The right atrium, sinus
venosus and vena cava are very distended. Frequently there is hypoplasia of the
left ventricle wall. The lungs are extremely congested and oedematous (Teucher
et al, 1971; Neumann et al, 1975; Useche et al, 1981; Huchzermeyer, 1984;
1985; Lopez-Coello et al, 1985a, 1985b, 1986; Rivera, 1985; Maxwell et al,
1986a, 1987, 1990; Hernandez 1987; Julian 1987a, 1990b; Riddell, 1987, 1991;
Cerruti-Sola et al, 1988; Wilson et al, 1988; Fraser, 1991; Quessy, 1991).
Not all broilers that die from PH have ascites. Death may occur suddenly
before clinical signs are observed or after a short period of dyspnoea and affected
428 R. J. JULIAN

broilers frequently die on their back. At necropsy there may be a swollen liver,
venous congestion, a dilated right atrium and vena cava and marked hypertrophy
of the right ventricle wall, as well as marked lung oedema and congestion (Julian
etal, 1987, 1989b; Julian, 1990b).
Various microscopic lesions, most of which are caused by increased venous
pressure, have been described in broilers with ascites by Hall & Machicao (1968),
Teucherera/. (1971), Riddell, (1985b, 1987, 1991), Maxwell et al. (1986, 1988),
Hernandez, (1987), Wilson et al. (1988), Dominguez et al. (1990), Maxwell,
(1990b), Witzel et al. (1990). Changes in the myocardium are mild. There is
oedema of the myocardium and slight proliferation of loose connective tissue in
some areas. Myocardial fibres show pallor of cytoplasm and atrophy or hypertro-
phy, with variation in size of myofibres and their nuclei. There is an increase in
the number of heterophils between myocardial fibres and fibrosis of the atrial
endocardium. There is diffuse oedema and congestion in the lung and there may
be an increase in interstitial connective tissue. Hypertrophy of smooth muscle
within the parabronchical walls is prominent and is accompanied by collapse of
the atria. Increased numbers of cartilaginous or bony nodules are present in the
pulmonary parenchyma. In the liver there is dilation of periacinar sinusoids and
atrophy of intervening hepatocytes. There is a decrease in the amount of vacuola-
tion of hepatocytes, and cholangioles are frequently filled with bile. Occasional
hepatocyte necrosis is present. Proliferation of fibrous tissue within the capsule is
often accompanied by dilation of capsular lymphatics. Similar changes occur in
the capsule of kidney, spleen and pancreas. Decreased numbers of lymphocytes
are apparent in most tissues examined. This includes lymphoid organs such as
spleen and thymus, and the aggregates of lymphoid tissue seen normally in most
other organs. Other changes observed include necrosis and mineralization of
scattered renal cortical tubules, dilation of collecting tubules, atrophy of skeletal
muscle fibres, and an increase in the amount of zymogen in pancreatic acinar
cells.
Maxwell et al. (1986b, 1989), Maxwell (1990c) and Dominguez et al. (1990)
described ultrastructural lesions in ascites secondary to RVF. Many of the
changes are the result of rather than the cause of PH and the myocardial changes
described are similar to those in spontaneous turkey cardiomyopathy and NaCl-
induced cardiomyopathy (Gough et al., 1981; Onderka & Bhatnagar, 1982).
Maxwell et al. (1986b) and Domiguez et al., (1990) describe thickening of the
respiratory membrane and marked swelling of the capillary endothelial cells in
broilers with ascites. Similar ultrastructural changes are described in broilers at
high altitude and in hypoxic conditions (Maxwell et al, 1989; Maxwell, 1990c).
Some of these broilers had ascites from RVF. Mitochondrial hyperplasia of
myocardial cells was prominent in young broilers at high altitude. Virus particles
were also seen by Maxwell et al. (1986b) in broilers with ascites. These particles
were identified as retrovirus by Payne et al. (1991) but they were not successful
in producing myocarditis with the isolate (Payne, unpublished). Haemorrhage
into parabronchi (Maxwell, 1990c) is a common iatrogenic change in chickens
killed by cervical dislocation (Julian, unpublished).
 ASCITES IN POULTRY 429

Signs and lesions caused by pulmonary hypertension

It is difficult to separate changes caused by hypoxia or PH from changes that
result from increased hydraulic pressure and the hypoxia caused by RVF unless
the examination is done before valvular insufficiency and RVF occur. In most
descriptions of the clinical, haematological, biochemical and morphological re-
sponses this has not been done. It was not done in the studies of spontaneous
pulmonary hypertension and percent haemoglobin oxygen saturation (SaO2) in
rapidly growing broiler chickens by Peacock et al. (1988, 1989a, b, 1990) and
Reeves et al. (1991). Researchers who have measured PH agree that RVH, as
measured by the ratio of the right ventricle (RV) to the total ventricle (TV)
(RV:TV), is caused by PH (Avervill et al, 1963; Cueva et al, 1974; Hernandez,
1979; Sillau et al, 1980; Aleman-Mendez, et al, 1987; Guthrie et al, 1987).
The RV to left ventricle (LV) ratio is also a measure of PH until RVF occurs,
after which atrophy of the LV distorts the ratio (Julian et al, 1989b). RV and LV
to body weight (BW) ratios have also been used to reflect pulmonary and systemic
hypertension Qulian & Wilson, 1986; Julian, 1987b; Mirsalimi et al, 1992). The
hypertrophy of the muscle of the muscular pulmonary arteries and arterioles that
has been reported in ascites at high altitudes (Montalvo et al, 1979; Sillau &
Montavalo, 1982) can be a response to PH (Owens & Schwartz, 1982; Meyrick,
1991) but it is not clear whether the small avian pulmonary arterioles respond to
hypoxia by constriction causing medial hypertrophy of the peripheral pulmonary
vessels as occurs in mammals (Black & Tenney, 1980; Scheid & Holle, 1978;
Meyrick, 1991; Elliot et al, 1991). The mitochondrial hyperplasia described by
Maxwell (1990c) in the heart of 7-day-old broilers was probably pressure-in-
duced. The other myocardial changes described by Maxwell et al, (1989) and
Maxwell (1990c) and others might be pressure-induced or they could result from
hypoxia following RVF.
If the capillaries are the resistance vessels in PH in broiler chickens, the
increased pressure in the normally low pressure capillary bed of the lung would
result in interstitial and air capillary oedema. That would increase the thickness
of the respiratory membrane as described by Maxwell et al. (1986b) and could
result in hypoxaemia. It would also decrease the size of the already small blood
capillaries and could further increase the resistance to blood-flow. Severe pul-
monary oedema as the result of PH would result in hypoxic respiratory failure and
death and would explain the increasing incidence of sudden death without ascites
in PHS (Julian et al, 1989b).

Pathogenesis of pulmonary hypertension

Hypoxia results in hypoxaemia, which increases haematopoietin production and
markedly increases the haematocrit (Burton & Smith, 1969; Burton et al, 1971;
Julian et al, 1986). Polycythaemia increases blood viscosity and is the most
important cause of the increased resistance to blood-flow that results in PH
(Burton & Smith, 1967, 1969; Burton et al, 1971; Snyder, 1971; Penney et al,
430 R. J. JULIAN

1988). Hypoxia also affects RBC deformability (Hakim & Macek, 1988). Hy-
poxia is probably the cause of the hypertrophy of the parabronchiolar smooth
muscle and the increase in the number of cartilaginous nodules in the lung
(Wilson et al, 1988), but the most severe hypoxia occurs after ascites and RVF
develop, so these changes are likely to be the result of hypoxia following PH-in-
duced RVF, rather than the cause of hypoxia. Some researchers investigating
PHS at low altitude, work on the premise that the condition is caused by lack of
environmental oxygen (Peacock et al, 1988) or lung damage interfering with
oxygen exchange (Wideman, 1988). Others suggest that PHS at low altitude and
the increased incidence at high altitude is related to the high oxygen requirement
of rapid growth and the inability of the heart and lung to deliver sufficient oxygen
to the tissue to maintain genetic and nutritional growth rate potential. High
incidence flocks are frequently those with superior growth rate and feed conver-
sion (Julian, 1987a, 1990c). Because PH-induced ascites at high altitude is
caused by low atmospheric oxygen tension from low barometric pressure, and
because PHS is easy to produce experimentally with hypobaric chambers (Boyd
& McDaniel, 1972; Owen et al, 1990; Witzel et al, 1990) or reduced oxygen
concentration (Maxwell etal, 1987, 1990; Hel et al, 1988), it has been assumed,
without any evidence, that PHS at low altitude is also associated with low
environmental oxygen concentration (Lopez-Coello et al, 1985b, 1986, 1989;
Dale & Villacres, 1986b; Maxwell, 1990b; Albers & Frankenhuis, 1990; Dale,
1990a) or negative pressure in pens caused by ventilation fans (Huchzermeyer,
1984).
There is no research that shows that low oxygen or high carbon dioxide are
associated with ascites at low altitude, and the few reports in which air was
analyzed indicate that pen oxygen concentration is only slightly below outside air
oxygen levels. Julian & Wilson (1992) reported 20.20% to 20.75% oxygen and
0.06% to 0.52% carbon dioxide in closed poultry pens with all fans off for 2 min
(outside air 20.80% to 20.90% oxygen). There was no difference in oxygen
concentration between pens with a high or low incidence of ascites. Many cases
of ascites caused by PH have been in small "farm-yard" flocks that have been
outdoors or in open-sided buildings (Julian, unpublished).
The response of birds to hypoxia has been studied for many years (Atland,
1961; Smith & Abbot, 1961; Butler, 1967; Jaeger and McGrath, 1974). Adult
Leghorn chickens showed no clinical signs or physiologic change and apparently
were able to oxygenate their haemoglobin fully, down to an oxygen concentration
of below 15%, equivalent to an altitude above 2500 m (Abati & McGrath, 1973;
Besch & Kadono, 1978; Mohan-Raj & Gregory, 1991). However, there may be
a wide variation in oxygen saturation capability in birds since Black et al (1978)
found a difference between ducks and Bar-headed geese. Julian et al. (unpub-
lished), using a hypobaric chamber at an atmospheric pressure of 592 mmHg
(equivalent to an altitude of 2054 m or 16.3% O2) produced polycythaemia but
not PH in young Leghorn chickens, Pekin ducks and heavy turkeys on a low
protein diet. Heavy turkeys on a high protein (fast growth diet) did develop PH
(Julian et al, 1992c).
 ASCITES IN POULTRY 431

Chickens have a thicker respiratory membrane than other birds, and broilers
have a thicker respiratory membrane than Leghorn-type fowl (Viyadaran et al,
1987, 1990) so the ability of broilers to move oxygen into haemoglobin is not as
good as that of other birds. There is no information on oxygen dissociation or
haemoglobin types in modern fast-growing meat-type chickens, or on how they
compare with other birds. Research on meat-type chickens indicates that fast-
growing broilers have a lower percentage SaO2 than slow-growing broilers
(Peacock et al, 1988, 1989a,b, 1990; Reeves et al, 1991; Julian & Mirsalimi,
1992) although Huchzermeyer et al. (personal communication) found no differ-
ence between strains. These results suggest that some meat-type chickens are not
fully oxygenating their haemoglobin at low altitude. If fast-growing meat-type
chickens are hypoxic, the hypoxia maybe the result of interference with respira-
tion because of the large breast muscle mass or intra-abdominal pressure from fat
and internal organs (Anderson et al, 1986; Fedde, 1989; Julian & Mirsalimi
1992), since pen oxygen levels are not low (Julian & Wilson, 1992). Tidal volume
is reduced in birds in the supine position (King & Payne, 1964) but Reeves et al.
(1991) could find no differences in respiratory rate or tidal volume in fast-growing
compared to slow-growing broilers. Problems with oxygen transfer through the
respiratory membrane and differences in haemoglobin oxygen affinity would also
have to be considered.
The heart of birds is different from mammals in that the LV is thick-walled and
the RV thin-walled. The right atrioventricular valve is also different and is
composed of a muscle flap made up mainly of muscle fibres from the RV wall.
The anatomy of this valve makes the bird very susceptible to valvular insufficiency
Qulian et al, 1987; Julian, 1990a). The thin RV responds very rapidly to
increased workload by dilation (stretch) and hypertrophy (response to stretch)
(Owens & Schwartz, 1982). When the RV wall hypertrophies the right atrioven-
tricular valve also hypertrophies, leading to valvular insufficiency and RVF
Qulian, 1987). Genetic or congenital differences in the RV wall or valve may
make some broilers even more susceptible to PH-induced RVF as suggested by
structural and electrocardiographic studies (Asson-Batres et al, 1989; Odom et
al, 1989, 1991, 1992c; Martinez et al, 1992).
Since PHS is caused by increased pressure in the pulmonary arteries and RV,
recent research has focused on the causes of PH. Stretch-induced muscle hyper-
trophy occurs because of increased intracardiac and intravascular pressure and is
the result of DNA ploidy (Owens & Schwartz, 1982; Maxwell et al, 1989;
Maxwell, 1990c; DeVol, 1991). RVH results from increased volume and/or
pressure work-load causing stretching of muscle fibres, and RVH reflects PH
(Cueva et al, 1974; Sillau et al, 1980; Guthrie et al, 1987). Increased pulmonary
pressure results from increased blood-flow (increased cardiac output) or in-
creased resistance to flow in the pulmonary vascular system (Figure 1) Qulian,
1987b, 1990a,b). PH may result from increased blood-flow causing both a
volume and pressure overload, due to:

(a) Increased oxygen requirement (tissue hypoxia)

432 R. J. JULIAN

(b) Incomplete oxygen saturation of haemoglobin (blood hypoxia, hypox-

aemia).
(c) Anaemia
(d) Increased blood volume (hypervolaemia)
(e) Intraventricular and interatrial septal defects and other cardiac defects
which may also increase RV blood volume and pressure. Right atrioventric-
ular valvular insufficiency increases blood volume. These heart defects will
not be considered further.
Alternatively PH may be due to increased resistance to flow, which would cause
only a pressure overload, due to:
(a) Factors affecting blood-flow dynamics:
(i) polycythaemia causing increased blood viscosity
(ii) increased RBC rigidity (reduced deformability)
(iii) megalocytosis
(b) Reduced vascular capacity, from:
(i) pulmonary vascular disease
(ii) emboli obstructing vessels
(iii) endothelial cell hypertrophy or hyperplasia
(iv) interstitial oedema or pneumonitis reducing or blocking capillary
blood flow.

PHS caused by increased blood-flow

Increased oxygen requirement
The most important cause of increased blood-flow (cardiac output) is increased
body oxygen requirement resulting in tissue hypoxia which occurs, for example,
with exercise in human and animal athletes and in which both heart-rate and
stroke-volume combine to increase blood-flow (Julian, 1990b). Research evidence
points to the increased metabolic oxygen requirement of high food intake and
rapid growth as the cause of the recent marked increase in PHS in broiler
chickens at both low and high altitude (Hernandez, 1982; Dale & Villacres, 1987,
1988; Julian et al, 1987, Odom et al, 1992c).
Meat-type chickens are selected for growth rate and muscle mass, which have
increased by up to 5% per year over the past 30 years. These birds have also been
selected for feed conversion, so that the digestive system and muscle mass have
developed at the expense of the heart and lung (Julian, 1990c). As a percentage
of body weight the lung of a meat-type chicken is smaller than that of other
chickens (Julian, 1989). There is now sufficient evidence to confirm that PHS is
related to metabolic oxygen requirement at both high and low altitude and that
anything that increases O2 requirement increases the incidence of ascites caused
by PH (Julian et al, 1987, 1989b; Da Silva et al, 1988; Scheele & Frankenhuis,
1989; Albers & Frankenhuis, 1990; Vereijhen & Albers, 1990; Vega et al,
1991a,b). Body size also affects O2 requirement.
 ASCITES IN POULTRY 433

Rapid growth High-density, pelleted ration, superior management and

HighBMR environment

Increased body Cold, moderate heat, activity, hyperthyroidism,

demand for -< • overeating, feed or toxic material increasing metabolic
oxygen oxygen requirement

' Hypervolaemia
— (Na* toxicity)
— Cardiac defects (left to right shunts) or valvular
Increased endocarditis
Increased flow - Hypoxaemia increasing blood flow
(cardiac output) flow — hypoxia (high altitude, severe rickets, internal
abdominal pressure, large breast mass, etc.)
— reduced O2 carrying capacity (carbon monoxide,
anaemia, nitrate)
— lung pathology affecting diffusion

t Increased Insufficient vascular capacity in pulmonary capillary bed

Increased (primary pulmonary hypertension)
pulmonary arterial Organic vascular obstruction (polycythaemia, reduced
resistance
pressure RBC deformability, lung pathology narrowing
to flow
capillary bed, megalocytosis, emboli)
[_ Vasoconstriction (Na* toxicity, hypoxia)

Right ventricular Increased intravascular pulmonary pressure, resulting in

hypertrophy hypertensive lung oedema & sudden death

Valvular insufficiency
Right ventricular dilation
Right ventricular failure

Liver congestion & oedema

\
ASCITES

Adapted from: JULIAN, R.J. The effect of increased sodium in the drinking water on right ventricular
hypertrophy, right ventricular failure and ascites in broiler chickens. Avian Pathology, 16, 61-71,1987.

Figure 1. Diagrammatic summary of possible causes of increased pulmonary arterial pressure in

broiler chickens resulting in increased right ventricular work-load.

Diet

There are many reports on the effect of growth rate, high energy and high density
rations and feed restriction on the incidence of PHS (Acosta-Jacome, 1986;
Albers et al., 1990; Arce et al., 1988, 1989a; Dale, 1987, 1990a,b; Dale &
434 R. J. JULIAN

Villacres, 1986a,b,c; Da Silva, et al, 1988; Hernandez, 1987; Julian, 1987a;

Lopez-Coello, 1985; Reeves et al, 1991). Studies have shown that PHS can be
reduced or prevented by using feeding regimes which slow growth or reduce
metabolic rate. Restricting growth by changing the texture, density, energy level,
or availability of feed are the usual methods used (Albers et al, 1990; Arce et al,
1989a; Berger, 1992; Dale, 1987, 1990a,b; Hernandez, 1982; Huchzermeyer,
1986; Moreno et al, 1991; Palos et al, 1991; Rubio & Lopez-Coello, 1986;
Shlosberg et al, 1991, 1992; Suarez & Rubio, 1989). Recovery may also occur
(Cerruti-Sola et al, 1988; Shlosberg et al, 1992;).

Cold and heat

High temperature (above 30°C) reduces food intake, which in turn reduces PHS,
although Huchzermeyer et al. (1989) have shown that oxygen requirement
increases above 22°C. If broilers continued to eat and grow well at 25°C to 30°C
the incidence of PHS would increase as it does with cold exposure.
The recent increase in ascites both at high and low altitude has been noted to
be more marked in cold weather (Villasenor & Rivera-Cruz, 1980; Hernandez,
1984; Huchzermeyer & DeRuyck, 1986; Fitz-Coy & Hartner-Dennis, 1988;
Julian et al, 1989b; Shlosberg et al, 1992). Although some workers have pointed
to the possibility of poor ventilation causing low environmental oxygen, or
noxious fumes causing lung damage in cold weather, there is no evidence to
support this pathogenesis, and recent research shows that the increased metabolic
rate induced by cold causes a marked increase in oxygen requirement and cardiac
output resulting in PH. Gleeson (1986) showed a 185% increase and Huchzer-
meyer et al. (1989) a 32.7% increase in oxygen requirement with cold
temperature. Julian et al. (1989b) and Stolz et al, (1992), reported a marked
increase in PHS with cold exposure. Increased oxygen requirement is probably
the most important factor in cold-induced PHS. Cold may also increase blood
viscosity (Moye et al, 1969), perhaps by decreasing blood volume.
Oxygen requirement is increased by some nutrients (Julian et al, 1992a). Drugs
and chemicals which are toxic because they increase tissue oxygen requirement
may contaminate feed or water (Gleesoo, 1986; Hatch, 1988). There are also
strain differences in growth rate and oxygen requirement (Arce et al, 1989b;
Huchzermeyer et al, 1988; Julian et al, 1989b; Martinez et al, 1991; Odom et al,
1992a; Vereijken & Albers, 1990). Increased thyroid activity increases the
metabolic rate and the oxygen requirement and increases the incidence of ascites
(Vega et al, 1991a,b). Triiodothyronine (T3) added to the diet will increase the
incidence of ascites (Decuypere et al, 1992).

Haemoglobin oxygen saturation

Incomplete oxygen saturation of haemoglobin is the most important cause of PH
at high altitude but increased blood-flow because of tissue hypoxia from hypoxic-
hypoxaemia is not likely to be the major reason that PH occurs. Increased blood
 ASCITES IN POULTRY 435

viscosity from polycythaemia and/or arteriolar vasoconstriction are likely to be

much more significant. This is also true of rickets-induced hypoxic-hypoxaemia
Qulian et al, 1986; Kradel et al, 1988). The low SaO2 levels related to rapid
growth may not be low enough to stimulate polycythaemia but this possibility
must be investigated. Haemoglobin oxygen affinity is altered by alkalosis and
acidosis. This is one of the explanations for the polycythaemia that occur with
ingested or injected cobalt chloride (Jelkman, 1992). Cobalt chloride will induce
polycythemia and PH-induced RVH and ascites in meat-type chickens Qulian et
al, unpublished).
It has frequently been suggested in poultry industry literature that hypoxia
resulting from lung damage caused by noxious fumes from poor ventilation,
respiratory disease and stress are the cause of the increased incidence of ascites
(Albers and Frankenhuis, 1990; Dale 1990a; Dale & Villacres, 1986b; Enciso &
Enciso, 1989; Lopez-Coello et al, 1985a, 1985b, 1986; Maxwell, 1990a; Wide-
man, 1984, 1988). However, there is no evidence from research that noxious
fumes or stress cause ascites. The report by Julian & Wilson (1984) on the effect
of carbon monoxide was a case report. The highest level of carbon monoxide
found was 70 parts/106 present only during the early brooding period. Carbon
monoxide has been shown to cause hypoxaemia and RVH in rats (Penney et al,
1988). In the epidemiologic study by Arce et al. (1986) on ascites, ammonia was
only 17 parts/106 and increased ammonia was directly related to decreased
temperature, which has been shown to increase oxygen requirement and PHS
(Huchzermeyer et al, 1989; Julian et al, 1989b). Experiments with high ammo-
nia have not produced significant lung damage (Al-Mashhadani & Beck, 1985).
In fact, high levels of ammonia and stress may reduce ascites by reducing
performance rather than, as suggested by Dale (1990a), increasing ascites. There
is no research to support the suggestion by Huchzermeyer (1986, 1989) that
E. colt toxins causing vasoconstriction produces PHS in broilers, although inhaled
endotoxin can be measured in the blood of poultry workers (Donham, 1991).
Aspergillosis is the only naturally occurring respiratory disease that has been
shown to cause PHS. Ascites has been observed following aspergillosis in broilers
(Agudelo, 1983; Huchzermeyer, 1986; Julian & Boulianne, 1988; Julian, 1990a).
Recent research indicates that severe pulmonary aspergillosis causes hypoxic-hy-
poxaemia-induced PHS and that less severe aspergillosis infection results in
fibrosis in the lung with PHS and RVF secondary to pulmonary pathology (cor
pulmonale)Qulian & Goryo, 1990). There are no reports of RVH associated with
viral or bacterial respiratory disease in broilers, but RVH has been observed in
12-week-old turkeys with severe airsacculitis caused by aspergillosis Qulian,
unpublished). Amiodarone-induced lung damage causing PHS has been reported
by Julian et al (1989a) but the restriction was in vascular flow not oxygen
exchange (an experimental model of cor pulmonale).
Bowes (1990) reported a high incidence of ascites in 3-week-old broilers that
had eaten feed containing a toxic level of dicalcium phosphate. There was severe
lung damage with calcification in affected broilers. This condition would have to
be differentiated from the cartilaginous and bony masses seen in broilers Qulian,
436 R. J. JULIAN

1983a) and which are much more frequent in ascites (Maxwell, 1988; Maxwell et
al, 1988; Julian et al, 1989a). These reports and the little research on lung
damage and PHS indicate that only severe lung damage, that causes hypoxia even
when growth rate is reduced, will result in PHS.

Anaemia
Anaemia reduces the oxygen-carrying ability of the blood and would result in
increased blood-flow; however it would also reduce growth rate and oxygen
requirement. Anaemia is reported to cause PH in chickens and turkeys (Huchzer-
meyer et al, 1987; Huchzermeyer, 1988) but no ascites was seen. The anaemia
was induced by blood parasites which also affect RBC rigidity and could increase
resistance to flow (Krogstad et al., 1991).

Increased blood volume

Increased blood volume may be a major factor in some forms of PHS. High
dietary salt increases blood volume and may be the main cause of PHS induced
by NaCl (Julian, 1987b; Mirsalimi & Julian, in press), but salt also increases RBC
rigidity (Mirsalimi et al, 1992) which increases resistance to flow. Sodium causes
hypertension-induced left ventricular hypertrophy in people (Fields et al, 1991).
High dietary salt is a common cause of PHS and should be considered whenever
there is an increased incidence of ascites (Adams et al, 1991; Julian et al, 1992b).
An increased incidence before 21 days suggests high dietary Na + particularly if
both sexes are affected Qulian, 1990a, 1991). Many reports of unexplained ascites
fit the description of salt toxicity (Lohr, 1975; Kamindjolo et al, 1977; Wilson et
al, 1988; Kapaga, 1990; Reece, 1991; Samaha and El-Bassiouny, 1991). In any
case of higher-than -normal ascites mortality, sodium level in both food and water
should be examined along with dietary potassium and calcium.
RVF increases blood volume and the hypoxaemia associated with RVF results
in polycythaemia Qulian & Mirsalimi, 1992), which, when the increased blood
volume is taken into account, indicates a marked increase in RBC numbers. Poly-
cythaemia increases both blood volume and viscosity (Burton & Smith, 1972; Cai
et al, 1984). Increased volume and polycythaemia both increase RV workload.

Increased resistance to blood-flow causing PHS

Although increased blood-flow may be the major contributor to PHS at low
altitude, increased resistance to flow may be more important at high altitude and
in other situations where hypoxaemia is involved.

Factors affecting blood-flow dynamics

Polycythaemia. This causes increased blood viscosity. Hypoxaemia very quickly
causes polycythaemia by stimulating erythropoietin production. Polycythaemia
increases blood viscosity and markedly increases the resistance to blood flow
through the lung (Smith & Abbott, 1961; Burton &' Smith, 1967, 1969; Cai et al,
 ASCITES IN POULTRY 437

1984). Polycythaemia occurs rapidly in hypoxic conditions and can be measured

within a few days (Maxwell et al, 1990; Yersin et al, 1992). RVF does not usually
occur for 2 to 3 weeks but hypoxic conditions in the incubator induce RVF more
quickly if chicks are subjected to hypoxic conditions following hatching (Odom et
al, 1992a,b; Rosenbaum et al, 1992). Cold also induces polycythaemia (Moye et
al., 1969) although it is not clear if it does this by causing hypoxaemia or by
reducing plasma volume.

Increased RBC rigidity. Blood flow dynamics is markedly affected by erythrocyte

deformability (Gregersen et al, 1968; Hakim & Macek, 1988). Because of the
small blood capillary size and its lack of ability to expand to accept increased flow,
reduced RBC deformability may be a significant cause of increased resistance to
flow and PH in the lung of meat-type chickens. The RBCs of meat-type chickens
are more rigid than those of Leghorn chickens (Mirsalimi & Julian, 1991).
Increased corpuscular haemoglobin concentration reduces RBC deformability.
Increased dietary NaCl also increases RBC rigidity and may be the most impor-
tant mechanism in salt-induced PH (Mirsalimi et al, 1992). Hypoxaemia has
been shown to increase RBC rigidity (Hakim & Macek, 1988). Blood parasites
also reduce RBC deformability (Krogstad et al, 1991) and have been reported in
PHS in poultry (Huchzermeyer et al, 1987; Huchzermeyer, 1988). Many things
may affect the RBC membrane and influence the ease of blood flow. This may be
the explanation for the reported reduction of the incidence of ascites by feeding
vitamin C (Agudelo, 1979; Landeros, 1983; Al-Taweil & Kassab, 1990) although
Molina et al. (1982) reported no effect with vitamin C and other vitamins.
Digoxin has also been reported to reduce the incidence of ascites (Otalora et al,
1988).

Megalocytosis. Increased RBC size has been suggested as a cause of increased

resistance to flow (Julian, 1987b; Maxwell, 1990a, 1991) but this has not been
confirmed. In fact, large RBCs are more deformable than small ones that tend to
be spherical rather than biconcave (Smith et al, 1979). Erythrocyte haemoglobin
concentration increases with age as cells become smaller and less deformable. A
large nucleus would probably increase rigidity and interfere with flow. The
elliptical shape may also affect blood-flow dynamics and deformability. Young
broiler chickens have more large RBC than Leghorns (Julian, 1990b) probably
because the increased demand of rapid growth results in a high proportion of
young cells. The deformability of large abnormal and large young avian RBCs has
not been investigated.

Reduced vascular capacity

Pulmonary vascular disease. Pulmonary arteriolar vasoconstriction may play a
significant role in increasing vascular resistance to blood-flow through the lung in
hypoxic conditions in birds as it does in mammals. The effect is much more
pronounced in some mammals than others (Elliott et al, 1991) but definitive
438 R. J. JULIAN

evidence for hypoxia-induced vasoconstriction is lacking in birds. Hypoxic vaso-

constriction was demonstrated by Scheid & Holle (1978) in ducks, but not by
Black & Tenney (1980) in geese and ducks. Most of the reports of medial
hypertrophy in chickens are based on morphometric analysis of muscular pul-
monary vessels from chickens with PH-induced ascites (Montalvo et al, 1979;
Sillau & Montalvo, 1981). The increased intra-arteriolar pressure in these birds
would induce muscle hypertrophy in the vessel walls, as it does in the RV (Owens
& Schwartz, 1982), so the changes reported in these arteries might not be caused
by hypoxia-induced vasoconstriction (Meyrick, 1991). Experimental restriction of
the pulmonary arteries in birds will produce PH as it does in mammals (Montejo
et al, 1984).

Embolic pulmonary vessel obstruction. Increased numbers of cartilaginous and bony

masses have been reported in the lungs of broilers with ascites (Maxwell, 1988;
Maxwell et al., 1988; Julian et al, 1989a; Reece, 1991; Wilson et al, 1988). Large
numbers of these nodules could obstruct blood-flow but there is no evidence that
the increased number are the cause of PHS (Julian, 1990b). It is more likely that
the physiologic changes associated with PH-induced hypoxia in the lung favour
the development and retention of nodules that would have been removed in
normal birds (Julian et al, 1989a). The ascites resulting from intravenous injec-
tion of carbon suspension reported by Olah et al. (1983) was probably caused by
acute PH arising from obstruction of blood capillaries, since capillaries were
blocked by carbon particles when this technique was used to produce ascites
(Julian, unpublished).

Endothelial cell hypertrophy or hyperplasia. The endothelial cells in birds are phago-
cytic and can be activated by biological and chemical materials. Intravenous
injection of carbon suspension caused blood capillary endothelial cell hypertrophy
(Julian, unpublished). In the experimental model of amiodarone-induced PH
there was endothelial hyperplasia and hypertrophy as well as damage to the
respiratory epithelium (Julian et al, 1989a). Endotheliosis has been associated
with dioxin toxicity in chickens (Simpson et al, 1959).

Interstitial oedema or pneumonitis reducing or blocking blood capillary flow. It is

frequently stated that lung damage is the cause of the increased incidence of
ascites in broiler chickens but there is little evidence to support this thesis. Since
injury to the respiratory system slows growth, the effect on oxygen exchange or
blood-flow would have to be severe before pulmonary hypertension would occur.
In humans and animals chronic fibrosis and fibrosis secondary to interstitial
pneumonitis, restrict capillary blood flow and cause cor pulmonale (Crystal et al,
1981). In birds, the lung is more rigid than in mammals and blood capillaries are
unable to expand significantly. Even mild interstitial oedema as occurs with
increased dietary salt (Julian, 1987b) or early PH (Julian, 1987a) could interfere
with blood flow and oxygen exchange. Early severe aspergillosis causes hypoxia
and ascites but early milder aspergillus pneumonia causes interstitial pneumonitis
 ASCITES IN POULTRY 439

and fibrosis resulting in reducing capillary flow and PH (Julian & Goryo, 1990).
The lung vasculature or epithelium may be injured by inhaled or circulating
ingested, or injected drugs and other chemicals (Adamson et al, 1977; Cooper et
al, 1986; Julian et al, 1989a; Rabinovitch, 1991). Cor pulmonale from lung
damage was one of the manifestations of the toxic oil syndrome resulting from
ingestion of contaminated rapeseed oil in humans in Spain (Gomez-Sanchez et
al, 1991). Dietary rapeseed oil has been reported to cause myocarditis and ascites
in poultry (Ratanasethkul et al, 1976; Hulan et al, 1984). Pulmonary hyperten-
sion was not reported in these cases. Since many by-products from industry,
human food preparation (waste cooking oil), animal and poultry processing and
chemically treated protein supplements are used in poultry feed, lung damage
from nutrients or chemical contaminants is possible.

ACKNOWLEDGEMENT
I would like to thank Dr F. Huchzermeyer for the use of his extensive list of
references and Dr G. Diaz for his assistance with manuscripts written in Spanish.

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RESUME

Les ascites chez les volailles

Une étude menée sur les ascites se déclarant sur les poulets de chair élevés à des altitudes
basses ou modérées a montré que la pathogenèse est similaire à la maladie en haute altitude.
L'hypertension pulmonaire (HP) causée par un débit sanguin accru ou par une plus grande
résistance au débit dans le poumon provoque une hypertrophie du ventricule droit (HVD), une
insuffisance valvulaire, une pression veineuse plus importante et des ascites. Chez la volaille,
l'HP peut provoquer rapidement une défaillance cardiaque du fait de la structure du coeur
avec un ventricule droit à fine paroi et une valve atrio-ventriculaire musculaire droite. Dans les
années 1980, l'augmentation rapide du syndrome de l'hypertension pulmonaire (SHP) chez les
poulets de chair a été associée avec une hausse rapide du taux de croissance et du taux de
conversion alimentaire. Ceci était le résultat d'une sélection génétique pour une croissance
rapide, des poulets de chair à poids élevé avec un taux de conversion alimentaire faible et des
aliments granulés hautement caloriques, apportant toutes les substances nutritives nécessaires
à une croissance rapide et permettant une consommation alimentaire élevée.
452 R. J. JULIAN

Le SHP chez les poulets de chair est en général une primo-hypertension pulmonaire,
c'est-à-dire une HP qui se déclare sans que l'existence d'une maladie antérieure des poumons
ou du coeur n'ait été démontrée, qui pourrait expliquer l'augmentation du flux sanguin ou de
la résistance au flux provoquant une pression artérielle accrue dans les poumons. Les poumons
des volailles sont fixés dans la cavité thoracique et ne se dilatent pas pour amener de l'air dans
le poumon. Les capillaires aériens et sanguins forment un réseau rigide qui permet une
expansion minimale des capillaires sanguins quand un flux sanguin plus important est
nécessaire. L'air se déplace dans le poumon par un mouvement abdominal qui aspire et expire
l'air des sacs aériens. L'anatomie et la physiologie du système respiratoire de la volaille jouent
un rôle important en ce qui concerne la sensibilité des poulets de chair au SHP. Il est possible
que les facteurs suivants soient impliqués dans la recrudescence du SHP : petite stature du
poulet de chair moderne, bréchet lourd et grand, pression du contenu abdominal sur les sacs
aériens et petit volume pulmonaire comparé au poids du corps.

Chez la volaille, le flux sanguin a un espace limité dans le poumon. Les facteurs qui
augmentent le flux sanguin ou la résistance au flux s'ajoutent. La viscosité sanguine accrue
causée par la polyglobulie de l'hypoxie, ou une rigidité accrue des érythrocytes à teneur élevée
en Na + sont plus susceptibles de provoquer IH'P chez la volaille à croissance rapide que chez
la volaille à croissance lente. Un flux accru dû à une exposition au froid a également un effet
additif. Les ascites provoquées par l'HP sont une maladie liée à la production en basse altitude.
Cette maladie peut être évitée facilement en limitant le taux de croissance. Il est possible que
certains poulets de chair du phénotype que nous avons créé atteignent la limite du flux sanguin
de leurs poumons et que des améliorations futures du taux de croissance ne soient réalisables
que si la taille du poumon et de la cavité abdominale est augmentée.

ZUSAMMENFASSUNG
Ascites beim Geflügel
Forschungen über die Ascites, die bei Hühnern vom Masttyp vorkommt, die in mäßiger und
geringer Höhe aufgezogen werden, haben gezeigt, daß die Pathogenese ähnlich ist wie die der
Erkrankung in großer Höhe. Pulmonaler Hochdruck (PH), der durch erhöhte Blutzufuhr oder
erhöhten Widerstand gegen den Blutfluß in den Lungen verursacht wird, führt zur Hypertro-
phie der rechten Herzkammer (RVH), zu Herzklappeninsuffizienz, erhöhtem Venendruck und
Ascites. Der Aufbau des Vogelherzens mit seiner dünnwandigen rechten Kammer und musku-
lären Atrioventrikularklappe läßt es zu, daß PH schnell einen Herzschaden hervorruft. Die in
den 80er Jahren plötzlich vermehrte Häufigkeit des pulmonalen Hochdruck-Syndroms (PHS)
bei Masthühnern war mit einer rapiden Zunahme von Wachstumsgeschwindigkeit und Futter-
verwertung verbunden. Dies war die Folge einer Kombination von genetischer Selektion auf
schnellwüchsige, schwere Mastküken mit guter Futterverwertung und einem gehaltvolleren,
kalorienreichen, pelletierten Futter, das alle die für ein schnelles Wachstum benötigten
Nährstoffe lieferte und eine hohe Nahrungsaufnahme förderte.

Das PHS bei Hühnern vom Masttyp ist in der Regel primärer pulmonaler Hochdruck, d.h ein
PH, der ohne Anzeichen einer vorherigen Herz- oder Lungenerkrankung auftritt, welche die
Steigerung der Blutzufuhr oder den Widerstand gegen den Blutfluß erklären könnte, die zu
dem erhöhten Druck in den Lungenarterien führen. Die Lungen der Vögel sind starr und in
der Brusthöhle fixiert, und sie dehnen sich nicht aus, um Luft einzuziehen. Die Blut- und
Luftkapillaren bilden ein starres Geflecht, das nur eine geringfügige Erweiterung der Blutkap-
illaren gestattet, wenn ein erhöhter Blutfluß benötigt wird. Die Atemluft wird durch
Bauchbewegungen über die Lungen in die Luftsäcke und wieder heraus befördert. Die
Anatomie und Physiologie des aviaren Atmungssystems sind bei der Empfänglichkeit von
Masthühnern für das PHS bedeutsam. Die kleine Statur der modernen Masthühner, die große,
 ASCITES IN POULTRY 453

schwere Brustmasse, der Druck vom Inhalt der Leibeshöhle auf die Luftsäcke und das im
Vergleich zum Körpergewicht kleine Lungenvolumen, das alles könnte mit dem vermehrten
Vorkommen des PHS zu tun haben.

In der Vogellunge gibt es nur beschränkten Raum für den Blutfluß. Faktoren, die den Blutfluß
erhöhen oder den Widerstand gegen den Blutfluß steigern, sind additiv. Erhöhte Blutviskosität,
die durch die Polyzythämie bei Hypoxie verursacht wird, oder erhöhte Starrheit der Ery-
throzyten bei hohem Na + bewirken pulmonalen Hochdruck wahrscheinlich eher bei
schnellwachsenden als bei langsamwachsenden Vögeln. Gesteigerter Blutfluß infolge von Kälte
ist ebenfalls additiv. Durch PH verursachte Ascites ist in niedriger Höhe eine leistungsbezogene
Erkrankung. Sie kann durch Einschränkung der Wachstumsrate verhütet werden. Es ist
möglich, daß manche der Masthühner des von uns geschaffenen Genotyps die Grenze des
Blutflusses durch ihre Lungen erreicht haben, und daß zukünftige Verbesserungen bei der
Wachstumsrate nur möglich sein werden, wenn die Kapazitäten von Lunge und Leibeshöhle
vergrößert sind.

RESUMEN

Ascitis en las aves domésticas

Las investigaciones sobre la ascitis producida en gallinas de carne a altitudes bajas y moderadas
ha mostrado que su patogenia es similar en ambos casos a la del cuadro a altitudes elevadas.
La hipertensión pulmonar (PH), causada por un incremento del flujo sanguíneo o un
incremento de la resistencia al flujo snaguineo en los pulmones, resulta en una hipertrofia
ventricular derecha (RVH), insuficiencia valvular, incremento de la presión venosa y ascitis. La
estructura del corazón de las aves, con un ventrículo derecho con una pared delgade y una
valvula atrioventricular derecha muscular, da lugar a que la RH induzca un fallo cardiaco
rápidamente. El incremento súbito del síndrome de hipertensión pulmonar (PHS) en las aves
de came durante la década de los 80 estuvo asociado a un rápido incremento en el ritmo de
desarollo y de conversion del alimento. Todo ello fue el resultado de una combinación
de selección genética para un crecimiento rápido, broilers pesados con una conversión
baja de alimento y una comida granulada más densa y alta en calorias que aportaba
todos los nutrientes requeridos para un rápido crecimiento y favorecía una ingestion elevada de
nutrientes.

El PHS en las aves de carne es generalmente una hipertension pulmonar primaria, es decir, PH
que ocurre sin evidencia de una enfermedad pulmonar o cardíaca previa que pudiera justificar
el incremento del flujo sanguíneo o la resistencia al flujo que da lugar a un incremento en la
presión de las arterias pulmonares. Los pulmones de las aves son firmes y están fijados a la
cavidad torácica, no expandiendose para incorporar aire a los pulmones. Los capilares
sanguíneos y aéreos forman un entramado rígido que permite una expansión minima de los
capilares sanguineos cuando se requiere un mayor flujo sanguíneo. El aire se mueve a través
del pulmón por el movimiento del abdomen que introduce y expulsa el aire de las sacos aéreos.
Es importante conocer la anatomía y fisiología del sistema respiratorio aviar en la susceptibil-
idad de aves de carne al PHS. La estatura pequeña de las aves de carne actuales, la pechuga
grande y pesada, la presión de los contenidos abdominales sobre los sacos aéreos y el volumen
pulmonar pequeño comparado al peso corporal pueden estar involucrados en el incremento de
la incidencia de PHS.

Hay un espacio limitado para la circulacion sanguínea en el pulmón de las aves. Los factores
que incrementan el flujo sanguíneo o el incremento de la resistencia al flujo son aditivos.
Factores como el incremento de la viscosidad sanguinea producido por la policitemia de la
454 R. ]. JULIAN

hipoxia o el incremento de la rigidez del eritrocito por Na + elevado son mas propensos a
producir PH en aves de crecimiento rápido que en las de crecimiento lento. El incremento del
flujo sanguíneo debido a la exposición a ambientes fríos es también aditivo. La ascitis
producida por el PH es una enfermedad relacionada con la producción a baja altitud. Puede
ser evitada fácilmente restringiendo el ritmo de crecimiento. Es posible que algunas aves de
carne del fenotipo que hemos creado hayan alcanzado el limite de flujo sanguineo a través de
sus pulmones y que las mejoras futuras en el ritmo de crecimiento seran sólo posibles si las
capacidades pulmonares y abdominales se incrementan.