Rev. sci. tech. Off. int. Epiz.

, 2000,19 (2), 405-424

Fowl typhoid and pullorum disease

H I . Shivaprasad

California Animal Health and Food Safety Laboratory System, Fresno Branch, University of California, Davis,
2789 South Orange Avenue, Fresno, California 93725, United States of America

The terms describing serovars of Salmonella enterica subsp. enterica are presented as follows: Salmonella
Enteritidis, S. Gallinarum, S. Pullorum.

Summary
Fowl typhoid (FT) and pullorum disease (PD) are septicaemic diseases, primarily
of chickens and turkeys, caused by Gram negative bacteria, Salmonella
Gallinarum and S. Pullorum, respectively. Clinical signs in chicks and poults
include anorexia, diarrhoea, dehydration, w e a k n e s s and high mortality. In mature
f o w l , FT and PD are manifested by d e c r e a s e d egg p r o d u c t i o n , fertility, hatchability
and anorexia, and increased mortality. Gross and m i c r o s c o p i c lesions due t o FT
and PD in chicks and poults include hepatitis, splenitis, typhlitis, omphalitis,
myocarditis, ventriculitis, pneumonia, synovitis, peritonitis and ophthalmitis. In
mature f o w l , lesions include oophoritis, salpingitis, orchitis, peritonitis and
perihepatitis. Transovarian infection resulting in infection of t h e egg and
subsequently t h e chick or poult is one of t h e most important modes of
transmission of these t w o diseases. Salmonella Gallinarum and S. Pullorum c a n
be isolated by use of selective and non-selective media. Salmonella Pullorum
produces rapid decarboxylation of ornithine w h e r e a s 5. Gallinarum does not, an
important biochemical difference b e t w e e n t h e t w o bacteria. Both FT and PD c a n
be detected serologically by use of a m a c r o s c o p i c tube agglutination test, rapid
serum test, stained antigen w h o l e blood test or microagglutination test. Both
diseases c a n be controlled and eradicated by use of serological testing and
elimination of positive birds. Vaccines m a y be used to control t h e disease and
antibiotics f o r t h e t r e a t m e n t of FT and PD. A l t h o u g h FT and PD are w i d e l y
distributed t h r o u g h o u t t h e w o r l d , t h e diseases have been eradicated f r o m
c o m m e r c i a l poultry in developed countries such as t h e United States of A m e r i c a ,
Canada and most countries of W e s t e r n Europe. Both 5. Gallinarum and
S. Pullorum are highly adapted t o t h e host species, and therefore are of little
public health significance.

Keywords
Avian diseases - Clinical signs - Control - Diagnosis - Fowl typhoid - Pathology -
Pullorum disease - Salmonella Gallinarum - Salmonella Pullorum.

Introduction Fowl typhoid was first recognised in 1 8 8 8 by Klein (81) and

Fowl typhoid (FT) and pullorum disease (PD) are septicaemic
bacterial diseases of primarily chickens and turkeys, although
other birds, such as pheasants, quail, ducks, guinea-fowl and
peafowl, are also susceptible. Fowl typhoid is caused by the
bacterium Salmonella Gallinarum and PD is caused by
S. Pullorum. Salmonella Gallinarum and S. Pullorum are
highly host adapted and seldom cause significant problems in
hosts other than chickens, turkeys and pheasants.
PD in 1899 by Rettger (109). Pullorum disease was called
bacillary white diarrhoea before 1929. These two diseases
seriously threatened the poultry industry in the early 1900s
due to widespread outbreaks accompanied by high mortality.
However, FT and PD have been eradicated from commercial
poultry in the United States of America (USA) and the United
Kingdom, primarily due to pullorum-typhoid programmes,
namely: the National Poultry Improvement Plan (NPIP) and
the Poultry Health Scheme, respectively. However, F T and PD
406
are still common in many countries throughout the world.
Details of various aspects of FT and PD can be found in
reviews (29, 9 8 , 1 0 7 , 1 2 2 , 1 3 1 ) .
The diseases
Historically, FT was thought to be primarily a disease of
growing and adult chickens and turkeys, whereas PD was
primarily a disease of chicks and poults. In fact, both PD and
FT are important and significant diseases of chicks and poults
(64, 8 4 , 9 1 , 1 1 5 , 1 5 6 ) . However, growing and mature
chickens and turkeys are probably more susceptible to FT
than to PD.
Clinical signs
The clinical signs in chicks and poults due to FT and PD have
been described previously ( 1 8 , 1 9 , 4 6 , 4 7 , 7 6 , 9 2 , 1 1 6 , 1 5 6 ) .
These include moribund and dead birds in the incubator or
shortly after hatching if the chicks and poults are hatched
from infected eggs. The birds may manifest depression,
somnolence, anorexia, huddling together, droopy wings,
dehydration, laboured breathing, diarrhoea, ruffled feathers,
weakness and adherence of faeces to the vent. In some
situations, FT or PD may not be observed until five to ten days
after hatching. The highest mortality usually occurs in birds of
two to three weeks of age. Survivors may be greatly reduced in
weight and poorly feathered, and may not mature into well
developed laying or breeding birds. Flocks that have
experienced a severe outbreak will have a higher percentage of
carriers at maturity. Other signs, including blindness, swelling
of the tibiotarsal joint and the humeral, radial and ulnar
articulations may be observed.
In growing and mature fowl, clinical signs of FT and PD may
not be apparent in some cases. Non-specific clinical signs,
including a decline in feed consumption, a droopy
appearance, or ruffled feathers and pale and shrunken combs
may be observed. Other signs, including decreased egg
production, fertility and hatchability, may also be observed
depending upon the severity of infection. Death can occur
within four days of exposure but usually occurs after five to
ten days. An increase in body temperature may occur as a
result of PD and FT. Other prominent cfinical signs include
anorexia, diarrhoea, depression, dehydration and loss of
weight.
Morbidity and mortality
Both morbidity and mortality can be highly variable due to
various factors such as age of the bird, strain of the bird,
nutritional status of the bird, flock management and
concurrent infections. Mortality can range from 0% to 1 0 0 % ,
especially in chicks and poults (64, 156). The greatest
mortality is seen during the second week after hatching, with
a rapid decline between the third and fourth week of age.
Morbidity is generally higher than mortality. Birds hatched
from an infected flock that are raised on the same premises
Rev. sci. tech. Off. int. Epiz., 19 (21
exhibit lower morbidity and mortality than birds that are
stressed by shipping. Economic losses due to PD and F T can
be very high. This is manifested in the loss of birds, feed costs,
veterinary costs, disposal of dead birds, etc. Although the
exact figures are not available, the following is an example to
illustrate the economic loss. Despite the eradication of PD in
the USA, the effect of the disease was felt in 1 9 9 0 - 1 9 9 1 when
a series of outbreaks occurred in a completely integrated
broiler operation involving five States in the eastern USA ( 7 6 ,
116). The outbreaks eventually involved nineteen breeder
flocks and more than 2 6 0 grower facilities. The outbreak was
ultimately traced back to an infected grandparent male line
breeding flock (76). Although the exact costs are not available,
eradication of the grandparent line, parent flocks and growout
birds, and the replacement of these birds entailed significant
expense. Currently, the principal economic significance of F T
and PD in developed nations is the cost of surveillance
programmes.
Pathology
Studies on gross and microscopic lesions of FT and PD have
been sporadic. The earliest descriptions were made by Rettger
(110, 1 1 1 ) . Since then, isolated cases have been reported in
different species of birds involving various organs and at
various ages, primarily in chickens and turkeys but also a few
reports in pheasants, quail, ducks and guinea-fowl ( 1 6 , 19,
2 8 , 3 4 , 4 1 , 4 5 , 4 6 , 5 0 , 5 4 , 6 4 , 6 5 , 67, 6 8 , 8 3 , 9 1 , 9 2 , 104,
115, 116, 118, 1 2 1 , 1 2 4 , 1 3 0 , 1 3 6 , 157).
Gross lesions
In peracute cases of F T and PD, chicks may die in the early
stages of brooding without exhibiting any gross lesions. In
acute cases, enlarged and congested liver, spleen and kidneys
can be seen (Figs 1 and 2 ) . Livers may be enlarged and have
white foci of necrosis (Fig. 3 ) . Spleens may be enlarged and
mottled white (Figs 2 and 4). Contents of the yolk sac may be
coagulated, creamy or caseous. There may be fibrinous
exudate in the pericardium, capsule of the liver and the
peritoneum. In some birds, white nodules may be present in
the epicardium and myocardium resembling tumours similar
to those seen in Marek's disease (Figs 1, 5 and 6).
Occasionally, these nodules in the heart may become
sufficiently large to cause distortion in the shape of the heart
(Fig. 7). This may lead to chronic passive congestion of the
liver, resulting in ascites.
Similar small white nodules may be present in the pancreas,
lung, muscle of the gizzard (Fig. 8 ) , and occasionally in the
wall of the caecum. The caecum may contain caseous cores in
the lumen (Figs 2 and 9 ) . Some birds may exhibit swollen
joints (Fig. 10) containing creamy viscous fluid. Other
changes include exudate in the anterior chamber of the eye,
swollen foot pads or wing joints (46, 4 7 , 7 6 , 116, 156, 157).
Rev.sci.tech.0ff.intEpiz.,W{2)
407

Fig.3
Liver with numerous foci of necrosis and inflammation
from a chick affected by puliorum disease
Photo: courtesy Dr L Hanson, University of Illinois

Enlarged and congested liver with white nodules in the myocardium

of an eighteen-day-old chick affected by puliorum disease
With permission from the American Association of Avian Pathologists

Fig.4
Spleen with white mottling from a chick affected by puliorum disease
Photo: courtesy Dr R.P. Chin, University of California, Davis

Enlarged and congested spleen and liver with pale yellow cast Fig.5
m the lumen of caecum in a chick affected by puliorum disease Heart with small nodules in the myocardium of a twenty-one-day-old
With permission from the American Association of Avian Pathologists chick affected by puliorum disease
408 Hev. sci. teck Off. int. Epiz.. 19(2)

cm 1

Fig.6
Heart with prominent white nodules resembling tumours in the
myocardium of a five-week-old chick affected by pullorum disease
With permission from the American Association of Avian Pathologists
Fig.8
Gizzard with yellow nodules of various sizes in the muscular wall
extending from serosa of a six-week-old chick affected by pullorum
disease
With permission from the American Association of Avian Pathologists

Fig.9
Caecum with multiple yellow casts in the lumen of a chick affected by
pullorum disease
Photo: courtesy Dr HP. Chin, University of California, Davis

Fig.7
Misshapen heart due to multiple yeliow nodules in the myocardium
and chronic passive congestion of the liver in a six-week-old chick Fig. 10
affected by pullorum disease Severeiy enlarged tibiotarsal joints in the legs of a chicken affected
Note the thickened pericardium by pullorum disease
With permission from the American Association of Avian Pathologists Photo: courtesy Dr M. Peckham, Corneil University
Rev. sci. tech. Off. int. Epiz., 19 (2)
In adult chickens, lésions may be minimal although the birds
may be serologically positive or active reactors. Minimal
lésions, such as small nodular or regressing ovarian follicles
can be found in the ovaries of chickens. However, the lésions
most frequently found in chronic carrier hens include a few
misshapened and discoloured cystic ova among a few ovules
of normal appearance (Figs 11, 12 and 13). Thèse misshapen
ova may be deformed, nodular, and may be attached to the
ovary with a long pedunculated stalk which sometimes may
become detached from the ovarian mass. The oviduct often
contains caseous exudate in the lumen (Fig. 13). Ovary and
oviduct dysfunction may lead to abdominal ovulation or
oviduct impaction resulting in extensive peritonitis and
adhésions of the abdominal viscera. Fibrinous peritonitis and
perihepatitis, with or without the involvement of the
reproductive tract, may be seen (Fig. 14). Ascites may also
develop, especially in turkeys. Occasionally, the culture of
salmonella from such lésions is difficult.
Other lésions may include increased pericardial fluid or
fibrinous pericarditis, a mottled pancréas, and caseous
granulomas in the lungs and air sacs (45). In the maie, the
testes may hâve white foci or nodules (54, 83). Lésions in
turkeys are similar to chickens (67, 68), but ulcération may be
observed in the small intestine as well as in the caecum.
Although uncommon in chickens, this is a common finding in
turkeys.
Fig. 11
Ovary with multiple misshapen grey nodular follicles from an adult chicken affected by pullorum disease
409
In guinea-fowl, lésions due to FT involving the respiratory
tract are common. Lésions due to FT in ducklings and adult
ducks are similar to those in chickens. In bobwhite quail
{Colinus virginianus), enlarged spleens, grey necrotic foci in
lungs and pale or discoloured livers were observed in PD (28).
In young pheasants, yolk sac infection, pneumonia, hepatitis
and typhlocolitis were the most common lésions; the gizzard
was occasionally involved (104).
Histopathology or microscopic lésions
In peracute cases, the only significant lésions may be vascular
congestion in various organs, including the liver, spleen and
kidney. In acute to subacute cases, typical lésions are acute
necrosis of hepatocytes with fibrinous exudation and
infiltration of a mixed population of inflammatory cells
composed of heterophils, macrophages, lymphocytes and a
few plasma cells (42, 136; H.L. Shivaprasad, unpublished
findings). Occasionally, granuloma formations may be found
within the liver, characterised by necrosis and accumulation
of necrotic débris surrounded by multinucleated giant cells.
Fibrinous exudate may be présent on the capsule of the liver
mixed with heterophils and mononuclear inflammatory cells.
In chronic protracted cases, where white nodules appear in
the heart, chronic passive congestion may occur in the liver,
characterised by the degeneration of hepatocytes around the
central veins and interstitial fibrosis. In acute stages, the
spleen may hâve fibrinous exudation in the vascular sinuses
410 Rev. sci. tech. Off. int. Epiz., 19 (2)

a) in the exposed abdominal cavity

b) separated from the abdominal cavity Fig. 14
Yellow fibrinous exudate on the capsule of the liver and peritoneum of
Fig. 12
an adult chicken affected by pullorum disease
Ovary with numerous yellow nodular follicles from an adult chicken
with pullorum disease
and in later stages, multifocal infiltration of mononuclear
phagocyte system cells which gives the spleen a mottled white
appearance on gross examination. Caeca may contain necrotic
caseous debris within the lumen and necrosis of the mucosa
with infiltration of heterophils into the lamina propria. In later
stages, heterophils may be replaced by lymphocytes,
macrophages and plasma cells, which may extend into the
muscularis mucosa and muscular layers. Fibrinosuppurative
and pyogranulomatous inflammation associated with large
numbers of bacteria is a common finding in the yolk sac.

Fibrinosuppurative serositis is also a common finding

Fig. 13
Oviduct with distension due to exudate from an adult chicken affected
by pullorum disease
Note many misshapen nodular follicles in the ovary and exudate on the
serosa
With permission from the American Association of Avian Pathologists
characterised by exudate in the pericardium which extends
into the epicardium and myocardium, in the peritoneal lining,
on the serosa of the intestine, and on the pleura (136).
However, the most characteristic lesions may be found in the
heart and gizzard (H.L. Shivaprasad, unpublished findings).
These lesions are characterised by locally extensive foci of
myofibre necrosis with infiltration of heterophils mixed with
few lymphocytes and plasma cells (Figs 15 and 16). In later
stages, these cells may be replaced by large numbers of
fairly uniform mononuclear cells of the histiocytic type
with irregular vesicular nuclei and faintly staining
foamyeosinophilic cytoplasm. These cells may be arranged in
Rev. sci. tech. Off. int. Epiz., 19 (2) 411

solid sheets, forming nodules that often protrude from the

epicardial surface. Such nodules, both grossly and
microscopically, can be confused with certain tumours caused
by Marek's disease virus or possibly retroviruses. A
similar process can also be seen in the gizzard and
pancreas. Other microscopic lesions found in chicks
include fibrinoheterophilic panophthalmitis, pneumonia
characterised by infiltration of heterophils mixed with
macrophages and plasma cells in the interstitium, and
fibrinosuppurative inflammation of the synovium.

Microscopic lesions in adults include fibrinosuppurative to

pyogranulomatous inflammation of ovarian follicles
characterised by necrosis and fibrinosuppurative
inflammation mixed with bacteria within the ovules Fig. 15
Histopathology of heart with diffuse infiltration of lymphocytes and
to chronic pyogranulomatous inflammation (Fig. 17)
histiocytes, from a chick affected by pullorum disease
(H.L. Shivaprasad, unpublished findings). In males, necrosis
(bar = 5 µm)
of the epithelial cells lining the seminiferous tubules may be With permission from the American Association of Avian Pathologists
seen, followed by fibrinosuppurative inflammation. Other
changes include catarrhal bronchitis, enteritis, interstitial
pneumonia and nephritis.

Pathogenesis
Little is known regarding the pathogenesis of FT and PD,
probably due to the highly successful eradication
programmes. Various salmonellae, including S. Gallinarum
and S. Pullorum, were thought to survive and multiply in
various organs due to an unknown control mechanism
involving the reticuloendothelial system ( 1 5 ) . This
observation was confirmed when S. Gallinarum was found to
be taken up by murine phagocytic cells in an in vitro
experiment (103). Furthermore, S. Pullorum was shown to
preferentially target the bursa of Fabricius prior to eliciting
inflammation in the intestine of chicks (65). Infection with
Fig. 16
S. Gallinarum may also cause anaemia (39). The molecular Histopathology of gizzard with necrosis of muscle fibres and
factors of pathogenicity include plasmids responsible for infiltration of heterophils, lymphocytes and macrophages
virulence and virulence factors such as the virulence plasmid (bar = 5 µm)
gene, invasion gene and fimbrial gene ( 1 , 1 2 , 1 3 , 3 6 , 4 1 , 1 0 1 , With permission from the American Association of Avian Pathologists
114).

Incidence and distribution

Fowl typhoid and PD are widely distributed throughout the
world. However, the diseases have been eradicated from
commercial poultry in the USA and other developed countries
including Canada, Australia, Japan and most countries of
Western Europe. The last outbreak of PD in commercial
poultry in the USA occurred from 1 9 9 0 to 1 9 9 1 ( 7 6 ) .
Similarly, an outbreak of FT occurred in commercial poultry
in Denmark in 1 9 9 2 (38). Fowl typhoid and PD are still
common in many regions of the world, including Mexico,
Central and South America, Africa and the Indian Fig. 17
subcontinent (14, 2 1 , 2 6 , 3 5 , 7 1 , 7 2 , 7 5 , 8 7 , 9 0 , 9 2 , 9 7 , 1 1 8 , Histopathology of an ovarian follicle with pyogranulomatous
124, 125). However, the frequency of outbreaks in other inflammation
areas, such as Eastern Europe, Russia, the People's Republic of (x320)
412
China, South-East Asia and New Zealand is unknown. Fowl
typhoid has not been reported in the USA since 1980
(4,105).
Aetiology
Salmonella Gallinarum and S. Pullorum are both members of
the family Enterobacteriaceae and are highly adapted to the
host. The bacteria belong to serogroup D according to the
Kauffmann-White scheme. The majority of strains of
S. Gallinarum and S. Pullorum are very similar at a
chromosomal level (99). Furthermore, S. Enteritidis, another
member of serogroup Group D, is thought to be closely
related to S. Gallinarum and S. Pullorum, based on multilocus
enzyme electrophoresis (132). According to one study, the
most recent common ancestor of S. Gallinarum and
S. Pullorum was non-motile (85). Since diverging from this
ancestor, the S. Pullorum lineage appears to have evolved
more rapidly than the S. Gallinarum lineage (85).
The organisms are Gram negative, non-sporogenic,
non-motile and facultatively anaerobic. The bacteria are
slender rods measuring approximately 1.0 pm-2.5 µm in
length and 0.3 pm-1.5 µm in width. Both S. Gallinarum and
S. Pullorum are considered to be non-motile. However,
motility and flagellation have recently been induced in
S. Pullorum grown on solid media ( 3 3 , 5 9 , 70). Other
workers were unable to induce motility in S. Pullorum when
grown on Hektoen agar (32).
Both S. Gallinarum and S. Pullorum grow readily on beef agar
or broth or other nutrient media. The bacteria are aerobic or
facultatively anaerobic and grow best at 37°C. The organisms
will grow in selective enrichment media including selenite F
and tetrathionate broths, and on differential plating media
including MacConkey, bismuth sulphite and brilliant green
(BG) agars. Salmonella Pullorum may occasionally fail to grow
on certain selective media such as BG or Salmonella shigella
agar, but grow satisfactorily on bismuth sulphite and
MacConkey agars (31).
Colonies of S. Gallinarum and S. Pullorum appear as small,
discrete, smooth, blue-grey or greyish-white, glistening
colonies that are homogenous and entire on meat extract or
meat infusion agar (pH 7.0-pH 7.2). Most of the colonies
remain small (1 mm or less), but isolated colonies may have a
diameter of 3 mm to 4 mm or more. Occasionally,
morphologically abnormal strains can be encountered.
Inoculation of gelatin slants yields greyish-white surface
growth with filiform growth in the stab and no liquefaction.
Growth in broth is turbid with a heavy flocculent sediment.
Both organisms can ferment arabinose, dextrose, galactose,
mannitol, mannose, rhamnose and xylose to produce acid
with or without gas production (23, 3 6 , 1 4 0 ) . Substances not
fermented include lactose, sucrose and salicin. One important
biochemical difference between the two organisms is that
S. Gallinarum ferments dulcitol whereas S. Pullorum does
Rev. sci tech. Off. int. Epiz., 19 (2)
not. In addition, S. Pullorum only occasionally ferments
maltose. However, the major difference is that S. Pullorum
produces rapid decarboxylation of ornithine, whereas
S. Gallinarum does not. In addition, S. Gallinarum uses
citrate, D - sorbitol, L - fucose, D - tartrate and cysteine
hydrochloride gelatin (38). Some of these differences may be
helpful in differentiating between the two organisms.
However, variation in the characteristics of some strains can
occasionally be observed, especially in regard to gas
production.
Other techniques, including ribotyping and polymerase chain
reaction, have been important tools to identify S. Gallinarum
and S. Pullorum (37, 74, 143). These bacteria can be further
typed for epidemiological studies by various techniques such
as random amplification of polymorphic deoxyribonucleic
acid (RAPD), plasmid profiling, phage typing and cloning of
chromosomal fragments (3, 3 6 , 37, 4 1 , 7 8 , 7 9 , 1 4 1 , 142,
155).
Antigenic variation
Both S. Gallinarum and S. Pullorum possess the O antigens 1,
9 and 12. Variation involving antigen 12 occurs in
S. Pullorum, but no evidence exists for such variation in
S. Gallinarum ( 4 3 , 4 4 , 149). The antigenic composition of
S. Pullorum was shown to be 1 , 9 , 1 2 1 , 1 2 , 1 2 ; the variation
2 3
involved minor somatic antigens 1 2 and 1 2 . Standard
2 3
strains of S. Pullorum contain a large amount of 1 2 and a 3
very small amount of 1 2 , but in variant strains the content of
2
the two antigens is reversed. Intermediate strains are usually
mixtures of 1 2 and 1 2 predominant colonies. However,
2 3
DNA fingerprint analysis of these strains has raised some
questions regarding such variation in the major somatic
antigen 12 (155). Strains may also vary in content of the O-l
antigen. Tests to differentiate standard, intermediate and
variant types of S. Pullorum have been described (147, 1 4 8 ,
150).
Like most pathogenic microorganisms, S. Gallinarum and
probably S. Pullorum may lose virulence rapidly in artificial
media; hence, cultures should be passaged serially in the
natural host (the chicken) before testing the pathogenicity of
the organisms. Pathogenicity of such cultures is best
maintained in the lyophilised or frozen state. This may explain
why various investigators have found variation in virulence
among cultures of S. Gallinarum.
Epidemiology
Natural hosts
Chickens are the natural hosts for both S. Gallinarum and
S. Pullorum. However, natural outbreaks of FT and PD have
been described in turkeys, guinea-fowl, quail, pheasants,
sparrows and parrots (107, 122, 131). In addition, outbreaks
of FT have been described in ring-necked doves, ostriches and
Rev. sci. tech. Off. int. Epiz., 19 (2)
peafowl, and cases of PD in canaries and bullfinches. The
susceptibility of ducks, geese and pigeons to S. Gallinarum
varies, but all of these birds generally appear to be resistant.
Significant differences also exist in susceptibility to PD among
breeds of chicken ( 3 0 , 120). White Leghorns appear to be
more resistant than heavy breeds such as Rhode Island Red,
New Hampshire, or crosses between the two (73). Differences
in resistance of S. Gallinarum and S. Pullorum have also been
shown in inbred lines of chickens (30). A greater percentage
of females appear to remain as reactors, probably due to the
sequestered nature of localised infection of the ovarian
follicles.
Pullorum disease has been described as a naturally occurring
or experimental infection in mammals such as chimpanzees,
rabbits, guinea-pigs, chinchillas, pigs, kittens, foxes, dogs,
swine, mink, cows and wild rats. Salmonella Gallinarum
could be cultured for up to 121 days from the faeces of
experimentally infected rats (9).
Transmission
Fowl typhoid and PD can be transmitted by a variety of means
( 1 6 , 1 7 , 5 5 ) . The infected bird, such as a carrier or a reactor, is
by far the most important means of perpetuation and spread
of the bacteria. Birds may not only infect their own
generation, but also succeeding generations, through egg
transmission. Egg transmission may result
contamination of the ovum following ovulation or localisation
of the bacteria in the ova before ovulation (16, 17). Other
modes of transmission include shell penetration, feed
contamination, contact transmission either in the hatcher,
brooder, cages or floor, cannibalism of infected birds, egg
eating, and through wounds on the skin ( 6 9 , 146, 151).
Faeces from infected birds are an important source of
contamination of other birds. Contaminated feed, water and
litter can also be sources of S. Gallinarum and S. Pullorum.
Attendants, feed dealers, bird buyers and visitors who move
between farms and between bird houses may spread disease
unless precautions are taken to disinfect footwear, hands and
clothing. Similarly, trucks, crates and feed sacks may also be
contaminated and can be the source of infection of birds.
Wild birds, mammals, flies and insects may be important in
mechanical spread of the organism.
Both S. Gallinarum and S. Pullorum may survive for several
years in a favourable environment, but are less resistant than
paratyphoid salmonellae to heat, chemicals and adverse
environmental factors ( 1 0 7 , 1 3 1 ) . For example, S. Gallinarum
was killed within 10 min at 60°C, within a few minutes by
direct exposure to sunlight, within 3 min by 1:1,000 phenol,
1:20,000 dichloride of mercury or 1% potassium
permanganate, and in 1 min by 2 % formalin (107). Agar
cultures may rapidly lose pathogenic character. Salmonella
Gallinarum was found to retain viability for up to forty-three
days, subject to daily freezing and thawing (100). Organisms
survived more than 148 days at - 2 0 ° C , even though they
were accidentally thawed twice. Salmonella Gallinarum can
413
survive in the faeces from infected chickens for up to 10.9
days when kept in a range house, and for two days less in the
open (128). Compounds containing phenol were the most
effective disinfectants for control of S. Gallinarum in the field,
followed by quaternary ammonium compounds and
iodophores (20).
Diagnosis
A definitive diagnosis of F T and PD requires the isolation and
identification of S. Gallinarum and S. Pullorum, respectively.
However, a tentative diagnosis can be made, based on the
flock history, clinical signs, mortality and lesions. Positive
serological findings can also be of great value in detecting
infection; however, negative results should not be considered
adequate for a definitive diagnosis, because of the delay of
three to ten or more days in appearance of agglutinating
antibodies following infection. In addition, cross-reactions
with other salmonellae, such as S. Enteritidis, should be
considered when interpreting serological results (52, 1 2 3 ,
145). A brief overview of diagnostic techniques will be given
here. More detailed information is provided elsewhere (98).
from
Isolation of Salmonella Gallinarum and
Salmonella Pullorum
Since F T and PD are systemic diseases, especially in young
chicks and poults, these bacteria can be isolated from most
body tissues. The liver, spleen, yolk sac and caeca are most
commonly involved in F T and PD, and are the preferred
organs for culture. Lesions may also occur in the heart,
gizzard, pancreas and lungs, which are also suitable
specimens for isolation. If lesions are present in the
reproductive organs of mature birds, the ovarian follicles,
oviduct and testes can be cultured. Other sites, such as
peritoneum, synovium and the interior of the eye can also be
cultured. Beef extract or infusion broth or tryptose agar in
tubes or Petri dishes are all satisfactory for primary isolation.
Enrichment broths or selective media may also be used if
tissues are decomposed.
Birds with chronic FT or PD that are detected by serological
tests may or may not have gross lesions. In such instances,
thorough culturing of the internal organs is necessary. A
detailed outline for examination of such specimens can be
found in the NPIP manual used in the USA (7). This
procedure may be summarised briefly as follows: grossly,
normal or diseased internal organs including heart, liver, gall
bladder, spleen, kidney, pancreas, testes/ovary and oviduct
should be cultured directly on veal infusion (VI) and BG agar
plates and incubated for 4 8 h at 37°C. In addition, portions of
internal organs should be pooled, ground, or blended in ten
times their volume of VI broth; 10 ml aliquots of the
suspension are transferred to 100 ml of both VI and
tetrathionate BG (TBG) broth and incubated for 2 4 h at 37°C.
414 Rev. sci tech. Off. int. Epiz., 19 (2)

The broths are then plated on VI and BG agar, incubated and- Table I
examined after 2 4 h and 4 8 h. If contamination with proteus Biochemical reactions used to differentiate between Salmonella
or pseudomonas is a problem, BG sulphapyridine agar plates Gallinarum and Salmonella Pullorum
can be used.
Reactant or
Salmonella Gallinarum Salmonella Pullorum
property
The digestive tract should be cultured using individual cotton
swabs for the upper, middle and lower intestinal tract, Dextrose Fermented with no gas Fermented with gas
including both the caecum and the rectum/cloacal area. The Lactose Not fermented Not fermented
swab should be deposited in 10 ml TBG broth, incubated and Sucrose Not fermented Not fermented
plated as previously described for the internal organs. In Mannitol Fermented with no gas Fermented with gas
addition, portions of the gut should be pooled, ground, or Maltose Fermented with no gas Usually not fermented
blended, in ten times their volume of TBG broth. A quantity of Dulcltol Fermented with no gas Not fermented
the suspension from the digestive tract (10 ml) is transferred Ornithine Not fermented Fermented
to 100 ml of TBG broth and incubated at 42°C or 37°C for Indole Not produced Not produced
Urea Not hydrolysed Not hydrolysed
2 4 h. The higher incubation temperatures for TBG broth
Motility Non-motile Non-motile
reduce populations of competitive contaminants common in
Agglutination Positive with group D Positive with group D
gut tissue.

Suspect colonies are transferred to triple sugar-iron (TSI) agar

and lysine-iron (LI) agar and incubated at 37°C for 2 4 h.
Cultures revealing typical reactions of salmonellae or arizonae
on TSI or LI agar slants should be identified by appropriate
biochemical or other tests. All salmonella cultures should be
serologically typed. Use of nonselective media demands
careful aseptic techniques but has the advantage of greater
dependability in securing isolation of S. Gallinarum and
S. Pullorum. Also, other bacteria capable of producing
cross-reactions with pullorum typhoid antigen may be more
dependably demonstrated. Polymerase chain reaction has also
been used to detect isolates of S. Gallinarum (143).
Serology
Various serological tests have been used to detect F T and PD.
These include the macroscopic tube agglutination (TA) test,
rapid serum (RS) test, stained antigen whole blood (WB) test,
and microagglutination (MA) test using tetrazolium-stained
antigens ( 5 1 , 7 7 , 1 1 3 , 1 1 9 , 1 3 9 , 1 5 2 ) . In some countries,
such as the USA, the standard procedure for detecting
breeding flocks chronically infected with S. Gallinarum and
S. Pullorum is to use the standard strains of S. Pullorum (1, 9,
1 2 ) for tube and serum plate antigens and both standard
3

Identification of cultures ( l , 9 , 1 2 ) and variant ( 1 , 9 , 1 2 ) strains of S. Pullorum for the

3 2

Colonies of S. Gallinarum may appear smooth, blue-grey, polyvalent rapid W B plate antigens. These antigens will detect
moist, circular and entire after 2 4 h of incubation. Colonies of flocks infected with either S. Gallinarum or S. Pullorum.
S. Pullorum are small, smooth and translucent on nutrient However, these antigens will cross react with the sera from
media. Careful initial culture of tissues on nonselective media birds infected with other salmonellae, most notably
should usually result in pure cultures. If pure cultures are not S. Enteritidis ( 5 1 , 123, 1 4 5 ) . In Japan, the antigen used for
obtained, or if an enriched medium has been used, transfer of the W B test is prepared from cultures grown in a
individual colonies to TSI agar slants for preliminary continuous-flow, broth-culture system in which it is
differentiation is often advantageous. Salmonella Gallinarum necessary to mix sublots to secure desired agglutination (138).
and S. Pullorum produce a red slant with a yellow butt that
shows delayed blackening from H S production. Reactions
2
Enzyme-linked immunosorbent assays (ELISA) for detecting
listed in Table I, which can be determined within 2 4 h, S. Gallinarum and S. Pullorum antibodies have been
provide identification of a number of other common developed by using lipopolysaccharides from these
salmonellae as antigens ( 1 4 , 9 3 , 9 4 ) . This technique can be
pathogens and allow differentiation between the two
used for screening large numbers of blood samples. As with
organisms.
other techniques, the ELISA may show positive reactions to
other salmonellae, especially those belonging to group D.
Additional differentiation tests described in the section Salmonella Pullorum can be detected serologically using
entitled Aetiology' may be necessary to identify isolates that S. Enteritidis flagella as an antigen in an ELISA (53). Recently,
produce atypical reactions (chiefly fermentation of maltose or a dot immunobinding assay (DIA) was compared with a
no gas production). Decarboxylation of ornithine by serum TA test for detecting serological responses in
S. Pullorum is the single most dependable test for vaccinated and unvaccinated chickens following a challenge
differentiating maltose-fermenting S. Pullorum strains from with virulence plasmid-cured S. Gallinarum ( 8 9 ) . The DIA
S. Gallinarum. was found to be very sensitive and detected antibodies to high
Rev. sci. tech. Off. int. Epiz., 19 (2)
titres in birds challenged with S. Gallinarum. This assay also
detected in high titres antibodies to S. Gallinarum in
vaccinated and unchallenged birds which failed to react by TA
(89).
Public health implications
Since S. Gallinarum and S. Pullorum are highly adapted to the
host, the diseases are of little public health significance.
Occasional PD in humans has been reported following
ingestion of contaminated food containing massive numbers
of S. Pullorum ( 9 5 , 108). The symptoms are characterised by
a rapid onset of acute enteritis followed by prompt recovery
without treatment. Experimental reproduction of
salmonellosis using four strains of S. Pullorum in humans and
large numbers (billions) of bacteria produced only transient
illness followed by prompt recovery (88). Salmonella
Gallinarum is rarely isolated from humans and is of little
public health significance. According to a report of the
Centers for Disease Control and Prevention, Atlanta, USA,
eight S. Gallinarum isolates and eighteen S. Pullorum isolates
have been detected out of a total of 4 5 8 , 0 8 1 salmonella
isolates from humans between 1982 and 1992 (5). The
presence or absence of symptoms in the individuals from
which the salmonellae were isolated was not recorded.
Prevention and methods of
control
Fowl typhoid and PD are excellent examples of diseases that
have decreased in prevalence in some of the advanced
countries or have been eradicated by application of basic
management procedures or eradication programmes. One of
the basic requirements is to establish breeding flocks free of
S. Gallinarum and S. Pullorum, and to hatch and rear progeny
under conditions that will preclude direct or indirect contact
with infected chickens or turkeys. Since egg transmission
plays an important role in the spread of these two diseases,
only eggs from flocks known to be free of FT and PD should
be introduced into hatcheries. Chickens and turkeys are the
primary hosts of S. Gallinarum and S. Pullorum, and free
flying birds and other fowl are not principal reservoirs of
infection. Thus, eradication of these diseases from chicken
and turkey breeding flocks is a fundamental step towards
eradication of FT and PD in commercial poultry flocks.
Management practices
Management practices broadly designed to prevent the
introduction of infectious agents should be applied to prevent
introduction of F T or PD. Carriers must be eliminated on a
415
regular basis. Some of the specific practices include the
following:
a) chicks and poults should be obtained from sources free of
FT and PD
b) typhoid-free and pullorum-free stock should not be mixed
with other poultry or confined with birds not known to be
free of F T and PD
c) chicks and poults should be placed in an environment that
can be cleaned and sanitised to eliminate any residual
salmonellae from previous flocks
d) in order to minimise the introduction of S. Gallinarum and
S. Pullorum through feed ingredients, chicks and poults
should receive pelletised, crumbled feed. Feed ingredients
must be free of salmonella
e) a sound biosecurity programme must be in place so that
the introduction of salmonellae from outside sources is
minimised.
Houses should be designed to exclude rodents and free-flying
birds. Insect control, the use of clean or chlorinated water,
and the use of thoroughly disinfected footwear and clothing
are essential for biosecurity. Measures must be implemented
to prevent exposure of birds to contaminated poultry
equipment, handling crates and trucks. Dead birds should be
disposed of properly.
Elimination of carriers
One of the most important methods of controlling FT and PD
is by serological monitoring of flocks (see the section entitled
'Serology'). Tube agglutination, RS, W B and MA tests are all
effective in detecting carriers, but the MA test offers an
economic advantage. In the USA, the W B test is not accepted
for testing turkeys as the test was determined to be unreliable.
Testing of birds by several methods at three to five week
intervals is essential to detect reactors which then can be
removed. A single test may miss reactors for several reasons,
as follows:
a) serum agglutinin titres in infected birds may be too low to
produce significant agglutination at the usual dilutions of 1:25
or 1:50
b) a delay of at least several days occurs between infection
and the development of agglutinins
c) following the removal of the reactors, environmental
contamination may serve as a source of infection for other
birds at a later date.
In the USA, testing for NPIP (7) accreditation is allowed after
chickens and turkeys reach approximately sixteen weeks of
age.
An ELISA test which can be economical for screening large
numbers of flocks and birds is also available for screening of
flocks for F T and PD (14, 9 3 , 9 4 ) .

416
Infection must also be confirmed by careful bacteriological
examination of one or more serological reactors. The antigen
which is used for detecting S. Gallinarum and S. Pullorum is
known to cross-react with other bacteria, resulting in false
positives ( 5 1 , 1 2 3 , 145). These bacteria could be other types
of salmonella such as S. Enteritidis or S. enterica subsp.
arizonae, or other bacteria such as Staphylococcus epidermidis,
Escherichia coli, and others (49, 145). Non-Gallinarum and
non-Pullorum reactors may range from a few birds in a flock
to as many as 3 0 % to 4 0 % . Thorough bacteriological
examination of representative reactors is often the only
dependable method for determining the infection status of a
flock. This is also probably the only method of distinguishing
between infections by S. Gallinarum and S. Pullorum.
If an attempt is made to free a flock of infection, retesting of
the infected flock should be performed at two to four week
intervals until two consecutive negative tests of the entire
flock are secured at an interval of twenty-one days or more. In
the majority of cases, infection can be eliminated from the
flock through testing at short intervals and removal of infected
birds. Two or three retests are often sufficient to detect all
infected birds. However, infection occasionally continues to
spread within a flock, and the disease cannot be eliminated by
repeated testing and removal.
Criteria of eradication
The essentials of an eradication programme for an area or a
country may include the following:
a) fowl typhoid and PD must be reportable diseases
b) infected flocks must be placed under quarantine and
infected flocks marketed under supervision
c) all reports of FT and PD must be investigated by an
authorised state or federal agency or other officials
d) importation regulations must require shipments of poultry
and hatching eggs to be from sources considered free of F T
and PD
e) regulations must require poultry at public exhibitions to be
from flocks free of FT and PD
f) total participation must be required of poultry breeding
flocks and hatcheries in a typhoid pullorum control
programme, such as NPIP in the USA or an equivalent in
other countries.
Although advanced countries have limited the presence and
spread of FT and PD in commercial flocks, these diseases are
still present in small backyard flocks (6, 4 5 , 1 0 4 , 139, 144;
H.L. Shivaprasad, unpublished findings). However, the usual
separation of commercial and non-commercial poultry has
been effective in preventing transmission of S. Gallinarum and
S. Pullorum between these populations. The infected
backyard flocks still continue to pose a threat to commercial
flocks. Therefore, continued testing of commercial breeding
Rev. sci. tech. Off. int. Epiz., 19 (2)
flocks is necessary to rapidly detect any spread of F T and PD
from non-commercial poultry.
Treatment
Every effort should be made to eradicate FT and PD, and
treatment should be the last option. Various sulphonamides,
followed by nitrofurans and several other antibiotics have
been found to be effective in reducing mortality from F T and
PD. However, no drug or combination of drugs have been
found to be capable of eliminating infection from treated
flocks. Sulphonamides that have been used in treatment of FT
and PD include sulphadiazine, sulphamerazine,
sulphathiaole, sulphamethazine and sulphaquinoxaline
( 2 , 2 4 , 9 6 ) . However, most studies have indicated that despite
treatment, a significant number of infected birds can remain
among the survivors and become carriers (24, 1 0 6 , 112).
Various other antibiotics can be used for controlling and
treating FT and PD, including furaltodone, furazolidone,
chloramphenicol, biomycin, apramycin, gentamicin and
chlorotetracycline (8, 2 2 , 2 7 , 4 8 , 5 6 , 57, 107, 127, 1 3 5 , 137,
153, 154). Resistance to some of these antibiotics has been
reported (63, 8 0 , 1 1 7 , 1 2 9 , 1 3 3 , 1 3 4 ) .
Care must be taken to follow the directions given by the
manufacturer in regard to the route of administration, dosage,
duration of treatment, and the withdrawal period for each
antibiotic before use. Some details regarding these aspects
have been described in reviews ( 1 0 7 , 1 2 3 , 1 3 1 ) . Furazolidone
treatment may interfere with antibody production and should
be avoided six weeks prior to testing ( 6 6 ) . A choice of
antibiotics available for use varies by country.
Vaccination
A number of investigators have evaluated killed and modified
live bacterins for FT. Studies on the use of 9R strain as live oral
or injectable vaccine with or without oil adjuvants have
reported variable results ( 6 0 , 6 1 , 6 2 , 102, 126). Similarly,
outer membrane proteins from S. Gallinarum have been
reported to offer better protection than the 9R live vaccine in
terms of clearance of the pathogenic strain from internal
organs ( 2 5 , 2 7 ) . More recently, immunisation against F T by
the use of mutant strains of S. Gallinarum and the
virulence-plasmid-cured derivative of S. Gallinarum appear to
be promising in protecting birds challenged with
S. Gallinarum ( 1 0 , 1 1 , 5 8 , 158). Since F T and PD have been
eradicated from commercial flocks in many developed
countries, the incentive for the production of vaccines is
small.
Though not a vaccine, the administration to young broiler
chickens of S. Enteritidis-induced immune lymphokines
significantly reduced the horizontal transmission of
Rev. sci. tech. Off. int. Epiz., 19 (2) 417

S. Gallinarum (82, 8 6 ) . Competitive exclusion has also been

attempted to control FT, using S. Enteritidis or S. Gallinarum
Acknowledgements
(40). The author wishes to thank Dr R.P. Chin and
Dr M. McFarland for reviewing the manuscript and
International trade implications Dr R. Crespo and Mrs H. Moriyama for technical assistance.
Export of poultry and poultry products should be made only
from flocks known to be serologically negative for F T and PD.

Typhose et pullorose aviaires

H i . Shivaprasad

Résumé
La typhose et la pullorose aviaires sont des maladies septicémiques t o u c h a n t
essentiellement les poules et les dindes et dues à des bactéries ne prenant pas la
coloration de Gram, Salmonella Gallinarum et S. Pullorum, respectivement. Les
signes cliniques chez les poussins et les dindonneaux sont, entre autres,
l'inappétence, la diarrhée, la déshydratation et l ' a n é m i e ; ils s ' a c c o m p a g n e n t
d'une forte mortalité. Chez les poules adultes, la typhose et la pullorose se
manifestent par une chute de ponte, une baisse de la fertilité et un trouble de
l'éclosion, ainsi que par de l'anorexie et une mortalité a c c r u e . Les lésions
m a c r o s c o p i q u e s et m i c r o s c o p i q u e s observées chez les poussins et les
dindonneaux atteints de typhose et de pullorose comprennent, notamment, une
hépatite, une splenite, une typhlite, une omphalite, une myocardite, une
ventriculite, une pneumonie, une synovite, une péritonite et une ophtalmie. Chez
les volailles adultes, on observe des lésions telles que des ovarites, des
salpingites, des orchites, des péritonites et des péri-hépatites.
L'infectiontransovarienne, qui se t r a d u i t par la contamination de l'œuf et donc du
poussin ou du d i n d o n n e a u , est l'un des principaux modes de transmission de ces
deux maladies. On peut isoler S. Gallinarum et S. Pullorum par des moyens
sélectifs ou non sélectifs. Salmonella Pullorum produit une décarboxylation
rapide de l'ornithine, contrairement à 5. Gallinarum ; c'est une différence
biochimique importante entre les deux bactéries. Des tests sérologiques
permettent de déceler la typhose et la pullorose, n o t a m m e n t la réaction de
macroagglutination en t u b e , l'agglutination rapide, le test de coloration de
l'antigène en sang entier ou la micro-agglutination. Les examens sérologiques et
l'élimination des volailles ayant réagi positivement permettent de prévenir et
d'éradiquer c e s deux maladies. Les v a c c i n s sont indiqués pour lutter contre la
t y p h o s e et la pullorose et les antibiotiques pour traiter c e s deux maladies.
Largement répandues dans le monde, la typhose et la pullorose ont, cependant,
été éradiquées des élevages avicoles c o m m e r c i a u x dans des pays développés
c o m m e les États-Unis d'Amérique, le Canada et la plupart des pays d'Europe
occidentale. Salmonella Gallinarum et S. Pullorum sont étroitement adaptées à
leurs hôtes et n'ont pas d'incidence significative en santé publique.

Mots-clés
Anatomo-pathologie - Diagnostic - Maladies aviaires - Prophylaxie - Pullorose -
Salmonella Gallinarum - Salmonella Pullorum - Signes cliniques - Typhose aviaire.
418 Rev. sci. tech. Off. int. Epiz., 19 (2)

Tifosis aviar y pulorosis

H.L. Shivaprasad

Resumen
La tifosis y la pulorosis son enfermedades septicémicas causadas por sendas
bacterias gramnegativas (Salmonella Gallinarum y S. Pullorum, respectivamente)
que afectan sobre todo a pollos y pavos. Entre los signos clínicos de esas
infecciones en pollitos y pavipollos cabe citar anorexia, diarrea, deshidratación,
decaimiento y elevada mortalidad. En aves maduras las principales
manifestaciones clínicas son, además de la anorexia y el aumento de la
mortalidad, la pérdida de fertilidad y el descenso de las tasas de producción
huevera y de eclosión. Las lesiones macro y microscópicas que ambas
enfermedades provocan en pollitos y pavipollos son: hepatitis, esplenitis, tiflitis,
onfalitis, miocarditis, ventriculitis, neumonía, sinovitis, peritonitis y oftalmitis. Las
aves maduras, por su parte, pueden presentar ooforitis, salpingitis, orquitis,
peritonitis y perihepatitis. La infección transovárica, que provoca la infección de
los huevos y después de los polluelos, es uno de los principales mecanismos de
transmisión de estas dos enfermedades. Para aislar S. Gallinarum y S. Pullorum
en cultivo pueden utilizarse medios selectivos o no selectivos. Entre S. Pullorum y
S. Gallinarum hay una importante diferencia bioquímica: la primera induce una
rápida descarboxilación de la ornitina y la segunda no. Tanto la tifosis aviar como
la pulorosis pueden detectarse por medios serológicos, utilizando pruebas de
macroaglutinación en tubo, de aglutinación rápida, de tinción antigénica en
muestras de sangre entera o de microaglutinación. Aplicando pruebas
serológicas y sacrificando después a los ejemplares positivos es posible luchar
contra ambas enfermedades hasta llegar a erradicarlas. También pueden
utilizarse vacunas para controlar la propagación de ambas infecciones, y
antibióticos para tratarlas. Pese a la amplia distribución (a escala mundial) de la
tifosis aviar y la pulorosis, países industrializados como los Estados Unidos de
América, Canadá y muchos países de Europa Occidental han conseguido
erradicarlas en las poblaciones de granjas avícolas. Tanto S. Gallinarum como
S. Pullorum están muy adaptadas a sus especies huéspedes, por lo que revisten"
escasa importancia en términos de salud pública.
Palabras clave
Anatomopatología - Control - Diagnóstico - Enfermedades aviares - Pulorosis -
Salmonella Gallinarum - Salmonella Pullorum - Signos clínicos - Tifosis aviar.

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