38 EQUINE VETERINARY JOURNAL

Equine w t . J. (1978), 10 ( l ) , 38-42

Chlamydia psittaci Infection of Horses

with Respiratory Disease
A. R. S. MOORTHY and P. B. SPRADBROW
Department o f Veterinary Pathology and Public Health, Veterinary School, University of Queensland, Brisbane,
Australia

SUMMARY
Two strains of Chlamydia psittaci were isolated from the nasal tract of horses with acute respir-
atory disease. These 2 isolates (NS 121 and NS 172) were characterized as chlamydia on the
basis of their morphology, rinctorial property, growth in chicken embryos, inability to grow on
bacterial media and their possession of chlamydia1 common complement fixing group antigen.
They were identified as C. psiltaci on the basis of resistance to sodium sulphadiazine. The present
strains were not pathogenic to mice and guinea pigs and non-toxigenic. They induced antibodies
and caused latent infection in mice and guinea pigs.
Acute and convalescent sera were available from one of the horses and rising levels of specific
antibody were demonstrated. No chlamydia were isolated from the materials of 14 aborted foals,
4 synovial fluids from horses with acute polyarthritis and nasal, tracheal and lung material from
another 276 horses.

INTRODUCTION The clinical signs shown by 2 horses that yielded

CHLAMYDIAL organisms have been incriminated as
aetiological agents in a number of diseases which include
pneumonia, abortion, polyarthritis, encephalomyelitis,
keratoconjunctivitis and genital infections of man and
domestic animals. There are reports of the isolation of
chlamydia from horses with various disease conditions;
from blood samples of foals with bronchopneumonia
(Popovici and Hiastru, 1968 and 1969), from fatal cases
of pneumonia, hepatitis, encephalitis and nephritis
( Blanco-Loizelier and Page, 1974), from keratocon-
junctivitis (Erasmus, 1973), from aborted foals (Popovici
and Hiastru, 1969, and Bosman, et a/., 1973), and from
a polyarthritic foal (McChesney, Bercerra and England,
1974). The present paper describes the isolation,
characterization and identification of two strains of
Chlamydia pstittaci from 2 horses with acute upper
respiratory tract disease in Queensland, Australia.
MATERIALS AND METHODS
Samples. The present study was part of a larger
investigation which involved the examination of samples
from the upper respiratory tract of 278 horses with a
variety of infectious agents. Nasal swabs were taken
from 158 live horses, including 63 from clinically normal
horses, 90 from horses with either acute or chronic upper
respiratory tract disease and 5 from horses with acute
parotiditis. Tracheal swabs were collected from 90
clinically normal slaughtered horses, from 28 slaughtered
horses and 2 dead horses with gross pathological lesions
in the respiratory tract. Lung tissues from horses with
respiratory lesions were also examined.
chlamydia are given below. NS I2 I , a 2 year old Arab
gelding, exhibited signs of acute upper respiratory
disease with rhinitis, serous nasal discharge, lachrymation
and fever. NS 172 was an 8 year old mare in advanced
pregnancy, imported from New Zealand only 3 weeks
before examination. The mare showed mucopurulent
nasal discharge, slight cough, abdominal respiration,
congestion of the conjunctiva, lachrymation and
subcutaneous oedema of all the legs and abdomen.
Nasal swabs were collected from both the horses,
while from the latter blood also was collected for
haematology and serology. It was reported that mare
NS 172 subsequently gave birth to a normal foal. Organs
from 14 aborted foetuses and synovial fluids from 4
horses with acute polyarthritis were also examined.
The methods of collection of nasal swabs into transport
medium have been described previously (Moorthy and
Spradbrow, 1976).
Isolation of chlamydias. Medium expressed from the
swabs was treated with a final concentration of strepto-
mycin of 5 mg/ml and kanamycin I mg/ml, kept at
4°C overnight and centrifuged at 900 x g for 20 min.
0.5 ml of the supernatant fluid was inoculated into the
yolk sacs of 6 to 7 day old chicken embryos, 4 for each
sample, which were incubated at 37°C. The eggs were
candled daily for 13 days. For controls, transport
medium was treated with antibiotics, processed and
inoculated into chicken embryos as described above.
Deaths of embryos within 48-72 hours of inoculation
were considered nonspecific. Those which died after
96 hours were opened. Yolk sacs were harvested and
EQUINE VETERINARY JOURNAL 39
impression smears were prepared. The smears were gross lesions in internal organs. Attempts were made to
lightly heat fixed and stained by the method of Giminez recover chlamydia from liver and spleen.
(1964). Chick embryos. Chicken embryos were also inocu-
All embryos, which survived to 13 days post-inocula- lated with yolk sac suspensions by the chorioallantoic
tion were killed. Yolk sac smears were stained and membrane (CAM) route.
yolk sacs were repassaged twice in chicken embryos.
Test for Toxin Production. This test was performed
Identification and differentiation of chlamydias as described by York and Baker (1951). Heavily
Yolk sac materials containing chlamydia were plated on infected yolk sacs from recently dead embryos were
bacteriological media and examined for bacterial growth. harvested and made into a suspension ( I :2) with allantoic
Boiled antigen was prepared from infected yolk sacs to fluid and yolk material from normal 7 day old eggs.
test against group specific chlamydial antisera by After centrifugation at 380 x g for 10 min, 2-fold dilutions
complement fixation test (Page, 1968), susceptibility of of the supernate from I :5 to 1 :40 were made with normal
chlamydial strains to sodium sulphadiazine was used to egg material. Each dilution of 0.5 ml was given to a
differentiate C. trachomatis from C . psittaci (Page, 1968). batch of 4 adult mice intravenously. The mice were
observed for 4 days.
Characterization of chlamydias
Staining. Morphological and tinctorial properties of Serology
the chlamydial agents were observed by staining yolk Serum samples
sac impression smears by Giminez, Giesma and Gram (i) Rabbit hyperimmune serum against LGV strain
methods and the acridine orange method of Starr, et (IMVS-11) was obtained from Dr. D. Graham,
al. (1960). Department of Microbiology, University of Mel-
Filtration. A 10-Ldilution of the yolk sac suspension bourne, Parkville, Victoria, 3052, Australia.
was centrifuged at 900 x g for 20 min and the supernate (ii) Paired sera from NS 172 mare, taken at the time of
was filtered through Millipore membrane filters having illness and 41 days later.
pore diameters of 220 nm and 450 nm. Each filtrate (iii) Pooled control mice sera.
was inoculated separately into a group of 4 chicken
embryos by the yolk sac route. Unfiltered suspension (iv) Pooled sera from infected mice.
was also inoculated into a set of embryos. (v) Pre- and post-infection guinea pig sera.
Thermostability. Yolk sac suspensions in sealed Antigen
ampoules were immersed in constant temperature water- (i) Complement fixing (CF) antigen and agar gel
bath at 56°C for 30 min before being used for yolk sac precipitation (AGP) antigen were prepared from the
inoculation of chicken embryos. present chlamydias according to the method
described by Page ( 1 974).
Antibiotic sensitivity. Infected yolk sac suspensions
were centrifuged at 900 g for 20 min and a portion of (ii) Chlamydia1 (Bedsonial) group complement fixing
the supernate was treated with 10,OOO iu/ml of penicillin antigen and control antigen (C.S.L., Victoria) was
(Crystapen, Glaxo) and another portion with 200 mg/ml purchased.
of streptomycin overnight at 4°C. Each of these was The CFT was conducted in microplates and the test
inoculated into a group of 4 embryos by the yolk sac procedure was as described by Casey (1965). The
route (Mendlowski, Kraybill and Segre, 1960). procedure of preparing agar gel plates, cutting wells,
inoculation and incubation were according to the method
Titration. Several 10-fold dilutions of yolk sac of Page (1974).
suspension were prepared in phosphate buffered saline
(PBS) and 0.5 ml of each dilution was inoculated into a Electron microscopy: Allantoic and pericardial fluids
group of 4 embryos and incubated at 37°C. Deaths of from dead embryos were collected for negative staining
embryos were recorded daily for 13 days. The 50 per with 1.5 per cent phosphotungstic acid of pH 7.0 and
cent ELD,, was calculated by the method of Reed and examined with a Semen’s Elmiskop (Model 1A)
Muench (1938). electron microscope.
Small pieces (5 x 5 mm) of positive yolk sacs were
Pathogenicity to laboratory animals: fixed with glutaraldehyde solution at 4°C for one hour
Mice. 0.05 ml of the yolk sac suspension containing and transferred to sucrose buffer at 4°C for further
chlamydia was used to inoculate suckling mice by the processing.
intraperitoneal route and adult mice by intravenous
(0.5 ml) and intranasal routes (0.3 ml). After 2 to 3 RESULTS
weeks of observation, inoculated mice were destroyed Isolation of Chlamydia
after collection of blood for serology. Examinations
were made for gross lesions and liver, spleen and lung Agents which resembled chlamydia microscopically
were used to inoculate chicken embryos. were isolated from nasal swab materials from 2 horses
(NS 121 and NS 172) by chicken embryo inoculation.
Guinea pigs. For each strain of chlamydia, 2 male No chlamydia were isolated from the remaining 276
guinea pigs were inoculated with 2.0 ml of yolk sac respiratory tract samples nor from aborted foetuses or
suspension by the intraperitoneal route. Pre-inoculation horses with polyarthritis.
blood was obtained. Daily temperatures were recorded NS 121 strain did not produce death of chicken
and animals were observed for 40 days for any signs of embryos on first passage. Yolk sac impression smears
disease. After this period blood was collected for of 3 of the 4 embryos showed intracytoplasmic
serology and they were destroyed and examined for inclusion bodies on Giminez staining although no
40
lesions were observed in embryos 13 days after inocu-
lation. On second passage of the yolk sac material,
death of embryos occurred by 10-1 1 days after infection.
The chicken embryos infected with NS 172 material
died after 10-12 days of incubation. Yolk sac im-
pression smears of all the embryos contained chlamydias
in both intracytoplasmic and extracytoplasmic locations.
On subsequent passages of yolk sac materials from both
samples, mortality of embryos occurred by 7-13 days
after infection.
The lesions observed in chicken embryos that died due
to chlamydial infection were deeply injected major blood
vessels of the yolk sac and congestion of the smaller
vessels. The embryos were hyperaemic, had cyanotic
legs and toes and were sometimes deep red in colour.
Patches of haemorrhage were observed in the skin.
Infected embryos were smaller than control embryos.
The embryos that died after 10 days of infection con-
sistently showed marked hydropericardium. On
subsequent passages embryos died within 7 to 8 days of
infection and no such lesions were observed. Areas
of hepatic necrosis were observed with both the strains.
Boiled antigens of both the strains NS 121 and NS 172
reacted with complement fixing antibodies against
known chlamydia and no such complement fixation
occurred with the known negative sera. The ELD,,
values per 0.5 ml of the sets of embryos receiving sodium
sulphadiazine and those receiving diluent alone were
10’ and lo‘.’ respectively in the case of NS 121 strain,
while the NS 172 strain gave titres of 10-b to 10”’
respectively.
Morphological and tinctorial properties of both the
strains were similar. By the Giminez method of staining,
the organisms appeared as small round dots of red colour
in both intra- and extracytoplasmic locations. Their
colour was purple in Giemsa stained smears and they
could not be stained with Gram’s method. These
organisms appeared as bright greenish yellow round
structures in both extra- and intracytoplasmic locations
in acridine orange stained smears, when examined under
U.V.illumination.
Negative staining of the allantoic and pericardial
fluids revealed small roundish structures which appeared
to be elementary bodies. They were enclosed by 2
membranes, and in the cytoplasm an electron dense
nucleoid was observed. The diameter of these particles
was about 275 nm.
Ultra thin sections of the infected yolk sac revealed
large round bodies with a diameter of 500 to 950 nm,
possessing a cell wall of 2 layers. The inner and outer
EQUINE VETERINARY JOURNAL
membranes were separated. An “hour glass” profile
seen in a reticulate body was suggestive of the division
by binary fission.
Both the NS 121 and NS 172 strains passed through
220 nm and 450 nm filters. Both the strains were
destroyed during 30 minutes exposure at 56°C. They
were sensitive to penicillin and resistant to streptomycin.
Materials containing chlamydiae failed to grow on
bacteriological media. There were no signs of disease
or autopsy lesions in experimentally infected mice.
Chlamydiae were reisolated from lung, liver and spleen
materials by chicken embryo inoculation. No deaths
due to toxicity were observed in mice with either of the
equine strains of C. psittaci. In guinea pigs also there
were no signs of disease and no fever. On autopsy,
there was enlargement of the spleen and increased
peritoneal fluid was observed. lmpression smears
were negative for chlamydia, but spleen from both the
cases yielded chlamydias by chicken embryo inoculation.
lnoculation of the CAM of chicken embryos resulted
in neither death of embryos nor lesions on the CAM.
The results of the CFT are shown in Table 1. They
indicate that both the present isolates and the type
chlamydia share a common complement-fixing antigen,
and that specific complement-fixing antibodies appeared
after infection in laboratory animals and in mare NS 172.
AGP Test
NS 172 chlamydial antigen and NS 172 allantoic
fluid gave precipitin lines when tested by AGP test
against convalescent sera of NS I72 mare, post-infection
guinea pig sera of NS 172 mare, post-infection guinea
pig sera raised against both the stains, sera of mice
infected with NS 172 strain and rabbit hyperimmune
serum against IMVC-II strain. Acute phase serum
from mare NS 172 was nonreactive, and no reactions
occurred with control allantoic fluid.
Haematological findings of the NS 172 horse included
a total erythrocyte count 9 x l O l 2 / 1 ; leucocyte count
10.1 x IO”/l; packed cell volume .41 1/1; haemoglobin
content 18.0 g/dl. The differential count of leucocytes
included neutrophils 56 per cent; lymphocytes 36 per
cent, basophils 2 per cent, eosinophils 4 per cent and
monocytes 2 per cent.
DlSCUSSION
Strains NS 121 and NS 172 produced characteristic
intracytoplasmic inclusions in infected cells, which were
identified after Giminez or Giemsa staining of impression

Rabbit Horse sera NS 172 Mice sera Guinea pig sera

Antigen sera Acute Conval. Control NS I21 NS 172 NS 121 NS 172
IMVS-11 phase phase sera pr.i. pi. pr.i. p.i.
- ~ ~ _ _ -~ _ ~ . .~

Control antigen < 4* <4 <4 <4 <4 <4 <4 <4 <4 <4
NS 121 256 NT NT <4 256 256 <4 64 <4 256
NS 172 512 <4 128 <4 512 256 <4 256 <4 256
SSL control antigen <4 <4 <4 <4 14 <4 <4 <4 <4 <4
CSL antigen 512 <4 128 <4 256 512 <4 128 <4 256
EQUINE VETERINARY JOURNAL
smears of yolk sacs, produced typical lesions in the
chicken embryos and yielded antigens that contained
group specific chlamydial antigen. These characters,
together with their failure to grown on bacteriological
media, allow their classification as members of the genus
Chlamydia. The present 2 strains of chlamydia are
considered as C. psittaci on the basis of their resistance
to sodium sulphadiazine.
The present equine strains of C. psittaci are non-
toxigenic and apathogenic to laboratory animals except
for chicken embryos, although recovery of organisms
and detection of antibodies was possible in the infected
mice and guinea pigs. Storz (1971) mentioned that
mammalian strains of C. psittaci have little effect on
mice which may remain latently infected. Marriot and
Storz (1966) reported that chlamydias from different
origins varied considerably in their ability to multiply
in cells of the CAM and most of them grew poorly in
these cells. The present equine isolates caused neither
deaths of embryos nor pock lesions on the CAM.
Chlamydial infections of animals with various disease
syndromes have been reported from Australia (French,
1959; French and Snowdon, 1960; Rofe, 1967; St.
George, 1971 and Cockram and Jackson, 1974). The
only previous evidence for the existence of equine
chlamydias in Australia was that of Studdert (1969)
who reported serological evidence for chlamydial
infection in 11 of 16 horses. There have been isolations
of chlamydia from various disease conditions of horses
or demonstrations of antibody in Europe by Sarateanu,
et al. (1963), Terzin and Miskov (1965), Friis (1967),
Popovici and Hiastru (1968 and 1969), Blanco-Loizelier
and Page (1974), Neuvonen and Estola (1974) and
Schmatz, et al. (1977), in Africa by Erasmus (1973)
and Bosman, et al. (1973) and in U.S.A. by McChesney,
et a/. (1974). The present study appears to be the first
isolation of chlamydia from nasal tract of horses with
upper respiratory disease.
In this study, mare NS 172 had acute upper respiratory
disease associated with oedema of the dependent parts.
The blood picture was in the normal range. Oedema
may have been due to advanced pregnancy, and it cannot
be determined whether this condition was due to
chlamydial infection or not. It was certain that this
mare was undergoing a chlamydial infection because of
the isolation of chlamydial agents and because of the
rise of antibody titre in convalescent serum.
Although chlamydial strains have been incriminated
as causative agents for abortion in cattle, sheep, goats,
pigs, horses and man (Storz, et al., 1960; Stamp, et al.,
1950; Staub, 1959; Bohac and Mensik, 1965; Bosman,
et a/., 1973 and Schacheter, 1967) and arthritis in lambs
(Storz, et al., 1963), in calves (Storz, Smart and Shape,
1964) and in a foal (McChesney, et al., 1974), in the
present study, chlamydia was not isolated from aborted
foals and polyarthritic horses.
Schmatz, et al. (1977) demonstrated a significant
correlation between respiratory disease in horses and
complement fixing antibodies to chlamydia. The present
isolation of C. psittaci from acute respiratory disease,
and experimental production in horses of chlamydial
pneumonia, abortions and polyarthritis (Omori, et al.,
1953; Saito, 1954 and Erasmus, 1973) should encourage
further studies in the role of chlamydias in equine
diseases.
41
ACKNOWLEDGEMENTS
This study was supported by a grant from the Queensland
Equine Research Foundation. The authors are indebted to
Dr. D. Graham, University of Melbourne, for supply of positive
chlamydial antiserum. The senior author was supported by the
Commonwealth Scholarship and Fellowship Programme.
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Accepted for publication 15.9.77