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UPDATE ON SMALL RUMINANT MEDICINE 0749-0720/01 $15.00 + .

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CHLAMYDIAL INFECTIONS IN
SMALL RUMINANTS
Jerome C. Nietfeld, DVM, PhD

Two species of the genus Chlamydophila (formerly Chlamydia) cause


diseases in small ruminants. Chlamydophila abortus has an affinity for
placental tissue and is an important cause of abortion in sheep and
goats. 1,5, 13,23,34,40,44,45 There is one reported case of its causing abortion
in llamas. 16 In male animals, C. abortus infection can cause orchitis and
seminal vesiculitis, resulting in shedding of the organism in semen. 4,26,
34, 45 C. abortus is zoonotic, and although most human infections are
mild and often unnoticed, pregnant women can develop severe, life-
threatening illness and abort. 1, 21, 34 Chlamydophila pecorum is commonly
isolated from the digestive tract of ruminants, and it is recognized as a
cause of conjunctivitis, arthritis, and inapparent infections in sheep and
goats. 11 , 12,34,45 Reports of diseases caused by C. pecorum in South Ameri-
can camelids are rare or nonexistent. C. pecorum is not known to cause
disease in humans.

CLASSIFICATION AND CHARACTERISTICS

Members of the order Chlamydiales are obligate, intracellular bacteria


that depend on the host cell for energy. 10, 37,46 They display a two-stage
developmental cycle that is different from other bacteria with two dis-
tinct developmental forms, elementary bodies and reticulate bodies.lO,
37,46 Elementary bodies are the infectious form and are small (200-300

nm), dense, metabolically inactive structures that are relatively stable in


the environment. Reticulate bodies are noninfectious, metabolically ac-
tive, larger (500-1000 nm), labile in the environment, and less electron-

From the Department of Diagnostic Medicine/Pathobiology, College of Veterinary Medi-


cine, Kansas State University, Manhattan, Kansas

VETERINARY CLINICS OF NORTH AMERICA:


FOOD ANIMAL PRACTICE

VOLUME 17 • NUMBER 2 • JULY 2001 301


302 NIETFELD

dense than elementary bodies. Elementary bodies attach to cells and are
endocytosed into cytoplasmic, membrane-bound vacuoles where they
inhibit fusion of the vacuoles with lysosomes, thus evading host cell
defenses. la, 37, 46 After 6 to 8 hours, the elementary bodies transform into
reticulate bodies, which divide multiple times by binary fission for
approximately 24 hours and then begin to transform into elementary
bodies. The result is an intracytoplasmic inclusion filled with elementary
and reticulate bodies as well as forms that are intermediate between the
two. Forty eight to 72 hours after infection, progeny are released by lysis
of the host cell or by fusion of the inclusion with the host cell mem-
brane.lO, 37, 46
All chlamydiae share lipopolysaccharide antigens that are serologi-
cally and structurally related to lipopolysaccharide antigens of rough
mutants of gram-negative bacteria of the family Enterobacteriaceae. 46 The
chlamydial lipopolysaccharides also possess a chlamydia-specific anti-
gen that is the basis for the complement fixation test used for serologic
diagnosis of chlamydial infections. I, 46
Until 1999, the order Chlamydiales contained one family, the Chlamyd-
iaceae, with one genus, Chlamydia, that contained four species, trachomatis,
pneumoniae, psittaci, and pecorum. IO C. trachomatis consisted of strains that
primarily infect humans, but also included strains isolated from mice,
hamsters, and swine. C. pneumoniae also consisted of strains that primar-
ily infected humans, but included isolates from koalas and a horse. C.
pecorum strains originated from ruminants, pigs, and koalas, and were
not known to infect humans. C. psittaci was the most diverse species
and included strains with reservoirs in a wide variety of birds and
mammals, and which were capable of being transmitted to and causing
disease in humans. Because of increasing evidence of great genetic
diversity, the genus Chlamydia was reorganized with the addition of one
new genus and five new species. lO Strains of C. trachoma tis retained the
genus name Chlamydia and the other three species were assigned to the
new genus Chlamydophila (Chla my do' philo a).l0 Human biovars of
0 0 0

C. trachomatis retained the name Chlamydia trachoma tis, whereas hamster


and mouse isolates were renamed Chlamydia muridarum and swine iso-
lates were renamed Chlamydia suis. Chlamydia pecorum and Chlamydia
pneumoniae were designated as Chlamydophila pecorum and Chlamydophila
pneumoniae, respectively. All serotypes of Chlamydia psittaci were as-
signed to the genus Chlamydophila and were reorganized into four spe-
cies, including three new species. Only avian-like strains retained the
name Chlamydia psittaci. Strains that cause abortion in ruminants, for-
merly Chlamydia psittaci serovar I, were renamed Chlamydophila abortus.
Chlamydia psittaci strains that affect cats and guinea pigs were renamed
Chlamydophila felis and Chlamydophila caviae, respectively.

REPRODUCTIVE FAILURE CAUSED BY


CHLAMYDOPHILA ABORTUS
Chlamydophila abortus has trophism for the placenta and causes the
disease commonly referred to as ovine enzootic abortion or enzootic abortion
CHLAMYDIAL INFECTIONS IN SMALL RUMINANTS 303

of ewes. It is one of the most important causes of ovine and caprine


abortion worldwide, except for Australia and New Zealand. 1, 17,22,23,30,34,
38,40,45 Additionally, it has been isolated from an epizootic of abortions
in llamas and is a cause of sporadic abortion in cattle. 16, 45 Most C. abortus
research has been conducted in sheep because of the important effect it
has on ovine reproduction.
In the initial outbreak, up to 30% of sheep and 60% of goats can
abort or give birth to stillborn and weak offspring. L 34 Thereafter, yearly
abortion rates of 5% to 10% with occasional flare-ups affecting newly
added animals are usual. Ewes typically abort during the final 2 to 3
weeks of gestation, or their gestation period is of normal length, but
they give birth to stillborn or weak lambs that usually die during the
first few days of life. Some lambs infected in utero are healthy and
survive to adulthood but are affected by enzootic abortion during their
first pregnancy.1, 54, 55 Except for reproductive failure, sheep rarely display
clinical signs of C. abortus infection. Goats can abort at any stage of
pregnancy, but most abortions are during the last 2 to 3 weeks of
gestation. 5, 23, 32, 40 In most cases, abortion is the only clinical evidence of
C. abortus infection in goats, but concurrent respiratory tract disease,
polyarthritis, conjunctivitis, and retained placentas have been reported. 5,32
After abortion, affected animals are immune and are unaffected in subse-
quent pregnancies. 54, 55
The most consistent and severe pathology is in the placenta, where
cotyledons and the surrounding intercotyledonary areas are thickened
because of edema, necrosis, and inflammation and are covered by red-
dish-brown exudate. 1, 8, 32, 34, 44 Affected female animals often pass reddish-
brown fluid for several days after abortion or parturition. Metritis is
more common in goats than sheep, but it is uncommon in both species.
Aborted lambs and goats are usually fresh and well developed with
little or no evidence of autolysis. L 8, 34, 44 Fetuses can be partially covered
by reddish-brown exudate from the necrotic placenta, and occasionally
there are excessive fluid in the abdominal cavity and pinpoint, white
foci of necrosis in the liver. In most cases, however, there are no external
or internal macroscopic lesions in the fetus itself. Microscopic lesions of
necrotizing vasculitis with infiltration by neutrophils and mononuclear
cells are consistently present in the placenta.8,56 Microscopic lesions are
usually mild or absent in fetuses, but focal, coagulative necrosis in the
liver and spleen and interstitial pneumonia are present in a few cases.
Although it has not been recognized clinically, experimental studies
indicate that C. abortus also might cause infertility. In male animals, C.
abortus causes orchitis, epididymitis, and seminal vesiculitis, and it can
be isolated from semen and seminal fluid. 4, 26, 34, 45 Insemination with
semen artificially mixed with C. abortus resulted in decreased conception
in ewes and heifers,4,7 which was shown in heifers to be the result of
metritis and not infection of the embryo? In another experiment, 5
(26.3%) of 19 ewes confirmed pregnant by ultrasonography at 40 days
of gestation and infected with C. abortus at day 50 of gestation were not
pregnant at 105 days of gestation. 3o In the flock from which the ewes
304 NIETFELD

originated, only 5 (1.4%) of 361 ewes that were confirmed pregnant at


day 40 of gestation failed to lamb.

Transmission

Placentas and fetal fluids from affected animals are massively in-
fected with C. abortus. Uterine secretions of ewes contain chlamydiae
from approximately 1 day before abortion to 2 to 3 weeks after abortion,1,
29, 35 and secretions from goats can contain chlamydiae from as early as
9 days before to 2 weeks after abortion. 32 During typical spring weather
when lambing usually occurs, elementary bodies can remain infectious
in the environment for several days, and if the temperature is freezing
or near freezing, for months. 1 Most animals become infected by ingestion
of organisms in contaminated feed or water, licking animals contami-
nated with placental fluids or tissues, or inhalation of aerosols created
in the contaminated environments. 19, 55 If infected 5 to 6 weeks before
parturition, sheep and goats can develop clinical disease during the
current pregnancy; however, if infected later in gestation, many animals
apparently develop latent infections and are normal until the next birth-
ing season when they experience reproductive failure due to C.
abortus. 54,55 Lambs infected in the perinatal period with C. abortus are
clinically normal until their first pregnancy, when some of them
abort. 54, 55
Initial attempts at venereal transmission by mixing C. abortus with
semen and by inoculation of C. abortus into the vagina after natural
breeding resulted in typical signs of enzootic abortion in only a minority
of cases. 4,55 It was concluded that venereal transmission was possible
but probably not common because of the management techniques used
in raising sheep; however, more recent experiments in sheep indicate
that venereal transmission may be more important than previously
thought. Intravaginal infection with C. abortus 6 weeks before breeding
or at 60 days of gestation can result in chlamydiaI placentitis and
birth of small, weak lambs or abortion. 28 After experimental and natural
abortion due to C. abortus, affected ewes conceive and lamb normally,
but they shed C. abortus from their reproductive tracts for at least 2.5 to
3 years. 27, 29, 31 Organisms can be detected for 3 to 4 days before and
after ovulation but not at any other time, including after subsequent
lambings. 29, 31 In addition, some virgin ewe lambs born into an infected
flock shed C. abortus from their reproductive tract. 25 Because rams can
become infected and shed C. abortus in their semen after breeding an
infected ewe,26 it is possible that clinically normal ewes with persistent
reproductive tract infection are a source of transmission within and
between flocks.
Chlamydophila abortus has not been found to be transmitted in milk
or colostrum from sheep,18, 47, 48,50 but it is said to be transmitted in goat's
milk. 23 C. abortus is occasionally isolated from the feces of ruminants,
raising the possibility of intestinal infection and fecal-oral transmis-
CHLAMYDIAL INFECTIONS IN SMALL RUMINANTS 305

sion. 34, 45 Most fecal isolates are C. pecorum,12, 34 however, which makes
the importance of intestinal infection by C. abortus unknown.

Pathogenesis

Subcutaneous inoculation of ewes with C. abortus as early as 25


days of gestation results in placentitis and abortion in the last 2 to 3
weeks of gestation. 8,30 Although C. abortus can be detected in the placenta
earlier, placental pathology is minimal or absent before 90 days of
gestation. 8,30 The initial placental lesions consist of chlamydial inclusions
within the trophoblastic epithelium,8 proceeding to necrosis, edema, and
infiltration by neutrophils, macrophages, lymphocytes, and plasma cells,
which spread to adjacent tissues. Associated vessels develop necrosis
and neutrophilic inflammation. Concurrently, there are chlamydial inclu-
sions in the endometrial epithelium, which elicit necrosis and inflamma-
tion. As the pregnancy proceeds, the fetus is infected, resulting in focal
inflammation and necrosis in the liver, lung, and lymph nodes. 8
After oral-nasal inoculation of nonpregnant sheep with C. abortus,
chlamydial antigen was detected at 27 hours after inoculation in the
tonsils, suprapharyngeallymph nodes, abomasum, and small intestine. 3
Between the second and seventh day after inoculation, C. abortus could
be isolated from the blood of most sheep. At the same time, chlamydial
antigen was detected immunologically but not isolated in lymph nodes
throughout the body and from most major organs, including the lung,
liver, spleen, and kidneys.3 Chlamydial antigen cannot be detected in
any tissue past 7 days after infection. 3,17 Thus, it seems that after oral-
nasal inoculation, primary infection occurs in the lymphoid tissue of the
pharyngeal area and the mucosa of the intestines. After a short period
of replication, there is chlamydemia that results in systemic infection
followed by clearance from the body. It is known, however, that some
ewes infected when not pregnant or during late pregnancy develop
chlamydial placentitis during their next pregnancy, after which they
are immune to reproductive failure caused by C. abortus. Therefore, in
nonpregnant sheep the organism must be able to establish a persistent,
undetectable infection that does not stimulate protective immunity, and
during the subsequent pregnancy something occurs that allows reactiva-
tion and multiplication of C. abortus.
After experimental infection before breeding or during pregnancy
by the oral-nasal, subcutaneous, and intravaginal routes, there is a rise
in anti-C. abortus titers that soon declines to low levels with many sheep
becoming serologically negative. 28, 29, 55 Antibody titers remain low until
late pregnancy, when, in ewes that develop placentitis, titers increase to
levels much higher than initially present, and they persist for at least 2.5
years. 28, 29, 55 After abortion, the ewes are immune to reproductive failure
caused by C. abortus, but they persistently excrete the organism from
their reproductive tracts during estrus. 29,31 This indicates that there is
initial multiplication of C. abortus, which stimulates an immune response
306 NIETFELD

that suppresses multiplication and induces latency. During the last tri-
mester of pregnancy, C. abortus is reactivated and multiplies in the
placenta, resulting in restimulation of the immune system. After abor-
tion, persistent infection of the reproductive tract causes persistent stim-
ulation of the immune system, resistance to clinical disease, and mainte-
nance of high antibody titers, but not elimination of infection.
In vitro studies may provide clues as to the mechanisms involved
in establishing latent infections. Under a variety of conditions, C. tracho-
matis, C. psittaci, and C. abortus can establish inapparent, persistent
infections in cell culture. 6, 9, 33 Persistently infected cell cultures have been
maintained for more than 1 year, and when the conditions used to
induce persistence were removed, there was resumption of chlamydial
growth that resulted in inclusion formation and celllysis. 6 Maintenance
of C. abortus in persistently infected McCoy cells for 6 months did not
reduce virulence for pregnant sheep.33 Interferon gamma (IFN-')') from
activated T cells restricts chlamydial growth in macrophages, fibroblasts,
and epithelial cells, and low levels of INF-')' added to cell cultures
infected with chlamydiae, including C. abortus, cause persistent infec-
tion. 6,9 Removal of the INF-')' results in resumption of chlamydial multi-
plication. Chlamydial infections induce INF-')' production, and depletion
of INF-')' in mice results in increased in vivo multiplication of C. tracho-
matis and C. abortus. 9
If the immune system of sheep can suppress chlamydial multiplica-
tion, something occurs during pregnancy that allows reactivation and
multiplication of C. abortus. 17 The factors that allow reactivation are
currently unknown. 9, 17 It is known that pregnancy results in immuno-
suppression of the dam and that sera from pregnant humans, dogs, and
mice depresses several lymphocyte functions. 9 Hormonal changes during
pregnancy also could directly stimulate or inhibit growth of C. abortus.
The finding that sheep persistently infected with C. abortus excrete the
organism from their reproductive tracts only during estrus29,31 seems to
indicate that hormones influence in vivo multiplication of C. abortus.

Diagnosis

Abortion of well-preserved lambs in association with necrotizing


placentitis in the last 2 to 3 weeks of pregnancy is sufficient to make a
tentative diagnosis of chlamydial abortion. 1 Microscopic lesions in the
placenta consisting of moderate to severe necrosis with necrotizing vas-
culitis further support the diagnosis. 56 Occasionally, the same clinical
picture is present in abortions caused by Toxoplasma gondii, l but vasculitis
in the placenta is not a feature of toxoplasmosis. 56 Coxiella burnetii, a
rickettsia that rarely causes ovine and caprine abortion, also causes
necrotic placentitis and histologically can be confused with chlamyd-
iosis.1, 56 Necrotic placentitis is not a feature of infection by Campylobacter
or Listeria Spp.1
Definitive diagnosis depends on identification of C. abortus in the
CHLAMYDIAL INFECTIONS IN SMALL RUMINANTS 307

placenta, fetal tissues, or vaginal secretions. Probably, the most common


method of identification of chlamydial elementary bodies is by micro-
scopic examination of impression smears of the placenta stained by the
Gimenez, Giemsa, modified Ziehl-Neelsen, or Machiavello methods. 1, 34,44
If the placenta is not available, vaginal smears are sometimes used, but
the inclusions are not as abundant. l Chlamydial inclusions appear as
groups of bright red, coccoid structures with the Gimenez, Ziehl-
Neelsen, and Machiavello staining techniques and as purple structures
with the Giemsa stain. Coxiella and Brucella spp. have similar appear-
ances. I Although Brucella spp. are larger than either C. abortus or C.
burnetii, experience is required to make that distinction. 34, 44 Fluorescent
antibody and immunohistochemical staining with specific antibodies of
smears or frozen sections of placenta or paraffin-embedded, formalin-
fixed sections of placenta differentiate C. abortus from Coxiella and Bru-
cella.2, 31, 44
Chlamydophila abortus can be isolated in embryonated chicken eggs
or, more commonly, cell culture. Isolation from placentas and vaginal
swabs taken the first 3 days after abortion is sensitive and specific, but
it is labor intensive, prone to contamination, and not offered by all
diagnostic laboratories. 34 Samples should be collected as soon as possible
after abortion, refrigerated, and kept on ice during transport to maintain
viability of the organisms and to keep growth of contaminating bacteria
to a minimum.
An experimental ELISA for specific detection of C. abortus in vaginal
swabs from aborting sheep and goats provided good results, but it is
not available commercially.43 Some commercial ELISA kits designed to
detect C. trachoma tis have shown good sensitivity and specificity in
identifying C. abortus antigens in samples from aborting sheep and
goats 36, 47, 51; however, immunoassay kits for C. trachoma tis should be
evaluated before use in identification of C. abortus, because occasionally
test kits have inadequate specificity due to cross reactions with other
gram-negative bacteria.35 The best samples for ELISA testing are placenta
and vaginal swabs obtained within the first 3 days after abortion. Fetal
tissues can be used, but they do not contain as many organisms and
give a higher percentage of false-negative results.
Numerous polymerase chain reaction (PCR) procedures for detec-
tion of chlamydial DNA have been developed, and several of these
procedures are able to identify chlamydiae to the species level. These
procedures are valuable for species identification of chlamydiae, but
most PCR procedures were developed using laboratory-grown cultures
and have not been rigorously tested using field samples. Unless stringent
precautions are taken in collection and testing of the samples, cross
contamination and false-positive results are possible. 34 Also, contami-
nants in field samples can inhibit the PCR, giving false-negative results,
and currently this may be a greater problem than false-positive results. 34
In the past few years, new methods of removing PCR inhibitors have
been and continue to be developed. As these techniques are incorporated
308 NIETFELD

into PCR methodology and verified as reliable, PCR will likely become
the method of choice for fast and accurate diagnosis.
The complement fixation (CF) test is the most widely used serologic
test, but it has some limitations. 34 The CF test detects antibodies to
antigens common to all chlamydiae and cannot differentiate between
titers to C. abortus, C. pecorum, or C. psittaci, which occasionally infects
ruminants. Antibody titers to C. abortus usually remain low or negative
until the termination of pregnancy when there is a marked rise in titer
that peaks in 14 to 21 days, at which time the CF titer of most animals
that have aborted is at least 1 : 80.40 The test is best used with paired
samples taken at the time of abortion and 2 to 3 weeks later, and when
used for diagnosis on a flock rather than on an individual basis. 34
The CF test cannot reliably identify infected rams and lambs. 34 Other
techniques such as immunofluorescence, microimmunofluorescence, and
ELISA have been evaluated for serologic diagnosis. These tests are
generally a little more sensitive and specific than the CF test, but they
still have some of the same problems. 34 A study that compared five
methods of detecting antibodies against C. abortus concluded that none
of the tests were entirely satisfactory.20 All tests could identify infected
flocks, but they were not capable of reliably identifying infected sheep
on an individual basis. Another problem is that in the United States,
standardized reagents for serologic tests are not available commercially
or through government laboratories. Recently, a commercial ELISA kit
(PANCLABORT; YabA Ltd, Bush Loan, Penicuik, Scotland) said to be
specific for antibodies to C. abortus has been marketed in Europe, but it
is not available in the United States.

Prevention and Control

In an outbreak the first goal is to limit spread of infection as much


as possible. 1, 23, 40 Affected animals should be removed immediately and
isolated from the main flock for about 3 weeks, by which time they
should stop shedding chlamydiae. Stillborn lambs and goats, aborted
fetuses, fetal membranes, and bedding should be removed and de-
stroyed. The pens should be thoroughly cleaned and disinfected, and, if
possible, the main flock moved to uncontaminated pens. Caretakers
should care for the affected animals last. Thorough hand washing after
handling aborted material and caring for affected sheep is important.
Footwear and clothing worn in pens with affected animals should be
cleaned and disinfected before being worn in pens with unaffected
animals.
Treatment of all clinically affected and pregnant animals with long-
acting oxytetracycline (20 mg/kg, intramuscularly) is the most com-
monly used method to decrease the number of abortions. 1, 16, 23, 40, 53 The
treatment is usually repeated at 10- to 14-day intervals until parturition/'
40, 53 but some recommend 3 treatments at 3-day intervals. 16, 23 Feed
medication with 400 to 450 mg oxytetracycline/head/day is an alterna-
CHLAMYDIAL INFECTIONS IN SMALL RUMINANTS 309

tive to individual animal treatment. 23,40 Oral tylosin (200 mg/head/ day)
has also been used successfully.40 Oxytetracycline and tylosin inhibit
growth of chlamydiae and help limit additional placental damage, but
they do not completely eliminate the infection or reduce the severity of
existing placental damage, so additional abortions and stillbirths are
possible.
After abortion, affected animals persistently shed C. abortus from
their reproductive tract during estrus and are sources of infection for
other flock members, subsequent new additions, and breeding male
animals. 29,31 If not culled, it is best to segregate previously affected
animals and to use separate rams for the infected and clean groups, or
place the ram with the infected animals after the clean group has been
bred. 1 After breeding, it is best to keep clean and infected animals
separated through gestation and parturition. 1
Vaccination with killed, whole-cell bacterins before breeding sig-
nificantly reduces the incidence of abortion, but it does not prevent all
abortions, eliminate the disease, or reduce shedding at lambing. 1,34 Thus,
the cycle of infection is maintained and vaccination of infected herds
needs to be continued indefinitely. A temperature-sensitive, avirulent C.
abortus vaccine that gives strong, long-lasting protection and significantly
reduces shedding is available in the United Kingdom and a few Euro-
pean countries, but not the United States. 1, 23 The vaccine is licensed for
sheep but not goats and, because it is live, precautions should be taken
to prevent human exposure. 1, 23

Zoonotic Potential

There are rare reports of life-threatening illness and abortion caused


by C. abortus in pregnant women who have had recent contact with
aborting sheep. 1, 10, 21, 34 In pregnant women, C. abortus causes a febrile,
flu-like illness with thrombocytopenia, coagulopathy, pneumonia, and
liver disease in most cases. 21 The organism invades the placenta, re-
sulting in fetal death and abortion. The only infants that have survived
have been cases in which the mothers were treated early with erythro-
mycin, and the infants were delivered by cesarean section before 34
weeks of gestation. 21 Pregnant women are best advised not to have
contact with sheep, especially during the lambing period. There are a
few reports of laboratory personnel working with C. abortus developing
mild respiratory tract infections but, except for pregnant women, people
working with sheep are not reported to develop clinical illness due to
C. abortus. 1

DISEASES CAUSED BY CHLAMYDOPHILA PECORUM

Initially, strains of C. pecorum were classified as serotypes 2, 3, 4, 6,


and 9 of C. psittaci. ll , 12 It became apparent that these strains exhibited
310 NIETFELD

20% or less DNA homology with the three species of the genus Chla-
mydia, and they were renamed Chlamydia pecorum in 1992 and reclassified
as Chlamydophila pecorum in 1999.11,12 The C. pecorum strains are a diverse
group, but they share at least two common antigens that are recognized
by species-specific monoclonal antibodies. 34 Strains of C. pecorum are
widely distributed in ruminants and have been isolated from a wide
variety of tissues and associated with a wide variety of diseases. Most
ruminant isolates of C. pecorum, however, are from the intestinal tract of
healthy animals, are noninvasive, and are associated with clinically
inapparent intestinal infections or localized infections of mucosal sur-
faces. 34 A few strains have been shown to be invasive and to cause
systemic infections after oral inoculation. 45 Strains of C. pecorum are
recognized as important causes of keratoconjunctivitis in sheep and
goats and polyarthritis in sheep. They also have been reported to cause
pneumonia in sheep and goats, but their role as primary respiratory
pathogens is far from certain.

Keratoconju nctivitis

Chlamydophila pecorum and Mycoplasma conjunctivae are the most


important primary causes of infectious keratoconjunctivitis in sheep and
goats. 14, 15, 24, 42, 52 C. pecorum is introduced into a flock by affected animals,
often with mild or inapparent infection, and transmission can occur
between sheep and goats. 15, 24, 45 Direct contact is the most important
method of transmission between animals, and the disease is most com-
mon in situations in which animals are closely confined. Morbidity rates
as high as 90% have been reported in feedlot lambs. 14

Clinical Signs
Initially, there are hyperemia of the vessels of the conjunctiva and
sclera, serous lachrymation, and blepharospasm. 14, 15,52 Many cases spon-
taneously regress at this point. 15, 42 If the disease progresses, hyperplastic
lymphoid follicles develop in the conjunctiva, and inflammation spreads
from the sclera onto the cornea, resulting in neovascularization of the
comea. 14, 15, 52 The exudate becomes purulent and small corneal erosions
may develop, but corneal ulceration is uncommon. 14, 15 Usually the dis-
ease is more severe in adult sheep than in lambs. 15 In the United States,
concurrent polyarthritis can occur in 10% to 85% of lambs with chlamyd-
ial keratoconjunctivitis,14 but arthritis is not a problem in the United
Kingdom or Europe. 49

Diagnosis
Specific diagnosis can be made by identification of chlamydiae by
fluorescent antibody staining of exfoliated cells in conjunctival scrapings,
or by isolation of C. pecorum in cell culture or embryonated eggs. 15, 24, 42
CHLAMYDIAL INFECTIONS IN SMALL RUMINANTS 311

Isolation in embryonated eggs is time consuming, and isolation of C.


pecorum in cell culture is more difficult than isolation of C. abortus. 1s
Exfoliated cells can also be stained with any of the stains used to
visualize C. abortus and examined for chlamydial inclusions; however,
fluorescent antibody staining is preferable because chlamydial organisms
can be confused with melanin granules. 1s The currently available ELISA
kits are manufactured for identification of C. trachoma tis and have not
been evaluated for diagnosis of C. pecorum. Identification of C. pecorum
by PCR is possible, but as with C. abortus, false-negative results due to
inhibitors in the samples could be a problem. 34

Treatment

The most effective treatment is a single intramuscular injection of


long-lasting oxytetracycline (20 mg/kg).1s In herds with high morbidity,
treatment of all exposed animals should be considered. Daily feeding of
150 to 200 mg of tetracycline/head to lambs and kids reduces the
incidence and severity of disease. Intramuscular administration of tylo-
sin also produces good results.42 In cases in which systemic administra-
tion of antibiotics is undesirable because of possible milk contamination,
tetracycline-containing powders, drops, and ointments provide satisfac-
tory results.1S, 24, 42

Polyarthritis

Outbreaks of polyarthritis caused by C. pecorum, often in conjunction


with keratoconjunctivitis, in lambs have been reported from the United
States,14, 39, 45 but there is no solid evidence that polyarthritis is a problem
in goats. 41 Arthrogenic strains of C. pecorum are shed in the feces, and
most infections are thought to be acquired by the oral route because the
disease can be reproduced by oral inoculation. 4s The disease occurs as
epizootics and is most common in lambs weighing 25 to 50 kg with
morbidity rates ranging from 2% to 750/0. 14, 39, 4S Onset is usually acute
and affected lambs are stiff, reluctant to move, febrile, and anorexic.
They lag behind their herd mates and often lie down and do not rise
when approached. Affected joints usually are not swollen, but when
opened, most joints contain excessive grayish-yellow, turbid, synovial
fluid that contains fibrin.39 The joint capsules become thickened, and in
some cases there is erosion of the articular cartilage. Histologically, there
is fibrosis and severe inflammation of the joint capsule.

Diagnosis

Chlamydial arthritis can be diagnosed by the same methods used


for diagnosis of chlamydial keratoconjunctivitis.
312 NIETFELD

Treatment
If treated early, chlamydiaI arthritis responds well to intramuscular
oxytetracycline (250 mg for 2 days), tylosin (200 mg for 2 days), and
penicillin G (300,000 units once).45 Long-lasting oxytetracycline should
also produce a good response. Oral medication with 150 to 200 mg
tetracycline/head/ day helps reduce the incidence and severity of arthri-
tis. As the disease becomes chronic and joint damage becomes more
severe, the response to treatment decreases.

Zoonotic Potential
Chlamydophila pecorum has not been reported to cause illness in
humans.

CONCLUSIONS

Chlamydial diseases in domestic animals are not well understood,


partially because, at least in the United States, they have received rela-
tively little attention. Worldwide, Chlamydophila abortus is and will re-
main for some time one of the most economically important diseases of
sheep and goats. Only recently was it discovered that sheep develop
persistent infections of the reproductive tract, which forces reassessment
of management procedures to prevent and control the disease. Chlamy-
dophila pecorum is less well understood than C. abortus, and much uncer-
tainty still exists as to its real role as a cause of several diseases. It is
hoped that future research will lead to better understanding and im-
proved methods of reliable diagnosis of Chlamydophila spp. and the
diseases that they cause.

References

1. Aitken ID: Chlamydial abortion. In Martin WB, Aitken ID (eds): Diseases of Sheep, ed
3. Oxford, Blackwell Science, 2000, pp 81-86
2. Amin JD, Wilsmore AJ: Detection of Chlamydia psittaci (ovis) antigen in tissue sections
and McCoy cells using streptavidin-biotin and the IMAGEN™ staining method. British
Veterinary Journal 150:555-560, 1994
3. Amin JD, Wilsmore AJ: Studies on the early phase of the pathogenesis of ovine
enzootic abortion in the non-pregnant ewe. British Veterinary JoumaI151:141-155, 1995
4. Appleyard WT, Aitken ID, Anderson IE: Attempted venereal transmission of Chlamydia
psittaci in sheep. Vet Rec 116:535-538, 1985
5. Appleyard WT, Aitken ID, Anderson I: Outbreak of chlamydial abortion in goats. Vet
Rec 113:63, 1983
6. Beatty WL, Morrison RP, Byrne GI: Persistent chlamydiae: From cell culture to a
paradigm for chlamydial pathogenesis. Microbiol Rev 58:686-699, 1994
7. Bowen RA, Spears P, Storz J, et al: Mechanisms of infertility in genital tract infections
due to Chlamydia psittaci through contaminated semen. J Infect Dis 138:95-98, 1978
8. Buxtom D, Barlow RM, Finlayson J, et al: Observations on the pathogenesis of Chla-
mydia psittaci infection of pregnant sheep. J Comp Pathol102:221-237, 1990
CHLAMYDIAL INFECTIONS IN SMALL RUMINANTS 313

9. Entrican G, Brown J, Graham S: Cytokines and the protective host immune response
to Chlamydia psittaci. Comp Immun Microbiol Infect Dis 21:15-26, 1998
10. Everett KDE, Bush RM, Andersen AA: Emended description of the order Chlamydiales,
proposal of Parachlamydiaceae fam. nov. and Simkaniaceae fam. nov., each containing
one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new
genus and five new species, and standards for the identification of organisms. Int J
Syst Bacteriol 49:415-440, 1999
11. Fukushi H, Hirai K: Chlamydia pecorum-the fourth species of genus Chlamydia. Micro-
bioI Immunol 37:515-522, 1993
12. Fukushi H, Hirai K: Proposal of Chlamydia pecorum sp. nov. for Chlamydia strains
derived from ruminants. Int J Syst BacterioI42:306-308, 1992
13. Gunson DE, Acland HM, Gillette DM, et al: Abortion and stillbirth associated with
Chlamydia psittaci var ovis in dairy goats with high titers to Toxoplasma gondii. J Am Vet
Med Assoc 183:1447-1450, 1983
14. Hopkins JB, Stephenson EH, Storz J, et al: Conjunctivitis associated with chlamydial
polyarthritis in lambs. J Am Vet Med Assoc 163:1157-1160, 1973
15. Hosie BD: Ocular diseases. In Martin WB, Aitken ID (eds): Diseases of Sheep, ed 3.
Oxford, Blackwell Science, 2000, pp 301-305
16. Johnson LW: Llama reproduction. Vet Clin North Am Food Anim Pract 5:159-182,1989
17. Jones GE: Chlamydia psittaci: Prevailing problems in pathogenesis. British Veterinary
Journal 151:115-118, 1995
18. Jones GE, Anderson IE: Chlamydia psittaci excretion in ovine milk tested. Vet Rec
124:562, 1989
19. Jones GE, Anderson IE: Chlamydia psittaci: Is tonsillar tissue the portal of entry in ovine
enzootic abortion? Res Vet Sci 44:260-261, 1988
20. Jones GE, Low JC, Machell J, et al: Comparison of five tests for the detection of
antibodies against chlamydial (enzootic) abortion of ewes. Vet Rec 141:164-168, 1997
21. Jorgensen DM: Gestational psittacosis in a Montana sheep rancher. Emerg Infect Dis
3:191-194, 1997
22. Kirkbride CA: Diagnoses in 1,784 ovine abortions and stillbirths. J Vet Diagn Invest
5:398-402, 1993
23. Matthews J: Abortion. In Diseases of the Goat. Oxford, Blackwell Science, 1999, pp
22-36
24. Matthews J: Eye disease. In Diseases of the Goat. Oxford, Blackwell Science, 1999,
pp 280-284
25. Morgan KL, Wills JM, Howard P, et al: Isolation of Chlamydia psittaci from the genital
tract of lambs: A possible link with enzootic abortion of ewes. Vet Rec 123:399-400,1988
26. Papp JR, Shewen PE: Chlamydia psittaci infection in sheep: A paradigm for human
reproductive tract infection. J Reprod Immunol 34:185-202, 1997
27. Papp JR, Shewen PE: Localization of chronic Chlamydia psittaci infection in the repro-
ductive tract of sheep. J Infect Dis 174:1296-1302, 1996
28. Papp JR, Shewen PE: Pregnancy failure following vaginal infection of sheep with
Chlamydia psittaci prior to breeding. Infect Immun 64:1116-1125, 1996
29. Papp JR, Shewen PE, Gartley CJ: Abortion and subsequent excretion of chlamydiae
from the reproductive tract of sheep during estrus. Infect Immun 62:3786-3792, 1994
30. Papp JR, Shewen PE, Gartley CJ: Chlamydia psittaci infection and associated infertility
in sheep. Can J Vet Res 57:185-189, 1993
31. Papp JR, Shewen PE, Thorn CE, et al: Immunocytologic detection of Chlamydia psittaci
from cervical and vaginal samples of chronically infected ewes. Can J Vet Res 62:72-
74, 1998
32. Rodolakis A, Boullet C, Souriau A: Chlamydia psittaci experimental abortion in goats.
Am J Vet Res 45:2086-2089, 1984
33. Rodolakis A, Bernard F, Souriau A, et al: Relationship between virulence of Chlamydia
psittaci strains and establishment of persistent infection of McCoy cells. Vet Microbiol
19:65-73, 1989
34. Rodolakis A, Salinas J, Papp J: Recent advances in ovine chlamydial abortion. Vet Res
29:275-288, 1998
35. Sanderson TP, Andersen AA: Evaluation of an enzyme immunoassay for detection of
314 NIETFELD

Chlamydia psittaci in vaginal secretions, placentas, and fetal tissues from aborting ewes.
J Vet Diagn Invest 1:309-315, 1989
36. Sanderson TP, Andersen AA: Evaluation of a commercial solid-phase enzyme immuno-
assay for the detection of ovine Chlamydia psittaci. J Vet Diagn Invest 4:192-193, 1992
37. Schachter J: Chlamydia. In Gorbach SL, Bartlett JG, Blacklow NR (eds): Infectious
Diseases. Philadelphia, WB Saunders, 1992, pp 1633-1641
38. Sharma KN, Mehrotra KP, Mehrotra PN: Chlamydial infections in sheep: Pneumonitis
and abortions. Indian J Comp Microbiol Immunol Infect Dis 4:145-148, 1983
39. Shupe JL, Storz J: Pathologic study of psittacosis-lymphogranuloma polyarthritis of
lambs. Am J Vet Res 25:943-951, 1964
40. Smith MC, Sherman DM: Chlamydiosis. In Goat Medicine. Philadelphia, Lea & Febiger,
1994, pp 421-422
41. Smith MC, Sherman DM: Musculoskeletal system. In Goat Medicine. Philadelphia,
Lea & Febiger, 1994, pp 63-121
42. Smith MC, Sherman DM: Ocular system. In Goat Medicine. Philadelphia, Lea &
Febiger, 1994, pp 179-192
43. Souriau A, Rokolakis A: Rapid detection of Chlamydia psittaci in vaginal swabs of
aborted ewes and goats by enzyme linked immunosorbent assay (ELISA). Vet Micro-
bioI 11:251-259, 1986
44. Storz J: Chlamydial abortions. In Kirkbride CA (ed): Laboratory Diagnosis of Livestock
Abortions, ed 3. Ames, lA, Iowa State University Press, 1990, pp 37-48
45. Storz J, Kaltenboeck B: Diversity of chlamydia-induced diseases. In Woldehiwet Z,
Ristic M (eds): Rickettsial and Chlamydial Diseases of Domestic Animals. New York,
Pergamon Press, 1993, pp 363-393
46. Storz J, Kaltenboeck B: The chlamydiales. In Woldehiwet Z, Ristic M (eds): Rickettsial
and Chlamydial Diseases of Domestic Animals. New York, Pergamon Press, 1993,
pp 27-64
47. Thomas R, Davison HC, Wilsmore AJ: Use of the IDEIA ELISA to detect Chlamydia
psittaci (avis) in material from aborted fetal membranes and milk from ewes affected
by ovine enzootic abortion. British Veterinary Journal 146:364-367, 1990
48. Venables C, Dawson M, Baskerville M: Chlamydia in ovine milk. Vet Rec 125:137, 1989
49. Watkins GH: Arthritis. In Martin WB, Aitken ID (eds): Diseases of Sheep, ed 3. Oxford,
Blackwell Science, 2000, pp 249-254
50. Wilsmore AJ: Chlamydia in ovine milk. Vet Rec 124:618-619, 1989
51. Wilsmore AJ, Davidson I: "Clearview" rapid test compared with other methods to
diagnose chlamydial infection. Vet Rec 128:503-504, 1991
52. Wilsmore AJ, Dagnall JR, Woodland RM: Experimental conjunctival infection of lambs
with a strain of Chlamydial psittaci isolated from the eyes of a sheep naturally affected
with keratoconjunctivitis. Vet Rec 127:229-231, 1990
53. Wilsmore AJ, Dawson M, Arthur MJ, et al: The use of a delayed hypersensitivity test
and long-acting oxytetracycline in a flock affected with ovine enzootic abortion. British
Veterinary Journal 142:557-561, 1986
54. Wilsmore AJ, Izzard KA, Wilsmore BC, et al: Breeding performance of sheep infected
with Chlamydia psittaci (avis) during their preceding pregnancy. Vet Rec 126:40-41, 1990
55. Wilsmore AJ, Parsons V, Dawson M: Experiments to demonstrate routes of transmis-
sion of ovine enzootic abortion. British Veterinary Jouma1140:380-391, 1984
56. Zeman DH, Kirkbride CA: Histopathology of food animal abortions. In Kirkbride CA
(ed): Laboratory Diagnosis of Livestock Abortions, ed 3. Ames, lA, Iowa State Univer-
sity Press, 1990, pp 191-201
Address reprint requests to
Jerome C. Nietfeld, DVM, PhD
Department of Diagnostic Medicine/Pathobiology
Mosier Hall
College of Veterinary Medicine
Kansas State University
Manhattan, KS 66506

e-mail: nietfeld@Vet.ksu.edu

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