Classical Diseases Related to Chlamydia or Chlamydophila spp. in Animals & Animal Models
ACVIM 2008
Petra Reinhold, Dr. med. vet. habil., PhD; Konrad Sachse, Dr. rer. nat.
Jena, Germany

Spontaneous Chlamydial Infections in Animals

Sheep and Goat

Chlamydophila (C.) abortus (formerly Chlamydia psittaci serotype 1) is an agent causing abortion in small ruminants. Enzootic abortion of ewes (ovine chlamydiosis) is listed as a notifiable disease by the World Organisation for Animal Health (OIE; Office International des Epizooties). Zoonotic infections are known to generate acute or even life-threatening situations in pregnant women who became infected with C. abortus from small ruminants.1

In sheep and goats, the disease is usually manifested as abortion in the last 2 to 3 weeks of gestation, regardless of when the animal was infected. Aborting ewes seem to be resistant to future reproductive failure due to C. abortus, but they become inapparent carriers and intermittently shed the organism from their reproductive tracts during estrus. C. pecorum is the other member of the genus that affects small ruminants, and it is recognized as a primary cause of keratoconjunctivitis in sheep and goats and of polyarthritis in sheep.2

Horses

The clinical outcome of equine chlamydiosis has been described to be very variable. Abortions in mares, polyarthritis in foals, broncho-pneumonia, hepatitis, and fatal cases of encephalomyelitis are a few examples of acute and severe diseases described in the literature. Based on serologic data, the existence of chronic and persistent infections with chlamydiae has also been frequently reported in horses, but a correlation to clinical symptoms is often lacking. Infection of the genital tract with C. psittaci has been suggested to be a possible factor in equine reproductive disorders.3 Recent data indicate a role of C. psittaci and/or C. abortus in equine recurrent airway obstruction (RAO) as trigger factors of inflammation or indicators of severe disease.4

Cattle

Several reports suggested a link between chlamydial infections and various disease syndromes; although neither the prevalence nor the economic impact can be adequately assessed at present. With the availability of modern diagnostic tools, high seroprevalence rates and high detection rates of Chlamydophila spp. in cows and calves underpin the assumption that chlamydial infections are nearly ubiquitous in cattle.5 The species that have been found in cattle so far include: C. pecorum, C. abortus, C. psittaci.

In traditional veterinary literature, the presence of chlamydial infections in cattle was mostly reported in connection with acute illness leading to severe, but rare, disease manifestations such as polyarthritis, enteritis, encephalomyelitis, abortion and fertility disorders.6,7 Respiratory chlamydial infections were mostly subsumed under the generic term of 'pneumonia' characterized by fever and depression, nasal secretions, cough, and dyspnoea.6 Recently an outbreak of acute upper respiratory tract disease was reported in calves aged less than 6 months.8 Furthermore, chlamydial infections have been found to be associated with kerato-conjunctivitis in calves.9

Literature of the last few years focused more on the impact of clinically latent chlamydial infections on both animal health and economic losses. In dairy cows, the presence of chlamydiae was significantly associated with subclinical mastitis and increased somatic cell counts in milk.10 In chlamydia-positive dairy herds, the adult cows are the most likely source of infection, and calves acquire mainly C. abortus and/or C. pecorum in the first 2 weeks after birth.11 Such infections do not necessarily lead to clinical illness, but may lead to chronic or recurrent chlamydial infections on a subclinical level with a significant impact on animal health and postnatal growth.12,13 Interestingly, C. pecorum was mainly found in gastro-intestinal samples, whereas C. abortus was predominant in samples of the respiratory tract and ocular secretions.12 Whether these findings represent different affinities to certain organ system has yet to be examined.

Swine

In pigs, chlamydial infections must be regarded as widespread but often under-diagnosed.14 Chlamydial species detected in pigs include Chlamydia suis (former porcine serovar of C. trachomatis), C. psittaci, C. abortus, and C. pecorum. Epidemiologic studies suggest that chlamydiae are important pathogens in pigs, but the pathogenetic role of the various species has not been clarified as mixed infections are common in herds and even in individual animals.15,16

Chlamydial infections in sows have been associated with reproductive disorders, the occurrence of MMA-syndrome (mastitis, metritis, agalactia), or perinatal mortality in piglets, and detection of chlamydiae in semen of boars suggests a potential for venereal transmission.17-19 In addition, there is some data that chlamydioses in swine can be associated with enteritis, pneumonia, conjunctivitis, polyserositis, pericarditis.14 The knowledge about the involvement of Chlamydiaceae in the porcine respiratory disease complex is still limited, and reports in literature are very inconsistent. While lung function was not affected in symptom-free pigs with a naturally acquired presence of chlamydiae in the respiratory system16, a clear pathogenic potential of Chlamydia suis for the porcine respiratory system has been proven experimentally.16,20,21

Observations in pigs with naturally acquired Chlamydiaceae led to the hypothesis that pigs might be carriers of persisting chlamydiae over months--in the absence of any clinical signs and specific antibody titers. The only significant difference between a group positive for Chlamydiaceae compared to PCR-negative animals was a higher average rectal temperature at a subclinical level, indicating at least some sort of host response.16

Poultry

'Psittacosis' and 'Ornithosis' are two names for an identical zoonotic disease. The causative agent is Chlamydophila psittaci (former avian serovars of Chlamydia psittaci), which might be transmitted to humans either by psittacine birds or by domestic and/or wild fowl. The infection in birds can be acute, protracted, or chronic, but can also be subclinical and asymptomatic. Clinical illness is accompanied by conjunctivitis, serositis, fibrino-pericarditis, hepto- or splenomegalia, anemia, leukocytosis or monocytosis. Avian chlamydiosis is listed by the OIE as a notifiable disease.

Recent data from Europe suggest that psittacosis in the poultry industry is underestimated because it is under-diagnosed, stressing the need for a veterinary vaccine and recommendations for zoonotic risk reduction strategies.22

Other Species

In cats, infections with C. felis clinically results in rhinitis and conjunctivitis, but a lot of serologically positive cats are asymptomatic. Transmission of this infection to humans may result in conjunctivitis or atypical pneumonia. A recent study in our group revealed the occurrence of C. psittaci in female dogs and indicated possible associations with reproductive failure.

C. muridarum and C. caviae cause ocular and genital tract infections in mice or hamsters and guinea pigs, respectively. C. psittaci was isolated (and confirmed by PCR and DNA sequencing) after spontaneous deaths from different organs of laboratory Wistar rats.23 In experimental units, unexpected or unknown chlamydial infections in laboratory rodents may have confounding effects on the results of experimental studies.

C. pneumoniae, a well-established pathogen in human beings, has been isolated from horses, koalas and frogs. There is no knowledge at present, whether strains of animal origin do represent a hazard to human health or whether people had been the source of C. pneumoniae transmitted to animals.

Availability of Large Animal Models of Chlamydial Infections

Respiratory Infections

More than 20 years ago, isolates of Chlamydia psittaci from ovine pneumonia (from today's perspective most likely C. abortus) were inoculated either endobronchially in red deers24 or intratracheally in pigs25, and pneumonia was produced in both species. At that time, experimentally-induced pneumonia by intratracheal inoculation of different strains of the former Chlamydia psittaci group was also reported for pigs and calves.26 In 2005, intrabronchial challenge has been reported for calves again using a pathogenic strain of Chlamydophila psittaci.27 Other experimental trials challenging the respiratory tract intranasally and/or intralaryngeally confirmed the pathogenicity of porcine isolates of C. trachomatis (from today's perspective most likely Chlamydia suis) in gnotobiotic pigs.20 To evaluate the role of Chlamydia suis in conventionally raised pigs, an experimental challenge model of aerosol infection was established by our group.16,21

Beside experimental challenge models, natural models of respiratory chlamydial infections are useful to study the pathogenesis of interactions between host and bacterium. The latter has been shown recently for calves12,13 and horses.4 Experimental and natural models of respiratory chlamydial infections reflect the diversity of pathophysiological features and result in very different clinical pictures. While the Chlamydia suis model in pigs led to acute clinical illness and severe imbalances in gas exchange (comparable to a life-threatening situation), natural infections in calves and horses represented chronic disease courses with clinical outcomes that might be clinically latent for a long time. Nevertheless, chronic inflammation often results in irreversible functional and structural consequences even in the absence of clinical symptoms.

Gastrointestinal Infections

The presence of intestinal chlamydiosis is recognized for various farm animals (e.g., swine and cattle), and rectal swabs are used frequently to identify chlamydial infections in these species. Experimental models have proven that Chlamydia suis can cause intestinal lesions in gnotobiotic piglets, as well as in young weanling pigs.28,29 Also, gnotobiotic piglets have been used to induce an experimental enteric infection with a Chlamydia psittaci strain of avian origin.30,31

Urogenital Infections

Chlamydiae are important reproductive tract pathogens in a wide variety of animals. In humans, chronic or repeated infection of the female genital tract with Chlamydia trachomatis has been identified as a significant factor in the development of occlusive infertility or increased risk of ectopic pregnancy. In man, Chlamydia trachomatis might cause prostatitis. Monkeys have been used in animal models to study chlamydial infections of the human urogenital tract and to understand sexual transmission routes.32,33 In dogs, chlamydial prostatitis was induced experimentally.34 Later, sheep has been postulated as a natural model of persistent chlamydial infection superior to more sophisticated models, in which the chlamydial isolate is not a normal reproductive pathogen of the study animal.35 Recently, the specific-pathogen-free pig has been evaluated as an alternative animal model for Chlamydia trachomatis female genital infection.36,37

Such alternative models for human diseases may be used for the benefit of both human and veterinary medicine. From a purely veterinary perspective, mainly experimental challenge models in sheep38-42, goats43, and sows44 have been used to study the pathogenesis of genital infection with C. abortus. A natural model of C abortus infection in heifers demonstrated that an asymptomatic, circulating, non-sexually transmitted herd infection by Cp. abortus has a profound influence on the fertility of cattle bred.45 In cats, urethritis and vaginitis have been produced with the feline keratoconjunctivitis agent.46

Ocular Infections

In humans, recurrent or persistent infections with Chlamydia trachomatis provide the antigenic stimulus for the chronic inflammation associated with blinding trachoma. Beside humans, only non-human primates are susceptible to conjunctival infection with Chlamydia trachomatis, and have therefore been used as models. Guinea pig inclusion conjunctivitis (GPIC), an analogous disease of guinea pigs, provides a useful, less expensive model to study ocular chlamydial infections.47

In the veterinary field, experimental conjunctival infections have been described in lambs (with chlamydial strains recovered from a sheep with keratoconjunctivitis)48 and in gnotobiotic pigs (with a strain recovered from growing and finishing swine with conjunctivitis or keratoconjunctivitis).49

Conclusions

The presence of natural chlamydial infections was mostly reported in connection with rare and acute diseases in veterinary literature over decades. With the availability of improved diagnostic tools, the presence of chlamydiae has been frequently noticed in clinically inconspicuous animals (pets and farm animals). Recent data from epidemiological surveys indicate that chlamydial infections are disseminated worldwide, but the epidemiological importance of these findings is still unknown. Furthermore, precise data on the zoonotic risk of chlamydiae other than ovine C. abortus or avain C. psittaci is not available.

Due to various pathogenetic peculiarities, chlamydial infections do not necessarily lead to clinical illness. Causing chronic inflammatory reactions and dysfunctions on different organ levels, clinically inapparent chlamydial infections are probably economically more important than rare outbreaks of severe chlamydial disease. From the pathogenetic point of view, the role of chlamydiae as by-standers, co-pathogens, or perpetrators of latent persisting infections is under discussion.

Furthermore, there is a lack of knowledge about the affinity of different chlamydiae to different host species. Especially in farm animals, the parallel presence of two or more Chlamydophila spp. is a regular finding without a clear consideration of their pathogenetic importance.

Improved large-animal models are urgently needed to understand the causative and pathogenetic role of the various chlamydial species in different hosts, as well as within a host in different organ systems. To clarify the impact of chlamydial infections in herds, relevance of co-infections and non-biotic co-factors has to be studied under controlled conditions closed to those in the field.

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Speaker Information
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Petra Reinhold, DMVH, PhD
Fed. Research Inst. for Animal Health
Jena, Germany


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