Avian Chlamydiosis Zoonotic Disease

Introduction

Chlamydia psittaci belongs to the Chlamydiaceae family and is a zoonotic pathogen associated primarily with avian chlamydiosis, also referred to as psittacosis. Chlamydia infection in birds, which shed periodically, is usually systemic and rarely fatal or chronic (Andersen et al. 2007). In humans, chlamydiosis may result in subclinical infection or flu-like illness, or less clinical manifestations, such as endocarditis, myocarditis, encephalitis, or multiorgan failure may be observed (Beeckman et al. 2009). Until recently, C. psittaci was considered to be the main causative agent of psittacosis. The detection and description of Chlamydia avium and Chlamydia gallinacea—new Chlamydia “players”—in birds in different parts of Europe (France, Greece, Croatia, Italy, Germany, Poland, and Slovenia) as well in China and Australia showed that C. psittaci is not the only possible agent of avian chlamydiosis (Gaede et al. 2008, Gasparini et al. 2011, Sachse et al. 2012, Zocevic et al. 2012, Szymańska-Czerwińska et al. 2013). Moreover, C. ibidis is an avian Chlamydia Candidatus. However, so far, the zoonotic transmission of new Chlamydia species has not been confirmed. On the basis of the currently available studies in this range, it could be speculated that these new Chlamydia species can also be a risk to humans.

C. psittaci Infection in Birds and Humans

C. psittaci has been isolated from around 470 bird species (Kaleta and Taday 2003). The highest percentage of infections is found in psittacine birds and pigeons, which can be vectors transmitting the bacterium to poultry and humans. The prevalence of C. psittaci is comparable in individual European countries. Domestic pigeons in Poland and Belgium showed a 7.6% and 6.3% prevalence, respectively, of this pathogen (Dickx et al. 2010, Stenzel et al. 2014). The European average is slightly lower in feral pigeons at 5.7% (Prukner-Radović et al. 2005, Heddema et al. 2006, Dickx et al. 2010, Sachse et al. 2012). A slightly higher percentage of C. psittaci in captive parrots was noted in Poland (10.3%) by Piasecki et al. (2012), whereas a recent survey performed in Central America showed that the prevalence of C. psittaci in captive psittacines was 3.2% in the region of Costa Rica (Sheleby-Elias et al. 2013). A study of feral pigeons in Amsterdam and Poland revealed that shedding of C. psittaci with feces was significantly higher during breeding than during the quiescent season (Stenzel et al. 2014).

C. psittaci is significant for public health because of the popularity of psittacine birds as pets and their increased placement in childcare facilities and in homes for the elderly. Moreover, the risk of infection is not only associated with direct contact with birds, but is also pertinent to rural environments and gardening activities. Psittacosis is a notifiable disease in Australia, the United States, and most European countries, e.g., Belgium, France, Germany, Italy, and Poland. Psittacosis cases are also noted in different countries. The US Centers for Disease Control and Prevention (CDC) confirmed 935 human cases of ornithosis between 1988 and 2003, whereas between 2005 and 2009 the CDC reported 66 human cases. Two cases of C. psittaci infection were reported by the National Institute of Public Health in Poland between 2012 and 2013. On the other hand, according to official statements, C. psittaci was not reported in humans in Poland between 2009 and 2011 (Anonymous 2013), whereas avian Chlamydia was recorded in birds during this period. In Australia, Germany, Sweden, and The Netherlands, 62, 10, nine, and 27 cases, respectively, were reported in 2007 (Harkinezhad et al. 2009). An evaluation of zoonotic transmission of C. psittaci within Belgian psittacine breeding facilities showed that 19.2% of parrots and 13% of bird owners were infected (Vanrompay et al. 2007). Generally, it is known that reported psittacosis cases have not reflected the real C. psittaci infection status, and this has been confirmed by the reports of European Cooperation in Science and Technology (COST) action 855 on animal chlamydiosis and zoonotic implications suggesting the underestimation of psittacosis in Europe (Anonymous).

Until recently, there were seven C. psittaci outer-membrane protein A (ompA) genotypes described, designated A–F and E/B. Vanrompay et al. (1993) and Madani and Peighambari (2013) described two new provisional genotypes I and J in psittacine birds. The first new genotype has the closest identity match with C. psittaci genotype F and the second with C. abortus. C. psittaci isolates from pigeons predominantly belong to ompA genotype B. The other genotypes A, C, D, or E were rarely noted (Heddema et al. 2006, Dickx et al. 2010, Sachse et al. 2012, Dolz et al. 2013). Genotype A is regarded as dominant in psittacine birds that are considered the major source of human infection. However, according to the literature, genotype A has also been identified in chickens, turkeys, and wild birds. Nevertheless, genotypes B and D seem to be most prevalent in chicken. Genotype D is mostly correlated with turkeys, but zoonotic transfer from chicken to slaughterhouse employees of this genotype has been described (Dickx et al. 2011). Genotype C was first isolated from ducks and geese, and this genotype is associated with waterfowl, but has additionally been found in chickens in China (Zhang et al. 2008). Vorimore et al. (2013) isolated genotype C from ibis specimens in France. The authors suggested that the pathogen may have been transmitted to the ibis from ducks, where it is relatively abundant, because the ibis lived and fed on open-air duck breeding premises where avian chlamydiosis is highly prevalent. Zoonotic transmission of genotypes A, C, and D and also mixed three-genotype A, C, and D infection in poultry workers has been observed and described by researchers (Dickx et al. 2011).

According to the literature, organisms with infections of C. psittaci are frequently co-infected with other Chlamydia species or bacteria and viruses. Mixed Chlamydia infections, including C. psittaci and new Chlamydia species, have been recorded, e.g., in Germany and Poland (Szymańska-Czerwińska et al. 2013, Sachse et al. 2014). In the Polish case, which was in a commercial flock of laying hens, in addition to C. psittaci and C. gallinacea infection, co-infection with pox virus was also noted (Karpińska et al. 2013). Stenzel et al. (2014) showed that two or three times as many pigeons are infected with C. psittaci and co-infected with pigeon circovirus (PiCV) as are infected with C. psittaci alone.

New Chlamydia Players in Birds

So far, the diagnosis and differentiation of Chlamydiaceae has been by the detection of the ompA gene using nested PCR. However, the external and internal oligonucleotide pairs of the nested PCR identify Chlamydia spp. according to the old four-species taxonomy and cannot differentiate between C. psittaci and C. abortus. The development of molecular assays has contributed to detection of new Chlamydia strains. Recently, a real-time PCR based on the enolase A (enoA) gene and the 16S rRNA target for the specific detection of new Chlamydiaceae (C. gallinacea and C. avium) was described (Zocevic et al. 2012, 2013). C. gallinacea with suspected zoonotic potential detected for the first time in domestic poultry in France (Laroucau et al. 2009). Then cases of new Chlamydia infection in chicken flocks from different European countries (France, Greece, Croatia, Poland, and Slovenia) as well as from China and Australia were noted (Robertson et al. 2010, Zocevic et al. 2012, 2013, Sachse et al. 2014). C. avium was detected in pigeons in Italy, France, and Germany (Gasparini et al. 2011, Sachse et al. 2014). Moreover, an infection with new Chlamydia was described in songbirds and waterfowl, although the strain was closely related to a recently found pigeon strain from France. A total of 11 new Chlamydia field strains have been isolated in the past decades in Germany, France, and Italy (Sachse et al. 2014). Phylogenetic analysis of ribosomal RNA and ompA genes and multilocus sequence analysis of these field isolates has shown the clustering of the strains into two different clades, i.e., one corresponding to pigeons and psittacine strains (C. avium) and a second one comprising the poultry strains (C. gallinacea).

So far, the pathogenic potential has not been elucidated, but it is possible that C. gallinacea and C. avium cause clinical symptoms in birds, for instance, in mixed infection with C. psittaci. Both new species can be transmitted by dust particles or feces. The zoonotic potential of C. avium is unknown but cannot be excluded and requires further study. Moreover, the zoonotic potential of C. gallinacea has been suggested by Laroucau et al. (2009) in her description of the clinical signs of atypical pneumonia observed in three workers in a French slaughterhouse outbreak. Further studies in the range of zoonotic transmission of new Chlamydia species should be focused on testing humans occupationally exposed to contact with breeding and wild birds. Diagnostic tools also need development, particularly in the range of serological methods, because the available enzyme-linked immunosorbent assay (ELISA) tests are only able to detect antibodies specific for C. psittaci. Currently, detection and identification of antibodies against C. gallinacea or C. avium are not possible either in birds or humans. It will be a very important scientific keystone to develop the serological tests that are the first line of study if the zoonotic potential of the new Chlamydia species is to be evaluated.

After detection of new avian Chlamydia players, a new area for researchers has opened up. The complex etiology of avian chlamydiosis and zoonotic risk should be reassessed.