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      Animal sources for zoonotic transmission of psittacosis: a systematic review

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          Abstract

          Background

          Human psittacosis, caused by Chlamydia (C.) psittaci, is likely underdiagnosed and underreported, since tests for C. psittaci are often not included in routine microbiological diagnostics. Source tracing traditionally focuses on psittacine pet birds, but recently other animal species have been gaining more attention as possible sources for human psittacosis. This review aims to provide an overview of all suspected animal sources of human psittacosis cases reported in the international literature. In addition, for each animal species the strength of evidence for zoonotic transmission was estimated.

          Methods

          A systematic literature search was conducted using four databases (Pubmed, Embase, Scopus and Proquest). Articles were included when there was mention of at least one human case of psittacosis and a possible animal source. Investigators independently extracted data from the included articles and estimated strength of evidence for zoonotic transmission, based on a self-developed scoring system taking into account number of human cases, epidemiological evidence and laboratory test results in human, animals, and the environment.

          Results

          Eighty articles were included, which provided information on 136 different situations of possible zoonotic transmission. The maximum score for zoonotic transmission was highest for turkeys, followed by ducks, owls, and the category ‘other poultry’. Articles reporting about zoonotic transmission from unspecified birds, psittaciformes and columbiformes provided a relatively low strength of evidence. A genotypical match between human and animal samples was reported twenty-eight times, including transmission from chickens, turkeys, guinea fowl, peafowl, pigeons, ducks, geese, songbirds, parrot-like birds and owls.

          Conclusions

          Strong evidence exists for zoonotic transmission from turkeys, chickens and ducks, in addition to the more traditionally reported parrot-like animal sources. Based on our scoring system, the evidence was generally stronger for poultry than for parrot-like birds. Psittaciformes should not be disregarded as an important source of human psittacosis, still clinicians and public health officials should include poultry and birds species other than parrots in medical history and source tracing.

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          Most cited references96

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          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.

          The current taxonomic classification of Chlamydia is based on limited phenotypic, morphologic and genetic criteria. This classification does not take into account recent analysis of the ribosomal operon or recently identified obligately intracellular organisms that have a chlamydia-like developmental cycle of replication. Neither does it provide a systematic rationale for identifying new strains. In this study, phylogenetic analyses of the 16S and 23S rRNA genes are presented with corroborating genetic and phenotypic information to show that the order Chlamydiales contains at least four distinct groups at the family level and that within the Chlamydiaceae are two distinct lineages which branch into nine separate clusters. In this report a reclassification of the order Chlamydiales and its current taxa is proposed. This proposal retains currently known strains with > 90% 16S rRNA identity in the family Chlamydiaceae and separates other chlamydia-like organisms that have 80-90% 16S rRNA relatedness to the Chlamydiaceae into new families. Chlamydiae that were previously described as 'Candidatus Parachlamydia acanthamoebae' Amann, Springer, Schönhuber, Ludwig, Schmid, Müller and Michel 1997, become members of Parachlamydiaceae fam. nov., Parachlamydia acanthamoebae gen. nov., sp. now. 'Simkania' strain Z becomes the founding member of Simkaniaceae fam. nov., Simkania negevensis gen. nov., sp. nov. The fourth group, which includes strain WSU 86-1044, was left unnamed. The Chlamydiaceae, which currently has only the genus Chlamydia, is divided into two genera, Chlamydia and Chlamydophila gen. nov. Two new species, Chlamydia muridarum sp. nov. and Chlamydia suis sp. nov., join Chlamydia trachomatis in the emended genus Chlamydia. Chlamydophila gen. nov. assimilates the current species, Chlamydia pecorum, Chlamydia pneumoniae and Chlamydia psittaci, to form Chlamydophila pecorum comb. nov., Chlamydophila pneumoniae comb. nov. and Chlamydophila psittaci comb. nov. Three new Chlamydophila species are derived from Chlamydia psittaci: Chlamydophila abortus gen. nov., sp. nov., Chlamydophila caviae gen. nov., sp. nov. and Chlamydophila felis gen. nov., sp. nov. Emended descriptions for the order Chlamydiales and for the family Chlamydiaceae are provided. These families, genera and species are readily distinguished by analysis of signature sequences in the 16S and 23S ribosomal genes.
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            Chlamydia psittaci (psittacosis) as a cause of community-acquired pneumonia: a systematic review and meta-analysis

            SUMMARY Psittacosis is a zoonotic infectious disease caused by the transmission of the bacterium Chlamydia psittaci from birds to humans. Infections in humans mainly present as community-acquired pneumonia (CAP). However, most cases of CAP are treated without diagnostic testing, and the importance of C. psittaci infection as a cause of CAP is therefore unclear. In this meta-analysis of published CAP-aetiological studies, we estimate the proportion of CAP caused by C. psittaci infection. The databases MEDLINE and Embase were systematically searched for relevant studies published from 1986 onwards. Only studies that consisted of 100 patients or more were included. In total, 57 studies were selected for the meta-analysis. C. psittaci was the causative pathogen in 1·03% (95% CI 0·79–1·30) of all CAP cases from the included studies combined, with a range between studies from 0 to 6·7%. For burden of disease estimates, it is a reasonable assumption that 1% of incident cases of CAP are caused by psittacosis.
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              Chlamydia psittaci: update on an underestimated zoonotic agent.

              Chlamydia (C.) psittaci is an economically relevant pathogen in poultry and pet birds, where it causes psittacosis/ornithosis, and also a human pathogen causing atypical pneumonia after zoonotic transmission. Despite its well-documented prevalence, the agent has received less attention by researchers than other Chlamydia spp. in the last decades. In the present paper, we review recently published data on C. psittaci infection and attempt to single out characteristic features distinguishing it from related chlamydial agents. It is remarkable that C. psittaci is particularly efficient in disseminating in the host organism causing systemic disease, which occasionally can take a fulminant course. At the cellular level, the pathogen's broad host cell spectrum (from epithelial cells to macrophages), its rapid entry and fast replication, proficient use of intracellular transport routes to mitochondria and the Golgi apparatus, the pronounced physical association of chlamydial inclusions with energy-providing cell compartments, as well as the subversive regulation of host cell survival during productive and persistent states facilitate the characteristic efficient growth and successful host-to-host spread of C. psittaci. At the molecular level, the pathogen was shown to upregulate essential chlamydial genes when facing the host immune response. We hypothesize that this capacity, in concert with expression of specific effectors of the type III secretion system and efficient suppression of selected host defense signals, contributes to successful establishment of the infection in the host. Concerning the immunology of host-pathogen interactions, C. psittaci has been shown to distinguish itself by coping more efficiently than other chlamydiae with pro-inflammatory mediators during early host response, which can, to some extent, explain the effective evasion and adaptation strategies of this bacterium. We conclude that thorough analysis of the large number of whole-genome sequences already available will be essential to identify genetic markers of the species-specific features and trigger more in-depth studies in cellular and animal models to address such vital topics as treatment and vaccination.
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                Author and article information

                Contributors
                lenny.hogerwerf@rivm.nl
                inge.roof@rivm.nl
                mariannedejong93@gmail.com
                frederika.dijkstra@rivm.nl
                wim.van.der.hoek@rivm.nl
                Journal
                BMC Infect Dis
                BMC Infect. Dis
                BMC Infectious Diseases
                BioMed Central (London )
                1471-2334
                4 March 2020
                4 March 2020
                2020
                : 20
                : 192
                Affiliations
                [1 ]ISNI 0000 0001 2208 0118, GRID grid.31147.30, Centre for Infectious Disease Control, , National Institute for Public Health and the Environment, ; Bilthoven, the Netherlands
                [2 ]ISNI 0000000120346234, GRID grid.5477.1, Faculty of Veterinary Medicine, , Utrecht University, ; Utrecht, the Netherlands
                Author information
                http://orcid.org/0000-0002-7173-0110
                Article
                4918
                10.1186/s12879-020-4918-y
                7057575
                32131753
                2d33c724-5ae1-49ef-abdc-d19517935568
                © The Author(s). 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 21 December 2018
                : 26 February 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001826, ZonMw;
                Award ID: 522001002
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100007192, Rijksinstituut voor Volksgezondheid en Milieu;
                Award ID: V/150207
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                Infectious disease & Microbiology
                psittacosis,chlamydia psittaci,zoonosis,animal sources,strength of evidence

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