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Chlamydia gallinacea and Chlamydia psittaci are intracellular bacteria belonging to the Chlamydiaceae family and are a cause of avian chlamydiosis in poultry. C. psittaci was considered the predominant chlamydial species in poultry until C. gallinacea was discovered in 2009. C. psittaci occurs worldwide, is zoonotic and has a wide host range. C. gallinacea is widespread in chickens, and infections appear asymptomatic, but reduced weight gain has been observed in broilers. Studies about the pathogenic potential of C. gallinacea are still limited, and any zoonotic potential has yet to be determined. The aim of this study was to gain insight into the prevalence of Chlamydia in Dutch chickens and to investigate the pathogenic potential of C. gallinacea. In a prevalence study, C. gallinacea was detected in around half of the 151 layer farms, but C. psittaci was not found. Subsequent research into the pathogenic potential of Dutch C. gallinacea strains showed that C. gallinacea mainly infects the mucosa of the chickens’ gut without causing clinical signs of inflammation. Finally, it was investigated whether a previous C. gallinacea infection in chickens could protect against a C. psittaci infection. This could explain why C. psittaci was not found during the field study in layers. However, protection against C. psittaci after a previous infection with C. gallinacea was not shown. In conclusion, Chlamydia infections in Dutch chickens cannot be considered a current One Health problem, but future introductions of C. psittaci cannot be excluded.

Psittacosis is a disease that can be transmitted from birds to humans and is caused by the intracellular bacterium Chlamydia psittaci. C. psittaci has been detected in more than 465 bird species and can cause clinical signs ranging from no symptoms to more severe symptoms such as conjunctivitis and pneumonia to liver failure and death. In humans, infection with C. psittaci can result in a flu-like illness and severe pneumonia, sometimes requiring hospitalisation. In the Netherlands, the disease is notifiable in humans and pet birds (except poultry). The number of human (40-70 per year) and veterinary (60-110 per year) notifications has been stable in recent years, but in 2019 there was a small increase in the number of human cases (91). The Netherlands Food and Consumer Product Safety Authority (NVWA) is responsible for the control in birds in the Netherlands, meaning the NVWA receives the notifications and carries out sampling. The owner of the birds is responsible for contacting a veterinarian to prescribe an antibiotic treatment. Two weeks after the treatment birds are retested. After treatment, birds regularly test positive with PCR, but the cause of these positive retests is unknown. In this report, existing NVWA dossiers were analysed to investigate which factors are associated with a positive retest after treatment. In total, 79 cases could be further analysed, of which 38 tested positive after the first treatment. Factors related to outdoor housing, possible outdoor contact and density appeared to be associated with a positive retest, although no strong relation was found. Additional research would be needed to confirm this relationship. In the data set, a large part of possible risk factors was missing, such as information related to treatment, housing, cleaning and disinfection. These factors could not be analysed. In addition, an improved treatment protocol for field cases was written based on existing literature. This protocol was used in one field case (autumn 2019). During this case study, it turned out that strict cleaning and disinfection is very difficult under field conditions. The analysis of the NVWA dossiers and the case study confirmed that bird husbandries are very diverse, with different types of housing and bird species. In addition, PCR results are sometimes difficult to interpret, as the presence of DNA is detected and not infectious C. psittaci bacteria, which requires a case-dependent approach. Overall, tailor-made advice is probably key in the control of psittacosis in pet birds. This report is the result of a research project within the statutory tasks of Wageningen Bioveterinary Research. This project aimed to improve the current control of psittacosis by evaluating information from available NVWA dossiers and systematically following up a number of field cases. In addition, antibiotic residues in bird feces were investigated. This information is not included in this report but will be reported to the Ministry of Agriculture, Nature and Food Quality via the usual reports. Psittacose is een ziekte die van vogels op mensen kan worden overgedragen en wordt veroorzaakt door de intracellulaire bacterie Chlamydia psittaci. C. psittaci is bij meer dan 465 vogelsoorten aangetoond en kan in vogels tot een variabel ziektebeeld leiden, variërend van geen verschijnselen tot meer ernstige verschijnselen als oog- en longontsteking of leverfalen en sterfte. Bij mensen kan een infectie met C. psittaci aanleiding geven tot een griepachtig beeld en ernstige longontsteking, waarbij ziekenhuisopname soms noodzakelijk is. De ziekte is in Nederland bij gehouden gezelschapsvogels (uitgezonderd pluimvee) en bij mensen meldingsplichtig. Bij vogels geldt ook een bestrijdingsplicht. Het aantal veterinaire (60-110 per jaar) en humane meldingen (40-70 per jaar) is de laatste jaren stabiel, maar in 2019 werd een kleine toename van het aantal humane gevallen (91) gezien. De Nederlandse Voedsel- en Warenautoriteit (NVWA) is in Nederland verantwoordelijk voor de bestrijding in vogels. Dit houdt in dat de NVWA de meldingen ontvangt en de bemonstering van de vogels uitvoert. De eigenaar van de vogels is verantwoordelijk om een dierenarts in te schakelen voor het voorschrijven van een antibioticum behandeling. De controle hierop vindt plaats door vogels twee weken na afloop van de behandeling opnieuw te testen. Regelmatig testen vogels na behandeling opnieuw positief (met PCR). De oorzaak hiervan is niet duidelijk. In dit rapport is daarom een verzameling van bestaande NVWA dossiers geanalyseerd om te onderzoeken welke factoren een rol spelen bij het herhaaldelijk positief testen. In totaal zijn 79 casussen geanalyseerd, waarvan 38 na de eerste antibiotica behandeling opnieuw positief testten. Factoren met betrekking tot buiten huisvesting, mogelijk contact met buiten en bezetting per verblijf leken geassocieerd te zijn met een positieve hertest, hoewel er geen sterke relatie is gevonden in dit onderzoek. Dit zou met aanvullend onderzoek verder bestudeerd kunnen worden. Een groot deel van de mogelijke risicofactoren ontbrak in deze dataset, zoals informatie met betrekking tot behandeling, huisvesting, reiniging en desinfectie. Deze factoren konden niet geanalyseerd worden. Daarnaast is op basis van bestaande literatuur een verbeterd behandelprotocol voor casussen in de praktijk opgesteld. Dit protocol is bij één veldcasus gebruikt (najaar 2019). Tijdens deze casus bleek dat het zeer lastig is om een strikte reiniging en desinfectie uit te voeren onder praktijkomstandigheden. Zowel de veldcasus als de analyse van de NVWA dossiers, laten zien dat de vogelhouderij een diverse sector is, met diverse typen huisvesting en vogelsoorten. Daarnaast blijken PCR uitslagen soms lastig te interpreteren, omdat de aanwezigheid van DNA wordt aangetoond en niet het aantal infectieuze C. psittaci bacteriën, waardoor de beoordeling sterk casus-afhankelijk is. Advies op maat lijkt daarom het sleutelwoord te zijn in de aanpak van psittacose bij gezelschapsvogels. Dit rapport komt voort uit een onderzoeksproject binnen de wettelijke taken van Wageningen Bioveterinary Research (WBVR). Het project is een samenwerking van WBVR met NVWA, WFSR (Wageningen Food Safety Research) en de Faculteit Diergeneeskunde van de Universiteit Utrecht. Naast de evaluatie van de bestrijding, is onderzoek gedaan naar antibioticumresiduen in vogelontlasting. Deze informatie is niet in dit rapport opgenomen, maar wordt wel teruggekoppeld via de gebruikelijke halfjaarlijkse rapportages aan het ministerie van Landbouw, Natuur en Voedselkwaliteit.

Chlamydia gallinacea is an obligate intracellular bacterium that has recently been added to the family of Chlamydiaceae. C. gallinacea is genetically diverse, widespread in poultry and a suspected cause of pneumonia in slaughterhouse workers. In poultry, C. gallinacea infections appear asymptomatic, but studies about the pathogenic potential are limited. In this study two novel sequence types of C. gallinacea were isolated from apparently healthy chickens. Both isolates (NL_G47 and NL_F725) were closely related to each other and showed 99.1% DNA sequence identity to C. gallinacea Type strain 08-1274/3. To gain further insight in the pathogenic potential, infection experiments in embryonated chicken eggs and comparative genomics with Chlamydia psittaci were performed. C. psittaci is an ubiquitous zoonotic pathogen of birds and mammals, and infection in poultry can result in severe systemic illness. In experiments with embryonated chicken eggs C. gallinacea induced mortality was observed, potentially strain dependent but lower compared to C. psittaci induced mortality. Comparative analyses confirmed all currently available C. gallinacea genomes possess the hallmark genes coding for known and potential virulence factors as found in C. psittaci albeit to a reduced number of orthologues or paralogs. The presence of (potential) virulence factors and the observed mortality in embryonated eggs indicates C. gallinacea should rather be considered as a (conditional) pathogen than an innocuous commensal.ImportanceChlamydiaceae are a family of bacteria comprising human and animal pathogens including the recently recognized Chlamydia gallinacea. C. gallinacea is widespread in poultry without causing clinical signs, which raises questions about its pathogenic potential. To assess this potential, two novel C. gallinacea strains were isolated, tested in infection experiments in embryonated chicken eggs and compared to C. psittaci. C. psittaci infection in poultry can result in severe systemic illness, depending on the conditions, and infections can be transmitted to humans. In the experiments C. gallinacea infection induced mortality of the embryo, but to a lower extent than infection with C. psittaci. Subsequent genome comparisons confirmed both C. gallinacea strains possess potential virulence genes typical for chlamydia, but fewer than C. psittaci. These results indicate C. gallinacea does have a pathogenic potential which warrants further research to elucidate its role as a poultry pathogen.

Recent reports highlight a growing awareness of the potential for Chlamydia considered to be traditionally veterinary pathogens to cause cases of community-acquired pneumonia in humans. Cases of Chlamydia caviae, a guinea pig pathogen, were detected in individuals with serious pneumonia requiring hospitalisation. Source tracking linked these infections to pet guinea pigs. Studies of horses have found that the avian and zoonotic pathogen, Chlamydia psittaci, may be more common in these mammalian hosts, further highlighting the risk of exposure to chlamydial causes of CAP. The realisation that CAP can be caused by a broader range of chlamydial agents highlights the need for better collaboration between primary care physicians, public health officials and veterinarians. In a Dutch model for this approach, surveillance of veterinary chlamydiae as a cause of CAP has been improved through harmonisation of detection and molecular typing methods to facilitate an easier exchange of detection and molecular typing data to support source tracking efforts by public health and veterinary authorities.

SUMMARYIn July 2013, a Belgian couple were admitted to hospital because of pneumonia. Medical history revealed contact with birds. Eleven days earlier, they had purchased a lovebird in a pet shop in The Netherlands. The bird became ill, with respiratory symptoms. The couple's daughter who accompanied them to the pet shop, reported similar symptoms, but was travelling abroad. On the suspicion of psittacosis, pharyngeal swabs from the couple were taken and sent to the Belgian reference laboratory for psittacosis. Culture and nested polymerase chain reaction (PCR) tests were positive for the presence ofChlamydia psittaci, andompAgenotyping indicated genotype A in both patients. The patients were treated with doxycycline and the daughter started quinolone therapy; all three recovered promptly. Psittacosis is a notifiable disease in Belgium and therefore local healthcare authorities were informed. They contacted their Dutch colleagues, who visited the pet shop. Seven pooled faecal samples were taken and analysed using PCR by the Dutch national reference laboratory for notifiable animal diseases for the presence ofChlamydia psittaci.Four (57%) samples tested positive, genotyping revealed genotype A. Enquiring about exposure to pet birds is essential when patients present with pneumonia. Reporting to health authorities, even across borders, is warranted to prevent further spread.

The gram-negative intracellular bacteria C. caviae was identified as the likely cause of severe community-acquired pneumonia in three patients. Guinea pigs were the likely source.