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An Experimentally Induced Chlamydia Suis Infection in Pigs Results In An experimentally induced Chlamydia suis infection in pigs results in severe lung function disorders and pulmonary inflammation Petra Reinhold, Nathalie Kirschvink, Dirk Theegarten, Angela Berndt To cite this version: Petra Reinhold, Nathalie Kirschvink, Dirk Theegarten, Angela Berndt. An experimentally induced Chlamydia suis infection in pigs results in severe lung function disorders and pulmonary inflammation. Veterinary Research, BioMed Central, 2008, 39 (3), pp.1. 10.1051/vetres:2008012. hal-00902933 HAL Id: hal-00902933 https://hal.archives-ouvertes.fr/hal-00902933 Submitted on 1 Jan 2008 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Vet. Res. (2008) 39:35 www.vetres.org DOI: 10.1051/vetres:2008012 C INRA, EDP Sciences, 2008 Original article An experimentally induced Chlamydia suis infection in pigs results in severe lung function disorders and pulmonary inflammation Petra Reinhold1*, Nathalie Kirschvink2,DirkTheegarten3, Angela Berndt1 1 Institute of Molecular Pathogenesis at the Friedrich-Loeffler-Institute, Federal Research Institute for Animal Health, Naumburger Str. 96a, 07743 Jena, Germany 2 Animal Physiology, Department of Veterinary Medicine, Faculty of Sciences, University of Namur, 61 rue de Bruxelles, 5000 Namur, Belgium 3 Institute of Pathology and Neuropathology, University Hospital Essen, University of Duisburg-Essen, Hufelandstrasse 55, 45122 Essen, Germany (Received 31 October 2007; accepted 22 February 2008) Abstract – This study was aimed at evaluating the pathophysiology of pulmonary dysfunctions and inflammatory consequences of an acute respiratory chlamydial infection induced experimentally in conventionally raised pigs (aged 39–44 days). Eight animals were exposed to Chlamydia suis (C. suis) and four non-infected animals served as controls. The total observation period was from seven days before challenge to seven days post exposure. While non-infected control pigs did not exhibit any clinical symptoms, animals exposed to C. suis developed fever and were severely respiratory distressed within the first week after exposure. After C. suis infection, pulmonary dysfunctions were characterised by a significant decrease in the diffusion capacity of the lung (i.e. transfer factor of the lung for carbon monoxide; TL CO), a significant increase in the functional residual capacity (FRC), and significant changes in the pattern of ventilation (respiratory rate increased while the tidal volume decreased). In exhaled breath condensate (EBC), leukotriene B4 (LTB4) and interleukin 6 (IL-6) showed a tendency to increase after infection. In the broncho-alveolar lavage fluid (BALF) of C. suis infected pigs, the activity of matrix metalloprotease 9 (MMP-9) was found to be increased compared to controls. BALF cytology was characterised by increased numbers of granulocytes and activated lymphocytes. Pulmonary inflammation in infected pigs was confirmed by post mortem histology. A prominent dissemination of chlamydial bodies in the lung was accompanied by an influx of macrophages, granulocytes and activated T-cells. Data obtained in this study provide new insight into the pathogenesis of acute respiratory chlamydial infections in pigs. Chlamydia suis model / pulmonary inflammation / lung functions / exhaled breath condensate (EBC) / BALF 1. INTRODUCTION clinically normal swine herds [4, 5, 10, 41] and relatively few reports of acute clinical The impact of Chlamydiaceae on animal illness. Chlamydial infections in sows have health on pig farms is controversial because been associated with reproductive disorders, an inconsistency seems to exist between the the occurrence of MMA-syndrome (mastitis, obviously high prevalence of chlamydiae in metritis, agalactia), or perinatal mortality in piglets, and detection of chlamydiae in semen * Corresponding author: petra.reinhold@fli.bund.de of boars suggests a potential for venereal Article available at http://www.vetres.org or http://dx.doi.org/10.1051/vetres:2008012 Vet. Res. (2008) 39:35 P. Reinhold et al. transmission [5, 15, 16]. In addition, there is 2. MATERIALS AND METHODS some data that chlamydioses in swine can be 2.1. Animals associated with enteritis, pneumonia, conjunc- tivitis, and pericarditis [22]. The knowledge Twelve colostrum-fed Deutsche Landrasse about the involvement of Chlamydiaceae in female pigs, conventionally raised on a farm the porcine respiratory disease complex is with no animals being bought from outside, were still limited and reports in the literature are provided by Charles River (Sulzfeld, Germany). At 3–4 weeks of age, they were brought into the very inconsistent. While lung function was not animal house of the institute. They were included affected in symptom-free pigs with a naturally in the study after a quarantine period of at least ten acquired presence of chlamydiae in the respi- days and confirmation of their clinically healthy ratory system [32], a clear pathogenic potential status. Throughout the entire study, they were of Chlamydia species for the porcine respi- housed in conformity with the guidelines for ratory system has been proven experimen- animal welfare. Feeding was twice a day with a tally [32, 35]. commercially available nutrition they received on According to current taxonomy, Chlamydia the breeding farm. Water was supplied ad libitum. suis (C. suis), i.e. the former porcine serovar None of the feed contained antibiotics. The animals of C. trachomatis, has been identified as were kept in three groups, each consisting of four the major agent causing chlamydioses in animals and housed separately. swine [22]. However, there appears to be a high prevalence of mixed infections with 2.2. Study design C. abortus making it difficult to attribute clini- At the age of 39–44 days, eight animals were cal pathology to C. suis alone [10]. In order to exposed to C. suis and four non-infected animals evaluate the aetiological importance of C. suis, served as controls. Each pig inhaled 35–40 L of an experimental challenge model of aerosol aerosol produced either from 1.0 mL of chlamydia infection was established by our group [38]. cell culture containing 109 IFU per mL (strain In contrast to the model described by Rogers DC6) or from non-infected culture. Aerosol was et al. [35] where three day old gnotobiotic administered to each pig individually over a period piglets were found to be susceptible to respira- of 10–15 min. Details about aerosol production, tory chlamydial infection, the pigs challenged aerosol administration and origin of the C. suis in our model were conventionally raised, older strain DC6 have been described previously [38]. (approximately six weeks), and had even a Daily clinical observation focussed on feed positive carrier status for chlamydiae [38]. intake, rectal temperature, respiratory rate and symptoms of diarrhoea or respiratory disorders, i.e. Despite lower infection dosages compared to cough, nasal discharge or ocular secretions. Within the model described by Rogers et al. [35], they a period ranging from seven days before challenge responded to the aerosol challenge of C. suis up to seven days after challenge, i.e. days post with acute phase reactions, severe clinical infection (dpi), pulmonary function tests, collection signs and significant increases of chlamydia- of blood samples and collection of exhaled breath specific antibody titres [38]. Additionally, condensate were performed as described below. the present study was undertaken in order to A number was assigned to each pig. The tests clarify pathophysiological consequences of each animal underwent are shown in Table I. Body C. suis challenge particularly for the porcine weight was measured individually prior to each respiratory system. Thus, (i) variables of lung function test. The pigs were euthanised for lung function, (ii) markers of pulmonary necropsy at different time points (Tab. I). The study inflammation measurable in exhaled breath, had ethical approval by the Commission for the broncho-alveolar lavage fluid and on the Protection of Animals of the state of Thuringia. cellular level, and (iii) immunohistochemical findings, as well as results of flow cytometric 2.3. Protocol of pulmonary function testing analysis, were evaluated in vivo and post Pulmonary functions were evaluated using mortem. MasterScreen Diffusion (Viasys Healthcare, Page2of19(page number not for citation purpose) Pulmonary dysfunctions caused by Table I. Study design. Animal −7d −2d +3 dpi +4 dpi +5 dpi +6 dpi +7 dpi +8 dpi +10 dpi +11 dpi +17 dpi +24 dpi +25 dpi number before before Chlamydia 1 Necropsy* 2 Necropsy 3 Necropsy* 4 Necropsy* 5 EBC PFT PFT, EBC PFT, EBC PFT, EBC Necropsy* 6 EBC PFT PFT, EBC PFT, EBC PFT, EBC Necropsy ( page number not for citation purpose 7 EBC PFT PFT, EBC PFT, EBC PFT, EBC Necropsy* 8 EBC PFT PFT, EBC PFT, EBC PFT, EBC Necropsy* C9 EBC PFT PFT, EBC Necropsy* C10 EBC PFT PFT, EBC PFT, EBC Necropsy* C11 EBC PFT PFT, EBC PFT, EBC Necropsy* C12 EBC PFT PFT, EBC PFT, EBC Necropsy* Animal numbers 1–8: challenged with C. suis. Animal numbers C9–C12: non-infected controls. dpi:
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