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Genital Tract Lesions in Sexually Mature Göttingen Minipigs During The Erneholm et al. BMC Veterinary Research (2016) 12:200 DOI 10.1186/s12917-016-0793-6 RESEARCH ARTICLE Open Access Genital tract lesions in sexually mature Göttingen minipigs during the initial stages of experimental vaginal infection with Chlamydia trachomatis serovar D Karin Erneholm1,2,3*, Emma Lorenzen1,2, Sarah Bøje1,2,4, Anja Weinreich Olsen2, Peter Andersen2, Joseph P. Cassidy5, Frank Follmann2, Henrik E. Jensen6 and Jørgen S. Agerholm1 Abstract Background: Chlamydia is one of the most common sexually transmitted diseases in humans worldwide, causing chronic lesions in the reproductive tract. Due to its often asymptomatic course, there is limited knowledge about the initial changes in the genital tract following infection. This study employs a novel sexually mature minipig model to investigate the initial histopathological changes following vaginal infection with Chlamydia trachomatis serovar D. Results: A vaginal inoculation resulted in an infection primarily affecting the lower genital tract. The histopathological changes were characterized by a subepithelial inflammation consisting of neutrophils and mononuclear cells, followed by an increase in the number of plasma cells within the sub-epithelial stroma of the vagina. Detection of Chlamydia was associated with expression of cyclooxygenase-2 and interleukin-8 by superficial epithelial cells. The infection was self-limiting, with a duration of 7 days. Conclusion: Neutrophils, plasma cells and IL-8 have been linked with Chlamydia genital infection of unknown duration in human patients. In this study, we observe a similar pattern of local immune response/inflammation following experimental inoculation suggesting this porcine model shows promise as a model for translational chlamydia research. Keywords: Chlamydia, Sexually mature, Pig model, Porcine, Genital tract, Initial lesions Background studies of Chlamydia infections and in particular using Chlamydia is one of the most common sexually trans- the mouse pathogen, Chlamydia muridarum [4]. Models mitted infections in humans, with more than 100 million based on non-human primates (NHPs) are in general new cases per year [1]. Genital infection with Chlamydia more comparative to humans than rodent models. trachomatis (C. trachomatis) in women can lead to long Different studies, reviewed by Bell et al., have shown that term sequelae such as infertility, chronic pelvic pain and a genital infection with C. trachomatis in NHPs elicits in worst case life threatening complications, e.g. ectopic histological changes in the mucosa of the vagina, cervix pregnancy [2]. Our understanding of the pathogenesis of and the oviducts, resembling the inflammatory response acute C. trachomatis infection in the genital tract of in humans [5]. However, pigs are increasingly being used women is limited because the majority are asymptomatic as models for the study of human diseases as they are [3]. Murine models are often used for translational less expensive and more accessible laboratory animals than NHPs. Moreover, compared with rodents, porcine * Correspondence: [email protected] physiology and the porcine immune system are more 1Section of Veterinary Reproduction and Obstetrics, Department of Large comparable to humans [6–8]. Also, with respect to Animal Sciences, Faculty of Health and Medical Sciences, University of reproductive biology porcine models are preferred, as Copenhagen, Frederiksberg C, Denmark 2Department of Infectious Disease Immunology, Statens Serum Institut, pigs are polyoestrous with a cycle length of 21 days; Copenhagen S, Denmark compared to a 5 day murine cycle [9]. Furthermore, the Full list of author information is available at the end of the article © 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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. Erneholm et al. BMC Veterinary Research (2016) 12:200 Page 2 of 11 porcine vagina is suitable for both in vitro and in vivo after which the media was enriched with 0.5 % glucose studies due to the similarities between its structure and and 1 μg/ml cyclohexamide. The plates were incubated function with that in women [10, 11]. The use of pigs at 37 °C for 48 h, and thereafter harvested and purified for experimental Chlamydia studies has been reported as described by Olsen et al. [27]. in a single study of a primary genital C. trachomatis The concentration of infectious bacteria was deter- infection, and in three vaccine studies [12–15]. In these mined by culturing bacterial suspensions on McCoy- studies, prepubertal gilts were used. No systematic cells [28]. The plates were incubated at 37 °C for 22 h. evaluations of histological changes have been reported Visualization of inclusions was made by incubating the for early stages of infection in pigs or NHPs. cells with polyclonal rabbit antibodies against chlamydial In humans, genital Chlamydia infection most often Major Outer Membrane Protein and chlamydial Heat occurs in sexually mature adolescents [16]. The sexually Shock Protein-60 [29], and thereafter stained with 4 μg/ mature genital tract differs from the immature tract, in ml Alexa Fluor 488 labelled goat-anti rabbit antibody size, epithelial thickness, vascularization, immune cell (Life Technologies) and kept in the dark at 4 °C until infiltration and hormonal fluctuation [17–20]. Given that microscopy was carried out. hormones influence the susceptibility of endometrial cells The cell plates were evaluated using a fluorescent to chlamydial infection [21, 22], sexually mature pigs microscope (Olympus IX71). Inclusion bodies were should constitute a good model for the human disease. enumerated by counting positively stained inclusions in In this study, we investigated the histopathological and at least 20 fields in each well using the 40x objective on immunological changes in the initial stages of infection microscope. Results were calculated as average of with C. trachomatis serovar D (SvD) in sexually mature duplicate samples. Göttingen minipigs, acting as a model of human genital chlamydia. The characterization included immunohis- Experimental animals tochemical staining of cyclooxygenase-2 (cox-2), a key Ten 7 to 8 month old sexually mature female Göttingen enzyme for prostaglandin synthesis in the early inflamma- minipigs were raised in a barrier facility at Ellegaard tory response in both pigs and humans, and interleukin-8 Göttingen Minipigs A/S, Dalmose, Denmark, declared free (IL-8), which has a similar function as proinflammatory of Chlamydia infection and a number of other infections cytokine and neutrophil chemoattractant in both pigs and as documented by a FELASA-approved health monitoring humans, and is additionally known to be upregulated report. The experimental study was performed in the following C. trachomatis infection [23–26]. Laboratory Animal Isolation Unit at the University of Copenhagen. The gilts were housed in groups of 3–4with wooden shavings as bedding material, fed twice daily with Methods standard minipig diet and had ad libitum access to water. Chlamydia trachomatis In addition, genital tracts were also obtained as histologic C. trachomatis SvD (Trachoma type D strain UW-3/Cx, control tissue from six age-matched gilts, raised at the ATCC® VR-885™) was propagated in HeLa cells as same facility as the experimental animals. previously described [27]. Briefly, the HeLa cells were cultured in six well plates and infected with 1.5 C. Study design trachomatis SvD inclusion forming units (IFU) per HeLa The study design is illustrated in Fig. 1. The gilts were cell. The infection was followed by centrifugation at treated orally for 18 days (20 mg/day) with a progesta- 750 g for 1 h, and thereafter incubated at 35 °C for 2 h, gen (Regumate Equine®, MSD Animal Health, Ballerup, Fig. 1 Experimental design. Ten sexually mature minipigs were intravaginally inoculated with C. trachomatis at oestrus. The pigs were euthanised and sampled on day 3, 5 and 7 post inoculation (PI). As controls for the histological stainings, genital organs from six age-matched, healthy, non-treated gilts were also included (not shown in the figure) Erneholm et al. BMC Veterinary Research (2016) 12:200 Page 3 of 11 Denmark) to synchronize their oestrus cycles and then knowledge of experimental treatment. The phase of the evaluated daily for signs of oestrus. When characteristic oestrous cycle was determined as “peri-oestrus” (ranging signs of oestrus were evident, such as vulvar erythema, from pro-oestrus to early di-oestrus) or “dioestrus”, based oedema, and increased physical activity (4–5 days after on histological changes in the uterine horns; Peri-oestrus discontinuation of treatment), the pigs were anaesthe- if the epithelium was pseudostratified, subbasilary bands tized with Zoletil-50® mixture [30] intramuscularly. of neutrophils were found, and apoptotic cells were Chlamydial inoculation was performed under sterile detected in the endometrial and/or glandular epithelium, conditions using an insemination catheter (Osiris, E-vet, and dioestrus if no apoptotic cells
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