{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,24]],"date-time":"2025-11-24T19:42:44Z","timestamp":1764013364675,"version":"3.45.0"},"reference-count":126,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2025,11,24]],"date-time":"2025-11-24T00:00:00Z","timestamp":1763942400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100015471","name":"Department of Agriculture, Water and the Environment, Australian Government","doi-asserted-by":"publisher","award":["GA189662"],"award-info":[{"award-number":["GA189662"]}],"id":[{"id":"10.13039\/501100015471","id-type":"DOI","asserted-by":"publisher"}]},{"name":"WIRES NSW","award":["IRMA 208595"],"award-info":[{"award-number":["IRMA 208595"]}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p>\n                    Several infectious agents concurrently infect wild koalas and so, as for similar agents in other species, co-infection interactions could affect disease presentation and clinical outcomes. This study determines the frequency of circulating and mucosal\n                    <jats:italic>Chlamydia pecorum<\/jats:italic>\n                    infections along with phascolarctid herpesvirus (PhaHV), Koala retrovirus (KoRV), and trypanosome infections in 115 wild koalas admitted to wildlife hospitals in the Australian states of Queensland and New South Wales.\n                    <jats:italic>C. pecorum,<\/jats:italic>\n                    PhaHV, trypanosomes, and KoRV (endogenous subtype A and exogenous subtype D) were detected in 61.1%, 68.9%, 63.3% and 100% of the individuals sampled, respectively. The co-infection relationships identified generate hypotheses for the observed variation in disease presentations in that they resemble co-infection interactions that drive the variations in presentation and response to treatment for chlamydiosis in other species, including humans. Among koalas with chlamydiosis, PhaHV-1 mucosal shedding positively predicted euthanasia on admission, and accounting for\n                    <jats:italic>Trypanosome irwini<\/jats:italic>\n                    infection status improved the model quality. Additionally, in female koalas, the detection of mucosal PhaHV-1 and greater KoRV proviral\n                    <jats:italic>pol<\/jats:italic>\n                    loads were equal predictors of chlamydial reproductive disease. While the detection frequency of\n                    <jats:italic>C. pecorum,<\/jats:italic>\n                    PhaHV-1, PhaHV-2, and\n                    <jats:italic>T. gilletti<\/jats:italic>\n                    in circulation were low, cases with circulating\n                    <jats:italic>C. pecorum<\/jats:italic>\n                    and without mucosal\n                    <jats:italic>C. pecorum<\/jats:italic>\n                    shedding or clinical chlamydiosis were observed presenting an important consideration for future diagnostic testing. This study serves as a basis for investigating co-infection interaction pathways through mechanistic studies to determine their effect on pathogenesis of chlamydiosis, improve our understanding of host-pathogen-environment dynamics impacting the koala, and identify novel intervention and screening methods.\n                  <\/jats:p>","DOI":"10.1371\/journal.ppat.1013632","type":"journal-article","created":{"date-parts":[[2025,11,24]],"date-time":"2025-11-24T18:25:21Z","timestamp":1764008721000},"page":"e1013632","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["The relationships of viral and protozoal co-infections to Chlamydia pecorum infection and chlamydiosis outcomes in northern koalas (Phascolarctos cinereus)"],"prefix":"10.1371","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0009-0009-2289-6956","authenticated-orcid":true,"given":"Yasmine S. S.","family":"Muir","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Belinda R.","family":"Wright","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andrea","family":"Casteriano","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mathew S.","family":"Crowther","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Amber","family":"Gillett","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mark B.","family":"Krockenberger","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1215-6523","authenticated-orcid":true,"given":"Damien P.","family":"Higgins","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2025,11,24]]},"reference":[{"issue":"9","key":"ppat.1013632.ref001","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0162207","article-title":"Phylogeography of the Koala, (Phascolarctos cinereus), and Harmonising Data to Inform Conservation","volume":"11","author":"LE Neaves","year":"2016","journal-title":"PLoS One"},{"issue":"2","key":"ppat.1013632.ref002","doi-asserted-by":"crossref","first-page":"301","DOI":"10.7589\/2015-05-120","article-title":"Prevalence and pathologic features of chlamydia pecorum infections in south australian koalas (phascolarctos cinereus)","volume":"52","author":"KN Speight","year":"2016","journal-title":"J Wildl Dis"},{"key":"ppat.1013632.ref003","unstructured":"DCCEEW. Koala listing under national environmental law. https:\/\/www.dcceew.gov.au\/environment\/biodiversity\/threatened\/species\/koalas\/listing-under-national-environmental-law#:~:text=The%20koala%20(combined%20populations%20of,have%20any%20impacts%20to%20koalas 2022."},{"key":"ppat.1013632.ref004","unstructured":"Deh NG. Wildlife rehabilitation data dashboard. https:\/\/www2.environment.nsw.gov.au\/topics\/animals-and-plants\/native-animals\/rehabilitating-native-animals\/wildlife-rehabilitation-data-and-reporting\/wildlife-rehabilitation-data-dashboard. 2022."},{"issue":"1","key":"ppat.1013632.ref005","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1071\/WR21181","article-title":"Insights and inferences on koala conservation from records of koalas arriving to care in South East Queensland","volume":"50","author":"DH Kerlin","year":"2022","journal-title":"Wildl Res"},{"issue":"5","key":"ppat.1013632.ref006","first-page":"632","article-title":"Association of uterine and salpingeal fibrosis with chlamydial hsp60 and hsp10 antigen-specific antibodies in Chlamydia-infected koalas","volume":"12","author":"DP Higgins","year":"2005","journal-title":"Clin Diagn Lab Immunol"},{"key":"ppat.1013632.ref007","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.theriogenology.2021.03.016","article-title":"The effect of Chlamydia infection on koala (Phascolarctos cinereus) semen quality","volume":"167","author":"L Hulse","year":"2021","journal-title":"Theriogenology"},{"key":"ppat.1013632.ref008","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.theriogenology.2021.12.011","article-title":"Investigation of pathology associated with Chlamydia pecorum infection in the male reproductive tract, and the effect on spermatogenesis and semen quality in the koala (Phascolarctos cinereus)","volume":"180","author":"L Hulse","year":"2022","journal-title":"Theriogenology"},{"issue":"6","key":"ppat.1013632.ref009","doi-asserted-by":"crossref","first-page":"1254","DOI":"10.1177\/0300985815570069","article-title":"Orchitis and Epididymitis in Koalas (Phascolarctos cinereus) Infected With Chlamydia pecorum","volume":"52","author":"SD Johnston","year":"2015","journal-title":"Vet Pathol"},{"issue":"2","key":"ppat.1013632.ref010","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1177\/0300985818806963","article-title":"Chlamydia pecorum Infection in the Male Reproductive System of Koalas ( Phascolarctos cinereus)","volume":"56","author":"C Palmieri","year":"2019","journal-title":"Vet Pathol"},{"issue":"9","key":"ppat.1013632.ref011","doi-asserted-by":"crossref","first-page":"1140","DOI":"10.3390\/pathogens10091140","article-title":"Is Chlamydia to Blame for Koala Reproductive Cysts?","volume":"10","author":"S Phillips","year":"2021","journal-title":"Pathogens"},{"key":"ppat.1013632.ref012","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1016\/j.theriogenology.2022.06.022","article-title":"Chlamydiosis and cystic dilatation of the ovarian bursa in the female koala (Phascolarctos cinereus): Novel insights into the pathogenesis and mechanisms of formation","volume":"189","author":"S Pagliarani","year":"2022","journal-title":"Theriogenology"},{"key":"ppat.1013632.ref013","unstructured":"NSW Government. Code of Practice for Injured Sick and Orphaned Koalas. (EHG20230250).2023 https:\/\/www.environment.nsw.gov.au\/research-and-publications\/publications-search\/code-of-practice-for-injured-sick-and-orphaned-koalas"},{"key":"ppat.1013632.ref014","article-title":"Code of Practice: Care of Sick, Injured or Orphaned Protected Animals Nature Conservation Act 1992","author":"WTOB","year":"2020"},{"issue":"1","key":"ppat.1013632.ref015","article-title":"Neisseria gonorrhoeae drives Chlamydia trachomatis into a persistence-like state during in vitro co-infection","volume":"92","author":"LM Ball","year":"2024","journal-title":"Infect Immun"},{"issue":"8","key":"ppat.1013632.ref016","doi-asserted-by":"crossref","first-page":"4366","DOI":"10.3934\/dcdsb.2023019","article-title":"Dynamics of herpes and chlamydia co-infection in a population","volume":"28","author":"B Das","year":"2023","journal-title":"DCDS-B"},{"issue":"9","key":"ppat.1013632.ref017","doi-asserted-by":"crossref","first-page":"1954","DOI":"10.3390\/v15091954","article-title":"When Bacteria and Viruses Collide: A Tale of Chlamydia trachomatis and Sexually Transmitted Viruses","volume":"15","author":"E Ghasemian","year":"2023","journal-title":"Viruses"},{"issue":"1","key":"ppat.1013632.ref018","doi-asserted-by":"crossref","first-page":"1030","DOI":"10.1038\/s41467-022-28569-1","article-title":"Modelling Chlamydia and HPV co-infection in patient-derived ectocervix organoids reveals distinct cellular reprogramming","volume":"13","author":"S Koster","year":"2022","journal-title":"Nat Commun"},{"key":"ppat.1013632.ref019","doi-asserted-by":"crossref","first-page":"180","DOI":"10.3389\/fcimb.2017.00180","article-title":"Productive and Penicillin-Stressed Chlamydia pecorum Infection Induces Nuclear Factor Kappa B Activation and Interleukin-6 Secretion In Vitro","volume":"7","author":"CA Leonard","year":"2017","journal-title":"Front Cell Infect Microbiol"},{"issue":"9","key":"ppat.1013632.ref020","doi-asserted-by":"crossref","first-page":"862","DOI":"10.3390\/medicina57090862","article-title":"Proinflammatory and Oxidative Stress States Induced by Human Papillomavirus and Chlamydia trachomatis Coinfection Affect Sperm Quality in Asymptomatic Infertile Men","volume":"57","author":"E P\u00e9rez-Soto","year":"2021","journal-title":"Medicina (Kaunas)"},{"issue":"10","key":"ppat.1013632.ref021","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0047427","article-title":"Imbalanced oxidative stress causes chlamydial persistence during non-productive human herpes virus co-infection","volume":"7","author":"BK Prusty","year":"2012","journal-title":"PLoS One"},{"key":"ppat.1013632.ref022","first-page":"159","article-title":"Chlamydia trachomatis as the Cause of Infectious Infertility: Acute, Repetitive or Persistent Long-Term Infection?","volume":"412","author":"L Schuchardt","year":"2018","journal-title":"Curr Top Microbiol Immunol"},{"issue":"10","key":"ppat.1013632.ref023","doi-asserted-by":"crossref","DOI":"10.1128\/IAI.00254-21","article-title":"Chlamydia Spreads to the Large Intestine Lumen via Multiple Pathways","volume":"89","author":"Z Zhou","year":"2021","journal-title":"Infect Immun"},{"issue":"2","key":"ppat.1013632.ref024","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1128\/IAI.00691-06","article-title":"Therapeutic Chlamydophila abortus and C. pecorum vaccination transiently reduces bovine mastitis associated with Chlamydophila infection","volume":"75","author":"C Biesenkamp-Uhe","year":"2007","journal-title":"Infect Immun"},{"key":"ppat.1013632.ref025","doi-asserted-by":"crossref","unstructured":"Poudel A, Elsasser TH, Rahman KS, Chowdhury EU, Kaltenboeck B. Asymptomatic endemic Chlamydia pecorum infections reduce growth rates in calves by up to 48 percent. 2012.","DOI":"10.1371\/journal.pone.0044961"},{"issue":"2","key":"ppat.1013632.ref026","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1016\/j.tvjl.2007.01.004","article-title":"Impact of latent infections with Chlamydophila species in young cattle","volume":"175","author":"P Reinhold","year":"2008","journal-title":"Vet J"},{"issue":"3","key":"ppat.1013632.ref027","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1016\/j.tvjl.2014.05.037","article-title":"Longitudinal prevalence and faecal shedding of Chlamydia pecorum in sheep","volume":"201","author":"R Yang","year":"2014","journal-title":"Vet J"},{"issue":"1","key":"ppat.1013632.ref028","doi-asserted-by":"crossref","first-page":"12670","DOI":"10.1038\/s41598-023-39832-w","article-title":"A retrospective study on antibacterial treatments for koalas infected with Chlamydia pecorum","volume":"13","author":"C-J Chen","year":"2023","journal-title":"Sci Rep"},{"issue":"1","key":"ppat.1013632.ref029","doi-asserted-by":"crossref","first-page":"13194","DOI":"10.1038\/s41598-019-49382-9","article-title":"Longitudinal study of wild koalas (Phascolarctos cinereus) reveals chlamydial disease progression in two thirds of infected animals","volume":"9","author":"A Robbins","year":"2019","journal-title":"Sci Rep"},{"key":"ppat.1013632.ref030","doi-asserted-by":"crossref","first-page":"664386","DOI":"10.3389\/fmicb.2021.664386","article-title":"Co-infections as Modulators of Disease Outcome: Minor Players or Major Players?","volume":"12","author":"P Devi","year":"2021","journal-title":"Front Microbiol"},{"key":"ppat.1013632.ref031","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.dci.2018.01.017","article-title":"Koala immunology and infectious diseases: How much can the koala bear?","volume":"82","author":"D Madden","year":"2018","journal-title":"Dev Comp Immunol"},{"issue":"10","key":"ppat.1013632.ref032","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0163780","article-title":"Altered Immune Cytokine Expression Associated with KoRV B Infection and Season in Captive Koalas","volume":"11","author":"IE Maher","year":"2016","journal-title":"PLoS One"},{"issue":"1","key":"ppat.1013632.ref033","doi-asserted-by":"crossref","first-page":"11170","DOI":"10.1038\/s41598-019-47666-8","article-title":"Altered immune parameters associated with Koala Retrovirus (KoRV) and Chlamydial infection in free ranging Victorian koalas (Phascolarctos cinereus)","volume":"9","author":"IE Maher","year":"2019","journal-title":"Sci Rep"},{"issue":"7","key":"ppat.1013632.ref034","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0133807","article-title":"Prevalence and Clinical Significance of Herpesvirus Infection in Populations of Australian Marsupials","volume":"10","author":"K Stalder","year":"2015","journal-title":"PLoS One"},{"issue":"3","key":"ppat.1013632.ref035","article-title":"Detection and Differentiation of Two Koala Gammaherpesviruses by Use of High-Resolution Melt (HRM) Analysis Reveals Differences in Viral Prevalence and Clinical Associations in a Large Study of Free-Ranging Koalas","volume":"57","author":"PK Vaz","year":"2019","journal-title":"J Clin Microbiol"},{"issue":"7","key":"ppat.1013632.ref036","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1017\/S0031182011000369","article-title":"The potential impact of native Australian trypanosome infections on the health of koalas (Phascolarctos cinereus)","volume":"138","author":"LM McInnes","year":"2011","journal-title":"Parasitology"},{"issue":"5","key":"ppat.1013632.ref037","article-title":"Koala retrovirus load and non-A subtypes are associated with secondary disease among wild northern koalas","volume":"18","author":"MDJ Blyton","year":"2022","journal-title":"PLoS 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Joyce","year":"2022","journal-title":"Sci Rep"},{"issue":"1","key":"ppat.1013632.ref045","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1038\/s41598-017-00137-4","article-title":"Infection with koala retrovirus subgroup B (KoRV-B), but not KoRV-A, is associated with chlamydial disease in free-ranging koalas (Phascolarctos cinereus)","volume":"7","author":"CA Waugh","year":"2017","journal-title":"Sci Rep"},{"issue":"11","key":"ppat.1013632.ref046","doi-asserted-by":"crossref","first-page":"5651","DOI":"10.1128\/JVI.02597-05","article-title":"Transspecies transmission of the endogenous koala retrovirus","volume":"80","author":"U Fiebig","year":"2006","journal-title":"J Virol"},{"issue":"7","key":"ppat.1013632.ref047","doi-asserted-by":"crossref","first-page":"2329","DOI":"10.4049\/jimmunol.139.7.2329","article-title":"A synthetic peptide homologous to the envelope proteins of retroviruses inhibits monocyte-mediated killing by inactivating interleukin 1","volume":"139","author":"ES Kleinerman","year":"1987","journal-title":"J Immunol"},{"key":"ppat.1013632.ref048","doi-asserted-by":"crossref","first-page":"1057791","DOI":"10.3389\/fimmu.2022.1057791","article-title":"Human endogenous retroviruses and the inflammatory response: A vicious circle associated with health and illness","volume":"13","author":"SC Rangel","year":"2022","journal-title":"Front Immunol"},{"issue":"12","key":"ppat.1013632.ref049","doi-asserted-by":"crossref","DOI":"10.1128\/JVI.02299-20","article-title":"Switching Sides: How Endogenous Retroviruses Protect Us from Viral Infections","volume":"95","author":"S Srinivasachar Badarinarayan","year":"2021","journal-title":"J Virol"},{"issue":"6277","key":"ppat.1013632.ref050","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1126\/science.aad5497","article-title":"Regulatory evolution of innate immunity through co-option of endogenous retroviruses","volume":"351","author":"EB 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