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      Pre-infection of pigs with Mycoplasma hyopneumoniae modifies outcomes of infection with European swine influenza virus of H1N1, but not H1N2, subtype

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          Abstract

          Swine influenza virus (SIV) and Mycoplasma hyopneumoniae (Mhp) are widespread in farms and are major pathogens involved in the porcine respiratory disease complex (PRDC). The aim of this experiment was to compare the pathogenicity of European avian-like swine H1N1 and European human-like reassortant swine H1N2 viruses in naïve pigs and in pigs previously infected with Mhp. Six groups of SPF pigs were inoculated intra-tracheally with either Mhp, or H1N1, or H1N2 or Mhp + H1N1 or Mhp + H1N2, both pathogens being inoculated at 21 days intervals in these two last groups. A mock-infected group was included. Although both SIV strains induced clinical signs when singly inoculated, results indicated that the H1N2 SIV was more pathogenic than the H1N1 virus, with an earlier shedding and a greater spread in lungs. Initial infection with Mhp before SIV inoculation increased flu clinical signs and pathogenesis (hyperthermia, loss of appetite, pneumonia lesions) due to the H1N1 virus but did not modify significantly outcomes of H1N2 infection. Thus, Mhp and SIV H1N1 appeared to act synergistically, whereas Mhp and SIV H1N2 would compete, as H1N2 infection led to the elimination of Mhp in lung diaphragmatic lobes. In conclusion, SIV would be a risk factor for the severity of respiratory disorders when associated with Mhp, depending on the viral subtype involved. This experimental model of coinfection with Mhp and avian-like swine H1N1 is a relevant tool for studying the pathogenesis of SIV-associated PRDC and testing intervention strategies for the control of the disease.

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          Most cited references21

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          Bacterial coinfections in lung tissue specimens from fatal cases of 2009 pandemic influenza A (H1N1) - United States, May-August 2009.

          (2009)
          In previous influenza pandemics, studies of autopsy specimens have shown that most deaths attributed to influenza A virus infection occurred concurrently with bacterial pneumonia, but such evidence has been lacking for 2009 pandemic influenza A (H1N1). To help determine the role of bacterial coinfection in the current influenza pandemic, CDC examined postmortem lung specimens from patients with fatal cases of 2009 pandemic influenza A (H1N1) for bacterial causes of pneumonia. During May 1-August 20, 2009, medical examiners and local and state health departments submitted specimens to CDC from 77 U.S. patients with fatal cases of confirmed 2009 pandemic influenza A (H1N1). This report summarizes the demographic and clinical findings from these cases and the laboratory evaluation of the specimens. Evidence of concurrent bacterial infection was found in specimens from 22 (29%) of the 77 patients, including 10 caused by Streptococcus pneumoniae (pneumococcus). Duration of illness was available for 17 of the 22 patients; median duration was 6 days (range: 1-25 days). Fourteen of 18 patients for whom information was available sought medical care while ill, and eight (44%) were hospitalized. These findings confirm that bacterial lung infections are occurring among patients with fatal cases of 2009 pandemic influenza A (H1N1) and underscore both the importance of pneumococcal vaccination for persons at increased risk for pneumococcal pneumonia and the need for early recognition of bacterial pneumonia in persons with influenza.
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            Infectious agents associated with respiratory diseases in 125 farrow-to-finish pig herds: a cross-sectional study.

            A study was carried out in 125 farrow-to-finish pig herds to assess the relationships between pathogens involved in respiratory disorders and to relate these findings to clinical signs of respiratory diseases and pneumonia and pleuritis at slaughter. Clinical examination and sampling were carried out on four different batches in each herd (pigs aged 4, 10, 16 and 22 weeks). Mycoplasma hyopneumoniae, Actinobacillus pleuropneumoniae, swine influenza viruses (SIV), porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2) were detected by serological or PCR tests. Pneumonia-like gross lesions and pleuritis were scored at the slaughterhouse. The results indicate that the percentage of pigs PCR-positive for PCV2 at 4, 10 and 16 weeks old was associated with the percentage of pigs PCR-positive for M. hyopneumoniae at these ages. On the other hand, the percentage of pigs with antibodies against PRRSV at 10, 16 and 22 weeks was positively correlated with the percentage of pigs seropositive for M. hyopneumoniae at 22 weeks, with the percentage of pigs with antibodies against SIV H1N1 and SIV H1N2 and the percentage of pigs sero-positive for A. pleuropneumoniae serotype 2. The findings also indicate that, within the five studied pathogens, M. hyopneumoniae, PRRSV and SIV H1N1 are the major pathogens involved in pneumonia-like gross lesions even though PCV2 may play a role. A. pleuropneumoniae serotype 2, in association with PRRSV, is significantly associated with extensive pleuritis. Respiratory diseases could be significantly reduced by implementing measures including appropriate management practices to control these pathogens. Copyright © 2011 Elsevier B.V. All rights reserved.
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              Increased production of proinflammatory cytokines following infection with porcine reproductive and respiratory syndrome virus and Mycoplasma hyopneumoniae.

              Induction of the proinflammatory cytokines interleukin-1 (IL-1) (alpha and beta), IL-6, IL-8, IL-10, IL-12, and tumor necrosis factor alpha (TNF-alpha) in pulmonary alveolar macrophages (PAMs) was assessed following experimental infection with porcine reproductive and respiratory syndrome virus (PRRSV) and/or Mycoplasma hyopneumoniae by using in vivo and in vitro models. The in vivo model consisted of pigs infected with PRRSV and/or M. hyopneumoniae and necropsied at 10, 28, or 42 days postinfection. Pigs infected with both pathogens had a greater percentage of macroscopic lung lesions, increased clinical disease, and slower viral clearance than pigs infected with either pathogen alone. The pigs infected with both PRRSV and M. hyopneumoniae had significantly increased levels of mRNA for many proinflammatory cytokines in PAMs collected by bronchoalveolar lavage (BAL) at all necropsy dates compared to those in uninfected control pigs. Increased levels of IL-1beta, IL-8, IL-10, and TNF-alpha proteins in BAL fluid, as measured by enzyme-linked immunosorbent assay, confirmed the increased cytokine induction induced by the pathogens. An in vitro model consisted of M. hyopneumoniae-inoculated tracheal ring explants cultured with PRRSV-infected PAMs. PAMs were harvested at 6 or 15 h postinfection with either or both pathogens. The in vitro study detected increased IL-10 and IL-12 mRNA levels in PAMs infected with PRRSV at all time periods. In addition, IL-10 protein levels were significantly elevated in the culture supernatants in the presence of M. hyopneumoniae-inoculated tracheal ring explants. The increased production of proinflammatory cytokines in vivo and in vitro associated with concurrent M. hyopneumoniae and PRRSV infection may play a role in the increased rates of pneumonia associated with PRRSV infection. The increased levels of IL-10 may be a possible mechanism that PRRSV and M. hyopneumoniae use to exacerbate the severity and duration of pneumonia induced by PRRSV and modulate the respiratory immune response.
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                Author and article information

                Contributors
                Journal
                Vet Microbiol
                Vet. Microbiol
                Veterinary Microbiology
                Elsevier B.V.
                0378-1135
                1873-2542
                29 December 2011
                25 May 2012
                29 December 2011
                : 157
                : 1
                : 96-105
                Affiliations
                [a ]Anses, Ploufragan-Plouzané Laboratory, Swine Virology Immunology Unit, Ploufragan, France
                [b ]Anses, Ploufragan-Plouzané Laboratory, Mycoplasmology – Bacteriology Unit, Ploufragan, France
                [c ]LDA22, Ploufragan, France
                [d ]Anses, Ploufragan-Plouzané Laboratory, Production of Decontaminated Pigs and Testing, Ploufragan, France
                Author notes
                [* ]Corresponding author at: Anses, Ploufragan-Plouzané Laboratory, Swine Virology Immunology Unit, B.P. 53, 22440 Ploufragan, France. Tel.: +33 2 96 01 62 22; fax: +33 2 96 01 62 94. celine.deblanc@ 123456anses.fr
                Article
                S0378-1135(11)00667-5
                10.1016/j.vetmic.2011.12.027
                7117109
                22261237
                c8954f7b-f126-4184-9141-0c1b6acae94a
                Copyright © 2012 Elsevier B.V. All rights reserved.

                Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.

                History
                : 10 November 2011
                : 16 December 2011
                : 20 December 2011
                Categories
                Article

                Veterinary medicine
                swine influenza virus,mycoplasma hyopneumoniae,porcine respiratory disease complex,pigs,co-infection

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