Coinfections and their molecular consequences in the porcine respiratory tract

Abstract

Understudied, coinfections are more frequent in pig farms than single infections. In pigs, the term "Porcine Respiratory Disease Complex" (PRDC) is often used to describe coinfections involving viruses such as swine Influenza A Virus (swIAV), Porcine Reproductive and Respiratory Syndrome Virus (PRRSV), and Porcine CircoVirus type 2 (PCV2) as well as bacteria like Actinobacillus pleuropneumoniae, Mycoplasma hyopneumoniae and Bordetella bronchiseptica. The clinical outcome of the various coinfection or superinfection situations is usually assessed in the studies while in most of cases there is no clear elucidation of the fine mechanisms shaping the complex interactions occurring between microorganisms. In this comprehensive review, we aimed at identifying the studies dealing with coinfections or superinfections in the pig respiratory tract and at presenting the interactions between pathogens and, when possible, the mechanisms controlling them. Coinfections and superinfections involving viruses and bacteria were considered while research articles including protozoan and fungi were excluded. We discuss the main limitations complicating the interpretation of coinfection/superinfection studies, and the high potential perspectives in this fascinating research field, which is expecting to gain more and more interest in the next years for the obvious benefit of animal health.

Figure 1

Impact of coinfection on multiplication/replication of the microorganisms. Heat maps depicting: A the impact of a secondary viral infection (top) on the replication of the virus (side) responsible of the primary infection in virus-virus dual infections (coinfections and superinfections) in vitro (up) and in vivo (down). B the impact of a bacterial infection on the replication of the infecting virus in virus-bacterium dual infections (coinfections and superinfections) in vitro (up) and in vivo (down). C the impact of a viral infection on the multiplication on the infecting bacteria in virus-bacterium dual infections (coinfections and superinfections) in vitro (up) and in vivo (down). D the impact of a secondary bacterial infection (top) on the multiplication of the bacteria (side) responsible of the primary infection in bacterium-bacterium dual infections (coinfections and superinfections) in vivo. The numbers shown on the maps correspond to the number of the identified studies for the same pathogen combination (see Additional file 1A and B). PRRSV: Porcine Reproductive and Respiratory Syndrome Virus, swIAV: swine Influenza A Virus, PCV2: Porcine Circovirus type 2, ADV: Aujeszky’s Disease Virus, PRCoV: Porcine Respiratory alphaCoronaVirus, CSFV: Classical Swine Fever Virus, HEV: Hepatitis E Virus, PorPV: Porcine RubulaVirus, PPV: Porcine ParvoVirus.

Figure 2

Impact of coinfection on inflammation. Heat maps depicting: A the impact of dual virus-virus infections (coinfections and superinfections) and B the impact of virus-bacterium infections (coinfections and superinfections) on the immune response of hosting cells (in vitro). The numbers shown on the maps correspond to the number of the identified studies for the same pathogen combination (see Additional file 1). PRRSV: Porcine Reproductive and Respiratory Syndrome Virus, swIAV: swine Influenza A Virus, PCV2: Porcine Circovirus type 2, PRCoV: Porcine Respiratory alphaCoronaVirus, CSFV: Classical Swine Fever Virus.

Figure 3

Impact of coinfection on clinical signs. Heat map depicting: A the clinical impact of dual virus-virus infections (coinfections and superinfections), B the clinical impact of virus-bacterium infections (coinfections and superinfections) and C the clinical impact of bacterium-bacterium infections (coinfections and superinfections) on the developed clinical signs (in vivo). The numbers shown on the maps correspond to the number of the identified studies for the same pathogen combination (see Additional file 1). M. hyop: Mycoplasma hyopneumoniae, A. pleuro: Actinobacillus pleuropneumoniae, B. bronchi: Bordetella bronchiseptica, P. multo: Pasteurella multocida, PRRSV: Porcine Reproductive and Respiratory Syndrome Virus, swIAV: swine Influenza A Virus, PCV2: Porcine Circovirus type 2, ADV: Aujeszky’s Disease Virus, PRCoV: Porcine Respiratory alphaCoronaVirus, HEV: Hepatitis E Virus, PorPV: Porcine RubulaVirus, PPV: Porcine ParvoVirus, TTsuV1: Torque Teno sus Virus 1.

Figure 4

Consequences of the different types of coinfections for the microorganisms and for the host. In the left box some parameters enable to affect coinfections and superinfections are listed. IFN: Interferon, IBP: Intracellular Bacterial Pathogen.