Hostname: page-component-89b8bd64d-72crv Total loading time: 0 Render date: 2026-05-10T13:49:37.246Z Has data issue: false hasContentIssue false
  • English
  • Français

Polymicrobial respiratory disease in pigs

Published online by Cambridge University Press:  09 December 2011

T. Opriessnig ,
L. G. Giménez-Lirola  and
P. G. Halbur
T. Opriessnig*
Affiliation:
Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, 1600 S. 16th Street, Ames, IA 50011, USA
L. G. Giménez-Lirola
Affiliation:
Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, 1600 S. 16th Street, Ames, IA 50011, USA
P. G. Halbur
Affiliation:
Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, 1600 S. 16th Street, Ames, IA 50011, USA
*
*Corresponding author. E-mail: tanjaopr@iastate.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Respiratory disease in pigs is common in modern pork production worldwide and is often referred to as porcine respiratory disease complex (PRDC). PRDC is polymicrobial in nature, and results from infection with various combinations of primary and secondary respiratory pathogens. As a true multifactorial disease, environmental conditions, population size, management strategies and pig-specific factors such as age and genetics also play critical roles in the outcome of PRDC. While non-infectious factors are important in the initiation and outcome of cases of PRDC, the focus of this review is on infectious factors only. There are a variety of viral and bacterial pathogens commonly associated with PRDC including porcine reproductive and respiratory syndrome virus (PRRSV), swine influenza virus (SIV), porcine circovirus type 2 (PCV2), Mycoplasma hyopneumoniae (MHYO) and Pasteurella multocida (PMULT). The pathogenesis of viral respiratory disease is typically associated with destruction of the mucocilliary apparatus and with interference and decrease of the function of pulmonary alveolar and intravascular macrophages. Bacterial pathogens often contribute to PRDC by activation of inflammation via enhanced cytokine responses. With recent advancements in pathogen detection methods, the importance of polymicrobial disease has become more evident, and identification of interactions of pathogens and their mechanisms of disease potentiation has become a topic of great interest. For example, combined infection of pigs with typically low pathogenic organisms like PCV2 and MHYO results in severe respiratory disease. Although the body of knowledge has advanced substantially in the last 15 years, much more needs to be learned about the pathogenesis and best practices for control of swine respiratory disease outbreaks caused by concurrent infection of two or more pathogens. This review discusses the latest findings on polymicrobial respiratory disease in pigs.

Keywords

porcineco-infectionrespiratory diseasepolymicrobialreview

Information

Type
Review Article
Information
Animal Health Research Reviews , Volume 12 , Issue 2 , December 2011 , pp. 133 - 148
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Allan, GM, Kennedy, S, McNeilly, F, Foster, JC, Ellis, JA, Krakowka, SJ, Meehan, BM and Adair, BM (1999). Experimental reproduction of severe wasting disease by coinfection of pigs with porcine circovirus and porcine parvovirus. Journal of Comparative Pathology 121: 1–11.CrossRefGoogle ScholarPubMed
Allan, GM, McNeilly, F, Ellis, J, Krakowka, S, Meehan, B, McNair, I, Walker, I and Kennedy, S (2000). Experimental infection of colostrum deprived piglets with porcine circovirus 2 (PCV2) and porcine reproductive and respiratory syndrome virus (PRRSV) potentiates PCV2 replication. Archives of Virology 145: 2421–2429.CrossRefGoogle ScholarPubMed
Amass, SF, Clark, LK, van Alstine, WG, Bowersock, TL, Murphy, DA, Knox, KE and Albregts, SR (1994). Interaction of Mycoplasma hyopneumoniae and Pasteurella multocida infections in swine. Journal of the American Veterinary Medical Association 204: 102–107.CrossRefGoogle ScholarPubMed
Asai, T, Okada, M, Ono, M, Irisawa, T, Mori, Y, Yokomizo, Y and Sato, S (1993). Increased levels of tumor necrosis factor and interleukin 1 in bronchoalveolar lavage fluids from pigs infected with Mycoplasma hyopneumoniae. Veterinary Immunology and Immunopathology 38: 253–260.CrossRefGoogle ScholarPubMed
Atanasova, K, Van Gucht, S, Barbé, F, Duchateau, L and Van Reeth, K (2011). Lipoteichoic acid from Staphylococcus aureus exacerbates respiratory disease in porcine respiratory coronavirus-infected pigs. Veterinary Journal 188: 210–215.CrossRefGoogle ScholarPubMed
Atanasova, K, Van Gucht, S, Barbé, F, Lefebvre, DJ, Chiers, K and Van Reeth, K (2008). Lung cell tropism and inflammatory cytokine profile of porcine respiratory coronavirus infection. Open Veterinary Science Journal 2: 117–126.CrossRefGoogle Scholar
Atanasova, K, Van Gucht, S and Van Reeth, K (2010). Anti-TNF-alpha therapy does not ameliorate disease in a model of acute virus-endotoxin mediated respiratory disease in pigs. Veterinary Immunology and Immunopathology 137: 12–9.CrossRefGoogle ScholarPubMed
Bertschinger, HU and Nicod, B (1970). Untersuchungen über die Nasenflora bei Schweinen: Vergleich zwischen SPF-Herden un schedisch sanierten Herden. Schweizer Archiv für Tierheilkunde 112: 493–499.Google Scholar
Brockmeier, SL (2004). Prior infection with Bordetella bronchiseptica increases nasal colonization by Haemophilus parasuis in swine. Veterinary Microbiology 99: 75–78.CrossRefGoogle ScholarPubMed
Brockmeier, SL, Loving, CL, Nicholson, TL and Palmer, MV (2008). Coinfection of pigs with porcine respiratory coronavirus and Bordetella bronchiseptica. Veterinary Microbiology 128: 36–47.CrossRefGoogle ScholarPubMed
Brockmeier, SL, Palmer, MV and Bolin, SR (2000). Effects of intranasal inoculation of porcine reproductive and respiratory syndrome virus, Bordetella bronchiseptica, or a combination of both organisms in pigs. American Journal of Veterinary Research 61: 892–899.CrossRefGoogle ScholarPubMed
Brockmeier, SL, Palmer, MV, Bolin, SR and Rimler, RB (2001). Effects of intranasal inoculation with Bordetella bronchiseptica, porcine reproductive and respiratory syndrome virus, or a combination of both organisms on subsequent infection with Pasteurella multocida in pigs. American Journal of Veterinary Research 62: 521–525.CrossRefGoogle ScholarPubMed
Brockmeier, SL and Register, KB (2007). Expression of the dermonecrotic toxin by Bordetella bronchiseptica is not necessary for predisposing to infection with toxigenic Pasteurella multocida. Veterinary Microbiology 125: 284–289.CrossRefGoogle Scholar
Brockmeier, SL, Register, KB, Magyar, T, Lax, AJ, Pullinger, GD and Kunkle, RA (2002). Role of the dermonecrotic toxin of Bordetella bronchiseptica in the pathogenesis of respiratory disease in swine. Infection and Immunity 70: 481–490.CrossRefGoogle ScholarPubMed
Brown, IH, Alexander, DJ, Chakraverty, P, Harris, PA and Manvell, RJ (1994). Isolation of an influenza A virus of unusual subtype (H1N7) from pigs in England, and the subsequent experimental transmission from pig to pig. Veterinary Microbiology 39: 125–134.CrossRefGoogle ScholarPubMed
Caruso, JP and Ross, RF (1990). Effects of Mycoplasma hyopneumoniae and Actinobacillus (Haemophilus) pleuropneumoniae infections on alveolar macrophage functions in swine. American Journal of Veterinary Research 51: 227–231.CrossRefGoogle ScholarPubMed
Carvalho, LF, Segalés, J and Pijoan, C (1997). Effect of porcine reproductive and respiratory syndrome virus on subsequent Pasteurella multocida challenge in pigs. Veterinary Microbiology 55: 241–246.CrossRefGoogle ScholarPubMed
Chang, HW, Jeng, CR, Liu, JJ, Lin, TL, Chang, CC, Chia, MY, Tsai, YC and Pang, VF (2005). Reduction of porcine reproductive and respiratory syndrome virus (PRRSV) infection in swine alveolar macrophages by porcine circovirus 2 (PCV2)-induced interferon-alpha. Veterinary Microbiology 108: 167–177.CrossRefGoogle ScholarPubMed
Chanter, N, Magyar, T and Rutter, JM (1989). Interactions between Bordetella bronchiseptica and toxigenic Pasteurella multocida in atrophic rhinitis of pigs. Research in Veterinary Science 47: 48–53.CrossRefGoogle ScholarPubMed
Charley, B, Riffault, S and Van Reeth, K (2006). Porcine innate and adaptative immune responses to influenza and coronavirus infections. Annals of the New York Academy of Sciences 1081: 130–136.CrossRefGoogle ScholarPubMed
Chiou, MT, Jeng, CR, Chueh, LL, Cheng, CH, and Pang, VF (2000). Effects of porcine reproductive and respiratory syndrome virus (isolate tw91) on porcine alveolar macrophages in vitro. Veterinary Microbiology 71: 9–25.CrossRefGoogle ScholarPubMed
Cho, JG, Dee, SA, Deen, J, Trincado, C, Fano, E, Jiang, Y, Faaberg, K, Murtaugh, MP, Guedes, A, Collins, JE and Joo, HS (2006). The impact of animal age, bacterial coinfection, and isolate pathogenicity on the shedding of porcine reproductive and respiratory syndrome virus in aerosols from experimentally infected pigs. Canadian Journal of Veterinary Research 70: 297–301.Google ScholarPubMed
Chung, WB, Backstrom, LR and Collins, MT (1994). Experimental model of swine pneumonic pasteurellosis using crude Actinobacillus pleuropneumoniae cytotoxin and Pasteurella multocida given endobronchially. Canadian Journal of Veterinary Research 58: 25–30.Google ScholarPubMed
Ciprián, A, Pijoan, C, Cruz, T, Camacho, J, Tórtora, J, Colmenares, G, López-Revilla, R and de la Garza, M (1988). Mycoplasma hyopneumoniae increases the susceptibility of pigs to experimental Pasteurella multocida pneumonia. Canadian Journal of Veterinary Research 52: 434–438.Google ScholarPubMed
Cloutier, G, D'Allaire, S, Martinez, G, Surprenant, C, Lacouture, S and Gottschalk, M (2003). Epidemiology of Streptococcus suis serotype 5 infection in a pig herd with and without clinical disease. Veterinary Microbiology 97: 135–151.CrossRefGoogle Scholar
Dea, S, Bilodeau, R, Sauvageau, R, Montpetit, C and Martineau, GP (1992). Antigenic variant of swine influenza virus causing proliferative and necrotizing pneumonia in pigs. Journal of Veterinary Diagnostic Investigation 4: 380–392.CrossRefGoogle ScholarPubMed
DeBey, MC and Ross, RF (1994). Ciliostasis and loss of cilia induced by Mycoplasma hyopneumoniae in porcine tracheal organ cultures. Infectious Immunology 62: 5312–5318.CrossRefGoogle ScholarPubMed
Done, SH (1991). Environmental factors affecting the severity of pneumonia in pigs. Veterinary Record 128: 582–586.CrossRefGoogle ScholarPubMed
Dugal, F, Belanger, M and Jacques, M (1992). Enhanced adherence of Pasteurella multocida to porcine tracheal rings preinfected with Bordetella bronchiseptica. Canadian Journal of Veterinary Research 56: 260–264.Google ScholarPubMed
Dugal, F, Girard, C and Jacques, M (1990). Adherence of Bordetella bronchiseptica 276 to porcine trachea maintained in organ culture. Applied Environmental Microbiology 56: 1523–1529.CrossRefGoogle ScholarPubMed
Edington, N, Smith, IM, Plowright, W and Watt, RG (1976). Relationship of porcine cytomegalovirus and B bronchiseptica to atrophic rhinitis in gnotobiotic piglets. Veterinary Record 98: 42–45.CrossRefGoogle Scholar
Edington, N, Watt, RG and Plowright, W (1977). Experimental transplacental transmission of porcine cytomegalovirus. Journal of Hygiene 78: 243–251.CrossRefGoogle ScholarPubMed
Ellis, JA, Allan, G and Krakowka, S (2008). Effect of coinfection with genogroup 1 porcine torque teno virus on porcine circovirus type 2-associated postweaning multisystemic wasting syndrome in gnotobiotic pigs. American Journal of Veterinary Research 69: 1608–1614.CrossRefGoogle ScholarPubMed
Fachinger, V, Bischoff, R, Jedidia, SB, Saalmuller, A and Elbers, K (2008). The effect of vaccination against porcine circovirus type 2 in pigs suffering from porcine respiratory disease complex. Vaccine 26: 1488–1499.CrossRefGoogle ScholarPubMed
Fraile, L, Alegre, A, López-Jiménez, R, Nofrarías, M and Segalés, J (2010). Risk factors associated with pleuritis and cranio-ventral pulmonary consolidation in slaughter-aged pigs. Veterinary Journal 184: 326–333.CrossRefGoogle ScholarPubMed
Fuentes, M and Pijoan, C (1986). Phagocytosis and intracellular killing of Pasteurella multocida by porcine alveolar macrophages after infection with pseudorabies virus. Veterinary Immunology and Immunopathology 13: 165–172.CrossRefGoogle ScholarPubMed
Fuentes, MC and Pijoan, C (1987). Pneumonia in pigs induced by intranasal challenge exposure with pseudorabies virus and Pasteurella multocida. American Journal of Veterinary Research 48: 1446–1448.Google ScholarPubMed
Galina, L, Pijoan, C, Sitjar, M, Christianson, WT, Rossow, K and Collins, JE (1994). Interaction between Streptococcus suis serotype 2 and porcine reproductive and respiratory syndrome virus in specific pathogen-free piglets. Veterinary Record 134: 60–64.CrossRefGoogle ScholarPubMed
Gutiérrez-Martín, CB, Rodríguez-Delgado, O, Alvarez-Nistal, D, De La Puente-Redondo, VA, García-Rioja, F, Martín-Vicente, J and Rodríguez Ferri, EF (2000). Simultaneous serological evidence of Actinobacillus pleuropneumoniae, PRRS, Aujeszky's disease and influenza viruses in Spanish finishing pigs. Research in Veterinary Science 68: 9–13.CrossRefGoogle ScholarPubMed
Halbur, PG (1998). Porcine viral respiratory diseases. In: Proceedings of the 14th International Pig Veterinary Society, Birmingham, UK, 8–12 July, pp. 1–10.Google Scholar
Halbur, PG, Rothschild, MF, Thacker, BJ, Meng, XJ, Paul, PS and Bruna, JD (1998). Differences in susceptibility of Duroc, Hampshire and Meishan pigs to infection with a high virulence strain (BR2385) of porcine reproductive and respiratory syndrome virus (PRRSV). Journal of Animal Breeding and Genetics 115: 181–189.CrossRefGoogle Scholar
Hansen, MS, Pors, SE, Jensen, HE, Bille-Hansen, V, Bisgaard, M, Flachs, EM and Nielsen, OL (2010). An investigation of the pathology and pathogens associated with porcine respiratory disease complex in Denmark. Journal of Comparative Pathology 143: 120–131.CrossRefGoogle ScholarPubMed
Harms, PA, Halbur, PG and Sorden, SD (2002). Three cases of porcine respiratory disease complex associated with porcine circovirus type 2 infection. Journal of Swine Health and Production 10: 27–30.Google Scholar
Harms, PA, Sorden, SD, Halbur, PG, Bolin, SR, Lager, KM, Morozov, I and Paul, PS (2001). Experimental reproduction of severe disease in CD/CD pigs concurrently infected with type 2 porcine circovirus and porcine reproductive and respiratory syndrome virus. Veterinary Pathology 38: 528–539.CrossRefGoogle ScholarPubMed
Hooper, P, Zaki, S, Daniels, P and Middleton, D (2001). Comparative pathology of the diseases caused by Hendra and Nipah viruses. Microbes and Infection 3: 315–322.CrossRefGoogle ScholarPubMed
Horiguchi, Y (2009). Bordetella dermonecrotic toxin and Pasteurella multocida toxin causing turbinate atrophy in pigs. Tanpakushitsu Kakusan Koso 54: 601–606.Google ScholarPubMed
Iglesias, G, Pijoan, C and Molitor, T (1989). Interactions of pseudorabies virus with swine alveolar macrophages: effects of virus infection on cell functions. Journal of Leukocyte Biology 45: 410–415.CrossRefGoogle ScholarPubMed
Iglesias, G, Pijoan, C and Molitor, T (1992). Effects of pseudorabies virus infection upon cytotoxicity and antiviral activities of porcine alveolar macrophages. Comparative Immunology, Microbiology and Infectious Diseases 15: 249–259.CrossRefGoogle ScholarPubMed
Janke, BH, Paul, PS, Landgraf, JG, Halbur, PG and Huinker, CD (2001). Paramyxovirus infection in pigs with interstitial pneumonia and encephalitis in the United States. Journal of Veterinary Diagnostic Investigation 13: 428–433.CrossRefGoogle ScholarPubMed
Jung, K, Renukaradhya, GJ, Alekseev, KP, Fang, Y, Tang, Y and Saif, LJ (2009). Porcine reproductive and respiratory syndrome virus modifies innate immunity and alters disease outcome in pigs subsequently infected with porcine respiratory coronavirus: implications for respiratory viral co-infections. Journal of General Virology 90: 2713–2723.CrossRefGoogle ScholarPubMed
Kamp, EM, Stockhofe-Zurwieden, N, van Leengoed, LA and Smits, MA (1997). Endobronchial inoculation with Apx toxins of Actinobacillus pleuropneumoniae leads to pleuropneumonia in pigs. Infectious Immunology 65: 4350–4354.CrossRefGoogle ScholarPubMed
Karasin, AI, Olsen, CW, Brown, IH, Carman, S, Stalker, M and Josephson, G (2000). H4N6 influenza virus isolated from pigs in Ontario. Canadian Veterinary Journal 41: 938–939.Google ScholarPubMed
Kim, J, Chung, HK and Chae, C (2003). Association of porcine circovirus 2 with porcine respiratory disease complex. Veterinary Journal 166: 251–256.CrossRefGoogle ScholarPubMed
Kishima, M and Ross, RF (1985). Suppressive effect of nonviable Mycoplasma hyopneumoniae on phytohemagglutinin-induced transformation of swine lymphocytes. American Journal of Veterinary Research 46: 2366–2368.Google ScholarPubMed
Kishima, M, Ross, RF and Kuniyasu, C (1985). Cell-mediated and humoral immune response to Mycoplasma hyopneumoniae in pigs enhanced by dextran sulfate. American Journal of Veterinary Research 46: 456–462.Google ScholarPubMed
Krakowka, S and Ellis, JA (2008). Evaluation of the effects of porcine genogroup 1 torque teno virus in gnotobiotic swine. American Journal of Veterinary Research 69: 1623–1629.CrossRefGoogle ScholarPubMed
Krakowka, S, Ellis, JA, Meehan, B, Kennedy, S, McNeilly, F and Allan, G (2000). Viral wasting syndrome of swine: experimental reproduction of postweaning multisystemic wasting syndrome in gnotobiotic swine by coinfection with porcine circovirus 2 and porcine parvovirus. Veterinary Pathology 37: 254–263.CrossRefGoogle ScholarPubMed
Krakowka, S, Hartunian, C, Hamberg, A, Shoup, D, Rings, M, Zhang, Y, Allan, G and Ellis, JA (2008). Evaluation of induction of porcine dermatitis and nephropathy syndrome in gnotobiotic pigs with negative results for porcine circovirus type 2. American Journal of Veterinary Research 69: 1615–1622.CrossRefGoogle ScholarPubMed
Labarque, G, Van Gucht, S, Nauwynck, H, Van Reeth, K and Pensaert, M (2003). Apoptosis in the lungs of pigs infected with porcine reproductive and respiratory syndrome virus and associations with the production of apoptogenic cytokines. Veterinary Research 34: 249–60.CrossRefGoogle ScholarPubMed
Labarque, G, Van Reeth, K, Van Gucht, S, Nauwynck, H and Pensaert, M (2002). Porcine reproductive-respiratory syndrome virus infection predisposes pigs for respiratory signs upon exposure to bacterial lipopolysaccharide. Veterinary Microbiology 88: 1–12.CrossRefGoogle ScholarPubMed
Lang, C, Söllner, H, Barz, A, Ladinig, A, Langhoff, R, Weissenböck, H, Kekarainen, T, Segalés, J and Ritzmann, M (2011). Investigation of the prevalence of swine torque teno virus in Austria. Berliner und Münchner Tierärztliche Wochenschrift 124: 142–147.Google ScholarPubMed
Lax, AJ and Grigoriadis, AE (2001). Pasteurella multocida toxin: the mitogenic toxin that stimulates signalling cascades to regulate growth and differentiation. International Journal of Medical Microbiology 291: 261–268.CrossRefGoogle ScholarPubMed
Lichtensteiger, CA, Steenbergen, SM, Lee, RM, Polson, DD and Vimr, ER (1996). Direct PCR analysis for toxigenic Pasteurella multocida. Journal of Clinical Microbiology 34: 3035–3039.CrossRefGoogle ScholarPubMed
Lin, JH, Chen, SP, Yeh, KS and Weng, CN (2006). Mycoplasma hyorhinis in Taiwan: diagnosis and isolation of swine pneumonia pathogen. Veterinary Microbiology 115: 111–116.CrossRefGoogle ScholarPubMed
Liu, X, Chen, L, Song, Q, Yang, F, Li, Y, Zuo, Y, Jiao, J and Wang, X (2011). Coinfection effects of porcine circovirus type 2 and porcine parvovirus in vivo on phagocytosis and interferon mRNA expression of porcine alveolar macrophages. Wei Sheng Wu Xue Bao 51: 105–114.Google ScholarPubMed
Loula, TJ (2011). What do we do with PRRS negative pigs? Proceedings of the Annual Meeting of the American Association for Swine Veterinarians. Phoenix, Arizona. 42: 531–532.Google Scholar
Loving, CL, Brockmeier, SL, Vincent, AL, Palmer, MV, Sacco, RE and Nicholson, TL (2010). Influenza virus coinfection with BORDetella bronchiseptica enhances bacterial colonization and host responses exacerbating pulmonary lesions. Microbial Pathogenesis 49: 237–245.CrossRefGoogle ScholarPubMed
Maes, D, Verdonck, M, Deluyker, H and de Kruif, A (1996). Enzootic pneumonia in pigs. Veterinary Quarterly 18: 104–109.CrossRefGoogle ScholarPubMed
Marois, C, Gottschalk, M, Morvan, H, Fablet, C, Madec, F and Kobisch, M (2009). Experimental infection of SPF pigs with Actinobacillus pleuropneumoniae serotype 9 alone or in association with Mycoplasma hyopneumoniae. Veterinary Microbiology 135: 283–291.CrossRefGoogle ScholarPubMed
Martínez, J, Peris, B, Gómez, EA and Corpa, JM (2009). The relationship between infectious and non-infectious herd factors with pneumonia at slaughter and productive parameters in fattening pigs. Veterinary Journal 179: 240–246.CrossRefGoogle ScholarPubMed
Messier, S and Ross, RF (1991). Interactions of Mycoplasma hyopneumoniae membranes with porcine lymphocytes. American Journal of Veterinary Research 52: 1497–1502.CrossRefGoogle ScholarPubMed
Nakai, T, Kume, K, Yoshikawa, H, Oyamada, T and Yoshikawa, T (1988). Adherence of Pasteurella multocida or Bordetella bronchiseptica to the swine nasal epithelial cell in vitro. Infection and Immunity 56: 234–240.CrossRefGoogle ScholarPubMed
Narita, M, Kawashima, K, Matsuura, S, Uchimura, A and Miura, Y (1994). Pneumonia in pigs infected with pseudorabies virus and Haemophilus parasuis serovar 4. Journal of Comparative Pathology 110: 329–339.CrossRefGoogle ScholarPubMed
Narita, M, Kawamura, H, Shirai, J and Haritani, M (1987). Morphologic study of inclusions in tissues from pigs inoculated with cytomegalovirus. American Journal of Veterinary Research 48: 1398–1402.Google ScholarPubMed
Neumann, EJ, Kliebenstein, JB, Johnson, CD, Mabry, JW, Bush, EJ, Seitzinger, AH, Green, AL and Zimmerman, JJ (2005). Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. Journal of the American Veterinary Medical Association 227: 385–392.CrossRefGoogle ScholarPubMed
Nicholson, TL, Brockmeier, SL and Loving, CL (2009). Contribution of Bordetella bronchiseptica filamentous hemagglutinin and pertactin to respiratory disease in swine. Infection and Immunity 77: 2136–46.CrossRefGoogle ScholarPubMed
Opriessnig, T, Fenaux, M, Thomas, P, Hoogland, MJ, Rothschild, MF, Meng, XJ and Halbur, PG (2006). Evidence of breed-dependent differences in susceptibility to porcine circovirus type-2-associated disease and lesions. Veterinary Pathology 43: 281–293.CrossRefGoogle ScholarPubMed
Opriessnig, T and Halbur, PG (2011). Concurrent infections are important for expression of porcine circovirus associated disease. Virus Research [Epub ahead of print, Sep 16].Google ScholarPubMed
Opriessnig, T, Madson, DM, Prickett, JR, Kuhar, D, Lunney, JK, Elsener, J and Halbur, PG (2008). Effect of porcine circovirus type 2 (PCV2) vaccination on porcine reproductive and respiratory syndrome virus (PRRSV) and PCV2 coinfection. Veterinary Microbiology 131: 103–114.CrossRefGoogle ScholarPubMed
Opriessnig, T, Madson, DM, Schalk, S, Brockmeier, S, Shen, HG, Beach, NM, Meng, XJ, Baker, RB, Zanella, EL and Halbur, PG (2011a). Porcine circovirus type 2 (PCV2) vaccination is effective in reducing disease and PCV2 shedding in semen of boars concurrently infected with PCV2 and Mycoplasma hyopneumoniae. Theriogenology 76: 351–360.CrossRefGoogle ScholarPubMed
Opriessnig, T, Meng, XJ and Halbur, PG (2007). Porcine circovirus type 2 associated disease: update on current terminology, clinical manifestations, pathogenesis, diagnosis, and intervention strategies. Journal of Veterinary Diagnostic Investigation 19: 591–615.CrossRefGoogle ScholarPubMed
Opriessnig, T, Patterson, AR, Madson, DM, Pal, N and Halbur, PG (2009a). Comparison of efficacy of commercial one dose and two dose PCV2 vaccines using a mixed PRRSV-PCV2-SIV clinical infection model 2–3-months post vaccination. Vaccine 27: 1002–1007.CrossRefGoogle ScholarPubMed
Opriessnig, T, Patterson, AR, Madson, DM, Pal, N, Rothschild, M, Kuhar, D, Lunney, JK, Juhan, NM, Meng, XJ and Halbur, PG (2009b). Difference in severity of porcine circovirus type 2 (PCV2)-induced pathological lesions between Landrace and Pietrain pigs. Journal of Animal Science 87: 1582–1590.CrossRefGoogle Scholar
Opriessnig, T, Shen, HG, Pal, N, Ramamoorthy, S, Huang, YW, Lager, KM, Beach, NM, Halbur, PG and Meng, XJ (2011b). A live-attenuated chimeric porcine circovirus type 2 (PCV2) vaccine is transmitted to contact pigs but is not upregulated by concurrent infection with porcine parvovirus (PPV) and porcine reproductive and respiratory syndrome virus (PRRSV) and is efficacious in a PCV2b-PRRSV-PPV challenge model. Clinical and Vaccine Immunology 18: 1261–1268.CrossRefGoogle Scholar
Opriessnig, T, Thacker, EL, Yu, S, Fenaux, M, Meng, XJ and Halbur, PG (2004). Experimental reproduction of postweaning multisystemic wasting syndrome in pigs by dual infection with Mycoplasma hyopneumoniae and porcine circovirus type 2. Veterinary Pathology 41: 624–640.CrossRefGoogle ScholarPubMed
Pol, JM, van Leengoed, LA, Stockhofe, N, Kok, G and Wensvoort, G (1997). Dual infections of PRRSV/influenza or PRRSV/Actinobacillus pleuropneumoniae in the respiratory tract. Veterinary Microbiology 55: 259–264.CrossRefGoogle ScholarPubMed
Pomorska-Mól, M, Markowska-Daniel, I, Rachubik, J and Pejsak, Z (2011). Effect of maternal antibodies and pig age on the antibody response after vaccination against Glässers disease. Veterinary Research Communications 35: 337–343.CrossRefGoogle ScholarPubMed
Qiao, S, Feng, L, Bao, D, Guo, J, Wan, B, Xiao, Z, Yang, S and Zhang, G (2011). Porcine reproductive and respiratory syndrome virus and bacterial endotoxin act in synergy to amplify the inflammatory response of infected macrophages. Veterinary Microbiology 149; 213–220.CrossRefGoogle ScholarPubMed
Rekik, MR, Arora, DJ and Dea, S (1994). Genetic variation in swine influenza virus A isolate associated with proliferative and necrotizing pneumonia in pigs. Journal of Clinical Microbiology 32: 515–518.CrossRefGoogle Scholar
Renukaradhya, GJ, Alekseev, K, Jung, K, Fang, Y and Saif, LJ (2010). Porcine reproductive and respiratory syndrome virus-induced immunosuppression exacerbates the inflammatory response to porcine respiratory coronavirus in pigs. Viral Immunology 23: 457–466.CrossRefGoogle ScholarPubMed
Rodríguez-Ropón, A, Hernández-Jauregui, P, Sánchez-Torres, L, Favila-Castillo, L, Estrada-Parra, S, Moreno-López, J and Kennedy, S (2003). Apoptosis in lymph nodes and changes in lymphocyte subpopulations in peripheral blood of pigs infected with porcine rubulavirus. Journal of Comparative Pathology 128: 1–8.CrossRefGoogle ScholarPubMed
Ross, RF, Hall, JE, Orning, AP and Dale, SE (1972). Characterization of an Actinobacillus isolates from the sow vagina. International Journal of Systemic Bacteriology 22: 39–46.CrossRefGoogle Scholar
Rovira, A, Balasch, M, Segalés, J, García, L, Plana-Durán, J, Rosell, C, Ellerbrok, H, Mankertz, A and Domingo, M (2002). Experimental inoculation of conventional pigs with porcine reproductive and respiratory syndrome virus and porcine circovirus 2. Journal of Virology 76: 3232–3239.CrossRefGoogle ScholarPubMed
Sakano, T, Okada, M, Taneda, A, Mukai, T and Sato, S (1997). Effect of Bordetella bronchiseptica and serotype D Pasteurella multocida bacterin-toxoid on the occurrence of atrophic rhinitis after experimental infection with BORD and toxigenic type AP. multocida. Journal of Veterinary Medical Science 59: 55–57.CrossRefGoogle Scholar
Sakano, T, Okada, M, Taneda, A, Ono, M and Sato, S (1992). Experimental atrophic rhinitis in 2 and 4 month old pigs infected sequentially with Bordetella bronchiseptica and toxigenic type D Pasteurella multocida. Veterinary Microbiology 31: 197–206.CrossRefGoogle ScholarPubMed
Sakano, T, Sakurai, K, Furutani, T and Shimizu, T (1984). Immunogenicity and safety of an attenuated Bordetella bronchiseptica vaccine in pigs. American Journal of Veterinary Research 45: 1814–1817.Google ScholarPubMed
Sakano, T, Shibata, I, Samegai, Y, Taneda, A, Okada, M, Irisawa, T and Sato, S (1993). Experimental pneumonia of pigs infected with Aujeszky's disease virus and Actinobacillus pleuropneumoniae. Journal of Veterinary Medical Science 55: 575–579.CrossRefGoogle ScholarPubMed
Segalés, J, Domingo, M, Balasch, M, Solano, GI and Pijoan, C (1998). Ultrastructural study of porcine alveolar macrophages infected in vitro with porcine reproductive and respiratory syndrome (PRRS) virus, with and without Haemophilus parasuis. Journal of Comparative Pathology 118: 231–243.CrossRefGoogle ScholarPubMed
Segalés, J, Domingo, M, Solano, GI and Pijoan, C (1999). Porcine reproductive and respiratory syndrome virus and Haemophilus parasuis antigen distribution in dually infected pigs. Veterinary Microbiology 64: 287–297.CrossRefGoogle ScholarPubMed
Shen, HG, Beach, NM, Huang, YW, Halbur, PG, Meng, XJ and Opriessnig, T (2010). Comparison of commercial and experimental porcine circovirus type 2 (PCV2) vaccines using a triple challenge with PCV2, porcine reproductive and respiratory syndrome virus (PRRSV), and porcine parvovirus (PPV). Vaccine 28: 5960–5966.CrossRefGoogle ScholarPubMed
Shibata, I, Okada, M, Urono, K, Samegai, Y, Ono, M, Sakano, T and Sato, S (1998). Experimental dual infection of cesarean-derived, colostrum-deprived pigs with Mycoplasma hyopneumoniae and pseudorabies virus. Journal of Veterinary Medical Science 60: 295–300.CrossRefGoogle ScholarPubMed
Shibata, I, Yazawa, S, Ono, M and Okuda, Y (2003). Experimental dual infection of specific pathogen-free pigs with porcine reproductive and respiratory syndrome virus and pseudorabies virus. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health 50: 14–19.CrossRefGoogle ScholarPubMed
Shimizu, M, Yamada, S, Kawashima, K, Ohashi, S, Shimizu, S and Ogawa, T (1996). Changes of lymphocyte subpopulations in pigs infected with porcine reproductive and respiratory syndrome (PRRS) virus. Veterinary Immunology and Immunopathology 50: 19–27.CrossRefGoogle ScholarPubMed
Sinha, A, Shen, HG, Schalk, S, Beach, NM, Huang, YW, Halbur, PG, Meng, XJ and Opriessnig, T (2010). Porcine reproductive and respiratory syndrome virus infection at the time of porcine circovirus type 2 vaccination has no impact on vaccine efficacy. Clinical and Vaccine Immunology 17: 1940–1945.CrossRefGoogle ScholarPubMed
Smith, HE, Damman, M, van d, V, Wagenaar, F, Wisselink, HJ, Stockhofe-Zurwieden, N and Smits, MA (1999). Identification and characterization of the cps locus of Streptococcus suis serotype 2: the capsule protects against phagocytosis and is an important virulence factor. Infectious Immunology 67: 1750–1756.CrossRefGoogle ScholarPubMed
Solano, GI, Bautista, E, Molitor, TW, Segalés, J and Pijoan, C (1998). Effect of porcine reproductive and respiratory syndrome virus infection on the clearance of Haemophilus parasuis by porcine alveolar macrophages. Canadian Journal of Veterinary Research 62: 251–256.Google ScholarPubMed
Sorensen, JT, Edwards, S, Noordhuizen, J and Gunnarsson, S (2006). Animal production systems in the industrialised world. Revue Scientifique et Technique 25: 493–503.CrossRefGoogle ScholarPubMed
Steenhard, NR, Jungersen, G, Kokotovic, B, Beshah, E, Dawson, HD, Urban, JF Jr, Roepstorff, A and Thamsborg, SM (2009). Ascaris suum infection negatively affects the response to a Mycoplasma hyopneumoniae vaccination and subsequent challenge infection in pigs. Vaccine 27: 5161–5169.CrossRefGoogle ScholarPubMed
Stewart, TB and Hoyt, PG (2006) Internal parasites. In: Straw, B, Zimmermann, JJ, D'Allaire, S and Taylor, DJ (eds) Diseases of Swine, Vol. 9. Oxford: Blackwell Publishing, pp. 901–914.Google Scholar
Taira, O, Ogawa, H, Nagao, A, Tuchiya, K, Nunoya, T and Ueda, S (2009). Prevalence of swine Torque teno virus genogroups 1 and 2 in Japanese swine with suspected post-weaning multisystemic wasting syndrome and porcine respiratory disease complex. Veterinary Microbiology 139: 347–350.CrossRefGoogle ScholarPubMed
Takada-Iwao, A, Uto, T, Mukai, T, Okada, M, Futo, S and Shibata, I (2007). Evaluation of an indirect enzyme-linked immunosorbent assay (ELISA) using recombinant toxin for detection of antibodies against Pasteurella multocida toxin. Journal of Veterinary Medical Science 69: 581–586.CrossRefGoogle ScholarPubMed
Tanabe, S, Bonifait, L, Fittipaldi, N, Grignon, L, Gottschalk, M and Grenier, D (2010). Pleiotropic effects of polysaccharide capsule loss on selected biological properties of Streptococcus suis. Canadian Journal of Veterinary Research 74: 65–70.Google ScholarPubMed
Thacker, EL (2001). Immunology of the porcine respiratory disease complex. Veterinary Clinics of North America: Food Animal Practice 17: 551–565.Google ScholarPubMed
Thacker, EL, Halbur, PG, Ross, RF, Thanawongnuwech, R and Thacker, BJ (1999). Mycoplasma hyopneumoniae potentiation of porcine reproductive and respiratory syndrome virus-induced pneumonia. Journal of Clinical Microbiology 37: 620–627.CrossRefGoogle ScholarPubMed
Thacker, EL, Thacker, BJ and Janke, BH (2001). Interaction between Mycoplasma hyopneumoniae and swine influenza virus. Journal of Clinical Microbiology 39: 2525–2530.CrossRefGoogle ScholarPubMed
Thacker, EL, Thacker, BJ, Kuhn, M, Hawkins, PA and Waters, WR (2000a). Evaluation of local and systemic immune responses induced by intramuscular injection of a Mycoplasma hyopneumoniae bacterin to pigs. American Journal of Veterinary Research 61: 1384–1389.CrossRefGoogle ScholarPubMed
Thacker, EL, Thacker, BJ, Young, TF and Halbur, PG (2000b). Effect of vaccination on the potentiation of porcine reproductive and respiratory syndrome virus (PRRSV)-induced pneumonia by Mycoplasma hyopneumoniae. Vaccine 18: 1244–1252.CrossRefGoogle ScholarPubMed
Thanawongnuwech, R, Brown, GB, Halbur, PG, Roth, JA, Royer, RL and Thacker, BJ (2000). Pathogenesis of porcine reproductive and respiratory syndrome virus-induced increase in susceptibility to Streptococcus suis infection. Veterinary Pathology 37: 143–152.CrossRefGoogle ScholarPubMed
Thanawongnuwech, R, Halbur, PG, Ackermann, MR, Thacker, EL and Royer, RL (1998a). Effects of low (modified-live virus vaccine) and high (VR-2385)-virulence strains of porcine reproductive and respiratory syndrome virus on pulmonary clearance of copper particles in pigs. Veterinary Pathology 35: 398–406.CrossRefGoogle ScholarPubMed
Thanawongnuwech, R, Thacker, B, Halbur, P and Thacker, EL (2004). Increased production of proinflammatory cytokines following infection with porcine reproductive and respiratory syndrome virus and Mycoplasma hyopneumoniae. Clinical and Diagnostic Laboratory Immunology 11: 901–908.Google ScholarPubMed
Thanawongnuwech, R, Thacker, EL and Halbur, PG (1997). Effect of porcine reproductive and respiratory syndrome virus (PRRSV) (isolate ATCC VR-2385) infection on bactericidal activity of porcine pulmonary intravascular macrophages (PIMs): in vitro comparisons with pulmonary alveolar macrophages (PAMs). Veterinary Immunology and Immunopathology 59: 323–335.CrossRefGoogle ScholarPubMed
Thanawongnuwech, R, Thacker, EL and Halbur, PG (1998b). Influence of pig age on virus titer and bactericidal activity of porcine reproductive and respiratory syndrome virus (PRRSV)-infected pulmonary intravascular macrophages (PIMs). Veterinary Microbiology 63: 177–187.CrossRefGoogle ScholarPubMed
Thanawongnuwech, R, Young, TF, Thacker, BJ and Thacker, EL (2001). Differential production of proinflammatory cytokines: in vitro PRRSV and Mycoplasma hyopneumoniae coinfection model. Veterinary Immunology and Immunopathology 79: 115–127.CrossRefGoogle Scholar
Tjørnehøj, K, Eriksen, L, Aalbaek, B and Nansen, P (1992). Interaction between Ascaris suum and Pasteurella multocida in the lungs of mice. Parasitology Research 78: 525–528.CrossRefGoogle ScholarPubMed
Van Gucht, S, Labarque, G and Van Reeth, K (2004). The combination of PRRS virus and bacterial endotoxin as a model for multifactorial respiratory disease in pigs. Veterinary Immunology and Immunopathology 102: 165–178.CrossRefGoogle Scholar
Van Reeth, K and Nauwynck, H (2000). Proinflammatory cytokines and viral respiratory disease in pigs. Veterinary Research 31: 187–213.CrossRefGoogle ScholarPubMed
Van Reeth, K, Nauwynck, H and Pensaert, M (1996). Dual infections of feeder pigs with porcine reproductive and respiratory syndrome virus followed by porcine respiratory coronavirus or swine influenza virus: a clinical and virological study. Veterinary Microbiology 48: 325–335.CrossRefGoogle ScholarPubMed
Van Reeth, K, Nauwynck, H and Pensaert, M (2000). A potential role for tumour necrosis factor-alpha in synergy between porcine respiratory coronavirus and bacterial lipopolysaccharide in the induction of respiratory disease in pigs. Journal of Medical Microbiology 49: 613–620.CrossRefGoogle ScholarPubMed
Van Reeth, K and Pensaert, MB (1994). Porcine respiratory coronavirus-mediated interference against influenza virus replication in the respiratory tract of feeder pigs. American Journal of Veterinary Research 55: 1275–1281.CrossRefGoogle ScholarPubMed
Vincent, AL, Thacker, BJ, Halbur, PG, Rothschild, MF and Thacker, EL (2005). In vitro susceptibility of macrophages to porcine reproductive and respiratory syndrome virus varies between genetically diverse lines of pigs. Viral Immunology 18: 506–512.CrossRefGoogle ScholarPubMed
Vincent, AL, Thacker, BJ, Halbur, PG, Rothschild, MF and Thacker, EL (2006). An investigation of susceptibility to porcine reproductive and respiratory syndrome virus between two genetically diverse commercial lines of pigs. Journal of Animal Science 84: 49–57.CrossRefGoogle ScholarPubMed
Wei, H, Lenz, SD, Van Alstine, WG, Stevenson, GW, Langohr, IM and Pogranichniy, RM (2010). Infection of cesarean-derived colostrum-deprived pigs with porcine circovirus type 2 and swine influenza virus. Comparative Medicine 60: 45–50.Google ScholarPubMed
Wills, RW, Doster, AR, Galeota, JA, Sur, JH and Osorio, FA (2003). Duration of infection and proportion of pigs persistently infected with porcine reproductive and respiratory syndrome virus. Journal of Clinical Microbiology 41: 58–62.CrossRefGoogle ScholarPubMed
Willson, PJ, Falk, G and Klashinsky, S (1987). Detection of Actinobacillus pleuropneumoniae infection in pigs. Canadian Veterinary Journal 28: 111–116.Google ScholarPubMed
Wilson, BA and Ho, M (2010). Recent insights into Pasteurella multocida toxin and other G-protein-modulating bacterial toxins. Future Microbiology 5: 1185–1201.CrossRefGoogle ScholarPubMed
White, M (2011). Porcine respiratory disease complex (PRDC): Part 2: Non-infectious factors. Livestock 16: 44–46.Google Scholar
Xu, M, Wang, S, Li, L, Lei, L, Liu, Y, Shi, W, Wu, J, Li, L, Rong, F, Xu, M, Sun, G, Xiang, H and Cai, X (2010). Secondary infection with Streptococcus suis serotype 7 increases the virulence of highly pathogenic porcine reproductive and respiratory syndrome virus in pigs. Virology Journal 7: 184.CrossRefGoogle ScholarPubMed
Young, TF, Thacker, EL, Erickson, BZ and Ross, RF (2000). A tissue culture system to study respiratory ciliary epithelial adherence of selected swine mycoplasmas. Veterinary Microbiology 71: 269–279.CrossRefGoogle ScholarPubMed
Zhang, H, Lunney, JK, Baker, RB and Opriessnig, T (2011). Cytokine and chemokine mRNA expression profiles in tracheobronchial lymph nodes from pigs singularly infected or coinfected with porcine circovirus type 2 (PCV2) and Mycoplasma hyopneumoniae (MHYO). Veterinary Immunology and Immunopathology 140: 152–158.CrossRefGoogle ScholarPubMed
Zheng, P, Zhao, YX, Zhang, AD, Kang, C, Chen, HC and Jin, ML (2009). Pathologic analysis of the brain from Streptococcus suis type 2 experimentally infected pigs. Veterinary Pathology 46: 531–535.CrossRefGoogle ScholarPubMed