Microbiome associations in pigs with the best and worst clinical outcomes following co-infection with porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2)
Abstract
Co-infections involving porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2) are common and contribute to a range of polymicrobial disease syndromes in swine and on a world-wide basis. Both viruses compromise host defenses, resulting in increased susceptibility to infections by primary and secondary pathogens that can affect growth performance as well as increased morbidity and mortality. An experimental population of 95 pigs was co-infected with PRRSV and PCV2. At 70 days post-infection (dpi), 20 representative pigs were selected as having the best or worst clinical outcome based on average daily gain (ADG) and the presence of clinical disease. Moreover, the worst clinical outcome pigs had prolonged and greater levels of viremia as measured by qPCR. Serum, lung and fecal samples collected at 70 dpi were analyzed using a comprehensive DNA microarray technology, the Lawrence Livermore Microbial Detection Array, to detect over 8000 microbes. Bacterial species, such as Bacillus cereus, were detected at a higher rate in the serum of worst performing pigs. At the level of the fecal microbiome, the overall microbial diversity was lower in the worst clinical outcome group. The results reinforce the importance of pathogen load in determining clinical outcome and suggestmore »
- Authors:
-
- Kansas State Univ., Manhattan, KS (United States)
- Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1258531
- Alternate Identifier(s):
- OSTI ID: 1348263
- Report Number(s):
- LLNL-JRNL-679863
Journal ID: ISSN 0378-1135
- Grant/Contract Number:
- AC52-07NA27344; 14ERD081
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- Veterinary Microbiology
- Additional Journal Information:
- Journal Volume: 188; Journal Issue: C; Journal ID: ISSN 0378-1135
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Swine; Microbiome; Porcine reproductive and respiratory syndrome virus; Porcine circovirus type 2; Clinical outcome; Virus load
Citation Formats
Niederwerder, Megan C., Jaing, Crystal J., Thissen, James B., Cino-Ozuna, Ada Giselle, McLoughlin, Kevin S., and Rowland, Raymond R. R. Microbiome associations in pigs with the best and worst clinical outcomes following co-infection with porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2). United States: N. p., 2016.
Web. doi:10.1016/j.vetmic.2016.03.008.
Niederwerder, Megan C., Jaing, Crystal J., Thissen, James B., Cino-Ozuna, Ada Giselle, McLoughlin, Kevin S., & Rowland, Raymond R. R. Microbiome associations in pigs with the best and worst clinical outcomes following co-infection with porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2). United States. https://doi.org/10.1016/j.vetmic.2016.03.008
Niederwerder, Megan C., Jaing, Crystal J., Thissen, James B., Cino-Ozuna, Ada Giselle, McLoughlin, Kevin S., and Rowland, Raymond R. R. 2016.
"Microbiome associations in pigs with the best and worst clinical outcomes following co-infection with porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2)". United States. https://doi.org/10.1016/j.vetmic.2016.03.008. https://www.osti.gov/servlets/purl/1258531.
@article{osti_1258531,
title = {Microbiome associations in pigs with the best and worst clinical outcomes following co-infection with porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2)},
author = {Niederwerder, Megan C. and Jaing, Crystal J. and Thissen, James B. and Cino-Ozuna, Ada Giselle and McLoughlin, Kevin S. and Rowland, Raymond R. R.},
abstractNote = {Co-infections involving porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2) are common and contribute to a range of polymicrobial disease syndromes in swine and on a world-wide basis. Both viruses compromise host defenses, resulting in increased susceptibility to infections by primary and secondary pathogens that can affect growth performance as well as increased morbidity and mortality. An experimental population of 95 pigs was co-infected with PRRSV and PCV2. At 70 days post-infection (dpi), 20 representative pigs were selected as having the best or worst clinical outcome based on average daily gain (ADG) and the presence of clinical disease. Moreover, the worst clinical outcome pigs had prolonged and greater levels of viremia as measured by qPCR. Serum, lung and fecal samples collected at 70 dpi were analyzed using a comprehensive DNA microarray technology, the Lawrence Livermore Microbial Detection Array, to detect over 8000 microbes. Bacterial species, such as Bacillus cereus, were detected at a higher rate in the serum of worst performing pigs. At the level of the fecal microbiome, the overall microbial diversity was lower in the worst clinical outcome group. The results reinforce the importance of pathogen load in determining clinical outcome and suggest an important role of microbial diversity as a contributing factor in disease.},
doi = {10.1016/j.vetmic.2016.03.008},
url = {https://www.osti.gov/biblio/1258531},
journal = {Veterinary Microbiology},
issn = {0378-1135},
number = C,
volume = 188,
place = {United States},
year = {Thu Mar 10 00:00:00 EST 2016},
month = {Thu Mar 10 00:00:00 EST 2016}
}
Web of Science
Works referenced in this record:
Enterotypes of the human gut microbiome
journal, April 2011
- Arumugam, Manimozhiyan; Raes, Jeroen; Pelletier, Eric
- Nature, Vol. 473, Issue 7346
Profiling the gastrointestinal microbiota in response to Salmonella: Low versus high Salmonella shedding in the natural porcine host
journal, June 2013
- Bearson, Shawn M. D.; Allen, Heather K.; Bearson, Bradley L.
- Infection, Genetics and Evolution, Vol. 16
The effect of selected factors on the survival of Bacillus cereus in the human gastrointestinal tract
journal, May 2015
- Berthold-Pluta, Anna; Pluta, Antoni; Garbowska, Monika
- Microbial Pathogenesis, Vol. 82
Evidence for a major QTL associated with host response to Porcine Reproductive and Respiratory Syndrome Virus challenge1
journal, June 2012
- Boddicker, N.; Waide, E. H.; Rowland, R. R. R.
- Journal of Animal Science, Vol. 90, Issue 6
Pathogenesis of porcine reproductive and respiratory syndrome virus
journal, June 2012
- Chand, Ranjni J.; Trible, Benjamin R.; Rowland, Raymond RR
- Current Opinion in Virology, Vol. 2, Issue 3
Molecular Characterization of Porcine Reproductive and Respiratory Syndrome Virus, a Member of the Arterivirus Group
journal, March 1993
- Conzelmann, Karl-Klaus; Visser, Nico; Van Woensel, Peter
- Virology, Vol. 193, Issue 1
Characterization of the Fecal Microbiota of Pigs before and after Inoculation with “Brachyspira hampsonii”
journal, August 2014
- Costa, Matheus O.; Chaban, Bonnie; Harding, John C. S.
- PLoS ONE, Vol. 9, Issue 8
The Microbiome and the Lung
journal, August 2014
- Cui, Lijia; Morris, Alison; Huang, Laurence
- Annals of the American Thoracic Society, Vol. 11, Issue Supplement 4
Microbiota in Allergy and Asthma and the Emerging Relationship with the Gut Microbiome
journal, May 2015
- Fujimura, Kei E.; Lynch, Susan V.
- Cell Host & Microbe, Vol. 17, Issue 5
A microbial detection array (MDA) for viral and bacterial detection
journal, January 2010
- Gardner, Shea N.; Jaing, Crystal J.; McLoughlin, Kevin S.
- BMC Genomics, Vol. 11, Issue 1
Immunopathogenesis of porcine reproductive and respiratory syndrome in the respiratory tract of pigs
journal, February 2013
- Gómez-Laguna, Jaime; Salguero, Francisco J.; Pallarés, Francisco J.
- The Veterinary Journal, Vol. 195, Issue 2
Development of a real-time PCR method for Firmicutes and Bacteroidetes in faeces and its application to quantify intestinal population of obese and lean pigs
journal, November 2008
- Guo, X.; Xia, X.; Tang, R.
- Letters in Applied Microbiology, Vol. 47, Issue 5
Temporal analysis of the effect of extruded flaxseed on the swine gut microbiota
journal, October 2014
- Holman, Devin B.; Baurhoo, Bushansingh; Chénier, Martin R.
- Canadian Journal of Microbiology, Vol. 60, Issue 10
Application of a pathogen microarray for the analysis of viruses and bacteria in clinical diagnostic samples from pigs
journal, April 2015
- Jaing, Crystal J.; Thissen, James B.; Gardner, Shea N.
- Journal of Veterinary Diagnostic Investigation, Vol. 27, Issue 3
Effects on weight gain and gut microbiota in rats given bacterial supplements and a high-energy-dense diet from fetal life through to 6 months of age
journal, March 2011
- Karlsson, Caroline L. J.; Molin, Göran; Fåk, Frida
- British Journal of Nutrition, Vol. 106, Issue 6
Longitudinal investigation of the age-related bacterial diversity in the feces of commercial pigs
journal, November 2011
- Kim, Hyeun Bum; Borewicz, Klaudyna; White, Bryan A.
- Veterinary Microbiology, Vol. 153, Issue 1-2
Comparative fecal metagenomics unveils unique functional capacity of the swine gut
journal, January 2011
- Lamendella, Regina; Santo Domingo, Jorge W.; Ghosh, Shreya
- BMC Microbiology, Vol. 11, Issue 1
In-feed antibiotic effects on the swine intestinal microbiome
journal, January 2012
- Looft, T.; Johnson, T. A.; Allen, H. K.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 5
Vaccination with a Porcine Reproductive and Respiratory Syndrome (PRRS) Modified Live Virus Vaccine Followed by Challenge with PRRS Virus and Porcine Circovirus Type 2 (PCV2) Protects against PRRS but Enhances PCV2 Replication and Pathogenesis Compared to Results for Nonvaccinated Cochallenged Controls
journal, October 2015
- Niederwerder, Megan C.; Bawa, Bhupinder; Serão, Nick V. L.
- Clinical and Vaccine Immunology, Vol. 22, Issue 12
Concurrent infections are important for expression of porcine circovirus associated disease
journal, March 2012
- Opriessnig, Tanja; Halbur, Patrick G.
- Virus Research, Vol. 164, Issue 1-2
Current State of Knowledge on Porcine Circovirus Type 2-Associated Lesions
journal, June 2012
- Opriessnig, T.; Langohr, I.
- Veterinary Pathology, Vol. 50, Issue 1
Porcine Circovirus Type 2 (PCV-2) Coinfections in US Field Cases of Postweaning Multisystemic Wasting Syndrome (PMWS)
journal, January 2002
- Pallarés, F. J.; Halbur, P. G.; Opriessnig, T.
- Journal of Veterinary Diagnostic Investigation, Vol. 14, Issue 6
Exposure to environmental stressors result in increased viral load and further reduction of production parameters in pigs experimentally infected with PCV2b
journal, June 2015
- Patterson, Robert; Nevel, Amanda; Diaz, Adriana V.
- Veterinary Microbiology, Vol. 177, Issue 3-4
Clinical and pathological observations on pigs with postweaning multisystemic wasting syndrome
journal, September 2001
- Quintana, J.; Segalés, J.; Rosell, C.
- Veterinary Record, Vol. 149, Issue 12
Variation in resistance to the Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) in Pietrain and Miniature pigs
journal, April 2010
- Reiner, G.; Willems, H.; Pesch, S.
- Journal of Animal Breeding and Genetics, Vol. 127, Issue 2
The Microbial Detection Array for Detection of Emerging Viruses in Clinical Samples - A Useful Panmicrobial Diagnostic Tool
journal, June 2014
- Rosenstierne, Maiken W.; McLoughlin, Kevin S.; Olesen, Majken Lindholm
- PLoS ONE, Vol. 9, Issue 6
Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women
journal, March 2010
- Santacruz, A.; Collado, M. C.; García-Valdés, L.
- British Journal of Nutrition, Vol. 104, Issue 1
Modulation of Systemic Immune Responses through Commensal Gastrointestinal Microbiota
journal, January 2013
- Schachtschneider, Kyle M.; Yeoman, Carl J.; Isaacson, Richard E.
- PLoS ONE, Vol. 8, Issue 1
Disease tolerance mediated by microbiome E. coli involves inflammasome and IGF-1 signaling
journal, October 2015
- Schieber, A. M. P.; Lee, Y. M.; Chang, M. W.
- Science, Vol. 350, Issue 6260
Porcine circovirus type 2 (PCV2) infections: Clinical signs, pathology and laboratory diagnosis
journal, March 2012
- Segalés, Joaquim
- Virus Research, Vol. 164, Issue 1-2
Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients
journal, October 2008
- Sokol, H.; Pigneur, B.; Watterlot, L.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 43
Antibody responses following vaccination versus infection in a porcine circovirus-type 2 (PCV2) disease model show distinct differences in virus neutralization and epitope recognition
journal, June 2012
- Trible, Benjamin R.; Ramirez, Alejandro; Suddith, Andrew
- Vaccine, Vol. 30, Issue 27
Works referencing / citing this record:
Comparative analysis of the fecal microbiota from different species of domesticated and wild suids
journal, September 2019
- Correa-Fiz, Florencia; Blanco-Fuertes, Miguel; Navas, Maria J.
- Scientific Reports, Vol. 9, Issue 1
Nasal and gut microbiota for sows of different health status within six commercial swine farms from one swine production system
posted_content, April 2019
- Arruda, Andréia Gonçalves; Deblais, Loic; Hale, Vanessa
- BioRxiv
Investigating the relationship between vaginal microbiota and host genetics and their impact on immune response and farrowing traits in commercial gilts
journal, August 2019
- Sanglard, Leticia P.; Schmitz‐Esser, Stephan; Gray, Kent A.
- Journal of Animal Breeding and Genetics, Vol. 137, Issue 1
Insights into the epidemic characteristics and evolutionary history of the novel porcine circovirus type 3 in southern China
journal, November 2017
- Fu, X.; Fang, B.; Ma, J.
- Transboundary and Emerging Diseases, Vol. 65, Issue 2
Prevalence of porcine circovirus type 3 in pigs in the southeastern Chinese province of Zhejiang
journal, July 2019
- Geng, Shichao; Luo, Hao; Liu, Yajie
- BMC Veterinary Research, Vol. 15, Issue 1
Coinfections and their molecular consequences in the porcine respiratory tract
journal, June 2020
- Saade, Georges; Deblanc, Céline; Bougon, Juliette
- Veterinary Research, Vol. 51, Issue 1
Axiom Microbiome Array, the next generation microarray for high-throughput pathogen and microbiome analysis
journal, February 2019
- Thissen, James B.; Be, Nicholas A.; McLoughlin, Kevin
- PLOS ONE, Vol. 14, Issue 2
Co-Infection of Swine with Porcine Circovirus Type 2 and Other Swine Viruses
journal, February 2019
- Ouyang, Ting; Zhang, Xinwei; Liu, Xiaohua
- Viruses, Vol. 11, Issue 2
Coinfections and their molecular consequences in the porcine respiratory tract.
text, January 2020
- Saade, Georges; Deblanc, Céline; Bougon, Juliette
- BioMed Central
Characterisation of Bergeyella spp. isolated from the nasal cavities of piglets
journal, April 2018
- Lorenzo de Arriba, M.; Lopez-Serrano, S.; Galofre-Mila, N.
- The Veterinary Journal, Vol. 234
Comparative analysis of the fecal microbiota from different species of domesticated and wild suids
journal, September 2019
- Correa-Fiz, Florencia; Blanco-Fuertes, Miguel; Navas, Maria J.
- Scientific Reports, Vol. 9, Issue 1
Prevalence of porcine circovirus type 3 in pigs in the southeastern Chinese province of Zhejiang
journal, July 2019
- Geng, Shichao; Luo, Hao; Liu, Yajie
- BMC Veterinary Research, Vol. 15, Issue 1
Fecal Microbiota Transplantation Is Associated With Reduced Morbidity and Mortality in Porcine Circovirus Associated Disease
journal, July 2018
- Niederwerder, Megan C.; Constance, Laura A.; Rowland, Raymond R. R.
- Frontiers in Microbiology, Vol. 9
Change of Gut Microbiota in PRRSV-Resistant Pigs and PRRSV-Susceptible Pigs from Tongcheng Pigs and Large White Pigs Crossed Population upon PRRSV Infection
journal, June 2022
- Wang, Tengfei; Guan, Kaifeng; Su, Qiuju
- Animals, Vol. 12, Issue 12
Co-Infection of Swine with Porcine Circovirus Type 2 and Other Swine Viruses
journal, February 2019
- Ouyang, Ting; Zhang, Xinwei; Liu, Xiaohua
- Viruses, Vol. 11, Issue 2