Infection dynamics, transmission, and evolution after an outbreak of porcine reproductive and respiratory syndrome virus

The present study was aimed at describing the infection dynamics, transmission, and evolution of porcine reproductive and respiratory syndrome virus (PRRSV) after an outbreak in a 300-sow farrow-to-wean farm that was implementing a vaccination program. Three subsequent batches of piglets (9–11 litte...

Full description

Bibliographic Details
Main Authors: Hepzibar Clilverd, Gerard Martín-Valls, Yanli Li, Marga Martín, Martí Cortey, Enric Mateu
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1109881/full
_version_ 1828038311415906304
author Hepzibar Clilverd
Gerard Martín-Valls
Yanli Li
Marga Martín
Martí Cortey
Enric Mateu
author_facet Hepzibar Clilverd
Gerard Martín-Valls
Yanli Li
Marga Martín
Martí Cortey
Enric Mateu
author_sort Hepzibar Clilverd
collection DOAJ
description The present study was aimed at describing the infection dynamics, transmission, and evolution of porcine reproductive and respiratory syndrome virus (PRRSV) after an outbreak in a 300-sow farrow-to-wean farm that was implementing a vaccination program. Three subsequent batches of piglets (9–11 litters/batch) were followed 1.5 (Batch 1), 8 (Batch 2), and 12 months after (Batch 3) from birth to 9 weeks of age. The RT-qPCR analysis showed that shortly after the outbreak (Batch 1), one third of sows were delivering infected piglets and the cumulative incidence reached 80% by 9 weeks of age. In contrast, in Batch 2, only 10% animals in total got infected in the same period. In Batch 3, 60% litters had born-infected animals and cumulative incidence rose to 78%. Higher viral genetic diversity was observed in Batch 1, with 4 viral clades circulating, of which 3 could be traced to vertical transmission events, suggesting the existence of founder viral variants. In Batch 3 though only one variant was found, distinguishable from those circulating previously, suggesting that a selection process had occurred. ELISA antibodies at 2 weeks of age were significantly higher in Batch 1 and 3 compared to Batch 2, while low levels of neutralizing antibodies were detected in either piglets or sows in all batches. In addition, some sows present in Batch 1 and 3 delivered infected piglets twice, and the offspring were devoid of neutralizing antibodies at 2 weeks of age. These results suggest that a high viral diversity was featured at the initial outbreak followed by a phase of limited circulation, but subsequently an escape variant emerged in the population causing a rebound of vertical transmission. The presence of unresponsive sows that had vertical transmission events could have contributed to the transmission. Moreover, the records of contacts between animals and the phylogenetic analyses allowed to trace back 87 and 47% of the transmission chains in Batch 1 and 3, respectively. Most animals transmitted the infection to 1–3 pen-mates, but super-spreaders were also identified. One animal that was born-viremic and persisted as viremic for the whole study period did not contribute to transmission.
first_indexed 2024-04-10T16:25:10Z
format Article
id doaj.art-da897b4507d949c1bd6214d1871e5cbd
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-04-10T16:25:10Z
publishDate 2023-02-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-da897b4507d949c1bd6214d1871e5cbd2023-02-09T08:00:59ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-02-011410.3389/fmicb.2023.11098811109881Infection dynamics, transmission, and evolution after an outbreak of porcine reproductive and respiratory syndrome virusHepzibar ClilverdGerard Martín-VallsYanli LiMarga MartínMartí CorteyEnric MateuThe present study was aimed at describing the infection dynamics, transmission, and evolution of porcine reproductive and respiratory syndrome virus (PRRSV) after an outbreak in a 300-sow farrow-to-wean farm that was implementing a vaccination program. Three subsequent batches of piglets (9–11 litters/batch) were followed 1.5 (Batch 1), 8 (Batch 2), and 12 months after (Batch 3) from birth to 9 weeks of age. The RT-qPCR analysis showed that shortly after the outbreak (Batch 1), one third of sows were delivering infected piglets and the cumulative incidence reached 80% by 9 weeks of age. In contrast, in Batch 2, only 10% animals in total got infected in the same period. In Batch 3, 60% litters had born-infected animals and cumulative incidence rose to 78%. Higher viral genetic diversity was observed in Batch 1, with 4 viral clades circulating, of which 3 could be traced to vertical transmission events, suggesting the existence of founder viral variants. In Batch 3 though only one variant was found, distinguishable from those circulating previously, suggesting that a selection process had occurred. ELISA antibodies at 2 weeks of age were significantly higher in Batch 1 and 3 compared to Batch 2, while low levels of neutralizing antibodies were detected in either piglets or sows in all batches. In addition, some sows present in Batch 1 and 3 delivered infected piglets twice, and the offspring were devoid of neutralizing antibodies at 2 weeks of age. These results suggest that a high viral diversity was featured at the initial outbreak followed by a phase of limited circulation, but subsequently an escape variant emerged in the population causing a rebound of vertical transmission. The presence of unresponsive sows that had vertical transmission events could have contributed to the transmission. Moreover, the records of contacts between animals and the phylogenetic analyses allowed to trace back 87 and 47% of the transmission chains in Batch 1 and 3, respectively. Most animals transmitted the infection to 1–3 pen-mates, but super-spreaders were also identified. One animal that was born-viremic and persisted as viremic for the whole study period did not contribute to transmission.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1109881/fullporcine reproductive and respiratory syndrome virusgenetic diversityevolutionfounder effectsuper-spreaderneutralizing antibodies
spellingShingle Hepzibar Clilverd
Gerard Martín-Valls
Yanli Li
Marga Martín
Martí Cortey
Enric Mateu
Infection dynamics, transmission, and evolution after an outbreak of porcine reproductive and respiratory syndrome virus
Frontiers in Microbiology
porcine reproductive and respiratory syndrome virus
genetic diversity
evolution
founder effect
super-spreader
neutralizing antibodies
title Infection dynamics, transmission, and evolution after an outbreak of porcine reproductive and respiratory syndrome virus
title_full Infection dynamics, transmission, and evolution after an outbreak of porcine reproductive and respiratory syndrome virus
title_fullStr Infection dynamics, transmission, and evolution after an outbreak of porcine reproductive and respiratory syndrome virus
title_full_unstemmed Infection dynamics, transmission, and evolution after an outbreak of porcine reproductive and respiratory syndrome virus
title_short Infection dynamics, transmission, and evolution after an outbreak of porcine reproductive and respiratory syndrome virus
title_sort infection dynamics transmission and evolution after an outbreak of porcine reproductive and respiratory syndrome virus
topic porcine reproductive and respiratory syndrome virus
genetic diversity
evolution
founder effect
super-spreader
neutralizing antibodies
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1109881/full
work_keys_str_mv AT hepzibarclilverd infectiondynamicstransmissionandevolutionafteranoutbreakofporcinereproductiveandrespiratorysyndromevirus
AT gerardmartinvalls infectiondynamicstransmissionandevolutionafteranoutbreakofporcinereproductiveandrespiratorysyndromevirus
AT yanlili infectiondynamicstransmissionandevolutionafteranoutbreakofporcinereproductiveandrespiratorysyndromevirus
AT margamartin infectiondynamicstransmissionandevolutionafteranoutbreakofporcinereproductiveandrespiratorysyndromevirus
AT marticortey infectiondynamicstransmissionandevolutionafteranoutbreakofporcinereproductiveandrespiratorysyndromevirus
AT enricmateu infectiondynamicstransmissionandevolutionafteranoutbreakofporcinereproductiveandrespiratorysyndromevirus