Domestic sheep show average coxiella burnetii seropositivity generations after a sheep-associated human Q fever outbreak and lack detectable shedding by placental, vaginal, and fecal routes

Authors: OLIVEIRA, RYAN - Washington State University; Mousel, Michelle; PABILONIA, KRISTY - Colorado State University; Highland, Margaret; Taylor, Joshua - Bret; Knowles Jr, Donald; White, Stephen

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/31/2017
Publication Date: 11/15/2017
Citation: Oliveira, R.D., Mousel, M.R., Pabilonia, K.L., Highland, M.A., Taylor, J.B., Knowles Jr, D.P., White, S.N. 2017. Domestic sheep show average coxiella burnetii seropositivity generations after a sheep-associated human Q fever outbreak and lack detectable shedding by placental, vaginal, and fecal routes. PLoS One. 12(11):e0188054. https://doi.org/10.1371/journal.pone.0188054.
DOI: https://doi.org/10.1371/journal.pone.0188054

Interpretive Summary: Coxiella burnetii is a globally distributed bacterium harbored by sheep, goats, and cattle, in which it causes abortions. These domestic livestock are believed to account for most human exposure, and in humans C. burnetii can cause a syndrome known as Q fever, a flu-like illness with the potential for chronic and sometimes fatal complications. A recent Netherlands outbreak resulted in over 4,100 human cases with estimated costs of more than 300 million euro/dollars, and sheep within the U.S. may present a similar large outbreak risk. In this study, we assessed bacterial shedding and serum antibody levels to C. burnetii in 100 sheep from an Idaho farm associated with a 1984 human Q fever outbreak. While five out of 100 sheep had detectable antibodies indicating past exposure at some point in their lives, zero shed bacteria were detected by quantitative PCR of placentas (gold standard diagnostic sample), vaginal swabs and fecal samples. No vaccine for C. burnetii is licensed in the U.S., and no farm intervention measures have been specifically targeted against C. burnetii since the outbreak. We provide an update of C. burnetii shedding in U.S. sheep and demonstrate a flock's ability to progress to lack of C. burnetii shedding after an outbreak event, even in the absence of vaccination or other targeted interventions.

Technical Abstract: Coxiella burnetii is a globally distributed zoonotic bacterial pathogen that causes abortions in ruminant livestock. In humans, an influenza-like illness results with the potential for hospitalization, chronic infection, abortion, and fatal endocarditis. Ruminant livestock, particularly small ruminants, are hypothesized to be the primary transmission source to humans. A recent Netherlands outbreak from 2007±2010 traced to dairy goats resulted in over 4,100 human cases with estimated costs of more than 300 million euros. Smaller human Q fever outbreaks of small ruminant origin have occurred in the United States, and characterizing shedding is important to understand the risk of future outbreaks. In this study, we assessed bacterial shedding and seroprevalence in 100 sheep from an Idaho location associated with a 1984 human Q fever outbreak. We observed 5% seropositivity, which was not significantly different from the national average of 2.7% for the U.S. (P>0.05). Furthermore, C. burnetii was not detected by quantitative PCR from placentas, vaginal swabs, or fecal samples. Specifically, a three-target quantitative PCR of placenta identified 0.0% shedding (exact 95% confidence interval: 0.0%-2.9%). While presence of seropositive individuals demonstrates some historical C. burnetii exposure, the placental sample confidence interval suggests 2016 shedding events were rare or absent. The location maintained the flock with little or no depopulation in 1984 and without C. burnetii vaccination during or since 1984. It is not clear how a zero-shedding rate was achieved in these sheep beyond natural immunity, and more work is required to discover and assess possible factors that may contribute towards achieving zero-shedding status. We provide the first U.S. sheep placental C. burnetii shedding update in over 60 years and demonstrate potential for C. burnetii shedding to reach undetectable levels after an outbreak event even in the absence of targeted interventions, such as vaccination.