Epidemiol Infect. 2016 Nov; 144(15): 3148–3165

Occurrence and spread of influenza A(H1N1)pdm09 virus infection in Norwegian pig herds based on active serosurveillance from 2010 to 2014

ER,1,*E. SKJERVE,2E. BRUN,1 T. FRAMSTAD,2 and B. LIUM1

1Norwegian Veterinary Institute, Oslo, Norway

2Norwegian University of Life Sciences, Campus Adamstuen, Oslo, Norway

*Author for correspondence: Dr Jwee Chiek Er, Norwegian Veterinary Institute, P.O. Box 750, 0106 Oslo, Norway. (Email: chiek.er@vetinst.no)

 

SUMMARY

The incursion of influenza A(H1N1)pdm09 virus was detected by Norway’s active serosurveillance of its pig population in 2009. Since then, surveillance data from 2010 to 2014 revealed that 54% of 5643 herd tests involving 1567 pig herds and 28% of 23 036 blood samples screened positive for antibodies against influenza A virus. Positive herds were confirmed to have influenza A(H1N1)pdm09 virus infection by haemagglutination inhibition test. In 50% of positive herd tests, ⩾60% of the sampled pigs in each herd had antibodies against influenza A(H1N1)pdm09 virus. This within-herd animal seroprevalence did not vary for type of production, herd size or year of test. The overall running mean of national herd seroprevalence, and annual herd incidence risks fluctuated narrowly around the means of 45% and 32%, respectively, with the highest levels recorded in the three densest pig-producing counties. The probability of a herd being seropositive varied in the five production classes, which were sow pools, multiplier herds, conventional sow herds, nucleus herds, and fattening herds in descending order of likelihood. Large herds were more likely to be seropositive. Seropositive herds were highly likely to be seropositive the following year. The study shows that influenza A(H1N1)pdm09 virus is established in the Norwegian pig population with recurrent and new herd infections every year with the national herd seroprevalence in 2014 hovering at around 43% (95% confidence interval 40–46%).

Key words: Active serosurveillance, influenza A, pandemic H1N1, pig, temporal and spatial

PMCID: PMC5080672; published online 2016 Jul 14. doi:  10.1017/S0950268816001424

 

Supplement:

Two more years, 2015 and 2016, of active national surveillance findings have provided additional data (n=2091 herd tests) since the publication of the article. Influenza A(H1N1)pdm09 has remained the sole influenza A virus (IAV) infection in the Norwegian pig population. The national herd prevalence in 2015 and 2016 were 462 /1038 or 45% (95%CI 42-48%) and 448/1056 or 42% (95%CI 39-45%) respectively which were as expected.   We used this additional information to extend the plots of herd prevalence temporal trends seen in figures 4 and 5 of the article. The new diagrams with the extended time lines to 31 December 2016 are seen below (Figure 1).

 

 

Figure 1: Temporal trends* of pig herds seroprevalence of influenza A(H1N1)pdm09 virus infection in Norway, an overall national herd prevalence and a stratification by the five production classes (fattening, nucleus, multiplier, conventional and sow pool herds) from 1 January 2010 to 31 December 2016 (*Using Stata’s lowess smoothing function to plot the running mean between positive herds and negative herds with date of sampling as the unit measure for cross-section calculation of the proportion of positive herds).

 

This supplementary information made available with the passing of time is useful in validating the deductions and predictions put forward in the article. One of which was that the national herd prevalence has stabilized between 40% and 50%. This endemic state may continue indefinitely with ongoing recurrent infections in positive herds and new infections in naïve herds if no interventions (e.g. vaccinations) or no new strains of IAV are introduced.  In addition, the sine-shaped prevalence trend seen in fattening pig herds could possibly be following the rise and fall of maternal antibody levels in weaned pigs from infected sow herds. The other factor mentioned was the spill-over infections from the human population, farmers in particular because they have close contact with pigs, a requirement for aerosol type transmissions. Since 2009, influenza A(H1N1)pdm09 virus has been the dominant IAV during the human influenza seasons in Norway. However, in 2016 (from week 12), the H3N2 virus strain has replaced H1N1pdm09 virus as the dominant IAV infections in the Norwegian human population[1]. It would be interesting to see in future whether significant tailing off in prevalence in pig-herds would also follow, thus supporting or disproving that reverse-zoonosis from the human reservoir had continued in a significant way since humans infected the first Norwegian pigs in 2009. We do see in figure 1 of this supplement, a dipping on the ends of the temporal trends especially in the nucleus, multiplier and sow pool herds. However, this should be read with caution as with the graphs in the article since the dipping is seen at the end of the time line towards 31 December 2016. These dips at the end of trend lines are misleading because the subsequent trajectories and gradients of the trend lines constructed by Stata lowess smoothing method depend on points immediately before and ahead in time (which is not available yet). We saw this situation in the fattening herds in figure 5 of our article where there appeared to be a decreasing trend in the herd prevalence as the end of 2014 approached.  But with results in 2015 and 2016 now available to extend the plots, we see that the dip in 2014 towards the end was just the bottoming of a trough before the prevalence swung upwards again in 2015.  Blood sampling scheme for all pig herds have not changed. The proportion of conventional pig herds with 4 or less pigs sampled per herd test in 2015 and 2016 remained very high (1166/1332 herd tests or 87%). This means that herd test sensitivities remained lower in conventional pig herds and therefore their herd prevalence had possibly been underestimated to a higher degree compared to the other four production groups. Given the bulk (n=5580 herd tests or 72%) of the overall national herds sampled were also conventional sow herds, the national herd prevalence were underestimated and the bias towards the null may be significant.

 

Reference

  1. Folkehelseinstituttet, Norwegian Institute of Public Health. Influenza season in Norway, 2015-2016. Folkehelseinstituttet webpage http://www.fhi.no/eway/?pid=240, 2016.

 

 

Figure 2. Authors from left: Jwee Chiek Er, Eystein Skjerve, Edgar Brun, Tore Framstad and Bjørn Lium.