Global mapping of highly pathogenic avian influenza H5N1 and H5Nx clade 2.3.4.4 viruses with spatial cross-validation

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Elife. 2016 Nov 25;5. pii: e19571. doi: 10.7554/eLife.19571. [Epub ahead of print]
[h=1]Global mapping of highly pathogenic avian influenza H5N1 and H5Nx clade 2.3.4.4 viruses with spatial cross-validation.[/h] Dhingra MS[SUP]1[/SUP], Artois J[SUP]1[/SUP], Robinson TP[SUP]2[/SUP], Linard C[SUP]1[/SUP], Chaiban C[SUP]1[/SUP], Xenarios I[SUP]3[/SUP], Engler R[SUP]3[/SUP], Liechti R[SUP]3[/SUP], Kuznetsov D[SUP]3[/SUP], Xiao X[SUP]4[/SUP], Von Dobschuetz S[SUP]5[/SUP], Claes F[SUP]6[/SUP], Newman SH[SUP]7[/SUP], Dauphin G[SUP]5[/SUP], Gilbert M[SUP]1[/SUP].
[h=3]Author information[/h]

[h=3]Abstract[/h] Global disease suitability models are essential tools to inform surveillance systems and enable early detection. We present the first global suitability model of highly pathogenic avian influenza (HPAI) H5N1 and demonstrate that reliable predictions can be obtained at global scale. Best predictions are obtained using spatial predictor variables describing host distributions, rather than land use or eco-climatic spatial predictor variables, with a strong association with domestic duck and extensively raised chicken densities. Our results also support a more systematic use of spatial cross-validation in large-scale disease suitability modelling compared to standard random cross-validation that can lead to unreliable measure of extrapolation accuracy. A global suitability model of the H5 clade 2.3.4.4 viruses, a group of viruses that recently spread extensively in Asia and the US, shows in comparison a lower spatial extrapolation capacity than the HPAI H5N1 models, with a stronger association with intensively raised chicken densities and anthropogenic factors.


[h=4]KEYWORDS:[/h] chicken; epidemiology; global health

PMID: 27885988 DOI: 10.7554/eLife.19571
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Excerpt from this study:
...
H5N1 HPAI is probably not as strongly environmentally constrained as other authors have suggested...

In the case of a directly contagious disease such as avian influenza, successful transmission and clinical
outbreaks have been observed over a wide range of temperature and humidity conditions
(e.g. Russia, Nigeria, Egypt, Northern China, Indonesia). Our results suggest that the main
large-scale constrains to suitability for H5N1 HPAI occurrence are related to the
distribution of hosts; densities of chickens and ducks raised in different systems, and to the
density of the human population, probably as a surrogate measure for various
anthropogenic transmission mechanisms. For the new H5Nx clade 2.3.4.4 viruses, we
found a somewhat different result, with a clear improvement of the extrapolation capacity
of models using a set of variables combining host distribution and environmental variables.
However, these models were of relatively low overall predictive power, most likely because
the virus has not yet had a chance to extend fully to its potential range of occurrence as
compared to H5N1 HPAI, and false pseudo-absences may have had a strong impact on
the construction of models and, therefore, on the accuracy of predictions. For this model,
and given its low extrapolation capacity, we emphasize that predictions made at long
distances from points of presence should be interpreted with caution, as there may still be
large areas where it could potentially become established and where the our model
predictions may be inaccurate.
...

A third set of important results consisted in the comparison of the H5N1 HPAI and H5Nx
clade 2.3.4.4 models, which showed areas of convergences and differences in the
geographic and predictor variables spaces. Domestic duck density was the most important
variable for both models, though with a lower RC for the H5Nx clade 2.3.4.4 model. Ducks
have always been strongly associated with areas of persistence and evolution of H5N1
HPAI (Gilbert and Pfeiffer, 2012), which relates to their capacity to act as an intermediate,
domestic reservoir between wild Anatidae, the main wild reservoir of avian influenza
viruses, and domesticated poultry. Ducks have been referred to as the ?Trojan horses? for
H5N1 HPAI H5N1 presence (Kim et al., 2014) on account of their role in virus introduction,
evolution, transmission and persistence (Hulse-Post et al., 2005), which has been
demonstrated in both host pathogenicity (Cornelissen et al., 2013; Smith GJD, 2015) and
geospatial studies (Gilbert and Pfeiffer, 2012).
...
The finding of a strong association between H5Nx clade 2.3.4.4 and ducks was somewhat
less expected as the disease was found mostly in chicken farms in more intensive poultry
production areas, but results are however in line with those of Hill et al. (Hill et al., 2015)
who found through phylogeographic analysis that the introduction of H5Nx clade 2.3.4.4 to
South Korea was associated with areas where domestic ducks and wild waterfowl
intermingled. Complex reassortment of multiple subtypes may also occur in areas where
domestic ducks and migratory birds have an opportunity to share food, water and habitat,
creating opportunities for virus transmission between different species, co-infection of
individual animals with different influenza viruses and subsequent gene reassortment
(Deng et al., 2013). It would be prudent for countries to put such areas under active
surveillance for early detection of HPAI introductions and for monitoring of virus evolution.
This would include the countries of the Americas and African continent where duck rearing
is not as common as in South East Asia. It is noteworthy that one of the most severe
recent H5 HPAI epidemics that started in 2015 in Dordogne region of France, a
traditionally important duck rearing area with some of the highest duck densities in the
country, even if the outbreaks were apparently caused by distinct H5 viruses from those
circulating in Asia. So, the association found with domestic duck densities fits with existing
knowledge of H5N1 spatial epidemiology, and was a major predictor in both the H5N1
HPAI and H5Nx clade 2.3.4.4 models.

In contrast, the association with extensively and intensively raised chickens provided
different results for the H5N1 HPAI and H5Nx clade 2.3.4.4 models, with the latter being
more strongly associated with intensified chicken production systems, found in intensive
crop production areas with high human population densities. An interesting hypothesis to
explain this pattern would be a greater fitness of H5Nx clade 2.3.4.4 viruses to spread
through intensive chicken production and poultry trade systems (Claes et al., 2016). We
still lack extensive published experimental infection results of the new clade in poultry, but
preliminary results are indicative of a lower pathogenicity of the H5Nx clade 2.3.4.4 virus in
chickens compared to H5N1 HPAI, with longer survival and shedding period (Kim et al.,
2014; Swayne et al., 2016). A lower virulence in chicken was also found for the reassortant
H5N2, H5N6 and H5N8 clade 2.3.4.4 viruses compared to previous 2.3.4 HPAI H5N1
viruses (Sun et al., 2016), although they remained highly pathogenic. A lower mortality and
longer period of infectivity may assist the virus in circulating longer and within intensified
poultry production and trading systems, leading to increased opportunities for onward
transmission. Evolution towards reduced pathogenicity would appear an asset in improving
farm-to-farm transmission and long-term persistence even in the absence of domestic
ducks. This could partly explain the stronger association of H5Nx clade 2.3.4.4 viruses
with intensive chicken production areas in eastern Asia and in the US.
...