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Environmental Drivers of

West Nile Virus Endemaization
in Europe
Shlomit Paz1 and Jan C. Semenza2
1University

2ECDC,

of Haifa, Israel

Stockholm, Sweden

2nd GRF One Health Summit 2013
November 2013, Davos, Switzerland
Background
West Nile virus (WNV), member of the
Flavivirus genus, is responsible for West Nile fever (WNF),
an emerging arbovirosis with a complex epidemiological

cycle.

The transmission cycle involve wild birds as the principal

hosts and mosquitoes (especially Culex), largely birdfeeding species, as the primary vectors.

Humans and horses do not produce significant viraemia and
WNV exists in rural ecosystems as well as in urban
areas where mosquitoes breed in organic-rich water in
artificial containers.

WNV is widely distributed throughout the tropical and
temperate regions of the world where it infects
birds, humans, horses and other mammals.

In fact, today it is a vector-borne pathogen of global
importance.
Humans are mainly infected through mosquito bites, but
infection can occur through organ transplantation and
blood.
An incubation period of 3-14 days precedes symptoms.
While most human infections are asymptomatic, the
majority of clinical cases are mild and present with flu-like
symptoms.
Severe cases with signs of encephalitis, meningoencephalitis or meningitis, are most often observed
among elderly.
No specific therapy or vaccine are available.
The main preventive measures are aimed at reducing
exposure to mosquito bites.
WNF in Europe
Over the last years, sporadic human cases or limited
outbreaks of WNF have been reported in Europe.

In summer 2010, the number of WNF cases in new areas in
Europe and its neighboring countries (particularly in South
Eastern Europe) was the highest ever reported.

Later, WNF outbreaks in Europe and Eurasia during the
summers of 2011, 2012 and 2013 occurred in most of the

disease locations in 2010.
How WNV has become an
endemic pathogen in many
parts
of Europe and Eurasia?
The epidemiology of WNF is multifactorial and
complex.

Abiotic and biotic conditions are both important
determinants of WNF epidemiology.

The transmission of WNV is determined by many
factors.
Temperature

Ambient temperature plays an important role in viral
replication rates and transmission of WNV, affecting the
length of extrinsic incubation, seasonal phenology of
mosquito host populations and geographical variation in
human case incidence.
Elevated ambient temperatures increase growth rates of
vector populations, decrease the interval between blood
meals, and accelerate the rate of virus evolution.
A recent example was an outbreak in the summer
of 2010, when southeastern Europe and Eurasia
experienced an unprecedented upsurge in the

number of human WNF cases, which was preceded
by hot spells (Paz et al., 2013).
Environmental Drivers of West Nile Virus Endemaization in Europe
Environmental Drivers of West Nile Virus Endemaization in Europe
Temperature anomalies during summer 2010 in selected
stations
Constanta, Romania

Volgograd, Russia

Min

C

Min

C

-

mean

-

mean

-

max

-

max

-

-

-

week #

week #

Thessaloniki, Greece

Ben Gurion Airport, Israel

Min

C

Min

C

-

mean

-

mean

-

max

-

max

-

-

-

week #

week #
Results of Pearson and lag correlations between the weekly
average temperature and the dates of WNF onset, at
selected stations
(bold values = significant results)
Volgograd, Russia

Constanta, Romania

Temperatur
e

min

mean

max

min

mean

max

Lag 0

0.16

0.25

0.26

0.17

0.17

0.12

lag 1 week

0.20

0.28

0.29

0.38

0.39

0.33

lag 2 weeks

0.38

0.44

0.44

0.59

0.61

0.56

lag 3 weeks

0.63

0.63

0.61

0.52

0.55

0.51

lag 4 weeks

0.61

0.65

0.64

0.37

0.40

0.38

Thessaloniki, Greece

Ben Gurion Airport, Israel

Temperatur
e

min

mean

max

min

mean

max

Lag 0

0.49

0.37

0.31

0.35

0.36

0.22

lag 1 week

0.45

0.36

0.32

0.33

0.27

0.16

lag 2 weeks

0.37

0.30

0.24

0.34

0.29

0.18

lag 3 weeks

0.29

0.24

0.19

0.37

0.26

0.08

lag 4 weeks

0.28

0.19

0.13

0.18

0.18

0.08
Results of the Multinomial Logistic Regression
between summer temperatures and
WNF occurrences
No-lag
Lag1
Lag2
Lag3
Lag4
p-val
estimate p-val
estimate p-val
estimate p-val
estimate p-val
estimate
Rostov, Russia
min
0.0562
0.1737
0.0134
1.32 0.0006
2.27
0.0011
2.05
mean
0.042
0.935 0.0053
1.41 0.0002
2.3
max
0.087
0.2636
0.009
1.29 0.0004
2.12
0.0003
2.25
Constanta, Romania
min
0.3067
0.1091
0.0013
2.13 0.0021
1.93
0.0362
1.036
mean
0.007 12.0496 0.0007
2.203 0.0017
1.85
0.03
1.03
max
0.0019
2.022 0.0043
1.758
0.028
1.19
Thessaloniki, Greece
min
0.0148
1.46 0.0377
1.05 0.0175
1.42 0.0236
1.345
0.0415
1.18
mean
0.0173
1.28
max
Haifa, Israel
min
0.0309
3.5871 0.0366
1.72 0.0108
2.19 0.0385
1.7
mean
max

0.0026

1.68

0.0298

1.11

0.014

1.29

0.0227

1.18
Reported cases of West Nile fever for the EU and neighboring countries.
Transmission season 2012 and previous transmission seasons. Source:
ECDC.

“WNV always dispersed into new areas during years with above-normal
temperatures and that amplification during the following year occurred during
summers with above- or normal temperatures ” (Reisen et al. , J. Med.
Entomol. 2006).
Environmental Drivers of West Nile Virus Endemaization in Europe
Precipitation
The scientific literature presents inconsistent results.
on one hand, heavy rainfall during spring may increase

standing water resources at the beginning of the hot
season.
In contrast, during drought conditions, standing water pools

-

June

July

Cordoba

Ben Gurion Airp
August

Venezia -Tessera

May

Mugla

April

Thessaloniki

March

Budapest

Constanta

Anomalies of Monthly
Surface Gauss
Precipitation Rate of
spring-summer
2010, relative to the 30
years period in selected
stations (per each
country)

Volgograd

needs to thrive.

Surface Gauss Precipitation Rate
Anomaly

become richer in the organic material that mosquitoes

September
Landscape Features and Land-Use
In Europe and Eurasia, circulation of WNV is mainly
confined to two land-use patterns:
1. rural areas where wetlands serve as bird-nesting

areas that provide ideal conditions for establishing
endemic cycles of WNV

(the Rhone delta, southern France; the

Volga delta, southern Russia; and the Danube delta in Romania).

2. urban areas where mosquitoes feed both on birds
and on humans and thus act as bridge vectors
(Bucharest, Romania; Volgograd, Russia and in Thessaloniki, Greece).
Overall, the urban environment in which the WNF
outbreaks

occur

is

a

diverse

mix

of

buildings, transportation routes, vegetation, land
uses and people associated with many aspects of
urban life, from economic activity to patterns of

illness.
Avian Hosts
• Bird migration influences new areas of spread.
• As a reaction to increasing spring temperature in recent
years, populations of migratory birds have advanced the
seasonal start of their reproduction.

• Changes

in

tropical

storms

may

influence

WNV

dispersal, by impacting the dynamics of storm-driven
birds.
A comparison between bird migration tracks during
spring (based on Leshem, 2010) and WNV infection
main locations
Other Drivers
Transportation
In a world that is ever more interconnected through rapid
transportation systems, such as passenger air travel and
global trade, the virus is now being dispersed
internationally.
Socio-demographic level
It can be expected that epidemiology of WNV-induced
disease in people will vary between regions as a result of
differences at the socio-demographic level. Populations
living in poverty might be less likely to have secure, airconditioned homes, and thus are more exposed to biting
mosquitoes.
Main conclusions

Abiotic and biotic environmental factors have both

contributed to the endemization of WNF in Europe, such as:
favorable climatic conditions (while temperature is the most
important climatic driver); hospitable habitats for high

densities of competent mosquitoes; infected migratory birds
for the dispersion of WNV; susceptible human and equine
populations.
ADDED VALUE TO THE ONE HEALTH APPROACH
Reduced human exposure to mosquitoes infected with
WNV, through vector abatement measures, is currently the

most effective way to prevent transmission.
Ecologically based land-use planning, combined with improved
development and sanitation, could reduce contact with and the

abundance

of

human-commensal

species

and

hence

transmission of their pathogens. A critical component of a
vector control program is concurrent public education and
health promotion to prevent and reduce risk of exposure.
Understanding

the

environmental

drivers

of

the

epidemiology will help guide these public health efforts.

WNF
For more details:
Paz, S., Malkinson, D., Green, M.S., Tsioni, G., Papa, A., Danis, K., Si
rbu, A., Ceianu, C., Katalin, K., Ferenczi, E., Zeller, H., Semenza, J.C.
, 2013. Permissive Summer Temperatures of the 2010 European
West Nile Fever Upsurge. PLOS ONE, 8(2): e56398.
Paz, S., Semenza, J.C., 2013. Environmental Drivers of West Nile
Fever Epidemiology in Europe and Eurasia - Review. International
Journal of Environmental Research and Public Health, 10, 3543-3562.
Thanks

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Environmental Drivers of West Nile Virus Endemaization in Europe

  • 1. Environmental Drivers of West Nile Virus Endemaization in Europe Shlomit Paz1 and Jan C. Semenza2 1University 2ECDC, of Haifa, Israel Stockholm, Sweden 2nd GRF One Health Summit 2013 November 2013, Davos, Switzerland
  • 2. Background West Nile virus (WNV), member of the Flavivirus genus, is responsible for West Nile fever (WNF), an emerging arbovirosis with a complex epidemiological cycle. The transmission cycle involve wild birds as the principal hosts and mosquitoes (especially Culex), largely birdfeeding species, as the primary vectors. Humans and horses do not produce significant viraemia and
  • 3. WNV exists in rural ecosystems as well as in urban areas where mosquitoes breed in organic-rich water in artificial containers. WNV is widely distributed throughout the tropical and temperate regions of the world where it infects birds, humans, horses and other mammals. In fact, today it is a vector-borne pathogen of global importance.
  • 4. Humans are mainly infected through mosquito bites, but infection can occur through organ transplantation and blood. An incubation period of 3-14 days precedes symptoms. While most human infections are asymptomatic, the majority of clinical cases are mild and present with flu-like symptoms. Severe cases with signs of encephalitis, meningoencephalitis or meningitis, are most often observed among elderly. No specific therapy or vaccine are available. The main preventive measures are aimed at reducing exposure to mosquito bites.
  • 5. WNF in Europe Over the last years, sporadic human cases or limited outbreaks of WNF have been reported in Europe. In summer 2010, the number of WNF cases in new areas in Europe and its neighboring countries (particularly in South Eastern Europe) was the highest ever reported. Later, WNF outbreaks in Europe and Eurasia during the summers of 2011, 2012 and 2013 occurred in most of the disease locations in 2010.
  • 6. How WNV has become an endemic pathogen in many parts of Europe and Eurasia?
  • 7. The epidemiology of WNF is multifactorial and complex. Abiotic and biotic conditions are both important determinants of WNF epidemiology. The transmission of WNV is determined by many factors.
  • 8. Temperature Ambient temperature plays an important role in viral replication rates and transmission of WNV, affecting the length of extrinsic incubation, seasonal phenology of mosquito host populations and geographical variation in human case incidence. Elevated ambient temperatures increase growth rates of vector populations, decrease the interval between blood meals, and accelerate the rate of virus evolution.
  • 9. A recent example was an outbreak in the summer of 2010, when southeastern Europe and Eurasia experienced an unprecedented upsurge in the number of human WNF cases, which was preceded by hot spells (Paz et al., 2013).
  • 12. Temperature anomalies during summer 2010 in selected stations Constanta, Romania Volgograd, Russia Min C Min C - mean - mean - max - max - - - week # week # Thessaloniki, Greece Ben Gurion Airport, Israel Min C Min C - mean - mean - max - max - - - week # week #
  • 13. Results of Pearson and lag correlations between the weekly average temperature and the dates of WNF onset, at selected stations (bold values = significant results) Volgograd, Russia Constanta, Romania Temperatur e min mean max min mean max Lag 0 0.16 0.25 0.26 0.17 0.17 0.12 lag 1 week 0.20 0.28 0.29 0.38 0.39 0.33 lag 2 weeks 0.38 0.44 0.44 0.59 0.61 0.56 lag 3 weeks 0.63 0.63 0.61 0.52 0.55 0.51 lag 4 weeks 0.61 0.65 0.64 0.37 0.40 0.38 Thessaloniki, Greece Ben Gurion Airport, Israel Temperatur e min mean max min mean max Lag 0 0.49 0.37 0.31 0.35 0.36 0.22 lag 1 week 0.45 0.36 0.32 0.33 0.27 0.16 lag 2 weeks 0.37 0.30 0.24 0.34 0.29 0.18 lag 3 weeks 0.29 0.24 0.19 0.37 0.26 0.08 lag 4 weeks 0.28 0.19 0.13 0.18 0.18 0.08
  • 14. Results of the Multinomial Logistic Regression between summer temperatures and WNF occurrences No-lag Lag1 Lag2 Lag3 Lag4 p-val estimate p-val estimate p-val estimate p-val estimate p-val estimate Rostov, Russia min 0.0562 0.1737 0.0134 1.32 0.0006 2.27 0.0011 2.05 mean 0.042 0.935 0.0053 1.41 0.0002 2.3 max 0.087 0.2636 0.009 1.29 0.0004 2.12 0.0003 2.25 Constanta, Romania min 0.3067 0.1091 0.0013 2.13 0.0021 1.93 0.0362 1.036 mean 0.007 12.0496 0.0007 2.203 0.0017 1.85 0.03 1.03 max 0.0019 2.022 0.0043 1.758 0.028 1.19 Thessaloniki, Greece min 0.0148 1.46 0.0377 1.05 0.0175 1.42 0.0236 1.345 0.0415 1.18 mean 0.0173 1.28 max Haifa, Israel min 0.0309 3.5871 0.0366 1.72 0.0108 2.19 0.0385 1.7 mean max 0.0026 1.68 0.0298 1.11 0.014 1.29 0.0227 1.18
  • 15. Reported cases of West Nile fever for the EU and neighboring countries. Transmission season 2012 and previous transmission seasons. Source: ECDC. “WNV always dispersed into new areas during years with above-normal temperatures and that amplification during the following year occurred during summers with above- or normal temperatures ” (Reisen et al. , J. Med. Entomol. 2006).
  • 17. Precipitation The scientific literature presents inconsistent results. on one hand, heavy rainfall during spring may increase standing water resources at the beginning of the hot season. In contrast, during drought conditions, standing water pools - June July Cordoba Ben Gurion Airp August Venezia -Tessera May Mugla April Thessaloniki March Budapest Constanta Anomalies of Monthly Surface Gauss Precipitation Rate of spring-summer 2010, relative to the 30 years period in selected stations (per each country) Volgograd needs to thrive. Surface Gauss Precipitation Rate Anomaly become richer in the organic material that mosquitoes September
  • 18. Landscape Features and Land-Use In Europe and Eurasia, circulation of WNV is mainly confined to two land-use patterns: 1. rural areas where wetlands serve as bird-nesting areas that provide ideal conditions for establishing endemic cycles of WNV (the Rhone delta, southern France; the Volga delta, southern Russia; and the Danube delta in Romania). 2. urban areas where mosquitoes feed both on birds and on humans and thus act as bridge vectors (Bucharest, Romania; Volgograd, Russia and in Thessaloniki, Greece).
  • 19. Overall, the urban environment in which the WNF outbreaks occur is a diverse mix of buildings, transportation routes, vegetation, land uses and people associated with many aspects of urban life, from economic activity to patterns of illness.
  • 20. Avian Hosts • Bird migration influences new areas of spread. • As a reaction to increasing spring temperature in recent years, populations of migratory birds have advanced the seasonal start of their reproduction. • Changes in tropical storms may influence WNV dispersal, by impacting the dynamics of storm-driven birds.
  • 21. A comparison between bird migration tracks during spring (based on Leshem, 2010) and WNV infection main locations
  • 22. Other Drivers Transportation In a world that is ever more interconnected through rapid transportation systems, such as passenger air travel and global trade, the virus is now being dispersed internationally. Socio-demographic level It can be expected that epidemiology of WNV-induced disease in people will vary between regions as a result of differences at the socio-demographic level. Populations living in poverty might be less likely to have secure, airconditioned homes, and thus are more exposed to biting mosquitoes.
  • 23. Main conclusions Abiotic and biotic environmental factors have both contributed to the endemization of WNF in Europe, such as: favorable climatic conditions (while temperature is the most important climatic driver); hospitable habitats for high densities of competent mosquitoes; infected migratory birds for the dispersion of WNV; susceptible human and equine populations.
  • 24. ADDED VALUE TO THE ONE HEALTH APPROACH Reduced human exposure to mosquitoes infected with WNV, through vector abatement measures, is currently the most effective way to prevent transmission. Ecologically based land-use planning, combined with improved development and sanitation, could reduce contact with and the abundance of human-commensal species and hence transmission of their pathogens. A critical component of a vector control program is concurrent public education and health promotion to prevent and reduce risk of exposure. Understanding the environmental drivers of the epidemiology will help guide these public health efforts. WNF
  • 25. For more details: Paz, S., Malkinson, D., Green, M.S., Tsioni, G., Papa, A., Danis, K., Si rbu, A., Ceianu, C., Katalin, K., Ferenczi, E., Zeller, H., Semenza, J.C. , 2013. Permissive Summer Temperatures of the 2010 European West Nile Fever Upsurge. PLOS ONE, 8(2): e56398. Paz, S., Semenza, J.C., 2013. Environmental Drivers of West Nile Fever Epidemiology in Europe and Eurasia - Review. International Journal of Environmental Research and Public Health, 10, 3543-3562.