Controlul Infectiei Cu Virusul WN

M I N I R E V I E W

Control ofarbovirus infectionsbya coordinated response:WestNileVirus inEnglandandWalesDilys Morgan

Emerging Infections and Zoonoses Department, Health Protection Agency, Centre for Infections, London, UK

Correspondence: Dilys Morgan, Emerging

Infections and Zoonoses Department, Health

Protection Agency, Centre for Infections, 61

Colindale Ave, London NW9 5EQ, UK. Tel.:

1020 8327 7474; fax: 1020 8200 7868;

e-mail: [email protected]

Received 12 June 2006; revised 7 August 2006;

accepted 18 August 2006.

First published online 20 October 2006.

DOI:10.1111/j.1574-695X.2006.00159.x

Editor: Alex van Belkum

Keywords

West Nile Virus; surveillance; vector-borne.

Abstract

Although there is no recognized transmission of human arboviral infections in the

UK, concerns about the possible spread of West Nile virus (WNV) have

precipitated coordinated activities around both surveillance and response. The

Department of Health has chaired a UK WNV task force since the end of 2000.

This is a multidisciplinary group of senior representatives from Agencies and

Government Departments involved in human and animal health, entomology and

academic departments. Activities include surveillance for WNV infections in

humans, and in dead birds, mosquitoes and horses. All have been negative for

WNV. A WNV contingency plan was produced in 2004, and this could be used as a

generic plan for an effective and coordinated response in the event of the

emergence of a new vector-borne zoonotic infection.

Introduction

West Nile Virus (WNV) is an arbovirus and was first isolated

from a woman with a fever in 1937 in the West Nile district

of Uganda (Smithburn et al., 1940). It was first recognized as

a cause of a human illness known as meningoencephalitis in

Israel in 1957 and as a cause of horse disease in Egypt and

France in the early 1960s (Murgue et al., 2001a).

Europe has had sporadic cases and outbreaks of WNV in

human and horses since the 1960s (Hubalek & Halouza,

1999). However, over the past 10 years there have been

significant outbreaks in the western hemisphere, including

Bucharest, Romania in 1996 (393 cases) (Tsai et al., 1998),

Volgograd, Russia in 1999 (over 800 cases) (Platonov et al.,

2001) and Israel in 2000 (417 cases) (Chowers et al., 2002).

In France, the first reported WNV outbreak affecting

horses and humans occurred during the summer of 1962.

This occurred in the Carmague region which is character-

ized by wetlands and marshes, with a great number of

migratory and resident bird species and large populations

of mosquitoes. Sporadic cases followed this outbreak but

after 1965 no cases in human or equine cases were reported

until 2000. During 2000, there were 76 cases in horses, and

WNV testing of over 5000 horses showed a WNV IgG

seroprevalence rate of 8.3%, with 42% of those with IgG

also being IgM positive. This suggested that WNV was not

endemic in the affected area, rather that sporadic outbreaks

were separated by long silent periods (Durand et al., 2002).

Two gamekeepers were also found to have serological

evidence of infection (Murgue et al., 2001b). Then in 2003,

seven human cases of infection were identified late August in

the Var District, which is adjacent to the Camargue. Three

patients had encephalitis and four had fever. Five equine

cases were also found; four had encephalitis and one was

asymptomatic (Institut de Veille Sanitaire, 2003; Mailles

et al., 2003). In 2004, 37 suspect cases in horses were

reported and 14/18 had WNV infection (WNV IgM detec-

tion or positive RT-PCR), however, no human cases were

found (Zeller et al., 2004). Two Irish tourists returning from

the Algarve, Portugal in the summer of 2004 were diagnosed

with WNV infections. They had been staying in an area of

swamp bird reserves where there were many mosquitoes

(Connell et al., 2004).

There has been a different epidemiological picture in the

United States of America (USA). Despite being endemic

for many other arboviruses, WNV had not been found in

the USA until 1999, when WNV activity was reported for the

first time in the New York City area (Nash et al., 2001).

The infection then showed increases in terms of the

annual case count, geographical spread and extension of

FEMS Immunol Med Microbiol 48 (2006) 305–312 c� 2006 Federation of European Microbiological SocietiesPublished by Blackwell Publishing Ltd. All rights reserved

the transmission period. During 2003, 9862 human cases

were reported, and the infection was found in all states

except Maine, Oregon, Washington, Alaska and Hawaii.

However, in 2004 the number of cases reported fell drama-

tically (2539 cases) and showed little increase in 2005 (3000

cases) (Centers for Disease Control and Prevention).

Transmission cycle

Figure 1 shows the life cycle of WNV.

Birds are the natural host for WNV. The infection is

transmitted to other birds by mosquitoes and the virus is

maintained in the bird population. The virus is amplified by

continuous transmission in this way between birds and

mosquitoes and transmission is therefore increased where

large numbers of mosquitoes are close to suitable bird

populations. Mosquitoes involved in the transmission of

WNV generally prefer to take blood meals from birds but

will sometimes bite and infect humans and animals and act

as ‘bridging vectors’. Humans and other animals such as

horses are classified as ‘incidental’ or ‘dead end’ hosts, in

that they are not important in maintaining transmission

cycles since they rarely develop high enough levels of virus in

their blood stream necessary to infect other mosquitoes.

WNV is not transmitted from person-to-person through

close contact. However, in a very small number of cases,

WNV has been spread through blood transfusions (Pealer

et al., 2003), organ transplants (Iwamoto et al., 2003),

breastfeeding and in utero mother to child transmission

(Centers for Disease Control and Prevention, 2002).

Clinical features of WNV infections

The incubation period is usually 3–15 days following the

bite of an infected mosquito. Approximately 80% of those

infected have no symptoms at all, and 20% have a mild

influenza-like illness (fever, headache, myalgia, occasionally

with rash, diarrhoea or lymphadenopathy) which generally

lasts 2–5 days. A small proportion (less than 1%) goes on to

develop more severe disease. Severe infection may present as

an aseptic encephalitis, meningitis or meningoencephalitis.

Patients may suffer headaches, fever, stiff neck, sore eyes,

disorientation, muscle weakness, convulsions and coma.

WNV infection spread throughout the USA, as an increasing

number of syndromes and presentations have been re-

ported. These include acute flaccid paralysis, cerebellar

ataxia, Parkinsonism, cranial nerve abnormalities, optic

neuritis and other neurological features, pancreatitis, hepa-

titis and myocarditis. Some patients suffer longer-term

physical, functional and cognitive symptoms (Klee et al.,

2004). Increasing age is the greatest risk factor for the

development of serious disease and death (Weinberger

et al., 2001).

WNV in England and Wales

In the UK, although there are suitable bird species to act as

hosts for WNV and potential WNV bridge vectors are

present (Medlock et al., 2005), the risk of cases occurring is

thought to be low, mainly because the mosquito population

densities are too small to maintain transmission (Crook

et al., 2002). Mosquito-borne diseases, and indeed transmis-

sion of mosquito-borne viral infections, are virtually un-

known in the UK, unlike in the USA and many parts of

Europe.

However, this has not resulted in complacency. The Chief

Medical Officer (CMO) for England has placed great

emphasis on the risks of WNV, and when he published his

strategy for combating infectious diseases ‘Getting ahead of

the curve’ he highlighted WNV as an example of the way

Incidental InfectionsMosquito vector

West Nile virus

West Nile virus

West Nile virus

Bird reservoir host

Fig. 1. West Nile Virus transmission Cycle.

FEMS Immunol Med Microbiol 48 (2006) 305–312c� 2006 Federation of European Microbiological SocietiesPublished by Blackwell Publishing Ltd. All rights reserved

306 D. Morgan

infections can emerge unexpectedly and unpredictably and

pose a new threat to the population (Department for

Health, 2002). In his annual report in 2002, the CMO

included a chapter on WNV outlining the three main factors

which would determine whether WNV became established

in the UK (Department for Health, 2003).

(1) The mosquito population

The distribution and abundance of different species of

mosquito are crucial for the transmission of WNV and of

the 32 species of mosquito recorded in Britain, at least seven

species could potentially transmit WNV. Should WNV be

introduced to the UK, the most likely vectors would be

mosquitoes belonging to the most widely distributed Culex

pipiens complex.

(2) The chances of the domestic bird population becoming

infected

Migratory birds have been instrumental in the periodic

reintroduction of WNV to Europe. A study looking for

evidence of infection with WNV virus amongst both migra-

tory and nonmigratory birds has suggested that virus is

already present in native birds in the UK (Buckley et al.,

2003). However, the confirmation of these results was needed.

(3) Climate Change

Insect vectors are very sensitive to meteorological condi-

tions. Temperature and humidity influence significantly

the transmission of WNV. Generally warmer weather

accompanied by increased risk of flooding associated

with climate change (Office of Science and Technology,

2004), would amplify the population density of vector

mosquitoes. Warmer weather would also influence people’s

behaviour, leading to them spending more time outdoors

in situations where they would be more prone to mosquito

bites.

In the report, the CMO stressed the importance of

assessing the risk of WNV and recommended enhanced

surveillance of birds, humans and mosquitoes and the need

for a WNV contingency plan.

In 2004, the Department of Health (DH) for England

published ‘West Nile virus: a contingency plan to protect the

public’s health’ (Department of Health, 2004a). The plan

sets out measures to enhance surveillance for the virus, to

alert clinicians to the symptoms of WNV, and control

mosquito populations. It includes sections on:

(1) background, and assessing the risk through surveillance

of people, birds, mosquitoes and horses

(2) diagnosis, patient care and protection of healthcare

professionals

(3) Public Health Action in partnership, outlining partner-

ships at a local, regional and national level of health,

veterinary and environmental agencies

(4) environmental control including advice on the control

of mosquitoes, and

(5) Action Plan, for use if WNV was found in the UK,

including laboratory diagnosis, public health action, sur-

veillance and environmental control

A coordinated response for WNV in the UK

The DH has had a UK WNV task force since the end of 2000.

It is chaired by the DH, but is a multidisciplinary group

bringing together senior representatives from Agencies and

Government Departments involved in human and animal

health, entomology and academic departments. Representa-

tives from the Devolved Administrations (Wales, Scotland

and Northern Ireland) also attend. It meets two to three

times a year and provides a focus and coordinating body for

research and surveillance activities for WNV.

Human enhanced surveillance and testing forWNV

So far, there have been two components of human surveil-

lance for WNV infections acquired in England and Wales, as

follows.

Retrospective surveillance

This involved examination of CSF from cases of encephalitis

or meningitis in patients where no causative organism was

found. This was coordinated by the Clinical Virology Net-

work, and 123 CSF samples from patients aged over 50 years

were tested for WNV. The patients came from most areas of

England and Wales and all were negative for WNV.

Prospective surveillance of suspect cases

The Public Health Laboratory Service [which became part of

the Health Protection Agency (HPA) in 2003] first alerted

clinicians and microbiologists to the possibility of WNV

infection in July 2001 and requested they send samples for

testing (Public Health Laboratory service, 2001). Enhanced

surveillance for cases acquired in England and Wales has

been undertaken during the summer months since 2002

(Health Protection Agency, 2003). An article in the Com-

municable Disease Report at the start of the surveillance

season requests Regional Epidemiologists contact clinicians

in their regions to raise awareness of the possibility of WNV

infection, particularly in those aged over 50 years, and

microbiologists are asked to consider WNV in patients with

otherwise unexplained neurological or compatible symp-

toms. The CMO also sends a letter to all clinicians in

England reminding them of the need to think of WNV and

alerting them to the WNV surveillance protocol on the

Health Protection Agency website.

Each year enhanced surveillance for human WNV infec-

tion in England and Wales starts on 1 June and operates


307West Nile virus surveillance in England and Wales

until the end of October, and case definitions were been

revised in line with the EU case definitions (European

Commission, 2005). The revised case definitions are shown

in Table 1.

Clinicians are requested to send a form outlining the

demographic and clinical details of the patient to the HPA

Centre for Infections, and following samples are sent to the

HPA Special Pathogens Laboratory.

(1) Paired serum or whole blood specimens. The acute

phase specimen 0–8 days after onset and the convalescent

phase sample 14–21 days after onset.

(2) CSF, ideally acute phase (o8 days of onset).

The case definitions based on laboratory investigations

are shown in Table 2.

Results of surveillance for human WNV infection

Between 2002 and 2005, a total of 36 surveillance forms were

received and although most of these had meningitis or

encephalitis, only seven fulfilled the case definition by

having no foreign travel in the 3 weeks before the onset of

symptoms and being aged over 50 years old. A further 38

patients were identified from the laboratory testing database

as fulfilling the case definition, but on whom surveillance

forms were not submitted. Of the 45 patients identified as

fulfilling the case definition, 32 were reported as having

encephalitis, six meningitis and seven had other symptoms

(including confusion, fever and rash, VI nerve palsy).

All of the patients resident in England and Wales, includ-

ing those who had a travel history in the 3 weeks before onset,

or were aged under 50 years; those fulfilling the case defini-

tion were negative for WNV infection on laboratory testing.

Birds

The Veterinary Laboratories Agency funded by the Depart-

ment for the Environment, Food and Rural Affairs (Defra)

has been examining dead birds for WNV since 2001, and

1295 birds had been submitted up to the end of 2004. These

include 87 different wild bird species. None of the 1250

tissue specimens tested have been positive for WNV.

Horses

Surveillance of neurological diseases in horses continues,

and Defra is about to publish for consultation a generic plan

for equine encephalitides which includes WNV. (Defra:

Table 1. Prospective surveillance: revised definition for suspected cases of West Nile Virus (WMV) infection in humans – indications for considering the

diagnosis of WNV infection and requesting a WNV test (adapted from European Union case definition)

WNV Neurological Syndrome: A case of encephalitis or meningoencephalitis or aseptic meningitis or acute flaccid paralysis, defined by the specific

criteria below, presenting from 1st June to 30th October 2005

1. Encephalitis or meningoencephalitis 1. Fever 4 381 and

Any person with suspected viral

encephalitis with all the following criteria

2. Altered mental state (altered level of consciousness, agitation, lethargy) and/or

other evidence of cortical involvement (e.g. focal neurological findings, seizures) and

3. Cerebrospinal fluid (CSF) pleocytosis with predominant lymphocytes and/or elevated

protein with a negative Gram stain and culture and

4. No alternative microbiological cause identified

2. Meningitis 1. Fever 4 381 and

Any person with suspected viral (aseptic)

meningitis with all the following criteria

2. Headache, stiff neck and/or other meningeal signs and

3. CSF pleocytosis with predominant lymphocytes and/or elevated protein with a negative

Gram stain and culture and


3. Acute Flaccid Paralysis (AFP) 1. Fever 4 381 and

Any person with suspected AFP (most cases

are polio-like) with all the following criteria

2. Asymmetric limb weakness without sensory loss with diminished deep tendon reflexes and

3. Anterior horn cell disease and

4. May have facial nerve palsy and


Table 2. Definitions of probable and confirmed West Nile Virus

infection

Probable case

1. Single serum specimen: A positive WNV IgM test

2. CSF: detection of WNV IgM�

Confirmed case (positive for one or more of the following criteriaw):

1. Serum or CSF: isolation of WNV

3. Serum or CSF: detection of WNV genomic RNA sequences by

RT-PCR

4. Serum or CSF: detection of neutralising WNV antibodies with

significant titre

5. Paired Serum specimens: A fourfold rise in WNV specific antibody

titre

�deviation from EU definitionwisolation of the virus or detection of nucleic acid is unusual and the most

likely confirmatory testing is through detection of neutralising antibodies

or a rising titre


308 D. Morgan

A contingency plan for the UK: Specified Type Equine

Exotic Disease (STEED) includes WNV, Western Equine

Encephalitis, Eastern Equine Encephalitis, Venezuelan

Equine Encephalitis, Borna Disease, Hendra and other viral

encephalitides e.g. St Louis and Japanese Encephalitis).

Although horses have been identified and reported with

neurological features, WNV has not been found on investi-

gation of these animals.

Mosquitoes

The DH has funded ongoing surveillance of mosquitoes in

England for WNV since 2003. The sentinel sites in various

parts of England were increased from four to six sites in

2004. Mosquitoes have been captured using mosquito

magnet traps at the six sites and, in addition, suction traps

at three of the sites. Over 13 000 mosquitoes have been

collected and these include species which could act as

possible vectors for WNV. Approximately half have been

tested by PCR at the HPA Special Pathogen Laboratory, and

WNV has not been detected. Work continues on optimal

trapping methods to look for potential WNV vectors,

especially female Culex pipiens.

Laboratory developments

Standard operating procedures have been developed for use

by the Veterinary Laboratories Agency and the HPA had

been upgrading their Standard operating procedures and

validating their tests against different strains of WNV. There

has also been standardization of test across agencies.

Other activities

Expert views

The views of the CMO’s National Expert Panel on New and

Emerging Infections were sought over whether more re-

sources should be committed to vector-borne disease. This

panel is an over-arching, horizon-scanning panel, reporting

to the CMO and advising the DH.

Following presentations on the human health implica-

tions of vector-borne diseases, and a review of possible

vectors a general discussion took place. The principal

conclusions of the Panel were as follows.

(1) With the exception of Lyme disease, vector-borne dis-

eases do not currently pose a significant public health threat

in England and Wales.

(2) Vector-borne disease risks in the UK are unlikely to

increase in the future.

(3) The risk of WNV emerging as a human disease is very

low, but research and surveillance should continue.

(4) Vector-borne surveillance should be linked to the scale

of potential public health disease risks, and should be

targeted to specific defined ecological sites. At present, the

public health risks posed do not justify wider surveillance of

potential vectors

(Department of Health, 2004b)

Encephalitis study

The DH has agreed to fund a 3-year study by the HPA on the

aetiology of encephalitis in England. This will investigate the

cause of encephalitis in cases admitted to 14 neurological

centres in England. Laboratories will be using an investiga-

tive protocol and WNV will be included in second line

testing, but will move up the list of agents tested for if the

patient is aged over 50 years.

West Nile exercise to test local responses

Exercise IBIS was an exercise to test the local multi-agency

response to a WNV outbreak. The exercise took place in

March 2005 and was organised by the HPA in collaboration

with Defra to see how links between local veterinary and

health partners would work in practice. The scenario was

phased, and moved from an initial outbreak affecting

horses, to human cases being confirmed and the suspicion

of a local community outbreak. The linkages between all the

partner agencies were tested from notification stage,

through investigation and case searching, media handling

and environmental vector control considerations. Many

agencies were involved due to the complexity of the issue.

For example, mosquito control measures may be needed to

reduce or eliminate the vector risk for WNV. Therefore the

involvement of agencies such as the Environment Agency,

the Health and Safety Executive and English Nature, as well

as local government, is crucial to assess all the potential risks

and consequences of control measures, which may well

include the use of pesticides or otherwise impact on the

environment.

The exercise highlighted a number of issues: local cross-

agency working, understanding of roles and responsibilities

in different organisations and within an Incident Control

team, the availability of resources and the importance of

communications. The principles of dealing with such an

incident would be applicable to any zoonotic disease requir-

ing a multi-agency response.

Discussion

Although there is no recognized transmission of human

arboviral infections in the UK, several concerns have pre-

cipitated coordinated activities around both surveillance

and response. Firstly, increased transmission of WNV infec-

tion in France, the UK’s closest geographical neighbour in

Europe, and its introduction in the USA, prompted con-

cerns that WNV could spread to the UK. However, the USA



has a history of arboviral infections and specific factors seem

to have operated to facilitate its spread. Also, the areas where

transmission has occurred in France, and probably did in

Portugal, provide a very different ecological environment

from that found in the UK. In both these areas, temperatures

exceed those in the UK and there is the combination of

extensive wetland marshes and large numbers of migratory

and nonmigratory birds with high population densities of

mosquitoes. The second concern is that cases of WNV

infection could be occurring but remain undiagnosed.

Only around one in 150 of those infected with WNV

develop serious neurological symptoms and so substantial

transmission might be taking place without detection. There

are around 700 hospital admissions of patients with

encephalitis a year in England and 60% of these do not have

the aetiology determined. Although only a small proportion

of these occur in older patients, there is a suggestion that the

numbers are increasing (Davison et al., 2003). We have

undertaken enhanced surveillance for cases of WNV

infection by looking at cases of viral encephalitis or menin-

gitis each summer since 2002. People older than 50 years

have a 10-fold higher risk of developing neurological illness

(Weiss et al., 2001; Sampathkumar , 2003) and so by

concentrating on older people with neurological features,

we are trying to maximize resources. Despite reminding all

clinicians of the features of WNV and the alerting them to

this scheme, we capture relatively small numbers of patients

through the surveillance scheme. More samples are referred

directly to the laboratory but relatively few of these are

from older patients with compatible symptoms and without

a travel history. So far all samples have been negative for

WNV. In addition, CSF from patients aged over 50 years

with viral encephalitis or meningitis have also been exam-

ined, and WNV was not found in this group either.

Although the occasional case of WNV infection may well

have been missed, we feel if there were clusters of cases of

neurological disease due to WNV we would have detected

them.

No bird die-offs have been noted in England and Wales,

but although birds have been found to show evidence of

WNV infection in many parts of Europe (Malkinson &

Banet, 2002), abnormal bird deaths do not appear to be a

feature of the European outbreaks (Murgue et al., 2001a)

unlike in the USA where mass bird die-off heralded WNV

cases in humans (Yaremych et al., 2004). One study in

England has reported finding evidence of WNV infection in

resident and migratory birds in two sites in England. All

birds were healthy and over 350 sera were tested, and 14.7%

were Plaque Reduction Neutralization Test positive for

WNV. A nested RT-PCR found the presence of WNV RNA

in six magpies and one blackbird. Infectious virus was not

detected (Buckley et al., 2003). The ongoing study of dead

birds has not yet detected WNV.

In England and Wales, there is a coordinated response to

WNV with ongoing surveillance of humans, horses, dead

birds and mosquitoes, and the development of a specific

WNV contingency plan. As we face more and more poten-

tial public health problems, it is a dilemma how much

resource should be spent looking for WNV infection,

especially given its sporadic and unpredictable mode of

presentation observed in many other countries. It is not

clear for how long these activities should be continued and

whether we need more or less action in future. However,

WNV has demonstrated the need for a multi-agency

approach to surveillance and preparedness. There needs to

be multi-agency working at the local, regional and national

level and plans exercised to identify gaps and ensure the

understanding of roles and responsibilities. If this is estab-

lished for WNV, then this would lead to an effective and

coordinated response in the event of the emergence of a new

vector-borne zoonotic infection.

Acknowledgements

This paper is based on a presentation made at the FEMS

symposium on Vector-borne Emerging and Re-emerging

Pathogens and their Infections held in Istanbul, June 2005. I

would like to thank the organisers for inviting me to the

meeting.

I would like to acknowledge members of the Depart-

ment of Health WNV task force including: Maggie Tomlin-

son, John Stephenson and Ailsa Wight (DH), Graham

Lloyd, David Brown, Amanda Walsh (HPA), Paul Manser

(Defra) Steve Lindsay (Durham University), Richard Har-

rington (BBSRC, Rothamstead Research), Bill Reilly (Health

Protection Scotland) Steve Edwards and Ian Brown (Veter-

inary Laboratories Agency)

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