**1. Introduction**

Mosquito-borne diseases (MBDs) are dangerously increasing in prevalence, geographical distribution and severity, representing a worldwide emerging threat for both humans and animals. Of great concern are the infections caused by viruses belonging to the *Flavivirus*

© 2016 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. © 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

genus. This genus includes viruses considered endemic in Italy as West Nile Virus (WNV) and Usutu virus (USUV) transmitted by *Culex* sp. and viruses as Dengue virus (DENV) and Zika virus (ZIKV), transmitted by *Aedes* sp., not endemic in Italy but with the potential to spread to new areas where the mosquito vector is present.

to a severe, sometimes fatal disease characterized by haemorrhage and shock, known as den-

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53

The classic clinical picture of ZIKV infection resembles that of dengue fever and is manifested by fever, headache, arthralgia, myalgia, conjunctivitis and maculopapular rash. Recently, a possible association between ZIKV infection in pregnancy and fetal malformations has been

Up to date, all the DENV and ZIKV human cases reported in Italy have been related only with returning travellers from endemic countries and not associated with transmission through

However, if vectors are present, infected returning travellers could initiate a local virus transmission as in the CHIKV outbreak occurred in the Emilia-Romagna Region, Italy, in 2007 [22].

Clinical onset is abrupt, with high fever, headache, back pain, myalgia and arthralgia; the latter can be intense, affecting mainly the extremities (ankles, wrists, phalanges) but also the large joints. Skin involvement is present in about 40–50% of cases and consists of a pruriginous maculopapular rash predominating on the thorax. The symptoms generally resolve within 7–10 days, except for joint stiffness and pain: up to 12% of patients still have chronic

Italy experienced two CHIKV autochthonous outbreaks, in Emilia Romagna Region in 2007 and in Lazio Region in 2017, due to returning infected travellers during the vectors' season

Given the complex epidemiology of MBDs, determined by the interaction between pathogens, hosts, vectors and ecosystem, the cooperation of multiple disciplines (veterinarians, epidemiologists, entomologists, biologists and doctors) is needed for an effective early warning, surveillance and control [24]. A deep knowledge is required to better perform the surveillance plans: viruses with different cycles need different surveillance approaches. The syndromic surveillance on human cases could be considered more adequate to detect the introduction of new viruses in which humans are the reservoir. However, the entomological surveillance can be a valuable additional tool, considering that the presence of risk factors as competent vectors and suitable climatic conditions significantly increases the potential risk for the possible

**1.1. West Nile virus national surveillance programme: origin and evolution towards** 

mainly through blood transfusion and organ transplantation.

central Italy); no cases of human encephalitis were reported [25].

Among MBDs, since almost 20 years, surveillance activities and control measures against WNV represent a deal both in human and in veterinary medicine, due to its complicated transmission cycle, the zoonotic potential and the risk of human-to-human transmission

In Italy, the WNV circulation was firstly detected in the late summer of 1998, in horses that displayed neurological clinical symptoms in a wetland area located in Toscana Region (West-

CHIKV is characterized by a human-to-mosquito-to-human cycle of transmission.

gue haemorrhagic fever/dengue shock syndrome [19].

local potentially competent vectors [21].

arthralgia, 3 years after onset of the illness [23].

autochthonous transmission of MBDs.

hypothesized [20].

with hundreds of cases.

**an integrated system**

Furthermore, in the last 10 years (2007/2017), two autochthonous Chikungunya virus outbreaks (CHIKV\_ *Alphavirus* genus, family Togaviridae transmitted by *Aedes* sp.) with hundreds of cases due to an imported case followed by local vectorial transmission occurred in Italy, showing the impact that this virus could have even in a non-endemic country [1, 2].

Given the complex epidemiology of MBDs, Public Health Authorities are encouraging the interaction between multiple disciplines to implement an effective early warning.

WNV and USUV are antigenically close flavivirus with similar enzootic birds-mosquitoes transmission cycle where co-circulation has been reported in several studies [3–6].

WNV can be occasionally transmitted, through mosquito bites, to vertebrates other than birds as humans and horses that are considered dead-end hosts. Human infection through blood transfusion and solid organ transplantation is also demonstrated [7].

WNV risk for human health is well recognized: the majority (\*80%) of infections in humans are asymptomatic, and symptomatic infections are mostly characterized by a mild, self-limiting febrile illness. WNV neuroinvasive disease develops in <1% of WNV-infected persons [8].

USUV is generally correlated with high mortality rates in its bird reservoirs. Mosquitoes infected with USUV can incidentally transmit the virus to other vertebrates, including humans, which can result in neuroinvasive disease [9].

In Italy, an increasing number of outbreaks of West Nile disease, with occurrences of human cases, have been reported since 2008, mainly in the North East part of the Country.

WNV lineage 1 (Lin1) was the only strain detected until 2011 when, for the first time, the presence of both WNV Lin1 and WNV lineage 2 (Lin2) was demonstrated. Since 2013, WNV Lin2 was the main strain detected, and a west bound spread of the virus started [8].

USUV has been detected in Italy since 2007 in mosquitoes, birds and humans [10–13].

Although characterized by a lower pathogenicity than WNV, USUV pathogenic potential for human is not completely characterized, and knowledge about this crucial aspect is constantly evolving [14–16]. In 2009, two cases of encephalitis in immunocompromised patients were reported in Italy [10, 12, 17], and additional USUV neuroinvasive infections in humans were described in Croatia in 2013 even in one healthy patient [18].

Finally, retrospective analyses to monitor the spread and to evaluate the role for public health of USUV in an endemic area conducted in the city of Modena showed a high seroprevalence in humans with or without neurologic impairments, underlying that USUV infection in humans should not be considered a sporadic event [16].

DENV and ZIKV are characterized by a human-to-mosquito-to-human cycle of transmission.

DENV is the most prevalent arthropod-borne viral disease in tropical and subtropical countries. The disease manifestations range from an influenza-like disease known as dengue fever to a severe, sometimes fatal disease characterized by haemorrhage and shock, known as dengue haemorrhagic fever/dengue shock syndrome [19].

genus. This genus includes viruses considered endemic in Italy as West Nile Virus (WNV) and Usutu virus (USUV) transmitted by *Culex* sp. and viruses as Dengue virus (DENV) and Zika virus (ZIKV), transmitted by *Aedes* sp., not endemic in Italy but with the potential to

Furthermore, in the last 10 years (2007/2017), two autochthonous Chikungunya virus outbreaks (CHIKV\_ *Alphavirus* genus, family Togaviridae transmitted by *Aedes* sp.) with hundreds of cases due to an imported case followed by local vectorial transmission occurred in Italy, showing the impact that this virus could have even in a non-endemic country [1, 2].

Given the complex epidemiology of MBDs, Public Health Authorities are encouraging the

WNV and USUV are antigenically close flavivirus with similar enzootic birds-mosquitoes

WNV can be occasionally transmitted, through mosquito bites, to vertebrates other than birds as humans and horses that are considered dead-end hosts. Human infection through blood

WNV risk for human health is well recognized: the majority (\*80%) of infections in humans are asymptomatic, and symptomatic infections are mostly characterized by a mild, self-limiting febrile illness. WNV neuroinvasive disease develops in <1% of WNV-infected persons [8]. USUV is generally correlated with high mortality rates in its bird reservoirs. Mosquitoes infected with USUV can incidentally transmit the virus to other vertebrates, including

In Italy, an increasing number of outbreaks of West Nile disease, with occurrences of human

WNV lineage 1 (Lin1) was the only strain detected until 2011 when, for the first time, the presence of both WNV Lin1 and WNV lineage 2 (Lin2) was demonstrated. Since 2013, WNV Lin2

Although characterized by a lower pathogenicity than WNV, USUV pathogenic potential for human is not completely characterized, and knowledge about this crucial aspect is constantly evolving [14–16]. In 2009, two cases of encephalitis in immunocompromised patients were reported in Italy [10, 12, 17], and additional USUV neuroinvasive infections in humans were

Finally, retrospective analyses to monitor the spread and to evaluate the role for public health of USUV in an endemic area conducted in the city of Modena showed a high seroprevalence in humans with or without neurologic impairments, underlying that USUV infection in

DENV and ZIKV are characterized by a human-to-mosquito-to-human cycle of transmission. DENV is the most prevalent arthropod-borne viral disease in tropical and subtropical countries. The disease manifestations range from an influenza-like disease known as dengue fever

cases, have been reported since 2008, mainly in the North East part of the Country.

USUV has been detected in Italy since 2007 in mosquitoes, birds and humans [10–13].

was the main strain detected, and a west bound spread of the virus started [8].

interaction between multiple disciplines to implement an effective early warning.

transmission cycle where co-circulation has been reported in several studies [3–6].

transfusion and solid organ transplantation is also demonstrated [7].

humans, which can result in neuroinvasive disease [9].

described in Croatia in 2013 even in one healthy patient [18].

humans should not be considered a sporadic event [16].

spread to new areas where the mosquito vector is present.

52 Current Topics in Tropical Emerging Diseases and Travel Medicine

The classic clinical picture of ZIKV infection resembles that of dengue fever and is manifested by fever, headache, arthralgia, myalgia, conjunctivitis and maculopapular rash. Recently, a possible association between ZIKV infection in pregnancy and fetal malformations has been hypothesized [20].

Up to date, all the DENV and ZIKV human cases reported in Italy have been related only with returning travellers from endemic countries and not associated with transmission through local potentially competent vectors [21].

However, if vectors are present, infected returning travellers could initiate a local virus transmission as in the CHIKV outbreak occurred in the Emilia-Romagna Region, Italy, in 2007 [22].

CHIKV is characterized by a human-to-mosquito-to-human cycle of transmission.

Clinical onset is abrupt, with high fever, headache, back pain, myalgia and arthralgia; the latter can be intense, affecting mainly the extremities (ankles, wrists, phalanges) but also the large joints. Skin involvement is present in about 40–50% of cases and consists of a pruriginous maculopapular rash predominating on the thorax. The symptoms generally resolve within 7–10 days, except for joint stiffness and pain: up to 12% of patients still have chronic arthralgia, 3 years after onset of the illness [23].

Italy experienced two CHIKV autochthonous outbreaks, in Emilia Romagna Region in 2007 and in Lazio Region in 2017, due to returning infected travellers during the vectors' season with hundreds of cases.

Given the complex epidemiology of MBDs, determined by the interaction between pathogens, hosts, vectors and ecosystem, the cooperation of multiple disciplines (veterinarians, epidemiologists, entomologists, biologists and doctors) is needed for an effective early warning, surveillance and control [24]. A deep knowledge is required to better perform the surveillance plans: viruses with different cycles need different surveillance approaches. The syndromic surveillance on human cases could be considered more adequate to detect the introduction of new viruses in which humans are the reservoir. However, the entomological surveillance can be a valuable additional tool, considering that the presence of risk factors as competent vectors and suitable climatic conditions significantly increases the potential risk for the possible autochthonous transmission of MBDs.

## **1.1. West Nile virus national surveillance programme: origin and evolution towards an integrated system**

Among MBDs, since almost 20 years, surveillance activities and control measures against WNV represent a deal both in human and in veterinary medicine, due to its complicated transmission cycle, the zoonotic potential and the risk of human-to-human transmission mainly through blood transfusion and organ transplantation.

In Italy, the WNV circulation was firstly detected in the late summer of 1998, in horses that displayed neurological clinical symptoms in a wetland area located in Toscana Region (Westcentral Italy); no cases of human encephalitis were reported [25].

After this outbreak, a national veterinary surveillance plan was implemented in 2001 under the coordination of the Italian Ministry of Health (MoH) and of the National Reference Centre for Exotic Diseases of Animals (CEntro Studi Malattie Esotiche; CESME), with the aim to early detect new incursions of WNV. Throughout the whole Italian territory, 15 risk wetland areas were identified, considering the presence of migrating birds as a possible risk of virus introduction. During the transmission season, active surveillance was conducted by the periodic serological screening of sentinel-chicken flocks and sentinel horses, in order to detect antibodies against WNV. Moreover, passive surveillance was conducted by virological screening of carcasses of dead birds and by clinical surveillance of neurological signs in equines all over the year [26].

In 2008, after 10 years of disappearance, a large WNV epidemic affected regions in the Northeast of Italy surrounding the Po river Delta. The virus was identified in mosquitoes, birds, horses and humans.

Following these events, the surveillance system was updated with the aim to detect as early as possible the WNV circulation. Three epidemiological areas were identified with different surveillance approach (**Figure 1**) [27]:

**1.** Area with Virus Circulation (AVC): areas of Northern Italy with WNV circulation during 2008. The aim of surveillance in this area was to evaluate WNV spread. Active surveillance was conducted by virological testing on synanthropic birds and/or by serological testing on sentinel-chicken flocks or free-range poultry flocks throughout the epidemiological season; entomological surveillance was enforced in 10 horse stables during the whole year with monthly mosquito trapping, in order to evaluate the role of mosquitoes as WNV vectors;

In Northern Italy, the virus has become endemic, progressively extending the range from the East to the West in the Po river valley area. The establishment of overwintering cycle was due to the presence of the main mosquito vector *Culex pipiens* at high density and the evidence of

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In 2010, the MoH published a National Plan for WNND Human Surveillance in Italy, which refer to the WNV veterinary Surveillance Plan. This was the first step towards the adoption of a comprehensive human and veterinary (animals and vectors) surveillance system against

The national definition of WNND suspected human case included every patient presenting with fever ≥38.5°C and neurological symptoms: encephalitis, meningitis or acute polyradiculoneuritis (Guillain-Barré syndrome) or acute flaccid paralysis. Every suspect case of WNV infection was promptly reported to the Public Health Department and laboratory investigated. Clinical suspected cases of WNND or West Nile Fever (WNF) were classified as confirmed cases if they fulfilled at least one of the following laboratory criteria: (1) isolation of WNV from blood or cerebrospinal fluid (CSF), (2)the presence of IgM antibodies in CSF by ELISA, (3) the detection of WNV RNA by RT-PCR in blood and/or CSF and (4) the detection of increased levels of IgM and IgG antibodies against WNV by neutralization testing [29].

Human or veterinary WNV confirmed cases have to be notified by the Regional authorities to

In line with the EU directive for blood safety (Directive 2004/33/EC, Annex III), from 2009 to 2014, the NBC implemented, as a preventive measure, a 28-day deferral period for blood

the national level, both to the MoH and to the National Blood Center (NBC).

virus transmission in resident wild bird species susceptible to WNV infection [28].

WNV in Italy.

**Figure 1.** Map of Italy with WNV surveillance areas.


Passive surveillance was carried throughout the year in the whole Italian area by the detection of neurological signs in equines and increased mortality among wild birds.

Since 2008, WNV has expanded to a wide geographical area in Europe and the Mediterranean basin, with an increasing number of outbreaks, including several human cases of West Nile Neuroinvasive Disease (WNND).

Mosquito-Borne Diseases and 'One Health': The Northwestern Italian Experience http://dx.doi.org/10.5772/intechopen.78985 55

**Figure 1.** Map of Italy with WNV surveillance areas.

After this outbreak, a national veterinary surveillance plan was implemented in 2001 under the coordination of the Italian Ministry of Health (MoH) and of the National Reference Centre for Exotic Diseases of Animals (CEntro Studi Malattie Esotiche; CESME), with the aim to early detect new incursions of WNV. Throughout the whole Italian territory, 15 risk wetland areas were identified, considering the presence of migrating birds as a possible risk of virus introduction. During the transmission season, active surveillance was conducted by the periodic serological screening of sentinel-chicken flocks and sentinel horses, in order to detect antibodies against WNV. Moreover, passive surveillance was conducted by virological screening of carcasses of dead birds and by clinical surveillance of neurological signs in equines all over

In 2008, after 10 years of disappearance, a large WNV epidemic affected regions in the Northeast of Italy surrounding the Po river Delta. The virus was identified in mosquitoes,

Following these events, the surveillance system was updated with the aim to detect as early as possible the WNV circulation. Three epidemiological areas were identified with different

**1.** Area with Virus Circulation (AVC): areas of Northern Italy with WNV circulation during 2008. The aim of surveillance in this area was to evaluate WNV spread. Active surveillance was conducted by virological testing on synanthropic birds and/or by serological testing on sentinel-chicken flocks or free-range poultry flocks throughout the epidemiological season; entomological surveillance was enforced in 10 horse stables during the whole year with monthly mosquito trapping, in order to evaluate the role of mosquitoes as WNV

**2.** Surveillance Zone (SZ): areas surrounding the AVC for an extension of 20 km. The aim of surveillance in this area was to monitor WNV spread over the AVC. Active surveillance was conducted by virological testing on synanthropic and/or by serological testing on chickens or poultry flocks as enforced in AVC and by recruitment of sentinel horses for repeated serological tests in May, August and September in order to detect seroconversion against WNV. Entomological surveillance was enforced in three horse stables with monthly mosquito trapping throughout the year, in order to evaluate the role of mosqui-

**3.** Areas at Risk (AR): 14 wetlands inherited from the previous surveillance plan. The aim of surveillance in this area was to detect WNV new introduction by migration routes. Active surveillance was conducted on synanthropic and chickens or poultry flocks as enforced as in AVC, and the same testing of sentinel horses as in SZ; entomological surveillance was enforced in one horse sentinel stable by monthly mosquito trapping during the epidemic

Passive surveillance was carried throughout the year in the whole Italian area by the detection

Since 2008, WNV has expanded to a wide geographical area in Europe and the Mediterranean basin, with an increasing number of outbreaks, including several human cases of West Nile

season, in order to evaluate the composition of mosquito fauna.

of neurological signs in equines and increased mortality among wild birds.

the year [26].

vectors;

toes as WNV vectors;

Neuroinvasive Disease (WNND).

birds, horses and humans.

surveillance approach (**Figure 1**) [27]:

54 Current Topics in Tropical Emerging Diseases and Travel Medicine

In Northern Italy, the virus has become endemic, progressively extending the range from the East to the West in the Po river valley area. The establishment of overwintering cycle was due to the presence of the main mosquito vector *Culex pipiens* at high density and the evidence of virus transmission in resident wild bird species susceptible to WNV infection [28].

In 2010, the MoH published a National Plan for WNND Human Surveillance in Italy, which refer to the WNV veterinary Surveillance Plan. This was the first step towards the adoption of a comprehensive human and veterinary (animals and vectors) surveillance system against WNV in Italy.

The national definition of WNND suspected human case included every patient presenting with fever ≥38.5°C and neurological symptoms: encephalitis, meningitis or acute polyradiculoneuritis (Guillain-Barré syndrome) or acute flaccid paralysis. Every suspect case of WNV infection was promptly reported to the Public Health Department and laboratory investigated. Clinical suspected cases of WNND or West Nile Fever (WNF) were classified as confirmed cases if they fulfilled at least one of the following laboratory criteria: (1) isolation of WNV from blood or cerebrospinal fluid (CSF), (2)the presence of IgM antibodies in CSF by ELISA, (3) the detection of WNV RNA by RT-PCR in blood and/or CSF and (4) the detection of increased levels of IgM and IgG antibodies against WNV by neutralization testing [29].

Human or veterinary WNV confirmed cases have to be notified by the Regional authorities to the national level, both to the MoH and to the National Blood Center (NBC).

In line with the EU directive for blood safety (Directive 2004/33/EC, Annex III), from 2009 to 2014, the NBC implemented, as a preventive measure, a 28-day deferral period for blood donor, leaving areas with ongoing transmission of WNV and WNV Nucleic Acid Test (NAT), testing of all donations (peripheral blood, bone marrow and cord blood stem cell donations) generally from July to November [30] and coming from Provinces in which human cases of WNND had been reported the previous year.

**3.** Human surveillance: active identification of all possible, probable and confirmed WNV

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The integrated plan was updated in 2017, including activities to control USUV and assess the risk for public health (MoH) [32]. Indeed, in the last years in Europe and northern Italy, the co-circulation of WNV and USUV was largely demonstrated [4–5, 33]. The two viruses seem to show biological cycle similarities, but while the WNV risks for human health are well recognized, knowledge about the medical importance of USUV is not fully understood and the transmission risk throughout blood transfusion has been recently sug-

This underlined the need to put in place surveillance measures to detect USUV activity and to assess the risk for public health. As in northern Italy, USUV shows a substantial geographic overlap with WNV circulation, surveillance was enforced in WNV endemic areas, by routine

After the CHIKV outbreak in 2007 in Italy, a national plan on imported and autochthonous human vector-borne disease (including CHIKV, ZIKA, DENV and WNV) has been implemented and annually updated on the basis of the epidemiological changes-based

The plan has been annually revised to 2017 with minor changes except for the exclusion of WNV and USUV in 2016/2017 from the human plan, due to the birth of the WNV/USUV

• to monitor imported cases in Italy, in particular in areas where there are competent mosquitoes, for the assessment of the risk of possible autochthonous transmission of the virus; • the early identification of outbreaks and the monitoring of local transmission in order to

• to prevent accidental transmission through blood or organs transfusion and to identify

The human surveillance is carried out throughout the year. However, during the period of a major vector activity (June–October), the surveillance system will have to be strengthened (in terms of timeliness and sensitivity) in mosquito-infested areas, to allow the identification of cases, for the immediate adoption of the necessary control measures (in relation to entomo-

differential diagnosis of all cases of WNV-positive test (serological/virological).

infection human cases, including WNND.

**2. Human MBDs national surveillance plan**

gested [34, 35].

evidences.

National integrated Plan.

Here, we summarize the main concepts.

Epidemiological surveillance of human cases.

The main objectives of human surveillance are the following:

other potential transmission pathways (e.g. sexual).

logical surveillance) and to reduce the risk of transmission.

implement control measures (prevention and response activities);

The NAT screening approach changed in 2015 for five Northern Italian Regions (Piemonte, Lombardy, Friuli Venezia Giulia, Veneto and Emilia-Romagna) concerned by WNV circulation in previous years. These regions guaranteed an active standardized integrated entomologic and veterinary WNV surveillance from June to October. In addition to the notification of human cases, the date detection of WNV in mosquitoes and wild birds or detection of WNV-IgM antibodies in horses was introduced as new trigger criteria for the implementation of WNV NAT testing for the screening of blood donors [31].

Since 2009, a total of 103 WNV positive samples in blood donors have been reported in Northern Italy (Veneto, Lombardia and Emilia-Romagna Regions).

Comprehensive epidemiological, virological and entomological surveillance system is crucial for the timely detection of the spread of WNV, implementation of control measures and prevention of virus transmission in humans. Both national WNV veterinary and human surveillance plan have undergone further revisions year by year, in order to adapt to the seasonal evolution of the epidemiological scenario.

In 2016, the MoH has released a National WNV veterinary-entomological-human integrated Surveillance Plan. According to 'One-Health' approach, real-time cross-sectorial collaboration by Public and Veterinary Health Institutions is crucial to timely achieve and share information in WNV surveillance as a key to improve the management of WNV outbreaks and mitigate the risk of human transmission.

The aim of the programme was to early detect WNV circulation, reducing the risk of infection in the human populations. The steps to achieve this goal are as follows:

	- **a.** Endemic areas, where WNV was detected in the previous 2 years (mainly Regions of the Po river Valley, Sicilia e Sardegna islands): reinforcement of the virological screening in migratory and resident wild birds, mainly belonging to *Corvidae* genus. Alternatively, serological testing of rural poultry or sentinel chickens groups.
	- **b.** Non-endemic areas (the remaining Italian Regions): serological testing of horses sera, in order to detect WNV-specific IgM early antibodies (recent infection).

**3.** Human surveillance: active identification of all possible, probable and confirmed WNV infection human cases, including WNND.

The integrated plan was updated in 2017, including activities to control USUV and assess the risk for public health (MoH) [32]. Indeed, in the last years in Europe and northern Italy, the co-circulation of WNV and USUV was largely demonstrated [4–5, 33]. The two viruses seem to show biological cycle similarities, but while the WNV risks for human health are well recognized, knowledge about the medical importance of USUV is not fully understood and the transmission risk throughout blood transfusion has been recently suggested [34, 35].

This underlined the need to put in place surveillance measures to detect USUV activity and to assess the risk for public health. As in northern Italy, USUV shows a substantial geographic overlap with WNV circulation, surveillance was enforced in WNV endemic areas, by routine differential diagnosis of all cases of WNV-positive test (serological/virological).
