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Vector- and Rodent-Borne Diseases in Europe and North America


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The vector- and rodent-borne diseases of Europe
and North America: their distribution and public
health of burden

There are a significant number of diseases carried by insects such as mosquitoes or sand flies or by ticks, mites and rodents, and these are far more common than is often realized. New diseases are constantly being discovered and are becoming more widely distributed with the increase in travelling, to and from tropical, disease-endemic countries. Here, Norman Gratz (former Director, Division of Vector Biology and Control, World Health Organization), reviews the distribution of the vector and rodent-borne diseases in Europe, the USA and Canada; their incidence and prevalence, their costs and hence their public health burdens are detailed, and their arthropod vectors and rodent reservoir hosts described. Armed with such information, the individual clinician is more likely to have a degree of epidemiological suspicion that will lead to an earlier diagnosis and correct treatment of these infections. Equally, authorities will more readily understand the measures necessary to control this group of infectious agents.

The vector-and
diseases of Europe
and North
America: their
distribution and
public health

Norman G. Gratz

World Health Organization, Geneva

Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo

Cambridge University Press
The Edinburgh Building, Cambridge CB2 2RU, UK

Published in the United States of America by Cambridge University Press, New York
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  Acknowledgements   xi
  Tribute to the author, Norman Gratz   xii
  Preface   xiii
  Introduction   1
Part I   The vector- and rodent-borne diseases of Europe
2   Vector and rodent-borne diseases in European history    5
3   The arboviruses    9
4   The mosquito-borne arboviruses of Europe    10
  West Nile Virus    10
  Batai virus (Calovo virus)    24
  Ockelbo virus    24
  Inkoo virus    27
  Tahyna virus    27
  Usutu virus    28
  Dengue virus    30
5   Mosquito-borne diseases of Europe – malaria    33
  Recrudescence of autochthonous malaria in Europe    34
  The problem of imported malaria in Europe    37
  Imported malaria in other countries of Europe    49
  Airport malaria    49
6   Mosquito-borne filarial infections    52
  The public health importance of dirofilariasis    53
7   Sandfly-borne diseases    55
  Sandfly-borne diseases – viruses    55
  Sandfly fever in Europe    55
  Sandfly-borne diseases – Leishmaniasis    57
  Distribution and incidence of visceral leishmaniasis    58
  Cutaneous leishmaniasis    67
  Leishmaniasis/HIV    68
  The sandfly vectors of leishmaniasis in Europe    70
  Conclusions on the public health importance of leishmaniasis in Europe    72
8   Ceratopogonidae – biting midge-borne diseases    74
9   Dipteran-caused infections – myiasis    75
10   The flea-borne diseases    78
  Plague    78
  Flea-borne rickettsial diseases    78
  The ELB agent    80
  Cat scratch disease    81
11   The louse-borne diseases    83
  Louse-borne rickettsial diseases    83
  Trench fever    84
  Louse-borne relapsing fever    86
  Body louse infestations    86
  Head louse infestations    86
  Pubic louse infestations    87
12   Tick-borne diseases of Europe    89
  Tick-borne viruses    89
  Bhanja virus    107
  Thogoto virus    108
  Dhori virus    108
  Tribec virus    109
  Tettnang virus    109
  Eyach virus    109
  Tick-borne bacterial infections    110
  Tick-borne relapsing fever    110
  Lyme disease    111
  Tick-borne rickettsial infections    134
  Other spotted fever rickettsiae in Europe    136
  Ehrlichiosis    140
  Q Fever    141
  Babesiosis    144
  The public health importance of babesiosis    145
  Tularaemia    146
  Tick paralysis    148
13   Mite-borne infections and infestations    149
  Scabies    149
  Rickettsial pox    151
  Mites and allergies    151
14   Cockroaches and allergies    154
15   Vector-borne disease problems associated with introduced vectors in Europe    156
16   Factors augmenting the incidence, prevalence and distribution of vector-borne diseases in Europe    159
  Ecological changes    159
17   The potential effect of climate change on vector-borne diseases in Europe    161
18   The rodent-borne diseases of Europe    163
  The hantaviruses    163
  Puumala virus    164
  Dobrava virus    167
  Saaremaa virus    168
  Lymphocytic choriomeningitis virus    168
  Bacterial diseases    169
  Rat bite fever    170
  Rodent-borne salmonellosis    171
  Protozoal diseases    172
  Rodent-borne cestode infections    173
  Rodent-borne nematode infections    175
  Conclusions    176
19   The economic impact and burden of vector- and rodent-borne diseases in Europe    177
  Costs associated with arboviruses    177
  Costs associated with malaria resurgence in Europe    178
  Costs associated with imported malaria    179
  Costs associated with mosquito control    180
  Costs associated with lice and scabies control    181
  Costs associated with Lyme disease    181
  Conclusions    182
part II   The vector- and rodent-borne diseases of North America
20   Vector- and rodent borne diseases in the history of the USA and Canada    185
  The arboviruses    185
  Epidemic or louse-borne typhus    187
  Rocky Mountain spotted fever    187
  Malaria    188
21   The mosquito-borne arboviruses    190
  Togoviridae    191
  Flaviviridae    195
  Bunyaviridae    202
  Conclusions on the public health importance of arboviruses in the USA and Canada    206
22   Mosquito-borne diseases – malaria    207
  Conclusions on the public health importance of malaria in the USA and Canada    209
23   Mosquito-borne filarial infections    211
  The public health importance of dirofilariasis    213
24   Sandfly-borne diseases    214
  The phleboviruses    214
  Leishmaniasis    214
25   Ceratopogonidae – biting midge-borne diseases    216
26   Dipteran caused infections – myiasis    217
27   Flea-borne diseases    220
  Plague    220
  Flea-borne rickettsial diseases    224
  Cat scratch disease (CSD)    226
28   The louse-borne diseases    228
  Louse-borne or epidemic typhus    228
  Trench fever    229
  Body louse infestations    230
  Head louse infestations    230
  Pubic louse infestations    231
29   Triatomine-borne diseases    233
  American trypanosomiasis or Chagas disease    233
  Chagas disease vectors    234
  Chagas disease reservoir hosts    234
  The public health importance of Chagas disease in the USA    235
30   Tick-borne diseases of the USA and Canada    236
  Tick-borne viruses    236
  Powassan virus    237
  Tick-borne bacterial infections    239
  Lyme disease    240
  Conclusions on the public health importance of Lyme disease in the USA and Canada    244
  Southern tick-associated rash illness    245
  Rocky Mountain spotted fever    246
  Reservoir hosts of Rocky Mountain spotted fever    248
  Conclusions regarding Rocky Mountain spotted fever    248
  Ehrlichiosis    249
  Q fever    252
  Babesiosis    253
  Tularaemia    255
  Tick paralysis    257
31   Mite-borne infections and infestations    259
  Scabies    259
  Rickettsial pox    261
  Mites and allergies    262
32   Cockroaches and allergies    267
  The public health importance of cockroach allergies    268
33   Factors augmenting the incidence, prevalence and distribution of vector-borne diseases in the USA and Canada    269
  The effect of ecological changes    269
  The possible effects of climate change    270
  Vector-borne disease problems associated with introduced vectors    271
34   The rodent-borne diseases of the USA and Canada    279
  The hantaviruses    279
  Rodent reservoir hosts    284
  Arenaviruses    286
  Leptospirosis    290
  Rat-bite fever    291
  Salmonellosis    292
  Toxoplasmosis    293
  Cestode infections    294
  Nematode infections – trichinosis    296
  Conclusions    296
35   The economic impact of vector- and rodent-borne diseases in the USA and Canada    298
  Eastern equine encephalitis    298
  La Crosse encephalitis    299
  St. Louis encephalitis    299
  West Nile virus    300
  Dengue    301
  Imported malaria    302
  Lice infestations    303
  Scabies infestations    303
  Lyme disease    303
  Mosquito control    304
  Conclusions    305
36   Conclusions on the burden of the vector and rodent-borne diseases in Europe, the USA and Canada    306
  References    310
  Index    370


The author gratefully acknowledges the assistance provided by Professor Mike Service who read the manuscript and provided many valuable suggestions and corrections for the text.

My thanks are due to Dr Graham White for his encouragement to me forbeginning the writing of the book.

I much appreciate the information provided to me by Dr Joseph M. Conlon.

Cambridge University Press would like to thank Professor Mike Service for all his efforts in editing this manuscript following the death of Norman Gratz.

Tribute to the author, Norman Gratz

Despite battling with illness Dr Norman Gratz valiantly tried to complete his manuscript of this book and send it to Cambridge University Press for publication. He succeeded in doing this. Sadly, however, he died in Geneva soon afterwards, in November 2005, and so never saw his magnum opus published.

Norman joined the World Health Organization in 1958 and remained with the organization for the rest of his working life. On retirement he continued to serve on WHO committees and act as a consultant for WHO, numerous chemical companies, and government and non-government agencies.

He was one of the few medical entomologists who was also involved with the role of rodent reservoir hosts in disease transmission and soon became recognized worldwide as an authority on vector-borne diseases and their control. Norman travelled extensively for WHO in Africa, Asia and Latin America advising on research and control strategies on the vectors of malaria, filariasis, Chagas disease, murine typhus, plague and various tick-borne diseases.

Norman published more than 100 scientific papers and in 1985 received the Medal of Honour from the American Mosquito Control Association. He built up an amazing database of more than 31000 abstracts on vector- and rodent-borne infections which became the foundation for this book.

On several occasions I told Norman that because of his vast knowledge of vector- and rodent-borne infections he was probably the only single person who could write this book.

Mike W. Service

Emeritus Professor of Medical Entomology

Liverpool School of Tropical Medicine


Until the early part of the twentieth century many vector-and rodent-borne infections were very serious public health problems in Europe and North America. Thousands of cases of malaria occurred annually throughout these regions and populations suffered greatly from the disease. Malaria transmission persisted in most of southern Europe and the USA until it was eradicated in the 1950s. Among the arboviruses, dengue transmitted by the mosquito Aedes aegypti, was the cause of a great epidemic in Athens, Greece in 1928 with over 650000 cases and more than a thousand deaths. The same species was also the vector of yellow fever which caused many thousands of deaths in the USA during the nineteenth century; the last epidemic of the disease occurred in New Orleans in 1905 with more than 3000 cases and at least 452 deaths being recorded. Great epidemics of louse-borne typhus occurred in many parts of Europe during World War I accounting for great human mortality. The war-associated louse-borne diseases such as epidemic typhus, epidemic relapsing fever and trench fever disappeared after 1945 due to the applications of the newly discovered DDT and related compounds; at the time, optimism ran high that this group of infections was unlikely to again be a problem, and indeed at the time effective control was obtained of most of the group.

Yet by the end of the twentieth century, vector and rodent-borne infections have again become serious public health problems; there has been a recrudescence of several diseases long thought to have been eradicated or under effective control; at the same time, new vector and rodent-borne diseases have been discovered both in Europe and North America, some of which now occur in high incidence. A number of diseases in this group have been introduced into geographical areas in which they have not previously been found such as the introduction of West Nile Virus into New York in 1999; the virus and diseases it causes have subsequently spread throughout the USA and much of Canada. At the time of writing, six years after the introduction of the virus, there is no sign of a significant diminution in its annual incidence in the USA.

Among the tick-borne infections, Lyme disease was first identified in 1975 as the cause of an epidemic of arthritis occurring near Old Lyme, Connecticut. This infection has now become the most common vector-borne disease in both the USA and Europe and in parts of eastern Canada. Tens of thousands of cases now occur yearly in Europe and the USA. In the years 2001 and 2002, nearly 41000 cases of Lyme disease were reported to the US Centers for Disease Control and Prevention (CDCP) and, in Europe, it has been estimated that as many as 60000 cases a year occur in Germany alone.

Tick-borne encephalitis virus transmitted by Ixodes ricinus in western Europe is endemic in central, eastern and northern Europe and may cause a wide spectrum of clinical forms, ranging from asymptomatic infection to severe meningo-encephalitis. In eastern Europe the virus is transmitted by I. persulcatus and its incidence has been increasing. Ecological changes have resulted in an important spread of the tick vectors and they are now commonly found in parks in the middle of many cities throughout Europe. It appears that climate change has resulted in a northward movement of the tick vector and the disease in Sweden.

Human ehrlichiosis and anaplasmosis are tick-borne zoonotic infections that have become increasingly recognized in the USA and Europe. The increased desire of humans to pursue outdoor recreational activities during the summer months has also amplified their potential exposure to pathogenic bacteria that spend a portion of their life cycle in invertebrate bloodsucking enzootic hosts. Just like Borrelia burgdorferi, the agent of Lyme borreliosis, Ehrlichia and Anaplasma species cycle within hard-bodied ticks. Rocky Mountain spotted fever is the most severe and most frequently reported rickettsial illness in the USA. The disease is caused by Rickettsia rickettsii.

The number of annual cases of babesiosis, which is transmitted by the same tick vector as Lyme disease, is unknown but in areas of the USA where infected ticks are common, up to 20% of people have antibody results suggesting exposure. Although most of those exposed have no evidence of the disease, about 6% of people with babesiosis severe enough to require hospitalization die.

In Europe, Mediterranean Spotted Fever (MSF), also known as Boutonneuse fever, is transmitted by the dog tick, Rhipicephalus sanguineus. The disease is endemic to the Mediterranean area, where, for the last few years, the number of cases has increased, possibly due, in part, to climatic factors; in the last few decades an increased incidence of MSF was reported for Spain, France, Italy, Portugal and Israel. Mediterranean Spotted fever was originally characterized as a benign rickettsiosis. However, there have been recent reports of very severe cases in France, Spain, Israel and South Africa, manifested by cutaneous and neurological signs, psychological disturbances, respiratory problems and acute renal failure. The presence of the infectious agent, Rickettsia conorii appears to be spreading north.

Omsk haemorrhagic fever, louping-ill disease and Crimean–Congo haemorrhagic fever are other tick-borne diseases in Europe.

In both Europe and North America, ectoparasite infestations of humans such as head lice and scabies are present in increasing numbers; both of these serious pests have developed resistance to many of the insecticides that have provided effective control in the past. Scabies is the cause of frequent nosocomial outbreaks in health-care facilities.

It is now realized that house dust mites and cockroaches are responsible for an extraordinary amount of allergies including serious cases of asthma virtually everywhere and their control poses a most difficult problem.

In the last few decades a substantial number of newly emerged rodent-borne diseases of man have been recognized. Some of these infections may be due to agents that were not recognized in the past but others are characterized by such dramatic clinical courses, often with significant mortality and rapid spread, that they are to be considered truly ‘emerging diseases’. The hantaviruses belong to the emerging pathogens having gained more and more attention in the last decades. Rodent-borne haemorrhagic fever with renal syndrome has spread widely in rodent populations in Europe, the USA and parts of Canada, with an increasing number of human cases. New species of hantaviruses with greater virulence are emerging in both Europe and North America. Transmission to humans occurs by direct contact with rodents or their excreta or by inhalation of aerosolized infectious material, e.g. dust created by disturbing rodent nests.

A new rodent-borne disease syndrome has appeared in the USA; named the hantavirus pulmonary syndrome (HPS), it is frequently associated with a case fatality rate of 30–60%; the disease was at first determined to be due solely to sin nombre virus, and was thought restricted to the western USA. However, new species of viruses giving rise to HPS have now been found throughout the USA and much of the Americas. As human populations grow and spread to suburban rodent-infested areas, it is likely that hantavirus diseases will become more common in the future especially as the elimination or effective control of their wild rodent reservoir hosts can not be considered as realistic.

Many public health authorities and medical practitioners are not aware of the reappearance of this group of diseases nor of the appearance of new diseases transmitted by insects, ticks and rodents. They are not necessarily familiar with the exotic infectious agents of this group that, with increased tourism, are increasingly being imported from disease-endemic countries. This has often resulted in the delayed or mistaken diagnosis of members of this group of infections to the detriment of patients. The failure of public health authorities to recognize this group has often resulted in delays before effective measures have been undertaken to control their arthropod vectors or rodent reservoir hosts.

The following book will review the distribution of the vector and rodent-borne diseases in Europe, the USA and Canada; their incidence and prevalence, their costs and hence their public health burden will be detailed and their arthropod vectors and rodent-reservoir hosts described. Armed with such information, the individual clinician is more likely to have a degree of epidemiological suspicion that will lead to an earlier diagnosis and correct treatment of these infections. Equally, authorities will more readily understand the measures necessary to control this group of infectious agents.

The arboviruses

There are between 500 and 600 known arthropod-borne viruses, or arboviruses, in the world of which some 100 may give rise to human disease. There are six families of arboviruses; Togaviridae, Flaviviridae, Bunyaviridae, Reoviridae, Rhabdoviridae and Orthomyxoviridae. By 1996, 51 arboviruses had been reported from Europe – they are the subject of a comprehensive review by Hubalek & Halouzka (1996). Many of these viruses are not known to cause human illness; some have only been isolated from arthropods, birds or other animals and their public health significance is unknown. Others, however, may cause significant human illness and mortality. The arboviruses will be considered by the four groups of arthropods that transmit them, i.e. mosquitoes, sandflies, biting midges and ticks. The epidemiology of the arboviruses is rapidly evolving and their distribution is spreading to areas in which they have not been previously endemic and, in some cases, as appear to be occurring with West Nile virus, increased virulence has been seen in some recent outbreaks.

The mosquito-borne arboviruses of Europe

West Nile virus

West Nile virus (WNV), a member of the Japanese encephalitis complex, is a neurotropic flavivirus virus that produces damage of varying severity in human, animal and avian hosts. The virus is amplified in birds and transmitted to humans usually by Culex mosquitoes. Most cases of WNV are subclinical, with overt clinical illness affecting 1:100 to 1:150 cases. Meningoencephalitis is the most common diagnosis in hospitalized WNV patients, affecting 50–84%. In the elderly the mortality rate may range as high as 10% though it is much lower in the current outbreak in the USA. The epidemiological cycle of WNV is shown in Figure .

Transmission cycle of West Nile virus.

West Nile virus was first isolated from a febrile woman in the West Nile District of Uganda in 1937 (Smithburn et al., 1940); in 1950 it was found that the virus was present in a large percentage of normal individuals in the vicinity of Cairo, Egypt. The majority of the children from whom the sera were collected appeared to be normal; there was no evidence that children with viremia were severely ill. In 1950 more than 70% of the Cairo inhabitants aged 4 years and over had antibodies to WNV (Melnick et al. 1950).

In 1951, WNV was recognized in Israel; the disease had probably already been present in that country for several years. There were large outbreaks in 1950–1951 and it is estimated that the number of cases was in the hundreds (Goldblum et al., 1954); none of the cases was fatal and there were apparently many subclinical cases. Israel is an important path for migrating birds to and from Africa and to Europe and the virus may have been introduced in this manner.

The known distribution of WNV is shown in Figure 4.2following map.

The global distribution (dark shading) of West Nile and Kunjin viruses.


The first report of WNV in Europe was the detection of the virus in 1958, in two Albanians found to have specific WNV antibodies (Brdos et al., 1959). The virus remains endemic in the country (Eltari et al., 1993).

Countries in Europe in which West Nile virus endemic activity has been detected

The subsequent spread of WNV through Europe is reflected in Table which records the presence of WNV as indicated by the occurrence of human cases or isolations or positive serology in humans, animals, birds or arthropods. The following section reviews the literature reporting on the presence and incidence of WNV by country in Europe.


Serological surveys reported in the 1960s and 70s indicated the presence of WNV in 12 dogs (33.3%), 17 pigs (6.9%), 25 cattle (26.7%) and 21 of 61 hedgehogs (Erinaceus europaeus) tested (Sixl et al., 1973). Antibodies to WNV were found in farmers in Eastern Austria (Sixl et al., 1976); 385 horses and 102 free-living birds found dead were all negative and WNV was not considered, at the time, a significant pathogen in Austria (Weissenbock et al., 2003a).


In 1985–1994 (see Table ) four strains of WNV were isolated; one from birds, two from Aedes mosquitoes and one from a febrile patient. Another isolation was made from Anopheles mosquitoes in 1999. Specific WNV antibodies in human blood sera were identified in 1.7% of the Belarusian population. In the Gomel and Brest regions the percentage of seropositive individuals was 5.8 and 15.4, respectively. Antibodies were found in 0.6–5.8% of cattle, in 2.9–6.8% of wild small mammals and in 6.5–16.7% of birds. Sixteen cases were confirmed among patients with a febrile aetiology (Samoilova et al., 2003).


In 1978 serum samples from 233 cattle on 22 farms in Bulgaria were examined. Fourteen cattle were positive for WNV antibodies (Karadzhov et al., 1982). Little other information is available on WNV in Bulgaria; a survey of mosquitoes reported in 1991 (Kamarinchev et al., 1991) found WNV in several species of Aedes and Culex.

Czech Republic

The first reports of the presence of WNV were made in 1976 (see Table ) (Prazniakova et al., 1976). Serological surveys in the country have shown that the virus is common in both migratory and non-migratory species of birds including domestic fowl. The first isolation of WNV in the Czech Republic was reported by Hubalek et al. (1998); 11334 mosquitoes from south Moravia were examined in 197 pools. Aedes vexans, Ae. cinereus and Culex pipiens were found positive.

In July 1997 heavy flooding occurred along the Morava river; populations of Aedes mosquitoes rapidly increased. During the surveillance, 11 334 mosquitoes were examined and WNV isolates were made from Aedes vexans and Culex pipiens. West Nile virus antibodies were detected in 13 (2.1%) of 619 persons seeking treatment at hospitals and clinics in the Brelav area and two children had clinical symptoms, the first recorded cases of WNV in central Europe (Hubalek et al., 1999).

Hubalek (2000) characterized WNV in Europe as follows: ‘European epidemics . . . reveal some general features. They usually burst out with full strength in the first year, but few cases are observed in the consecutive 1 to 2 (exceptionally 3) years, whereas smaller epidemics or clusters of cases only last for one season. The outbreaks are associated with high populations of mosquitoes (especially Culex spp.) caused by flooding and subsequent dry and warm weather, or formation of suitable larval breeding habitats. Urban WNF outbreaks associated with Culex pipiens biotype molestus are dangerous. Natural (exoanthropic, sylvatic) foci of WNV characterized by the wild bird-ornithophilic mosquito cycle probably occur in many wetlands of climatically warm and some temperate parts of Europe; these foci remain silent but could activate under circumstances supporting an enhanced virus circulation due to appropriate abiotic (weather) and biotic (increased populations of vector mosquitoes and susceptible avian hosts) factors. It is very probable that WNV strains are transported between sub-Saharan Africa and Europe by migratory birds’.


West Nile virus was first reported in the Carmargue region of southern France in 1962–1965 and had been apparently introduced in 1962. There was a high mortality rate among horses in the area with some 50 dying during this period, and 13 human cases. West Nile virus was isolated from two mild human cases in 1964. There was an epidemic outbreak in 1962 during which severe cases of the disease were observed; an epidemic occurred again in 1963 at a lower incidence. In 1964 and 1965, only a few mild cases were seen in the Camargue (Panthier et al., 1968). The horse is the principal victim of WNV infection in the French Mediterranean littoral; in 1962–1965 there were 500 clinical cases and 50 equine deaths. Human infection is usually benign. The vector is Culex modestus. Infection in the horse ranges from unapparent infection to clinical symptoms. Antibodies to WNV were frequent in man in an area to the west and north of the Camargue and were also often found in horses, wild rabbits and hares but not in birds or small rodents (Joubert, 1975).

In September 2000, WNV again appeared in the south of France when 47 horses in the Herault region, close to the Camargue, developed symptoms of WNV encephalitis. There were 12 equine deaths but no human cases (Zientara, 2000). Equine cases were reported in the Department of Gard (16 horses) and the Department of Bouches du Rhone (3 horses). In total there were 76 clinical cases and 21 deaths. Seroconversions were detected in two sentinel birds in October 2001 in a mallard and in August 2002 in a chicken indicating a low circulation of WNV in the Camargue region. Cx. pipiens was considered the main vector.

The most recent case of WNV in France occurred in October 2003, in a man in the department of the Var; his wife also tested positive and there was a report of WNV infection in a horse some 20 km from the human cases. Two suspected equine cases were notified in the Var, in mid-September. The occurrence of 2 human cases (one confirmed and one probable) and 3 equine cases (one confirmed, 2 probable), in the same area in a 5-week period, suggests that infection was contracted in the Var located more than 100 km east from the Camargue. A total of 3 encephalitis and 4 mild illness cases were identified in humans, all living or having stayed in the vicinity of Fréjus city. Four equine cases were identified within 25 km from the human cases (Del Giudice et al., 2005).


No autochthonous human cases of WNV have been reported from Germany. However, Malkinson & Banet (2002) considered that the findings of anti-WNV antibodies in a population of storks maintained in northern Germany could be evidence for local infection. They pointed out that the unique susceptibility of young domestic geese in Israel in 1997–2000 to WNV and the isolation of similar strains from migrating White storks in Israel and Egypt suggest that the recent isolates are more pathogenic for certain avian species and that migrating birds play a crucial role in geographical spread of the virus. There have been no reports of isolations of WNV from mosquitoes in Germany or other reports of seropositive birds.


Lundstrom (1999) noted that in serological surveys, antibody prevalence to WNV was more prevalent in Greece than that to tick-borne encephalitis (TBE); Lundstrom also cites the presence of WNV in human serum collected by Pavlatos & Smith (1964) and again in 1972 (Papapanagiotuo et al. 1974). In a survey of animals reported from Greece in 1980 (Koptopoulos & Papadopoulos, 1980), antibodies to WNV were found in 8.8% of sheep, 8.7% of goats, 3.9% of cattle, 20.4% of horses, 1.4% of pigs, 24.5% of birds, 29% of humans, in 1 of 2 hares and in 1 of 26 rabbits.


The earliest report of the presence of WNV in Hungary was the isolation of the virus from small mammals in the course of surveys for TBE (Molnar et al., 1976). In another survey (Molnar, 1982) reported the presence of antibodies to WNV in ticks and mosquitoes in the country.


West Nile virus was first reported in Italy in 1966 when three clinical cases were described in children (Gelli Peralta, 1966) and surveys showed antibodies to WNV in small mammals of various regions.

The first equine outbreaks occurred in 1998 in 14 horses in Tuscany. Eight animals recovered without important consequences. West Nile virus was serolo- gically detected in all 14 horses and was isolated from an affected horse (Cantile et al., 2000). The outbreak involved race horses and racehorse breeding stock of high economic value (Autorino et al. 2002). No human cases were reported.

In 1998, virus isolated from a horse in Tuscany with encephalitis was sequenced. The strain appeared to share 99.2% nucleotide identity with a Senegalese strain isolated in 1993 from a mosquito (Culex neavei), indicating a link with viruses isolated in France (1965), Algeria (1968) and Morocco (1996), and suggests the hypothesis of an introduction of WNV by migratory birds crossing the Mediterranean Sea.


In 1973–1974, WNV was isolated from ticks in what was then Soviet Moldavia (Chumakov et al., 1974). No human cases of WNV have been reported from the country.


Sparrows from central Poland were examined by Juricovaet al. (1998) between 1995 and 1996 and antibodies to WNV were detected in 12.1% of the tree sparrows, Passer montanus. As these were non-migratory birds, the virus can be considered as endemic in Poland despite the absence of any reports of human cases.


In 1972, Filipe described the first finding of an arbovirus in mosquitoes in Portugal; it was identified as WNV, or a virus antigenically closely related, and was isolated from a female Anopheles maculipennis in Beja, in the south of the country in 1969. The site of collection was to the north of the farms where an outbreak of WN encephalitis had occurred in 1962–1965. There have been no reports of human WNV cases or of antibodies in humans.

In 1967, Filipe collected sera from cattle and sheep in south Portugal; antibodies were detected to WNV. Filipe & Pinto (1969) described a survey of cattle and sheep in the south for antibodies to WNV and TBE; of the bovine serum, 16% had antibodies to WNV and also reacted to TBE as an overlap reaction. Several cases ofequine encephalitis with 10 or 12 deaths had occurred in horses at a farm near Aljustrel in southern Portugal in 1962–1965; antibodies against WNV were found in animals on nearby farms. Tests in 1970 of 24 horses that had survived the disease in the 1962–65 epizootic revealed antibodies against WNV in 7 of them (Filipe et al., 1973).


In 1975, Draganescu et al. reported antibodies to several flaviviruses in humans and domestic animals in a biotope with a high frequency of migratory birds. There were human antibodies in a proportion of 11.8% to TBE and 25.5% to WNV; in domestic animals, WNV antibodies were detected in 4.9% of the sheep, 4.1% of the cattle and 12% of the goats tested. In 1977, Draganescu et al. described an outbreak of a febrile disease affecting 14 of 41 crew members of a ship that passed from Romania through the Suez Canal and the Red Sea on its way to Japan. Serological studies of the crew showed WNV antibodies in 25 of the 35 crew members checked. One patient died. The illness in other patients was mostly benign. The crewmen were probably infected in Romania before departure of the vessel.

High titres of antibodies to WNV were detected in 66 sera from 133 stray dogs in Romania (Rosiu et al., 1980). Antipa et al. (1984) took sera from 8 species of migratory birds; 22 serum samples gave positive reactions (titres: 1/20 – 1/80) to WNV and Ntaya viruses. Seroprevalence data suggest that WNV activity in southern Romania dates to the 1960s or earlier (Campbell et al., 2001).

In mid-July 1996, a clustering of meningoencephalitis cases was noted in Bucharest. Several hundred cases were reported in August. By the first week of September, antibodies to WNV had been demonstrated in several patients. The epidemic started at the end of July, peaked in the first week of September, and the last confirmed patient fell ill at the end of September. There were reports of 683 suspected cases; 527 met a clinical case definition of aseptic meningitis or encephalitis. By October, serological testing had been completed on 200 of the 527 suspected cases, yielding 168 laboratory-confirmed cases. Nine confirmed cases were fatal, a case fatality rate of 5.4%, all in people aged 60 years or older. The age-specific incidence in persons above 70 years was more than six times the incidence among children and young adults. It is likely that some of the 31 fatal unconfirmed cases represented true WNV cases. Disease incidence was highest in an agricultural area surrounding Bucharest. The epidemic involved an extensive area of southern and eastern Romania. A serosurvey of 75 blood samples demonstrated IgG antibodies to WNV in 4.1% of blood samples. Extra- polated to the city as a whole, it was estimated that between 90 000 and 100 000 people were infected. Culex pipiens is the dominant mosquito in Bucharest and was the most likely vector in 1996 (WHO, 1996). This epidemic was the largest outbreak of WNV reported in Europe and was characterized by a high virulence of the WNV strains involved.

The risk factors for WNV during the epidemic were analysed by Han et al. (1999). There was widespread subclinical infection during the outbreak. The risk factors for acquiring infection and for developing clinical meningoencephalitis after infection were mosquitoes in the home, reported by 37 of 38 (97%) asymptomatically seropositive persons compared with 36 of 50 (72%) seronegative controls. Among apartment dwellers, flooded basements were a risk factor (reported by 15 of 24 (63%) seropositive persons vs. 11 of 37 (30%) seronegative controls. Meningoencephalitis was associated with spending more time outdoors.

Surveillance after the 1996 epidemic showed that sporadic human cases continued to occur in Bucharest and the lower Danube delta in 1997 and in Bucharest in 1998, giving evidence of ongoing virus transmission in southeastern Romania.

Ceianu et al. (2001) reviewed WNV surveillance in Romania from 1997 to 2000. It was noted that the virus was still circulating in both human and avian cycles – surveillance found 39 clinical human WNV cases during 1997–2000. Retrospective sampling of domestic fowl in the vicinity of patient residences during 1997– 2000 demonstrated seroprevalence rates of 7.8–29%. Limited wild bird surveillance showed seroprevalence rates of 5–8%.

Apparently WNV persists locally in poorly understood transmission cycles and the virus remains a serious threat to public health in Romania; the implementation of an effective mosquito control is imperative.


West Nile virus has been isolated in Russia from species of ticks, mosquitoes and birds in many areas of the country. Seventeen virus strains were isolated from the tick Ornithodoros capensis collected in 1970 in the nesting grounds of herring gulls (Larus argentatus) in the Baku Archipelago, Azerbaijan. One strain was identical to WNV (Gromashevsky et al., 1973). West Nile virus was isolated from Ixodes ricinus in what was then Soviet Moldavia in 1973–1974. A single isolate with both Crimean–Congo haemorrhagic fever CCHF and WNV was obtained from Dermacentor marginatus though no human cases were reported in the areas where these viruses were isolated (Chumakov et al., 1974).

In a study in what is now Turkmenistan, Berdyev et al. (1975) found antibodies to WNV in 8 of 116 human serum samples, and 9 of 37 serum samples from wild animals. Antibodies were also detected in 6 out of 88 camel samples, 2 out of 3 horse samples, 30 out of 338 sheep samples and 189 out of 534 cattle samples.

In the Volgograd and Krasnodar regions, WNV antibodies were found in 50 out of 64 patients examined. The large number of reported cases suggested that an epidemic caused by the virus occurred in these regions in the summer of 1999 involving as many as 1000 cases and dozens of deaths (L’vov et al., 2000a). Two strains of WNV were isolated from the brain of a dead subject and from a patient during the 1999 outbreak. These strains reacted with convalescent sera proving their aetiological role in this outbreak (L’vov et al., 2000b). From 25 July to 1 October 1999, 826 patients were admitted to Volgograd Region hospitals with acute aseptic meningoencephalitis, meningitis or fever consistent with arboviral infection. Of 84 cases of meningoencephalitis, 40 were fatal. The authors believed that the unusual pathogenic characteristics may have been due to the extension of new pathogenic WNV strain(s) or to the peculiarities of the human host response (Platonov et al., 2001).

In 1963–1993, strains of WNV were isolated from ticks, birds andmosquitoes in southern European Russia and western Siberia and WNV antibody was found in 0.4–8% of healthy adult blood donors. Sporadic human clinical cases were observed in the Volga River delta. In spite of these reports, WNV infection was not considered by the health authorities as a potentially emerging infection, and the large WNV outbreak in southern Russia, starting in late July 1999, was not recognized in a timely fashion. First evidence suggesting WNV circulation was obtained by IgM-capture enzyme-linked immunosorbent assay (ELISA) in September and two weeks later, WNV disease was confirmed in all 14 non-survivors from whom brain tissue samples were available. Moreover, 35 of 56 patients who contracted aseptic meningitis in 1998 had a high titre of WNV antibody, indicating that WNV infection may have been introduced into the Volgograd region before 1999. The Volgograd isolate had the greatest homology (99.6%) with the WN-Romania-1996 mosquito strain. Specimens from a patient in the 2000 outbreak of WNV in Israel indicated a closer relationship of this isolate to 1996 Romanian and 1999 Russian strains than to 1998–99 Israeli or 1999 New York isolates (Briese et al., 2002). The possible role of migratory birds in this pattern must be considered.

Isolations of WNV from migratory and non-migratory birds was indeed made by L’vov et al. (2002a) in the Volga region. Four strains were isolated from birds and their ticks in the Volga delta. The strains were isolated from the great cormorant (Phalacrocorax carbo), the crow (Corvus corone) and Hyalomma marginatum nymphs.

The emerging situation in Russia is probably the result of natural and social factors and may also be due to the introduction of more virulent strains or by evolution of the virus. Whatever the source, the increased virulence of WNV in the recent outbreaks in Russia is of serious public health concern.


In 1972, 2043 mosquitoes of 10 species were collected while biting man and were tested in 129 pools. A strain of virus identified as WNV was isolated from a pool of Aedes cantans (Labuda et al., 1974). A serological survey of birds found a single mallard duck (Anas platyrhynchos) positive for WNV (Emek et al., 1975). In an additional survey, tick-borne encephalitis and WN viruses were isolated from the blood, brain and liver of migrating birds (Emek et al., 1977).

Juricova (1988) investigated sera from 62 Passeriformes birds of 14 species, caught during the autumn migration of 1987 in the Krkonose mountains in Slovakia; 6.4% of the birds were positive for WNV.


West Nile virus activity was detected in Spain between the 1960s and the 1980s in the regions of Catalunya, Andalucia, Valencia and Galicia (Lozano & Filipe, 1998).

A survey in the northern provinces of La Coruna, Orense, Pontevedra, Leon and Asturias obtained sera from 701 persons. Tests confirmed that there had been earlier infection with WNV (Gonzalez & Filipe, 1977). The sera of 386 small mammals (rodents, insectivores, small carnivores and bats (Chiroptera)) trapped in 1978 and 1979 were tested for antibody against 10 arboviruses. Positive reactions were found against flaviviruses, among them 3.1% to WNV.

Lozano & Filipe (1998) studied the prevalence of WNV and other viruses among the human population of the Ebro Delta; 1037 samples of serum were taken in 10 towns and analysed for the presence of WNV antibodies and 12 other arboviruses. Antibody titres revealed a significant percentage of samples with high titres to WNV and other antigens. In three localities located in the Delta, the prevalence of Flaviviridae antibodies was as high as 30%, with residual levels of WNV-related IgM in some serum samples; these results suggest that WNV is moving throughout the human population, periodically giving rise to epidemic outbreaks. Bearing in mind the high percentage of neurological complications in the most recent outbreaks of WNV infections recorded in the Mediterranean basin it was felt that WNV plays a role in the factors contributing to viral meningitis and encephalitis within the population of risk areas within Spain.


While no human cases of WNV have been reported from the UK, the Health Protection Agency has an annual enhanced surveillance programme for possible human cases. The scheme operates during the summer, when there is WNV activity in other countries and involves looking for WNV in blood and cerebrospinal fluid samples, taken from patients with encephalitis or viral meningitis with no known cause.

Buckley et al. (2003) reported the presence of virus-specific neutralizing antibodies to WNV, Usutu virus (USUV) and Sindbis virus (SINV) in the sera of resident and migrant birds in the UK, implying that each of these viruses is being introduced to UK birds, possibly by mosquitoes. This was supported by nucleotide sequencing that identified three slightly different sequences of WNV RNA in tissues of magpies (Pica pica) and a blackbird (Turdus merula). The detection of specific neutralizing antibodies to WNV in birds provides a plausible explanation for the lack of evidence of a decrease in the bird population in the UK compared with North America. Many birds migrate annually from regions in Africa where WNV, USUV and SINV co-circulate and are actively transmitted between birds and mosquitoes. It is, therefore, possible that they are carried by birds to the UK and transmitted via indigenous mosquitoes to non-migratory birds and to other wildlife species. A relatively high proportion of resident birds were positive, implying efficient transmission from the migrant bird population. The authors concluded that there is no evidence that British citizens suffer from febrile illness, fatal encephalitis or polyarthritis arising from the bite of mosquitoes infected with WNV, USUV or SINV. They also observed that on balance, it seems unlikely that these viruses present significant health problems to humans, birds or horses in the UK, since the likely risk of exposure to WNV-, USUV- or SINV-infected mosquitoes for humans living in urban or peri-urban areas of the country at the present time should be reasonably low. Nevertheless, as the impact of climate change takes effect and as more people spend increasing periods of time in the countryside, where mosquitoes are likely to occur in the highest densities, the risk of human exposure to encephalitic infection by WNV will almost certainly increase.


The first isolation of WNV in Ukraine was made from a rook (Corvus frugilegus) caught in May 1980, in the Black Sea area (Vinograd et al., 1982).

Active foci of TBE, WNV, California serologic group (CSG) and Batai viruses have been identified as a result of investigations in the forest-steppe zone of Ukraine. Of the viruses identified, WNV was the leading arboviral infection in the forest-steppe zone with 53.1% of the infections (Lozyns’kyi & Vynohrad, 1998).


There is little information available on the presence of WNV in Serbia; Vesenjak Hirjan (1991) mentions that antibodies to WNV have been found in 8% of 397 people in the west of Serbia, 1% of 479 people in the east of Serbia, 1% of 826 people in Montenegro and 1% of 629 people in Kosovo. There have been no reports of human clinical cases.

The vectors of West Nile virus in Europe

Table lists the countries in which the vectorial status of an arthropod has been determined or in which isolations of virus have been made from an arthropod.

Arthropod species confirmed as vectors or from which West Nile virus was isolated

In countries in which there have been epidemic outbreaks of the disease in man or animals, it can be assumed that the vectors are mosquitoes. Birds may be infected by mosquitoes or ticks but it seems quite unlikely that ticks are involved as vectors in large outbreaks.

The reservoir hosts of West Nile virus in Europe

West Nile virus has been isolated from many animals in Europe but most, including horses, cattle, camels, sheep, pigs, boars, hares, dogs and cats, are dead-end hosts and not reservoir hosts of the infection. It has been found in humans, birds and other vertebrates in Africa, eastern and western Europe, western Asia and the Middle East, but until 1999 had not previously been documented in the Americas.

It is likely that WNV was originally introduced into Europe by migratory birds coming from Africa. Malkinson & Banet (2002) reviewed the role of wild birds in the epidemiology of WNV and the following observation is taken from their review. Surveys on wild birds conducted during the last two decades in Europe, notably Poland, the Czech Republic and the UK have revealed endemic foci of infection. Some species of seropositive birds were non-migrators while others were hatchlings of migrating species. Persistently infected avian reservoir hosts are potential sources of viruses for mosquitoes that multiply in the temperate European zone in hot, wet summers. In the past, evidence for geographical circulation of WNV was based on antigenic analysis of strains from different countries while more recent epidemiological studies have relied on analysis of nucleotide sequences of the envelope gene. With the reappearance of epidemic WNV in European countries, interest has been focused again on the African origin of the causal agent carried by migrating wild birds. In some epidemics, isolates were made from human cases or mosquitoes and only serologic evidence for infection was available from domestic and wild bird populations. It remains to be determined whether the European endemic foci of WNV are in themselves sources of infection for other birds that migrate across Europe and do not necessarily reach sub-Saharan Africa.

As has been described above, specific neutralizing antibodies identified by nucleotide sequencing show three slightly different sequences of WNV RNA in tissues of magpies and a blackbird in the UK (Buckley et al., 2003).

Juricova (1988) in the then Czech Republic, examined sera from 62 passeriform birds of 14 species, during the autumn migration of 1987 in the Krkonose mountains; 6.4% were positive for antibodies to WNV.

Much remains to be determined about the role of migratory birds in the introduction of WNV into the countries of Europe. Non-migratory birds are frequently found infected, but unlike North America do not appear to suffer from massive mortality.

Conclusions on the public health importance of West Nile virus in Europe

Although the presence of WNV in Europe has been recorded since at least the early 1960s, the disease is now emerging more frequently in outbreaks with greater virulence. L’vov et al. (2004) believes that the emerging WNV situation in Russia has, in part, resulted from the introduction of more virulent strains or by evolution of the virus. In the 1990s and up to the present, encephalitis has been a more prominent feature of WNV infection in Europe, the Middle East and the USA, suggesting the emergence of more neurovirulent strains (Johnson & Irani, 2002). Since 1996, epizootics involving hundreds of humans, horses and thousands of wild and domestic bird cases of encephalitis and mortality have been reported in Europe, North Africa, the Middle East, Russia and the USA. The biological and molecular markers of virus virulence should be characterized to assess whether novel strains with increased virulence are responsible for the proliferating outbreaks. In an outbreak in Volgograd, Russia in 1999, 40 of 84 (48%) patients with encephalitis died (Gelfand, 2003). Mortality appears to have increased as well among infected animals and birds. Many recent outbreaks of WNV show increasing virulence to the elderly; overall case fatality rates in recent epidemics of WNV ranged from 4% to 14% with higher rates in elderly patients. In an outbreak in Israel in 2000, the overall mortality rate in patients aged 70 years or older was 29%, and 32 of 33 deaths occurred in patients older than 68 years.

West Nile virus in Europe is of growing public health importance. The virus appears to be spreading to geographic areas in which human infections have not previously been reported. Effective surveillance programmes must be considered an imperative. In the absence of an effective vaccine, control of the transmission of WNV must depend on effective control of the mosquito vectors. The extent to which tick vectors are of epidemiological importance remains uncertain.

Batai virus (Calovo virus)

Batai virus, also identified as Calovo virus, a bunyavirus, was first isolated in Slovakia from Anopheles maculipennis in 1960. It has been isolated in Norway, Sweden, Finland and northern and southern Russia, the Ukraine, the Czech and Slovak Republics, Austria, Germany, Hungary, Portugal and Romania. The principal western European vectors appear to be mainly An. maculipennis and An. claviger; it has been isolated from Aedes communis and other mosquito species in Sweden (Francy et al., 1989).

Lundstrom (1994) considered that Batai or Calovo viruses are not associated with human disease in Western Europe and that their potential for human disease was low (Lundstrom, 1999). Calovo virus has a very low prevalence in humans in the Czech Republic due to the marked zoophilia of its vectors (Danielova, 1990). Surveys in the Czech Republic showed a high prevalence of Batai/Calovo virus in mammals ranging as high as 23% among deer, boars and hares (Hubalek et al., 1993). The virus is present at a low level in house sparrows (Passer domesticus) in Poland (Juricova et al., 1998) and at a higher level (10.9%) in 608 sheep in Slovakia (Juricova et al., 1986). The virus has also been identified both in otherwise healthy human subjects and domestic animals in Croatia (Vesenjak Hirjan et al., 1989).

Shcherbakova et al. (1997) did not find Batai virus in a survey of healthy residents of the Saratov region of Russia, but 61.2% of 80 bovine samples had antibodies. While Batai/Calovo virus is widespread in Europe, it does not appear, at present, to be of public health importance and no clinical disease associated with it has been reported.

Ockelbo virus

Ockelbo virus is a Sindbis-related virus. First described in Sweden in the 1960s, it is probably also the causative agent of ‘Pogosta disease’ in Finland and Karelian fever in western Russia (Francy et al., 1989). The many strains of the Sindbis group are widely distributed throughout Europe, Asia and Africa and are closely related to Ockelbo and other viruses in northern Europe. The virus is maintained in nature in a mosquito–bird transmission cycle and is transmitted in endemic areas by migratory birds and ornithophilic Culex species and Culiseta morsitans as vectors (Lundstrom et al., 1992).

The identification of Ockelbo virus as a Sindbis virus was confirmed when an alphavirus isolated from Culiseta mosquitoes was associated with Ockelbo disease, an exanthema arthralgia syndrome occurring in Sweden. The isolate was made from mosquitoes collected in an area of central Sweden with a considerable Ockelbo morbidity and was indistinguishable from Sindbis virus. Patients with Ockelbo disease developed neutralizing antibodies to the virus in their convalescent sera, suggesting that it is the aetiologic agent of the disease (Niklasson et al., 1984).

In the 1980s Ockelbo disease caused outbreaks involving hundreds of cases in parts of northern Europe. Russia reported 200 and Finland 300 laboratory-confirmed cases in 1981. An outbreak occurred again in Finland in 1995 when 1400 laboratory confirmed cases were reported. In Sweden, an annual average of 31 laboratory confirmed cases were diagnosed during the period 1981–1988 although it is believed that as many as 600–1200 cases a year occur (Lundstrom et al., 1991). In 1982 an outbreak of Ockelbo disease with rash, arthralgia and moderate fever reactions occurred in Sweden. A virus, designated Edsbyn 5/82, isolated from mosquitoes and closely related to Sindbis virus, was the probable aetiologic agent. Most cases occurred in central Sweden. The frequency of antibody in healthy individuals (blood donors) within the endemic area was 2–3% and in foci with a high incidence, reached 8%. Arthralgia is the dominating feature of Ockelbo disease and may immobilize patients for a week or up to a month or more (Niklasson et al., 1988).

Ockelbo virus is also identical to Karelian fever, an infection reported from western Russia. L’vov et al. (1988) examined the causative agents of Ockelbo disease in Sweden, Pogosta disease in Finland and Karelian fever in Russia; the results indicated that Ockelbo and Karelian fever viruses are essentially identical and that Ockelbo disease, Pogosta disease and Karelian fever are synonyms for the same disease.

The virus has been isolated from many species of mosquitoes including Aedes cantans, Ae. cinereus, Ae. communis, Ae. excrucians, Ae. intrudens, Culex pipiens, Culiseta morsitans and Culex torrentium, species which feed upon Passeriformes bird reservoir hosts and man.

In Sweden, the incidence of Ockelbo disease and the prevalence of Ockelbo virus antibodies were investigated in 100–250 human sera from out patient volunteers in each of 21 towns in 11 counties. The disease was found to occur throughout most of Sweden but with higher incidence and antibody prevalence in the central part of the country. It generally affects middle-aged men and women and is uncommon in people younger than 20 years of age. It occurs each year between the third week of July and the first week of October, with a peak during the second half of August. During the 8 years studied (1981–1988), an average of 31 Ockelbo patients per year were diagnosed. Antibody prevalence rates were highest in the oldest age groups. It is suggested that many cases are asymptomatic and/or unreported (Lundstrom et al. 1991).

Sera from 324 birds collected in an Ockelbo endemic area in central Sweden were examined for specific antibodies to Ockelbo virus. Birds examined belonged to the orders Anseriformes, Galliformes and Passeriformes. Ockelbo virus antibodies were detected in 8% of the specimens, including species from each of the three orders tested. Specific antibodies found in caged birds and in 6- to 10-week-old birds suggested local transmission. The highest prevalence (27%, 14/51) was observed in the Passeriformes in which 5 of 9 species tested contained antibodies. The high antibody prevalence in Passeriformes and the very large populations of this group in relation to other avian groups in Sweden gives them a high potential as amplification hosts for Ockelbo virus (Lundstrom et al., 1992).

In northern Finland, a disease given the name of Pogosta disease and characterized by arthritis, rash and fever was described in 1974. As indicated above, this disease was later found to be closely related if not identical to Ockelbo disease. Some 93% of the patients had joint inflammation, 40% with polyarthritis. Rash was seen in 88% of the patients, and 23% had fever. A follow-up study found that 50% of the patients suffered from chronic muscle and joint pain at least 2.5 years after the initial symptoms. Outbreaks of Pogosta disease in Northern Karelia seem to occur every 7 years. A study was made of antibodies in 2250 serum samples in Finland; 400 of the sera were from healthy blood donors and 1850 samples from patients from different parts of Finland suspected to have a viral infection. Antibody prevalence was almost equally distributed throughout the country, but highest in western Finland (17%). The authors concluded that (1) Pogosta disease is more common than previously thought; (2) it is not restricted to eastern Finland but is spread throughout Finland; and (3) it is also common in children. In Finland the yearly incidence of Sindbis virus is 2.7/100 000 (18 in the most endemic area of northern Karelia). The annual average was 136 (varying from 1 to 1282) with epidemics occurring in August–September with a 7-year interval (Brummer Korvenkontio et al., 2002). As with other virus infections of the group, the main symptom in humans is a febrile arthritis-like disease (Toivanen et al., 2002).

While the number of cases of Ockelbo virus in Sweden has recently declined, the magnitude of the outbreaks in the 1980s demonstrates that there is a considerable potential for further outbreaks. As has been noted in Finland, what has been termed Pogosta disease in that country is much more widely spread than earlier believed (Toivanen et al. 2002) and this may also be the case for Ockelbo virus.

Inkoo virus

Inkoo virus is a member of the California serogroup of the bunyaviruses, and has been reported from Estonia, Finland, Norway, Russia and Sweden. Inkoo virus is transmitted by Aedes communis and Ae. punctor in Scandinavia; it has been isolated from Ae. communis in Sweden (Francy et al., 1989). In Russia the virus has been isolated from Ae. hexodontus and Ae. punctor (Mitchell et al., 1993). The virus is quite common in Finland with its prevalence increasing towards the north where its prevalence rises to 69% of the population (Brummer Korvenkontio & Saikku, 1975). Antibody prevalence is also high in parts of Sweden (Niklasson & Vene, 1996) but in neither country is there any evidence of human disease caused by this virus. However, in Russia, Demikhov (1995) noted that patients with antibodies to Inkoo virus had chronic neurological disease; 16.7% of convalescents after the febrile form of the disease and 30.7% of convalescents after the neuroinfection form had for 1–2.5 years (the follow-up period) after the initial disease developed neurological disturbances and neurological symptoms. Demikhov & Chaitsev (1995) described severe illness ascribed to infection with the virus but there was no mortality. While the true incidence of Inkoo virus is not known, Inkoo and, as will be seen below, Tahyna virus are the most common California group viruses in Eurasia and must remain under close surveillance.

Tahyna virus

In 1958 a virus transmitted by a mosquito was isolated in the Slovakian village of Tahyna (Bardos & Danielova, 1959). The virus was unknown in Europe and was found to belong to the California group and eventually found to occur in most European countries. It was considered possible that young hares (Lepus species) are the hosts for this virus, and that it multiplies in them. Foals and suckling pigs are also hosts and possibly also increase the virus. In human patients, infection with the Tahyna virus appears with influenza-like symptoms. In some cases, meningoencephalitis and atypical pneumonia were observed but no fatal cases have been reported (Bardos, 1976). There are no significant clinical differences between Tahyna and Inkoo viruses. The symptoms seen in 41 patients were fever in 25 patients, neuroinfection in 13, and in 3 subjects the infection was unapparent. Of the patients with the neuroinfectious form of the disease, 3 presented with aseptic meningitis, 2 with meningoencephalitis and 5 with encephalitis.

Butenko et al. (1995) examined 221 healthy persons and 520 patients suffering from acute fevers and neurological infections in four districts of the Ryazan region of Russia. Of the healthy subjects, 40.7% reacted positively with Tahyna and Inkoo viruses, indicating many contacts of the population with these viruses. The aetiological role of viruses of the California encephalitis complex was demonstrated in 9.8% of 520 patients suffering from acute fevers and neurological infections. The disease was frequently preceded by a visit to woodlands where the patients had been bitten by mosquitoes. The incubation period lasted 3–7 days and the morbidity was sporadic. In 1991, antibodies to Tahyna virus were found in 60% of the population of the Sverdlovsk region (Glinskikh et al., 1994).

Kolman et al. (1979) examined a human population from the southern Moravian region of Czechoslovakia for antibodies against Lednice, Sindbis, TBE, WNV, Tahyna and Calovo. No antibodies to Sindbis, WN and Calovo viruses were found but 17.8–42.0% of antibodies to Tahyna virus were detected in all age groups. The total infection rate was 26.0%. Serum samples from 475 men from different districts of the West Bohemian region were examined for the presence of antibodies against viruses of TBE, Tahyna and Tribec; antibodies against Tahyna were detected in 4.4% of the sera (Januska et al., 1990).

After the 1997 floods in the Czech Republic, serosurveys were carried out in the Breclav area. In sera of 619 inhabitants, antibodies to Tahyna virus were detected in 333 (53.8%) and to WNV in 13 (2.1%).

The vectors of Tahyna virus are mainly pasture-breeding Aedes species; most isolations of the virus have been made from Ae. vexans. The anthropophilic nature of this species accounts for the high antibody rates in humans in countries where the infection is endemic and there is wide distribution of the virus (Danielova, 1990). Table presents a listing of countries in which Tahyna virus has been isolated or in which antibodies have been detected.

Reports of Tahyna virus found in surveys in Europe

Countries Reported activity or outbreaks
∗ Birds, animals or arthropods only.
Albania 1958
Austria 1964–1977 1988
Belarus 1972–1973∗ 1977
Bulgaria 1960–1970 1978∗
Czech Republic 1978∗ 1980s∗



France 1962–65, 1975–1980



Germany 1990s∗
Greece 1970–1978 1980–1981
Hungary 1970s 1984
Italy 1966–1969 1981∗ 1998∗







Romania 1966–1970 1975




Russia 1962–1976 1977∗






Slovakia 1970–1973∗ 1984–1987    1998
Spain 1960s 1979∗



Ukraine 1980s 1998
Country Species
Azerbaijan Ornithodoros capensis
Belarus Aedes spp., Anopheles spp.
Bulgaria Ae. cantans.
Czech Republic Ae. cinereus, Ae. vexans, Culex pipiens, Ixodes ricinus
France Culex modestus, Cx. pipiens
Italy Cx. impudicus? Cx. pipiens?
Moldavia Dermacentor marginatus, Ixodes ricinus
Portugal Anopheles maculipennis
Slovakia Ae. cantans, I. ricinus
Romania Cx. pipiens, Cx. pipiens molestus
Russia Ae. vexans, Cx. modestus, Cx. molestus, Cx. univittatus, D. marginatus, Hyalomma marginatum, Ixodes lividus, I. ricinus
Ukraine An. maculipennis
Country Results – isolations or antibodies Reference
Austria Aedes caspius Pilaski & Mackenstein, 1989
Austria Aedes caspius, Aedes vexans Pilaski, 1987
Croatia humans Vesenjak Hirjan et al., 1989
Croatia bears Madic et al., 1993
Czech Rep. Aedes cinereus, Aedes vexans Danielova et al., 1976
Czech Rep. Aedes sticticus, Culex modestus Danielova & Holubova, 1977
Czech Rep. birds Hubalek et al., 1989
Czech Rep. Aedes spp., humans Danilov, 1990
Czech Rep. game animals-deer, boars Hubalek et al., 1993
Czech Rep. birds-cormorants Juricova et al., 1993
Czech Rep. birds-ducks Juricova & Hubalek, 1993
Czech Rep.

Aedes cinereus, Aedes vexans,


Hubalek et al., 1999
Czech Rep. birds-sparrows Juricova et al., 2000
France Aedes caspius, humans Joubert, 1975
Germany Aedes caspius Pilaski & Mackenstein, 1989
Germany domestic animals, humans Knuth et al., 1990
Hungary Aedes caspius Molnar, 1982
Italy small mammals Le Lay Rogues et al., 1983
Poland birds-sparrows Juricova et al., 1998
Portugal cattle and sheep Filipe & Pinto, 1969
Russia Anopheles hyrcanus L’vov, 1973
Russia humans Kolobukhina et al., 1989
Russia humans Butenko et al., 1990
Russia humans Glinskikh et al., 1994
Russia Aedes communis, Aedes excrucians L’vov et al., 1998
Romania Cx. pipiens Arcan et al., 1974
Romania cattle, sheep, goats, humans Draganescu & Girjabu, 1979
Slovakia humans, hares (?) Bardos, 1976
Serbia Aedes vexans Gligic & Adamovic, 1976
Slovakia Aedes vexans Danielova et al., 1978
Slovakia humans Kolman et al., 1979
Slovakia sheep Juricova et al., 1986
Slovakia Culiseta annulata larvae Bardos et al., 1978
Spain rodents Chastel et al., 1980

Usutu virus

In the summer of 2001, a massive die-off of birds occurred in Austria; it was first feared that this was due to WNV as a similar massive die-off had occurred in the USA. A virus was subsequently isolated from birds which exhibited 97% identity to Usutu virus (USUV), a mosquito-borne Flavivirus of the Japanese encephalitis virus group; USUV had never previously been observed outside of Africa nor had it been associated with fatal disease in animals or humans. It seems likely that the virus was brought to Europe by migrating birds from Africa. It was first isolated from bird-biting mosquitoes (Coquillettidia aurites) in South Africa in 1959 (Williams et al., 1964) and isolations have been made from birds, mosquitoes, from a Praomys rat, and one from a man with fever and rash. In Africa, the virus circulates between birds and mosquitoes with mammals being inadvertent hosts if bitten by infected mosquitoes. There are no reports of severe disease in man.

Usutu virus now appears to be established in central Europe, and may have considerable effects on avian populations; whether the virus has the potential to cause severe human disease is unknown (Weissenbock et al., 2002). In 2002 the virus continued to kill birds, predominantly blackbirds (Turdus merula); it is estimated 30% of the blackbirds around Vienna have died since spring 2001. High numbers of avian deaths were recorded within the city of Vienna and in surrounding districts of the federal state of Lower Austria, while single mortalities were noticed in the federal states of Styria and Burgenland. Laboratory-confirmed cases of USUV infection originated from the federal states of Vienna and Lower Austria only. Usutu virus has over-wintered and established a transmission cycle in Austria and seems to have become a resident pathogen of Austria with a tendency to spread to other geographic areas (Weissenbock et al., 2003b).

By 2004 the virus had spread across the entire east of the country and prob- ably as far as Slovakia and Hungary. While nuthatches, owls, sparrows, swallows, thrushes and tits were also dying, blackbirds (Turdus merula) have been by far the worst-hit species, accounting for 95% of the deaths.

Buckley et al. (2003) reported the presence of virus-specific neutralizing antibodies to WNV, Usutu virus and Sindbis virus in the sera of resident and migrant birds in the UK, implying that each of these viruses is being introduced to UK birds; however, no decrease has been seen in avian populations in the country. The appearance of an arbovirus not previously seen in Europe emphasizes the need for continual surveillance.

Dengue virus

Dengue was once endemic in the countries of southern Europe where Aedes aegypti was present. The occurrence in 1927–1928 of a massive epidemic of dengue with high mortality in Athens, Greece has already been described. Dengue is the most important arboviral human disease globally, but it has disappeared from Europe as an endemic disease. The disappearance of dengue transmission was mainly due to the virtually universal availability of piped water supplies in Europe and the disappearance of containers such as water jars and barrels which had been used for storing water for household use and which served as larval habitats for Ae. aegypti. Grist & Burgess (1994) pointed out that while the spread of Ae. aegypti in Europe is limited by its cold intolerance, this is not the case with Ae. albopictus; the reintroduction of dengue transmission must be considered as a possibility as Ae. albopictus, a species which has been invading Europe, is a vector of dengue in some parts of the world (Gratz, 2004). Aedes albopictus strains from Albania have readily transmitted dengue in the laboratory (Vazeille Falcoz et al., 1999). Dengue is often introduced into Europe by travellers from endemic countries; a viraemic traveller bitten by Ae. albopictus could be the source of renewed transmission in Europe (Ciufolini & Nicoletti, 1997), particularly in areas where the density of Ae. albopictus populations is high.

Each year, an estimated 3 million German residents spend time in dengue-endemic countries. Schwarz et al. (1996) studied 249 German tourists returning from tropical areas with a febrile infection. Acute infection with dengue was diagnosed in 26 (10.4%): most infections were acquired in Thailand (57.7%). In a study of 670 German aid workers who had spent 2 years in the tropics, 49 (7.3%) were positive for antibodies to dengue, none (1.3%) to chikungunya and 1 (0.1%) to Sindbis virus. The steady increase in case reports of imported dengue in Germany in early 2001 likely reflects a recently improved surveillance system. The further steep rise in German case reports, particularly during late 2001 and the first half of 2002, corresponds to a surge of local dengue reporting from many dengue-endemic areas and probably reflects a true increase in the number of imported cases. In the number of reports of travel-associated infectious diseases, dengue fever is second only to malaria (about 1000 cases per year, with a 15% drop in cases from 2001 to 2002) in Germany. The increase in cases from the fourth quarter of 2001 to the first quarter of 2002 is mainly due to cases imported from Brazil. During the first quarter of 2002, the state of Rio de Janeiro recorded an incidence that was 6.5 times higher than it had been in January through March of 2001. This state alone accounted for almost 50% of the total cases in Brazil during this period, including an urban epidemic in the city of Rio de Janeiro. The city draws large numbers of German tourists, especially during the festival of Carnival, which may well have contributed to the high number of cases acquired in Brazil in February and March 2002. The peak in cases imported to Germany in the second and third quarter of 2002 reflects the dengue season in Thailand and other parts of South East Asia. In Thailand, dengue transmission is associated with the rainy season, which varies regionally but in most areas of the country starts around April. In mid-April 2002, an out-of-season outbreak of dengue was reported at the island resort of Koh Phangan, which may explain the high incidence among German travellers in March and April (Frank et al., 2004).

Lopez Vélez et al. (1996) carried out a clinical study on 37 travellers returning to Spain from dengue-endemic areas. Anti-dengue antibodies were found in 24 of 37 patients. In 71.4% of the cases seen, dengue was acquired in Asia.

The European Network on Imported Infectious Disease Surveillance has noted that 45% of dengue cases among returning travellers were acquired by patients in South East Asia, 19% were imported from South and Central America, 16% from the Indian subcontinent, 12% from the Caribbean and 8% from Africa. This distribution reflects worldwide dengue activity, as well as the popularity of these countries as tourist destinations. Thailand alone was the place of acquisition for 134 cases (28%) of all travel-associated dengue infections. In 2002 there was a proportional rise in the number of infections acquired in South East Asia compared with 2001. Most patients were European-born travellers (94%), but immigrants born outside Europe and foreign visitors had a 4.3 times higher risk of developing dengue haemorrhagic fever compared with those born in Europe (Wichmann & Jelinek, 2003).

There are many records in the literature of cases of dengue which have been imported into Europe. The possible renewal of dengue transmission in Europe would depend on either Ae. aegypti populations being reEntity Error ːːestablished at high density, which appears unlikely, or the possibility that Ae. albopictus, a species that has recently been introduced into several European countries where it has become established, begins to transmit the virus.



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