Parasitology Research

, 105:313 | Cite as

Bluetongue disease in Germany (2007–2008): monitoring of entomological aspects

  • Heinz Mehlhorn
  • Volker Walldorf
  • Sven Klimpel
  • Günter Schaub
  • Ellen Kiel
  • René Focke
  • Gabriele Liebisch
  • Arndt Liebisch
  • Doreen Werner
  • Christian Bauer
  • Henning Clausen
  • Burkhard Bauer
  • Martin Geier
  • Thomas Hörbrand
  • Hans-Joachim Bätza
  • Franz J. Conraths
  • Bernd Hoffmann
  • Martin Beer
Original Paper

Abstract

In the summer of 2006, a bluetongue epidemic started in the border area of Belgium, The Netherlands, and Germany, spread within 2 years over large areas of Western and Central Europe, and caused substantial losses in farm ruminants. Especially sheep and cattle were severely affected, leading to a case–fatality ratio of nearly 40% in sheep (Conraths et al., Emerg Inf Dis 15(3):433–435, 2009). The German federal ministry of food, agriculture, and consumer protection (BMELV) established a countrywide monitoring on the occurrence of the vectors of this virus, i.e., midges (family Ceratopogonidae) of the genus Culicoides. The monitoring was done on 91 sites, most of which were localized in the 150-km restriction zone that existed in December 2006. A grid consisting of 45 × 45 km2 cells was formed that covered the monitoring area. As a rule, one trap was placed into each grid cell. The monitoring program started at the end of March 2007 and lasted until May 2008. It included the catching of midges by ultraviolet light traps—done each month from days 1 until 8, the selection of midges of the Culicoides obsoletus, Culicoides pulicaris group, and other Culicoides spp., the testing of midges for bluetongue virus (BTV) by polymerase chain reaction (PCR), and the daily registration of weather data at each trap site for the whole monitoring period. The following main results were obtained: (1) Members of the C. obsoletus group were most commonly found in the traps, reaching often 3/4 of the catches. The African and South European vector of BTV—the species Culicoides imicola—was never found. (2) Members of the C. obsoletus group were most frequently found infected with BTV besides a few cases in the C. pulicaris group and other species. (3) Members of the C. obsoletus group were also found in winter. Their numbers were reduced, however, and they were caught mostly close to stables. Therefore, a true midge-free period does not exist during the year in Germany. (4) The amounts of midges caught daily depended on the weather conditions. If it was cold and/or windy, the traps contained only a few specimens. Since the months from January to May 2008 were considerably colder (at all farms) than their correspondents in 2007, the growing of the population of midges started 2–3 months later in 2008 than in 2007. (5) The highest populations of midges occurred in both years (2007 and 2008) during the months September and October. This corresponded significantly to the finding of highest numbers of infected midges and to the number of diseased cattle and sheep during these 2 months. (6) It is noteworthy that in general, the first virus-positive midges of the species C. obsoletus were found about 1 1/2 months later than the first clinical cases had occurred or later than the first PCR-proven virus-positive sentinel animals had been documented. In 2007, the first BTV-positive cattle were detected in May in North Rhine-Westphalia, while the first positive Culicoides specimens were only found in August on the same farm. Evaluating these main results of the entomological monitoring and the fact that many wild ruminants have also been infected with BTV, it becomes evident that bluetongue disease has become endemic in Central Europe, and that only constant effort including vaccination and perhaps also insecticidal protection of cattle and sheep will keep the economical losses at a reasonable level. The following papers (1–10) in this journal will contribute more details obtained from this worldwide unique entomological monitoring: Bartsch et al. 2009; Bauer et al. 2009; Stephan et al. 2009; Clausen et al. 2009; Hörbrand and Geier 2009; Kiehl et al. 2009; Mehlhorn et al. 2009; Kiel et al. 2009; Vorsprach et al. 2009; Balczun et al. 2009.

Introduction

Bluetongue disease (BTD) was first described in 1876 in South Africa by an anonymous author in a veterinarian report (Anonymous 1876). It occurred in cattle and sheep and later became referred to as “fever” and “malarial catarrhal fever of sheep” by Hutcheon (1881, 1902), threatening all imports of ruminants from Europe, e.g., those of the “Bures”, who—immigrating from the Netherlands—introduced the name “bekziekte” for this peculiar disease. The Swiss scientist Theiler—famous for his studies on East Coast fever of cattle (theileriosis: Mehlhorn et al. 1992; Dobbelaere and McKeever 2002)—suggested in 1906, in letters sent to Robert Koch—the founder of modern microbiology—that this peculiar disease attacking imported ruminants might be the result of the action of a “virus”, similar to those described by Loeffler and Frosch (1897) in the foot-and-mouth disease. Therefore, bluetongue was also described for a long time as “pseudo-foot-and-mouth disease”. The recent name “bluetongue disease” refers to the appearance of symptoms in the late stage of lethal cases due to cyanosis (blue color of the tongue and of the mucous epithelia as signs of the lack of oxygen).

In August 2006, the disease was suddenly found in Central Europe and started from Belgium, Germany, and The Netherlands, and it is quick and constant in spreading (Mehlhorn et al. 2007, 2008a; Wilson and Mellor, 2008; Hoffmann et al. 2008; Meiswinkel et al. 2007; Saegerman et al. 2008; Toussaint et al. 2007; Conraths et al. 2007, 2009; Hoffmann et al. 2009; Darpel et al. 2007).

After a local, permanent screening of suspected vectors at two farms in Aachen (North Rhine-Westphalia) in the months August 2006 until January 2007 (Mehlhorn et al. 2007), the German federal ministry of food, agriculture, and consumer protection (BMELV) installed in the year 2007 a monitoring system on the abundance of midges and their role as vectors of the BTD. The monitoring program was designed according to a “Working document on enhancing bluetongue monitoring and surveillance in the EU” issued by the Directorate General for Health and Consumer Affairs to ensure harmonized monitoring approaches in the European Union. At that time in Western and Central Europe, only BTV serotype 8 was found, which had never before been found in Europe, while South Africa harbors approximately 20 out of a total of 24 known serotypes.

The 10 papers following this introducing overview in the present volume of the journal (Mehlhorn et al. 2009; Vorsprach et al. 2009; Balczun et al. 2009; Kiel et al. 2009; Kiehl et al. 2009; Bartsch et al. 2009; Clausen et al. 2009; Stephan et al. 2009; Bauer et al. 2009; Hörbrand and Geier 2009) describe the results obtained during this monitoring program, which ran from the end of March 2007 until the end of May 2008.

Methods and aims

Tasks of the project

The German monitoring project had the task to find answers to the following questions:
  1. 1.

    Has Culicoides imicola, the vector of the bluetongue virus (BTV) in South Africa and South Europe, arrived in Central Europe, and is it involved here in the transmission of BTV?

     
  2. 2.

    Are the midges of the Culicoides obsoletus group, which had been found as vectors of BTV in Aachen (Western Germany; Mehlhorn et al. 2007), present in the whole Germany in the same quantities (approximately 3/4 of the catches) as in Western Germany?

     
  3. 3.

    Are there other vectors of BTV than members of the C. obsoletus group?

     
  4. 4.

    What are the months with the highest rates of occurrence of midges?

     
  5. 5.

    Is there any midge-free period during the year in Germany?

     
Some groups enlarged their goals and tried to contribute to further questions:
  1. 1.

    Where and when do the midges attack their hosts?

     
  2. 2.

    Which are the conclusions that can be drawn with respect to animal protection from bites of vector midges?

     
  3. 3.

    Are there hints on the pathways of introduction of BTV in Central Europe?

     
  4. 4.

    Are there peculiar regulations needed in future with respect to animal transportations, e. g. spraying of insecticides to avoid transportation of biting insects?

     

Installation and running of the monitoring project

In January 2007, the BMELV invited several research groups with entomological experience to join the virologists and epidemiologists of the Friedrich-Loeffler-Institut for a common program to monitor the putative vectors of BTV. During several meetings, the following ten groups agreed to cooperate: (1) Prof. Dr. H. Mehlhorn (Düsseldorf), as coordinator, (2) PD Dr. M. Beer (Riems), (3) Dr. C. Bauer (Gießen), (4) PD Dr. C. Clausen (Berlin), (5) PD Dr. F. J. Conraths (Wusterhausen), (6) Dr. G. Geier (Regensburg), (7) Prof. Dr. E. Kiel (Oldenburg), (8) Prof. Dr. A. Liebisch and Dr. G. Liebisch (Burgwedel), (9) Prof. Dr. G. Schaub (Bochum), and (10) Dr. D. Werner (Berlin).

To select the sites for monitoring, a grid consisting of 45 × 45 km2 cells was formed that covered the monitoring area. As a rule, one trap was placed into each grid cell. Ninety-one sites, normally on farms, were selected with the help of the local veterinary authorities. Most sites were localized in the 150-km restriction zone that existed in December 2006. By the end of March 2007, one ultraviolet lamp trap (Biogents, Regensburg, Germany; Figs. 1 and 2) was (Hobo H8 Pro, Fa. Onset Computer Corp., MA, USA) placed on each selected farm accompanied by a weather station, which collected and registered electronically the relevant data at intervals of 4 h. The farmers were informed how to handle the traps during the catching period lasting from day 1 to 8 of each month. After the eighth day of catching insects during the night time between dusk and dawn, the farmers transferred the catches in fresh 70% ethanol inside of 100-ml plastic bottles and sent them by regular mail to one of the above cited institutes, where the insects were investigated by means of stereo light microscopes. The midges were separated from the other insects, classified as C. obsoletus (group), Culicoides pulicaris (group), or other Culicoides spp. (Fig. 3) and stored in fresh 70% ethanol. The female midges—separated into groups of fed and unfed individuals—were finally sent each month to the German national reference laboratory for bluetongue disease at the FLI (Riems), where groups of 50 female midges were pooled and examined for BTV serotype 8 genome by real-time polymerase chain reaction (PCR). The obtained data were introduced into a database collecting the results of all groups and species involved. This database was also fed with the data obtained from the different weather stations.
Fig. 1

Diagrammatic construction plan of the BG-Sentinel™ midge trap provided by Fa. Biogents (Regensburg). The ultraviolet lamp (see Fig. 2) is not shown. Insects are attracted by ultraviolet light during night and become sucked into a catch back (dry catches) or into an ethanol filled catch beaker (wet catches) by help of an air stream produced by a fan (detail 12)

Fig. 2

Trap in action during night showing UV-light

Fig. 3

Life cycle stages of Culicoides species. a Adult female. b Larva hatching from egg. c Larval stage. d Pupa. e Anterior protrusion of pupa

Fig. 4

Scanning electron micrograph of the head of a female Culicoides obsoletus. Note the large compound eyes and the short but very strong mouthparts. The antennae show only a few hairs

Results

The detailed results of the monitoring in the different German regions are presented in the ten papers following this introducing overview in the present volume of the journal (Mehlhorn et al. 2009; Kiehl et al. 2009; Vorsprach et al. 2009; Balczun et al. 2009; Kiel et al. 2009; Clausen et al. 2009; Bartsch et al. 2009; Stephan et al. 2009; Bauer et al. 2009; Hörbrand and Geier 2009). However, the common features can be summarized as follows:
  1. 1.

    The African and South European BTV vector C. imicola was never found in Germany during the whole monitoring period.

     
  2. 2.

    The 91 farms of the monitoring program were situated at different heights above sea level and in different weather regions with considerable differences in the yearly mean temperatures. The traps were exposed to changing winds under different circumstances. Despite these differences, members of the C. obsoletus group (see Mehlhorn et al. 2009) was most abundant in the entire monitoring area, representing in most catches more than 70% of all caught midges. In some catches, even more than 90% of the determined midges belonged to the C. obsoletus (group). C. pulicaris and relatives came second and reached up to about 20% of the caught midges, while the others (belonging to up to 24 other species or taxa) occurred in rather scarce numbers. This was also true for C. dewulfi, which—according to literature—was expected to be more common as it was found in high abundance in some sites in the Netherlands (Saegerman et al., 2008). Only on a few farms and only during a few catching periods do members of the C. pulicaris group occurred in higher numbers than members of the C. obsoletus group.

     
  3. 3.

    As in 2006 (Mehlhorn et al. 2007), members of the C. obsoletus group were found infected with BTV 8 since numerous pools were found positive for BTV 8 beginning in August 2007 until November 2007. Among them, several groups/pools of unfed female specimens of the C. obsoletus group (Fig. 4) contained the virus, too. Therefore, it is likely that the main vector(s) of BTV 8 in Germany belong to the C. obsoletus group. However, in addition to pools of midges of the C. obsoletus group, several pools of with midges of the C. pulicaris group were proven to be carriers of BTV 8 in 2007. However, the number of positive C. pulicaris group pools was considerable lower than in midges of the C. obsoletus group. In the catches from North Rhine-Westphalia and Brandenburg (Mehlhorn et al. 2009; Clausen et al. 2009), also, unfed females of the C. pulicaris group contained the virus. These findings underline that members of the C. pulicaris group may be suitable as vectors for BTV, but they seem less important than members of C. obsoletus group.

     
  4. 4.

    The catches indicated that there is no midge-free period during the year in the monitoring area, since midges were caught also during the cold months in December until February. This supports the idea that BTV may be able to overwinter in midges, and that transmission may occur during the cold season at a very low level. This is furthermore underlined by the finding that midges apparently stay inside the stables, since in traps placed inside stables or at stable doors, many fed females were caught.

     
  5. 5.

    The highest numbers of midges were found in the months September and October at most places when also the highest numbers of BTV-infected pools of midges were detected.

     
  6. 6.

    The first BTV-positive pools were not found before August 2007, although the first cases of clinical or PCR-positive cattle had been documented already in May 2007. This indicates that the sensitivity of the midge monitoring is lower than the sensitivity of the clinical surveillance in ruminants. Moreover, the number of infected midges is rather low at the beginning of the transmission season and increases in the months of July, August, until November, where it starts to decrease.

     
  7. 7.

    The method to investigate pools of about 50 female midges for BTV genome might be rather crude since it is not clear how many positive midges are needed until a pool of 50 midges reacts virus-positive. Thus, it might be suspected that a larger amount of virus positive midges occurs earlier than now seen with the present method used.

     
  8. 8.

    The microscopic species determination during the present monitoring was mainly based on the appearance of the wing feathers, where peculiar black dots (formed by fine hair) and white fields (without hair) were combined with a characteristic pattern of wing veins. Especially the disappearance of hair in some specimens (due to the catching and preparation procedures) made it often difficult to a clear species determination. Furthermore, other criteria (such as the shape of palps, the shape of ovary, ootheca, and hair at the feet) that had been used during the establishment and description of the different Culicoides species are often misleading and do not respond to modern criteria. Therefore, several species, which look very similar to C. obsoletus or C. pulicaris, cannot clearly become differentiated. Thus, many authors describe groups of C. obsoletus or C. pulicaris species or name these groups “complexes”. Both are not systemic units. Thus, the true existence of species has to be tested by molecular biological methods, as was started by several authors (Lit. c.f. Kiehl et al. 2009). There, it turned out that several species can be united in given species such as C. obsoletus or C. pulicaris.

     

Conclusions

The present monitoring showed that midges which are able to transmit BTV occurring in the entire monitoring are in high abundance, while the main vector in the Mediterranean and Africa, C. imicola, was not found in Germany. This makes it unlikely that BTD was introduced by northward wandering infected C. imicola. This seems also reasonable because BTV 8 has never been detected in Southern Europe. In Germany, at least member of the C. obsoletus and the C. pulicaris groups may act as vectors of BTV. Midges of these groups overwinter inside or close to stables. The invasion of BTV may have been stabilized by the infection of wild ruminants which may serve as reservoir for the virus. These facts make it necessary to protect susceptible domestic animals from BTV infection or clinical disease. One method is to treat stables and/or the herds with long-lasting insecticides (Mehlhorn et al. 2008a, b, c, d; Schmahl et al. 2008). Alternatively, the animals can be vaccinated against the relevant BTV serotypes. For Europe, an inactivated vaccine against serotype 8 was developed in a very short period from 2007 until its first inoculation in May 2008 into sheep and cattle (Table 1). In combination with the existing immunity after natural infection, the mass immunization cattle and sheep led to a considerable reduction of new infections. However, the success of this vaccination campaign is endangered by the presence of BTV serotype 1 in France and the occurrence of serotype 6 in The Netherlands and Germany in 2008. Thus, the vaccination—although being very effective—has to be adapted to new BTV serotypes as was done in other parts of Europe in the years before (see Table 1).
Table 1

Vaccination programs against different serotypes of bluetongue virus in Europe

Vaccine

France/Corse

Italy

Spain

Portugal

Bulgaria

Central Europe, England

 

serotypes

sheep

sheep

cattle

sheep

cattle

sheep

cattle

sheep

sheep

cattle

Live vaccine

BTV 3, 8, 9, 10, 11

       

1999–2000

  

BTV 2

2002–2002

2002–2006

2002–2006

2000–2001

      

BTV 4

   

2004–2006

 

2005–2006

    

BTV 2 + 4

2003–2004

2004–2006

2004–2006

2003

      

BTV 2 + 9

 

2002–2006

2002–2006

       

BTV 16

2004

         

BRV 2, 4, 16

 

2004

2004

       

BRV 2, 4, 9, 16

 

2004

2004

       

BTV 2, 4, 9

 

2005–2006

2005–2006

       

Inactivated vaccine

BTV 1

2008

  

2007

2007

2007

    

BTV 2

2005

         

BTV 4

   

2005–2006

2005–2006

2005–2006

2005–2006

   

BTV 2 + 4

2006

2005–2006

        

BTV 8

2008

  

2008

2008

2008

2008

 

2008

2008

However, both methods of prophylaxis (vaccination and protection against insect bites) give hope to decrease the possible losses due to BTV. Since other virus diseases—including those of humans—are luring at the doors of good old Europe, special attention is needed in times of enormously increasing globalization when animals or troops are transported from overseas back to Europe.

Of course, even such an intense and broad monitoring project as the present one on BTV vectors left a series of questions without significant or final answers. It remained unsolved, where the involved vector midges have their definitive breeding sites and how long it takes until maturity is reached. Therefore, it remained unclear, too, whether the virus is potentially transmitted to the eggs and larvae of the Culicoides species. Furthermore, experiments have to be done in order to find out whether other blood-sucking arthropods or licking flies are mechanical vectors of BTV. In addition, the questions, how many bites of midges and how many viruses are needed to establish a persistent infection inside a vertebrate host, remain unsolved. Thus, ongoing research is urgently needed, which, however, requires significant funding and establishment of positions for scientists, in this for a long time, completely neglected field of medical and veterinary entomology.

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Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Heinz Mehlhorn
    • 1
  • Volker Walldorf
    • 1
  • Sven Klimpel
    • 1
  • Günter Schaub
    • 2
  • Ellen Kiel
    • 3
  • René Focke
    • 3
  • Gabriele Liebisch
    • 4
  • Arndt Liebisch
    • 4
  • Doreen Werner
    • 5
  • Christian Bauer
    • 6
  • Henning Clausen
    • 7
  • Burkhard Bauer
    • 7
  • Martin Geier
    • 8
  • Thomas Hörbrand
    • 8
  • Hans-Joachim Bätza
    • 9
  • Franz J. Conraths
    • 10
  • Bernd Hoffmann
    • 11
  • Martin Beer
    • 11
  1. 1.Department of ParasitologyHeinrich Heine UniversityDüsseldorfGermany
  2. 2.Department of Special ZoologyRuhr UniversityBochumGermany
  3. 3.AG Gewässerökologie und NaturschutzCarl von Ossietzky UniversityOldenburgGermany
  4. 4.ZecklabBurgwedelGermany
  5. 5.German Entomological InstituteLeibniz-Zentrum für Agrarlandforschung (ZALF)MünchenbergGermany
  6. 6.Department of ParasitologyJustus Liebig UniversityGiessenGermany
  7. 7.Institute for Parasitology and Tropical Veterinary MedicineFree University BerlinBerlinGermany
  8. 8.Fa. BiogentsRegensburgGermany
  9. 9.Bundesministerium für Ernährung Landwirtschaft und Verbraucherschutz (BMELV)BonnGermany
  10. 10.Institute of EpidemiologyFriedrich-Loeffler-InstitutWusterhausenGermany
  11. 11.Institute of Diagnostic VirologyFriedrich-Loeffler-InstitutGreifswald-Insel RiemsGermany

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