| Sažetak | Bolest plavog jezika (BPJ) je vektorima prenosiva zarazna bolest preživača čija pojava uzrokuje
značajne ekonomske gubitke u sektoru poljoprivredne proizvodnje. Tijekom posljednjih
dvadesetak godina u Europi u nekoliko je navrata došlo je do značajnog širenja bolesti, a unatoč
činjenici da su pogođene zemlje većinom usvajale standardizirane politike kontrole,
primijenjeni pristup nije rezultirao zaustavljanjem cirkulacije virusa. U navedenom razdoblju
zabilježeno je ponovno izbijanje BPJ na područjima gdje se isto nije pojavio duže od 10 godina,
niska razina cirkulacije određenih serotipova od kojih se nekima nije uspjelo utvrditi podrijetlo,
pojava novih serotipova, širenje bolesti na potpuno nova područja te manjkavost kontrole
cijepljenjem uz ponovno izbijanje bolesti. Slijedom navedenog, glavni cilj ovog istraživanja
bio je razvoj novog pristupa provedbi mjera kontrole i prevencije BPJ koji će biti utemeljen na
dokazima i definiranju ključnih čimbenika, uzimajući u obzir sve osobitosti ove bolesti u RH.
U tu je svrhu provedena sveobuhvatna analiza koja je uključivala utvrđivanje mjera učestalosti,
magnitude varijabilnosti seroprevalencije, analizu čimbenika rizika, prostorno-vremensko
mapiranje i analizu procijepljenosti. Utvrđeni su i razlozi neuspješnog provođenja dosadašnjih
politika kontrole ove bolesti kao što su ograničenja trenutnog načina prikupljanja i pohrane
podataka, te neprilagođeno, nedostatno i nepotpuno provođenje mjera kontrole i prevencije.
Temeljem dobivenih rezultata definirani su ključni čimbenici u osmišljavanju nove strategije
koji uključuju razvoj modela praćenja koji bi osigurali rano alarmiranje sustava i poduzimanje
potrebnih mjera i prije nego se bolest unese na područje RH; kontinuiranu obnovu znanja i
podizanja razine svijesti veterinara i posjednika životinja o ranom prepoznavanju bolesti;
prilagođeno usmjeravanje mjera na razinu najveće varijabilnosti – županiju; planiranje
entomoloških istraživanja na način da se omogući analiza utjecaja klimatoloških i ekoloških
čimbenika na pojavnost i distribuciju različitih vrsta vektora, a isto usporedi sa pojavom
slučajeva u preživača; istraživanje možebitne uloge divljih preživača u održavanju infekcije i prezimljavanju virusa. Uz prospektivno planiranje mora biti detaljno osmišljen način
prikupljanja, procjene i integracije podataka te provjere postupaka tijekom samog provođenja
programa. Pristup primijenjen u ovom istraživanju te dobiveni rezultati predstavljaju temelj za
izradu buduće strategije kontrole i prevencije BPJ u RH, no isto bi se moglo primijeniti, kao
znanstveni temelj, i za planiranje nacionalnih strategija kontrole ostalih vektorskih zaraznih
bolesti životinja |
| Sažetak (engleski) | Introduction
Bluetongue disease (BTD) is a vector-borne, viral disease of domestic and wild ruminants
associated with considerable impact on the animal health and consequently significant
economic losses in the agricultural production sector. Circulation of the BTD virus until 1998
had been localized within the tropical and sub-tropical climate zones while after this period the
virus spread to the north, and by 2006 had spread to western and central Europe encompassing
the belt of temperate and sub-polar climate zones. Over the past twenty years, BTD outbreaks
caused by a variety of serotypes have occurred and spread several times across different regions
of Europe. Although the affected countries have largely adopted standardized control measures,
the approaches used has not resulted in elimination of disease. The occurrence of BTD during
this period included unexpected epidemics in areas where the disease had never been confirmed
before, low level circulation of certain serotypes, some of which have an unclear origin,
incursions of new serotypes, vaccine incidents and disease reoccurrence. Implementation of
appropriate surveillance, control and preventive measures are further complicated by the
incomplete understanding of the ecology of the vectors, viral transmission dynamics and
maintenance in a given area.
In the Balkan Peninsula region, where BTD had not occurred for more than 10 years, an
unexpected epidemic of serotype 4 occurred in 2014. The first detection of this serotype in the
region was followed by rapid spread to 11 south-eastern European countries over a very short
time period. Although many studies have investigated BTD in Europe, no nationwide study on
the prevalence of BTD serotype 4, influence of climatological factors, vectors and
overwintering mechanism or efficiency of applied vaccination programs from Croatia have
been carried out.
In 2015, the Croatian Ministry of Agriculture implemented a comprehensive mass vaccination
campaign against BTD for all ruminants in Croatia. Vaccination campaign followed the
recommendations of the EFSA 2017 Scientific report on Bluetongue: control, surveillance and
safe movement of animals until the end of implementation in 2019. Despite implemented
measures, only 18 months upon last vaccination campaign BTD re-occurred in 2020 when
serotype 4 was re-confirmed in sentinel animals in Istarska, Dubrovačko-neretvanska and
Požeško-slavonska counties.
Objectives
The recent BTD outbreaks in Croatia suggest that the implementation of measures cannot be
generalized. Planning must take into account the specific conditions of the area, such as
population density and demographics, climatic factors, vector ecology and availability of
administrative resources, to ensure that a strategy for BTD disease control and potential
eradication is based on a case-by-case approach.
In a view of the above, the main objective of this research was to develop a new approach to
the implementation of BTD control and prevention measures that is evidence-based and
includes forward strategy planning on the basis of relevant data, taking into account all the
characteristics of the disease epidemiology in Croatia. For that purpose, certain specific
objectives of the research included calculation of disease frequency measures, assessment of
the magnitude of seroprevalence variability, analysis of risk factors, spatial-temporal mapping
and evaluation of the impact of vaccination programs.
Material and methods
This research covered the areas of all Croatian counties where measures for the control and
monitoring of BTD where implemented in the period 2014 to 2019. In order to do a
comprehensive epidemiological analysis, data on laboratory testing, dynamics of ruminant population, movement of live animals, clinical signs detected, vaccination of cattle, sheep and goats, entomological studies of Culicoides species and climatic factors were collected. All data were analysed after being separated into a clinical phase that lasted from 27 October 2014 till 01 July 2015 and a phase of active control from 15 August 2015 till 31 December 2019.
Descriptive statistics included frequency tables and epidemiological curves. Hierarchical
logistic regression with binary outcome of serological testing in sheep was used to establish
relative variability in serological positive response at the county, municipality and herd level,
where the latter administrative and organizational units were used as random effects in a
hierarchical logistic regression model. Risk factors for the number of BTD cases in the county
over time during the clinical phase were determined through negative binomial regression with
county as a random effect on intercept. Univariable analysis was followed by building the final
multivariable regression model. During the phase of active control, likelihood of detecting a
positive sentinel animal was determined by fitting the logistic regression model with county as
a random effect on the intercept. The main exposures of interest were the percentage of
vaccinated cattle, sheep, goats and ruminants in general. Regression models containing
individual exposures of interest, and adjusted for the fixed effect of year, as well as random
effect of county were used to inform development of the final multivariable models.
Results
Analysis of the ruminant population dynamics from 2014 to 2019 showed that mixed-type herds
with more than one ruminant species predominated in Croatia and that more than 83% of herds
kept less than 50 animals. Bovine population is continuously declining while sheep and goats
are slightly increasing. In the territory of Croatia, two serotypes of the BTD virus were
circulating; serotype 4 circulated throughout the area of the entire country whereas serotype 1
did not spread beyond the boundaries of the location of the island of Lastovo.
During the clinical phase of epidemic, the morbidity and mortality in affected herds were
19.33% and 3.31%, respectively. Severe clinical signs described in the literature were not be
observed and disease had a mild course. In the four southern counties where clinical disease
was observed during clinical phase, herd-level seroprevalence confirmed by ELISA in the study
population was 89.83% and animal-level seroprevalence was 29.38%. The overall herd-level
prevalence in the study population confirmed by RT-PCR was 68.08% with the animal-level
prevalence 23.66%. All animals laboratory tested due to clinical suspicion were positive by RTPCR. The highest number of seropositive herds was located near the first confirmed case in the
affected area. Results of the variance component analysis which included three hierarchical
levels county, municipality and herd revealed that the highest level of variability was detected
at county level, regardless of the type of model and the approach used. This suggested that
implementation of disease control and prevention measures at the county level would indeed
be the most effective way to implement disease control measures. Univariabile analysis of
climatological factors detected a statistically significant association with the number of new
cases in the county only for temperature. The increase in mean daily temperature to 18⁰ C
increases the number of cases in the county by 4.18 times (95% CI 1,18 -14,73). For
precipitation, humidity and wind speed no statistically significant association was found with
the occurrence and spread of BTD.
Seropositive sentinel animals confirmed by ELISA were detected during the entire phase of
active control of epidemic, with the highest animal-level seroprevalence (23%) in 2015 and the
lowest (9%) in 2019. At the species level, the highest seroprevalence was found in cattle
(10.62%), followed by sheep (5.64%) and then goats (0.13%) which actually corresponded to
the number of sentinels used per ruminant species. Overall 5.06% sentinel samples tested by
RT-PCR were positive with the highest prevalence during October, a tendency to decrease in
November and December and no recorded BTD positive cases from February to August. The highest overall prevalence (15.53%) was in 2016, and the lowest in 2017 (0.52%), while in
2018 and 2019 BTD was not confirmed by RT-PCR. Such findings are directly related to the
results of the vaccination. Cumulative herd vaccination coverage was 88.93% and 84.55% at
the animal level. Statistical analysis of the vaccination impact has shown that as the percentage
of vaccinated animals increase, the probability of detecting seropositive sentinel animals
decreases. This type of association was found to be statistically significant for all variables
(year, animals and herds of cattle and goats) except for the percentage of vaccinated sheep at
herd and animal level, which was an unexpected finding.
The dominant presence of palearctic Culicoides species from Obsoletus and Pulicaris
complexes was confirmed, as well as the complete absence of C. imicola. Circulation of vectors
in Croatia has two peaks, the first (larger) during May-June and the second (smaller) during
October. A smaller number of vectors was isolated during December and the period JanuaryMarch which could indicate that the specified period could be considered as a vector-free
period.
Discussion and Conclusions
The last introduction of BTD in Croatia is likely a consequence of passive transport of infected
vectors by wind. In the overall sample morbidity and mortality were low and the circulation of
serotypes detected was not evenly distributed throughout the country. The analysis of variance
at three hierarchical administrative levels (county, municipality, herd) in all models indicated
that the highest proportion of total variance resided at the county level. Using univariable and
multivariable regression models among all the analysed climatological factors that may affect
BTD incidence, statistically significant association was found only for temperature.
Precipitation, relative humidity, and wind speed could not be identified as statistically
significant factors. A comparison of the vaccination results and the overall prevalence
suggested that vaccination leaded to a decrease in prevalence and that the percentage of seropositive herds declined, but without complete elimination of infection. Evidence of
seropositive sentinel animals during all five years of vaccination clearly indicated that
vaccination coverage less than 90% of total population did not ensure complete elimination of
the virus and it continued to circulate at low levels throughout the whole period. The reasons
for the lack in the implementation of the previous policies for the control of BTD, such as
limited data collection and storage as well as inadequate, insufficient and incomplete
implementation of control and prevention measures, were identified.
Based on the obtained results, key factors in design of a new strategy were defined and the most
significant includes: development of disease monitoring models that would ensure early
response of the system and implementation of necessary measures before the disease is
introduced into the territory of Croatia; continuous renewal of knowledge and raising the level
of awareness among veterinarians and animal owners about early detection of the disease;
adjusted targeting of measures to the level of the highest variability - county; planning of the
entomological research to enable the analysis of the influence of climatological and ecological
factors on the occurrence and distribution of different types of vectors and to compare the same
with the occurrence of cases in ruminants; research of possible role of wild ruminants in
maintaining infection and overwintering.
In addition to prospective planning, a detailed method for data collection, evaluation and
integration as well as verification of procedures during the implementation of the program must
be developed. The approach applied in this research and the obtained results represent the basis
for the development of future strategy for control and prevention of BTD in Croatia, and the
same could be applied, as a scientific base, for planning the national control strategies of other
vector borne animal diseases. |
