Environmental epidemiology of bovine tuberculosis in pastured cattle and deer
Csivincsik, Ágnes
, Zsuzsanna Rónai
, József Szabó
, László Lövey
, Szilárd Jánosi
Somogy County Agricultural Office Food-chain Safety and Animal Health Directorate
Central Agricultural Office Veterinary Diagnostic Directorate
Kaposvár University Game Management Centre
*Corresponding author:
In present days most of European countries are free from bovine tuberculosis. In
the last century test-and-slaughter method of eradication was the only by which the present
situation has been reached. Nowadays epidemiologists can’t reach further results because
of sylvatic reservoir of the bovine tuberculosis. The interdisciplinary research of this disease
began in England where Eurasian badger (
Meles meles
) proved to be the most important
reservoir of the disease. In our study we examined two cattle and a red deer farm proved to
be infected with Mycobacterium caprae in the same region of Hungary. We collected data
about husbandry systems of the farms and about the environment for determining the risk of
unwanted events occurring. Our results suggest that strict recordkeeping, good
management practice, fencing system and herd size are the most important factors in the
epidemiology of bovine tuberculosis in pastured herds in a highly infected forest
Bovine tuberculosis is one of the most important animal health problems of pastured herds in
many regions of Europe. Since the last two decades the research carried out in connection
with natural reservoir of bovine tuberculosis has got more important in the maintenance of
freedom from the disease. (7)
The reservoir research in Europe began in England in the 1970s as the connection between
the infection of badgers and cattle was confirmed. (4) Since then an interdisciplinary
approach has been applied by epidemiologists as the results of ecology, population
biology, geology, meteorology, mathematics, statistics and of course veterinary
epidemiology has been used in planning strategy against bovine tuberculosis. In England
Eurasian badger (
Meles meles
) proved to be the most important reservoir but either red
Cervus elaphus
) and fallow deer (
Dama dama
) were found to be infected in some area of
the UK. (4, 9)
In continental Europe the European badger hasn’t got such importance in the
epidemiology of bovine tuberculosis. The European studies suggest that wild boar is the
most important reservoir of the disease but in some areas red and fallow deer can also play
an important role in the epidemiology. In the course of the research it was found that dense
wildlife population and intensive hunting management were predisposing factors to make
the disease endemic in an area. (8, 13)
Areas with the above-mentioned predisposing factors are risky for grassland based animal
husbandry. But as the environmental requirements of intensive wildlife (especially large
game species) management and pasturing animal keeping are very similar so these areas
are mostly the best for grassland and pasture management. For this reason environmental
epidemiology and risk assessment is applied in Europe to prevent tuberculosis infection of
herds managed in endemic area. (1, 7)
Risk assessment can be conducted in a qualitative or a quantitative manner. A qualitative
assessment presents data in a logical way and aims at summing up the risk in words using
terms like “negligible”, “low”, “moderate” and “high” without allocating exact numerical
values to probabilities, costs and consequences. Quantitative risk assessment uses the tools
of mathematics, statistics and computing and is suitable for modelling epidemics. (10)
Materials and methods
In our study first we analysed the environment of three (2 cattle, 1 deer) farms in the view of
spread the bovine tuberculosis. Then we used the qualitative risk assessment as we analysed
the steps of the technology of the three farms, identified hazardous steps, assessed the
probability and the consequence of hazards and made recommendations to prevent risk.
In the assessment we used the above-mentioned terms without exact numerical values.
Study area
Our research was carried out in the Region of Zselic. This is a highly forested area of South
Tarnsdanubia. The climate is sub-Mediterranean, sub-Atlantic so in contrast with the other
parts of Hungary the summer is less hot and less dry, the winter is mild, and the rainfall is
more frequent all the year round. Soil type is clayed brown forest soil with high iron content
and low pH. These conditions are favourable for mycobacteria surviving in the environment.
The habitat has got a varied structure and contains a wide range of natural and agricultural
plant community so it can support game populations. The bottle-neck factor in the habitat
is the relative lack of surface water which makes the habitat overpopulated in dry periods
of the year. Few watering places appeal a lot of animals in a wide range of species.
The big game population of the area is very dense and intensively managed. There are
seven game parks on an almost 1200 km
area. The waste materials of hunting are not
rendered in accordance with professional rules and law. After big hunting bags a lot of risk
materials remain in the forests availably for wild boars. This is why wild boars are infected
M. caprae
. The prevalence of infection is more than 20 %. (3) In red deer the infection
prevalence was found to be 5.88 %. (2)
Study farms
All three farms are in the same valley of the Zselic about 3km far from each other. Animals
are pastured in a year-round grazing system. Every farm has got natural watercourse with
source outside the farm. All are confirmed to be infected within a period of two years. The
deer farm is fenced around with a 2.4m height wire fence. At the beginning of the study
around the two cattle farms were electric fences only.
Cattle-farm ‘A’
This farm holds a Limousine herd with 450 cows, 8-10 breeding bulls and offspring. The
animals are kept in 5 groups. The owner and the stockmen are not professionals. The
production and animal health records are kept at the headquarter office of the owner’s
firm far from the farm. Data which should be the base of the records are collected by the
stockmen. The management of the herd is not good. Winter nutrition and spring condition of
the cows are very weak. The lack of professional education of the management made the
eradication very hard. It lasted 20 months.
The method of the eradication programme was test-and-slaughter. We examined every
individuals elder than 6 weeks by single intradermal tuberculin test (SITT) in accordance with
the European Council Directive 64/432/EEC in every 42 days and slaughtered all animals
which had got 2mm or greater sized skin test response. All culled animals’ lymph nodes and
all tuberculosis-like lesions were sent to the national bovine tuberculosis reference laboratory
for culture. With this method we found four culture (
M. caprae
) positive animals. In the
course of diagnostic slaughtering we found serious signs of paratuberculosis in many animals
culled as reactors. These findings were confirmed by the reference laboratory.
After the first year of the eradication programme the owner decided and began to fence
round the farm with 1.2m height wire fence which can fence wild boars off but can be
jumped across by red deer.
Cattle-farm ‘B’

This farm holds a Charolais herd with 50 cows, 1 breeding bull and offspring. The animals are
kept in two groups: calved and pregnant cows. The owner is not but the stockmen are
professionals. The records collected by professional personnel are kept on the farm. The
farm management, nutrition, animal health programme are excellent. The eradication
programme was the same as on Farm ‘A’ and lasted for 10 months. Only one animal were
confirmed to be infected with
M. caprae
. The culture positive lesion was a small abscess in
the cow’s retropharyngeal lymph node. Signs of paratuberculosis were found at culling and
infection was confirmed too.
After half a year of eradication effort the owner began to fence the farm round with 2.4m
height wire fence and ended the work within a month. This is a good tool for fencing also
deer species off the farm.
This farm holds 220 red deer hinds, 14 stags and offspring. The animals are kept in smaller (20-
30 hinds) groups in the summer and in bigger (40-60 hinds) ones in the winter. The nutrition is
well-managed, every husbandry action is planned, and record-keeping is strict and can be
traced back for decades. The farm management has got special profession in deer
farming. This farm couldn’t have been eradicated yet.
Only the hinds and youngsters can be tested by SITT twice a year, in the period from
November to February and in July-August. Stags can be tested only in February when they
haven’t got hard antlers. After the confirmation of infection in every year one-three animals
prove to be infected by laboratory confirmation. Paratuberculosis was also found and
confirmed in this herd.
The base of this deer herd originates from different part of Hungary. In the early history of the
herd there was bovine tuberculosis which ‘disappeared’ more than a decade ago.
Analysing the environmental data we can declare that Zselic Region of Hungary is a bovine
tuberculosis high risk area because of the following reasons. The climatic and geographic
factors can help mycobateria to survive in the environment so the time when shed bacteria
is able to infect a new host is much longer than in a dryer, warmer climate with intensive
ultraviolet radiation (e. g. in the lack of forest cover) or in another type of soil. The dense big
game population which is bothered by intensive hunting management and sometimes
concentrated by scarcity of water is at epidemiologic risk largely. The confirmed bovine
tuberculosis infection of wild boar and red deer gives special importance to these species
and highlights the incorrect waste management of hunters.
Analysing the relevant epidemiologic data of the three farms the main differences can be
summarized in Table 1.
Point of view
Cattle-farm A
Cattle-farm B
red deer
Herd size
Group size
very good
very good
very good
Data collection and record-keeping
freedom from BTB
42 days
42 days
6 months
<1 %
1-2 %
<1 %
beginning of the eradication
20 months
10 months
not ended yet
Height of the round fence
Paratuberculosis infection
Table 1: Epidemiologic data of study farms
Our results suggest that successful grassland based animal husbandry can be run on in a
bovine tuberculosis high risk area if the animal keeper takes into consideration the results of
epidemiologic risk assessment and applied effective prevention programme.
In our study we found that good animal keeping practice and appropriate nutrition have
got great importance. Considering that the tuberculosis in many species e. g. in humans is
an indicator disease of well-being this is not surprising. And the same holds true of herd size
and stocking density. It is very possible that every species has got an ‘ideal’ herd size which
is not advisable to exceed. As either in humans the tuberculosis epidemics began when the
population settled down and began to increase and got dense. (6, 12, 13)
Animal health records are also very important in chronic diseases’ management. On the
deer-farm the record-keeping is excellent and this is why we could trace back in the past
and found the early tuberculosis epidemic out. On Cattle-farm A unreliable record-keeping
made the eradication so hard as it lasted for 20 months and it was possible that the first
animals hadn’t been found at the first testing after infection as contrasted with Cattle-farm
B. In herds where either paratuberculosis infection worsens the diagnostic ability of skin test
the correct data collection and record-keeping for years are essential to find infected
animals as soon as possible.
Frequency of tuberculin testing is also a very important factor of eradication. It is clear that 6
months interval is not enough to reach the freedom from bovine tuberculosis because the
possibility that a new host gets infected and begins to shed bacteria is at least moderate. It
is very necessary to increase the frequency of testing if the aim is freedom from the disease.
Because of the biologic cycle of red deer species in an extensive game farm system more
frequent testing is impossible. This is why we recommend that high quality breeding animals
should be kept in an intensive, small-grouped system where individual treatment and
record-keeping and more frequent tuberculin testing can be carried out. The 6 months
interval with good animal keeping practice are enough just to keep the prevalence low.
Fences round the farms can keep big game out. The longer time data of the deer-farm
suggest that an adequately high fence is able to isolate the domesticated herd from wildlife
correctly. It is possible that the studied deer-farms’ epidemic is independent from the
environments’ one and correctly managed by husbandry tools as the average prevalence
on the deer-farm is lower than the prevalence of red deer population in the environment
and lower than experienced on New Zealand and Irish deer-farms. (5, 11)
1. Courtenay, O. et al. (2006): Is Mycobacterium bovis in the environment important for
the persistence of bovine tuberculosis? Biology Letters doi:10.1098/rsbl.2006.0468
Published online
2. Csivincsik Á et al. (2008): The possible role of red deer (Cervus elaphus) in the
maintenance of bovine tuberculosis in Zselic region of Hungary. In: Enclosures – A
Dead End? CIC Symposium, Sopron
3. Csivincsik Á., Jánosi Sz., Rónai Zs. (2009): A vaddisznó fertızésfenntartó szerepe a
szarvasmarha-gümıkór járványtanában a Zselicben. Academic Reports – Hungarian

Academy of Science Veterinary Committee, Szent István University Veterinary
Doctoral School
4. Gallagher J, Clifton-Hadley R. S. (1999): Tuberculosis in badgers; a review of the
disease and its significance for other animals. Veterinary Laboratories Agency,
Addlestone, Surrey
5. Griffin J. F. T. et al (2003): Diagnostic strategies and outcomes on three New Zealand
deer farms with severe outbreaks of bovine tuberculosis. Tuberculosis 84, (5) 293-302
6. Hershkovitz I. et al. (2008): Detection and molecular characterization of 9000-year-old
Mycobacterium tuberculosis from a Neolithic settlement in the Eastern Mediterranean.
PLos ONE 3 (10): e3426 on
7. Humblet M-F. et al. (2009): Classification of worldwide bovine tuberculosis risk factors in
cattle: a stratified approach. Vet. Res. 40:50 doi: 10.1051/vetres/2009033
8. Machackova M. et al. (2003): Wild boar (Sus scrofa) as a possible vector of
mycobacterial infections: review of literature and critical analysis of data from Central
Europe between 1983 to 2001. Vet. Med.- Czech, 48, (3) 51-65
9. Matthews F. et al. (2005): Bovine tuberculosis (M. bovis) in British farmland wildlife: the
importance to agriculture. Proceedings of the Royal Society doi:
10.1098/rspb.2005.3298 Published online
10. Nurminen M. et al. (1999): Methodologic Issues in epidemiologic risk assessment.
Epidemiology 10, 585-593
11. Partridge, T. et al. (2008): Control of Mycobacterium bovis infection in two sika deer
herds in Ireland – Irish Veterinary Journal 61, 27-32
12. Taylor, M. T. et al. (2007) : First report of Mycobacterium bovis DNA in human remains
from the Iron Age. Microbiology 153, 1243-1249
13. Vicente, J. et al. (2007): Risk factors associated with prevalence if tuberculosis-like
lesions in fenced wild boar and red deer in south central Spain. Vet. Res. 38, 451-464