Rev. Sci.
Tech. Off. Int. Epiz., 2003, 22 (3),1003-1012
A
method of accelerated eradication of bovine brucellosis in the
V.
Kouba
Former
Vice-Director and Chief Epizootiologist, Czechoslovak State Veterinary Service
and Professor, Brno University of Veterinary Sciences, P.B. 516, 17000 Praha 7,
Czech Republic
Submitted
for publication:
Accepted for
publication:
Summary
A
method of accelerated eradication of bovine brucellosis was developed and
applied in the
Keywords
Benefit/cost – Bovine brucellosis – Depopulation – Disease control –
Eradication – Surveillance – Zoonosis.
Introduction
The
By
1960, most countries in the world had reported the occurrence of bovine
brucellosis. Only a few countries managed to eradicate the disease using the
‘test and slaughter’ method, namely
This
paper deals only with the eradication of the disease in the
The
following data concerns brucellosis in
The pre-eradication (preparatory)
phase
The
first countrywide serological survey in 1959 covered 52.49% of the cattle
population, including all females of reproductive age. The disease was
discovered or confirmed in 34 of 75 regions, including 654 localities with
99,787 intrafocal bovines (3.34%), i.e. 153 animals per outbreak (half of these
were dairy cows). Of all the outbreaks, 99% occurred in dairy ranches and only
1% in small farms. The number of newly detected positive cattle was 6,299
animals, i.e. 213 per 100,000 with a prevalence on
Knowledge
of bovine brucellosis characteristics and diagnosis was considered to be
sufficient for eradication. The decision was therefore made to initiate the
programme as soon as possible, without waiting for further results of national
and international research, considering that later, the situation would worsen
(with the risk of introducing the disease into wildlife), i.e. be much more
difficult and expensive to manage. The same approach was applied to bovine
tuberculosis control.
Initially,
the veterinary community and decision-makers had to be convinced about the
methodology to be adopted and the economic feasibility of brucellosis
eradication at national level within a short period of time. In 1959, based on
complex analysis and recommendations presented by veterinary and public health
services, the Government of the former Czechoslovakia adopted a resolution to
eradicate bovine brucellosis (goal – zero incidence) and to eliminate bovine
tuberculosis (goal – zero prevalence). The Government created a special
committee (representing relevant ministries and institutions), chaired by the
Director of the State Veterinary Service, identified subsidies, introduced
obligatory pasteurisation of market milk and issued appropriate directives for
administrative authorities and cattle owners (12, 13, 14). The aim of the programme
was to eradicate bovine brucellosis using simple depopulation of affected farms
and ranches and to meet the objective, by 1965, of zero prevalence and
incidence without recurrence (eradication of all sources of Brucella abortus)
without reducing national milk and beef production, cow populations or the
income of farmers. For the first time, a fixed deadline was imposed upon a
national animal health programme. This was different compared to the previous
attempts of trying to fulfil long-term disease control programmes without fixed
deadlines for achieving the specific targets of reducing or eliminating disease
occurrence.
One
of the first steps implemented was to discontinue vaccination with strain B-19,
which had been useful in reducing negative impacts (abortions, disease spread,
etc.), but was not suitable for the new task, i.e. speedy final eradication. An
additional reason for stopping B-19 vaccination was that distinguishing between
post-vaccination and post-infection antibodies was impossible. This complicated
interpretation of serological test results, as well as identification of
affected and non-affected herds. Relying on the vaccination weakened the
motivation for and consistency in applying other demanding measures necessary
for success.
Materials and methods
Sources
of information for this article include the literature, official statistics and
documents of agriculture and health ministries as well as those of the
veterinary service administration, publications (12, 13, 14, 15) and the
experience of the author (responsible for the preparation and management of the
programme). Diagnostic methods adhered to international recommendations (6).
The
accelerated eradication methodology was based upon the results of comparative
experiments carried out in selected regions by national specialists such as
Anderle (2) and Drazan (4). The eradication philosophy and procedure were based
upon exploitation of the current replacement (‘turnover’) policy of older
generations of the national cattle population. Culling was performed in
priority in diseased herds to avoid risky breeding of affected animals. This
approach also supported the development of a new generation of calves born from
brucellosis- and tuberculosis-free parents and the sale of selected, healthy,
genetically suitable animals to depopulated ranches.
The eradication (attack) phase
Initially,
the traditional ‘test and slaughter’ method was applied without interrupting
the herd breeding process. A ranch could be declared brucellosis-free after
three years of observation following elimination of the last positive case
discovered during repeated testing of all intrafocal cattle. This method helped
to gradually ‘clean’ affected localities with very low prevalence and showing
no clinical manifestation. However, the method was not always reliable,
particularly in outbreaks with higher morbidity, and was found to be too slow
considering the deadline for final eradication. New cases were often discovered
during next herd tests and sometimes, even after declaration of the herd as
brucellosis-free (= recurrence). Isolation measures complicating husbandry and
trade were demanding, costly and difficult to sustain over a prolonged period.
Continuing exposure of animals and people caused new cases, thus aggravating
the situation. Consequently, eradication, particularly in larger ranches with
brucellosis abortions, required a more drastic approach.
The
decision was therefore made to adopt the accelerated radical method without
recurrence (tested previously in a selected region as one of alternative
procedures), based upon affected ranch depopulation after previous interruption
of breeding. Artificial insemination and natural mating were stopped one year
prior to farm depopulation to avoid new conceptions and slaughter of pregnant
animals (the calves were not used for breeding) and to prevent further disease
spread. Intrafocal testing was no longer required with this approach. All
cattle and other susceptible animals were sent to slaughter on the planned
depopulation day(s). Following thorough, final mechanical and chemical
disinfection, the ranch was left without cattle for at least six months,
assuming that natural devitalisation of Brucella abortus would take
place in the environment.
Another
procedure consisted in introducing negatively tested castrated male or female
cattle into the depopulated and disinfected cattle facilities. This was to
enable fattening (temporary feedlot), to maintain the production process and
provide income to farmers. These animals, serving as biological filters, were
again tested before slaughter. New, healthy cattle from brucellosis-free
regions were then introduced following final sanitation.
The
depopulation policy was applied to gradually expand the brucellosis-free
territory to cover the entire country. To facilitate this expansion, a network
of selected highly affected farms, i.e. ‘isolators’, was established,
especially in the region of Melnik. The purpose was to temporarily exploit
selected, high-yielding pregnant milking cows introduced from other brucellosis
farms where all other cattle were sent for slaughter. The numbers of
brucellosis isolator farms were as follows: 1961 – 133, 1962 – 80, 1963 – 51
and 1964 – 64. These farms were depopulated by the end of 1964.
Complex and demanding eradication procedures required extraordinary professional, organisational, economic and social measures, as well as temporary adjustment of national trade policy. Specific trade regulations consisted of allocating a temporary meat and milk purchase quota to the national agency in charge of purchasing agriculture products. Brucellosis-free regions reduced cattle slaughter and thus, affected regions were given a chance to increase slaughter as required by the accelerated eradication programme. The national demand for meat was met in this manner. The meat of cattle with clinical symptoms of brucellosis was classified as conditionally comestible after heat-treatment. Brucellosis-free provinces and regions delivered healthy cattle, mainly pregnant heifers, to depopulated ranches to recommence breeding and production. The quota for milk trade was set in the opposite manner, i.e. lower in affected regions because of the reduction in number of milking cows due to premature slaughter. In the free regions, the quota was increased to maintain national milk trade level.
The
brucellosis eradication campaign covering the entire area of former
Diagnosis and surveillance
International
methods available at that time were used for intravital diagnosis. The tube
agglutination test was used as recommended by the Food and Agriculture
Organization of the United Nations (FAO) and the World Health Organization
(WHO) (6). To increase detection of all affected cattle, the test was combined,
in dubious and suspect cases, with a complement fixation test and, eventually,
with Coomb’s test as modified by Hajdu (9), as well as Kolar’s allergic test
(11). The agglutination test, with a titre of 1:80 and
Brucellosis
surveillance and monitoring was based upon intensive serological testing, as
follows (Fig. 2):
– pre-eradication phase (1955-1959) 5,517,733 tests,
– eradication (attack) phase (1960-1964) 6,743,901 tests,
– initial post-eradication phase (1965-1969)
5,581,964 tests,
– follow-up period
(1970-1999) 16,199,954 tests.
Altogether,
between 1955 and 1999, 34,043,552 tests were carried out, i.e. the annual
average was 756,523 tests. A maximal annual test/population ratio of 0.5 was
reached in the first year of the attack phase while the average annual value
for the 45 evaluated years was 0.25 (Table I).
Particular
attention was paid to clinical and post-mortem suspect cases, newly discovered
outbreaks, contact animals and new cases in man. Immediate action was taken to
trace the disease source and route of spread using complex diagnostic methods
and thorough epizootiological analysis. Every case was different, requiring
different approaches. The national reference centre for brucellosis was
referred to for a final opinion in dubious cases.
Programme management
Programme
management played a very important role, establishing a dense network of
well-staffed and equipped veterinary diagnostic laboratories operating
according to international standards. Specific antigens, sera and allergens
produced by a veterinary biologics factory were tested by the new Institute for
Control of Veterinary Biologics. A new Veterinary Sanitation Institute with a
network of rendering plants was made responsible for the processing of dead
animals and non-consumable animal products, but also for carrying out demanding
intrafocal disinfection by specially trained staff provided with modern
equipment.
Specific
legislation (ministerial decrees), instructions from the Director of the State
Veterinary Service and diagnostic standards were issued (12). A national
register of all diseased herds was established, and a particular
target-oriented information system of reporting was introduced (number of
tests, results, diseased animals and herd incidence and prevalence, programme
achievement, etc.), together with data processing, evaluation and feedback.
Postgraduate training of all professional staff involved was organised to
ensure uniformity in application of instructions and standards. Intensive
extension activities, supported by national mass media, played an important
role in the effective implementation of the accelerated eradication programme.
The eradication process was stimulated by financial motivation (premiums) and
by competitions. Entrances of brucellosis-free ranches were identified with
signboards declaring this status.
Streamlining
the national brucellosis eradication programme required adapting the
organisational structure of the State Veterinary Service (mainly expanding
laboratory diagnostic capacities), improving the manpower of the organisation,
providing material, logistic and financial backups, and strengthening the
vertical management of the structure. For example, a network of regional and
provincial epizootiologists was established and placed under the direct
technical supervision of the national chief epizootiologist. This resulted in an uniform professional approach, programme preparation,
management, co-ordination and evaluation. This structure was linked with a
similar network of epidemiologists in the public health service. The veterinary
and public health services played a key role in undertaking intensive
surveillance with adequate follow-up response. Their collaboration in the
field, in laboratories,
as well as at managerial level was excellent.
Plans
for brucellosis control were elaborated in all affected provinces, regions and
ranches, and implemented as an integral part of their production and managerial
programmes. Individual plans, respecting national instructions and local
conditions, contained the objectives, i.e. final date(s) for depopulation of
brucellosis ranches and lists of anti-brucellosis activities with deadlines and
responsibilities of personnel. Provincial and regional
inter-sectorial committees for zoonoses control co-ordinated the activities of
participating organisations.
The
eradication programme was supported by direct financial aid to the farmers and
co-operatives, mainly to offset the difference between real and slaughter
prices. All activities in implementing the programme were financed by the
state, i.e. they were free of charge. Insurance agencies contributed as well.
Results and post-eradication period
The
main result of the preparatory phase was identification of specific
epizootiological situations and influencing factors, selection of an
appropriate eradication method and creation of indispensable conditions.
During
the eradication phase, 19,247 new brucellosis-positive bovines were detected.
All existing 39,835 diseased animals (i.e. 20,841 found at the beginning plus
new ones) and more than one hundred thousand intrafocal serologically negative
cattle and contacts were eliminated and replaced by healthy animals. Finally,
previously vaccinated animals were eliminated to avoid future diagnostic
complications. Total eradication comprised 654 initial and 91 new outbreaks,
i.e. 745 outbreaks (Table II).
Zero
prevalence in cattle was achieved by the end of 1964 (Table III), followed by
zero incidence (Fig. 3). Simultaneous zero incidence was achieved in humans
(Fig. 4). Complete recovery of the cattle population was reached by removing
and replacing all diseased and suspect intrafocal animals (Table IV). No
recurrence appeared during the post-eradication period (14, 15). Eradication
was achieved simultaneously in the
Eradication
cost about US$ 28 million (US$ 15 million – state subsidies,
US$ 6 million – services, US$ 4 million – local source expenses and
US$ 3 million – insurance agencies). All expenses included,
replacement of one diseased bovine with a healthy animal cost an average of
US$ 703 (eradication cost/number of replaced diseased animals) and
eradication of one outbreak cost an average of US$ 37,584. A simple annual
benefit/cost ratio of > 1 was reached by the third year of the programme.
The cumulative benefit was represented by the specific disease-free status
being transferred to following cattle generations, thereby preventing
repetition of previous losses. A cumulative benefit/cumulative cost ratio of
> 1 was reached by the fourth year of the programme.
Ten
years after eradication of the disease, this indicator reached the value of
5:1, taking into account the cost of post-eradication surveillance. The ratio
of cumulative benefits to the cost of eradication was 7:1 and to the discounted
eradication cost, 12:1 (Fig. 5). However, the discount method could not be used
on the cumulative public health, biological, ecological and economic benefits
which were increasing, i.e. multiplying (not decreasing), in time. The
difference between the total cumulative benefit (US$ 236 million) and the
total cumulative cost (US$ 43 million) reached a value of US$ 193
million by the tenth year of the programme.
Brucellosis
eradication in cattle helps to prevent the occurrence of new cases in the human
population (Table V). Monetary criteria are not suitable for evaluating the
benefit to human health.
To
retain the success achieved, the post-eradication period was dedicated to a
special surveillance system consisting mainly of intensive serological
investigation with priority being given to critical places and strategic timing
(Table VI). Following international recommendations (7), the Rose Bengal plate
agglutination test was also used for mass preventive investigation from the
beginning of the nineties.
During
the post-eradication period, in spite of extraordinary strict protection
measures, the disease was introduced twice from abroad. In 1973, affected
cattle penetrated from a neighbouring country in one border pasture. The
country concerned eliminated the Brucella-infected animals in the frontier zone
after an official request of the Minister of Agriculture (referring to the
current inter-governmental bilateral veterinary agreement). In 1974,
brucellosis was reintroduced through the exceptional import of cattle with
official guarantee of being from a brucellosis-free ranch based on negative
serological tests. All tests carried out after the import as well as the tests
after first parturition were negative. However, abortions occurred in the
quarantine ranch on second parturition. The outbreaks were immediately
eliminated upon detection. Several persons were infected. Foreigners were
responsible for a new, exceptional occurrence of the disease in humans. Some
cases were caused by Brucella suis (eradicated in 1994), while Brucella
melitensis has never occurred.
Conclusion
Eradication
of bovine brucellosis at national level is not an easy task (8, 16). Approximately half the countries in the world are
still reporting the occurrence of the disease (17). Vaccination and ‘test and
slaughter’ control methods continue to prevail in these countries (1, 3, 7, 10,
17). However, the imposition of a relatively short
final eradication deadline and the more radical approach described above proved
to be useful and effective in the Czech (and Slovak) Republics.
Accelerated
eradication in less than one cattle generation consisted of exploiting the
reproduction process of the national cattle population with a temporary quota
regulating national trade in meat and milk. Discovering and isolating all outbreaks
and a consistent system approach were the most important preconditions to the
programme.
The
active participation of about two thousand veterinarians in the field,
slaughterhouses, laboratories, research and service management, as well as the
close co-operation of the public health service, were crucial to the success
achieved. A centralised State Veterinary Service, strong in manpower, material,
facilities and budget proved to be the backbone of this extremely complex and
demanding programme. Co-operation with farmer organisations and support of the
public and their representatives were exemplary. Strict measures for very
limited imports of cattle, due to increasing self-sufficiency in meat and milk
production, helped to protect the country from re-infection.
The
drastic method adopted proved to be not only biologically, but also
economically effective under the given conditions. The results have been
reflected in substantial improvement of the breeding, production and
reproductive performances of the cattle population and in ensuring
brucellosis-free milk and milk products. The absence of an effective
eradication programme would probably have resulted in the disease spreading and
the economic losses and number of new diseased humans would be at least the
same as at the beginning of the programme. Up to the year 2000, eradication has
prevented economic losses of about seven hundred million US$ and saved more
than two thousand people from being affected by the zoonosis.
References
1. Acha P.N. & Szyfres B. (2001). –
Zoonoses and communicable diseases common to man and animals. In
Bacterioses and mycoses, 3rd Ed., Vol. I. Pan American Health Organization,
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skotu metodou radikalni likvidace [Eradication of brucellosis by radical
liquidation method]. Vet. Med. (Praha), 7, 335-338.
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Cin, Ed.). American Public Health Association,
Washington, DC, 75-78.
4. Drazan J. (1962). – Metody ozdravovani
chovu skotu zamorenych brucelozou [Methods for the recovery of cattle herds
affected by brucellosis]. Veterinárství, 7, 331-334.
5.
6. Food and Agriculture Organization
(FAO)/World Health Organization (WHO) (1952). – Report of the Second Joint
FAO/WHO Expert Committee on brucellosis. FAO,
7. Food and Agriculture Organization
(FAO)/World Health Organization (WHO) (1986). – Report of the Sixth Joint
FAO/WHO Expert Committee on brucellosis. Technical Report
Series No. 740. WHO,
8. Garin-Bastuji B. (1994). – Brucelloses
humaines et animales: une evolution favorable, une
eradication difficile. Point vét., 26, 851-858.
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serodiagnostice brucelozy [New methods for serodiagnosis of brucellosis]. Vet.
cas.
10. Kasyanov A.N. (1982). – Methods of
brucellosis control in animals. In Zoonoses control, Vol. II. United
Nations Environment Programme,
11. Kolar J. (1953). – Alergicka diagnostika
bruceloz [Allergic diagnosis of brucellosis]. Veterinárství, 3,
163-164.
12. Kouba V. (1962). – Problematika brucelozy
hospodarskych zvirat v Ceskoslovensku [Problems of brucellosis in domestic
animals in
13. Kouba V. (1964). – Konecna faze eradikace brucelozy skotu v Ceskoslovensku [Final phase
of cattle brucellosis eradication in
14. Kouba V. (1965). – Eliminace brucelozy skotu
v Ceskoslovensku [Elimination of Brucellosis in cattle in
15. Kouba V. (2000). – Historie eradikace bovinni
brucelozy v Ceske Republice [History of bovine brucellosis eradication in
16. Nolen S. (1999). – Brucellosis deadline came
and went, but USDA’s campaign continues. J. Am. vet. med.
Assoc., 214 (8), 114.
17. OIE (World organisation for animal health)
(2001). – World animal health in 2000. OIE, Paris, 701 pp.
18. Sandvik O. & Naess B. (1994). – Animal
health standards in
19. Suntych F. & John C. (1956). – Nemocnost
brucelozou u veterinarnich lekaru v Cechach [Brucellosis among veterinarians in
__________
Table I
Bovine brucellosis surveillance – serological tests in cattle, Czech Republic,
1955-1969
Year |
Number of
serological tests |
Ratio
tests/total population |
Pre-eradication
(preparatory) phase |
|
|
1955 |
713,597 |
0.2499 |
1956 |
974,108 |
0.3367 |
1957 |
1,023,803 |
0.3601 |
1958 |
1,238,204 |
0.4255 |
1959 |
1,568,021 |
0.5249 |
Eradication
(attack) phase |
|
|
1960 |
1,515,000 |
0.5000 |
1961 |
1,412,843 |
0.4511 |
1962 |
1,333,487 |
0.4294 |
1963 |
1,226,446 |
0.3949 |
1964 |
1,256,125 |
0.4098 |
Initial
post-eradication phase |
|
|
1965 |
1,276,203 |
0.4238 |
1966 |
1,244,231 |
0.4101 |
1967 |
1,268,323 |
0.4176 |
1968 |
1,003,252 |
0.3405 |
1969 |
789,955 |
0.2687 |
Table II
Brucellosis in cattle – affected regions and outbreaks (new, extinct), Czech
Republic, 1960-1969
Year |
Number of
regions with cattle with brucellosis |
Number of outbreaks of brucellosis |
|||
Beginning of the year |
new |
extinct – eliminated |
End of the year |
||
1960 |
34 |
654 |
29 |
165 |
518 |
1961 |
32 |
518 |
17 |
107 |
428 |
1962 |
22 |
428 |
17 |
61 |
384 |
1963 |
15 |
384 |
15 |
110 |
289 |
1964 |
6 |
289 |
10 |
85 |
214 |
1965 |
0 |
214 * |
3 |
107 |
110 * |
1966 |
0 |
110 * |
0 |
110 * |
0 |
1967 |
0 |
0 |
0 |
0 |
0 |
1968 |
0 |
0 |
0 |
0 |
0 |
1969 |
0 |
0 |
0 |
0 |
0 |
* in
observation, i.e. without diseased animals
Table III
Prevalence of brucellosis in cattle, Czech Republic, 1955-1969
Year |
Number of
diseased animals |
Prevalence per
100,000 heads |
1955 |
19,500 * |
683 * |
1956 |
22,000 * |
760 * |
1957 |
26,186 |
921 |
1958 |
24,000 * |
824 * |
1959 |
22,000 * |
736 * |
1960 |
20,481 |
676 |
1961 |
33,211 |
1,060 |
1962 |
36,656 |
1,083 |
1963 |
25,288 |
750 |
1964 |
7,998 |
261 |
1965 |
0 |
0 |
1966 |
0 |
0 |
1967 |
0 |
0 |
1968 |
0 |
0 |
1969 |
0 |
0 |
* estimates
Table
IV
Elimination of cattle affected by Brucella abortus in former
Year |
Number at the beginning of the year |
New cases |
Eliminated |
Number at the end of the year |
1960 |
98,596 |
9,823 |
2,186 |
106,133 |
1961 |
106,133 |
4,279 |
22,091 |
88,421 |
1962 |
88,421 |
1,188 |
20,649 |
68,960 |
1963 |
68,960 |
1,511 |
42,184 |
28,287 |
1964 |
28,287 |
2,631 |
30,918 |
0 |
Total 1960-1964 |
98,596 |
19,432 |
118,028 |
0 |
Table V
Incidence of brucellosis in the human population, Czech Republic, 1955-1999
Year |
New Cases |
Year |
New Cases |
Year |
New Cases |
1955 |
39 |
1971 |
0 |
1987 |
1 |
1956 |
75 |
1972 |
0 |
1988 |
2 |
1957 |
38 |
1973 * |
11 |
1989 |
1 |
1958 |
45 |
1974 * |
4 |
1990 |
1 |
1959 |
32 |
1975 |
1 |
1991 |
1 |
1960 |
67 |
1976 |
0 |
1992 |
0 |
1961 |
71 |
1977 |
0 |
1993 |
0 |
1962 |
74 |
1978 |
0 |
1994 |
0 |
1963 |
49 |
1979 |
1 |
1995 |
1 |
1964 |
37 |
1980 |
0 |
1996 |
0 |
1965 |
2 |
1981 |
1 |
1997 |
0 |
1966 |
10 |
1982 |
0 |
1998 |
0 |
1967 |
3 |
1983 |
1 |
1999 |
1 |
1968 |
2 |
1984 |
4 |
2000 |
0 |
1969 |
0 |
1985 |
1 |
|
|
1970 |
0 |
1986 |
1 |
|
|
The
exceptional cases observed during the post-eradication period occurred among
foreigners and some were caused by Brucella suis
* Cases related to imported cattle infected by Brucella abortus
Table VI
Bovine brucellosis post-eradication surveillance – tests in cattle, Czech
Republic, 1970-1999
Year |
Total serological tests |
Positive results |
Annual average of tests |
Annual ratio tests/total population |
1970-1974 |
2,172,708 |
111 * |
434,542 |
0.1412 |
1975-1979 |
2,314,050 |
0 |
462,812 |
0.1394 |
1980-1984 |
1,547,611 |
0 |
309,522 |
0.0877 |
1985-1989 |
686,896 |
0 |
137,379 |
0.0395 |
1990-1994 |
6,038,143 |
0 |
1,207,629 |
0.4640 |
1995-1999 |
3,440,539 |
0 |
688,108 |
0.3952 |
Total 1970-1999 |
16,199,954 |
111 * |
539,999 |
0.1825 |
* imported
cattle
Fig. 1 Distribution of brucellosis-infected cattle in
Fig. 2 Cattle brucellosis investigations, Czech
Republic, 1955-1990
Fig. 3 Brucellosis incidence in cattle, Czech Republic, 1955-2000
Fig. 4 Brucellosis incidence in man, Czech Republic, 1955-2000
Fig. 5 Bovine brucellosis control – benefit to cost ratio, Czech
Republic, 1960-1974