TITLE: AN EPIDEMIOLOGICAL RETROSPECTIVE STUDY OF RABIES
DIAGNOSIS AND CONTROL IN ISRAEL, 1948-1997
AUTHORS: B. Yakobson*, D. L. Manalo**, K. Bader***, S. Perl*, A. Haber*1, B.
Shahimov*, N. Shechat* and U. Orgad*
*. Department of Pathology, Kimron Veterinary Institute, Beit Dagan, Israel
**. Philippines, International MPH Program, The Braun School of Public Health and Community Medicine,
The Hebrew University-Hadassah, Jerusalem, Israel
***. Al Quds University, Palestinian Authority
Summary
The only rabies diagnostic center in Israel is located at Kimron Veterinary Institute,
belonging to the State Veterinary Services. Animal rabies records from the center
were analyzed to provide an epidemiological summary of 50 years diagnostic activity.
Human post-exposure treatment (PET) data, supplied by the Ministry of Health, were
included in this review. A total of 2243 rabies cases were diagnosed between 1948
and 1997. Rabies occurred in almost all parts of the country with an apparent
clustering in the North. Monthly or seasonal patterns were not apparent when the data
of 50 years were analyzed for all animal species, nor when the data were grouped into
ten-year intervals. When farm animals and fox-jackal cases were analyzed separately
a pattern did emerge where fox and jackal numbers rose gradually from April to peak
in October, followed by a decline and a minor peak in February. Farm animals
followed the same pattern with each peak occurring two months after the fox-jackal
peaks. Dogs comprised 50% of the animals diagnosed as rabid over the 50 year
period, while most of the rabid, dogs were identified before 1958 and were mainly
urban. From the mid 1970s, sylvatic rabies supervened, and rabid foxes accounted for
49% of all diagnosed cases between 1988 and 1997, establishing that foxes are
currently the main reservoir of rabies virus in Israel.
Despite the implementation of rabies control measures, such as compulsory dog
vaccination, elimination of stray dogs and cats and quarantine of suspected rabid
animals, the prevalence of rabies in domestic animals has remained static over the
past 30 years. Three cases of human rabies in 1996 and 1997 have highlighted the risk
of virus transmission if contact occurs between peoples and unvaccinated domestic or
wild animals. The cost of rabies control activities and post-exposure treatment
presents a high financial burden to the state.
In Israel control of rabies requires concerted efforts in three areas. Firstly,
increasing the vaccination coverage of dogs to over 70%, introducing obligatory cat
vaccination and establishing a national register with electronic identification.
Secondly, to implement an oral vaccination program for wildlife which would include
monitoring fox and jackal populations, and thirdly, to extend the comprehensive
rabies control program throughout the region to include Egypt, Israel, Jordan and the
Palestinian Authority.
Introduction
Rabies has been described in the Middle East since Biblical times and its Hebrew
name, "Kalevet", was coined at the start of this century by the physician, Beham (1),
who established the Jerusalem Pasteur Institute in 1913 (2). Its rabies department
reported that between 1914 and 1920, 1414 people were bitten (925 by dogs, 197
foxes,188 cats, 6 wolves and 98 others animals) and 198 people received postexposure treatment. On microscopic examination, 26 cases were diagnosed positive
for rabies (3). The Central Laboratory of the Department of Health of the Government
of Palestine began to keep records on the frequency of the disease in the 1920s and
1930s. These and subsequent data were analyzed by Goor (4), who documented 2207
cases of rabies between the years 1930 and 1947 (annual average of 122) as follows:
dogs accounted for 67%, cats 12,1%, jackals 10,2%, horses and donkeys 5%, oxen
3,3% and others 1,7%. Between 1923 and 1946 at least 75 people died from the
disease (4). Soon after the establishment of the State of Israel in 1948, the Kimron
Veterinary Institute (KVI) assumed responsibility for rabies diagnosis in animals and
subsequently also for the confirmation of fatal human cases. Nobel and Neumann (5),
Perl et al. (6), Klopfer et al. (7) and Bader (8) have described epidemiological trends
up to 1980. In 1949-1961, dogs and cattle were the most commonly affected domestic
animals, and the jackal and mongoose among the wild animals (5). In 1971, foxes
replaced jackals as the most commonly affected wild animal (6). Between 1980 and
1994 fox cases reached 45.8%, while dog cases were 28.6% (7). Shimshony has
recently reviewed the role of the fox as a vector (9).
The epidemiology of rabies and its trends in Israel have changed over the past 70
years. This retrospective analysis of rabies diagnosis deals with the period of 1948 to
1997, looking at case distribution by animal species, geography, and monthly and
seasonal variations. Rabies control activities and their impact on rabies cases were
also examined in this study.
Legislative rabies prevention and control by the Israel Veterinary Services are
based on the Rabies Ordinance 1934 (Ordinance to Provide For the Prevention of
Rabies), revised in 1943, 1957, 1991 and 1992 (10). Rabies remains a significant
public health concern in Israel. In 1996-97, three humans succumbed to the disease,
after 26 years in which no human cases occurred.
The economic aspects of rabies and of related control activities were evaluated in
1988 (11). The total nation-wide expense for 1988 was estimated at US$5,225,000, of
which 84% was the cost of control activities carried out by municipal veterinary
services. The expenses for rabies diagnosis by the Veterinary Services and Animal
Health Division were estimated at US$273,000. Livestock vaccination costs were
approximately US$190,000 and an additional US$11,000 were attributed to losses
from quarantine of suspected farms. The annual cost of post -exposure treatment of
humans, carried out by the Ministry of Health was US$ 316,000 in 1988. This figure
rose to US$ 3,428,000 in 1997.
Recurrence of rabies in people prompted the Ministries of Health and Agriculture and
the National Reserve Authority to reconsider rabies as a priority zoonosis. Active and
intensive surveillance is being carried out and budgets have been allocated to research
on rabies prevention, especially in wildlife.
Sylvatic rabies is a serious zoonotic problem in many countries of the world,
including Israel. Successful national disease control program require several basic
coordinated and scientifically-based operative steps. These include the collection,
mapping and processing of epidemiological data with rapid dissemination among
veterinarians, public health officials, National Parks Authority personnel, and the
general public. These steps are essential for implementing a regional Middle East
rabies control in accordance with World Health Organization recommendations (12).
Materials and Methods
Data were collected retrospectively from the records of Kimron Veterinary
Institute’s Pathology department which conducts rabies testing free of charge. The
department keeps records of every animal submitted for rabies examination, the
species and origin, and, if the animal had bitten, the names of the bite victims and the
date of the incident. The records of the positive cases from 1948 to 1997 were entered
in MS-Excel and analyzed by SPSS.
Distances between the diagnostic center and locations of rabies cases were
determined by SPSS analysis of measurements on a 1:500,000-scale map of Israel.
Data on rabies control programs and activities were obtained from the Veterinary
Services’ annual reports.
Data on human post-exposure treatment (PET) between 1963 and 1997 were
obtained from the Epidemiology Unit of the Ministry of Health (MOH). In Israel, the
decision to begin PET is the legal responsibility of MOH district physicians. Persons
in contact with suspected rabid animals are referred to district offices and data of each
incident are recorded. PET is recommended according to the circumstances of the
exposures and MOH guidelines (12). The MOH distributes the vaccine free of charge.
The frequency distribution for the past 50 years were determined and grouped into
10-year intervals and proportions were calculated.
Results
Animal Rabies Cases and Submissions
Figure 1 shows the number of animal submissions and confirmed positive cases
over the 50-year period. Submissions increased more than thirteen fold between 1948
and 1997, from 200 to 2700, with the greatest annual increases in 1954, 1990 and
1997. The number of animal submissions in 1997 was twice that of the previous year,
as a consequence of the deaths in 1996-97 of three people from rabies. Nevertheless,
there was no correlation between the increased number of submissions and the
number of positive cases. Figure 2 shows the reduction in the positivity rate from 50%
in the years 1948-1956 to a current rate of 5%.
Figure 1. Animal Submissions and Positive Cases in Israel, 1948-1997
Figure 2. Positivity Rate of Animal Rabies Cases Israel, 1948-1997
Figure 3 shows the distribution of animal rabies cases over five decades. The highest
number of cases occurred between 1948 and 1957. Thereafter fewer cases occurred,
reaching a minimum in 1968-1977. However, during the last decade a clear increase
in the number of rabies cases can be observed, despite a decrease in the positivity rate.
Figure 3. Distribution of Animal Rabies Cases, 1948-1997
Figure 4 plots the number of positive animal cases, grouped according to the distance
from the rabies diagnostic center. Considering that the positivity rate is about 5%,
these results demonstrate that distance does not hinder the submission of animals for
diagnosis. Similar results were obtained when the data were analyzed by 10-year
intervals.
Figure 4. Comparison of the Number of Positive Animal Cases with the Distance from the KVI
Rabies Diagnostic Center (Beit Dagan)
Geographical Distribution of Animal Rabies 1948-1997
From the cumulative data of 50 years, Zefat district had most (10%) of diagnosed
positive animals. However, when the data were analyzed in decade, different districts
predominated at each interval, and no single district predominated in the number of
cases. In the first decade, Hasharon, which is located in the center of Israel, had the
most diagnoses, accounting for 13% of the total cases. In the last decade, Beer Sheva,
a district in the South, had the highest number of cases, 22.3% of the diagnoses.
Monthly and Seasonal Variation of Rabies
No monthly or seasonal pattern emerged from the cumulative data of 1948 to 1997,
ever when the cases were grouped in 10 year intervals. However, a pattern did emerge
when farm animal and fox-jackal cases were analyzed separately for monthly
variation (Figure 5) The number of rabies cases in wild living carnivores (foxes and
jackals) increased from April to a peak in October with a following decline and small
increase in February. In farm animals and humans the increase starts in June peaks in
December with following sharp decline and a second peak in May. The difference of
two months in peaks from vector animals to farm animals reflects the mean rabies
incubation period. Dogs and cats are not represented in this calculation as a major
change occurred during last 50 years from non-vaccinated and non-controlled stray
animals to mainly vaccinated and owned pets.
Figure 5. Frequency of Monthly Distribution of Positive Rabies Cases in Wild and Farm Animals
(Israel, 1948 - 1997).
Animal Species Distribution of Rabies
The distribution of rabies cases by animal species between 1948 and 1997 is shown in
Figure 6. Dogs accounted for almost 50% of all cases while cattle predominated
among farm animals. Figure 7 presents the distribution statistics for 1977-97, and
shows
a transition from urban to sylvatic rabies. In the last 20 years foxes accounted for 48%
of positive cases thereby becoming the major reservoir and vector.
Figure 6. Species Distribution of Rabies in Animals, 1948-1997
Figure 7. Species Distribution of Rabies in Animals, 1977-1997
The species trends in rabies cases showed an exponential growth in the number of
wild foxes, (Vulpes vulpes) and jackals, (Canis aureus) with rabies during 1985-1997.
The trend in rabid dog
numbers did not change during the same period, although an exception was observed
during 1991-1992 (Figure 8).
Figure 8. Species trends in Rabies cases (Israel 1985-1997)
The distribution of rabies among wild species, including the mongoose (Herpestes
ichneumon ichneumon), badger ( Meles meles canescens), wolf ( Canis lupus), striped
hyena (Hyaena
hyaena) and stone marten (Martes foina syriaca) is presented in Table 1.
Table 1. Rabies in wildlife species (Israel, 1948-1997)
Species
No. of Cases
%
Fox
386
69.2
Jackal
146
26.2
Badger
10
1.7
Wolf
9
1.6
Mongoose
5
0.9
Hyena
2
0.3
Marten
1
0.1
Total
557
100
Control Programs
The rabies control program in Israel comprises:
1. Rabies surveillance through diagnosis of animal and human cases
2. Animal vaccination
3. Elimination of stray animals
4. Quarantine of suspected rabid animals
Table 2. Rabies Control Activities, (Israel).
Activity
Submission for
diagnosis
Year
1948-1997
Dog vaccination 1976-1997
Annual Mean Std. Deviation
Range
Min
Max
115
1656
676
363
94414
23029
68179 135587
Cattle
Vaccination
1978-1997
36437
23000
4245
72508
Vaccination of
other animal
1976-1997
7853
6334
81
20467
Dog elimination 1976-1997
18320
2966
13109 22541
Elimination of
other animals
1976-1997
7844
2058
4747
13522
Quarantined
animals
1976-1997
4908
1636
2987
8609
Table 2 shows statistics for rabies control activities in Israel. The average annual
number of vaccinated of dogs was 94,414, cattle 36,437, and other animals - 7,853.
The number of vaccinated dogs increased between 1978 and 1997 (Figure 9), with the
highest increase occurring in 1991, i.e., 37% more than the previous year.
The number of vaccinated cattle also increased between 1978 and 1997. Cats and
horses were the only other animals vaccinated in the vicinity of rabies outbreaks, their
numbers reaching an average of 8000, which was about 5.5% of all animals
vaccinated annually in Israel (Figure 9).
Figure 9. Number of Vaccinated Animals (Israel 19781997)
Figure 10. shows the number of animals euthanized from 1976 to 1997. There was no
significant change in the number of animals destroyed over this period, however since
1991 the seems to be in decline. On average 18,322 dogs were eliminated each year.
(Table 2).
Figure 10. Number of Animals Destroyed (Israel 19761996)
The number of animals quarantined by government and municipal veterinary services
are shown in Figure 11. The number of quarantined animals has been decreasing since
1978. The annual average of quarantined animals was 4,908 (Table 2).
Figure 11. Number of Quarantined Animals (Israel 19761996)
A positive correlation was observed (r=0.8648, p<0.0005) between the number of
positive animals and numbers of dogs vaccinated, but no correlation was found
between the number of positive cases and dogs eliminated (r = - 0.4445, p=0.38). The
eliminated animals were mainly dogs and cats.
Table 3. Human Exposure to Rabid Animals (Israel, 1948-1997)
Year
No. of Positive
cases
No. of
Humans
exposed
(%)
Involvement
1948-1957
940
682
72.6
1958-1967
358
166
46.5
1968-1977
149
44
32.1
1978-1987
205
15
7.3
1988-1997
591
119
20.1
Total
2243
1026
48.4
Table 3 shows that human exposure was registered in about 50% of animals
diagnosed as rabies positive. The highest rate of involvement occurred in 1948-1957
(72.6% of positive cases). Subsequent there were decreases in both the number of
submissions of animals and the degree of human involvement. In 1997, following the
death of 3 people from rabies, the number of people who consulted and received
treatment for possible rabies exposure increased by a factor of 2.3. However the
percentage of those treated remained at 10 %. The Ministry of Health reported that
4400 of the 5000 people who received post-exposure treatment in 1997 had been
exposed to dogs and cats ( Figure 12).
Figure 12. Reported Number of Human Post-exposure Treatments (Israel, 19911997)
Discussion
This report analyses data of animal rabies records obtained from passive rabies
surveillance. Domestic animals submitted for rabies examinations have usually bitten,
scratched or attacked humans. Wild animals, mostly foxes and jackals, with unusual
behaviour are brought to the diagnostic center by National Reserve Authority
personnel. The total number of submissions for rabies diagnosis has increased tenfold
since 1948. This is probably due to the increase in local human and animal
populations, increased public awareness and the fact that rabies diagnosis is free of
charge. The Rabies Diagnostic Center at Kimron Veterinary Institute is located in the
center of the country and is easily reached. Our records show that geographic distance
has not prevented submission of animals.
The positivity rate, which is the proportion of rabies-positive submissions within
the total number of animals submitted for diagnosis, is not indicative in the current
study; it is the absolute number and distribution of positive cases by animal species
which reflects the epidemiological situation.
The highest number of cases was registered during the first decade (1948-1957).
Dogs were the most commonly affected animals and this held true until the third
decade, a situation still existing in neighboring Jordan (13). Studies of rabies in the
USA also indicated that dogs constituted the majority of the cases in the early 1950s
(14,15). The implementation of the Rabies Ordinance, mass poisoning of jackals
throughout the country, and compulsory vaccination of dogs initiated in 1957,
resulted in a 62 percent decrease in the number of cases during the subsequent ten
years. The Rabies Ordinance legislates compulsory vaccination of animals,
elimination of stray animals and quarantine of suspected rabid animals.
From the mid 1970s a major transition from urban dog rabies to sylvatic fox rabies
occurred and the total number of positive cases increased significantly (7). In 1991
there was a high percentage of dog rabies (73.5%) in Israel, probably due to the Gulf
War in January 1991, when many residents of the metropolitan Tel Aviv area
evacuated their homes and abandoned their pets, resulting in a large stray dog
population and a resurgence of urban rabies (9). Intensive control measures were then
implemented (16), the number of vaccinated, eliminated and quarantined animals
increased and urban rabies was successfully eliminated within several years. In the
last quarter of 1996, the first human case for 26 years occurred. Media coverage
increased awareness of the disease and the number of submissions in 1997 rose
sharply. Public awareness and fear, improved accessibility to veterinary and public
health services, and free-of-charge diagnosis resulted in many submissions that were
not backed by substantial clinical evidence. These included submissions of caged pet
mice, hamsters, guinea pigs, and young kittens that had scratched or bitten young
children. Consultations and treatment for possible rabies exposure increased by 2.3,
however the number of people who received treatment did not change.
Between 1976 and 1997, foxes accounted for 46% of rabies cases whereas jackals
accounted for only 4%. The increase of disease in foxes is probably the result of
human intervention. In the late 1950s the jackal population was decimated by
countrywide poisoning, and the fox population replaced the jackal. This has been
proposed as the reason for the reemergence of the fox as the reservoir and vector of
rabies in Israel. However, it is possible that the apparent absence of rabies in foxes
between 1949 and 1970 was a result of misclassification of foxes as jackals.
Urbanization and agricultural development have resulted in increase in untreated
garbage dump, which are a food source for wild canidae, whose population density
has increased as a result of the enhanced carrying capacity of their habitats. This
animal overload is a major factor in the incidence of rabies in Israel. The close contact
between the habitats of humans, foxes and jackals is a major factor in transmission of
the disease to domestic animals.
Cattle are the major domesticated species of economic importance affected by
rabies. In Israel rabies transmission often involves a carnivore-bovine link. Voluntary
immunization of cattle against rabies started in 1970; in 1997 the number of
vaccinated animals reached 72,000, which is 25% of the Israeli cattle population.
The Israel rabies control program is comprehensive compared to its neighbors. In
the West Bank and Gaza there is no active dog vaccination program (8); the only
control measure is stray dog removal conducted in response to complaints of residents
It is well documented that vaccination of pets is perhaps the most effective measure
to control rabies (17-20). Dog vaccination coverage in Israel is estimated at 60% (9)
which falls short of the WHO required recommended vaccination coverage of at least
70%. The number of vaccinated dogs has increased from 1976 to 1997. However,
there is a positive correlation between the number of positive cases and the number of
vaccinated dogs as most positive cases of rabies are in wild animals, and oral
vaccination of foxes and jackals has not yet been implemented.
The Rabies Ordinance (10) requires that an animal that has bitten a person be
quarantined for ten days. If the animal shows clinical signs of rabies, it must be
euthanized and the brain submitted for laboratory diagnosis. Stray dogs or
unvaccinated dogs aged six months and older in areas of an outbreak must be
destroyed (21). Smith has stated that the removal of stray animals is an effective way
to control rabies (22). In Israel, between 1976 and 1996, the number of dogs removed
was negatively correlated to the number of animal rabies cases.
Monthly or seasonal patterns were not evident when cumulative data encompassing
all species were summarized, nor when the data were grouped in ten-year intervals.
When data for foxes and jackals were analyzed as a group, a monthly pattern did
emerge. Seasonal variation has been reported in Europe; cases increased during the
winter when foxes breed (23) and during summer when they migrate to new habitats
(24). During these seasons contact and fighting among animals increase the
transmission of rabies virus. In summer there is also an increase in the young fox
population, that is more susceptible to infection (25). In Alaska, Canada and Russia,
rabies only occurs during the winter (26).
Rabies is endemic in some districts of Israel. In the first three decades, the majority
of cases were found in the north and west of the country. In the last decade, 19881997, rabies predominated in the southern part of the country (27). Since 1948, rabies
has been diagnosed throughout the country with annual clusters of cases in certain
areas. For the last 20 years the densely populated and urbanized coastal area has been
almost rabies free, with the exception of 1991-1992.
The proportion of people who started PET was positively correlated with the
number of animal rabies cases (r=0.6699, p<.0005). Only 10-15% of the people
consulted for possible rabies exposure were advised to undergo PET which indicates
that people have developed a high rabies awareness and seek consultation following
any sort of animal contact.
Ministry of Health regulations strictly conform to WHO PET guidelines. The
decision to treat a person exposed to a suspected rabid animal is made by of the
government physician. In Israel PET is free of charge which allows the patient to
receive full treatment if needed without any financial constraint, unlike in some
developing countries were the high cost of PET may be a limiting factor.
Treatment of people for rabies in Jerusalem began in the 1920s (2, 3). The first
human rabies vaccine used in Israel was grown in nervous tissue. It was replaced by
the duck egg vaccine in the 1970s, which caused minor anaphylactic reactions (28). In
the 1980s, the PDEV vaccine was replaced by a highly antigenic rabies vaccine grown
in human diploid cells (HDCV) and known to be safe and effective in eliciting
protective antibodies (29,30). The rabies immunoglobulin used in Israel is of human
origin, it is costly and available only through regional health officers.
Acknowledgment
We would like to thank Prof. A. Robinson for his advise on preparation of this article, Drs. O. Fridgut
and M. Malkinson for editing the manuscript and Dr. Y. Grinberg for helping with the historic
materials.
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