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Wildlife Pathogen Surveillance in Israel to Inform Human and
Animal Infectious Disease Control: a Prioritization Exercise
Lapid, R.,1* King, R.,2 Yakobson, B.,3 Shalom, U.4 and Moran-Gilad, J.5,6
Hai Park Zoo, 79th Ha-Hashmonaim Street, Qiryat Motzkin, 2633761, Israel.
Science and Conservation Division, Israel Nature and Parks Authority, 3rd Am Ve’Olamo Street, Jerusalem, 95463, Israel.
3
Kimron Veterinary Institute, Bet Dagan, 50250, Israel.
4
Pest Surveillance and Control Division, Ministry of Environment Protection, Jerusalem, Israel.
5
Public Health Services, Ministry of Health, Jerusalem, Israel.
6
Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel.
1
2
* Corresponding author: Dr. Roi Lapid, Hai Park Zoo, Qiryat Motzkin, 2633761, Israel. Tel: +972-54-4986652. Email: lapid220@gmail.com.
AB S T RAC T
In December 2013, as a part of the establishment of the ’Israel Wildlife Diseases Surveillance’(IWDS)
Program, building on the ‘One Health’ approach for human, livestock and wildlife disease control,
a prioritization exercise using a validated risk analysis method was carried out by distributing online
questionnaires to 86 relevant experts. The results were subsequently presented in the prioritization of a
wildlife surveillance workshop, compiling the risk assessments of 51 pathogens by human, livestock, wildlife
and total risks. The endemic diseases, brucellosis, rabies and foot and mouth disease ranked as the highest
risks. The Risk Analysis method was used successfully in the prioritization exercise. Furthermore, the results
combined surveillance priorities of relevant stakeholders and will be used in planning and implementing the
national surveillance program.
Keywords: Surveillance; Wildlife; Pathogen; Israel; One Health; Risk Analysis; Surveillance
Program.
INTRODUCTION
Emergence and reemergence of infectious diseases has occurred globally over the last decades. The majority (60%) of
emerging infectious diseases in humans are zoonotic diseases and 75% of them are of wildlife origin (1).This global
phenomenon is a result of varying processes. Exponential
growth in human population and livestock together with
habitat destruction of wildlife increased the interface between wildlife, human and their livestock. Furthermore, the
increased transport of livestock and animal products, tourism,
global trade, climate change and emergence of pathogens
resistance to antimicrobial drugs are all contributors to this
phenomenon (2).
The understanding that the health of human, livestock,
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wildlife and the environment are connected to each other is
expressed in the ‘One Health’ approach (3). This approach
was initiated in 2004 and subsequently adopted by the World
Health Organization (WHO), World Organization of
Animal Health (OIE), Food and Agriculture Organization
of the United Nations (FAO), World Bank and the Wildlife
Disease association (WDA) (4). According to the One-Health
approach, dealing with the increment of the emerging diseases
mandates ongoing nationwide wildlife surveillance (4).
Early detection of emerging diseases allows implementation of preventive measures to avoid the spread of disease in
human and livestock populations (5). For example, SARS and
avian Influenza epidemics were relatively contained due to
rapid interventions following surveillance (6). Epidemics can
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incur a heavy loss of human and animal life and also financial
damage even without counting the direct effect of morbidity
and mortality. SARS caused morbidity in only 9,000 people
but the financial damage reached about 30-50 billion US dollars (6). Without early detection epidemics could go beyond
containment and have devastating effects. For example, an
Avian Influenza Pandemic could cause 71 million deaths,
which is estimated to entail an economic significance of 3
trillion US dollars, which is 4.8% of the world Gross National
product (GNP) (6).
As a part of the establishment of an Israeli national surveillance program for wildlife pathogens, in 2013, a steering
committee including representatives from Nature and Parks
Authority, Ministry of Health, Ministry of Environmental
Protection and the Veterinary Services, Ministry of
Agriculture held a workshop that discussed the prioritization
of wildlife pathogens for surveillance for a national program.
Conducting a surveillance program for wildlife is one of
the recommendations of OIE Performance of Veterinary
Services (PVS) evaluation report of the veterinary services
of Israel (7) infectious disease threats in relation to livestock
and public health.
Prioritization is a central aspect of setting up the surveillance system and decision making regarding resource
allocations. Prioritization helps meeting the needs of the
stakeholders, maximizes the use of limited resources (fiscal
and human) and ensures that planning and resource allocation are fit-for-purpose and transparent (4, 8, 9).
Prioritization exercise in relation to zoonoses has never
been performed in Israel, neither in the veterinary nor in
the public health sectors. A review of possible approaches
and methods was initially carried out. The methods for prioritization differ mainly by the number of criteria, scoring
system and the methodology of collating results (workshops,
electronically, etc.) (8, 10, 11). A published methodology for
prioritizing pathogens for wildlife surveillance applicability
and relevance termed ‘Rapid risk analysis’ was adopted. This
methodology is based on the OIE framework and involves
hazard identification, risk estimation and ranking of the
diseases. The rapid assessment is made by using a semiquantitative system for scoring the introduction, spread and
consequences of each pathogen. The qualitative risk estimated
results are then combined to a score that can be used to prioritize pathogens for surveillance (12). Rapid risk analysis was
chosen mainly because of the relative ease of data collection
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and analysis, the ability to separate risks by different populations and adding up the populations’ risks to a total risk.
Deliberate release of pathogens was not considered in the
prioritization exercise. Malicious introductions are dependent
on complex variables some of which are profoundly different
from those associated with natural occurrence of infections
due to transmission routes of pathogens. Thus man-made
and natural incidents are difficult to prioritize one against
the other. Additionally, deliberate release involves a range of
stakeholders that is somewhat different from those represented in the current process.
The ultimate goal of the prioritization exercise was to
produce a list of wildlife pathogens that will be included,
after critical review, in the future Israeli national surveillance
program for wildlife related pathogens.
MATERIALS AND METHODS
The ’Rapid Risk Analysis’ method was chosen by the steering
committee after reviewing different options for the prioritization exercise (8, 10, 11, 12). The chosen method included
three consecutive steps: hazard identification, risk assessment
and ranking of pathogens.
For hazard identification, a list of 51 diseases (Table 1)
was formulated by the steering committee of the surveillance
program. The list was based on literature review and reportable
animal (OIE disease lists) and human diseases (per national
public health laws). The majority of the diseases were zoonotic
or affecting livestock. A disease card was prepared for each
disease based on various sources (13, 14, 15, 16, 17, 18).
The risk assessment, the scoring system of which is presented in Table 2 utilized a semi-quantitative approach to
score pathogens and included (12):
yy Probability of entry (POE) to Israel: The POE is
the release assessment. The POE depends on various
factors: route of transmission, the existence of environmental conditions that allow the survival of the vectors
and the natural hosts of the disease. The responders
were asked to consider all the potential paths that can
enable the entrance of the pathogen into Israel, including paths by which wildlife are not involved (sick
humans, transportation, imported livestock, food, etc.).
Scoring of POE had six options: 0.2, 0.4, 0.6, 0.8, 0.9
and 1. The scores of 0.2-0.8 represent the probability
of a pathogen to enter Israel and scores of 0.9 and 1
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Table 1: Diseases list (in alphabetical order)
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
38
40
41
42
43
44
45
46
47
48
49
50
51
Disease
Anthrax
Aujeszky’s disease
Avian influenza
Avian mycoplasmosis
Bluetongue
Bovine spongiform encephalopathy
Bovine tuberculosis
Bovine viral diarrhea
Brucellosis
Campylobacteriosis
Canine distemper
Caprine arthritis/encephalitis and Maedi-visna
Chronic wasting disease
Classical swine fever
Congo-Crimean Hemorrhagic fever
Cryptosporidiosis
Dengue fever
Ebola haemorrhagic fever
Echinococcosis
Epizootic haemorrhagic disease
Foot and mouth disease
Glanders
Hantavirus disease
Human granulocytic anaplasmosis
Human monocyticehrlichiosis
Japanese encephalitis
Leishmaniasis
Leptospirosis
Listeriosis
Lumpy skin disease
Lyme disease
Middle East respiratory syndrome coronavirus
Morbillivirus
Newcastle disease
Nipah virus encephalitis
Old World screwworm
Ovine chlamydiosis
Pasteurellosis
Porcine cysticercosis
Psittacosis
Q fever
Rabies
Ranavirus disease
Rift valley fever
Salmonellosis
Spotted fever (Rickettsiosis)
Swine influenza
Toxoplasmosis
Trichinellosis
Tularemia
West Nile fever
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represent pathogens that are likely to be already present in Israel or known to be present, respectively.
yy Likelihood of spread (LOS): The LOS is the exposure assessment. The likelihood that the pathogen will
become established in Israel was evaluated separately
for each of the three groups: human, livestock and
wildlife. The responders were asked to consider the
transmission patterns (routes) (animal to animal, animal to human, human to human, or via an arthropod
vector), population dispersal, survival of pathogen in
the environment, morbidity, virulence, and the rate of
spread. Scoring of LOS ranged from 1 to 4, where 1
represented a very low LOS and 4 a very high LOS.
yy Consequences of spread (COS): The COS is the consequence assessment. The COS was also evaluated for
each of the three affected groups (human, livestock and
wildlife). The responders were asked to consider the
disease incidence, morbidity and mortality (case fatality
rate), public health impact (ability to infect humans, the
ability of transmission from human to human, the ability to control spread among humans), economic effects
on production and trade, international consequences,
the ability to control the spread (diagnosis, vaccination,
treatment), and the public perception of the disease.
Scoring of COS had 4 options from 1 to 4, where 1
represented minor COS and 4 severe COS.
yy Risk estimation: For each disease and each target
group (human, livestock, wildlife) the risk was estimated as follows:
Risk (group) = POE X LOS X COS
The score of a disease risk could range between 0.2
(minimal) to a maximal score of 16.
For each disease a total risk was estimated as
follows:
Total Risk= Risk (Humans)+ Risk (Livestock)+ Risk
(Wildlife)
The score of a total risk could range between a
minimal score of 0.6 to a maximal score of 48.
yy Ranking of pathogens: After collecting questionnaire
results and calculating group risks and total risks for
all the diseases, ranking was carried out for each target
group, by total risk and by exotic and endemic diseases
(low and high POE).
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Table 2: Scoring system framework based on the ’Rapid risk analysis’ method (12)
Probability of entry to Israel
(POE)
1-Known to be Present
0.9- Likely to be present but
undetected
0.8- Very likely to enter
0.6- Moderately likely to enter
0.4- Moderately unlikely to enter
0.2- Very unlikely to enter
Likelihood of spread (LOS) and Consequences of spread (COS)
Humans
Livestock
Wildlife
LOS (1-4)
COS (1-4)
LOS (1-4)
COS (1-4)
LOS (1-4)
COS (1-4)
1- Extremely
1- Extremely
1- Extremely
1- Minor
1- Minor
1- Minor
unlikely
unlikely
unlikely
2- Moderately
unlikely
2- Moderate
2- Moderate
3- Moderately
likely
3- Major
3- Moderately
likely
3- Major
4- Extremely
likely
4- Severe
4- Extremely
likely
4- Severe
4- Extremely
likely
4- Severe
Of the 86 experts approached, responses were received from
38 (44% response rate). The majority of the responders were
veterinarians (n=27) and 15 of them held advanced degrees
JUNE 2016.indb 36
2- Moderately
unlikely
3- Major
RESULTS
Lapid R.
2- Moderate
3- Moderately
likely
The questionnaire was generated on Google formsTM
platform and was distributed electronically to 86 relevant
experts representing key stakeholders whom were chosen
by the steering committee of the surveillance program. The
questionnaire was open for response from 12/11/13 till
12/12/13. For each responder personal information was collected (name, institute, job title, academic degrees). Partial
response was allowed. The questionnaire summary was presented at the prioritization of wildlife surveillance workshop
daywhich was held at the Kimron Veterinary Institute, Bet
Dagan Israel on the 17th of December 2013.
The workshop itself was held between the 15th to the 20th
of December 2013 and engaged the steering committee of the
national surveillance program and three international experts
of wildlife diseases: Dr. Paolo Calistri (Istituto G. Caporale,
Campo Boario, Teramo, Italy), Dr. Paul Duff (Project leader
of Diseases of Wildlife Scheme, AHVLA Penrith, United
Kingdom( and Dr. William B. Karesh (Executive Vice
President for Health and Policy at EcoHealth Alliance,
New York, USA). The expert mission was funded by TAIEX
(Technical Assistance and Information Exchange Instrument
of the European Commission). Based on the Prioritization
questionnaire results and the workshop, the experts created
a policy paper with recommendations for initiation of a
national surveillance program in Israel.
36
2- Moderately
unlikely
(PhD/MPH/MSc/specialist). The rest were medical doctors
(n=5) and researchers (n=4). The majority of the responders
held governmental positions (n=24) and the rest were based
at universities (n=6), hospitals (n=3), zoos (n=3) and other
organizations (n=2). The specialization of the responders
included public health (n=10), research specialties (n=7),
wildlife (n=6), human health (n=5), livestock (n=3), pathology (n=3), bacteriology (n=3), poultry (n=2) and other areas
(n=1).
The risk estimates of the pathogens and their rankings
according to the risk assessment are presented in Table 3. The
ranking of the twenty highest risk estimates of pathogens
according to the Human risk, Livestock risk and Wildlife
risk are presented in Figures 1-3. Figure 4 presents the upper
twenty Total Risks of non-endemic pathogens which were
defined by POE as 0.6-0.8.
DISCUSSION
The objective of the prioritization exercise was to prepare for
the conception of a national surveillance system for wildlife
pathogens in Israel (IWDS). The IWDS program aims to
promote disease control in humans, livestock and wildlife.
Such an approach has never been carried out in Israel, neither
in the veterinary nor in the health sector. We adopted an
existing method of prioritization which has already been
validated (12), with certain modifications.
Human risks ranking placed Brucellosis and
Leishmaniasis the first and second highest risks. Most
of the top twenty ranked diseases are endemic to Israel.
Other diseases like Congo-Crimean hemorrhagic fever
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Table 3: Ranking of the 51 wildlife pathogens according to Total risk in descending order.
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
Disease
Brucellosis
Rabies
Foot and mouth disease
Salmonellosis
Leishmaniasis
Leptospirosis
Anthrax
Newcastle disease
Avian influenza
Campylobacteriosis
Bluetongue
Listeriosis
Q fever
West Nile fever
Echinococcosis
Toxoplasmosis
Trichinellosis
Cryptosporidiosis
Lumpy skin disease
Rift valley fever
Classical swine fever
Psittacosis
Congo-Crimean Hemorrhagic fever
Avian mycoplasmosis
Pasteurellosis
Ovine chlamydiosis
Spotted fever (Rickettsiosis)
Canine distemper
Middle East respiratory syndrome coronavirus
Epizootic haemorrhagic disease
Bovine viral diarrhea
Bovine tuberculosis
Dengue
Swine influenza
Caprine arthritis/encephalitis and Maedi-visna
Tularemia
Human monocyticehrlichiosis
Porcine cysticercosis
Hantavirus disease
Bovine spongiform encephalopathy
Lyme disease
Glanders
Aujeszky’s disease
Nipah virus encephalitis
Ebola haemorrhagic fever
Ranavirus disease
Human granulocytic anaplasmosis
Morbillivirus
Japanese encephalitis
Chronic wasting disease
Old World screwworm
POEa
1.0
1.0
1.0
1.0
0.9
1.0
0.9
1.0
0.8
0.9
0.9
1.0
0.9
0.9
0.9
0.9
1.0
0.8
1.0
0.6
0.8
0.9
0.7
1.0
0.9
0.8
0.9
0.9
0.7
0.7
0.8
0.5
0.6
0.6
0.8
0.5
0.8
0.7
0.4
0.4
0.5
0.4
0.4
0.3
0.3
0.5
0.5
0.5
0.3
0.2
0.2
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Human risk
9.7
7.7
1.0
7.4
9.6
7.0
5.1
1.3
5.6
7.3
1.1
8.0
6.8
7.0
6.1
5.6
4.4
4.4
1.0
4.3
1.0
5.3
4.7
1.3
3.2
2.3
4.0
1.4
3.9
0.9
1.0
2.7
5.5
2.4
1.0
2.9
4.1
1.8
3.0
1.6
2.0
1.4
0.8
1.1
2.3
0.7
1.9
1.4
1.8
0.3
0.4
Livestock risk
11.0
8.4
12.8
7.1
2.6
7.8
8.6
11.7
8.2
7.6
10.1
5.8
5.1
4.1
5.0
4.8
4.4
5.9
10.2
5.6
6.0
3.8
3.9
5.4
5.1
4.7
1.7
2.3
2.3
4.5
4.8
2.6
0.8
2.5
3.3
1.6
1.0
2.4
1.4
2.5
1.6
1.7
1.6
1.5
0.6
0.7
0.7
0.7
0.4
0.7
0.6
Wildlife risk
5.4
9.7
8.1
5.8
8.0
5.2
6.0
6.2
5.0
3.6
7.2
4.5
4.0
4.3
3.9
4.1
5.3
3.5
2.5
3.5
6.3
3.8
3.2
4.7
3.0
2.8
2.6
4.4
1.8
2.2
1.8
2.3
0.8
2.1
2.2
1.9
1.1
1.8
1.2
1.1
1.5
1.2
1.4
1.1
0.8
2.0
0.9
0.9
0.4
0.7
0.6
Total riskb
26.1
25.9
21.9
20.4
20.2
19.9
19.8
19.1
18.8
18.5
18.5
18.3
15.9
15.4
15.0
14.6
14.1
13.7
13.7
13.4
13.3
12.8
11.8
11.5
11.3
9.8
8.3
8.2
8.0
7.6
7.6
7.5
7.1
7.0
6.6
6.4
6.2
5.9
5.7
5.2
5.1
4.3
3.8
3.8
3.7
3.5
3.5
3.0
2.6
1.7
1.5
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Figure 1. Top 20 Human risks. Risk(H)=Human risk
Figure 2. Top 20 Livestock risks. Risk(L)=Livestock risk
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Figure 3. Top 20 Wildlife risks. Risk(W)=Wildlife risk
Figure 4. Top 20 total risks (Trisk) of non-endemic pathogens (POE=0.6-0.8).
Trisk=Total risk; POE=Probability of entry
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which have never been diagnosed in Israel are ranked lower.
For the Livestock risks, Foot and Mouth, Bluetongue, and
Newcastle diseases were ranked the highest and included
diseases from the top twenty which are endemic in Israel
or which have appeared in the in recent times (19). For the
Wildlife risks, Rabies, Foot and Mouth and Bluetongue
diseases were ranked the highest and also here in the top
twenty the majority are those diseases that are endemic to
Israel.
Total risk ranking, which is the combination of Human,
Livestock and Wildlife risks, placed Brucellosis, Rabies and
Foot and Mouth diseases as highest risks. Brucellosis, which
is a highly transmissible disease that is caused by several
Brucella species and affects a variety of mammals including
humans, is endemic in Israel but the epidemiology of the
disease in wildlife is not well known, therefore the high
ranking of the disease seems reasonable (20,21). Rabies, a
well-known viral disease that can affect all mammals is also
endemic in Israel. The prevalence of this disease in wildlife
is well studied but the mortality rate of the disease caused
the disease to be ranked high in the questionnaire (21,22).
Foot and mouth disease is also a well-known viral disease
that affects livestock and can have major economic impact.
Despite this, there are still gaps in knowledge regarding
wildlife epidemiology in Israel where the disease exists
(21,23).
Seventy five percent (15 diseases) of the top 20 Human
risks and 85% (17 diseases) of the top twenty Livestock Risks
were included in the top twenty Total risks.
As a project that involves four governmental offices, the fact that the top risks combined Human and
Livestock risks represented complementarily of purpose
and actually strengthened the project as a One-Health
targeted venture. Nonetheless, risk scores can be used for
ranking pathogens within One-Health sector or across
all sectors which can help to target specific issues and
diseases.
The probability of entry (POE) has major influence on
the risk estimation. As a national surveillance program, it
was envisaged that exotic pathogens would also be monitored. The top twenty exotic pathogens, which were defined
by a POE between 0.6 to 0.8 (moderately likely to highly
likely to enter), showed some variance. From diseases like
Classical Swine Fever that have been circulating in the
past in Israel (19) to Middle East Respiratory Syndrome
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coronavirus that is a newly emerging disease in bordering
countries (24) and to the Rana virus which is restricted
to amphibians and has never been reported in Israel. The
ability to differentiate between endemic to exotic pathogens
risks will aid in decision making concerning the relative
weight of exotic pathogens versus endemic pathogens in
the surveillance program.
A notable limitation of this study may have been a
lack of balance between different One Health disciplines
among the group of responders. In addition, some of the
responders are not involved in policy making and thus
further critical validation of the risk assessments was
required by the steering committee. This is important as
a means to provide credibility to the results and ensure
acceptability (12).
The next stage will be to consider costs and practicability of surveillance systems for the high-priority pathogens.
Each of the high priority pathogens will be discussed by the
steering committee and the stakeholders and decisions will
be made regarding the inclusion in the surveillance program.
For example: Foot and Mouth disease is a well-known disease
but the role of wild boars in the epidemiology of the disease
is not well understood and thus it is highly likely that this
disease will be included in the surveillance program. On the
other hand, campylobacteriosis is ranked high in the total
risk but the source of the disease being poultry is already
well-known and is already surveyed in other programs and
thus it is unlikely that this disease will be included in the
surveillance program. In addition, wildlife sampling is logistically demanding and sampling for different pathogens
simultaneously is expected to improve the efficiency of the
surveillance (12).
In conclusion, using a modification of the Rapid Risk
Analysis method for prioritization of pathogens, the Israel
Wildlife Diseases Surveillance (IWDS) program steering
committee successfully performed the first prioritization
exercise in Israel. The questionnaire results showed a good
representation of Human and Livestock risks by grading
diseases that are both zoonotic and livestock related and thus
strengthening the program as a ‘One-Health’ orientation.
The results will be further discussed and decisions will be
made by the steering committee and stakeholders as to which
pathogens will be included in the surveillance program with
emphasis placed on pathogens of public and livestock health
importance.
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ACKNOWLED GMENTS
The authors would like to thank the responders of the questionnaire
and the participants of the workshop. We would also like to thank
executives from the Nature and Parks Authority, Veterinary Services
and the Ministries of Health, and of Environmental Protection for
the initiation of this project. We would like to thank TAIEX for
founding the participation of the international experts and special
thanks to Dr. Paolo Calistri, Dr. Paul Duff and Dr. William B.
Karesh for their participation in the workshop and their contribution to the initiation of the surveillance program.
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