A country classification system to inform rabies prevention guidelines and regulations
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Journal of Travel Medicine, 2022, 1–9
https://doi.org/10.1093/jtm/taac046
Original Article
Original Article
A country classification system to inform rabies
prevention guidelines and regulations
Ronnie E. Henry, BA†, Jesse D. Blanton, DrPH*, Kristina M. Angelo, DO,
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Emily G. Pieracci, DVM, Kendra Stauffer, DVM, Emily S. Jentes, PhD, Jessica Allen,
MPH, Marielle Glynn, MSc, Clive M. Brown, MBBS, Cindy R. Friedman, MD and
Ryan Wallace, DVM
Centers for Disease Control and Prevention, Atlanta, GA, USA
*To whom correspondence should be addressed. asi5@cdc.gov
† Author deceased
Submitted 15 December 2021; Revised 16 February 2022; Editorial Decision 18 February 2022; Accepted 25 March 2022
Abstract
Background: Assessing the global risk of rabies exposure is a complicated task requiring individual risk assess-
ments, knowledge of rabies epidemiology, surveillance capacity and accessibility of rabies biologics on a national
and regional scale. In many parts of the world, availability of this information is limited and when available is
often dispersed across multiple sources. This hinders the process of making evidence-based health and policy
recommendations to prevent the introduction and spread of rabies.
Methods: CDC conducted a country-by-country qualitative assessment of risk and protective factors for rabies to
develop an open-access database of core metrics consisting of the presence of lyssaviruses (specifically canine
or wildlife rabies virus variants or other bat lyssaviruses), access to rabies immunoglobulins and vaccines, rabies
surveillance capacity and canine rabies control capacity. Using these metrics, we developed separate risk scoring
systems to inform rabies prevention guidance for travelers and regulations for the importation of dogs. Both scoring
systems assigned higher risk to countries with enzootic rabies (particularly canine rabies), and the risk scoring
system for travelers also considered protective factors such as the accessibility of rabies biologics for post-exposure
prophylaxis. Cumulative scores were calculated across the assessed metrics to assign a risk value of low, moderate
or high.
Results: A total of 240 countries, territories and dependencies were assessed, for travelers, 116 were identified as
moderate to high risk and 124 were low or no risk; for canine rabies virus variant importation, 111 were identified
as high-risk and 129 were low or no risk.
Conclusions: We developed a comprehensive and easily accessible source of information for assessing the rabies
risk for individual countries that included a database of rabies risk and protective factors based on enzootic status
and availability of biologics, provided a resource that categorizes risk by country and provided guidance based on
these risk categories for travelers and importers of dogs into the United States.
Key words: Rabies, travel health, pre-exposure prophylaxis, importation, dogs
Published by Oxford University Press on behalf of International Society of Travel Medicine 2022.
This work is written by US Government employees and is in the public domain in the US.
2 Journal of Travel Medicine, 2022, Vol. 29, 4
Introduction Country assessments were conducted primarily at a national
Reported cases of rabies and rabies exposures among interna- level; however, independent assessments of select territories,
tional travelers are rare. An estimated 0.01–2.3% of travelers dependencies or sub-national jurisdictions were also conducted.
experience a bite from a rabies-suspect animal per month of Assessments occurred over a 5-day period in February 2020
stay in a rabies endemic area.1 Since 2013, 23 cases of travel- reflective of data from the previous 5 years. Individual country
associated human rabies have been reported, three of which assessments considered the presence of three risk factors: (i)
involved US residents.2 The true burden of rabies exposures and CRVV, (ii) wildlife rabies virus variants and (iii) bat lyssaviruses
infections among international travelers is unknown. (bat rabies virus variants only present in western hemisphere or
Although rabies remains nearly 100% fatal after the onset non-rabies lyssaviruses only present in the eastern hemisphere).
of symptoms, it is preventable when appropriate post-exposure Each of these risk factors was assessed as either broadly enzootic,
prophylaxis (PEP) is administered promptly.3 The variation of the partially controlled or geographically limited, or not present in
global distribution of rabies reservoirs, particularly for canine the country. We also considered the following factors protective
rabies, and the lack of rabies biologics [i.e. vaccine and rabies against rabies:
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immunoglobulin (RIG)] in certain regions of the world result in
considerable variability in the risk of rabies exposure and severe • Quality of rabies surveillance including laboratory diagnostic
consequences for international travelers.4 Clinicians adminis- and viral characterization capacity
tering pretravel care provide their patients information about • Efforts towards control of rabies in dogs (such as dog vaccina-
reducing the risk of rabies exposure and infection including pro- tion coverage, dog population management and existence and
viding rabies pre-exposure prophylaxis (PrEP), when indicated.3 enforcement of legal codes to limit rabies transmission in dogs).
Deciding when PrEP should be given in the pretravel clinic is • Accessibility of human rabies vaccine for PEP within the coun-
a complicated process and should include an evaluation of a try.
traveler’s age, health status, length of stay, planned activities, • Accessibility of RIG for PEP within the country.
local rabies epidemiology and availability of biologics (vaccine
and RIG) in the country.5 Evidence related to risk and protective factors is reviewed on
Much of the same information used for rabies pretravel an ad hoc basis and a comprehensive reassessment of all countries
guidance can also inform animal importation regulations. Inter- is conducted every 2 years.
national importation of dogs increases the risk of introduction Because there is no single comprehensive source of infor-
or reintroduction of canine rabies virus variants (CRVVs) to mation pertaining to the factors used in these assessments,
regions where it has been eliminated.6 Since 2015, three separate a framework was developed for evaluating data elements
importation events of rabid dogs from Egypt and one from and sources (Table 1). Multiple databases were queried for
Azerbaijan were reported in the United States. These 4 events quantitative rabies surveillance data.12 –17 Published data were
resulted in 86 human exposures with an estimated cost between searched from multiple indexes [Search term: rabies AND
$800 000 and $1.6 million USD for PEP and the subsequent (country name)].18,19 Public media reports were also searched for
public health response.6–9 To prevent the reintroduction of CRVV reports of outbreaks, importation or control efforts [Search term:
in the United States, CDC regulations require dogs imported rabies AND (country name)].20 –22 Criteria were defined for the
from CRVV enzootic countries to be healthy and fully immu- evidence related to each factor and weighted as most preferable,
nized against rabies before entry into the United States.10 Local acceptable or least preferable. Most preferable evidence sources
rabies epidemiology and control measures are critical for making were quantitative in nature and publicly accessible from national
evidence-based assessments to determine importation risks in authorities, particularly when following international standards
different animal species and to determine importation require- for collection and reporting (e.g. WHO or OIE declarations of
ments for dogs. However, easily accessible and reliable country- rabies-free status). Acceptable sources included quantitative and
by-country information outlining the endemicity of rabies and qualitative data from published literature involving surveys or
the availability of biologics is lacking.11 case reports. Least acceptable sources included regional expert
We established a database using indicators including the opinion or inference based on animal reservoir distributions. For
presence and relative burden of animal rabies, availability of all evidence criteria, reviewers sought information from multiple
biologics and status of surveillance capacity by country and a sources to corroborate assessed levels where possible. In addition,
systematic scoring algorithm to help clinicians determine the national health authorities are invited to provide feedback
need for PrEP among US international travelers and to facilitate and additional evidence on any posted rabies assessments to
decisions for US dog importation regulations. trigger an ad hoc reevaluation and updates between biennial
assessments.
Methods
To assess the status of rabies globally, scientists at the Cen-
ters for Disease Control and Prevention (CDC) reviewed pub- Developing rabies risk levels for travelers’ health
licly available data, including scientific publications, government recommendations
reports, data from international organizations such as the World The database of rabies metrics described above was used to
Health Organization (WHO) and the World Organization for develop a scoring system. Scores were based on five variables
Animal Health (OIE), and information provided by national and (presence of CRVV, wildlife rabies, or bat lyssavirus and acces-
international rabies experts. sibility of rabies vaccine or RIG) for 240 locations (including
Journal of Travel Medicine, 2022, Vol. 29, 4 3
Table 1. Framework for assessing rabies criteria data
Assessment Category Guidance Domain Assessment Criteria Assessment Elements Evidence Weight
Animal Rabies Traveler’s Health and Reported Presence of National Authority (Human or Animal Health Most preferable
Dog Importation Rabies in Dogs, Agency) rabies surveillance report
Wildlife and Bats Regional surveillance report (WHO/OIE) Most preferable
Report of presence in published manuscript Acceptable
Regional expert opinion Least preferable
Reported animal source of human rabies infections Acceptable
Reported source of infection in exported human or Acceptable
animal rabies cases
Inferred based on known presence of regional Least preferable
rabies reservoir species (specifically for wildlife
species)
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Free Status: Self Freedom of dog-mediated human rabies deaths Acceptable
Declaration Freedom of dog-mediated rabies (canine variant) Acceptable
Rabies virus freedom Acceptable
Non-Rabies Lyssavirus freedom Acceptable
Free Status: WHO Validation of zero human deaths from rabies Most preferable
Declaration24 Verification of interruption of rabies transmission Most preferable
Free Status: OIE Freedom from rabies virus Most preferable
Declaration30 No case of indigenously acquired infection with Most preferable
rabies virus has been confirmed during the past
24 months
Free Status: Other WHO reports Acceptable
Declaration APHA / EU / Australia dog importation Acceptable
requirements
Biologics Traveler’s Health Rabies Vaccine National authority reports on vaccine types and Most preferable
administration rates
Regional surveys of rabies vaccine availability Acceptable
Published manuscripts regarding rabies vaccine Acceptable
administration in country
Regional expert opinion Least preferable
NGO reports and databases of rabies vaccine Least preferable
availability through private clinics
RIG National authority reports on vaccine types and Most preferable
administration rates
Regional surveys of rabies vaccine availability Acceptable
Published manuscripts regarding rabies vaccine Acceptable
administration in country
Regional expert opinion Least preferable
NGO reports and databases of rabies vaccine Least preferable
availability through private clinics
Adequate Dog Importation OIE Rabies Regular and prompt animal disease reporting Most preferable
Surveillance Surveillance Rabies virus is a notifiable disease in the entire Acceptable
Criteria30 country
Any change in the epidemiological situation or Acceptable
relevant events are reported
Animals showing signs suggestive of rabies are Most preferable
subjected to appropriate field and laboratory
investigations
Surveillance in accordance with OIE Chapter 1.4. Acceptable
and Article 8.14.12. has been in place for the past
24 months
A system to ensure investigation and reporting of Least preferable
suspected rabid animals is in place
If an imported case is confirmed, epidemiological Acceptable
investigations have ruled out the possibility of
secondary cases
Has diagnostic capability, including regular Acceptable
submission of samples to a laboratory using
OIE-recognized assays
Continued4 Journal of Travel Medicine, 2022, Vol. 29, 4
Table 1. Continued
Assessment Category Guidance Domain Assessment Criteria Assessment Elements Evidence Weight
Other Surveillance Rate of testing suspected Most preferable
Criteria rabid animals (per
100 000 population)
Rate of viral Most preferable
characterization of
rabid dogs and domestic
animals
Adequate Rabies Dog Importation OIE-Endorsed Documented evidence (including relevant Most preferable
Control Program Official Control legislation) of its capacity to control
Program30 dog-mediated rabies. This evidence may be
provided using data generated by the OIE PVS
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Pathway
Measures implemented to prevent introduction Most preferable
of infection
Dog population management program in Acceptable
accordance with OIE Chapter 7.7
Evidence (such as copies of legislation) that Acceptable
vaccination of selected populations is
compulsory and the vaccines are produced in
accordance with the OIE Terrestrial Manual
Vaccination coverage in the target population Most preferable
(>70%)
Other Control Rabies vaccination required for dogs arriving Acceptable
Program Criteria from canine rabies endemic countries
countries, dependencies and other political entities) (Table 2).23 Developing rabies risk levels for dog importation
Because most human rabies deaths are attributed to bites from regulations
rabid dogs, the presence of CRVV was weighted more heavily
A similar process was used to develop a composite score for
than the other factors.24 This was done by doubling the score
the risk of importing CRVV from a country, based on three
for CRVV compared with the maximum score for wildlife rabies.
indicators (presence of CRVV, adequate rabies surveillance and
Scoring for the presence of bat lyssaviruses was stratified between
adequate rabies control program). The composite score values
the western and eastern hemisphere. Bat rabies virus variants,
range from negative 6 to 12 with higher values representing
which are only present in the western hemisphere, were scored
higher risk. Countries were categorized into two groups
higher due to their higher association with human rabies cases.
according to their composite scores: high-risk (score 1–12),
Non-rabies lyssaviruses, which are restricted to bats in the east-
low-risk (score −6 to 0). A third group, CRVV-free (no-risk),
ern hemisphere, were scored lower due to infrequent reports of
was designated for countries where CRVV has been eliminated
human infection. We considered accessibility to rabies vaccine
(Supplementary Table S3). Dog importation requirements for
and RIG for PEP in the event of a suspected rabies exposure
each group of countries were developed to reflect federal
protective factors; therefore, they were assigned negative scores
guidelines that are available on the CDC website.25
(Table 2).
A composite score ranging from negative 12 to 21 was gen-
erated. Higher scores indicated a higher risk of rabies exposure Results
for travelers including limited accessibility to PEP. Each rabies Of 240 locations assessed in February 2020, 125 (52%) were
enzootic country was sorted into three categories according to determined to be free of CRVV, 29 (12%) had partially con-
its composite score: high/moderate risk of exposure AND PEP trolled CRVV and 82 (34%) were broadly enzootic. The sta-
accessibility limited (score 7–21), high/moderate risk of exposure tus of CRVV could not be determined in four (2%) countries
AND PEP accessible (score 1–6) and low risk of exposure AND (Supplementary Table S1; Figure 1). Rabies in wildlife was not
PEP accessible (score −11 to 0). A fourth category, lyssavirus- present in 101 countries, limited distribution in 27 and broadly
free AND robust surveillance in place, was also designated enzootic in 31 countries. There was incomplete information
representing countries that are lyssavirus-free (Supplementary available about wildlife rabies, with 81 countries being classified
Table 2). We developed recommendations for travelers based on as unknown. Bat lyssaviruses were not present in 31 countries,
the country category which appears on each country’s destina- present in 139 countries (bat rabies virus variants in 25 and non-
tion page on the CDC Travelers’ Health website (www.cdc.gov/ rabies lyssaviruses in 114), and could not be determined for 70
travel). countries.Journal of Travel Medicine, 2022, Vol. 29, 4 5
Table 2. Determinants of rabies risk and associated scores used to develop recommendations
Score Criterion
Presence of CRVV
12 CRVV is enzootic throughout country, cases reported in rural and suburban/urban settings OR surveillance insufficient to
determine status of CRVV presence
6 CRVV is enzootic in some regions of country, cases reported primarily in rural settings
0 Country is CRVV-free
Presence of wildlife rabies virus variants
6 Rabies virus variants associated with terrestrial wildlife enzootic throughout country, cases reported in rural and suburban/urban
setting OR surveillance insufficient to determine status of wildlife rabies
3 Rabies virus variants associated with terrestrial wildlife enzootic in some regions of country, cases reported primarily in rural
settings, human exposures rarely reported
0 Country terrestrial wildlife rabies virus variants free
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Presence of bat lyssaviruses
3 Bat rabies virus variants are enzootic in country OR surveillance insufficient to determine status of bat rabies virus variants
1 Non-rabies lyssaviruses are enzootic in country OR surveillance insufficient to determine status of non-rabies lyssaviruses
0 Country is bat lyssavirus-free
Availability of rabies vaccine
–6 A rabies vaccine (which meets WHO guidelines) is available for PEP within 48 h of a patient presenting for care throughout most of
the country
–3 A rabies vaccine (which meets WHO recommendations) is available for PEP within 48 h of a patient presenting for care only in
larger suburban/urban medical facilities
0 A rabies vaccine (which meets WHO recommendations) is not readily available within 48 h in country OR insufficient information
to determine vaccine availability
Availability of RIG
–6 RIG is available for PEP within 48 h of a patient presenting for care throughout most of the country
–3 RIG is available for post-exposure prophylaxis within 48 h of a patient presenting for care only in larger suburban/urban medical
facilities
0 RIG is not readily available within 48 h OR insufficient information to determine RIG availability
Rabies Surveillance Capacity
0 No reporting or inadequate reporting of animal and human rabies to OIE and WHO, no laboratory capacity for rabies diagnosis
–3 Human and animal rabies surveillance data reported publicly to WHO and/or OIE, recognized laboratory rabies diagnostic capacity
Canine Rabies Control Capacity
0 No large-scale vaccination efforts conducted on a routine schedule
–3 Large-scale vaccination efforts to reach ∼70% of the susceptible dog population are held annually and intermittent or introduced
cases are only sporadically detected in focal parts of the country
WHO, World Health Organization; RIG, rabies immunoglobulin
There was some level of PEP accessibility in the majority of
countries. There was high vaccine access (defined as available in Discussion6 Journal of Travel Medicine, 2022, Vol. 29, 4
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Figure 1. Geographic distribution of canine and wildlife rabies virus variants and bat-associated lyssaviruses, 2020. ∗ Diagonal line-filled area indicates
territory of Western Sahara
Figure 2. Geographic distribution of rabies protective factors (rabies biologics access, surveillance and canine rabies control capacity), 2020.
∗ Diagonal line-filled area indicates territory of Western SaharaJournal of Travel Medicine, 2022, Vol. 29, 4 7
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Figure 3. Geographic distribution of assessed rabies risk levels for travel health guidance (a) and dog importation (b), 2020. ∗Diagonal line-filled area
indicates territory of Western Sahara.
countries. Clinicians should visit the CDC Travelers’ Health web- Importation of CRVV into the United States is a concern and
site destination pages for the most up-to-date recommendations could significantly impact the ability of federal and state health
for rabies vaccination. As annual updates are provided, country partners to control the spread of rabies within the United States.
classifications are also available on the CDC Rabies website The importation of CRVV can have deadly consequences for
(www.cdc.gov/rabies/resources/countries-risk.html). humans, pets and wildlife.6 Since the elimination of CRVV in the
In 2018, WHO updated recommendations for PrEP, reducing United States in 2004, importations of rabid dogs infected with
the schedule from 3 doses administered over 21 days to 2 total CRVV have cost public health systems hundreds of thousands of
doses of vaccine administered on Days 0 and 7.24 The evidence dollars per event.6 –8 On 14 July 2021, CDC issued a temporary
for this new recommendation has been reviewed by the US suspension for dogs arriving from CRVV high-risk countries
Advisory Committee on Immunization Practices (ACIP) and was using existing regulatory authorities under 42 CFR 71.51 and 42
approved in February 2021.27 The new two-dose rabies PrEP CFR 71.63. The suspension was necessary to halt the increase of
schedule will likely increase accessibility of rabies PrEP for US fraudulent and incomplete rabies vaccination certificates docu-
travelers by reducing the cost and allowing the series to be mented in 202028 and to ensure the health and safety of dogs
completed in 7 days (as opposed to 21 days previously). imported into the United States while protecting the public’s8 Journal of Travel Medicine, 2022, Vol. 29, 4
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