Rabies is a highly virulent, globally distributed viral encephalitic zoonotic disease. The major etiological agent, rabies virus (RABV), belongs to the Lyssavirus
] and is the only Lyssavirus species found in the Americas, where it circulates mainly in bats and mesocarnivores [2
]. The virus is most commonly transmitted by bite exposure, with virus-laden saliva being introduced directly into the host through broken skin [3
]. The clinical syndrome is variable with the disease presenting as either furious or paralytic [5
]. Bat-transmitted rabies differs from canine-transmitted rabies, with the latter manifesting more encephalitic symptoms (hyperactivity and dysautonomia) typical of furious rabies, compared to the more peripheral symptoms (ascending flaccid paralysis) of the former [7
]. Genetically, two major viral clades occur in the Caribbean: the cosmopolitan and the American clades [8
]. The cosmopolitan clade consists of canine-maintained and canine-derived viruses, the latter resulting from spill-over and maintenance of canine-maintained lineages in neo-tropical mesocarnivores [9
]. Canine-maintained viruses are disseminated as canine-transmitted rabies, which was first noted in the Americas during the 18th century [10
] after being introduced during European colonization with the importation of domestic dogs [11
]. Alternatively, phylogenetic, historical, and archaeological evidence suggests that the existence of bat-maintained rabies viruses, which falls within the American clade, predated European colonization of the New World [9
]. Early reports indicate the presence of vampire bats that attacked Spanish colonists and likely fed on wildlife before the introduction of domestic livestock [14
], which provided an abundant, readily-available resource for the expansion of vampire bat populations [16
]. However, vampire bat-transmitted rabies in humans was only diagnosed during the beginning of the 20th century on the island of Trinidad [17
], with later reports from countries in Central and South America [18
]. With the concomitant decline in canine-transmitted rabies towards the end of the 20th century, these bats are now recognized as a major reservoir for RABV [20
]. Rabies affects public, animal, and ecosystem health, and, as such, it is recognized as a key One Health issue [16
]. With such issues, interventions are possible from many angles. However, in the case of rabies, intervention at the human health interface is unpredictable and very expensive; therefore, the most effective strategy is to target the animal source [16
]. Prevention and control measures consequently mainly focus on the protection of susceptible animal populations through vaccination schemes, import control, and source reduction through reservoir animal population control.
In 1980, the annual average burden for canine rabies in Latin America and the Caribbean was approximately 25,000 cases in dogs and 350 cases in humans [23
]. These high case numbers prompted the introduction of a regional Pan American Health Organization (PAHO) coordinated program for the control of canine-transmitted rabies in 1983 [23
]. Since its implementation, there has been a dramatic decrease (>90%) in canine-transmitted rabies in both humans and dogs, with complete elimination in many countries [24
] due to large-scale dog vaccination and population control, increased technical cooperation between ministries of health and agriculture, and improved access to pre-and post-exposure prophylaxis [26
]. Despite these successes, which were hindered by political and economic constraints, the disease still exists in pockets in Latin America and the Caribbean (i.e. Bolivia, Brazil, Peru, Honduras, Guatemala, Haiti, Dominican Republic, and Cuba) [23
]. As such, the action plan and expected elimination date have been updated several times, with the latest revision running up until 2022 [27
]. The aforementioned regional program was launched at the first Meeting of National Rabies Program Directors in the Americas (REDIPRA), which is coordinated by PAHO and supported by numerous non-governmental organizations and public-private partnerships [28
]. REDIPRA usually meets biennially to advocate for and review existing control strategies, compare program achievements against objectives, and update the regional action plan accordingly [27
]. These meetings have been instrumental in the success of the regional program, aligning the countries towards a common goal and facilitating practical amendments to their national rabies control programs through shared experiences [29
]. As part of the regional strategy, the Regional Information System for Epidemiological Surveillance of Rabies (SIRVERA), coordinated by the Pan American Foot-and-Mouth Disease Center (PANAFTOSA), PAHO, is an essential online database that facilitates monthly reporting of rabies for countries in the Americas. This system, which has been in operation since 1969, has recently been improved and is now a searchable database that facilitates accessibility to detailed information on reported cases such as diagnosis, viral variant, and aggressor animal species [30
]. Although no information is collected on the type of surveillance method employed to capture cases, in Latin America and the Caribbean, as in other areas within the Americas, passive surveillance based on exposures and clinical suspicion may account for the majority of cases [31
]. PAHO provides recommendations for active surveillance within canine populations [21
]; however, they currently do not provide such recommendations for sylvatic reservoirs. Laboratory-based surveillance activities in Latin America and the Caribbean are supported by PAHO/WHO Research Centers in North America [32
]. However, it has been recognized that there has been limited systematic evaluations of rabies surveillance carried out within the region [27
Generally, in discussions about rabies in the Americas in the existing literature, Latin America and the Caribbean are often grouped as one area. However, due to limited surveillance and reporting, data available from most Caribbean countries is deficient and incomplete, whereas data from Latin America is usually more readily available. Hence, rabies data from the Caribbean is usually inadequately represented in the existing literature. Rabies is one of the priority diseases of the Caribbean Animal Health Network (CaribVET), which is a non-profit organization that involves the veterinary services from 34 Caribbean countries and territories, academic institutes, and regional and international organizations [34
]. The network promotes collaborations and coordinated actions in the field of animal and veterinary public health to increase knowledge and improve the prevention and control of diseases in the Caribbean. This study, conducted by the Rabies Subgroup of the CaribVET Veterinary Public Health Working Group, therefore aims to present an analysis of the current rabies situation in the Caribbean to fill the existing gap in the literature and to examine changes in the spatio-temporal epidemiology of the disease since the 1930s.
3.1. Rabies Status and Main Animal Reservoir
Rabies was reported to be endemic in ten Caribbean countries and territories, with the dog, mongoose, and vampire bat being the main enzootic reservoirs (Table 1
and Figure 1
). On the island republic of Trinidad and Tobago, rabies was only reported to be endemic on the island of Trinidad. The other twenty countries and territories that responded to the survey (as shown in Table S1
) reported that their locality was ‘rabies-free’ or ‘non-endemic’ i.e. by the World Health Organization (WHO) criteria, no indigenous case of rabies (human or animal) was reported within the last two years in the presence of a robust surveillance system [35
]. Only 20% of these non-endemic areas indicated that a control program (i.e., import control, vaccination, and surveillance) was implemented to achieve their non-endemic status.
At the time of survey administration, responses indicated that animal rabies cases were nationally notifiable in all rabies-endemic areas but in only 85% of non-endemic countries/ territories (see Table S1
). Likewise, rabies in humans was nationally notifiable for all rabies-endemic cases, but in only 75% of non-endemic countries/territories.
3.2. Risk of Rabies Introduction
The risk of rabies introduction was considered low by the majority (60%) of non-endemic areas. However, St. Maarten and the British Virgin Islands deemed the risk to be high, whereas the remainder indicated intermediate-risk levels. Illegal importation of dogs from endemic areas was identified as a major risk for the introduction of rabies into almost all (95%) reporting non-endemic areas. For Trinidad, Guyana, and French Guiana, illegal importation of dogs and cats posed a risk for the re-introduction of canine-transmitted rabies, and wildlife migration was noted to be an additional risk with respect to sylvatic (bat-transmitted) rabies in Grenada, Trinidad, Suriname, and Belize.
3.3. Rabies Case Burden
3.3.1. Animal Rabies
As illustrated in Table 1
, in general amongst the rabies-endemic countries/territories, most animal cases (>20 cases per year) reported on the survey were from the Dominican Republic, Haiti, and Puerto Rico. Among countries where there was rabies surveillance, the fewest cases occurred in French Guiana (0–1 cases per year). No cases were reported from Suriname, where there was no rabies surveillance. In the other localities with vampire bat-transmitted rabies (i.e., Belize, French Guiana, Guyana, and Trinidad), the main animals affected were cattle. In Trinidad, small ruminant cases were also common. In other areas (Cuba, Grenada, and Puerto Rico), the majority of cases occurred in mongoose. Cats were also a notably affected species in Cuba, Haiti, and Grenada, with the latter also reporting cases in small ruminants transmitted by mongoose. Similarly, in Haiti and the Dominican Republic, where dog-transmitted rabies was prevalent, the majority of cases occurred in this species.
3.3.2. Human Rabies
illustrates the occurrence of human rabies cases within Caribbean rabies-endemic localities. Haiti had the highest human mortality with 6–10 cases estimated to be reported per year; however, sub-notification was suspected. Isolated cases were reported from French Guiana (2008), Puerto Rico (2015), and Suriname (1998). The Dominican Republic and Cuba reported cases more often, with the last reported cases being less than 5 years prior to this study. No cases were reported in Belize, Grenada, and Trinidad for at least 25 years. Guyana did not report the occurrence of any human cases in this survey. Dog and cat bites were reported to be the main source for human RABV exposure in Belize, Haiti, and Puerto Rico, and bat exposures were likewise reported in French Guiana and Cuba. In Grenada, mongoose exposures were listed as most common.
3.4. Rabies Case Definitions, Protocols, and Legislation
The existence of case definitions for suspect animal rabies cases was reported in most rabies-endemic localities (80%) but only in 20% of the non-endemic localities. Thirty percent (30%) of ‘rabies-free’ localities indicated that they had a case definition for a human rabies suspect, whereas 60% of rabies-endemic respondents had such a definition including those areas that had reported human cases. Only eight non-endemic localities (40%) reported having standard protocols in place for dealing with a suspected or confirmed animal rabies case compared to 70% of endemic areas. Likewise, 30% of non-endemic localities had protocols for dealing with a suspected or confirmed human rabies case compared to 60% of endemic rabies countries. Specific national legislation for the prevention and control of animal rabies existed in 70% of endemic and only 45% of non-endemic localities.
3.5. Rabies Virus Exposure Incidents
Human bite incidents from potential rabies animal reservoirs were reportable in 70% of endemic localities (Table S2
), with less than half of these specific to bites from bats (French Guiana, Cuba, and Belize). Dog bites in humans were reportable in French Guiana, Cuba, Haiti, Belize, and Grenada. Animal bite incidents from potential rabies reservoirs were reportable in 70% of endemic localities, with Suriname, Belize, and Cuba being the exceptions. Incidents of humans being bitten by potential rabies virus reservoirs were reportable in 45% of non-endemic areas, with dog bites being the most common type of bite incident specified and Guadeloupe being the only respondent to specify the inclusion of bat bites. Only 30% of non-endemic areas indicated that animal bite cases from other animals considered potential rabies reservoirs were reportable, with dog bites being the most common and bat bites not specified for any country.
3.6. National Agencies with Responsibility for Rabies Surveillance
All endemic localities reported having governmental departments responsible for rabies surveillance in either animals or humans. In the Spanish-speaking Caribbean (Cuba, Dominican Republic, and Puerto Rico), the health ministry was responsible for both animal (canine) and human rabies surveillance, whereas in the other endemic localities, responsibilities for animal and human surveillance were held by the agriculture and health ministries, respectively. In non-endemic areas, 35% of respondents had departments responsible for syndromic surveillance for human rabies and 50% had departments responsible for animal rabies surveillance (passive). In contrast, in rabies-endemic localities, nearly all (90%) indicated that they had governmental departments responsible for human rabies surveillance, and all reported having departments responsible for animal surveillance (although no surveillance was noted to be conducted in Suriname).
3.7. Rabies Surveillance Programs in Animal Populations
All endemic localities, apart from Suriname, indicated they conducted some form of surveillance for animal rabies. Passive surveillance was conducted in domestic and wildlife populations in all other (9) endemic areas, with testing of suspected cases for rabies virus antigens based on the reporting of clinical signs and human exposures. For example, in the Dominican Republic, an average of 2–3 (brain) samples from suspect animals was estimated to be tested per week. Active surveillance for rabies was less commonly implemented and mainly focused on rabies reservoirs in endemic areas. For the purpose of this study, active surveillance was defined as targeted sampling and testing (for antigen or antibody) of specific groups of animals based on risk factors.
Routine active surveillance was conducted in the bat and mongoose populations in Trinidad and Puerto Rico, respectively. In Grenada, mongooses killed by animals or humans were opportunistically submitted for diagnostic testing of brain tissue. Likewise, in Guadeloupe, only bats that were involved in human bite incidents were submitted to the Institut Pasteur (Paris) for testing. In Haiti, a rabies prevalence research project was being conducted in the bat population at the time of administration of this survey and a similar project in the mongoose population was pending. Similarly, in Curacao, although the disease was not endemic, a research project was reported as being implemented to test for rabies within the bat population.
3.7.3. Domestic Animals
Opportunistic (passive) rabies diagnostic testing of dogs and cats was conducted in 55% of non-endemic localities. This was based on the reporting of public health exposures and clinically suspect animals. Active surveillance in domestic animals was mainly conducted in rabies-endemic areas with meso-carnivore rabies. The stray dog population was the main target for this type of surveillance in Cuba, Haiti, and Grenada, with Cuba estimating a sample size of 0.1% of their dog population.
3.8. Animal Rabies Vaccination
As illustrated in Table 3
, with the exception of Suriname, routine vaccination programmes for various animal species were conducted for all endemic areas. The vaccine was provided free of charge in six (60%) of the rabies-endemic countries (Belize, Cuba, Grenada, Haiti, Dominican Republic, and Trinidad). Four (40%) of the rabies-endemic localities indicated that they experienced unspecified difficulties in obtaining animal rabies vaccines for routine vaccination. The main target populations for animal vaccination strategies were herbivores (mainly cattle) and domestic carnivores (mainly dogs). Dogs were the main species vaccinated in Belize, Cuba, the Dominican Republic, Grenada, and Haiti, with the highest population coverage (>90%) estimated for Cuba. Ruminants were targeted in Guyana, French Guiana, and Trinidad, with Trinidad reporting the highest estimated population coverage (70%) and Guyana the lowest (10%). Rabies vaccination was generally a recommended practice in most of these areas, as compared to being legislatively mandatory in French Guiana and Trinidad.
3.9. Human Pre-Exposure and Post-Exposure Prophylaxis (PEP)
As shown in Table 2
, pre-exposure rabies vaccination for at-risk personnel was routinely conducted in all endemic areas and included veterinarians, veterinary students, laboratory personnel, and animal health field assistants. Only 6 (30%) of non-endemic countries/territories conducted human vaccination for rabies. Immunized persons included bat researchers (Aruba and Curacao), travellers to high-risk areas (Bermuda), laboratory personnel (Guadeloupe and Martinique), and veterinarians and animal health field assistants (Turks and Caicos and Martinique). All 7 countries/territories (6 endemic, 1 non-endemic) that responded to the survey question indicated that they used modern cell culture vaccines for immunization. At the time of survey, rabies immune globulin for PEP was only available in 8 (27%) Caribbean localities, 5 (50%) endemic (as shown in Table 2
), and 3 (15%) non-endemic (Bonaire, Bermuda, and Guadeloupe). All endemic countries also had vaccine available for PEP.
3.10. Animal Reservoir Population Control Programs
National programs to control rabies animal reservoir populations were present in 70% of rabies-endemic locations. Dog spay and neuter programs were existent for population control in 50% of endemic countries. Although no rabies cases occurred, 30% of non-endemic respondents indicated that they implemented dog and cat spay and neuter programs for animal population control. These were mainly implemented by non-governmental organizations in both endemic and non-endemic countries. In two countries where vampire bat rabies was endemic, anticoagulant poisoning of these bats was conducted for population control. Similarly, at the time of survey administration, culling was also noted to be conducted for the mongoose populations in two countries where mongoose rabies was endemic.
3.11. Rabies Laboratory Diagnostics
Only Cuba, the Dominican Republic, and Puerto Rico conducted human rabies diagnostic testing, but animal testing was carried out in these three countries, as well as in Grenada, Haiti, and Trinidad. The direct fluorescent antibody test (DFA) was available in all the laboratories detailed above with the capacity for rabies diagnostics, but PCR was only routinely available for rabies diagnosis in Cuba and Grenada. The direct rapid immunohistochemistry test (dRIT) and histological techniques for rabies diagnosis were also used in Haiti. Belize, Guyana, and Suriname indicated that they expected to set-up facilities for animal rabies diagnostics within the next 5 years, and Haiti was the only country that indicated plans to set up facilities for human rabies diagnostics. Laboratories external to the Caribbean region to which samples were sent for animal rabies diagnostics included the Ministerio de Desarrollo Agropecuario Laboratory in Panama, Laboratorio Nacional de Salud in Villa Nueva in Guatemala, the Animal Health and Veterinary Laboratories Agency (AHVLA) in the United Kingdom, the Institut Pasteur de Paris in France, and the Rabies Program at the Centers for Disease Control and Prevention (CDC) in the United States of America.
3.12. National Import Health Regulations Related to Rabies
National import health restrictions related to rabies were in place for almost all rabies non-endemic and endemic localities. These applied mainly to dogs, cats, and wild carnivores and essentially included a requirement for rabies vaccination with or without rabies titre testing. In instances in which titre testing was also required, the minimum time allowed between vaccination and sample collection was most commonly one month but ranged from 3 weeks to 3 months. Most rabies non-endemic (90%) and endemic (80%) localities indicated that they had protocols in place for dealing with imported animals that did not meet their import health requirements. These mainly included re-exportation or refusal of entry (73%), euthanasia (66%), and quarantine with or without rabies vaccination (30%). For 26% of all respondents, the course of action in implementing these protocols was reported to differ between importations from OIE listed rabies non-endemic and endemic countries. Nine (30%) (4 non-endemic and 5 rabies-endemic) localities reported having a quarantine station for animal importation. Species of animals that could be housed mainly included equine (77%), dogs and cats (66%), ruminants (66%), avian (11%), and wildlife (22%). The length of the quarantine period varied according to species, ranging from 7 days (equine) to 6 months (dogs and cats).
Rabies epidemiology across the Caribbean differs from the situation in Latin America and North America. Historically, wildlife rabies in the Western Hemisphere was first suspected in this region. However, with the possible exception of Trinidad, programs for control of wildlife rabies are not as well established or consistent as those in these other regions, mainly due to financial constraints. The diversity and inconsistencies between rabies programs within the Caribbean make it difficult to establish a standard regional approach to rabies control and prevention, as was done in Latin America. More realistically, best practice guidelines for rabies control independently addressing the various RABV reservoirs can be developed based on evidence-based information and adapted to the individual epidemiological status, existing infrastructure, and available resources in the implementing country. The mongoose is one of the main rabies reservoirs in the Caribbean, but due to its absence from other regions in the Americas, it is often overlooked as a transmitting animal, which can lead to fatal consequences [102
Sustained infection of dog-transmitted rabies in areas such as Haiti, where severe economic challenges exist, presents barriers to the elimination of the disease in the region. If the goal of elimination is to be attained in such areas, consistent external support will be necessary. As noted in other regions, since short-term goals are more suited for encouraging donor investment [27
], it might be worthwhile implementing programs in phases. A minimum requirement for the certification of a country as being ‘rabies-free’ is a functional laboratory-based surveillance program. However, rabies diagnostic capacity is limited within the Caribbean, which may compromise surveillance efforts and pose challenges to national declarations of rabies freedom. Training and laboratory networking such as that facilitated by CaribVET can function to improve rabies diagnostic capacities and surveillance in Caribbean countries. Furthermore, even if the elimination of canine rabies is on the distant horizon for the Caribbean, the approach to wildlife rabies control, related to mongoose and particularly bat-transmitted rabies, is not as straightforward, and the possibility of realistic prevention and control in these populations is debatable. The latter may be a more long-term goal with the adoption of measures successfully utilized in developed countries, e.g., oral vaccination programs [103
] with the application of novel species appropriate techniques, such as vaccination of mongoose populations and perhaps vampire bats by oral administration during routine feeding and social grooming [100
]. Nevertheless, coordinated efforts towards improving rabies control in the Caribbean should be continued through networks like CaribVET, which represents an asset to the region by promoting communication, increasing awareness, developing strategies, and sharing of human and material resources between Caribbean countries.