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1.  Complex Epidemiology of a Zoonotic Disease in a Culturally Diverse Region: Phylogeography of Rabies Virus in the Middle East 
PLoS Neglected Tropical Diseases  2015;9(3):e0003569.
The Middle East is a culturally and politically diverse region at the gateway between Europe, Africa and Asia. Spatial dynamics of the fatal zoonotic disease rabies among countries of the Middle East and surrounding regions is poorly understood. An improved understanding of virus distribution is necessary to direct control methods. Previous studies have suggested regular trans-boundary movement, but have been unable to infer direction. Here we address these issues, by investigating the evolution of 183 rabies virus isolates collected from over 20 countries between 1972 and 2014. We have undertaken a discrete phylogeographic analysis on a subset of 139 samples to infer where and when movements of rabies have occurred. We provide evidence for four genetically distinct clades with separate origins currently circulating in the Middle East and surrounding countries. Introductions of these viruses have been followed by regular and multidirectional trans-boundary movements in some parts of the region, but relative isolation in others. There is evidence for minimal regular incursion of rabies from Central and Eastern Asia. These data support current initiatives for regional collaboration that are essential for rabies elimination.
Author Summary
Despite being one of the oldest recognised infectious diseases, rabies continues to cause thousands of preventable human deaths per year. As a zoonotic disease, control of infection in the reservoir has been proven the most efficient route to reduction of human cases. In some regions, the epidemiology is well understood, with either dogs or wildlife known to be the primary reservoir and with little or no movement from, or into other regions. This is not the case in the Middle East, where rabies is underreported in animals and humans, there is little laboratory confirmation of infection, and the extent of rabies spread from country to country is not known. Previous studies have demonstrated trans-boundary movement of rabies but have been limited by a low number of available samples from some countries, and the direction of spread has been difficult to estimate. Here we use rabies virus partial genome sequences of 183 viruses from over 20 countries, combined with geographical and temporal information, to reconstruct the evolution of rabies viruses circulating in the Middle East. The results reveal an apparent barrier to spread between some regions but regular movement between others. These analyses will support policy on rabies control by indicating the relative importance of local control and animal movement restrictions when allocating resources.
PMCID: PMC4374968  PMID: 25811659
2.  Rabies in Iraq: Trends in Human Cases 2001–2010 and Characterisation of Animal Rabies Strains from Baghdad 
Control of rabies requires a consistent supply of dependable resources, constructive cooperation between veterinary and public health authorities, and systematic surveillance. These are challenging in any circumstances, but particularly during conflict. Here we describe available human rabies surveillance data from Iraq, results of renewed sampling for rabies in animals, and the first genetic characterisation of circulating rabies strains from Iraq. Human rabies is notifiable, with reported cases increasing since 2003, and a marked increase in Baghdad between 2009 and 2010. These changes coincide with increasing numbers of reported dog bites. There is no laboratory confirmation of disease or virus characterisation and no systematic surveillance for rabies in animals. To address these issues, brain samples were collected from domestic animals in the greater Baghdad region and tested for rabies. Three of 40 brain samples were positive using the fluorescent antibody test and hemi-nested RT-PCR for rabies virus (RABV). Bayesian phylogenetic analysis using partial nucleoprotein gene sequences derived from the samples demonstrated the viruses belong to a single virus variant and share a common ancestor with viruses from neighbouring countries, 22 (95% HPD 14–32) years ago. These include countries lying to the west, north and east of Iraq, some of which also have other virus variants circulating concurrently. These results suggest possible multiple introductions of rabies into the Middle East, and regular trans-boundary movement of disease. Although 4000 years have passed since the original description of disease consistent with rabies, animals and humans are still dying of this preventable and neglected zoonosis.
Author Summary
Control of rabies requires cooperation between government departments, consistent funding, and an understanding of the epidemiology of the disease obtained through surveillance. Here we describe human rabies surveillance data from Iraq and the results of renewed sampling for rabies in animals. In Iraq, it is obligatory by law to report cases of human rabies. These reports were collated and analysed. Reported cases have increased since 2003, with a marked increase in Baghdad 2009–2010. There is no system for detecting rabies in animals and the strains circulating in Iraq have not previously been characterized. To address this, samples were collected from domestic animals in Baghdad and tested for rabies. Three out of 40 were positive for rabies virus. Comparison of part of the viral genetic sequence with other viruses from the region demonstrated that the viruses from Iraq are more closely related to each other than those from surrounding countries, but diverged from viruses isolated in neighbouring countries approximately 22 (95% HPD 14–32) years ago. Although 4000 years have passed since the original description of disease consistent with rabies, animals and humans are still dying of this preventable and neglected zoonosis.
PMCID: PMC3585036  PMID: 23469303
3.  The Activity of Rabies Vaccines against Genetic Clusters of Rabies Virus Circulating at the Territory of Ukraine 
To identify the presence of genetic clusters of rabies virus at the territory of Ukraine and to determine the degree of activity of rabies vaccines against these genetic clusters.
To develop and implement an effective program of rabies eradication in Ukraine in 2008 was founded the unique collection of samples of pathological materials confirmed as positive in rabies at the regional veterinary laboratories of Ukraine. The collection is constantly updated and to present moment it includes 1389 samples from all regions of Ukraine, selected from 17 animal species and humans.
Identification of the rabies virus in samples of pathological material for their further selection was carried out using the test developed by us which based on RT-PCR with primers complementary to the conservative fragments of the 5’-end of nucleoprotein gene of rabies virus.
For the study of the street rabies virus isolates from the collection we use RT-PCR with the primers pair (509, 304) flanking the variable 3’-end part of nucleoprotein gene of the reference strain of rabies virus CVS (fragment in 377 bp).
Studies of rabies vaccines activity were carried out with modified method of U.S. National Institutes of Health using rabies virus street isolates of both genetic clusters instead of the Challenge Virus Standard (CVS). All isolates of street rabies virus were inoculated in a dose of 5–50 LD50. The criteria for evaluation of protective activity of rabies vaccine was effective dose (− lg ED50).
In molecular genetic studies with variant-specific primers we established the presence in Ukraine of two clusters of rabies virus. Clusters I circulates on the right bank of the Dnipro river (the largest water barrier that divides the country into eastern and western side), and cluster II – on the left bank of the Dnieper.
The relationship of these variants with the epizootic situation was researched. For this purpose epizootological zoning of Ukraine according to the intensity of the epizootic situation in 2005–2009 was carried out. As a result of this analysis all the regions of Ukraine belong to three categories: high, medium and low epizootic situation intensity of rabies.
The projection of differentiated genetic clusters on the epizootic situation showed that cluster II circulating at Left Bank of the Dnieper in areas with high and medium intensity of the epizootic situation, and the cluster I – at the Right Bank of the Dnieper, mainly in the areas with low intensity of the epizootic situation.
That’s why our interest was in the degree of protection of rabies vaccines against street rabies virus isolates belonging to these two genetic clusters.
The commercial vaccines made with rabies virus vaccine strains SAD (Street-Alabama-Dufferin) and Wistar PM/WI were chosen to evaluate this parameter.
After the mathematical calculations of effective dose and the analysis of the data the less effective protection of rabies vaccines (at 29–30 %) against street rabies virus isolates belonging to cluster II in comparison with isolates belonging to cluster I irrespective to the strain vaccine is made was shown.
The data will be used for the effective planning of specific prophylaxis of rabies in Ukraine based on differentiated approach to distribution of rabies vaccines in according to region and their activity.
PMCID: PMC3692803
rabies vaccine; vaccine activity; street rabies virus isolates; genetic variants of rabies virus
4.  Risk of Potentially Rabid Animal Exposure among Foreign Travelers in Southeast Asia 
Each year millions of travelers visit Southeast Asia where rabies is still prevalent. This study aimed to assess the risk of rabies exposure, i.e., by being bitten or licked by an animal, among travelers in Southeast Asia. The secondary objective was to assess their attitudes and practices related to rabies.
Methodology/Principal Findings
Foreign travelers departing to the destination outside Southeast Asia were invited to fill out the study questionnaire in the departure hall of Bangkok International Airport. They were asked about their demographic profile, travel characteristics, pre-travel health preparations, their possible exposure and their practices related to rabies during this trip. From June 2010 to February 2011, 7,681 completed questionnaires were collected. Sixty-two percent of the travelers were male, and the median age was 32 years. 34.0% of the participants were from Western/Central Europe, while 32.1% were from East Asia. Up to 59.3% had sought health information before this trip. Travel clinics were the source of information for 23.6% of travelers. Overall, only 11.6% of the participants had completed their rabies pre-exposure prophylaxis, and 15.3% had received only 1–2 shots, while 73.1% had not been vaccinated at all. In this study, the risk of being bitten was 1.11 per 100 travelers per month and the risk of being licked was 3.12 per 100 travelers per month. Among those who were bitten, only 37.1% went to the hospital to get post exposure treatment. Travelers with East Asian nationalities and longer duration of stay were significantly related to higher risk of animal exposure. Reason for travel was not related to the risk of animal exposure.
Travelers were at risk of being exposed to potentially rabid animals while traveling in Southeast Asia. Many were inadequately informed and unprepared for this life-threatening risk. Rabies prevention advice should be included in every pre-travel visit.
Author Summary
Rabies is a fatal disease most commonly transmitted through a bite or a lick of a rabid animal on the broken skin. Most deaths from rabies are reported in Asia and Africa where animal rabies is poorly controlled. Not only local people, but travelers in these areas are inevitably at risk also. In this study we surveyed foreign travelers just before they departed Southeast Asia at Bangkok International Airport. We aimed to determine the risk of possible rabies exposure and their attitudes and practices related to rabies. The risk of being bitten among 7,681 participants studied was 1.11 per 100 travelers per month and the risk of being licked was 3.12 per 100 travelers per month. Among those who were bitten, only 37.1% went to the hospital to get rabies post exposure treatment. Travelers with East Asian nationalities and who stay longer were more likely to be exposed to animals. The risk of animal exposure was not related with the reason for travel. These findings confirm that travelers in Southeast Asia were at real risk of possible exposure to rabies. However, most of them were inadequately informed and unprepared for this life-threatening disease. Rabies prevention advice should be given to all travelers in rabies endemic area.
PMCID: PMC3459869  PMID: 23029598
5.  Twelve Years of Rabies Surveillance in Sri Lanka, 1999–2010 
Rabies is endemic in Sri Lanka, but little is known about the temporal and spatial trends of rabies in this country. Knowing these trends may provide insight into past control efforts and serve as the basis for future control measures. In this study, we analyzed distribution of rabies in humans and animals over a period of 12 years in Sri Lanka.
Accumulated data from 1999 through 2010 compiled by the Department of Rabies Diagnosis and Research, Medical Research Institute (MRI), Colombo, were used in this study.
The yearly mean percentage of rabies-positive sample was 62.4% (47.6–75.9%). Three-fourths of the rabies-positive samples were from the Colombo, Gampaha, and Kalutara districts in Western province, followed by Galle in Southern province. A high percentage of the rabies samples were from dogs (85.2%), followed by cats (7.9%), humans (3.8%), wild animals (2.0%), and livestock (1.1%). Among wild animals, mongooses were the main victims followed by civets. The number of suspect human rabies cases decreased gradually in Sri Lanka, although the number of human samples submitted for laboratory confirmation increased.
The number of rabid dogs has remained relatively unchanged, but the number of suspect human rabies is decreasing gradually in Sri Lanka. These findings indicate successful use of postexposure prophylaxis (PEP) by animal bite victims and increased rabies awareness. PEP is free of charge and is supplied through government hospitals by the Ministry of Health, Sri Lanka. Our survey shows that most positive samples were received from Western and Southern provinces, possibly because of the ease of transporting samples to the laboratory. Submissions of wild animal and livestock samples should be increased by creating more awareness among the public. Better rabies surveillance will require introduction of molecular methods for detection and the establishment of more regional rabies diagnostic laboratories.
Author Summary
Rabies is a public health concern in Sri Lanka. The incidence of dog rabies remains unchanged, but the incidence of suspect human rabies is decreasing gradually in Sri Lanka. This finding indicates the effects of improved access to postexposure prophylaxis by animal bite victims and increased rabies awareness. As in other rabies-endemic countries, in Sri Lanka, human rabies is transmitted mainly by dogs, although domestic and wild animals have been diagnosed rabid, and can pose a risk of exposure to humans. In this study, we analyzed 12 years of data accumulated in the national reference laboratory of Sri Lanka to identify the trends of rabies in this country. This study showed that rabies has been recorded mainly in Western and Southern Provinces of Sri Lanka, possibly because of the ease of communication with rabies diagnostic laboratories from these areas. Regional rabies diagnosis laboratories should be established to improve surveillance of rabies in Sri Lanka. There were few submitted animal samples from livestock and wild animals, indicating that greater awareness is needed among the public regarding the need to submit suspect rabid animals for diagnostic evaluation. These data could help policy makers improve rabies prevention and to control rabies in Sri Lanka.
PMCID: PMC4191952  PMID: 25299511
6.  Rabies in Nonhuman Primates and Potential for Transmission to Humans: A Literature Review and Examination of Selected French National Data 
The nonhuman primate (NHP)-related injuries in rabies-enzootic countries is a public health problem of increasing importance. The aims of this work are to collect data concerning rabies transmission from NHPs to humans; to collate medical practices regarding rabies postexposure prophylaxis (PEP) in different countries, and to provide an evidence base to support the decision to apply rabies PEP in this context.
To retrieve information, we conducted a literature search from 1960 to January 2013. All reports of rabies in NHPs and rabies transmission to humans by infected NHPs were included. Also included were studies of travelers seeking care for rabies PEP in various settings.
Data collected by the French National Reference Centre for Rabies concerning NHPs submitted for rabies diagnosis in France and human rabies exposure to NHPs in travelers returning to France were analyzed for the periods 1999–2012 and 1994–2011, respectively.
Principal findings
A total of 159 reports of rabies in NHPs have been retrieved from various sources in South America, Africa, and Asia, including 13 cases in animals imported to Europe and the US. 134 were laboratory confirmed cases. 25 cases of human rabies following NHP-related injuries were reported, including 20 from Brazil. Among more than 2000 international travelers from various settings, the proportion of injuries related to NHP exposures was about 31%. NHPs rank second, following dogs in most studies and first in studies conducted in travelers returning from Southeast Asia. In France, 15.6% of 1606 travelers seeking PEP for exposure to any animal were injured by monkeys.
Although less frequently reported in published literature than human rabies, confirmed rabies cases in NHPs occur. The occurrence of documented transmission of rabies from NHPs to human suggests that rabies PEP is indicated in patients injured by NHPs in rabies-enzootic countries.
Author Summary
No international consensus or even a consensus among existing national recommendations about rabies postexposure prophylaxis (PEP) following a nonhuman primate (NHP)-related injury currently exists. Epidemiologic studies and reports collated in this review indicate that the number of rabies case reported in NHPs are rare compared with humans. This finding might be because of a lower contact rate of NHPs with rabid reservoir but also very likely because of underreporting. Nevertheless, documented cases and subsequent transmission to humans have been reported from various sources in South America, Africa, and Asia. Further, international travelers often report NHP-related injuries and NHPs can be close to humans. Little is currently known of the pathobiology of rabies virus shedding in primates, which implies that rabies PEP and administration of rabies immunoglobulin should be considered in patients with a possible exposure.
PMCID: PMC4022521  PMID: 24831694
7.  Molecular Epidemiology of Rabies Viruses Circulating in Two Rabies Endemic Provinces of Laos, 2011–2012: Regional Diversity in Southeast Asia 
PLoS Neglected Tropical Diseases  2015;9(3):e0003645.
Although rabies is endemic in Laos, genetic characterization of the viruses in this country is limited. There are growing concerns that development in the region may have increased transport of dog through Laos for regional dog meat consumption, and that this may cause spillover of the viruses from dogs brought here from other countries. This study was therefore undertaken to evaluate the current rabies situation and the genetic characteristics of rabies viruses currently circulating in Laos.
We determined the rate of rabies-positive samples by analyzing data from animal samples submitted to the Lao Ministry of Agriculture and Forestry’s National Animal Health Centre rabies laboratory from 2004 through 2011. Twenty-three rabies-positive samples were used for viral genetic characterization. Full genome sequencing was performed on two rabies viruses.
Rabies-positive samples increased substantially from 40.5% in 2004 to 60.2% in 2009 and continued at this level during the study period. More than 99% of the samples were from dogs, followed by cats and monkeys. Phylogenetic analyses showed that three rabies virus lineages belonging to the Southeast Asian cluster are currently circulating in Laos; these are closely related to viruses from Thailand, Cambodia and Vietnam. Lineages of the circulating Laos rabies viruses diverged from common ancestors as recently as 44.2 years and as much as 55.3 years ago, indicating periodic virus invasions.
There is an increasing trend of rabies in Laotian animals. Similar to other rabies-endemic countries, dogs are the main viral reservoir. Three viral lineages closely related to viruses from neighboring countries are currently circulating in Laos. Data provide evidence of periodic historic exchanges of the viruses with neighboring countries, but no recent invasion.
Author Summary
Laos is a land-locked rabies-endemic country in Southeast Asia that is surrounded by five rabies-endemic countries. Thus, there is increasing concern that the epidemiology of rabies in Laos is influenced by infrastructure development and economic activities, including international transport of dogs for meat consumption. Studies on the epidemiology of rabies are limited in this country. Therefore, to gain further information about the epidemiology and the genetic characteristics of circulating rabies viruses, this study was conducted using samples submitted to the rabies Lao Ministry of Agriculture and Forestry’s National Animal Health Centre rabies laboratory. Out of 18 provinces, samples were submitted mainly from the capital Vientiane and Champasak province. Data from the period 2004 through 2011 showed a gradual increase in rabies-positive samples. Dogs were the main viral reservoir, and genetic analyses of samples collected from February 2011 through March 2012 showed that three viral lineages are currently circulating in the country. These rabies viruses are related to those of neighboring countries, indicating shared ancestry but no recent viral invasion.
PMCID: PMC4380407  PMID: 25825907
8.  The Phylogeography of Rabies in Grenada, West Indies, and Implications for Control 
In Grenada, West Indies, rabies is endemic, and is thought to be maintained in a wildlife host, the small Indian mongoose (Herpestes auropunctatus) with occasional spillover into other hosts. Therefore, the present study was undertaken to improve understanding of rabies epidemiology in Grenada and to inform rabies control policy. Mongooses were trapped island-wide between April 2011 and March 2013 and examined for the presence of Rabies virus (RABV) antigen using the direct fluorescent antibody test (dFAT) and PCR, and for serum neutralizing antibodies (SNA) using the fluorescent antibody virus neutralization test (FAVN). An additional cohort of brain samples from clinical rabies suspects submitted between April 2011 and March 2014 were also investigated for the presence of virus. Two of the 171 (1.7%) live-trapped mongooses were RABV positive by FAT and PCR, and 20 (11.7%) had SNAs. Rabies was diagnosed in 31 of the submitted animals with suspicious clinical signs: 16 mongooses, 12 dogs, 2 cats and 1 goat. Our investigation has revealed that rabies infection spread from the northeast to the southwest of Grenada within the study period. Phylogenetic analysis revealed that the viruses from Grenada formed a monophyletic clade within the cosmopolitan lineage with a common ancestor predicted to have occurred recently (6–23 years ago), and are distinct from those found in Cuba and Puerto Rico, where mongoose rabies is also endemic. These data suggest that it is likely that this specific strain of RABV was imported from European regions rather than the Americas. These data contribute essential information for any potential rabies control program in Grenada and demonstrate the importance of a sound evidence base for planning interventions.
Author Summary
Rabies, a fatal disease of animals and humans has been endemic in Grenada, West Indies, since the early 1900s. The small Indian mongoose, an introduced animal, is the most likely rabies reservoir, with spillover into domestic animals and humans. To control rabies, large numbers of mongooses were killed in the 1960s/1970s, but this effort did not alter long-term rabies dynamics. Vaccination of dogs, cats and livestock is efficient in protecting these animals, yet is not regularly undertaken. Post-exposure prophylaxis (PEP) in humans is routinely done and no human has died of rabies in Grenada since 1970. However, the threat of rabies and potential to adversely affect the tourism industry, are a burden on the Grenadian government and public. This study has re-evaluated the role of the mongoose in the maintenance of rabies in Grenada, and for the first time, the rabies virus circulating in Grenada has been described. Grenada offers optimal conditions for an oral rabies vaccination (ORV) program, being an island with strict live animal import controls, and a single wildlife rabies reservoir. Although further work is needed before an ORV campaign could be implemented, elimination of rabies from Grenada seems a realistic goal.
PMCID: PMC4199513  PMID: 25330178
9.  Development of a Novel Rabies Simulation Model for Application in a Non-endemic Environment 
PLoS Neglected Tropical Diseases  2015;9(6):e0003876.
Domestic dog rabies is an endemic disease in large parts of the developing world and also epidemic in previously free regions. For example, it continues to spread in eastern Indonesia and currently threatens adjacent rabies-free regions with high densities of free-roaming dogs, including remote northern Australia. Mathematical and simulation disease models are useful tools to provide insights on the most effective control strategies and to inform policy decisions. Existing rabies models typically focus on long-term control programs in endemic countries. However, simulation models describing the dog rabies incursion scenario in regions where rabies is still exotic are lacking. We here describe such a stochastic, spatially explicit rabies simulation model that is based on individual dog information collected in two remote regions in northern Australia. Illustrative simulations produced plausible results with epidemic characteristics expected for rabies outbreaks in disease free regions (mean R0 1.7, epidemic peak 97 days post-incursion, vaccination as the most effective response strategy). Systematic sensitivity analysis identified that model outcomes were most sensitive to seven of the 30 model parameters tested. This model is suitable for exploring rabies spread and control before an incursion in populations of largely free-roaming dogs that live close together with their owners. It can be used for ad-hoc contingency or response planning prior to and shortly after incursion of dog rabies in previously free regions. One challenge that remains is model parameterisation, particularly how dogs’ roaming and contacts and biting behaviours change following a rabies incursion in a previously rabies free population.
Author Summary
Rabies in domestic dog populations still causes >50,000 human deaths worldwide each year. While its eradication by vaccination of the reservoir population (dogs and wildlife) was successful in many parts of the world, it is still present in the developing world and continues to spread to new regions. Theoretical rabies models supporting control plans do exist for rabies endemic regions; however these models usually provide information for long-term programs. Here, we describe a novel rabies simulation model for application in rabies-free regions experiencing an incursion. The model simulates a rabies outbreak in the free-ranging dog population in remote indigenous communities in northern Australia. Vaccination, dog density reduction and dog confinement are implemented as control strategies. Model outputs suggest that the outbreak lasts for an average of 7 months and typically spreads through all communities of the region. Dog vaccination was found to be the most effective response strategy. The model produces plausible results and can be used to provide information for ad-hoc response planning before and shortly after rabies incursion.
PMCID: PMC4482682  PMID: 26114762
10.  Implementation of an Intersectoral Program to Eliminate Human and Canine Rabies: The Bohol Rabies Prevention and Elimination Project 
The province of Bohol, located in the Visayas islands region in the Philippines has a human population of 1.13 million and was the 4th highest region for human rabies deaths in the country, averaging 10 per year, prior to the initiation of the Bohol Rabies Prevention and Elimination Project (BRPEP).
The BRPEP was initiated in 2007 with the goal of building a sustainable program that would prevent human rabies by eliminating rabies at its source, in dogs, by 2010. This goal was in line with the Philippine National Rabies Program whose objective is to eliminate rabies by 2020.
The intersectoral BRPEP was launched in 2007 and integrated the expertise and resources from the sectors of agriculture, public health and safety, education, environment, legal affairs, interior and local government. The program included: increasing local community involvement; implementing dog population control; conducting mass dog vaccination; improving dog bite management; instituting veterinary quarantine; and improving diagnostic capability, surveillance and monitoring. Funding was secured from the national government, provincial, municipal and village units, dog owners, NGOs, the regional office of the WHO, the UBS Optimus Foundation, and the Global Alliance for Rabies Control. The BRPEP was managed by the Bohol Rabies Prevention and Eradication Council (BRPEC) under the jurisdiction of the Governor of Bohol. Parallel organizations were created at the municipal level and village level. Community volunteers facilitated the institution of the program. Dog population surveys were conducted to plan for sufficient resources to vaccinate the required 70% of the dogs living in the province. Two island-wide mass vaccination campaigns were conducted followed by “catch up” vaccination campaigns. Registration of dogs was implemented including a small fee that was rolled back into the program to maintain sustainability. Children were educated by introducing rabies prevention modules into all elementary schools in Bohol. Existing public health legislation at the national, provincial, and municipal level strengthened the enforcement of activities. A Knowledge, Attitude and Practices (KAP) survey was conducted in 2009 to evaluate the educational knowledge of the population. Increased surveillance was instituted to ensure that dogs traveling into and out of the province were vaccinated against rabies. Human and animal cases of rabies were reported to provincial and national authorities.
Key Results
Within the first 18 months of the BRPEP, human rabies deaths had decreased annually from 0.77 to 0.37 to zero per 100,000 population from 2007–2009. Between October 2008 and November 2010 no human and animal cases were detected. Increased surveillance on the island detected one suspected human rabies case in November 2010 and one confirmed case of canine rabies in April 2011. Two mass vaccination campaigns conducted in 2007 and 2008 successfully registered and vaccinated 44% and 70% of the dogs on the island. The additional surveillance activities enabled a mobilization of mop up vaccination activities in the region where the human and canine case was located. Due to the increased effective and continuous surveillance activities, rabies was stopped before it could spread to other areas on the island. The program costs totaled USD 450,000. Registration fees collected to maintain the program amounted to USD 105,740 and were re-allocated back into the community to sustain the program.
Author Summary
The Province of Bohol, Philippines has eliminated dog and human rabies in less than three years by empowering the community and implementing an intersectoral strategy. In 2006, Bohol ranked 4th highest in the Philippines for human rabies, averaging 10 deaths per year. Launched in 2007, the program utilized a social awareness campaign, dog population control, mass dog vaccination campaigns, improved dog bite management and veterinary quarantine, a new diagnostic laboratory, expanded surveillance, and the inclusion of education modules into the school curriculum. Improving community compliance to existing national and provincial rabies laws and engaging volunteers to help conduct the project was a key to success. The program, led by the Governor of Bohol, was administered through a group of departments working together at a provincial and local level, and supervised through the Office of the Provincial Veterinarian. Financial support came through the Governor and several NGOs including the Global Alliance for Rabies Control. The program is self-sustaining, through a small dog registration fee fed back into the program, through the continuing education of children in their classrooms, and through the dedicated efforts of over 15,000 staff and volunteers throughout the island.
PMCID: PMC3516573  PMID: 23236525
11.  Eliminating Rabies in Estonia 
The compulsory vaccination of pets, the recommended vaccination of farm animals in grazing areas and the extermination of stray animals did not succeed in eliminating rabies in Estonia because the virus was maintained in two main wildlife reservoirs, foxes and raccoon dogs. These two species became a priority target therefore in order to control rabies. Supported by the European Community, successive oral vaccination (OV) campaigns were conducted twice a year using Rabigen® SAG2 baits, beginning in autumn 2005 in North Estonia. They were then extended to the whole territory from spring 2006. Following the vaccination campaigns, the incidence of rabies cases dramatically decreased, with 266 cases in 2005, 114 in 2006, four in 2007 and three in 2008. Since March 2008, no rabies cases have been detected in Estonia other than three cases reported in summer 2009 and one case in January 2011, all in areas close to the South-Eastern border with Russia. The bait uptake was satisfactory, with tetracycline positivity rates ranging from 85% to 93% in foxes and from 82% to 88% in raccoon dogs. Immunisation rates evaluated by ELISA ranged from 34% to 55% in foxes and from 38% to 55% in raccoon dogs. The rabies situation in Estonia was compared to that of the other two Baltic States, Latvia and Lithuania. Despite regular OV campaigns conducted throughout their territory since 2006, and an improvement in the epidemiological situation, rabies has still not been eradicated in these countries. An analysis of the number of baits distributed and the funding allocated by the European Commission showed that the strategy for rabies control is more cost-effective in Estonia than in Latvia and Lithuania.
Author Summary
This paper reports the strategy of oral rabies vaccination of wildlife in Estonia, the measures undertaken to check the method's efficacy and the results obtained. Initiated in autumn 2005, oral vaccination programmes resulted in a dramatic decrease in rabies incidence. All the recommended tests were regularly applied, including the systematic testing of vaccine baits prior to release in the field, serological testing and bait uptake assessment in adult and young animals as well as the typing of all rabies virus isolates. The disease was completely controlled by March 2008, with only three cases reported in summer 2009 and one case in January 2011 in areas very close to the South-Eastern border. The costs associated with rabies control have been calculated and compared on a similar basis for the three Baltic countries. The example of rabies control in Estonia shows that rabies can be quickly and successfully eliminated through successive oral vaccination campaigns by strictly following the recommendations of international organisations. These recommendations concern general strategy, vaccination method and choice of vaccine. To our knowledge, this is the first study showing extensive data from a rabies control programme. The underlying strategy, leading to rabies elimination, is advantageous in terms of cost/effectiveness.
PMCID: PMC3289618  PMID: 22393461
12.  National Borders Effectively Halt the Spread of Rabies: The Current Rabies Epidemic in China Is Dislocated from Cases in Neighboring Countries 
China has seen a massive resurgence of rabies cases in the last 15 years with more than 25,000 human fatalities. Initial cases were reported in the southwest but are now reported in almost every province. There have been several phylogenetic investigations into the origin and spread of the virus within China but few reports investigating the impact of the epidemic on neighboring countries. We therefore collected nucleoprotein sequences from China and South East Asia and investigated their phylogenetic and phylogeographic relationship. Our results indicate that within South East Asia, isolates mainly cluster according to their geographic origin. We found evidence of sporadic exchange of strains between neighboring countries, but it appears that the major strain responsible for the current Chinese epidemic has not been exported. This suggests that national geographical boundaries and border controls are effective at halting the spread of rabies from China into adjacent regions. We further investigated the geographic structure of Chinese sequences and found that the current epidemic is dominated by variant strains that were likely present at low levels in previous domestic epidemics. We also identified epidemiological linkages between high incidence provinces consistent with observations based on surveillance data from human rabies cases.
Author Summary
Rabies as a fatal zoonotic disease continues to be a public threat to global public health. After India, China reports the second highest number of human cases, with more than 117,500 deaths and three major epidemics since 1950. China remains in the middle of the third epidemic. In this work we investigate the impact of China on rabies in South East (SE) Asia. We collected nucleoprotein sequences from samples isolated throughout SE Asia and investigated their phylogenetic and geographic relationships. Our results indicate that clear geographic patterns exist within rabies virus in SE Asia, with isolates mainly clustered according to their geographic origin. While we found evidence of the sporadic exchange of strains between neighboring countries, the major strain responsible for the current Chinese epidemic does not appear to spread to neighboring countries. Our findings suggest that national geographical boundaries and border controls act as effective barriers to halt the spread of rabies from China into adjacent regions. We further investigated the geographic structure of Chinese sequences and found the current epidemic is dominated by variant strains that likely evolved from previous domestic epidemics. Our study provides valuable insight for rabies control and prevention in China and SE Asia.
PMCID: PMC3561166  PMID: 23383359
13.  Improvement Control System of Rabies in Ukraine 
The purpose of the research was to find out the reasons of rabies antropurgisation in Ukraine.
In Ukraine in spite of considerable financial expenses on oral immunization of foxes and parenteral immunization of dogs and cats, it is not succeeded to reach considerable results in the fight with rabies. Unfortunately there was a negative tendency to increasing a part of dogs and cats in the structure of rabies disease which are the main source of rabies in people.
Analysis of 228 anamnesis data of rabies infected dogs during 2008–2012. Research of 234 samples of the blood serum from dogs on existence of antibodies to the rabies virus by the ELISA method.
Analysis of animal morbidity on rabies in Ukraine in period of 2006–2011 found out the changes of structure of morbidity in animal species that means decreasing a part of wild animals (from 49,0 % in 2006 to 38,7 % in 2011) and increasing a part of dogs (from 18,3 % in 2006 to 23,2 % in 2011) and cats (from 19,8 % in 2006 to 25,0 % in 2011) in the general amount of animals which perished from rabies (Fig. 1).
A lot of Ukrainian scientists and doctors of veterinary medicine consider that the main reason of spreading the rabies is a great number of homeless animals which factually are the reservoirs of infection in towns and villages.
However, in our opinion spreading of rabies shows the insufficient level of measures of control of rabies among home animals. It was confirmed with conducted analysis that only 26 (12,9 %) dogs were stray, others 202 (87,1 %) had owners, but didn’t get necessary protective rabies vaccination.
According to Ukrainian instruction “Preventive measures against rabies of animals”, all the dogs must be vaccinated against rabies, but it actually appears it is quite not so.
At research of 234 samples of the blood serum of dogs on existence of antibodies to the rabies virus it was determined that the level of population immunity in dogs is 36,6 % in Ukrainian towns, but the protective level of antibodies was found in 9,1 % of village dogs. We consider that the main reason of this is imperfection of the Ukrainian legislation in the questions of responsibility of proprietors of animals.
For breaking of epizootic chain it is necessary the percent of vaccinated animals (in this case dogs) to be on a high level – more than 50%. Nowadays for reaching epidemic welfare in rabies it is important within the framework of the registered epidemic incidents dogs to be brought over to the ecocycles of infection sporadically without taking part in circulation of exciter, stay their biological deadlock and have low epidemic potential.
The conducted analysis expressly demonstrates that at present problems the eradication of rabies in Ukraine is impossible considering the low level of dogs’ protection from rabies. Obtained results were sent to the State committee of veterinary medicine of Ukraine and will be the argument for enhancement of control after conducting rabies vaccination of dogs.
Rabies cases in the years 2006–2011.
PMCID: PMC3692804
population rabies immunity; rabies vaccination; stray dogs
14.  Deaths from Symptomatically Identifiable Furious Rabies in India: A Nationally Representative Mortality Survey 
It is estimated that India has more deaths from rabies than any other country. However, existing estimates are indirect and rely on non-representative studies.
Methods and Principal Findings
We examined rabies deaths in the ongoing Million Death Study (MDS), a representative survey of over 122,000 deaths in India that uses enhanced types of verbal autopsy. We estimated the age-specific mortality rates of symptomatically identifiable furious rabies and its geographic and demographic distributions. A total of 140 deaths in our sample were caused by rabies, suggesting that in 2005 there were 12,700 (99% CI 10,000 to 15,500) symptomatically identifiable furious rabies deaths in India. Most rabies deaths were in males (62%), in rural areas (91%), and in children below the age of 15 years (50%). The overall rabies mortality rate was 1.1 deaths per 100,000 population (99%CI 0.9 to 1.4). One third of the national rabies deaths were found in Uttar Pradesh (4,300) and nearly three quarters (8,900) were in 7 central and south-eastern states: Chhattisgarh, Uttar Pradesh, Odisha, Andhra Pradesh, Bihar, Assam, and Madhya Pradesh.
Conclusions and Significance
Rabies remains an avoidable cause of death in India. As verbal autopsy is not likely to identify atypical or paralytic forms of rabies, our figure of 12,700 deaths due to classic and clinically identifiable furious rabies underestimates the total number of deaths due to this virus. The concentrated geographic distribution of rabies in India suggests that a significant reduction in the number of deaths or potentially even elimination of rabies deaths is possible.
Author Summary
Rabies, a disease of antiquity, has been partially controlled in many countries and eliminated in a few. However, according to the World Health Organization, rabies continues to kill thousands of people in India each year, more than in any other country. We used an enhanced type of verbal autopsy (a structured interview of the relatives or close associates of the dead by non-medical staff with central medical coding by at least two doctors) to identify the causes of over 122,000 deaths in a large scale, representative sample in India in 2001–03. Using these data, we estimate that in 2005 approximately 12,700 people died from symptomatically identifiable furious rabies. Because verbal autopsy is not able to identify atypical presentations of rabies, our figure underestimates the actual number of rabies deaths in India. The majority of rabies deaths occurred in males, in rural areas, in children below the age of 15 years, and in a few states. The concentrated geographic distribution of rabies in India suggests that targeting with preventive campaigns including vaccination of animals and post exposure vaccination of humans might achieve a significant reduction in the number of deaths or potentially even elimination of deaths from this disease.
PMCID: PMC3464588  PMID: 23056661
15.  Genetic Diversity and Geographic Distribution of Genetically Distinct Rabies Viruses in the Philippines 
Rabies continues to be a major public health problem in the Philippines, where 200–300 human cases were reported annually between 2001 and 2011. Understanding the phylogeography of rabies viruses is important for establishing a more effective and feasible control strategy.
We performed a molecular analysis of rabies viruses in the Philippines using rabied animal brain samples. The samples were collected from 11 of 17 regions, which covered three island groups (Luzon, Visayas, and Mindanao). Partial nucleoprotein (N) gene sequencing was performed on 57 samples and complete glycoprotein (G) gene sequencing was performed on 235 samples collected between 2004 and 2010.
The Philippine strains of rabies viruses were included in a distinct phylogenetic cluster, previously named Asian 2b, which appeared to have diverged from the Chinese strain named Asian 2a. The Philippine strains were further divided into three major clades, which were found exclusively in different island groups: clades L, V, and M in Luzon, Visayas, and Mindanao, respectively. Clade L was subdivided into nine subclades (L1–L9) and clade V was subdivided into two subclades (V1 and V2). With a few exceptions, most strains in each subclade were distributed in specific geographic areas. There were also four strains that were divided into two genogroups but were not classified into any of the three major clades, and all four strains were found in the island group of Luzon.
We detected three major clades and two distinct genogroups of rabies viruses in the Philippines. Our data suggest that viruses of each clade and subclade evolved independently in each area without frequent introduction into other areas. An important implication of these data is that geographically targeted dog vaccination using the island group approach may effectively control rabies in the Philippines.
Author Summary
Rabies continues to be a major public health problem in the Philippines. We conducted a molecular epidemiological study of rabies using the complete glycoprotein (G) gene from 235 animal brain samples collected in the Philippines between 2004 and 2010. We identified three major clades and two distinct genogroups in the Philippines. The three major clades L, V, and M were found specifically in the Luzon, Visayas, and Mindanao island groups, respectively. Additionally, two minor genogroups were located in the Luzon island group. These data suggest that although human mediated transmission may have occurred, these virus clades evolved independently after a single introduction into each island group. All of the analyzed Philippine strains were clustered into Asian 2b, which diverged from the Chinese strain Asian 2a. No recent introduction of rabies into the Philippines from other countries was apparent. The elimination of rabies by 2020 is a national goal in the Philippines, necessitating urgent development of a more effective and feasible strategy for controlling rabies. Our findings indicate that a geographically targeted dog vaccination campaign may effectively control rabies in island nations such as the Philippines.
PMCID: PMC3617229  PMID: 23593515
16.  High Diversity of Rabies Viruses Associated with Insectivorous Bats in Argentina: Presence of Several Independent Enzootics 
Rabies is a fatal infection of the central nervous system primarily transmitted by rabid animal bites. Rabies virus (RABV) circulates through two different epidemiological cycles: terrestrial and aerial, where dogs, foxes or skunks and bats, respectively, act as the most relevant reservoirs and/or vectors. It is widely accepted that insectivorous bats are not important vectors of RABV in Argentina despite the great diversity of bat species and the extensive Argentinean territory.
We studied the positivity rate of RABV detection in different areas of the country, and the antigenic and genetic diversity of 99 rabies virus (RABV) strains obtained from 14 species of insectivorous bats collected in Argentina between 1991 and 2008.
Based on the analysis of bats received for RABV analysis by the National Rabies system of surveillance, the positivity rate of RABV in insectivorous bats ranged from 3.1 to 5.4%, depending on the geographic location. The findings were distributed among an extensive area of the Argentinean territory. The 99 strains of insectivorous bat-related sequences were divided into six distinct lineages associated with Tadarida brasiliensis, Myotis spp, Eptesicus spp, Histiotus montanus, Lasiurus blosseviilli and Lasiurus cinereus. Comparison with RABV sequences obtained from insectivorous bats of the Americas revealed co-circulation of similar genetic variants in several countries. Finally, inter-species transmission, mostly related with Lasiurus species, was demonstrated in 11.8% of the samples.
This study demonstrates the presence of several independent enzootics of rabies in insectivorous bats of Argentina. This information is relevant to identify potential areas at risk for human and animal infection.
Author Summary
In Argentina, successful vaccination and control of terrestrial rabies in the 1980s revealed the importance of the aerial route in RABV transmission. Current distribution of cases shows a predominance of rabies by hematophagous bats in the Northern regions where rabies is a major public health concern; in contrast, in Central and Southern regions where rabies is not a major public health concern, little surveillance is performed. Based on the analysis of insectivorous bats received for RABV analysis by the National Rabies system of surveillance, the positivity rate of RABV in insectivorous bats in these regions ranged from 3.1 to 5.4%. This rate is comparable to other nations such as the United States (9–10%) where insectivorous bats are an important cause of concern for RABV surveillance systems. Antigenic and genetic analysis of a wide collection of rabies strains shows the presence of multiple endemic cycles associated with six bat insectivorous species distributed among an extensive area of the Argentinean territory and several countries of the Americas. Finally, inter-species transmission, mostly related with Lasiurus species, was demonstrated in 11.8% of the samples. Increased public education about the relationship between insectivorous bats and rabies are essential to avoid human cases and potential spread to terrestrial mammals.
PMCID: PMC3348165  PMID: 22590657
17.  Laboratory data of dog rabies in southern Cameroon from 2010 to 2013 
BMC Research Notes  2014;7:905.
Dog rabies is endemic in most African countries and the risk of human rabies is estimated to be high in Cameroon according to WHO estimations in 2010. This study aimed to describe the circulation rabies virus (RABV) among dogs in the southern regions of Cameroon from 2010 to 2013 in a context, where mass vaccination campaigns are launched annually in order to control rabies in domestic animals including dogs and cats.
From 2010 to 2013, 93 animal specimens (dogs: 91, monkey: 1, pig: 1) originating from the southern regions of Cameroon were collected and tested for rabies virus at the Centre Pasteur of Cameroon by fluorescent antibody test (FAT) and virus isolation. Of the total dog specimens, 69.2% (63/91) originated from the central part of the southern regions and 50.5% (46/91) were from the capital city Yaounde. Overall, 74.2% (66/89) of dogs’ specimens that could be tested were found rabies-positive while specimens from the monkey and pig were tested negative. Overall, dog rabies was repeatedly detected in the southern regions of Cameroon especially in the nation capital, Yaounde even though low specimen submission and geographic bias did not permit major conclusions about its actual rate, geographical and over time distribution.
The results of this study indicate that rabies is endemic in the dog population which is of public health concern. Therefore, coordinated rabies control program should be conducted to reduce the rabies incidence in dogs and in humans. In addition, proper rabies surveillance program including reporting system should be established to monitor the success of the control program in Cameroon.
PMCID: PMC4295264  PMID: 25495597
Rabies; Dogs; Cameroon; Surveillance
18.  On the Occasion of the 4th Congress of Infectiologists of Bosnia and Herzegovina with International Participation 
Materia Socio-Medica  2012;24(Suppl 1):20-31.
The 4th Congress of Infectiologists of Bosnia-Herzegovina with international participation was held in Konjic, on 30. May to 02. June 2012. In addition to the prominent infectious disease experts from almost all university centers in B&H, the teachers at medical schools in Bosnia-Herzegovina, infectious disease specialists who work in health institutions in B&H, this Congress was attended by infectious disease experts from Serbia (12 participants), Turkey (3 participants), Croatia (3 participants), Macedonia (3 participants), Germany (2 participants) and Montenegro (2 participants). Topics included: Infections of the skin, soft tissue and bones, Sepsis and endocarditis, Infectious diseases emergencies and pediatric infectology, Emerging and reemerging infectious diseases, Hospital infections, Sexualy transmitted diseases, Infectious diagnostic and therapeutic protocols. Participating invited speakers were following professors: Salih Hosoglu (Turkey), Hakan Leblebicioglu (Turkey), Resat Ozaras (Turkey), Karsten Plötz (Germany), Ilija Kuzman (Croatia), Bruno Baršić (Croatia), Goran Tešović (Croatia). In addition to experts in infectious diseases at this Congress, their works were presented by experts from other medical disciplines, but with infectious character issues (Professors: Sead Ahmetagić, Ismet Gavrankapetanović, Zora Vukobrat-Bijedić, Senija Rašić, Halima Resić, Adnan Kapidžić, Ivo Curić, Jelena Ravlija, Amela Begić, Izet Mašić, Sadeta Hamzić, and others). Some of the papers that were presented at this Congress have been published in extenso, in the Medical Archives and Materia Socio Medica. One part as abstracts (both journals are indexed in over 10 databases), and will be electronically available to the general scientific community in Bosnia-Herzegovina, Europe and worldwide. In this way, the Bosnian infectious disease experts, as a science and profession, will be worthily represented to the colleagues from other countries in the region and beyond.
PMCID: PMC3829089  PMID: 24493992
infectious diseases; Bosnia and Herzegovina; the fourth congress of infectious diseases B&H
19.  Rabies Post-Exposure Prophylaxis of Overseas Travelers in the International Travel Clinic of the National Medical Center from 2006 to 2012, Korea 
Infection & Chemotherapy  2014;46(1):13-20.
Rabies is an acute fatal viral disease generally transmitted from infected animals to humans through bites. It is distributed worldwide. The number of Korean people traveling to rabies-endemic countries and being bitten by infected animals has been increasing recently. Therefore, we investigated international travelers who received rabies post-exposure prophylaxis (PEP) at the National Medical Center (NMC) and compared the data with those of other clinics.
Materials and Methods
This study was a retrospective review of 106 patients who visited the International Travel Clinic of the NMC and received rabies PEP between July 2006 and December 2012. During that period, we used the Essen intramuscular regimen protocol. Complete rabies PEP was defined as 5 doses of rabies vaccination with or without rabies immunoglobulin (RIG) administration according to the World Health Organization guidelines.
A total 106 cases documented within the period of 6 years were selected, including 10 children younger than 15 years and 96 older than 15 years. The mean age of the patients who received PEP was 33.4 years. Of the patients, 53 were male and another 53 were female. Most of the exposures occurred in Southeast Asia, predominantly from dog bites (71, 66.9%). The lower extremities were the most frequent site of exposure (37, 34.9%). All the patients began receiving rabies vaccination for prophylaxis after exposure, and 51 received rabies vaccination with RIG. Meanwhile, 74 cases (69.8%) initiated rabies vaccination overseas, but only 10 of them received RIG while overseas; the remaining 32 (30.2%) initiated rabies vaccination after returning to Korea. Within 7 days, all the children and 74 adults received their first rabies vaccination. Six adults initiated first rabies vaccination after 1 week. Eleven of the 106 patients stopped PEP before 5 doses, among whom 4 (1 child and 3 adults) discontinued vaccination after confirming that the biting animal remained healthy throughout 10 days of observation. None of the patients had been previously vaccinated against rabies.
Most of the overseas travelers who visited our clinic after being bitten by suspected rabid animals received appropriate rabies PEP. However, the interval between exposure and first rabies vaccination was often delayed. Tourists who plan to travel in rabies enzootic regions need to be aware that prompt initiation of PEP is important to reduce the risk for developing human rabies.
PMCID: PMC3970303  PMID: 24693465
Rabies; Post-exposure prophylaxis; Vaccination
20.  Rabies Risk: Difficulties Encountered during Management of Grouped Cases of Bat Bites in 2 Isolated Villages in French Guiana 
In French Guiana, from 1984 to 2011, 14 animal rabies cases and 1 human rabies case (2008) were diagnosed. In January 2011, vampire-bat attacks occurred in 2 isolated villages. In mid-January, a medical team from the Cayenne Centre for Anti-Rabies Treatment visited the sites to manage individuals potentially exposed to rabies and, in April, an anti-rabies vaccination campaign for dogs was conducted. Twenty individuals were bitten by bats in 1 month, most frequently on the feet. The median time to start management was 15 days. The complete Zagreb vaccination protocol (2 doses on day 0 and 1 dose on days 7 and 21) was administered to 16 patients, 12 also received specific immunoglobulins. The antibody titration was obtained for 12 patients (different from those who received immunoglobulins). The antibody titers were ≥0.5 EU/mL for all of them. The serology has not been implemented for the 12 patients who received immunoglobulins. Accidental destruction of a vampire-bat colony could be responsible for the attacks. The isolation and absence of sensitization of the populations were the main explanations for the management difficulties encountered. Sensitization programs should be conducted regularly.
Author Summary
Rabies is a disease almost invariably fatal in humans once the first clinical signs appear. In French Guiana bats represent the virus reservoir, especially vampire bats. From 1984 to 2011, 14 animal rabies cases and 1 human rabies case (2008) were diagnosed. In case of bat bite, anti-rabies immunoglobulins (RIG) and rabies vaccine must be rapidly administrated. The specific rabies management is exclusively performed by Centre for Anti-Rabies Treatment (CART), located at the Institut Pasteur in Cayenne, the prefecture of French Guiana, and 6 Anti-Rabies Treatment Outposts distributed along the coastal edge and along the two main rivers. Only a CART physician can administer RIG. In January 2011, vampire-bat attacks occurred in 2 isolated villages. In mid-January, a medical team from the CART visited the sites to manage individuals potentially exposed to rabies and, in April, an anti-rabies vaccination campaign for dogs was conducted. The most relevant contribution of this study is to underline difficulties to provide rabies post-exposure prophylaxis to remote populations exposed to bat rabies in the Amazonian region and to show the lack of awareness of these rural populations concerning rabies and the risk associated to vampire bats.
PMCID: PMC3694830  PMID: 23826400
21.  Knowledge, attitudes and practices towards rabies: questionnaire survey in rural household heads of Gondar Zuria District, Ethiopia 
BMC Research Notes  2015;8:400.
Rabies is a fatal animal disease of significant public health importance. Domestic dogs are the main reservoir and transmitter of this disease particularly in developing countries. Even though rabies is a highly fatal disease, it is a preventable disease. Community awareness about rabies is one of the key components for prevention. This study describes the knowledge, attitudes and practices of a rural community in Gondar Zuria District, Ethiopia.
A cross sectional study was conducted from March to June, 2013. A structured questionnaire was used to collect the data through face to face interviews among 400 respondents. The data were then analyzed using SPSS statistical software version 20.
The current study indicated that almost all (99.3 %) of the surveyed individuals were aware of the disease rabies. Rabies is considered to be a fatal disease in humans by 67.8 % of the respondents while 27.8 % believe that it is a treatable disease. Dogs were indicated as source of infection for humans by all respondents followed by equines (27.2 %) and cats (12.1 %). Bite was known as mode of rabies transmission by majority of the respondents (94 %) while other means were given less weight. Aggression was described as a major clinical sign of rabies in animals. Consumption of cooked or boiled meat from rabid animals was considered as safe by 67.0 % of the respondents and about 19 % replied even raw meat is safe for human consumption. The need for immediate treatment after exposure was mentioned by less than half (47.4 %) of the respondents and only 38.8 % of the respondents considered modern medicine as appropriate treatment after exposure to rabid animals. Nearly 42 % of respondents had experienced a dog bite. Following the dog bites, only 30.7 % practiced washing of the wounds with water as first aid.
Rabies was found to be well known in the study area. However, knowledge and practices in prevention of rabies were limited. Education of rabies about possible sources of infection, mode of transmission and measures to be taken after exposure is very important in the study area.
Electronic supplementary material
The online version of this article (doi:10.1186/s13104-015-1357-8) contains supplementary material, which is available to authorized users.
PMCID: PMC4566865  PMID: 26328612
Knowledge; Practices; Questionnaire; Rabies; North Gondar
22.  Imported Episodic Rabies Increases Patient Demand for and Physician Delivery of Antirabies Prophylaxis 
Imported cases threaten rabies reemergence in rabies-free areas. During 2000–2005, five dog and one human rabies cases were imported into France, a rabies-free country since 2001. The Summer 2004 event led to unprecedented media warnings by the French Public Health Director. We investigated medical practice evolution following the official elimination of rabies in 2001; impact of subsequent episodic rabies importations and national newspaper coverage on demand for and delivery of antirabies prophylaxis; regular transmission of epidemiological developments within the French Antirabies Medical Center (ARMC) network; and ARMC discussions on indications of rabies post-exposure prophylaxis (RPEP).
Methodology/Principal Findings
Annual data collected by the National Reference Center for Rabies NRCR (1989–2006) and the exhaustive database (2000–2005) of 56 ARMC were analyzed. Weekly numbers of patients consulting at ARMC and their RPEP- and antirabies-immunoglobulin (ARIG) prescription rates were determined. Autoregressive integrated moving-average modeling and regression with autocorrelated errors were applied to examine how 2000–2005 episodic rabies events and their related national newspaper coverage affected demand for and delivery of RPEP. A slight, continuous decline of rabies-dedicated public health facility attendance was observed from 2000 to 2004. Then, during the Summer 2004 event, patient consultations and RPEP and ARIG prescriptions increased by 84%, 19.7% and 43.4%, respectively. Moreover, elevated medical resource use persisted in 2005, despite communication efforts, without any secondary human or animal case.
Our findings demonstrated appropriate responsiveness to reemerging rabies cases and effective newspaper reporting, as no secondary case occurred. However, the ensuing demand on medical resources had immediate and long-lasting effects on rabies-related public health resources and expenses. Henceforth, when facing such an event, decision-makers must anticipate the broad impact of their media communications to counter the emerging risk on maintaining an optimal public health organization and implement a post-crisis communication strategy.
Author Summary
Rabies has been eliminated from a large part of the European Union and, thus, any newly imported cases threaten its reemergence. The 2000–2005 data derived from the exhaustive surveillance system implemented in France was analyzed to evaluate the impact on demand for and delivery of antirabies prophylaxis following introduction of five rabies-infected dogs and one infected human into this rabies-free area. Using these events, we were able to illustrate the difficulties encountered in reducing the demand for and prescription of post-exposure rabies prophylaxis in this context of episodic importation. Moreover, we highlighted the need for public health decision-makers to anticipate the broad spectrum of consequences of their media communications and to prepare appropriate responses (in terms of health resources) to maintain an optimally effective public health organization after importation of an exotic infectious agent or its emergence. These responses are particularly relevant in the context of limited availability of rabies post-exposure prophylaxis, especially antirabies immunoglobulin.
PMCID: PMC2889823  PMID: 20582307
23.  Is tuberculosis crossing borders at the Eastern boundary of the European Union? 
Background: The Eastern border of the European Union (EU) consists of 10 countries after the expansion of the EU in 2004 and 2007. These 10 countries border to the East to countries with high tuberculosis (TB) notification rates. We analyzed the notification data of Europe to quantify the impact of cross-border TB at the Eastern border of the EU. Methods: We used TB surveillance data of 2010 submitted by 53 European Region countries to the European Centre for Disease Prevention and Control and the World Health Organization Regional Office for Europe. Notified TB cases were stratified by origin of the case (national/foreign). We calculated the contribution of foreign to overall TB notification. Results: In the 10 EU countries located at the EU Eastern border, 618 notified TB cases (1.7% of all notified TB cases) were of foreign origin. Of those 618 TB cases, 173 (28.0%) were from countries bordering the EU to the East. More specifically, 90 (52.0%) were from Russia, 33 (19.1%) from Belarus, 33 (19.1%) from Ukraine, 13 (7.5%) from Moldova and 4 (2.3%) from Turkey. Conclusions: Currently, migrants contribute little to TB notifications in the 10 EU countries at the Eastern border of the EU, but changes in migration patterns may result in an increasing contribution. Therefore, EU countries at the Eastern border of the EU should strive to provide prompt diagnostic services and adequate treatment of migrants.
PMCID: PMC3840804  PMID: 23813718
24.  Prioritization of capacities for the elimination of dog-mediated human rabies in the Americas: building the framework 
Pathogens and Global Health  2013;107(7):340-345.
The region of the Americas pledged to eliminate dog-transmitted human rabies by 2015. After 30 years of sustained efforts, regional elimination appears possible as dog-mediated human rabies cases are at an all-time low, and a number of countries and territories have already eliminated the disease. In this setting, there is an opportunity to generate a framework to support countries strategies in the achievement and maintenance of rabies-free status (RFS). To this end, we describe the development of a multi-criteria decision analysis (MCDA) model to help the evaluation of rabies programmes and the identification of the best investment strategy for countries and territories to improve and efficiently maintain their rabies status. The model contemplates human and animal related capacities, six in each area, to comprehensively assess the wide scope of rabies programmes. An initial elicitation of expert opinion of values and weights for the MCDA model was performed via a web-based questionnaire. Even at this pilot stage, the model produces comparable capacity-scores, and overall (combined for public and animal health areas) as well as area-specific investment strategies. The model is being developed by the Pan American Health Organization (PAHO) as part of the regional efforts towards dog-mediated human rabies elimination and will be presented to the countries for review, refinement, contextualization, and testing. The aspiration is that countries use the model to identify the best allocation of resources towards the elimination of dog-mediated human rabies.
PMCID: PMC4083153  PMID: 24392676
Dog-mediated human rabies; Elimination; Multi-criteria decision analysis; Prioritization
25.  Estimating the Global Burden of Endemic Canine Rabies 
PLoS Neglected Tropical Diseases  2015;9(4):e0003709.
Rabies is a notoriously underreported and neglected disease of low-income countries. This study aims to estimate the public health and economic burden of rabies circulating in domestic dog populations, globally and on a country-by-country basis, allowing an objective assessment of how much this preventable disease costs endemic countries.
Methodology/Principal Findings
We established relationships between rabies mortality and rabies prevention and control measures, which we incorporated into a model framework. We used data derived from extensive literature searches and questionnaires on disease incidence, control interventions and preventative measures within this framework to estimate the disease burden. The burden of rabies impacts on public health sector budgets, local communities and livestock economies, with the highest risk of rabies in the poorest regions of the world. This study estimates that globally canine rabies causes approximately 59,000 (95% Confidence Intervals: 25-159,000) human deaths, over 3.7 million (95% CIs: 1.6-10.4 million) disability-adjusted life years (DALYs) and 8.6 billion USD (95% CIs: 2.9-21.5 billion) economic losses annually. The largest component of the economic burden is due to premature death (55%), followed by direct costs of post-exposure prophylaxis (PEP, 20%) and lost income whilst seeking PEP (15.5%), with only limited costs to the veterinary sector due to dog vaccination (1.5%), and additional costs to communities from livestock losses (6%).
This study demonstrates that investment in dog vaccination, the single most effective way of reducing the disease burden, has been inadequate and that the availability and affordability of PEP needs improving. Collaborative investments by medical and veterinary sectors could dramatically reduce the current large, and unnecessary, burden of rabies on affected communities. Improved surveillance is needed to reduce uncertainty in burden estimates and to monitor the impacts of control efforts.
Author Summary
Rabies is a fatal viral disease largely transmitted to humans from bites by infected animals—predominantly from domestic dogs. The disease is entirely preventable through prompt administration of post-exposure prophylaxis (PEP) to bite victims and can be controlled through mass vaccination of domestic dogs. Yet, rabies is still very prevalent in developing countries, affecting populations with limited access to health care. The disease is also grossly underreported in these areas because most victims die at home. This leads to insufficient prioritization of rabies prevention in public health agendas. To address this lack of information on the impacts of rabies, in this study, we compiled available data to provide a robust estimate of the health and economic implications of dog rabies globally. The most important impacts included: loss of human lives (approximately 59,000 annually) and productivity due to premature death from rabies, and costs of obtaining PEP once an exposure has occurred. The greatest risk of developing rabies fell upon the poorest regions of the world, where domestic dog vaccination is not widely implemented and access to PEP is most limited. A greater focus on mass dog vaccination could eliminate the disease at source, reducing the need for costly PEP and preventing the large and unnecessary burden of mortality on at-risk communities.
PMCID: PMC4400070  PMID: 25881058

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