Reservoir dynamics of rabies in Southeast Tanzania and the roles of cross-species transmission and domestic dog vaccination

1) Understanding the role of different species in the transmission of multi-host pathogens, such as rabies virus, is vital for effective control strategies. Across most of sub-Saharan Africa domestic dogs (Canis familiaris) are considered the reservoir for rabies, but the role of wildlife has been long debated. Here we explore the multi-host transmission dynamics of rabies across southeast Tanzania. 2) Between January 2011 and July 2019 data on probable rabies cases were collected in the regions of Lindi and Mtwara. Hospital records of animal-bite patients presenting to healthcare facilities were used as sentinels for animal contact tracing. The timing, location and species of probable rabid animals was used to reconstruct transmission trees to infer who infected whom and the relative frequencies of within-and between-species transmission. 3) During the study, 688 probable human rabies exposures were identified, resulting in 47 deaths. Of these exposures, 389 were from domestic dogs (56.5%) and 262 from jackals (38.1%). Over the same period 549 probable animal rabies cases were traced: 303 in domestic dogs (55.2%) and 221 in jackals (40.3%). 4) Although dog-to-dog transmission was most commonly inferred (40.5% of transmission events), a third of inferred events involved wildlife-to-wildlife transmission (32.6%) and evidence suggested some sustained transmission chains within jackal populations. 5) A steady decline in probable rabies cases in both humans and animals coincided with the implementation of widespread domestic dog vaccination during the first six years of the study. Following the lapse of this programme dog rabies cases began to increase in one of the northernmost districts. 6) Synthesis and applications: in southeast Tanzania, despite a relatively high incidence of rabies in wildlife and evidence of wildlife-to-wildlife transmission, domestic dogs remain essential to the reservoir of infection. Continued dog vaccination alongside improved surveillance would allow a fuller understanding of the role of wildlife in maintaining transmission in this area. Nonetheless, dog vaccination clearly suppressed rabies in both domestic dog and wildlife populations, reducing both public health and conservation risks and, if sustained, has potential to eliminate rabies from this region

Comparing methods of assessing dog rabies vaccination coverage in rural and urban communities in Tanzania

Frontiers in Veterinary Science, 2017; 4 (33).Rabies can be eliminated by achieving comprehensive coverage of 70% of domestic dogs during annual mass vaccination campaigns. Estimates of vaccination coverage are, therefore, required to evaluate and manage mass dog vaccination programs; however, there is no specific guidance for the most accurate and efficient methods for estimating coverage in different settings. Here, we compare post-vaccination transects, school-based surveys, and household surveys across 28 districts in southeast Tanzania and Pemba island covering rural, urban, coastal and inland settings, and a range of different livelihoods and religious backgrounds. These approaches were explored in detail in a single district in northwest Tanzania (Serengeti), where their performance was compared with a complete dog population census that also recorded dog vaccination status. Post-vaccination transects involved counting marked (vaccinated) and unmarked (unvaccinated) dogs immediately after campaigns in 2,155 villages (24,721 dogs counted). School-based surveys were administered to 8,587 primary school pupils each representing a unique household, in 119 randomly selected schools approximately 2 months after campaigns. Household surveys were conducted in 160 randomly selected villages (4,488 households) in July/August 2011. Costs to implement these coverage assessments were $12.01,$66.12, and $155.70 per village for post- vaccination transects, school-based, and household surveys, respectively. Simulations were performed to assess the effect of sampling on the precision of coverage estimation. The sampling effort required to obtain reasonably precise estimates of coverage from household surveys is generally very high and probably prohibitively expensive for routine monitoring across large areas, particularly in communities with high human to dog ratios. School-based surveys partially overcame sampling constraints, however, were also costly to obtain reasonably precise estimates of coverage. Post-vaccination transects provided precise and timely estimates of community-level coverage that could be used to troubleshoot the performance of campaigns across large areas. However, transects typically overestimated coverage by around 10%, which therefore needs consideration 2 Sambo et al. Assessing Dog Rabies Vaccination Coverage Frontiers in Veterinary Science | www.frontiersin.org March 2017 | Volume 4 | Article 33 inTrODUcTiOn Rabies is a fatal viral disease transmitted to humans by animal bites, usually from domestic dogs. Although under control in most industrialized countries, rabies continues to kill an estimated 59,000 people each year in low- and middle-income countries (LMICs) (1). Reliable estimates of the proportion of dogs vaccinated against rabies are crucial to determine the performance of vaccination programs and their impact on disease transmission. Empirical and theoretical evidence shows that mass dog vaccination campaigns that reach at least 70% of the dog population can control rabies (2, 3). While achieving this coverage in all communities can lead to elimination, even small gaps in coverage can delay the time to elimination (4). As progress is made toward reaching global targets of zero human rabies deaths from dog-mediated rabies through the implementation of mass dog vaccinations (5), there is a clear need to identify reliable, cost-effective, and feasible approaches that can be used, at scale, to assess community-level vaccination coverage. Limited population data on owned and free-roaming dogs in most LMICs make estimation of vaccination coverage challenging. Several methods have been used to estimate coverage including (i) the use of pre-campaign estimates of dog population size through human to dog ratios (HDRs) as the denominator, and the number of dogs vaccinated during the campaign as the numerator (6); (ii) post-vaccination household surveys to estimate the proportion of vaccinated dogs (7–11); and (iii) post-vaccination transects to estimate the proportion of marked (vaccinated) dogs (4, 12–14). However, these methods all have limitations. If dog populations are estimated from data on HDRs, inaccuracies in estimates of the human population will invariably affect the accuracy of dog population estimates. This may occur, for example, through errors in extrapolating current human population sizes from census data (for example, using average population growth rates) or from administrative/boundary changes that affect village demarcations across different time periods. Furthermore, published data on HDRs usually reflect a sample from surveys across several communities (15), and even a small degree of variation in HDRs can have a major effect on dog population estimates at the community level. Household surveys are restricted to capturing estimates of vaccination coverage in owned dog populations and are relatively intensive to complete. Moreover, there is known to be wide variability in patterns of dog ownership within communities—for example, in Tanzania, a much smaller proportion of Muslim and urban households own dogs in comparison with rural, livestockkeeping communities (15). This variability and the highly skewed pattern of dog ownership in some communities make household surveys prone to selection and measurement biases (16). Additional uncertainty from household surveys arises in relation to validation of dog vaccination status. In Tunisia, for example, about 14% of dog owners who claimed their dogs were vaccinated were unable to provide certificates (17). Post-vaccination transects are limited to observations of freeroaming dogs and will, therefore, be biased toward dogs that are more likely to be observed from transects. For example, young puppies are likely to be less visible and are known to represent an age group that typically has a low vaccination coverage (9, 18, 19), thus resulting in the potential for overestimating coverage. In a recent study from Tanzania, post-vaccination transects were shown to overestimate coverage by approximately 7% in comparison with household surveys, although it was unclear in this study which of the approaches was most accurate (19). Here, we present a detailed assessment of three methods to estimate dog vaccination coverage across settings in Tanzania. We use a complete household census as reference data for a simulation experiment to determine the impacts of sampling on the precision of coverage estimates. Specifically, we aim to answer the following questions: (i) What are the resources (personnel, time, and money) required to implement these methods? (ii) Which methods provide the most precise estimates of coverage? and finally (iii) Which approaches, therefore, generate acceptable coverage estimates to provide operational guidance to improve the performance of current or future campaigns? MaTerials anD MeThODs study sites The study was conducted in 29 districts across Tanzania: 24 districts from southeast Tanzania, 4 districts from Pemba island, and 1 district (Serengeti district) from northwest Tanzania (Figure 1). These areas are inhabited by an estimated 9.1 million people (20% of the Tanzanian population) according to the 2012 national census (20) and represent districts that span a wide range of settings, comprising rural, urban, coastal and inland areas, and a range of livelihoods and religious backgrounds. Mass dog vaccination campaigns were conducted in all these districts by local government teams, with support of WHO and collaborating institutions. Various methods of estimating vaccination coverages achieved during campaigns were compared. Table 1 summarizes the methods used in different locations and the rationale for data collection. Post-Vaccination Transects To generate rapid estimates of village-level vaccination coverage, post-vaccination transects were conducted on the same day as when evaluating the impacts of campaigns. We discuss the advantages and disadvantages of these different methods and make recommendations for how vaccination campaigns can be better monitored and managed at different stages of rabies contro

Comparing methods of assessing dog rabies vaccination coverage in rural and urban communities in Tanzania

Frontiers in Veterinary Science, 2017; 4 (33).Rabies can be eliminated by achieving comprehensive coverage of 70% of domestic dogs during annual mass vaccination campaigns. Estimates of vaccination coverage are, therefore, required to evaluate and manage mass dog vaccination programs; however, there is no specific guidance for the most accurate and efficient methods for estimating coverage in different settings. Here, we compare post-vaccination transects, school-based surveys, and household surveys across 28 districts in southeast Tanzania and Pemba island covering rural, urban, coastal and inland settings, and a range of different livelihoods and religious backgrounds. These approaches were explored in detail in a single district in northwest Tanzania (Serengeti), where their performance was compared with a complete dog population census that also recorded dog vaccination status. Post-vaccination transects involved counting marked (vaccinated) and unmarked (unvaccinated) dogs immediately after campaigns in 2,155 villages (24,721 dogs counted). School-based surveys were administered to 8,587 primary school pupils each representing a unique household, in 119 randomly selected schools approximately 2 months after campaigns. Household surveys were conducted in 160 randomly selected villages (4,488 households) in July/August 2011. Costs to implement these coverage assessments were $12.01,$66.12, and $155.70 per village for post- vaccination transects, school-based, and household surveys, respectively. Simulations were performed to assess the effect of sampling on the precision of coverage estimation. The sampling effort required to obtain reasonably precise estimates of coverage from household surveys is generally very high and probably prohibitively expensive for routine monitoring across large areas, particularly in communities with high human to dog ratios. School-based surveys partially overcame sampling constraints, however, were also costly to obtain reasonably precise estimates of coverage. Post-vaccination transects provided precise and timely estimates of community-level coverage that could be used to troubleshoot the performance of campaigns across large areas. However, transects typically overestimated coverage by around 10%, which therefore needs consideration 2 Sambo et al. Assessing Dog Rabies Vaccination Coverage Frontiers in Veterinary Science | www.frontiersin.org March 2017 | Volume 4 | Article 33 inTrODUcTiOn Rabies is a fatal viral disease transmitted to humans by animal bites, usually from domestic dogs. Although under control in most industrialized countries, rabies continues to kill an estimated 59,000 people each year in low- and middle-income countries (LMICs) (1). Reliable estimates of the proportion of dogs vaccinated against rabies are crucial to determine the performance of vaccination programs and their impact on disease transmission. Empirical and theoretical evidence shows that mass dog vaccination campaigns that reach at least 70% of the dog population can control rabies (2, 3). While achieving this coverage in all communities can lead to elimination, even small gaps in coverage can delay the time to elimination (4). As progress is made toward reaching global targets of zero human rabies deaths from dog-mediated rabies through the implementation of mass dog vaccinations (5), there is a clear need to identify reliable, cost-effective, and feasible approaches that can be used, at scale, to assess community-level vaccination coverage. Limited population data on owned and free-roaming dogs in most LMICs make estimation of vaccination coverage challenging. Several methods have been used to estimate coverage including (i) the use of pre-campaign estimates of dog population size through human to dog ratios (HDRs) as the denominator, and the number of dogs vaccinated during the campaign as the numerator (6); (ii) post-vaccination household surveys to estimate the proportion of vaccinated dogs (7–11); and (iii) post-vaccination transects to estimate the proportion of marked (vaccinated) dogs (4, 12–14). However, these methods all have limitations. If dog populations are estimated from data on HDRs, inaccuracies in estimates of the human population will invariably affect the accuracy of dog population estimates. This may occur, for example, through errors in extrapolating current human population sizes from census data (for example, using average population growth rates) or from administrative/boundary changes that affect village demarcations across different time periods. Furthermore, published data on HDRs usually reflect a sample from surveys across several communities (15), and even a small degree of variation in HDRs can have a major effect on dog population estimates at the community level. Household surveys are restricted to capturing estimates of vaccination coverage in owned dog populations and are relatively intensive to complete. Moreover, there is known to be wide variability in patterns of dog ownership within communities—for example, in Tanzania, a much smaller proportion of Muslim and urban households own dogs in comparison with rural, livestockkeeping communities (15). This variability and the highly skewed pattern of dog ownership in some communities make household surveys prone to selection and measurement biases (16). Additional uncertainty from household surveys arises in relation to validation of dog vaccination status. In Tunisia, for example, about 14% of dog owners who claimed their dogs were vaccinated were unable to provide certificates (17). Post-vaccination transects are limited to observations of freeroaming dogs and will, therefore, be biased toward dogs that are more likely to be observed from transects. For example, young puppies are likely to be less visible and are known to represent an age group that typically has a low vaccination coverage (9, 18, 19), thus resulting in the potential for overestimating coverage. In a recent study from Tanzania, post-vaccination transects were shown to overestimate coverage by approximately 7% in comparison with household surveys, although it was unclear in this study which of the approaches was most accurate (19). Here, we present a detailed assessment of three methods to estimate dog vaccination coverage across settings in Tanzania. We use a complete household census as reference data for a simulation experiment to determine the impacts of sampling on the precision of coverage estimates. Specifically, we aim to answer the following questions: (i) What are the resources (personnel, time, and money) required to implement these methods? (ii) Which methods provide the most precise estimates of coverage? and finally (iii) Which approaches, therefore, generate acceptable coverage estimates to provide operational guidance to improve the performance of current or future campaigns? MaTerials anD MeThODs study sites The study was conducted in 29 districts across Tanzania: 24 districts from southeast Tanzania, 4 districts from Pemba island, and 1 district (Serengeti district) from northwest Tanzania (Figure 1). These areas are inhabited by an estimated 9.1 million people (20% of the Tanzanian population) according to the 2012 national census (20) and represent districts that span a wide range of settings, comprising rural, urban, coastal and inland areas, and a range of livelihoods and religious backgrounds. Mass dog vaccination campaigns were conducted in all these districts by local government teams, with support of WHO and collaborating institutions. Various methods of estimating vaccination coverages achieved during campaigns were compared. Table 1 summarizes the methods used in different locations and the rationale for data collection. Post-Vaccination Transects To generate rapid estimates of village-level vaccination coverage, post-vaccination transects were conducted on the same day as when evaluating the impacts of campaigns. We discuss the advantages and disadvantages of these different methods and make recommendations for how vaccination campaigns can be better monitored and managed at different stages of rabies contro

Progress towards rabies elimination from Pemba Island, Southern Tanzania.

Online Journal of Public Health Informatics. Volume 9(1); 2017Using active surveillance approaches to investigate the transmission dynamics of rabies on Pemba Island and across Southern Tanzania, whilst a large-scale dog vaccination program was underway1 , to gain a greater understanding of the dynamics of infection as the disease is driven towards eliminatio

Reservoir dynamics of rabies in south-east Tanzania and the roles of cross-species transmission and domestic dog vaccination

1. Understanding the role of different species in the transmission of multi-host pathogens, such as rabies virus, is vital for effective control strategies. Across most of sub-Saharan Africa domestic dogs Canis familiaris are considered the reservoir for rabies, but the role of wildlife has been long debated. Here we explore the multi-host transmission dynamics of rabies across south-east Tanzania. 2. Between January 2011 and July 2019, data on probable rabies cases were collected in the regions of Lindi and Mtwara. Hospital records of animal-bite patients presenting to healthcare facilities were used as sentinels for animal contact tracing. The timing, location and species of probable rabid animals were used to reconstruct transmission trees to infer who infected whom and the relative frequencies of within- and between-species transmission. 3. During the study, 688 probable human rabies exposures were identified, resulting in 47 deaths. Of these exposures, 389 were from domestic dogs (56.5%) and 262 from jackals (38.1%). Over the same period, 549 probable animal rabies cases were traced: 303 in domestic dogs (55.2%) and 221 in jackals (40.3%), with the remainder in domestic cats and other wildlife species. 4. Although dog-to-dog transmission was most commonly inferred (40.5% of transmission events), a third of inferred events involved wildlife-to-wildlife transmission (32.6%), and evidence suggested some sustained transmission chains within jackal populations. 5. A steady decline in probable rabies cases in both humans and animals coincided with the implementation of widespread domestic dog vaccination during the first 6 years of the study. Following the lapse of this program, dog rabies cases began to increase in one of the northernmost districts. 6. Synthesis and applications. In south-east Tanzania, despite a relatively high incidence of rabies in wildlife and evidence of wildlife-to-wildlife transmission, domestic dogs remain essential to the reservoir of infection. Continued dog vaccination alongside improved surveillance would allow a fuller understanding of the role of wildlife in maintaining transmission in this area. Nonetheless, dog vaccination clearly suppressed rabies in both domestic dog and wildlife populations, reducing both public health and conservation risks and, if sustained, has potential to eliminate rabies from this region.</p

Toward Elimination of Dog-Mediated Human Rabies: Experiences from Implementing a Large-scale Demonstration Project in Southern Tanzania

A Rabies Elimination Demonstration Project was implemented in Tanzania from 2010 through to 2015, bringing together government ministries from the health and veterinary sectors, the World Health Organization, and national and international research institutions. Detailed data on mass dog vaccination campaigns, bite exposures, use of post-exposure prophylaxis (PEP), and human rabies deaths were collected throughout the project duration and project areas. Despite no previous experience in dog vaccination within the project areas, district veterinary officers were able to implement district-wide vaccination campaigns that, for most part, progressively increased the numbers of dogs vaccinated with each phase of the project. Bite exposures declined, particularly in the southernmost districts with the smallest dog populations, and health workers successfully transitioned from primarily intramuscular administration of PEP to intradermal administration, resulting in major cost savings. However, even with improved PEP provision, vaccine shortages still occurred in some districts. In laboratory diagnosis, there were several logistical challenges in sample handling and submission but compared to the situation before the project started, there was a moderate increase in the number of laboratory samples submitted and tested for rabies in the project areas with a decrease in the proportion of rabies-positive samples over time. The project had a major impact on public health policy and practice with the formation of a One Health Coordination Unit at the Prime Minister’s Office and development of the Tanzania National Rabies Control Strategy, which lays a roadmap for elimination of rabies in Tanzania by 2030 by following the Stepwise Approach towards Rabies Elimination (SARE). Overall, the project generated many important lessons relevant to rabies prevention and control in particular and disease surveillance in general. Lessons include the need for (1) a specific unit in the government for managing disease surveillance; (2) application of innovative data collection and management approaches such as the use of mobile phones; (3) close cooperation and effective communication among all key sectors and stakeholders; and (4) flexible and adaptive programs that can incorporate new information to improve their delivery, and overcome challenges of logistics and procurement