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The Feasibility of Canine Rabies Elimination in Africa: Dispelling Doubts with Data

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The Feasibility of Canine Rabies Elimination in Africa: Dispelling Doubts with Data

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Canine rabies causes many thousands of human deaths every year in Africa, and continues to increase throughout much of the continent. This paper identifies four common reasons given for the lack of effective canine rabies control in Africa: (a) a low priority given for disease control as a result of lack of awareness of the rabies burden; (b) epidemiological constraints such as uncertainties about the required levels of vaccination coverage and the possibility of sustained cycles of infection in wildlife; (c) operational constraints including accessibility of dogs for vaccination and insufficient knowledge of dog population sizes for planning of vaccination campaigns; and (d) limited resources for implementation of rabies surveillance and control. We address each of these issues in turn, presenting data from field studies and modelling approaches used in Tanzania, including burden of disease evaluations, detailed epidemiological studies, operational data from vaccination campaigns in different demographic and ecological settings, and economic analyses of the cost-effectiveness of dog vaccination for human rabies prevention. We conclude that there are no insurmountable problems to canine rabies control in most of Africa; that elimination of canine rabies is epidemiologically and practically feasible through mass vaccination of domestic dogs; and that domestic dog vaccination provides a cost-effective approach to the prevention and elimination of human rabies deaths.
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The Feasibility of Canine Rabies Elimination in Africa:
Dispelling Doubts with Data
Tiziana Lembo
1,2
*, Katie Hampson
3
, Magai T. Kaare
4{
, Eblate Ernest
4
, Darryn Knobel
1
, Rudovick R.
Kazwala
5
, Daniel T. Haydon
1
, Sarah Cleaveland
1
1Boyd Orr Centre for Population and Ecosystem Health, University of Glasgow, Glasgow, United Kingdom, 2Davee Center for Epidemiology and Endocrinology, Lincoln
Park Zoo, Chicago, Illinois, United States of America, 3Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, United Kingdom,
4Serengeti Carnivore Viral Transmission Dynamics Project, Tanzania Wildlife Research Institute, Arusha, Tanzania, 5Sokoine University of Agriculture, Department of
Veterinary Medicine and Public Health, Morogoro, Tanzania
Abstract
Background:
Canine rabies causes many thousands of human deaths every year in Africa, and continues to increase
throughout much of the continent.
Methodology/Principal Findings:
This paper identifies four common reasons given for the lack of effective canine rabies
control in Africa: (a) a low priority given for disease control as a result of lack of awareness of the rabies burden; (b)
epidemiological constraints such as uncertainties about the required levels of vaccination coverage and the possibility of
sustained cycles of infection in wildlife; (c) operational constraints including accessibility of dogs for vaccination and
insufficient knowledge of dog population sizes for planning of vaccination campaigns; and (d) limited resources for
implementation of rabies surveillance and control. We address each of these issues in turn, presenting data from field
studies and modelling approaches used in Tanzania, including burden of disease evaluations, detailed epidemiological
studies, operational data from vaccination campaigns in different demographic and ecological settings, and economic
analyses of the cost-effectiveness of dog vaccination for human rabies prevention.
Conclusions/Significance:
We conclude that there are no insurmountable problems to canine rabies control in most of
Africa; that elimination of canine rabies is epidemiologically and practically feasible through mass vaccination of domestic
dogs; and that domestic dog vaccination provides a cost-effective approach to the prevention and elimination of human
rabies deaths.
Citation: Lembo T, Hampson K, Kaare MT, Ernest E, Knobel D, et al. (2010) The Feasibility of Canine Rabies Elimination in Africa: Dispelling Doubts with Data. PLoS
Negl Trop Dis 4(2): e626. doi:10.1371/journal.pntd.0000626
Editor: Charles E. Rupprecht, Centers for Disease Control and Prevention, United States of America
Received May 26, 2009; Accepted January 22, 2010; Published February 23, 2010
Copyright: ß2010 Lembo et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Work in Tanzania was supported by the Wellcome Trust, National Science Foundation (DEB0513994), National Institutes of Health/National Science
Foundation Ecology of Infectious Diseases Programme (NSF/DEB0225453), Pew Charitable Trusts award (2000-002558), Lincoln Park Zoo, the Disney Conservation
Fund and Fauna and Flora International, the Tusk Trust, the Department for International Development Animal Health Programme, the RCVS Trust and Intervet.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: T.Lembo@vet.gla.ac.uk
{Deceased October 2008.
Introduction
Rabies is a viral zoonosis caused by negative-stranded RNA
viruses from the Lyssavirus genus. Genetic variants of the genotype 1
Lyssavirus (the cause of classical rabies) are maintained in different
parts of the world by different reservoir hosts within ‘host-adaptive
landscapes’ [1]. Although rabies can infect and be transmitted by a
wide range of mammals, reservoirs comprise only mammalian
species within the Orders Carnivora (e.g. dogs, raccoons, skunks,
foxes, jackals) and Chiroptera (bats). From the perspective of human
rabies, the vast majority of human cases (.90%) result from the
bites of rabid domestic dogs [2] and occur in regions where domestic
dogs are the principal maintenance host [3].
Over the past three decades, there have been marked
differences in efforts to control canine rabies. Recent successes
have been demonstrated in many parts of central and South
America, where canine rabies has been brought under control
through large-scale, synchronized mass dog vaccination campaigns
[4]. As a result, not only has dog rabies declined, but human
rabies deaths have also been eliminated, or cases remain
highly localized [5]. The contrast with the situation in Africa
and Asia is striking; here, the incidence of dog rabies and human
rabies deaths continue to escalate, and new outbreaks have been
occurring in areas previously free of the disease (e.g. the islands of
Flores and Bali in Indonesia – [6]; http://wwwn.cdc.gov/travel/
contentRabiesBaliIndonesia2008.aspx).
In this paper, we identify four major reasons commonly given
for the lack of effective domestic dog rabies control including (1)
low prioritisation, (2) epidemiological constraints, (3) operational
constraints and (4) lack of resources (Table 1), focussing on the
situation in Africa. We address each of these issues in turn, using
outputs from modelling approaches and data from field studies to
demonstrate that there are no insurmountable logistic, practical,
epidemiological, ecological or economic obstacles. As a result, we
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conclude that the elimination of canine rabies is a feasible
objective for much of Africa and there should be no reasons for
further delay in preventing the unnecessary tragedy of human
rabies deaths.
Methods
This paper compiles previously published data (see references
below) and additional analyses of those data, but we present a brief
summary of the data collection methods below.
Hospital records of animal-bite injuries compiled from
northwest Tanzania were used as primary data sources. These
data informed a probability decision tree model for a national
disease burden evaluation [7], which has since been adapted for
global estimates of human rabies deaths and Disability-Adjusted
Life Years (DALYs) lost due to rabies [3], a standardized measure
for assessing disease burden [8,9]. Hospital records were also used
to initiate contact tracing studies [10–12], whereby bite-victims
were interviewed to obtain more detail on the source and severity
of exposure and actions taken, allowing subsequent interviews
with other affected individuals (not documented in hospital
records) including owners of implicated animals. Statistical
techniques applied to these data for estimating epidemiological
parameters and inferring transmission links are described
elsewhere [10,12].
Rabies monitoring operations including passive and active
surveillance involving veterinarians, village livestock field officers,
paravets, rangers and scientists were used to collect samples from
carcasses (domestic dogs and wildlife whenever found), which were
subsequently tested and viral isolates were sequenced [10,13–16],
with results being used to inform estimates of rabies-recognition
probabilities [7] and for phylogenetic analyses [10,16]. Opera-
tional research on domestic dog vaccination strategies was carried
out in a variety of settings [14,17]. Household interviews were also
used for socio-economic surveys and to evaluate human:domestic
Author Summary
Elimination of canine rabies has been achieved in some
parts of the world, but the disease still kills many
thousands of people each year in Africa. Here we counter
common arguments given for the lack of effective canine
rabies control in Africa presenting detailed data from a
range of settings. We conclude that (1) rabies substantially
affects public and animal health sectors, hence regional
and national priorities for control ought to be higher, (2)
for practical purposes domestic dogs are the sole
maintenance hosts and main source of infection for
humans throughout most of Africa and Asia and sufficient
levels of vaccination coverage in domestic dog popula-
tions should lead to elimination of canine rabies in most
areas, (3) the vast majority of domestic dog populations
across sub-Saharan Africa are accessible for vaccination
with community sensitization being of paramount impor-
tance for the success of these programs, (4) improved local
capacity in rabies surveillance and diagnostics will help
evaluate the impact of control and elimination efforts, and
(5) sustainable resources for effective dog vaccination
campaigns are likely to be available through the develop-
ment of intersectoral financing schemes involving both
medical and veterinary sectors.
Table 1. Reasons commonly given for the lack of effective dog rabies control.
Reason Explanation Oral evidence Published evidence
LOW
PRIORITISATION
Lack of accurate data on the disease burden
and low recognition among public health
practitioners and policy makers; lack of
inclusion of rabies in global surveys of disease
burden; only recent recognition of rabies as a
neglected tropical disease; statements of rabies
as an ‘insignificant human disease’
Ministries of Health; statements by doctors and health
workers; WHO (up until 2007)
I-VI*
EPIDEMIOLOGICAL
CONSTRAINTS
Abundance of wild animals and uncertainties
about the required levels of vaccination
coverage
SEARG meetings, scientific meetings, national veterinary
meetings; statements from district veterinary officers and
local communities; draft rabies control policies
VII-XIX
OPERATIONAL
CONSTRAINTS
Perception of existence of many inaccessible
stray/ownerless dogs
SEARG meetings, inter-ministerial meetings, national
veterinary meetings; statements from district veterinary and
medical officers, and livestock officers; draft rabies control
policies; international organizations
XX-XXVIII
Owners unwilling or unable to bring dogs for
vaccination
SEARG meetings, inter-ministerial meetings, national
veterinary meetings, scientific meetings; statements by
veterinary and livestock officers
XXIX,XXX
Insufficient knowledge of dog population size
and ecology
SEARG meetings, inter-ministerial meetings, scientific
meetings; statements from veterinary and livestock officers
and wildlife authorities; draft rabies control policies;
international organizations
XIV,XXIV,XXXI
LACK OF
RESOURCES
Weak surveillance and diagnostic capacity SEARG meetings, inter-ministerial meetings; international and
national reference laboratories; international organizations
VI,XXIII,XXIV,XXXII-XXXVIII
Insufficient resources available to veterinary
services
SEARG meetings, inter-ministerial meetings, scientific
meetings, national veterinary meetings; statements from
politicians, veterinary authorities, local communities, wildlife
authorities; international organizations; media
XXVI,XXXIV,XXXVII,XXXIX,XL-XLIII
SEARG = Southern and Eastern Africa Rabies Group.
*Including indirect evidence (e.g. absence of any mention of rabies in published literature indicating lack of priority). See Appendix S1 for references.
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dog ratios, levels of vaccination coverage achieved and reasons for
not bringing animals to vaccination stations [17,18].
The study was approved by the Tanzania Commission for
Science and Technology with ethical review from the National
Institute for Medical Research (NIMR). This retrospective study
involved collection of interview data only, without clinical
intervention or sampling, therefore we considered that informed
verbal consent was appropriate and this was approved by NIMR.
Permission to conduct interviews was obtained from district
officials, village and sub-village leaders in all study locations. At
each household visited, the head of the household was informed
about the purpose of the study and interviews were conducted with
verbal consent from both the head of the household and the bite
victim (documented in a spreadsheet). Approval for animal work
was obtained from the Institutional Animal Care and Use
Committee (IACUC permit #0107A04903).
Results/Discussion
(a) There is not enough evidence to define rabies control
as a priority
A principal factor contributing to a low prioritization of rabies
control has been the lack of information about the burden and
impact of the disease [19,20]. Data on human rabies deaths,
submitted from Ministries of Health to the World Health
Organization (WHO), are published in the annual World Surveys
of Rabies and through the WHO Rabnet site (www.who.int/
rabies/rabnet/en). For the WHO African region (AFRO)
comprising 37 countries, these surveys report an average of 162
human deaths per year between 1988 and 2006. It is therefore
unsurprising that for national and international policy-makers,
rabies pails into insignificance in comparison with other major
disease problems.
This perceived lack of significance of human rabies is reflected
in the absence of any mention of rabies in either of the two
published Global Burden of Disease Surveys [21,22], which
assessed more than 100 major diseases. These surveys adopted the
metric of the DALY which is widely used as the principal tool for
providing consistent, comparative information on disease burden
for policy-making. Until recently no estimates of the DALY
burden were available for rabies.
Official data on human rabies deaths submitted to WHO from
Africa are widely recognized to greatly under-estimate the true
incidence of disease. The reasons for this are manifold: (1) rabies
victims are often too ill to travel to hospital or die before arrival, (2)
families recognize the futility of medical treatment for rabies, (3)
patients are considered to be the victims of bewitchment rather
than disease, (4) clinically recognized cases at hospitals may go
unreported to central authorities, and (5) misdiagnosis is not
uncommon. The problems of misdiagnosis were highlighted by a
study of childhood encephalitis in Malawi, in which 3/26 (11.5%)
cases initially diagnosed as cerebral malaria were confirmed as
rabies through post-mortem tests [23].
Several recent studies have contributed information that
consistently demonstrates that the burden of canine rabies is not
insubstantial.
Human rabies deaths. Estimates of human rabies cases
from modeling approaches, using the incidence of dog-bite injuries
and availability of rabies post-exposure prophylaxis (PEP), indicate
that incidence in Africa is about 100 times higher than officially
reported, with ,24,000 deaths in Africa each year [3,7].
Consistent figures have subsequently been generated from
detailed contact-tracing data: in rural Tanzanian communities
with sporadic availability of PEP (a typical scenario in developing
countries), human rabies deaths occur at an incidence of ,1–5
cases/100,000/year (equivalent to 380–1,900 deaths per year for
Tanzania) [11]. Similarly, a multi-centric study from India
reported 18,500 human rabies deaths per year [24], consistent
with model outputs of 19,700 deaths for India [3].
A crude comparison of annual human deaths for a range of
zoonotic diseases is shown in Figure 1 (top). While diseases such as
Severe Acute Respiratory Syndrome (SARS), Rift Valley Fever
and highly pathogenic avian influenza cause major concerns as a
result of pandemic potential and economic losses, these figures
provide a salutary reminder of the recurrent annual mortality of
rabies and other neglected zoonoses, such as leishmaniasis and
Figure 1. Annual human deaths for a range of zoonoses and
global disability-adjusted life years (DALYs) scores for ne-
glected zoonoses. Top figure - Numbers of human deaths per year
for rabies compared with peak annual deaths from selected epidemic
zoonoses (Severe Acute Respiratory Syndrome, SARS, 2003; H5N1, 2006;
Nipah, 1999; and Rift Valley Fever 2007). Data sources: Rabies (LVII),
Leishmaniasis, Human African Trypanosomiasis (HAT), Chagas Disease
and Japanese Encephalitis (LVIII), SARS (LIX), Influenza A H5N1 (LX),
Nipah (LXI), Rift Valley Fever (LXII,LXIII). See Appendix S1 for references.
Bottom figure - Global DALY scores for neglected tropical diseases
reported in LXIV and LVII and also assuming no post-exposure
treatment (dark grey). See Appendix S1 for references.
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Human African Trypanosomiasis (HAT). Decision-tree models
applied to data from East Africa and globally indicate that the
DALY burden for rabies exceeds that of most other neglected
zoonotic diseases (Figure 1 - bottom) [3,25,26].
Human animal-bite injuries and morbidity. Most of the
rabies DALY burden is attributed to deaths, rather than morbidity
because of the short duration of clinical disease. The DALY
burden for rabies is particularly high, because most deaths occur in
children and therefore a greater number of years of life are lost
[25,27]. DALY estimates incorporate non-rabies mortality and
morbidity in terms of adverse reactions to nerve-tissue vaccines
(NTVs) [3], which are still widely used in some developing
countries such as Ethiopia, however rabies also causes substantial
‘morbidity’ as a direct result of injuries inflicted by rabid animals,
and this is not included in DALY estimates.
Contact-tracing studies suggest an incidence as high as 140/
100,000 bites by suspected rabid animals in rural communities of
Tanzania [11]. Thus, for every human rabies death there are
typically more than ten other rabid animal-bite victims who do not
develop signs of rabies, because they obtain PEP (Figure 1 -
bottom) or are simply fortunate to remain healthy. The severity of
wounds has not yet been quantified, but case-history interviews
suggest that injuries often involve multiple, penetrating wounds
that require medical treatment.
Economic burden. The major component of the economic
burden of rabies relates to high costs of PEP, which impacts both
government and household budgets. With the phasing out of
NTVs, many countries spend millions of dollars importing supplies
of tissue-culture vaccine (,$196 million USD pa [3]).
At the household level, costs of PEP arise directly from anti-rabies
vaccines and from high indirect (patient-borne) costs associated with
travel (particularly given the requirement of multiple hospital visits),
medical fees and income loss [3,28]. Indirect losses, represent
.50% of total costs (Figure 2). Total costs have been estimated
conservatively at $40 US per treatment in Africa and $49 US in Asia
accounting respectively for 5.8% and 3.9% of annual per capita
gross national income [3]. Poor households face difficulties raising
funds which results in considerable financial hardship and
substantial delays in PEP delivery [11,28]. Shortages of PEP, which
are frequent in much of Africa, further increase costs as bite victims
are forced to travel to multiple centres to obtain treatment, also
resulting in risky delays [11].
Additional economic losses relate to livestock losses derived
from an incidence of 5 deaths/100,000 cattle estimated to cost
$12.3 million annually in Africa and Asia [3]. However,
substantially higher incidence has been recorded in Tanzania,
with 12–25 cases/100,000 cattle reported annually in rural
communities (Hampson, unpublished).
Canine rabies introduced from sympatric domestic dog
populations is also recognized as a major threat to endangered
African wild dogs (Lycaon pictus) and Ethiopian wolves (Canis
simensis) [29–32]. Potential losses of tourism revenue may be
substantial; African wild dogs are a major attraction in South
Africa National Parks with the value of a single pack estimated at
$9,000 per year [33] and Ethiopian wolves are a flagship species
for the Bale Mountains National Park.
Psychological impact. An important, but often under-
appreciated component of disease burden is the psychological
impact on bite-victims and their families. In rural Tanzania,
.87% of households with dog bite victims feared a bite from a
suspected rabid animal more than malaria [28] because malaria
can be treated whereas clinical rabies is invariably fatal and
malaria treatment is generally affordable and available locally in
comparison to PEP. When human rabies cases occur, the
horrifying symptoms and invariably fatal outcome result in
substantial trauma for families, communities and health care
workers [34].
(b) Epidemiological constraints
Increasing incidence of rabies in Africa has prompted concerns
that the epidemiology of the disease may be more complex,
involving abundant wildlife carnivores that may sustain infection
cycles [13,35–38]. There is also uncertainty about the level of
vaccination coverage needed to control rabies particularly in
rapidly growing domestic dog populations [39,40].
To eliminate infection, disease control efforts need to be
targeted at the maintenance population [41]. This is clearly
demonstrated for fox rabies in Western Europe, whereby control
of rabies in foxes (through mass oral vaccination) has led to the
disappearance of rabies from all other ‘spill-over’ hosts [42].
Despite the predominance of domestic dog rabies in Africa, the
role of wildlife as independent maintenance hosts has been
debated, and many perceive the abundance of wildlife as a barrier
to elimination of canine rabies on the continent. It has also been
argued that the predominance of dog rabies is an artefact of poor
surveillance and under-reporting in wildlife populations [43].
In the wildlife-rich Serengeti ecosystem in Tanzania, evidence
suggests that domestic dogs are the only population essential for
maintenance [10,13,16]: (1) phylogenetic data showed only a
single southern Africa canid-associated variant (Africa 1b)
circulating among different hosts [16]; (2) transmission networks
suggested that, for wildlife hosts, within-species transmission
cannot be sustained [16]; and (3) statistical inference indicated
that cross-species transmission events from domestic dogs resulted
in only relatively short-lived chains of transmission in wildlife with
no evidence for persistence [10]. The conclusion that domestic
Figure 2. Economic burden of canine rabies (data source: LVII in Appendix S1). PET, Post-exposure treatment.
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dogs are the only maintenance population in such a species-rich
community suggests that elimination of canine rabies through
domestic dog vaccination is a realistic possibility, and provides
grounds for optimism for wider-scale elimination efforts in Africa.
In other parts of central and west Africa, transmission of rabies
appears to be driven by domestic dogs [44]. An outstanding
question relates to southern Africa. Earlier and recent evidence
indicate that jackal species (Canis mesomelas and C. adustus) and
bat-eared foxes (Otocyon megalotis) may maintain the canid variant
in specific geographic loci in South Africa and Zimbabwe
[2,36–38,45–50], but it is still not clear whether these cycles can
be sustained over large spatial and temporal scales in the absence
of dog rabies [13,51,52]. Independent wildlife cycles may preclude
continent-wide elimination of this variant through dog vaccination
alone and wildlife rabies control strategies, in conjunction with dog
vaccination, may need to be considered in specific locations [38].
A critical proportion of the population must be protected (P
crit
)to
eliminate infection and this threshold can be calculated from the
basic reproductive number (R
0
, defined as the average number of
secondary infections caused by an infected individual in a
susceptible population) [53]. Vaccinating a large enough proportion
of the population to exceed P
crit
will not only protect the vaccinated
individuals but will reduce transmission such that, on average, less
than one secondary infection will result from each primary case
(effective reproductive number, R
e
,1), which can ultimately lead to
elimination. Vaccination has eliminated canine rabies in many
countries demonstrating the success of this concept [54]. However,
theory suggests that R
0
increases with population density [39] and
thus higher coverage will be needed in higher density populations.
However, evaluation of historical outbreak data from around the
world and recent data from Tanzania indicate that R
0
in domestic
dog populations is consistently low (between 1.0 and 2.0) [12],
confirming the feasibility of rabies elimination through vaccination
in African domestic dog populations.
An important conclusion of this study was that in populations
with rapid turnover (such as those in many African countries) at
least 60% of the population must be vaccinated during annual
campaigns to prevent coverage falling below P
crit
between
campaigns. Data from Africa clearly show that very few control
efforts have reached these levels of coverage [Table 2], which is
why rabies remains a persistent problem [12]. Although
emergence of new variants maintained in wildlife also remains a
possibility, as shown in the USA, where wildlife rabies now
dominates since elimination of canine rabies [55]. For Africa, these
questions are likely only to be resolved with large-scale
intervention involving mass vaccination of dogs.
(c) Operational constraints
Several arguments are given for why mass vaccination
campaigns have failed to achieve the high levels of coverage that
are necessary to interrupt rabies transmission. We counter these
arguments below:
A perception of many inaccessible stray/ownerless
dogs. A common claim is that the majority of dogs in Africa
are unowned ‘stray’ animals, and therefore inaccessible for
parenteral vaccination. It is not hard to see why this perception
has arisen - unrestrained dogs, without any apparent evidence of
ownership, are commonly observed. Further investigation,
however, usually reveals that the vast majority are owned, and
at least one household claims some responsibility, including
presentation for vaccination. Published studies in Africa, which
quantify the proportion of unowned dogs, are admittedly sparse,
but all support this observation [56–58]. Capture-mark-recapture
methodologies and household questionnaires used in African
Table 2. Reported and estimated vaccination coverages in domestic dog populations from various settings in sub-Saharan Africa
since 1990.
Region Country Dates
Vaccines
delivered Dog population
Estimated
coverage (%) Source of data and notes
N’djamena Chad 2001 23,560 19.00 XLV
Machakos Kenya 1992 24.00 XIV
National Kenya 2003 33.00 XXXIX
Mzuzu Malawi 1996–2000 7823* 44,932 12.1–20.2 XLVII
National Mozambique 1997–2000 175,769* 7,000,000 ,1 XLVIII
Northern communal land Namibia 2001 115,000 12.00 XXIX
Borno State (urban) Nigeria 2007 ,46.00 XLIX
Borno State (rural) Nigeria 2007 ,15.6 XLIX
National Sudan 1992–2002 37,620* 71,540 5.26 Dog population from 1992 census data
reported in XXXVI
Khartoum state Sudan 2000 2,946 91,000 3.24 L
National Swaziland 1994–1998 57,204 63.2–91.7 (dropped
to 3% in 1998)
LI
National Tanzania 1992 11,635 ,1 Extrapolated from LII using human:dog ratios
from XLVI, census data from LIII and estimated
dog population growth rates from LIV
National Uganda 2001–2003 16.00 XXVI
National Zimbabwe 2002 314,319 1,300,000 13.93 Extrapolated from LV, with dog population
sizes and growth rates in 1986 from LVI
Targeted mass vaccination campaigns carried out by research projects have been excluded (e.g. XLIV-XLVI).
*Indicates total vaccinations delivered over stated period. See Appendix S1 for references.
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settings have all found consistently low estimates (Tunisia ,7%
[57], 1%, 8% and 11% in three sites in N’Djamena, Chad [56],
and 1% in a peri-urban site in Tanzania [58]). Notably, the
Tanzanian site was selected specifically on the basis of reports of
many unowned dogs. While mark-recapture methods yield reliable
estimates of unowned dog numbers, their implementation and
analysis is not trivial and efforts are underway to develop simpler,
yet robust methodologies [59]. Certainly in traditional Africa, i.e.
most of sub-Saharan Africa, the issue of roaming dogs seems not to
be one of a lack of ownership, but rather an inability or
unwillingness by owners to confine their dogs.
Unwillingness/inability to bring dogs for
vaccination. Published studies tend to refute the idea that
owners are often unable or unwilling to restrain their dogs for
parenteral vaccination. A multi-country WHO-commissioned
study (Tunisia, Sri Lanka and Ecuador) concluded that ‘‘dogs
which are not catchable by at least one person are rare and
represent generally less than 15% of the dog population’’ [57].
Similarly a study from Nepal found that 86–97% of dogs were
accessible to parenteral vaccination [60]. Although an early study
in Turkey concluded that 48% of all free-roaming owned dogs
could not be captured by their owners [61], more recent surveys
found that most unvaccinated dogs could be handled (only 16%
could not) and that a much larger proportion (56%) resulted from
a lack of information about the campaign – a much easier problem
to remedy (unpublished data). In Africa, very similar figures were
obtained in a multi-site study in urban and rural Tanzania, where
only 15% of vaccination failures were due to a reported inability
by the owner to handle the dog, while 53% of cases were due to
poor information dissemination [17]. However, there may be
settings in transitional Africa (e.g. parts of southern Africa
including KwaZulu Natal [2]) where handling of dogs is more
difficult due to a break-down in traditional animal husbandry and
other social factors, and more intensive efforts may be required for
these special cases.
Given that most dogs are accessible for parenteral vaccination,
high coverage can be achieved with well-planned vaccination
campaigns. During pilot programmes in urban and rural Africa
which have not charged owners for vaccination, coverages
obtained have exceeded 60% [14,17,56]. Pastoral communities
pose particular challenges due to remote locations and semi-
nomadic lifestyles, but .80% coverages can still be achieved
through house-to-house delivery strategies or community-based
animal health workers [17].
Young pups usually make up a large proportion (.30%) of
African dog populations [62] and there is a widespread perception
among veterinary authorities and dog owners that they should not
be vaccinated, which leads to insufficient coverage [17]. However,
rabies vaccines can safely be administered to pups ,3 months of
age [63], and in village campaigns in Tanzania, vaccines
consistently induced high levels (.0.5 IU/ml) of rabies virus
neutralizing antibody [64]. The issue of inclusion of pups can
effectively be addressed through appropriate advertising before
campaigns.
Cost-recovery, through charging dog owners for rabies
vaccination, is widely promoted for sustainable programmes and
to encourage responsible dog ownership. However, charging for a
vaccination that represents a public rather than a private good,
can be counterproductive, resulting in low turnouts and coverage
(,30%) with little or no impact [65]. Charging for vaccination
may indeed be the principal reason why owners are unwilling to
bring dogs for vaccination.
Ineffective campaigns that achieve ,30% coverage are a waste
of resources and can be highly demoralising for veterinary staff
and communities. When resources are spread thinly, such that
only low coverage is achieved or only small pockets are well
vaccinated, then large-scale failure is inevitable. A more
epidemiologically sensible strategy is to focus resources into a
single (preferably well-bounded) area where high coverage can be
consistently achieved.
Uncertainty about dog population sizes and ecology for
effective design and planning of vaccination
campaigns. Official figures used for planning frequently
underestimate true population sizes. For example, Gsell [58]
found that the owned dog population in a municipality in
Tanzania was six times larger than official records. Although
standard survey methodologies for estimating dogs/household or
dog:human ratios [57,66–68] are not without problems (for
example, double ownership of dogs), a rough estimate of owned
dog populations can be derived from national (human) population
censuses, and can be corrected for different demographic and
ecological settings [18,69]. More detailed studies can be conducted
to identify key household determinants of dog ownership (for
example, religion, age and sex of household heads, household
size, socio-economic level, and livestock presence/absence
[18,28,70,71]. Such determinants have been used to generate a
‘dog density’ map of Tanzania, for assistance in planning national
rabies vaccination campaigns (Figure 3).
(d) Lack of resources
The above factors are all generally described as obstacles that
ultimately lead to a lack of investment into rabies control and
surveillance. We suggest that investment would actually reap
multiple benefits including economic ones, if appropriate strategies
are implemented overcoming the constraints described.
A lack of surveillance and diagnostic capacity for rabies
detection. Poor surveillance and diagnosis capacity means that
Figure 3. ‘Dog density’ map of Tanzania (courtesy of
Hawthorne Beyer; data source: LXV in Appendix S1). Hashed
areas represent the location of wildlife protected areas.
doi:10.1371/journal.pntd.0000626.g003
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(1) data is insufficient to demonstrate disease burden and motivate
policy-makers, and (2) impacts of control efforts cannot be
evaluated.
Considerable progress has been made in the development of
simple and inexpensive techniques for sample preservation and
rapid post-mortem diagnosis suitable for laboratories with limited
storage and/or diagnostic resources with potential to increase in-
country capabilities for surveillance. A new direct rapid immuno-
histochemical test (dRIT) requires only light microscopes [72],
which are widely available. The test is simple and can be
performed by a range of operators if appropriate training is
provided. Field evaluation studies in Africa demonstrated that this
assay has characteristics equivalent to those of the direct
fluorescent antibody (DFA) test, the global standard for rabies
diagnosis, including excellent performance on glycerolated field
brain material [15,73], the preservative of choice under field
conditions [74,75]. Other simple field-diagnostics that allow rapid
screening, including enzyme immunoassays [76], dot blot enzyme
immunoassays [77] and lateral-flow immunodiagnostic test kits
[78,79] are being evaluated. These tools offer hope of extending
diagnostic capacity in resource-limited settings.
Animal-bite injury data from hospitals are an easily accessible
source of epidemiological information and have been verified as
reliable indicators of animal rabies incidence and human
exposures [11,14]. Furthermore, increasing availability of com-
munication infrastructure through mobile phone network access in
remote areas could enhance surveillance by allowing real-time
reporting.
Costs of effective dog vaccination campaigns are beyond
the budget of veterinary services. Veterinary services in
Africa usually report very limited budgets and often have to divert
resources during outbreaks of other diseases [80,81]. This is clearly
the most significant constraint to effective rabies control. However,
with increasing human and dog populations, dog rabies incidence,
human exposures to rabies and the costs required to prevent
human rabies deaths through PEP will invariably continue to rise
unless rabies can be controlled at the source, i.e. in domestic dog
populations [82]. Many countries in Asia, such as Thailand,
Vietnam and Sri Lanka have greatly reduced human rabies deaths
through increased PEP use, but at a very high cost [83]. In
Vietnam, for example, deaths fell from 285 in 1996 to 82 in 2006
with administration of .600,000 PEP courses per year at an
estimated cost of ,$27 million/year [84].
Although domestic dog populations need to be targeted for the
effective control of rabies, this is usually deemed to be the
responsibility of veterinary services even though many of the
benefits accrue to the medical sector. In rural Tanzania, dog
vaccination campaigns led to a rapid and dramatic decline in
demand for costly human PEP [14]. In pastoral communities,
vaccination not only reduced rabies incidence, but has now
resulted in a complete absence of exposures reported in local
hospitals for over two years (Figure 4).
Large-scale campaigns can therefore translate into human lives
and economic savings through reduced demand for PEP. Costs
per dog vaccinated are generally estimated to be low (rural
Tanzania ,$1.73 [17], Philippines ,$1.19–4.27 [85], Tunisia
,$1.3 [86], Thailand ,$1.3 [86] and Urban Chad ,$1.8 [87])
and preliminary studies suggest that including dog vaccination in
human rabies prevention strategies would be a highly cost-effective
intervention at ,US $25/DALY averted (S. Cleaveland, unpub-
lished data; see also 82).
Developing joint financing schemes for rabies prevention and
control across medical and veterinary sectors would provide a
mechanism to use savings in human PEP to sustain rabies control
programs in domestic dogs. Although conceptually simple, the
integration of budgets across different Ministries is likely to pose
political and administrative challenges. However, given sufficient
political will and commitment, developing sustained programmes
of dog vaccination that result in canine rabies elimination should
be possible.
In conclusion, here we show that a substantial body of
epidemiological data have now been gathered through multiple
studies demonstrating that: (1) rabies is an important disease that
exerts a substantial burden on human and animal health, local and
national economies and wildlife conservation, (2) domestic dogs
are the sole population responsible for rabies maintenance and
main source of infection for humans throughout most of Africa
and Asia and therefore control of dog rabies should eliminate the
disease, (3) elimination of rabies through domestic dog vaccination
is epidemiologically feasible, (4) the vast majority of domestic dog
populations across sub-Saharan Africa are accessible for vaccina-
tion and the few remaining factors compromising coverage can be
addressed by engaging communities through education and
awareness programs, (5) new diagnostic and surveillance ap-
proaches will help evaluate the impact of interventions and focus
efforts towards elimination, and (6) dog rabies control is affordable,
but is likely to require intersectoral approaches for sustainable
programmes that will be needed to establish rabies-free areas.
Supporting Information
Appendix S1 Appendix with additional references.
Found at: doi:10.1371/journal.pntd.0000626.s001 (0.07 MB
DOC)
Acknowledgments
We are indebted to the Ministries of Livestock Development and Fisheries
and of Public Health and Social Welfare, Tanzania National Parks,
Tanzania Wildlife Research Institute, Ngorongoro Conservation Area
Authority, Tanzania Commission for Science and Technology, and
National Institute for Medical Research for permission and collaboration;
the Frankfurt Zoological Society and the Mwanza and Arusha Veterinary
Figure 4. Number of cases of bite injuries reported to hospitals
in pastoralist communities to the east of Serengeti National
Park (north-western Tanzania). Numbers are recorded as a result of
bites from both rabid and normal healthy animals as well as those of
unknown status (either the bite victims could not be traced, or
insufficient information could be obtained during interviews to make
an informed judgement about the health of the biting animal). The
arrows mark the end of successive dog vaccination campaigns.
doi:10.1371/journal.pntd.0000626.g004
Feasibility of Canine Rabies Elimination
www.plosntds.org 7 February 2010 | Volume 4 | Issue 2 | e626
Investigation Centres for logistical and technical support; Intervet for
providing vaccines; Andy Dobson, Craig Packer, Dominic Travis and
Karen Laurenson for helpful discussions; and Hawthorne Beyer for
assistance with Figure 3. We are particularly grateful to Machunde
Bigambo, Iddi Lipende, Kaneja Ibrahim Mangaru, Israel Silaa, Imam
Mzimbiri, Mathias Magoto, Emmanuel Sindoya, and Paul Tiringa for
their hard work in the field.
We would like to acknowledge the enormous contributions to these studies
by Magai Kaare, who tragically died on the 6th of October 2008 as a
consequence of a car accident in Tanzania. His work has been highly
influential in shaping rabies policy in Tanzania and worldwide. Magai’s
death is a grave loss and he will be great ly m i ss ed.
Author Contributions
Conceived and designed the experiments: TL KH MTK DK RRK DTH
SC. Performed the experiments: TL KH MTK EE DK RRK DTH SC.
Analyzed the data: TL KH MTK DK DTH SC. Wrote the paper: TL KH
DK SC.
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Supplementary resource (1)

... BP 74., 1002 Tunis, Tunisia Full list of author information is available at the end of the article Trabelsi et al. BMC Biotechnology (2022) 22:17 annually in Africa and Asia [6]. Furthermore, studies have estimated the global burden of canine rabies to approximately 124 billion dollars per year [7]. ...
... For example, Turkey reports an incidence rate of 0.10 to 3.87 cases/100 000 cattle [29]. Substantially higher incidence has been reported in Tanzania with 12-25 cases/100 000 cattle annually in rural communities [6]. Annual livestock loss was estimated to accumulate to $12.3 million in Africa and Asia [3]. ...
Article
Full-text available
Background Mass vaccination of dogs as important rabies reservoir is proposed to most effectively reduce and eliminate rabies also in humans. However, a minimum coverage of 70% needs to be achieved for control of the disease in zoonotic regions. In numerous developing countries, dog vaccination rate is still dangerously low because of economic constraints and due to a high turnover in dog populations. Improved vaccine production processes may help to alleviate cost and supply limitations. In this work, we studied and optimized the replication and vaccine potency of PV rabies virus strain in the muscovy-duck derived AGE1.CR and AGE1.CR.pIX suspension cell lines. Results The BHK-21-adapted PV rabies virus strain replicated efficiently in the avian cell lines without requirement for prior passaging. CR.pIX was previously shown to augment heat shock responses and supported slightly higher infectious titers compared to the parental CR cell line. Both cell lines allowed replication of rabies virus also in absence of recombinant IGF, the only complex component of the chemically defined medium that was developed for the two cell lines. After scale-up from optimization experiments in shake flask to production in 7-l bioreactors peak virus titers of 2.4 × 10⁸ FFU/ml were obtained. The potency of inactivated rabies virus harvest according to the NIH test was 3.5 IU/ml. Perfusion with the chemically defined medium during the virus replication phase improved the potency of the vaccine twofold, and increased the number of doses 9.6 fold. Conclusion This study demonstrates that a rabies vaccine for animal vaccination can be produced efficiently in the AGE1.CR.pIX suspension cell line in a scalable process in chemically defined medium.
... Despite these reasons, rabies remains endemic in many settings and only limited dog vaccination is undertaken. A possible concern should mass dog vaccination be scaled up is that, despite the critical vaccination threshold being low, to sustain vaccination coverage above this level over the course of the year, annual vaccination campaigns must reach a higher proportion of dogs, of around 70% [1,7,8]. ...
... However, annual team-delivered approach (subsequently referred to in this study as the pulse approach) is affected by several factors that limit its ability to achieve and sustain vaccination coverages above the critical threshold to control rabies. These include: high rates of dog population turnover in most endemic countries, which results in rapid declines in population immunity in the interval between annual campaigns [9,10]; teams needing to travel long distances on dirt roads from cold chain facilities, which is sometimes possible only at certain times of the year; campaign day(s) being negatively affected by agricultural cycles, inclement weather, school days, funerals, and local festivals [8]; high fixed vehicle and personnel costs, with the cost-per-dog vaccinated reaching as high as $7.36 [11][12][13]. ...
Article
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Objectives Dog vaccination can eliminate rabies in dogs, but annual delivery strategies do not sustain vaccination coverage between campaigns. We describe the development of a community-based continuous mass dog vaccination (CBC-MDV) approach designed to improve and maintain vaccination coverage in Tanzania and examine the feasibility of delivering this approach as well as lessons for its optimization. Methods We developed three delivery strategies of CBC-MDV and tested them against the current annual vaccination strategy following the UK Medical Research Council’s guidance: i) developing an evidence-based theoretical framework of intervention pathways and ii) piloting to test feasibility and inform optimization. For our process evaluation of CBC-MDV we collected data using non-participant observations, meeting reports and implementation audits and in-depth interviews, as well as household surveys of vaccination coverage to assess potential effectiveness. We analyzed qualitative data thematically and quantitative data descriptively. Results The final design included delivery by veterinary teams supported by village-level one health champions. In terms of feasibility, we found that less than half of CBC-MDV’s components were implemented as planned. Fidelity of delivery was influenced by the strategy design, implementer availability and appreciation of value intervention components, and local environmental and socioeconomic events (e.g. elections, funerals, school cycles). CBC-MDV activities decreased sharply after initial campaigns, partly due to lack of supervision. Community engagement and involvement was not strong. Nonetheless, the CBC-MDV approaches achieved vaccination coverage above the critical threshold (40%) all-year-round. CBC-MDV components such as identifying vaccinated dogs, which village members work as one health champions and how provision of continuous vaccination is implemented need further optimization prior to scale up. Interpretation CBC-MDV is feasible to deliver and can achieve good vaccination coverage. Community involvement in the development of CBC-MDV, to better tailor components to contextual situations, and improved supervision of activities are likely to improve vaccination coverage in future.
... In pursuit of the goal to eliminate dog-mediated rabies, risk-based regionalization, and application of consistent and targeted approaches are commonly proposed when conducting disease surveillance and control programs in resource-limited environments instead of spreading the resources thinly across an entire geographic region [1,12,13]. In an attempt to support such programmatic efforts, we used a risk-estimation approach that makes use of available data. ...
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Despite ongoing control efforts, rabies remains an endemic zoonotic disease in many countries. Determining high-risk areas and the space-time patterns of rabies spread, as it relates to epidemiologically important factors, can support policymakers and program managers alike to develop evidence-based targeted surveillance and control programs. In this One Health approach which selected Thailand as the example site, the location-based risk of contracting dog-mediated rabies by both human and animal populations was quantified using a Bayesian spatial regression model. Specifically, a conditional autoregressive (CAR) Bayesian zero-inflated Poisson (ZIP) regression was fitted to the reported human and animal rabies case counts of each district, from the 2012–2017 period. The human population was used as an offset. The epidemiologically important factors hypothesized as risk modifiers and therefore tested as predictors included: number of dog bites/attacks, the population of dogs and cats, number of Buddhist temples, garbage dumps, animal vaccination, post-exposure prophylaxis, poverty, and shared administrative borders. Disparate sources of data were used to improve the estimated associations and predictions. Model performance was assessed using cross-validation. Results suggested that accounting for the association between human and animal rabies with number of dog bites/attacks, number of owned and un-owned dogs; shared country borders, number of Buddhist temples, poverty levels, and accounting for spatial dependence between districts, may help to predict the risk districts for dog-mediated rabies in Thailand. The fitted values of the spatial regression were mapped to illustrate the risk of dog-mediated rabies. The cross-validation indicated an adequate performance of the spatial regression model (AUC = 0.81), suggesting that had this spatial regression approach been used to identify districts at risk in 2015, the cases reported in 2016/17 would have been predicted with model sensitivity and specificity of 0.71 and 0.80, respectively. While active surveillance is ideal, this approach of using multiple data sources to improve risk estimation may inform current rabies surveillance and control efforts including determining rabies-free zones, and the roll-out of human post-exposure prophylaxis and anti-rabies vaccines for animals in determining high-risk areas.
... There are increasing reports of the inadequacies of this approach among important subpopulations of susceptible dogs. Perhaps the greatest challenge is maintaining adequate herd immunity in free-roaming dog populations [14][15][16]. A promising alternative solution to this problem maybe oral rabies vaccination (ORV) [16,17]. ...
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Dog-mediated rabies is responsible for tens of thousands of human deaths annually, and in resource-constrained settings, vaccinating dogs to control the disease at source remains challenging. Currently, rabies elimination efforts rely on mass dog vaccination by the parenteral route. To increase the herd immunity, free-roaming and stray dogs need to be specifically addressed in the vaccination campaigns, with oral rabies vaccination (ORV) of dogs being a possible solution. Using a third-generation vaccine and a standardized egg-flavoured bait, bait uptake and vaccination was assessed under field conditions in Namibia. During this trial, both veterinary staff as well as dog owners expressed their appreciation to this approach of vaccination. Of 1,115 dogs offered a bait, 90% (n = 1,006, 95%CI:91–94) consumed the bait and 72.9% (n = 813, 95%CI:70.2–75.4) of dogs were assessed as being vaccinated by direct observation, while for 11.7% (n = 130, 95%CI:9.9–17.7) the status was recorded as “unkown” and 15.4% (n = 172, 95%CI: 13.4–17.7) were considered as being not vaccinated. Smaller dogs and dogs offered a bait with multiple other dogs had significantly higher vaccination rates, while other factors, e.g. sex, confinement status and time had no influence. The favorable results of this first large-scale field trial further support the strategic integration of ORV into dog rabies control programmes. Given the acceptance of the egg-flavored bait under various settings worldwide, ORV of dogs could become a game-changer in countries, where control strategies using parenteral vaccination alone failed to reach sufficient vaccination coverage in the dog population.
... Rabies is a fatal zoonotic disease caused by viruses of the Rhabdoviridae family (Lyssavirus genus and order of the Mononegavirales) [1,2]. Every year, at least 59,000 human rabies deaths are estimated to occur throughout the world [3], with the exception of nation islands. ...
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Background: Rabies is a fatal zoonotic disease that is maintained in domestic dogs and wildlife populations in the Republic of South Africa. A retrospective study was conducted to improve understanding of the dynamics of rabies in humans, domestic dogs, and wildlife species, in relation to the ecology for three northern provinces of South Africa (Limpopo, Mpumalanga, and North-West) between 1998 and 2017. Methods: A descriptive epidemiology study was conducted for human and animal rabies. Dog rabies cases were analyzed using spatio-temporal scan statistics. The reproductive number (Rt) was estimated for the identified disease clusters. A phylogenetic tree was constructed based on the genome sequences of rabies viruses isolated from dogs, jackals, and an African civet, and Bayesian evolutionary analysis using a strict time clock model. Several ecological and socio-economic variables associated with dog rabies were modeled using univariate analyses with zero-inflated negative binomial regression and multivariable spatial analyses using the integrated nested Laplace approximation for two time periods: 1998-2002 and 2008-2012. Results: Human rabies cases increased in 2006 following an increase in dog rabies cases; however, the human cases declined in the next year while dog rabies cases fluctuated. Ten disease clusters of dog rabies were identified, and utilizing the phylogenetic tree, the dynamics of animal rabies over 20 years was elucidated. In 2006, a virus strain that re-emerged in eastern Limpopo Province caused the large and persistent dog rabies outbreaks in Limpopo and Mpumalanga Provinces. Several clusters included a rabies virus variant maintained in jackals in Limpopo Province, and the other variant in dogs widely distributed. The widely distributed variant maintained in jackal populations in North-West Province caused an outbreak in dogs in 2014. The Rt was high when the disease clusters were associated with either multiple virus strains or multiple animal species. High-risk areas included Limpopo and Mpumalanga Provinces characterized by woodlands and high temperatures and precipitation. Conclusion: Canine rabies was maintained mainly in dog populations but was also associated with jackal species. Rural communities in Limpopo and Mpumalanga Provinces were at high risk of canine rabies originating from dogs.
... While all the species in the Lyssavirus genus are causative agents for the disease rabies, the prototype member is Rabies lyssavirus (RABV), which has the greatest public health impact due to its association with domestic dogs (Canis lupus familiaris) [2]. While canine-mediated rabies has been eliminated from some regions and territories around the world [3,4], the disease is still endemic to every landmass except for Antarctica and a few isolated islands [2]. ...
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Rabies is a viral zoonosis that causes an estimated 59,000 preventable human fatalities every year. While more than 120 countries remain endemic for dog-mediated rabies, the burden is the highest in Africa and Asia where 99% of human rabies cases are caused by domestic dogs. One such rabies-endemic country is South Africa where an estimated 42 preventable human deaths occur every year. Although canine rabies had been well described for most of the provinces in South Africa, the epidemiology of rabies within the North West Province had not been well defined prior to this investigation. As such, the aim of this study was to use nucleotide sequence analyses to characterise the extant molecular epidemiology of rabies in the North West Province of South Africa—with specific focus on the interface between dogs and sylvatic species. To this end, Rabies lyssavirus isolates originating from the North West Province were subjected to molecular epidemiological analyses relying on the Bayesian Markov Chain Monte Carlo methodology on two distinct gene regions, viz. the G-L intergenic region and partial nucleoprotein gene. Our results provided strong evidence in support of an endemic cycle of canine rabies in the East of the province, and three independent endemic cycles of sylvatic rabies spread throughout the province. Furthermore, evidence of specific events of virus spill-over between co-habiting sylvatic species and domestic dogs was found. These results suggest that the elimination of canine-mediated rabies from the province will rely not only on eliminating the disease from the dog populations, but also from the co-habiting sylvatic populations using oral rabies vaccination campaigns.
Article
Rabies is a lethal zoonotic disease mainly transmitted to humans by dog bites. The purpose of this study was to assess the efficacy of rabies control policies in Japan, which resulted in the elimination of the disease from the country in 1957. Using historical records from the Kanto region (Chiba, Kanagawa, Saitama and Tokyo Prefectures) between 1947 and 1956 where the final canine cases were recorded, we undertook a descriptive epidemiological study, applying spatio‐temporal scan statistics using SaTScan and estimating the effective reproduction number (Rt) for the clusters and each prefecture using the growth rates. There were 1,567 dog rabies and 161 human rabies cases recorded during this period. Vaccination coverage in registered dogs was over 70% after 1951, with much lower coverage in free‐roaming and unregistered dogs. Eight clusters of dog rabies cases were identified: the first appeared in 1947 in Tokyo and was linked to three further clusters in peripheral prefectures between 1947 and 1951. Three more clusters occurred in Tokyo again between 1952 and 1954, and the last cluster was in Tokyo and Kanagawa between 1955 and 1956. Rt in the first cluster was 1.68, and Rt values in the others ranged between 1.18 and 1.86, with an exception of 4.05 in the smallest cluster in Tokyo in 1952 (10 cases). The moving average of Rt coincided with the clusters. As dog vaccination and dog management progressed, and the number of dog rabies cases declined, the moving average of Rt declined to below 1. Delays in the implementation of dog management policies in Kanagawa may have prolonged this last outbreak. These results demonstrate the effectiveness of coordinated control policy involving dog vaccination and management of free‐roaming dog populations for rabies elimination.
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Human rabies can be prevented through mass dog vaccination campaigns; however, in rabies endemic countries, pulsed central point campaigns do not always achieve the recommended coverage of 70%. This study describes the development of a novel approach to sustain high coverage based on decentralized and continuous vaccination delivery. A rabies vaccination campaign was conducted across 12 wards in the Mara region, Tanzania to test this approach. Household surveys were used to obtain data on vaccination coverage as well as factors influencing dog vaccination. A total 17,571 dogs were vaccinated, 2654 using routine central point delivery and 14,917 dogs using one of three strategies of decentralized continuous vaccination. One month after the first vaccination campaign, coverage in areas receiving decentralized vaccinations was higher (64.1, 95% Confidence Intervals (CIs) 62.1–66%) than in areas receiving pulsed vaccinations (35.9%, 95% CIs 32.6–39.5%). Follow-up surveys 10 months later showed that vaccination coverage in areas receiving decentralized vaccinations remained on average over 60% (60.7%, 95% CIs 58.5–62.8%) and much higher than in villages receiving pulsed vaccinations where coverage was on average 32.1% (95% CIs 28.8–35.6%). We conclude that decentralized continuous dog vaccination strategies have the potential to improve vaccination coverage and maintain herd immunity against rabies.
Thesis
Rabies is an ancient zoonotic disease that still persists as significant public health problem affecting largely poor and marginalized people in poor countries of the developing world. The disease is also a cause of substantial wildlife conservation concern and an economic burden to governments where it occurs. However, the disease is grossly under-reported in most developing countries, with the result that the burden of the disease is widely under estimated and rabies perceived to be an insignificant problem. Although human rabies is completely preventable, through vaccination of animal reservoirs and post-exposure prophylaxis (PEP) of people exposed to the virus, no effective large-scale control of rabies has been achieved in sub-Saharan Africa in the past 30 years and information is still needed to optimise and sustain dog vaccination programmes. In Chapter 2, data obtained through a mass domestic dog vaccination campaign in northwest Tanzania are used to investigate strategic factors that influence the design and effectiveness of domestic dog rabies vaccination campaigns in rural Africa. The findings of this study show the feasibility of controlling rabies in a wide range of agro-pastoral socio-economic settings in rural Tanzania through central point based vaccine delivery approach and demonstrate that the use of combined central point and community-based animal-health workers (CAHWs) offers an effective alternative to central point approach as a vaccine delivery strategy in remote and dispersed pastoral communities. In Chapter 3, the economic burden of rabies at the household level is evaluated; the study demonstrates that rabies is a substantial economic concern to households in rural Tanzania, disproportionately affecting households with low socio economic status. It is also shown that dog bite victims with low socio economic status are at higher risk of dying from rabies. The per capita cost for dog vaccination and potential benefits of domestic dog vaccination in agro-pastoral and pastoral communities are estimated in Chapter 4. The per capita cost for central point dog vaccination is estimated as $1.73 and 5.56 in the agro- pastoral and pastoral communities respectively. The study also shows that rabies control through domestic dog vaccination will results in substantial net benefits to the public health sector. In Chapter 5, using both cross sectional and longitudinal data, the impact of multivalent vaccination of domestic dogs against rabies, canine distemper, canine parvo virus and canine hepatitis virus on the demography of the dog population is investigated over two consecutive years, demonstrating a significant increase in survival and dog population growth in vaccinated dogs (vaccination zone) in comparison with unvaccinated (control zone) dog populations in adjacent areas. In Chapter 6 the study demonstrates a substantial decline in incidence of human and animal rabies as a result of dog vaccination. However, despite a decline in reporting of animal rabies cases and human bite injuries from suspected rabid dogs, use of PEP at district hospitals did not decline. In Chapter 7 data from previous chapters are used to parameterise a spatially explicit stochastic model to theoretically explore the optimal design of domestic dog mass vaccination campaigns in rural Tanzania. The results of the model demonstrate that inter-vaccination interval and vaccination coverage are likely to be critical factors in designing domestic dog mass vaccination programmes in rural Tanzania. In Chapter 8 the implications of the findings in previous chapters are discussed to show that rabies control is economically and logistically feasible in Tanzania and a multi sectoral approach to rabies control is proposed as a way forward for the country.
Thesis
Rabies, one of the oldest diseases known to man, remains uncontrolled in many parts of the world. This is in spite of the availability of safe, effective and economical tools for its control. The wide-spread distribution and rapid growth of its primary reservoir host population in the developing world, the domestic dog, together with their ubiquitous association with human populations, explains why canine rabies is endemic across much of the globe. However, given that effective dog vaccines are available, and that rabies has been eliminated from dog populations in many countries (including large, non-island countries like the United States) through the implementation of these vaccines and other control measures, why does the disease continue to exact such a toll in other countries? One reason must be a lack of political and institutional will to tackle the problem. This in turn is based in part on a lack of awareness of the extent of the problem, coupled with competing interests for scarce public health resources. Reliance on the reporting of rabies cases via official channels may lead to underestimation of the true incidence of the disease by up to one hundred-fold, and a subsequent lack of prioritisation of resources for its control. This leads to a vicious circle of neglect - low priority means no resources available for surveillance, which in turn ensures that the true extent of disease occurrence remains unknown. It is hoped that the quantitative estimates of rabies burden presented in Chapter 2 will redress this, and provide impetus for policy makers and donors to tackle the problem. One advantage of the quantitative risk assessment method used in Chapter 2 is its transparency - as more detailed data become available so the model can be updated and refined. Knowledge of the estimated burden of the disease, together with preliminary data which shows that, in terms of cost per DALY saved, rabies is among one of the most cost-effective diseases to target (through the mass vaccination of dogs), have already encouraged international health agencies and donors to reconsider their prioritisation of this disease. In this respect, further research is needed to develop more refined models of cost-effectiveness estimates across different time horizons and under different epidemiological scenarios.
Article
Detailed assumptions used in constructing a new indicator of the burden of disease, the disability-adjusted life year (DALY), are presented. Four key social choices in any indicator of the burden of disease are carefully reviewed. First, the advantages and disadvantages of various methods of calculating the duration of life lost due to a death at each age are discussed. DALYs use a standard expected-life lost based on model life-table West Level 26. Second, the value of time lived at different ages is captured in DALYs using an exponential function which reflects the dependence of the young and the elderly on adults. Third, the time lived with a disability is made comparable with the time lost due to premature mortality by defining six classes of disability severity. Assigned to each class is a severity weight between 0 and 1. Finally, a three percent discount rate is used in the calculation of DALYs. The formula for calculating DALYs based on these assumptions is provided.
Article
Rabies is caused by a number of genetically closely related viruses belonging to the genus Lyssavirus, of which the species type is rabies virus. A true generalist pathogen, rabies virus is isolated from nearly all mammalian orders, and the disease occurs on all continents except Antarctica. Although rabies can infect all mammals, only a few mammalian species are known to act as reservoirs of the disease, with domestic dogs being the major reservoir throughout Africa and Asia. The association between the bite of a mad dog and rabies has been recognized since antiquity and rabid dogs are still responsible for the vast majority of human deaths from rabies worldwide. This can be true even in some areas where wildlife species are the rabies reservoir, as the proximity between dogs and humans provides a link in transmission between wildlife and people. Further consequences of dog rabies relate to animal welfare and conservation. While the effects of canine rabies on public attitudes and treatment of dogs are poorly investigated, there is no doubt that in areas where canine rabies is endemic, fear of the disease has important implications for animal welfare, with suspected rabid dogs and unknown, stray dogs often killed inhumanely in an attempt to control rabies and human exposure.
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Chapter
A variety of epidemiological and ecological factors has to be considered for vaccination as well as for dog population control campaigns. The goal of a vaccination campaign is 70% immune individuals in a population. The percentage of dogs accessible for vaccination is determined by the ratio of owned versus unowned dogs, and by owner attitudes. The frequency (yearly, biannually) of campaigns depends on the population recruitement rate (reproduction, rearing success, immigration) and on the epidemiological situation (pure dog epizootic or dog cycle plus wildlife reservoir). A high proportion of dogs unaccessible for vaccination demands dog population control. Several methods are available to attempt population reduction. In any situation citizens should be educated to reduce the number and the reproduction of unsupervised dogs, and to reduce habitat carrying capacity by giving up littering. Habitat control can also be improved by organized garbage disposal. Unowned, poorly supervised and unwanted dogs should be eliminated. The rate of elimination (including natural mortality) needs to be higher than the actual population (or segment) recruitment rate. This means that between 50% and 80% of a stray dog population has to be eliminated each year. An administration faced with the problem of preventing human rabies has to make decisions on control strategies. The incidence of rabies in man can be controlled by eradication of the disease in an area by immunization and/or decimation of the main host species by elimination or immunization of the species or host population segment responsible for the transmission to man by prophylactic vaccination and post-exposure treatment of man. The decisions should be based on cost—benefit analysis of alternative or combined strategies. Such analysis is possible only when a certain amount of information is available on the epidemiology and on the ecology of the host species. In the following some further reflections will be made for areas where dogs represent the main vector of rabies.