Wildlife Tuberculosis in Southeast Asia: A Less Known Potential Hot-Spots and Issues in Disease Surveillance and Management
Azlan Che-Amat1* and Bee Lee Ong2
1Department of Veterinary Clinical Studies, University Putra Malaysia (UPM), Malaysia
2Faculty of Veterinary Medicine, University Malaysia Kelantan (UMK), Malaysia
Submission: April 05, 2018; Published: May 24, 2018
*Corresponding author: Azlan Che-Amat, Department of Veterinary Clinical Studies, Faculty of Veterinary Medicine, University Putra Malaysia (UPM), 43400 Serdang, Selangor, Malaysia, Tel: +603 8609 3923; Email: [email protected]
How to cite this article: Azlan Che-Amat,Bee Lee Ong. Wildlife Tuberculosis in Southeast Asia: A Less Known Potential Hot-Spots and Issues in
Disease Surveillance and Management. Dairy and Vet Sci J. 2018; 6(2): 555683. DOI: 10.19080/JDVS.2018.06.555683
Wildlife tuberculosis is a threat to the domestic livestock, other wildlife species and human, which may cause an impact to economy, wildlife conservation and serious public health issues. Increasing trend in detection of wildlife tuberculosis reservoir has hindered the progress of controlling this disease. South East Asia is known for her biodiversity hot spots in the world, with high species richness including abundance potential wildlife tuberculosis reservoirs such as wild boar and multi species of deer. Furthermore, one-third of the world’s human tuberculosis is found in the South East Asia. With very little information of livestock and wildlife tuberculosis and potential hot-spot region, attention should be given by the researcher, policy makers and various stakeholders to assess the disease threat and the impact on tuberculosis control in livestock in South East Asia. South East Asia countries also face issues and limitation in conducting tuberculosis surveillance and detection. Such limitations may be overcome by collaboration and networking with expertises under One Health alliance by outsourcing the capabilities of funding, human and laboratory resources and knowledge. This paper gives an overview of potential wildlife tuberculosis occurrence in South East Asia due to her wildlife biodiversity which could potentially act as a reservoir for domestic livestock at the wildlife interface, and discuss the challenges and benefits that could arise from the global experience and resources.
Keywords: Wildlife tuberculosis domestic livestock; Wildlife reservoir; Wildlife species diversity; South East Asia; Disease surveillance; Wildlife reservoirs; Mycobacterium bovis; Geographical; Domestic cattle; Livestock; Encroachment; Goats; Cattle; Buffaloes; Asian elephant; Eradication; Indian races.
Abbrevations: TB: Tuberculosis; MTC: Mycobacterium tuberculosis Complex; NHP: Non-Human Primates; WAHID: World Animal Health Information Database; EPT: Emerging Pandemic Programme; USAID: U.S. Agency for International Development.
In recent decades, many Mycobacterium bovis (M. bovis) infection causing tuberculosis (TB) has been detected in wildlife reservoirs, restricting the progress in eradicating the disease especially from cattle . Across the world, several evidences had shown severe problems associated with wildlife reservoirs of bovine tuberculosis, involving different host species in different geographical conditions. These include popularly known wildlife reservoir for M. bovis in United Kingdom, i.e., the European badger (Meles meles) causing spill over to domestic cattle [2,3]; brushtail possum (Trichosurus vulpecula) in New Zealand causing spread to cattle, deer and ferrets [4-7]; African buffaloes (Syncerus caffer) in South Africa which spill over to other wild animals [8,9]; cervids including white-tailed deer (Odoicoileus virginianus) and elk (Cervus canadensis) in North America and Canada [10-12] and red deer (Cervus elaphus)
[13,14] and Eurasian wild boar (Sus scrofa) in Spain causing spill over to livestock animals (cattle, goats, pigs), deer and wild animals such as in Iberian lynx [14-17]. Human encroachment of the natural environment by agricultural expansion and supplemental feeding to wildlife may introduce the causative agent of bovine tuberculosis at the interface of domestic cattle and wildlife species leading to development of tuberculosis in wildlife reservoir .
From 25 recognized biodiversity hot spots in the world, seven are in Asia which covers the entire ASEAN region. South East Asia (SEA) contains the highest mean proportion of country-endemic bird (9%) and mammal species (11%) compared to the other tropical regions and has the highest mammal species diversity in Asia. The high species richness and endemism in SEA is linked to its complex geographical history [18,19]. Around 33% of t world’s human tuberculosis or about 4.9 million cases are found
in the SEA with more than 2 million human diagnosed annually
by national TB programmes . The most widely recognized
aetiology causing human TB is Mycobacterium tuberculosis (M.
tuberculosis), yet an obscure proportion of cases are due to M.
bovis . In most SEA countries, though bovine TB is notifiable,
there is no proper eradication and control programme for this
disease. To date, human tuberculosis remains a major public
health concern and alarming due to increasing in prevalence of
multidrug-resistant tuberculosis worldwide .
This non-systematic review attempts to give an overview
on Mycobacterium tuberculosis complex (MTC) causing wildlife
tuberculosis in SEA, a less known status region with a potential
disease occurrence based on their bio diversified wildlife
population which could potentially act as a reservoir for
domestic livestock at the wildlife interface. We also discussed
the challenges that might be faced by the SEA countries in
surveillance programme and the benefits that could derive from
the global experience and resources.
From the data of World Animal Health Information Database
(WAHID) Interface of World Animal Health Organization (OIE)
, the incidence of bovine and wildlife TB is low in Malaysia,
Thailand, Myanmar and a few unverified cases in Vietnam.
These include domestic goats, cattle, buffaloes, Asian elephant
and few unknown wildlife species. Figure 1 demonstrated a less
characterized geographical circumstance of bovine and wildlife
tuberculosis in SEA region.
Cases of wildlife TB mainly elephant TB has been reported
in various countries in SEA. In Thailand (2005-2008), four Asian
elephants (Elephas maximus) were confirmed to be infected
with M. tuberculosis by bacterial isolation and sequencing. This
M. tuberculosis may be classified into ancestral and modern
strains based on M. tuberculosis–specific deletion TbD1, identical
strains of the ancient TbD1-positive and identical strains of M.
tuberculosis ATCC 27294, the modern type. On the basis of
the molecular studies, it was believed that M. tuberculosis was
probably transmitted to these elephants from humans . Also a
case of captive Malayan tapir (Tapirus indicus) with disseminated
tuberculosis confirmed M. tuberculosis by molecular test was
reported in 2010 in Thailand. The macroscopic lesions were
indicative of disseminated form of TB characterized by multiple
abscesses and granulomas with caseous necrotic centre in most
of the organs.
The infection may rise through close prolonged contact
with a person or animal with active tuberculosis, and imported
animals that were already infected with tuberculosis and
develop the disease after being imported . Since Thailand is
endemic for tuberculosis , the possible disease transmission
are either direct contact with the animals by the public or
access to contaminated carcasses, animal carriers, or food and
water containing the bacteria. In Peninsular Malaysia, studied
on the TB seroprevalence of Asian elephant and their handlers
were estimated at 20.4% and 24.8% respectively. From 151
trunk wash examines, 24 acid-fast organism were isolated, 23
were identified by hsp65-based sequencing as non-tuberculous
mycobacteria which are M. arupense, M. columbines, M.
intracellular, M. asiaticum, M. mantenii, M. fortuitum, M. gilvum,
M. hiberniae and M. kumamotonense. These high seroprevalence
in the elephants and their handlers suggests frequent, close
contact, two-way transmission between animals and humans
within confined workplaces .
In non-human primates (NHP) example, one potentially
infected macaque in animal research facilities in Thailand was
related with a grade 4 reaction of tuberculin test but showed
no signs of active disease . The culture samples confirmed
the presence of M. tuberculosis. This case demonstrated that
mycobacterium infections can occur in closed macaque colonies,
even with strict assurance measures. Construction activities
at the facility may be possibly infected by exposure to either
aerosols or sputum from construction personnel. In other
findings, buccal swabs collected from macaques representing
numerous species in three SEA countries (Thailand, Indonesia
and Singapore) included pets, show monkeys free ranging, zoos
and monkey temples. DNA was isolated and the PCR amplified
IS6110 from 84 (31.9%) of the macaques.
Based on the known epidemiology of MTC species, M.
tuberculosis and M. bovis are the most likely mycobacterial
species to be present in these specimens. M. tuberculosis is
endemic in human populations in countries such as Indonesia,
Nepal and Thailand, providing wide opportunity for human to
NHP transmission. Few published research were available on
the interaction of macaques and domestic cattle, though range
overlap is not uncommon, giving an opportunity for crossspecies
transmission to macaques .
Based on the reported TB control program in SEA by the
WAHID OIE, bovine TB is known to be a notifiable disease for
the most countries which deployed a passive surveillance
which they were interested in zoonotic disease only when the
incidence/prevalence was high or during epidemics. Bovine TB
was surveyed in livestock including cattle, buffaloes, goats, sheep,
farmed deer and undetermined wildlife species. As with any
surveillance system, the fulfilment of information is problematic
in SEA . It can be advocated by the number reported TB
cases from 2005-2013 where only 4 countries have an incidence
of only few cases. Like many TB reported cases in livestock and
wildlife in other regions, the likelihood of TB disease cases in
SEA are expected to have a similar outcome.
Examples are the Eurasian wild boar and wild cervids such
as white tailed-deer, elk, red deer and fallow deer suggested
that MTC could survived and maintained in these population.
Interestingly, red deer and wild boar share similar molecular
type of MTC and about 54% of MTC antigens spoligotypes
similar to human types eventually may cause a public health
risk especially to hunters, wildlife personnel and game meat
consumers. Existence and widespread of suids and cervids in
SEA is an important factor to be considered for active bovine TB
disease surveillance. There are 3 subspecies grouping of native
wild boar throughout SEA , namely ‘Indian races’ (Sus scrofa
cristatus) ranged in Myanmar and Thailand, ‘Eastern races’ (Sus
scrofa moupinensis) in Vietnam and ‘Indonesian/banded pig’
(Sus scrofa vittatus) ranged from Indonesia to Malaysia. Wild
pigs are abundant in many parts of its range in SEA and have
been recorded high in some area as tabulated in Table 1.
As for cervids, the species are widespread in their native
region. They can be found in a wide range of habitats and
geographical landscape from cold to the tropics. In areas where
extensive carnivore populations are present and have not
been significantly reduced by humans, predation serves as an
important reason for mortality in cervids. As in many species,
predation is the dominant medium of controlling population
densities . Many cervids in SEA are categorized as endangered
species including Calamian deer (Axis calamianensis), hog deer
(Axis porcinus), Philippines spotted deer (Rusa alfredi) and Eld’s
deer (Rucervus eldii). Human settlement, agricultural expansion,
local hunting for meat, skin, velvet and trophy are the significant
threat for the population declining [33-36].
Sambar deer, Timor deer (Rusa timorensis) and Philippines
deer are the remaining that are still locally common and under
vulnerable status Timmins et al. . Sambar deer have been
recorded to have 0.01-0.02/km2 population densities in some
national park in Malaysia, widespread population based on 80%
detection by the camera trapping sites in Myanmar, abundant
in some wildlife sanctuary in Thailand which estimated at 2-3
individuals/km2, common spread in Vietnam and Cambodia and
is not under major threat in Indonesia [37-39].
SEA is considered an important regional livestock market
on swine meat. Available data swine livestock population in SEA
for 2012-2013 indicated the population ranged from 792,000-
21,700,00. Although many of countries has moving towards
close house system and intensive farming, nevertheless, they
are still many farmers operating in their traditional way of open
house and extensive livestock management especially in rural
area. This would be a major possible way of wildlife-livestock
The common species of deer farming among SEA region are
Timorensis (Javan) deer. This is the commonest deer since they
are smaller than the sambar deer which likewise used as farmed
deer. The handling is much less demanding and it can occupy open
grasslands, thereby presenting an alternative to diversification
in the livestock production industry. Deer farming is rather
small in SEA but interest is growing. As presented by WAHIDOIE,
accessible information in 2012 demonstrated farmed deer
population were 13,136 (Malaysia) and 7,777 (Thailand) and the
population are believed to be increased over the year.
Bovine TB in wildlife is typically viewed as a potential
zoonotic disease threat. Indeed, wild animals can and do play
as reservoirs of infection and may act a direct health risk to
consumers of infected wildlife products. Nonetheless, it is
the indirect risk route, by which wildlife reservoirs may affect
livestock animals, that is the foundation for concern, because
it is the bovine link which poses the greatest risk for human
infection. The current concern is that the presence of infection in
certain wild maintenance hosts may hamper disease control in
livestock. The SEA can be separated into two regions, the islands
(consist of the Philippines, Indonesia and part of Malaysia) and
the mainland (Figure 2). On the mainland, the movement of
livestock between different areas can occur via a wide range of routes. Often there is not even a need for roads, and animals
can be transported between any two points with little chance of
detection by the authorities. Controlling livestock movement in
these circumstances poses great challenges .
Another risk factor identified with the emergence of
TB disease from wildlife has been the significant increment
in consumption of bush-meats in many parts of the world.
Consuming a diseased meat by public, zoo animals or prey of
wild boar or deer by exotic native species such as tiger, may
implicated the conservation issue of exotic species in the future.
In 2009 in Malaysia , about 4 tons of wild boar meat were
seized by the local authorities in the east coast part of Peninsular
Malaysia and it was believed illegally hunted and to be smuggling
across border. The episodes of illegal meat-seized were
continues. Based on series of capture in Malaysia, it has become
a significant source of illegally harvested wildlife for the export
market to other parts of SEA and East Asia. Within the period
1998–2007, about 35 million animals were trades, 30 million
animals of around 300 species being wild-caught which by the
SEA members, specifically Malaysia, Vietnam and Indonesia
are the significant exporters . In view of reports via ASEAN
Wildlife Enforcement Network , number of enforcement
action recovered for dead animals was increasing over the year,
where from 2009 to 2010 alone, a level up from 9,932 to 74,183
dead animals were recovered. This critical estimation of animals
seized for illegal market for exportation either for animal trade
or meat consumption may help transmitting potential diseases
to other region.
In developing countries, respondent from local wildlife
officials and scientist came out with high assertion that lack
of resources or financing and absence of existing government
wildlife surveillance are the main issues in wildlife disease
surveillance . In addition, insufficient human and laboratory
limits as well as poor coordination hampered the surveillance
system. They likewise concur that the lack of wildlife surveillance
is due to limited interest or awareness regarding wildlife disease.
Hence a One Health approach which stressed on coordinated
interdisciplinary joint effort is highly recommended to address
A large portion of the nations in SEA is focusing on
selected diseases such foot and mouth disease, brucellosis and
haemorrhagic septicaemia control and eradication program
in livestock due to its high economic impact. Wildlife disease
surveillance is less important and does not exist at all until issue
or problem arises such as ecological surveillance of bats due to
Nipah outbreak. However in recent year many emerging diseases
have arisen from wildlife such as Ebola and Henipah virus and
wildlife department have been made aware. Through the current
Emerging Pandemic Programme (EPT) under U.S. Agency for
International Development (USAID) , fund has been created
for wildlife surveillances under the component “PREDICT” .
Opportunities are now available for many countries to build
capacity and participate in wildlife surveillance in the SEA
Emerging Pandemic Threats (EPT) program aims to enhance
surveillance in potential wildlife hosts so as to address emerging
infectious diseases from wildlife by strengthening local, regional
and global networks. From their survey, the respondents have
indicated the importance of working at key human-animal
interfaces, such as the hunting area, markets, wildlife-lives interaction and wildlife in captivity. Other than that, working
areas also should be focused on areas where wildlife was
butchered, shared water sources, and land utilization change.
The determinant of key sites of surveillance is pivotal for the
further venture of surveillance system implementation.
Given the challenges of getting samples from wild animals, the
convenience or opportunistic sampling remains an effective and
essential tool to detect wildlife pathogens in general surveillance.
Collaboration and involvement with the wildlife department’s
program will giving the opportunity to do convenience sampling
of wild animals and enhance surveillance programs. Targeted
surveillance is a more active approach focused on a particular
pathogen in a specified wildlife population which is classified as
healthy, but is considered at risk of exposure to this pathogen
from an identified source, e.g. screening a wildlife population
when positive cases in nearby cattle have been found . A
general surveillance on gross pathology for diagnosis of bovine
TB in white-tailed deer in north eastern Michigan (USA) has
brought about usage of targeted sampling by necropsies and
culturing tissues of the white-tailed deer population .
Development of zoo-based hospital or wildlife captive
centre health and disease information may help to the large
scale or national free-living wildlife investigation focal area.
In Australia, zoo based wildlife hospital disease surveillance
or sentinel surveillance uses a collaborative approach and
provides a strong model for a disease surveillance program for
free-ranging wildlife that enhances the national capacity for
early detection of emerging diseases . This system showed
that it had the capacity to capture valuable data on disease in
free-ranging wildlife that may generally not have been reported,
or was reported earlier than would otherwise have happened.
Testing individuals at small setting such as zoo may have a trace
back capabilities such as in an outbreak of tuberculosis due to M.
bovis occurred in pot-bellied pigs (Sus scrofa vittatus), red deer
(Cervus elaphus), buffalo (Bison bonasus) and European lynxes
(Lynx lynx) .
Another important issue of managing wildlife TB is the
availability of diagnostic tools, which is frequently constrained
to those developed for domestic animals and humans .
There are current reviews on diagnostic application in wildlife
for the last 5 years as a result of the expanding understanding of
particular wildlife species play a role in maintaining the M. bovis
pathogen [50-53]. In wildlife disease surveillance, an extreme
care should be taken to ensure the validity of diagnostic tests
utilized to identify pathogens applied to a particular wild animal
species and the sensitivity and specificity of the tests used should
be incorporated in the analysis and interpretation .
Under the RESPOND-USAID initiative, SEA One Health
University Network (SEAOHUN) has emerged to nurture a
capacity building under One Health disciplines to respond to
emerging and reemerging infectious and zoonotic diseases. This
involves universities network from four countries including
Indonesia, Malaysia, Thailand and Vietnam. The mission is
to give the preparation by training, education and research
capacities of the university network to develop knowledge, skills
and attitude of One Health. This would be one platform for the
regional scientists, veterinarians and wildlife officials to take
up research or surveillance on wildlife diseases. Knowledge of
outbreaks originating potentially from wildlife varied by global
region suggests that there was a lack of communication across
stakeholder groups and that there is a need to bring awareness
among stakeholders on wildlife health issues in relation to public
Opportunities, for example a growing interest or awareness
regarding wildlife disease or surveillance programs, could
be used as a starting point to acquire the funding needed to
increase both human and laboratory capacity for wildlife
pathogen surveillance. Essential tasks that should be taken
by the international community include better alliance
and coordination of international surveillance systems in
industrialized and developing countries, improved reporting
systems and sharing of international information, active
surveillance by incorporating rural populations and wildlife
habitats, training of professionals such as veterinarians and
biologists in wildlife health management and foundation of joint
multidisciplinary groups ready to intervene when disease occur
Data on tuberculosis and the disease nature are still
questionable and lacking in most of the SEA countries. Targeted
surveillance system should be applied in order to get a better
status of unknown livestock and wildlife diseases particularly
for bovine tuberculosis. Knowledge transfer from the global
disease surveillance and advances in diagnostic tools in wildlife
tuberculosis may be useful for the disease investigation.
Determination from unknown to known tuberculosis status in
wildlife in this region may help to complete the global maps of
bovine TB distribution and will help to understand a potential
spread of disease due to further exportation of disease from
this region to other region. Increasing global interest in defining
wildlife tuberculosis reservoir may help developing countries
such as in SEA in terms of collaboration and networking with
an expertise under One Health alliance by outsourcing the
capabilities of funding, human and laboratory resources and