Biosecurity and Bioterrorism: Biodefense Strategy, Practice, and Science

Volume 11, Supplement 1, 2013 ª Mary Ann Liebert, Inc.

DOI: 10.1089/bsp.2012.0085

Rodents as Potential Couriers for Bioterrorism Agents

Mare Lõhmus, Ingmar Janse, Frank van de Goot, and Bart J. van Rotterdam

Many pathogens that can cause major public health, economic, and social damage are relatively easily accessible and could be
used as biological weapons. Wildlife is a natural reservoir for many potential bioterrorism agents, and, as history has shown,
eliminating a pathogen that has dispersed among wild fauna can be extremely challenging. Since a number of wild rodent species
live close to humans, rodents constitute a vector for pathogens to circulate among wildlife, domestic animals, and humans. This
article reviews the possible consequences of a deliberate spread of rodentborne pathogens. It is relatively easy to infect wild rodents
with certain pathogens or to release infected rodents, and the action would be difficult to trace. Rodents can also function as
reservoirs for diseases that have been spread during a bioterrorism attack and cause recurring disease outbreaks. As rats and mice
are common in both urban and rural settlements, deliberately released rodentborne infections have the capacity to spread very
rapidly. The majority of pathogens that are listed as potential agents of bioterrorism by the Centers for Disease Control and
Prevention and the National Institute of Allergy and Infectious Diseases exploit rodents as vectors or reservoirs. In addition to
zoonotic diseases, deliberately released rodentborne epizootics can have serious economic consequences for society, for example,
in the area of international trade restrictions. The ability to rapidly detect introduced diseases and effectively communicate with
the public in crisis situations enables a quick response and is essential for successful and cost-effective disease control.

D eliberate release of pathogens can have a huge

impact on society. At the same time, access to a range
of pathogens can be relatively easy. Therefore, bioterrorism
remains an important area of infectious disease prepared-
ness. Many infectious diseases that have rodents as reser-
voirs are mentioned among the prime candidates for
bioterrorism agents: hemorrhagic fevers, hantavirus, Lassa
fever, Rift Valley fever, Q fever, tularemia, brucellosis, and
bubonic plague are all rodent-reservoir zoonoses with po-
tentially serious health effects.1 It seems, however, that
medical and veterinary scientists have not yet realized the
full implication of being able to attack human or livestock
populations indirectly through another host-organism and
how chronic and insidious the consequences of such an
attack would be.1 This lack of awareness among medical
professionals could lead to misdiagnosis and failure to
recognize the need for rapid intervention in critical situa-
tions. Consequently, when discussing effects and damage
control during a bioterrorism event, it is important to know
not only the pathogen but also its potential reservoirs.
Biological Weapons
Approximately 17 countries in the world, including the
former USSR and 5 countries that are implicated as

Mare Lõhmus, PhD is Associate Professor, Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala, Sweden.
Ingmar Janse, PhD, is Senior Scientist, and Bart J. van Rotterdam, PhD, is a Microbiologist, both in the Department of Zoonoses &
Environmental Microbiology, Centre for Infectious Disease Control, National Institute for Public Health and the Environment
(RIVM), Section I & V, Bilthoven, the Netherlands. Frank van de Goot, PhD, is Senior Forensic Pathologist, Symbiant (pathology
expert centre), Alkmaar, the Netherlands.

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RODENTS AS COURIERS FOR BIOTERORISM AGENTS
sponsors of international terrorism, have or have had an
active biowarfare research program, and several interna-
tional terrorist organizations are believed to have the fi-
nancial resources and political contacts needed to gain
access to modern bioweapon cultures and production
technologies.2,3 Additionally, groups and individuals dis-
satisfied with a government or society have been known to
use or plan to use biological weapons for personal reasons.3
Current classification of potential biological weapons is
based on agent characteristics, such as the ease of obtaining
and dispersing the agent, its virulence, morbidity, mortal-
ity, and also the capacity for individual-to-individual
transmission. On the web pages of the Centers for Disease
Control and Prevention (CDC) and the National Institute
of Allergy and Infectious Diseases (NIAID), potential bi-
ological weapons are classified, according to the criteria
mentioned above, into A, B, and C categories. Category A
lists the pathogens that are most feared in the context of
bioterrorism events.4 Most attention may need to be fo-
cused on combatting infections that have serious medical
consequences, but in several cases, the economic damage
caused by a pathogen may demand actions even though the
medical effects are trivial.1 Bioterrorists may not always be
constrained by the need to target or predict their outcome
precisely, and extensive epidemics are not a prerequisite for
creating great public anxiety.4,5 Simple fear of a disease
could be enough to cause economic problems for a region
because of, for example, diminished interest in recreational
activities and tourism. Consequently, virtually any patho-
genic microbe could be used by bioterrorists.
Besides human health concerns, the agricultural sector is
vulnerable to bioterrorist attacks because domestic animals
rarely have an innate resistance to foreign pathogens and are
usually not vaccinated against these diseases.4 Even small
outbreaks of exotic diseases in livestock could remove a
country from the global market for its agricultural prod-
ucts.4 Agricultural bioterrorism is especially insidious as
animals themselves may become the primary vectors for
transferring agents.4 Furthermore, the majority of category
A and B potential biological weapons on the CDC lists are
of a zoonotic nature,5 and thus an attack on animal pop-
ulations could pose a health risk for humans as well.
Bioterrorism and Wildlife
Unless an area is intensively monitored for pathogens, a
deliberate release of infectious agents will probably not be
detected at the time of release, but only after people or
domestic animals exhibit symptoms of infection. The
incubation periods of different kinds of infectious diseases
vary, but in many cases, days or even weeks can pass before
an outbreak is noticed. This provides the pathogen with
the opportunity to spread and infect other organisms that
may not have been targeted by the bioattack, such as local
wildlife.
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Wildlife is a natural reservoir for many diseases, and, as
seen in the emergence of West Nile virus in the United States,
the existence of wildlife reservoirs makes eradication of a
disease that has had time to establish itself unrealistic.6 The
damage can become extensive when the released agents
manage to spread over large geographic areas before they are
discovered. Many wildlife species are highly susceptible to
high-priority bioterrorism agents,7 and, consequently, path-
ogens released during a bioattack directed at humans or
livestock can either jump to wildlife or persist in the envi-
ronment and cause zoonotic epidemics for a long time. Fur-
thermore, several diseases with serious medical or economic
significance for humans (eg, many viral hemorrhagic fevers)
can infect wildlife species without their exhibiting overt
clinical signs of infection, which can make the source iden-
tification of outbreaks complicated. Control measures of in-
fectious diseases often involve immunization, but in the case
of wildlife infections in which humans and domestic animals
are not the reservoirs, herd immunity is not achievable, and
pathogens cannot be eliminated through immunization.1
Rodents and Infectious Diseases
Rodents can function as reservoirs and vectors spreading
infectious diseases.8 Many rodent species are highly op-
portunistic, meaning that they can easily adapt to new
conditions and are able to take advantage of temporarily
suitable environmental conditions for rapid reproduction.
These characteristics have allowed some species, such as the
house mouse (Mus musculus) and brown rat (Rattus norve-
gicus), to spread over most of the Earth’s terrestrial areas.
Opportunistic qualities may also support a potential dis-
persal of other accidentally or deliberately introduced ro-
dent species outside their endemic areas in the future.
Moreover, the opportunistic species often have perido-
mestic affinities and often live in close proximity to hu-
man settlements, which makes them an important link
for transmitting infections among wildlife, humans, and
livestock.9
The absolute numbers of infectious diseases associated
with rodents are not known, mainly because of the lack of
complete systematic surveys of rodents for pathogens.9
However, according to Hugh-Jones et al.,10 rodents func-
tion as reservoirs for approximately 46% of all globally
known zoonoses, and more people are believed to have died
in the past thousand years because of rodentborne infec-
tions than wars.8 The symptoms of infections that are
transmissible by rodents vary from relatively trivial (ie, skin
lesions at the site of infection in cases of cowpox) to
commonly fatal ones (ie, bubonic plague).1 Transmission
of rodentborne infections (Figure 1) may happen directly
from rodents to humans (ie, hantaviruses) or via an ar-
thropod vector (ie, fleas in cases of plague, ticks in cases of
Lyme disease, and sand flies in cases of leishmaniasis).1
Studies have also shown a direct connection between the
Biosecurity and Bioterrorism: Biodefense Strategy, Practice, and Science
 LÕHMUS ET AL.

Figure 1. Examples of possible routes for human infection with rodentborne pathogens. Rodentborne pathogens in aerosolized form
can be obtained directly through inhalation. Human infection can also occur by consuming contaminated water, or through skin and
wounds when in contact with infected soil/water. Diseases can also be transmitted through rodent bites; however, compared to other
sources this pathway is relatively uncommon. An indirect way to obtain pathogens is through contact with rodent-infected domestic
animals or by consuming food products from these animals. Another route for indirect infection is through arthropod vectors (ticks,
mosquitoes, flies, and so on) that after being infected from a rodent reservoir transmit the disease to humans when obtaining blood meals.

abundance of rodents in the wild and the number of ro-
dentborne human infections.11
Rodents as a Dispersal Mechanism
A deliberate release of infected rodents or the contamination
of wild rodents with pathogens would be a relatively easy
way to threaten public health. For example, a diseased an-
imal that is left on the ground or in a water source would be
easily accessible to wild rodents and could cause a disease
outbreak in an unexpected location. Many diseases are en-
vironmentally hardy and will be able to persist in organic or
inorganic matrices for an extended period4 and could thus
potentially infect, for instance, burrowing rats. Subsequent
contact of these animals with humans or domestic animals
could spread the disease. No incidences of rodent-targeted
bioterrorism have been described in modern times. But
during World War II, the Japanese army, Unit 731, was
reported to have experimented with plague by harvesting
plague-infected fleas from infected rodents and dropping
them over populated areas in China and Manchuria.12
The likelihood of unintentionally infecting wild rodents
during a bioattack targeted against humans or livestock is
plausible. Most of the diseases caused by category A path-
ogens exploit rodents as vectors or reservoirs (eg, plague,
tularemia, arena viruses, etc). This is also true for many of
the diseases caused by category B pathogens (eg, toxoplas-
mosis, brucellosis, Q fever, etc). It might not be very likely
that rodents come across anthrax letters targeted at certain
individuals, but aerosolized pathogens that are released into
the environment in a less targeted way could infect rodents,
especially if the pathogen can survive in the environment
for a long period. In cases of bioterrorism directed toward
livestock, soil and water contamination by infected excreta
from domestic livestock could spread pathogens to the
sympatric rodent populations and in this way establish a
rodent reservoir of infection.13
Rodents as Disease Vectors
Humans often provide rodents with an abundance of
supportive resources and favorable microclimatic condi-
tions that allow them to grow in population size, especially
in areas where humans have greatly reduced the number of
their natural predators.14,15 In Europe, brown rats and
house mice are among the most recognized urban rodents.

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RODENTS AS COURIERS FOR BIOTERORISM AGENTS
These 2 species have quite different behavioral character-
istics; while the house mouse is a highly inquisitive species,
rats are cautious and prefer the familiarity of a known en-
vironment.14 Rats also show a more dominant nature,
suppressing and occasionally preying on house mice.
Urban rodent metapopulations usually consist of many
small groups that may have little contact with each other
except in cases of disturbance.14,16 However, disturbance in
the form of road work or building activities is a common
event in cities, and it is likely that these human activities
enhance the transmission of pathogens between rodent
groups. These activities could also increase the opportunities
for contact among rodents, humans, and pets. In undis-
turbed rodent groups, young males typically leave their na-
tive groups to disperse into new areas.16 Hence, young males
can be expected to be responsible for spreading pathogens
between rodent groups. Local overpopulation of rats in cities
is most common in areas of failing hygiene, as, for example,
near train and bus stations with abundant remains of food
and other materials.17 Additionally, unrestricted food sup-
plies in gardens with compost heaps are thought to function
as valuable shelters for rats. Just as train and bus stations
might be a preferred target for a bioterrorism attack because
of the potential for the maximum effect on public health,
such areas would also be a prime place for the introduction of
pathogens into rodent reservoirs.
The structure of rodent communities in rural areas is
similar to that in urban ones, but the size of individual
territories may be more flexible and may vary with the
season and food availability. Furthermore, the structure of
rodent communities depends on the local land use and
differs, for example, from the areas that are used for live-
stock farming and cultivation of crops. The mobility of rats
depends of the reliability of their food sources. For instance,
brown rats can be immobile during food abundance but
may roam more than 6 kilometers in other circum-
stances.18,19 According to Taylor,18 rats that lived near
reliable food sources in agricultural areas rarely moved
more than 30 m from their home sites, but when the food
was removed, they expanded their range considerably.
Ironically, that means that rodent-proofing a farm after a
bioterrorism event would ensure transmission between
neighboring farms and probably even to wildlife species. In
this case, if the goal is to prevent disease dispersal, it would
be wiser to use trapping or rodenticides locally and follow
recommendations from an ecological rodent management
approach20 rather than rodent-proofing a farm and with-
drawing all food sources.
Ecological Context
of Disease Dispersal
The lack of predators and low biodiversity are often ignored
ecological parameters that greatly facilitate infectious dis-
ease dispersal. Modern cities have a low level of biodiver-
S250
sity, and natural competition and predation mechanisms
are altered, allowing abnormal and unbridled growth of
certain species. Generally, when a pristine ecosystem is
disturbed, specialist species with specific food, nesting, or
breeding requirements cannot survive. In the absence of
such specialist competitors, opportunistic species with high
fecundity will thrive.21 As mentioned above, several op-
portunistic species also possess characteristics such as high
mobility and high population densities that make them
ideal hosts and transmitters of zoonotic pathogens.21
In recent years, it has become increasingly evident that
the loss of biodiversity tends to increase pathogen trans-
mission and disease incidence.9,22 Consequently, the term
‘‘dilution effect’’ has been admixed into public health fo-
rums. The ‘‘dilution effect’’ hypothesis suggests that high
biodiversity reduces the risk of transmission of certain
diseases.23 ‘‘Dilution effect’’ functions only when the
pathogen is transmitted horizontally and when the reservoir
competence for a certain pathogen varies among potential
host species. Increased biodiversity would then increase the
likelihood that infected organisms meet more individuals
from a non–host species that would limit pathogen trans-
mission. Indeed, epidemiologic and experimental studies
have shown that lower diversity of small mammals increases
the prevalence of hantaviruses in their hosts, leading to
increased transmission risk to humans.22 Consequently, as
a deliberate release of pathogens can be expected to take
place in areas of low biodiversity, this condition will con-
siderably facilitate pathogen dispersal. However, in areas
where municipalities are regularly performing rodent con-
trol, the dynamics of rodent populations and diseases may
greatly differ from more degraded urban areas. Ad-
ditionally, the increasing populations of urban foxes in
many European cities may lower the rodent populations
but, unfortunately, also add to the dispersal of parasites
with complex life cycles, such as Echinococcus multi-
locularis and other helminths.24-26
The ‘‘One Health’’ Approach
Understanding disease management as a multifactorial is-
sue is critical for preventing disease expansion including in
the context of bioterrorism. Behavior and physiology of
reservoir organisms (ie, organisms that can amplify a
pathogen but are not necessarily a direct link to transmis-
sion, often rodents), including humans, wildlife, and do-
mestic animals, and of the disease vectors (ie, organisms
that actually transmit the disease, often arthropods but also
rodents in some cases) are important factors contributing to
infectious disease expansion. Dealing with an outbreak is
therefore a task beyond medical and public health special-
ists alone. It demands the additional understanding of
veterinary and environmental factors and knowledge of
issues regarding human social behavior and political
changes, basic science-related information about pathogen
Biosecurity and Bioterrorism: Biodefense Strategy, Practice, and Science

life cycles and evolution, and aspects related to vector/res-
ervoir life history.27 Cooperation between specialists with
different expertise is necessary because the factors associated
with disease expansion are not independent: For example,
modifications in human behavior can change the ecology of
wildlife reservoirs and/or disease vectors and in this way
affect the transmission patterns of pathogens. It can be
expected that, for example, family doctors and veterinarians
in countries that are nonendemic for a particular disease
will not be aware of its clinical manifestations. This can
cause a delay in the diagnosis, leading to higher numbers of
fatalities and increased dispersal, including to wildlife. In
order to recognize the role of wildlife in the context of
bioterrorism, it is important that veterinarians be aware of
clinical signs of infection with biothreat agents in wildlife.7
If disease outbreaks occur in nonendemic areas, outside
the expected season, or in unexpectedly large numbers,
these events could be investigated for the possibility of
bioterrorism.4
Examples of Rodent Reservoir
Bioagents
Plague
The life cycle of plague, Yersinia pestis, involves a complex
interaction between rodents and fleas, occasionally involv-
ing human infections.28 The most important enzootic and
epizootic reservoirs of plague are different kinds of ro-
dents.29 Plague agents are able to survive in the soil for long
periods and can be transmitted to burrowing animals for
extended periods.30,31 Plague occurs worldwide but pri-
marily in certain locations in Africa and Asia.7
The 3 major forms of Y. pestis infection in humans are
classic bubonic plague, primary septicemic plague, and
pneumonic plague.28 Untreated bubonic plague has a fa-
tality rate of 40% to 60%, whereas the pneumonic and
septicemic forms are usually fatal. Human infection can be
acquired by flea bites from infected fleas, but also by con-
tact with fluids from infected animals and by respiratory
droplets from infected humans or animals.28
Human cases are most commonly associated with die-
offs of rodent hosts that lead to fleas leaving the dead ani-
mal and seeking new hosts. The mouthparts of rodent fleas
are often too weak to penetrate the human skin, but cat fleas
can do it with ease.31 Cats are highly sensitive to plague and
can be infected both by flea bites and by ingestion of in-
fected rodents. They are also the most likely animals to
bring plague into human facilities.7,28 Clinical signs in
humans develop 1 to 6 days after becoming infected, pro-
viding the pathogen with a time-lag that could be sufficient
for both people and animals to move and spread the disease,
making control of the disease more difficult.7
Plague is a high-risk potential weapon of bioterrorism.
Humans can be easily infected via aerosols, and aerosolized
Volume 11, Supplement 1, 2013
LÕHMUS ET AL.
bacteria are easily transmitted between infected humans
and animals. This disease has a high attack rate and
produces severe clinical disease.28 Moreover, antibiotic-
resistant Y. pestis strains are known to exist, and, in aero-
solized form, it would be a formidable weapon.32 Plague
still occurs naturally in several locations in the world, so it is
a relatively easy agent to obtain. It can also be easily dis-
seminated into wild rodent populations in both urban and
rural areas.
Tularemia
At least 4 subspecies of Francisella tularensis (tularemia) are
recognized, 2 of which are human pathogens: Francisella
tularensis biovar tularensis and Francisella tularensis biovar
palaeartica.7 F. tularensis infection has been demonstrated
in an impressive number of wildlife species,33 but it is still
mainly considered to be a disease of rodents and lago-
morphs. Arthropods, such as ticks, biting flies, and mos-
quitoes, serve as vectors for tularemia and potentially even
as long-term reservoirs.33 Tularemia infections occur
mainly in the northern hemisphere, most frequently in
Scandinavia, Central Europe, North America, Japan, and
Russia.15
Tularemia is highly infectious and can be transmitted by
several epidemiologic routes: through arthropod vectors,
direct contact with infected blood and tissues, intact skin
and wounds, ocular mucous membranes, inhalation, and
ingestion.7,28 The infectious dose depends on the mode of
transmission: Only 10 organisms are needed to cause dis-
ease by inhalation, whereas 108 organisms are required
parenterally.28 Six different forms of tularemia have been
classified according to their clinical presentation and route
of exposure, although the pneumonic form is the most
likely bioterrorism agent because it can be transmitted as an
aerosol and has 30% to 60% mortality if untreated.34
F. tularensis has been weaponized by the United States and
very likely by several other countries.33,34 The highly in-
fectious nature of tularemia makes it possible to use it in the
most ‘‘unsophisticated’’ ways of bioterrorism, as both ro-
dents and humans are able to acquire infections through
direct contact with infected rodent carcasses or by con-
sumption of food or water that is contaminated by an in-
fected animal.15
Brucellosis
Six species with numerous biotypes of Brucellae have been
identified, but only Brucella abortus, B. melitensis, B. suis,
and B. canis can cause human disease.28 Brucellosis is a
worldwide zoonosis that mainly infects domesticated ani-
mals, but different wild mammals, including rodents (es-
pecially brown rats and even voles), act as reservoirs.35,36 In
livestock, brucellosis is a lifelong infection. The bacteria
localize in the reproductive tract and cause spontaneous
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RODENTS AS COURIERS FOR BIOTERORISM AGENTS
abortions and sterility.28 Transmission to humans can oc-
cur when open wounds are exposed to animal secretions, by
infected aerosols, or via consumption of unpasteurized
dairy products.
In the case of Brucellae, a major threat arises from
agroterrorism—that is, the deliberate infection of domestic
animals. Brucellosis is an economically important disease in
production animals worldwide.35 Countries that are pres-
ently free from animal brucellosis could suffer serious
economic losses if brucellosis were to be introduced into
their livestock.35 Brucellae are a highly virulent pathogen in
humans and animals and would be an effective biological
weapon.35 Only 10-100 aerosolized organisms are needed
to cause disease, and the early symptoms of the disease are
nonspecific, often leading to delayed diagnosis and inef-
fective treatment. Although Brucella is sensitive to heat and
most disinfectants, it can survive in the environment for up
to 2 years, thus constituting a continuous threat to both
humans and animals.37 In 1954, B. suis became the first
agent to be weaponized by the United States, but several
other countries have or are suspected to have weaponized
this agent, including the United Kingdom.28,37
Q Fever
Coxiella burnetii, which causes Q fever, is a category B
bioterrorism agent that is highly infectious in both hu-
mans and livestock. C. burnetii spores are extremely re-
sistant to heat and desiccation but also to cold.28 C.
burnetii is a worldwide zoonosis that infects various
mammals (including domestic goats, sheep, and cattle),
birds, fish, and arthropods. Urine, feces, and birth ma-
terial of infected animals are sources for C. burnetii
contamination in the environment. Human infections
usually occur after inhalation of aerosolized bacteria: A
single inhaled organism is enough to produce clinical
illness.28 The placentas of infected animals can be heavily
contaminated with these bacteria, and during parturition
bacteria are released into the environment and may cause
infection for up to 150 days.28 The bacterium can survive
in the environment for years and may travel long dis-
tances in the form of aerosol.19
Although cultivation of Coxiella is rather laborious,
large amounts of infectious material can be produced.38
Coxiella may not cause high mortality, but if released as an
aerosol, it could cause acute disabling disease and great
economic losses in the agricultural sector. Acute infection
of Q fever can be followed by fatal (eg, endocarditis)
or debilitating (eg, chronic fatigue syndrome) disorders.
Because of nonspecific symptoms, the diagnosis of Q fever
might be delayed. Antibiotic treatment is available for
the acute form of C. burnetii but not for the chronic
complications.38
Brown rats are thought to function as an important
factor in the dissemination of endemically circulating Q
fever between wild and domestic animals and humans.19
S252
Cats may have a role in these infection routes as well since
they prey on the wild reservoirs.
Viral Hemorrhagic Fevers
Viral hemorrhagic fevers (VHFs) are caused by a group of
viruses that require an animal or insect host reservoir for
transmission.39 They are usually geographically restricted
to specific regions of the world where they create enzootic
infections. Humans generally get infected after exposure to
contaminated saliva, urine, or feces of infected animals or
by rodent or insect bites.39 VHFs include arenaviruses, such
as Lassa fever and South American hemorrhagic fever
viruses; bunyaviruses, such as hantaviral infections (HTVs)
and Rift Valley fever virus (RVFV); flaviviruses, such as
dengue hemorrhagic fever, tickborne encephalitis, and
yellow fever viruses; and filoviruses, represented by Ebola
and Marburg viruses. For most of these diseases, there are
only limited treatment and vaccination options. Some
VHFs have been weaponized by researchers in the former
Soviet Union, the US, and possibly North Korea.40
Arenaviruses
Arenaviruses are included in the category A pathogen list
and as such pose a threat to public health if used as a
bioterrorism agent. Traditionally, arenaviruses are divided
into the Old and New World arenaviruses. The reservoir
hosts of almost all arenaviruses are different kinds of
commensal or semicommensal rodents that live close to
humans or in cultivated fields.41 In rodents, most of the
arenaviruses cause a persistent, asymptomatic infection
with chronic viremia and viruria. Lymphocytic chor-
iomeningitis virus (LCMV) is an arenavirus with a world-
wide distribution because of its association with the house
mouse, Mus musculus. LCMV rarely causes severe infection
except in infants and immunocompromised individu-
als.41,42 In contrast, Old World viruses (ie, Lassa virus and
Lujo virus), which are found in Africa, and several New
World viruses in South America (eg, Junin, Machupo,
Sabia, Guanarito, and Chapere) can cause severe disease
and hemorrhagic fever syndrome.43 Rodent-to-human in-
fections of arenaviruses are thought to occur through
aerosols and fomites.41 This indicates that these agents
could potentially be used as bioweapons if propagated to
high titer in cell culture and in aerosols.43
Most cases of arenavirus transmission occur in rural,
agricultural areas. The lack of rapid diagnostic methods for
specific diagnoses of arenaviral hemorrhagic fevers means
that diagnoses are usually made late in the illness and in
most cases vaccination is not available.43 Because arena-
viruses are rarely transmitted from person-to-person and
are not carried by arthropods, each arenaviral disease is
tightly constrained in the geographic range of its rodent
reservoir host.43 This means that a bioterrorism attack
could increase the infection prevalence in local rodent fauna
Biosecurity and Bioterrorism: Biodefense Strategy, Practice, and Science

in endemic areas only (although a possible spill-over in-
fection in other species cannot be ruled out). When an
attack also involves the release of infected rodents, the
spread of the disease would depend on the ability of the
infected host to establish itself in a nonendemic area. Given
the opportunistic nature of many rodent species, it may be a
possibility in some cases.
Hantaviral Infections
HTVs are transmitted to people via aerosols of infectious
excreta (urine, feces, saliva) from chronically infected small
wild rodents.44 HTVs are often classified as either hanta-
viral fever with renal syndrome (HRS) in the Old World or
hantaviral pulmonary syndrome (HPS) in the New World,
but this dichotomy is not clear in all cases.45 All HTVs are
parasitic in small rodents, such as mice, rats, and voles,
causing a relatively asymptomatic lifelong infection. HTVs
are often species specific, sometimes infecting only a single
rodent species.39
HPSs cause severe, sometimes fatal, respiratory disease
and are mainly associated with wild rodent species of the
subfamily Sigmodontinae.46 In the US and Canada, the Sin
Nombre virus (also found in other parts of the Americas) is
responsible for the majority of cases of HPS. The host of
the Sin Nombre virus is the deer mouse (Peromyscus man-
iculatus), found throughout the western and central US and
Canada but also southward in the Americas. In South
America a myriad of different HTVs can be found: Andes
virus has been reported in Argentina, Chile, and Uruguay;
Laguna Negra virus in Paraguay and Bolivia; Rio Mamoré
virus in Bolivia; Caño Delgadito virus in Venezuela; and
Araraquara and Juquitiba viruses in Brazil.47
The most severe form of HRS is caused by Hantaanvirus
(ie, carried by wild urban rats Rattus norvegicus and Rattus
rattus and Apodemus mice) and Dobrava-Belgrade virus
(associated with Apodemus mice) that occur in Asia and
Eastern Europe. A moderate form, the Seoul virus (carried
by various species of rats), occurs only in Asia. The majority
of mild hantavirus infections in Europe are caused by
Puumala virus (primarily associated with the bank vole,
Clethrionomys glareolus).44 Mortality after exposure to the
severe forms is approximately 5% to 15% and to the milder
form, 1% to 2%.
Because HTVs exist worldwide and are mainly trans-
mitted by aerosols, there is concern about their potential
use as biological weapons, even if they are only listed as
category C agents on the CDC’s list of bioagents. Their
potential threat is increased by the fact that immunity in
populations is generally very low, many strains without
cross-protection exist, and no vaccines are available.39
Furthermore, diagnosis can be difficult when the disease
occurs outside its typical range, as initial clinical symptoms
are nonspecific.39 Still, HTVs are notoriously difficult to
isolate and produce, even with the means available in the
most advanced laboratories, and they usually do not
transmit from person-to-person.44 The relative rodent
Volume 11, Supplement 1, 2013
LÕHMUS ET AL.
host-specificity of the most virulent HTVs means that in-
troduction of the disease to local wild rodents is possible
only in endemic areas (although spill-over effects to local
species outside of the endemic areas have not yet been in-
vestigated and must be considered a possibility). In-
troduced into rural or urban rodent fauna, HTVs have
the potential to cause long-term medical episodes and to
spread fear.
Filoviruses
Filoviruses, Marburg and Ebola, are highly virulent path-
ogens that have a high mortality rate. If terrorists were to
cause even a small outbreak of Marburg or Ebola, the
public perception of the threat alone could cause major
social and economic disruption.48 However, the life cycle of
these viruses and the potential capacity of rodents as vectors
or reservoirs for Ebola and Marburg is still largely un-
known. Fruit bats are commonly suggested as the main
reservoirs for these diseases,49 but Morvan et al.50 detected
Ebola virus glycoprotein and polymerase gene sequences in
rodents and shrews and suggested that common small ter-
restrial mammals living in peripheral forest areas could be
reservoirs for Ebola. Even though these results have been
debated,49 the possibility that rodents would function as
vectors or reservoirs for these viruses in the event of bio-
terrorism cannot be ruled out. Furthermore, since more
than a week would elapse before the first symptoms of
illness appear, and since Filoviruses survive at room tem-
perature in liquid or dried material for a number of days,
the release of these viruses in an urban area48 could result in
their transmission (eg, to rodents) before the disease is
discovered.
Rift Valley Fever Virus
RVFV is a zoonotic arthropodborne pathogen native to
Africa that increasingly causes severe morbidity and mor-
tality in humans and livestock.51 The lack of prophylactic
and therapeutic methods, the potential for human-to-
human transmission, and the significant threat to livestock
associated with RVFV make this pathogen a serious bio-
terrorism threat.52 RVFV is transmitted through a broad
range of mosquito genera and by other vectors including
sand flies.51 This broad range of competent mosquito
vectors, some with a worldwide distribution, makes the
prospect of transmission and spread to native wildlife fol-
lowing a bioterrorism event possible. Rodents, among them
brown rats, have shown RVFV antibodies in endemic areas
and have been suggested to serve as potential intermediate
amplifying hosts during periods of livestock immunity
following an epizootic. In this way, rodents would play a
crucial role in the maintenance of the virus’s natural cycle.53
Human RVFV infections are usually preceded by trans-
mission from wild to domestic animal hosts. RVFV has a
devastating effect on livestock: For example, in sheep,
mortality in lambs under 2 weeks of age approaches 100%,
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RODENTS AS COURIERS FOR BIOTERORISM AGENTS
in older animals 30%, and abortions approach 100%.
Cattle also show high abortion rates (up to 100%), with
adult mortality at approximately 10%.51
Contagious Animal Diseases
Even if they do not affect human health, an outbreak of
contagious animal diseases can have serious economic con-
sequences for livestock. Consequently, enzootic livestock
diseases represent a potentially serious threat against national
agricultures as well as many wildlife species.2 Several for-
merly devastating diseases that have been eradicated from
livestock populations in the western world over the past
century are still common and readily accessible elsewhere.2
For some diseases, samples or cultures obtained from in-
fected animals are all that would be required to initiate a
serious outbreak. Foot-and-mouth disease, malignant ca-
tarrhal fever, Newcastle disease, and Rift Valley fever are
examples of diseases that can pose major threats to livestock
and wildlife and that have been cultivated and possibly
weaponized according to Office International des Epizoo-
ties.2 Furthermore, these diseases have been shown to infect
or be transported by rodents. Other diseases that can infect
rodents and could cause economic losses in agricultural set-
tlements are classical swine fever, porcine parovirus, clinical
encephalomyocarditis fever virus, and neosporosis.15
Will Human Infections Be Detected
in Time?
The degree and spread of human infections after a bioattack
depends on local circumstances. In well-developed areas
with good medical resources, the disease dispersal is likely
to be noticed and stopped earlier than in poor and degraded
areas. If an urban bioattack should result in roaming in-
fected rodents, the most likely humans to first encounter
the pathogens are people in degraded urban areas with poor
hygiene and especially homeless people. Because of their
isolation from the community, these groups can see the
disease developing to full lethal proportions before it is
discovered. If an affected person is alive when transported
to the hospital, the hospital has a chance of performing
diagnostics, and it is likely that the pathogen will be
identified. But this depends on the standards and experi-
ence of the hospital staff, and in cases of bioattacks the
previous experience and consequently the capacity to expect
a disease may be lacking even if the hospital has high
standards. When a person who died due to an unknown,
uncommon disease is presented for autopsy, the chances are
small that the pathologist will recognize it immediately, and
there is a risk that no extra precaution will be taken initially,
thus providing the pathogen with the potential to spread to
those in the autopsy room. As is the case with tuberculosis
transmission in autopsy rooms,54 other pathogens can be
S254
aerosolized during an autopsy and spread to workers. If the
body is still fresh at the autopsy, an infectious disease may
be recognized, but if a body is already decomposing, there is
no chance that a forensic pathologist will recognize an in-
fection because the decomposition will hide every possible
sign. In this scenario, the chances of transmitting the
pathogen to, for instance, a pathologist or members from
the police team, in addition to the wildlife that may have
been previously rooting around the body, are significant.
Additionally, no alarm will reach the public until days later
when more infections have been discovered.
Prevention, Communication,
and Education
It is obvious that the best way to, at least partly, avoid the
dispersal of rodentborne diseases after a bioattack is to
control the number of (commensal) rodents before the
possible incidence. The efficacy of proactive rodent control
programs is evident from several reports, but today
complaint-based reactive pest control seems to be the most
popular strategy for rodent management among policy-
makers, as these control actions are easy to document and
demonstrate to those with a rodent problem.55 Un-
fortunately, data from the UK show that if no proactive
control is undertaken, it is unlikely that more than about
30% of infestations would be eliminated by a reactive
complaints-based strategy. An alternative proactive rodent
control strategy enables resources to be targeted where the
risk is greatest and is more likely to achieve effective
control.55 One of the best examples of this strategy is the
long-term urban rodent control program undertaken in
Budapest, Hungary, where a strategy applied and moni-
tored over 30 years has not only involved effective control
methods but also an analysis of the behavior and habitat use
of urban rats.55 Furthermore, several ecological manage-
ment approaches to control city rats, involving changing
the location of food sources in buildings so that the envi-
ronment is less predictable to rats and breaking links be-
tween populations in resource-rich patches have been
demonstrated to be efficient in the long term.20 However,
resources for proactive work are in many places in the world
being withdrawn in favor of less effective and poorly tar-
geted reactive strategies.55
When a bioattack happens, in an emergency, there is no
time to develop an elaborate strategy for public health com-
munication. If the situation has not been analyzed properly,
officials will most likely improvise, and the risk of spreading
incorrect information is great.31 Methods of communication
that function without inducing panic among the general
public must therefore be developed in advance.
Local pest management and control agencies are valuable
partners for officials in case of a rodentborne disease out-
break, since they most likely have the data about current
rodent activity, and they are specialists in pest elimination
Biosecurity and Bioterrorism: Biodefense Strategy, Practice, and Science

methods. Consequently, they need to be involved in the
lines of communication both with officials and the general
public.
After a bioattack involving rodentborne pathogens, rats
and mice, both dead and live, should be considered po-
tentially infectious.31 People should be advised not to touch
dead animals and to make their homes, shelters, and cabins
rodent-proof. Homes should also be kept clean, and food
and garbage should be covered in rodent-proof containers.7
However, as discussed above, rodent-proofing and cutting
off the food flow of rodents in a facility that already con-
tains infected rodents would just result in spreading the
pathogens to other households as the rodents will try to find
new food sources. Local trapping is recommended, but it is
difficult to perform efficient trapping over large rural areas.
Rodenticides may be a more efficient solution, but not
many rodenticides are allowed in outdoor environments, as
the side effects of them on nontarget species may be dev-
astating and cause liver toxicity and increased parasite and
pathogen burden.56-58 Furthermore, many rodent species
have been shown to become resistant to the most com-
monly used rodenticides.59 Consequently, developing an
efficient and nature-friendly way to implement rodent
control would be of high importance.
A failure to involve the public as a key partner in a public
health crisis could hamper effective epidemic manage-
ment.60 Simple, clear language should be used for public
instructions, making it easier for all groups of society to
follow them. As described above, when a pathogen has been
introduced among wildlife species, the eradication of it will
be difficult, and recurring disease outbreaks can be expected
in the future. Consequently, the recommendations for
handling the situation must be made with a long-term
perspective.
Tailored messages are needed for people with jobs that
create special exposures. Special education may be provided
for, for example, hunters and outdoor recreationists. Re-
stricting activities in areas that are likely to harbor infected
animals can also be an important preventive strategy.7
People who are frequently outdoors should also make sure
they wear tick-, flea-, and mosquito-proof clothes and wash
their hands with clean water after contact with soil. Do-
mestic pets should be treated for ectoparasites, as they often
can bring disease home.7
Active surveillance of wild animal populations both be-
fore and after a bioterrorism attack is necessary for identi-
fying common baseline values for occurrence of certain
diseases and sources of infection in the environment. Better
approaches for intervention are needed to be able to prevent
the spread of an introduced biological warfare agent into a
wild animal population.6 We also need additional research
about relative susceptibilities and exposure pathways for
animal species living near human populations. An ability to
rapidly detect introduced diseases and react quickly to
hazards is essential for successful and cost-effective disease
control. Diagnostic methods that facilitate early detection
Volume 11, Supplement 1, 2013
LÕHMUS ET AL.
(eg, analyses that can detect hundreds of pathogens in a
single sample, multiplex assays) can help in the process.
Acknowledgments
Writing of this publication has been supported by the
framework of the EU project AniBio Threat (Grant Agreement:
Home/2009/ISEC/AG/191) with financial support from the
Prevention of and Fight against Crime Programme of the
European Union, European Commission—Directorate Gen-
eral Home Affairs. This publication reflects the views only of the
authors, and the European Commission cannot be held re-
sponsible for any use that may be made of the information
contained therein.
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Manuscript received December 21, 2012;
accepted for publication May 30, 2013.
Address correspondence to:
Mare Lo˜hmus, PhD
Associate Professor
Department of Ecology and Genetics
Evolutionary Biology Centre
Uppsala University
Uppsala, Sweden
E-mail: mare.lohmus@gmail.com
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