Progress, challenges, and the role of public engagement to improve tick-borne disease literacy

Article (PDF Available)inCurrent Opinion in Insect Science 28 · May 2018with 95 Reads
DOI: 10.1016/j.cois.2018.05.011
Abstract
Vector-borne diseases have increased worldwide, facilitated by globalization and variations in climate. Tick and tick-borne disease researchers, veterinarians, medical practitioners, and public health specialists are working to share their expertise on tick ecology, disease transmission, diagnostics, and treatment in order to control tick-borne epidemics and potential pandemics. This review will be a brief overview of the current status of tick-borne diseases, challenges on the scientific and public fronts, and the role of public engagement in improving citizen education within the context of ticks and tick-borne disease research.
Progress,
challenges,
and
the
role
of
public
engagement
to
improve
tick-borne
disease
literacy
Joyce
M
Sakamoto
1,2
Vector-borne
diseases
have
increased
worldwide,
facilitated
by
globalization
and
variations
in
climate.
Tick
and
tick-borne
disease
researchers,
veterinarians,
medical
practitioners,
and
public
health
specialists
are
working
to
share
their
expertise
on
tick
ecology,
disease
transmission,
diagnostics,
and
treatment
in
order
to
control
tick-borne
epidemics
and
potential
pandemics.
This
review
will
be
a
brief
overview
of
the
current
status
of
tick-borne
diseases,
challenges
on
the
scientific
and
public
fronts,
and
the
role
of
public
engagement
in
improving
citizen
education
within
the
context
of
ticks
and
tick-borne
disease
research.
Addresses
1
Department
of
Entomology,
The
Pennsylvania
State
University,
University
Park,
PA
16802
United
States
2
Center
for
Infectious
Disease
Dynamics,
The
Pennsylvania
State
University,
University
Park,
PA
16802
United
States
Corresponding
author:
Sakamoto,
Joyce
M
(jms1198@psu.edu)
Current
Opinion
in
Insect
Science
2018,
28:81–89
This
review
comes
from
a
themed
issue
on
Vectors
and
medical
and
veterinary
entomology
Edited
by
Jason
Rasgon
https://doi.org/10.1016/j.cois.2018.05.011
2214-5745/ã
2018
Elsevier
Inc.
All
rights
reserved.
Introduction
Humans
live
in
a
globally
connected
world,
where
activities
in
one
part
of
the
world
may
have
impacts
on
other
distantly
connected
part.
Fluctuations
in
climate
have
been
corre-
lated
with
changes
in
vector
biology
and
increased
vector-
borne
diseases
at
local
and
global
scales
[1–3,4

].
Although
tick-borne
diseases
(TBD)
may
not
be
as
dramatically
impacted
by
sudden
short-term
changes
in
temperature
as
mosquito-borne
diseases,
warmer
winters
have
been
correlated
with
invasion
and
establishment
of
certain
tick
vector
species
into
northern
latitudes
[3,4

,5].
Scientists,
medical
and
veterinary
practitioners,
and
pub-
lic
health
specialists
strive
to
understand
vector
biology
and
disease
dynamics,
design
better
diagnostic
tools,
and
develop
better
treatments
for
vector-borne
diseases
on
behalf
of
the
public.
TBD
experts
therefore
have
a
responsibility
to
disseminate
their
findings
and
recom-
mendations
to
the
public
in
a
clear,
concise
manner
that
can
be
readily
understood.
This
review
provides
an
overview
of
the
current
status
of
research
on
ticks
and
TBD,
challenges
facing
TBD
experts,
and
the
impor-
tance
of
active,
bidirectional
engagement
with
the
public.
Ticks
Ticks
are
obligate
bloodfeeding
arachnids
in
the
order
Acari
[6].
Fossil
evidence
from
Baltic
amber
suggest
ticks
have
been
parasitizing
vertebrates
since
the
Cretaceous
(ca
99
MYA)
[7,8].
Although
known
for
their
role
as
vectors
of
pathogens,
ticks
themselves
are
considered
noxious
pests
whose
bites
can
be
cause
irritations,
anemia,
localized
or
systemic
allergic
reactions
(including
meat
allergies),
as
well
as
more
serious
issues
such
as
tick
paralysis
[9–11].
At
the
time
of
this
writing,
there
are
722
described
species
of
hard
ticks
(Ixodidae)
and
208
species
of
soft
ticks
(Argasidae)
[6].
Approximately
5%
of
known
Ixodidae
and
2%
of
Argasidae
are
known
vectors
of
zoonotic
dis-
eases
[12].
Since
at
least
38%
of
all
tick
species
are
known
to
bite
humans
(though
not
necessarily
the
intended
hosts),
it
is
likely
that
new
TBD
will
continue
to
be
identified
[12,13

].
As
human
populations
grow,
broader
encroachment
and
fragmentation
of
wild
habitats
may
increase
contact
with
pathogen-laden
ticks
[14].
Global
tick-borne
diseases
TBD
incidence
is
increasing
at
an
alarming
rate,
signaling
the
need
for
a
more
proactive
stance
to
prevent
outbreaks
of
pandemic
proportions
[15].
While
Borrelia
burgdorferi
(the
causal
agent
of
Lyme
borreliosis)
is
by
far
the
most
prevalent
tick-borne
pathogen
in
the
temperate
countries
of
the
world,
other
emerging
or
newly
discovered
tick-
borne
pathogens
(many
of
which
are
potentially
fatal)
are
also
being
described
annually
[4

,16–18].
Worldwide
there
are
two
TBD
of
pandemic
or
epidemic
scale
recog-
nized
by
the
World
Health
Organization
(Crimean-Congo
Hemorrhagic
Fever
and
Tularemia
[http://www.who.int/
emergencies/diseases/en/]).
Rocky
Mountain
Spotted
Fever,
an
emergent
TBD
that
is
spreading
throughout
the
Americas,
can
be
transmitted
by
multiple
tick
species
[19
].
Factors
contributing
to
increased
TBD
incidence
include
habitat
fragmentation,
global
travel,
importation
of
animals,
changing
environmental
conditions,
and
shifts
in
host
populations
in
response
to
light
pollution,
habitat
removal
or
encroachment,
or
altered
migration
behaviors
of
reservoir
hosts)
[4

,14,20–24].
Available
online
at
www.sciencedirect.com
ScienceDirect
www.sciencedirect.com
Current
Opinion
in
Insect
Science
2018,
28:81–89
While
some
countries
have
dedicated
significant
scien-
tific,
political,
and/or
monetary
resources
toward
TBD
research,
other
countries
lack
the
facilities
or
funds
for
monitoring
and
combatting
TBD,
or
do
not
consider
TBD
as
top
priorities
for
public
health,
particularly
when
they
are
being
impacted
by
other
vector-borne
diseases
[25].
Nevertheless,
the
impacts
of
TBD
in
poorer
coun-
tries
can
exacerbate
already-existing
socioeconomic
inequalities
[25,26].
In
a
globally
connected
world,
public
health
concerns
in
one
country
are
no
longer
isolated
and
the
‘every
country
for
itself’
attitude
of
the
past
no
longer
holds
true.
Global
exports,
exotic
pet
trade,
and
human
travel
have
all
contributed
to
introduction
of
novel
vector
species
and
their
pathogens
into
nonnative
areas
[23,24,27].
Excluding
global
human
traffic
and
trade,
many
migrating
wild
species
(such
as
birds)
travel
between
tropical
and
arctic
biorealms
and
have
been
implicated
as
vehicles
for
invading
tick
species
as
far
north
as
the
arctic
circle
[28
,29–31].
Ticks
and
tick-borne
disease
in
USA
Although
40
of
84
described
species
of
ticks
in
the
contiguous
United
States
are
known
to
bite
humans,
eight
species
are
responsible
for
the
majority
of
TBD
[13

,32,33].
These
few
species
represent
multiple
taxa,
yet
the
common
characteristics
that
make
them
such
effective
vectors
is
the
generality
of
host
preference
and
the
behavior
of
actively
seeking
out
hosts.
In
contrast,
many
species
of
ticks
are
nidicolous,
preferring
to
remain
within
the
nest
or
burrows
of
their
hosts
for
the
entirety
of
their
lifecycles
[34].
However,
if
their
preferred
host
is
no
longer
available,
some
nidicolous
species
will
readily
seek
non-typical
hosts
[35,36].
This
can
result
in
sudden
out-
breaks
of
diseases
when
an
unsuspecting
human
comes
in
contact
with
a
hungry
tick
(e.g.
tickborne
relapsing
fever
transmitted
by
the
soft
tick
Ornithodoros
hermsii
feeding
on
rodents
and
humans
co-inhabiting
cabins)
[35].
Between
2004
and
2016,
reported
cases
of
TBD
have
more
than
doubled
[37].
Lyme
disease
(LD)
(principally
caused
by
Borrelia
burgdorferi
sensu
stricto
in
the
United
States)
accounted
for
402,502
of
the
642,602
total
reported
vector-borne
(62.6%),
and
82%
of
all
reported
TBD
cases
[18].
It
is
estimated
that
300,000
cases
of
LD
are
diagnosed
each
year,
although
only
10%
of
these
cases
are
actually
reported
to
the
Centers
for
Disease
Control
(CDC)
[18].
LD
was
first
described
in
the
early
1970s,
manifesting
first
as
a
juvenile
form
of
arthritis
in
Lyme
Connecticut,
but
until
the
incidence
rates
rose
signifi-
cantly,
it
was
not
a
priority
for
public
health
[38,39].
Eventually,
LD
did
garner
enough
national
attention
to
inspire
a
Senate
bill
that
increased
federal
funds
for
improving
tick-borne
disease-related
activities
(research,
treatment,
prevention,
and
education).
In
December
of
2016,
President
Obama
signed
the
21st
Century
Cures
Act,
which
included
authorization
of
the
Department
of
Health
and
Human
Services
to
support
TBD
research
and
create
a
multidisciplinary
‘Tick-borne
Disease
Work-
ing
Group’.
Although
national
effort
toward
TBD
control
can
be
slow,
there
is
at
least
hope
that
support
is
now
available
for
research.
Challenges
on
the
scientific
front
Vector
biologists
can
play
a
key
role
in
providing
insight
into
environmental
management
to
prevent
tick
infesta-
tion
or
disease
transmission.
Improving
communication
between
vector
researchers
and
other
TBD-related
fields
would
greatly
improve
disease
surveillance.
Some
diag-
nostic
facilities
have
an
expert
who
can
identify
vector
species
using
morphological
and/or
molecular
character-
istics
(e.g.
New
York
State
Veterinary
Diagnostic
Laboratory).
There
is
a
need
for
fast,
affordable,
and
reliable
multiplex
diagnostic
tools,
and
many
new
options
are
on
the
hori-
zon.
Whole
genome
sequencing
technology
has
made
it
possible
to
identify
novel
tick-borne
pathogens
as
they
are
encountered
(such
as
Borrelia
mayonii,
Heartland
and
Bourbon
viruses)
[37].
While
these
diagnostic
tools
are
promising,
many
are
proprietary,
making
it
difficult
for
those
doing
field
vector
surveillance
to
find
a
standardized
diagnostic
approach
without
sending
off
materials
to
a
commercial
laboratory.
Challenges
on
the
public
front
When
TBD
specialists
do
not
effectively
communicate
with
the
public,
the
public
may
not
be
aware
of
the
research
progress
being
made.
As
medical,
veterinary,
and
scientific
professions
develop
and
test
methods
for
combatting
new
or
emerging
tick-borne
pathogens,
the
public
is
ultimately
the
intended
beneficiary.
Yet
many
TBD
experts
will
refrain
from
public
engagement,
par-
ticularly
when
they
feel
an
issue
is
politicized
and
that
the
intended
audience
does
not
want
to
listen.
Tick
bite
prevention
education
is
not
easy
and
may
require
repetition,
persistence,
and
patience.
In
response
to
changes
in
climate
and
the
eventual
spread
of
LD,
the
Canadian
government
launched
an
aggressive
campaign
of
tick
and
reservoir
host
surveillance,
assessment
of
public
TBD
literacy,
and
public
education
in
2014
[3,40–42,43
].
Over
time
they
have
observed
that,
despite
overall
increase
in
general
awareness
of
LD,
less
than
half
the
population
was
utilizing
tick
prevention
strategies
[44].
Humans
can
be
slow
to
change
health
behavior,
but
communications
on
TBD
risk
need
to
be
persistent
about
the
importance
of
preventative
measures
for
eventual
change
[44].
TBD-literacy
The
most
effective
strategies
for
tick
bite
prevention
(and
TBD
transmission)
are
avoidance
of
high-risk
areas,
pre-
ventative
approaches
such
as
showers
and
tick
checks,
and
proper
application
or
usage
of
acaricides
and/or
82
Vectors
and
medical
and
veterinary
entomology
Current
Opinion
in
Insect
Science
2018,
28:81–89
www.sciencedirect.com
repellents.
It
is
important
to
ensure
that
these
strategies
are
clear
to
maximize
the
likelihood
that
the
public
will
follow
these
strategies
correctly
and
consistently.
One
hurdle
that
a
successful
TBD
prevention
and
man-
agement
program
needs
to
overcome
is
the
level
of
TBD
awareness
of
the
average
patient.
Patients
may
not
know
how
to
prevent
tick
bites
or
identify
symptoms
beyond
the
not-always-present
erythema
migrans,
the
classic
LD
expanding
annular
rash
(bullseye)
[38].
Patients
may
hold
misconceptions
about
TBD,
often
acquired
through
online
browsing,
social
media,
or
television
sources.
Local
or
regional
efforts
to
improve
public
education
on
tick
bite
prevention
are
sometimes
available
in
more
popu-
lated
or
well-funded
areas,
but
these
approaches
often
fail
to
effectively
reach
disadvantaged
people,
areas
in
which
technology-based
dissemination
is
not
an
option,
or
very
rural
or
wilderness
areas.
Publicly
available
sources
of
TBD
information
Passive
dissemination
of
TBD
knowledge
has
its
role
in
providing
information
regarding
the
outcomes
of
data
analysis
and
recommendations
for
high-risk
areas.
The
Centers
for
Disease
Control
maintains
several
informa-
tive
pages
on
their
website
ranging
from
recommenda-
tions
on
communicating
risk,
reporting
recent
TBD-
related
findings,
as
well
as
suggested
approaches
to
com-
municating
TBD
risk
for
medical
professionals
[10]
(https://www.cdc.gov/ticks/;
https://www.cdc.gov/ncezid/
;
https://www.cdc.gov/niosh/topics/tick-borne/resources.
html).
The
CDC
site
represents
a
wealth
of
information,
but
much
of
it
is
geared
toward
disseminating
information
to
scientists,
practitioners,
or
public
health
experts,
or
on
best
practices
when
communicating
to
the
public.
Although
some
pages
are
intended
for
the
public,
they
can
sometimes
be
difficult
to
navigate.
Nevertheless,
the
information
presented
is
usually
up-to-date
and
cites
information
based
on
current
or
recently
completed
stud-
ies
published
in
peer-reviewed
journals.
Another
publicly
available,
but
not
readily
discoverable
resource
is
available
from
the
US
Army.
The
Disease
Epidemiology
Division
US
Army
Zoonotic
Disease
Report
for
2015
was
released
by
the
Army
Public
Health
Center
in
2017
(http://phc.amedd.army.mil/Periodical%
20Library/ZDR_CY2015_v2.pdf).
These
data
reflect
the
One
Health
approach
in
that
the
data
collected
here
include
all
zoonotic
incidents
from
active-duty
military
personnel,
incidents
from
non-active
duty
beneficiaries,
the
location
of
acquisition
of
zoonotic
diseases,
veterinary
disease
summaries
on
DoD-associated
animals,
and
wild-
life
and
vector
surveillance
results.
Several
universities
maintain
TBD
educational
resource
(e.g.
University
of
Rhode
Island’s
http://www.
tickencounter.org).
These
sites
balance
information,
lev-
ity,
and
effective
visual
aids
to
engage
the
nonscientist.
Some
universities
have
developed
apps,
collect
citizen-
based
data
state-
or
nationwide
(including
photos
of
ticks),
and
present
tick
risk
predictions
relevant
to
season,
tick
species,
and
present
regional
TBD
diseases.
Tick-
encounters.org
uses
compelling
(and
sometimes
enter-
taining)
multimedia
presentations
that
appeal
to
the
public
sector
ranging
from
computer
graphics,
mobile
applications,
resources
on
tick
pathogen
testing,
and
several
educational
how-to
videos
on
pesticide
applica-
tion,
tick
checks,
and
tick
removal.
Dispelling
misconceptions
through
engagement
Community
engagement
has
been
shown
to
be
highly
effective
in
providing
citizens
the
opportunity
to
ask
questions,
voice
concerns,
and
dispel
fears
about
mos-
quito
control
strategies
implemented
by
the
World
Mos-
quito
Program
(formerly
Eliminate
Dengue
[45
]).
Simi-
larly,
TBD
active
engagement
at
the
local
or
regional
scales
may
encourage
citizens
to
learn
how
to
protect
themselves,
but
also
to
dispel
certain
misconceptions
about
risk,
symptom
recognition,
and
prevention.
For
instance,
TBD
may
be
perceived
as
a
disease
of
more
rural
environments,
but
in
fact,
people
in
urban
areas
may
also
be
at
risk
if
at
least
one
vector
and
one
zoonotic
reservoir
host
are
present
[11,46].
Even
though
urban
areas
are
mostly
managed,
many
species
of
wildlife
can
adjust
to
and
thrive
in
manmade
habitats
(parks,
trails,
gardens,
attics,
backyards,
etc.)
[11].
While
it
is
assumed
that
people
who
engage
in
‘outdoor
activities’
are
at
risk,
what
constitutes
‘outdoor
activity’
may
not
necessarily
be
as
obvious
as
hunting,
biking,
or
camping.
Gardeners,
pet
owners,
farmers,
scouts,
hunters,
foresters,
as
well
as
citizens
utilizing
common
green-
spaces
(e.g.
parks)
may
be
potentially
exposed
to
tick
habitats
[44,47

,48–50].
Those
who
provide
support
such
as
environmental
health
specialists
or
wilderness
provi-
ders
also
need
to
be
trained
in
being
tick-vigilant
[48,51].
“One
Health
Initiative”
Globalization
has
connected
the
world
in
remarkable
ways,
but
has
also
accelerated
the
spread
of
vector-borne
diseases
[37].
Each
new
or
re-emerging
infectious
disease
highlights
the
need
for
rapid
disease
prevention
and
control.
This
requires
multidisciplinary
communication
between
veterinary
and
medical
health
care
workers,
wildlife
biologists,
ecologists,
anthropologists,
and
others.
‘One
Health’
reflects
the
realization
that
emerging
zoo-
notic
diseases
occur
at
the
interfaces
of
animal–human–
ecosystem
[13

].
Although
veterinary
and
medical
professionals
have
largely
pioneered
much
of
the
effort,
‘One
Health
Initi-
ative’
was
intended
to
foster
communication
across
mul-
tiple
disciplines
[52].
The
value
of
One
Health-based
multidisciplinary
communication
between
physicians
and
Engaging
the
public
about
tick-borne
disease
Sakamoto
83
www.sciencedirect.com
Current
Opinion
in
Insect
Science
2018,
28:81–89
veterinarians
is
evident
in
the
example
of
a
fatal
disease
outbreak
is
the
Rocky
Mountain
Spotted
Fever
(RMSF)
case
in
Mississippi
[13

,53].
Two
dogs
misdiagnosed
with
ehrlichiosis
died
of
RMSF,
followed
thereafter
by
their
owner.
Subsequently,
there
was
an
investigation
and
successful
treatment
of
the
remaining
two
dogs
for
RMSF.
The
surviving
dogs
had
been
infested
with
Rhi-
picephalus
sanguineus
(the
brown
dog
tick),
previously
not
considered
a
vector
of
RMSF
[53].
This
case
identified
R.
sanguineus
as
a
competent
vector
of
RMSF
and
indicated
that
dogs
can
serve
as
sentinels
for
RMSF.
Furthermore,
if
a
dog
is
suspected
of
being
infected
with
RMSF,
both
veterinary
and
medical
professionals
should
report
this
to
the
appropriate
medical
authority
(e.g.
state
public
health
agencies
or
the
CDC)
[53].
Human
health
is
integrally
tied
to
the
health
of
domestic
and
wild
animals.
The
importance
of
cross-communica-
tion
between
veterinary
and
medical
professionals
is
evident,
particularly
in
respect
to
zoonoses[13

,52,54].
Pet
owners
may
have
an
increased
risk
of
tick
bites
[47

].
Dogs
can
acquire
ectoparasites
when
multiple
dogs
are
in
contact,
or
if
the
dogs
are
boarded
in
a
kennel,
and
then
bring
the
ticks
home
with
them
[55].
Similarly,
cats
that
hunt
outdoors
may
encounter
wildlife
(e.g.
groundhogs,
squirrels,
chipmunks)
and
become
exposed
to
zoonotic
diseases
[56–59].
More
generally,
humans
and
domesti-
cated
animals
are
at
higher
risk
of
acquiring
tick-borne
pathogens
from
reservoir
hosts
when
living
in
close
prox-
imity
to
or
in
contact
with
wildlife
[47

,57,60,61].
Passive
tick
surveillance
Passive
tick
surveillance
usually
involves
submissions
by
non-acarologists to expertsat regional,state, or national level
institutions.
This
requires
doctors,
veterinarians,
or
other
citizens
to
submit
tick
samples
for
identification
and/or
testing
for
pathogens.
The
advantage
to
this
approach
is
that
it
can
cover
a
wide
geographic
range,
providing
a
finer-
scale
resolution
of
the
tick/TBD
load
[41,43
,62,63].
The
main
caveat
is
that
associated
data
may
be
incomplete,
the
samples
can
be
damaged
during
removal
(losing
important
morphological
characteristics),
and
there
is
an
intrinsic
host-
association
bias
for
ticks
found
on
humans
or
domestic
animals
[64].
It
is
also
time-consuming
and
effort-intensive
to
catalog
and
curate
the
database
generated
from
the
samples
and
the
metadata
[65,66].
Nevertheless,
these
data
represent
a
measure
of
the
risk
of
bites
because
the
ticks
are
usually extracted
from
or
associated
with
host
tissue.
Passive
surveillance
data
can
be
complementary
to
active
surveil-
lance
data,
and
can
also
be
used
to
tailor
experimental
designs
for
downstream
host-association
studies
using
trapped,
hunted,
or
road-killed
animals,
or
combined
with
CO
2
or hostvolatile-modified trapping from nestsor burrows
[40,67–69].
Because
animals
may
represent
sentinels
for
zoonotic
diseases,
indirect
mining
of
electronic
pet
health
records
can
be
useful
alternative
for
identifying
increased
risk
of
TBD
through
records
of
tick
infestations
[70].
This
approach
did
not
require
intensive
surveillance
or
molec-
ular
diagnostics
and
could
serve
as
a
cost-effective
com-
plement
to
an
already
existing
tick
surveillance
program
to
identify
pockets
of
tick
activity
that
might
be
missed
by
passive
surveillance
alone.
Collectively,
tick
from
com-
panion
animals
could
be
used
to
create
a
real-time
map
of
TBD
risk
(e.g.
http://www.capcvet.org).
Novel
public
engagement
approaches
Multi-disciplinary
approaches
to
TBD
education
through
citizen
engagement
can
cultivate
exciting,
creative,
and
sometimes
unusual
methods
(Figure
1).
The
Dutch
National
Institute
for
Public
Health
and
the
Environment
(RIVM)
has
used
a
multimedia
strategy
(website,
media,
video
game,
leaflets)
to
target
adults
and
children
for
TBD
education
[71,72].
Alone,
these
approaches
have
not
been
shown
to
significantly
improve
tick
bite
prevention,
but
together
they
work
as
complementary
strategies
to
reinforce
good
preventative
practices.
Additionally,
RIVM
launched
a
website
and
an
affiliated
app
(https://www.tekenradar.nl/)
that
allows
citizens
to
record
data
associated
with
when
they
were
bitten
(age,
photo
of
the
tick,
the
bite,
whether
they
have
had
Lyme
disease
before,
whether
or
not
they
develop
a
bulls-eye
rash)
[73].
While
citizens
are
responsible
for
initial
symptom
diag-
nosis
and
reporting,
ticks
can
also
be
submitted
for
identification
and
testing
by
trained
professionals
[73].
Public
submissions
of
tick
photos
for
identification
have
also
been
used
in
Canada
and
in
the
USA
[74].
Another
nontraditional
public
engagement
approach
is
the
use
of
mass
participation
events
(e.g.
marathons)
to
engage
a
large
group
of
people
converging
at
a
single
location
in
contributing
to
a
tick
risk
study
[75

].
Mass
participation
events
are
great
opportunities
for
large-scale
citizen
contributions
in
a
localized
area
[75

].
In
many
ways,
it
has
the
advantages
of
a
‘bioblitz’,
a
group
event
in
which
scientists
and
citizens
meet
at
a
particular
location
for
a
brief
period
of
time
to
capture
and
identify
as
many
species
in
an
area
to
estimate
local
biodiversity
(https://
www.inaturalist.org/pages/bioblitz+guide).
However,
the
mass
participation
tick
collection
takes
advantage
of
an
already
existing
event
to
collect
data
and
to
educate
the
participants
about
tick
checks
and
TBD.
Citizen
science
approach
can
be
useful
for
fine-scale
active
tick
surveillance
[76].
Each
citizen
enrolled
in
the
study
monitored
a
small
plot
(e.g.
their
backyard)
and
provided
repeated
measures
of
tick
load
from
multi-
ple
sources
such
as
pets,
gardens,
or
flags
(using
a
white
towel
or
cloth
on
vegetation)
[76].
This
fine-scale
approach
concurs
with
the
finding
by
the
CDC,
which
found
that
for
residential
properties,
determining
abso-
lute
numbers
of
infected
ticks
would
provide
a
better
estimate
of
risk,
particularly
if
the
degree
of
human
use
of
84
Vectors
and
medical
and
veterinary
entomology
Current
Opinion
in
Insect
Science
2018,
28:81–89
www.sciencedirect.com
the
property
is
also
taken
into
account
[77].
This
becomes
a
much
more
tenable
undertaking
once
citizens
are
involved
in
the
data
collection
process.
In
another
study,
Seifert
et
al.
(2016)
partnered
with
rural
high
school
teachers
to
teach
high
school
students
about
science,
TBD,
and
tick
surveillance
[78
].
This
model
could
be
extended
toward
other
community-based
groups
such
as
elementary
schools,
school
nurses,
parent–teacher
orga-
nizations,
or
clubs
to
train
children
and
their
parents
about
how
to
prevent
tick
bites.
Suggestions
for
public
engagement
One
of
the
ways
we
can
encourage
TBD
literacy
is
to
cultivate
more
active
community
involvement
in
tick
surveillance
and
provide
control
strategies
that
are
easy
to
follow.
There
are
many
potential
approaches
that
can
be
explored
or
implemented.
Multiple
social
medial
plat-
forms,
citizen
science,
groups,
and
formal
science
com-
munication
(scicomm)
training
of
TBD
experts
collec-
tively
may
expand
the
reach
and
efficacy
of
outreach
education.
Approaches
to
improve
TBD
literacy
need
to
go
beyond
the
deficit
model
of
public
engagement
(i.e.
unidirec-
tional
dissemination
of
information).
It
is
important
to
assess
public
familiarity
with
tick
bite
prevention,
resis-
tance
to
pesticide
use,
likelihood
of
compliance,
recognition
of
TBD
symptoms,
and
necessity
of
consult-
ing
a
physician
or
veterinarian.
The
public
should
also
be
directed
to
scientists
who
specialize
in
identifying
ticks.
Social
media
can
be
highly
effective
at
disseminating
infor-
mation
rapidly,
but
requires
careful
planning
and
proper
timing
for
maximum
impact.
The
platform
chosen
for
out-
reach
needs
to
match
the
audience
different
platforms
appeal
to
different
demographics
[79,80].
Social
media
may
also
provide
data
on
local
or
regional
tick
abundance
and
seasonality
or
report
invasive
tick
species
(https://twitter.
com/Contagion_Live/status/979056024119373826).
How-
ever,
strategic
forethought
and
marketing
expertise
is
advis-
able
to
avoid
potential
unwanted
outcomes
(e.g.
ticks
on
poppy
seed
muffins,
https://twitter.com/CDCgov/status/
993523011281145858).
Citizen
science
can
be
used
to
facilitate
public
submis-
sion
of
data
and
allow
interested
citizens
to
be
more
actively
involved
in
a
scientific
process
that
may
benefit
them.
Citizen
science-based
projects
allow
scientists
to
increase
the
amount
of
data
collected
or
handled
that
would
otherwise
be
difficult
to
achieve.
It
is
important,
however,
to
ensure
a
bidirectional
conversation
between
the
public
and
researchers,
providing
regular
updates
on
the
progress
of
studies
in
which
they
are
participating.
Engaging
the
public
about
tick-borne
disease
Sakamoto
85
Figure
1
Universities
Wildlife Research
Veterinarians
Diagnostic
Companies
Hospitals/Clinics
Veterinary databases
Mass participation
events
Multimedia
Public submission
Current Opinion in Insect Science
Sources
of
ticks
from
surveillance.
Tick
surveillance
provides
useful
information
that
can
be
used
to
identify
risk
of
tick
bites
and
TBD
traditional
sources.
Information
can
be
from
more
traditional
sources
such
as
veterinary
or
medical
hospitals
or
clinics,
universities,
or
wildlife
biologists.
Other
sources
of
ticks,
host-association,
or
pathogen
data
may
include
tick
testing
companies,
electronic
veterinary
record
databases,
mass
participation
events,
or
various
public-based
contributions
(physical
or
photographic
submissions,
citizen
scientists,
etc).
www.sciencedirect.com
Current
Opinion
in
Insect
Science
2018,
28:81–89
Formal
training
of
TBD
specialists
in
science
communi-
cation
is
not
normally
part
of
graduate
or
postgraduate
career
experience,
but
perhaps
it
should
be.
TBD
spe-
cialists
need
to
be
able
to
disseminate
their
data
beyond
the
academic
and
professional
spheres
to
journalists,
policy
makers,
stakeholders,
industry,
but
without
the
use
of
jargon
[81
].
Developing
positive
bidirectional
lines
of
communication
between
TBD
experts
and
the
media
provides
journalists
with
news
on
scientific
prog-
ress
and
insight
into
what
tick
species
is
a
vector
of
which
disease,
and
gives
scientists
the
opportunity
to
reach
a
large
audience.
TBD
experts
in
turn
need
to
listen
and
adjust
management
recommendations
while
taking
into
consideration
the
cultural,
socio-economical,
and
physical
limitations
of
citizens.
Best
models
for
engagement
may
be
dependent
on
the
target
audience.
An
effective
engagement
approach
would
be
to
firstly
keep
the
message
simple
and
jar-
gon-free,
secondly
have
easy-to-understand
protocols,
and
lastly
use
visual
aids.
While
there
is
definitely
an
appeal
to
incorporate
next-gen
technology
(e.g.
aug-
mented,
virtual,
or
mixed
reality),
the
emphasis
should
be
on
the
message
and
not
on
the
‘glitz’.
Conclusion
TBD
researchers,
practitioners,
and
experts
have
the
advantage
over
many
other
members
of
the
scientific
community.
The
public
loves
to
hate
ticks
and
is
there-
fore
much
more
likely
to
engage
in
conversation
about
ticks,
TBD,
and
ways
to
prevent
tick
bites.
This
makes
public
engagement
that
much
easier,
but
taken
a
step
further,
public
involvement
can
provide
insight
into
activities
and/or
studies
in
which
the
average
citizen
can
feel
personally
empowered
as
contributors
to
the
scientific
process.
Although
there
may
be
the
perception
amongst
scientists
that
the
public
does
not
trust
scientific
research,
this
is
a
misconception
and
in
fact
the
opposite
is
true
[82].
Scien-
tists
are
becoming
acutely
aware
of
the
importance
of
effective
science
communication
and
this
applies
to
TBD
experts
as
well.
It
is
the
responsibility
of
those
studying
vector
biology,
vector-borne
diseases,
and
public
health
to
teach
the
public
how
to
protect
themselves,
prevent
or
minimize
vector-borne
disease
transmission,
recognize
symptoms
that
require
immediate
attention,
and
to
record
information
that
will
facilitate
correct
diag-
nosis
and
treatment.
Transitioning
from
simply
providing
information
to
actively
engaging
communities
will
ulti-
mately
improve
our
vector-borne
disease
education
efforts.
The
United
States
is
a
very
large
country,
so
while
there
are
many
great
local
or
regional
efforts,
there
is
still
a
need
for
unifying
TBD
education
efforts
and
integration
of
resources.
Efforts
at
state
or
regional
levels
vary
in
some
states,
dedicated
staff
members
spend
a
great
deal
of
effort
on
vector
control
and
on
public
outreach,
while
in
others,
the
burden
falls
on
academic
institutions
or
public
health
departments.
Perhaps
with
the
passing
of
the
21st
Century
Cures
Act
and
the
CDC
report
on
vector-borne
disease
on
the
rise,
support
for
improved
TBD
public
education
is
just
on
the
horizon
[37,83

].
Conflict
of
interest
statement
Nothing
declared.
Acknowledgements
Many
thanks
to
Rebecca
M
Johnson,
Dr
Chen
Heu
for
formatting
and
editing
suggestions,
to
Drs
Brittany
Dodson
and
Donghun
Kim
for
insightful
discussion,
and
the
anonymous
reviewers
for
constructive
suggestions.
Funding
support
from
NSF/BIO
grant
1645331.
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Environ
Res
Public
Health
2018,
15.
The
author
present
a
review
of
current
research
on
potential
implications
of
climate
change
for
disease
transmission
by
four
of
the
most
important
vector
species
of
ticks
in
the
USA.
5.
Jore
S,
Vanwambeke
SO,
Viljugrein
H,
Isaksen
K,
Kristoffersen
AB,
Woldehiwet
Z,
Johansen
B,
Brun
E,
Brun-Hansen
H,
Westermann
S
et
al.:
Climate
and
environmental
change
drives
Ixodes
ricinus
geographical
expansion
at
the
northern
range
margin.
Parasites
Vectors
2014,
7:11.
6.
Nava
S,
Venzal
JM,
Gonza
´lez-Acun
˜a
D,
Martins
TF,
Guglielmone
AA:
Chapter
1
tick
classification,
external
tick
anatomy
with
a
glossary,
and
biological
cycles.
Ticks
of
the
Southern
Cone
of
America.
Academic
Press;
2017:1-23.
7.
Klompen
H,
Grimaldi
D:
First
mesozoic
record
of
a
parasitiform
mite:
a
larval
Argasid
tick
in
Cretaceous
Amber
(Acari:
Ixodida:
Argasidae).
Ann
Entomol
Soc
Am
2001,
94:10-15.
8.
Dunlop
JA,
Garwood
RJ:
Tomographic
reconstruction
of
the
exceptionally
preserved
Trigonotarbid
Arachnid
Eophrynus
prestvicii.
Acta
Palaeontol
Pol
2014,
59:443-454.
9.
Morshed
M,
Li
L,
Lee
M-K,
Fernando
K,
Lo
T,
Wong
Q:
A
Retrospective
Cohort
Study
of
Tick
Paralysis
in
British
Columbia.
Vector
Borne
Zoonotic
Dis
2017,
17:821-824.
10.
Mead
P,
Hinckley
A,
Hook
S,
Beard
CB:
TickNET
a
collaborative
public
health
approach
to
tickborne
disease
surveillance
and
research.
Emerg
Infect
Dis
2015,
21:1574-1577.
11.
Brites-Neto
J,
Duarte
KMR,
Martins
TF:
Tick-borne
infections
in
human
and
animal
population
worldwide.
Vet
World
2015,
8:301-315.
12.
Guglielmone
AA,
Robbins
RG,
Apanaskevich
DA,
Petney
TN,
Estrada-Pen
˜a
A,
Horak
IG:
The
Hard
Ticks
of
the
World.
Netherlands:
Springer;
2014.
13.

Dantas-Torres
F,
Chomel
BB,
Otranto
D:
Ticks
and
tick-borne
diseases:
a
One
Health
perspective.
Trends
Parasitol
2012,
28:437-446.
86
Vectors
and
medical
and
veterinary
entomology
Current
Opinion
in
Insect
Science
2018,
28:81–89
www.sciencedirect.com
Although
this
is
not
a
paper
from
the
last
2
years,
it
is
an
important
paper
that
highlights
the
importance
of
cross-disciplinary
communication
for
tick-borne
zoonoses,
putting
them
in
the
context
of
One
Health.
14.
Simon
JA,
Marrotte
RR,
Desrosiers
N,
Fiset
J,
Gaitan
J,
Gonzalez
A,
Koffi
JK,
Lapointe
F-J,
Leighton
PA,
Lindsay
LR
et
al.:
Climate
change
and
habitat
fragmentation
drive
the
occurrence
of
Borrelia
burgdorferi,
the
agent
of
Lyme
disease,
at
the
northeastern
limit
of
its
distribution.
Evol
Appl
2014,
7:750-764.
15.
de
la
Fuente
J,
Waterhouse
RM,
Sonenshine
DE,
Roe
RM,
Ribeiro
JM,
Sattelle
DB,
Hill
CA:
Tick
genome
assembled:
new
opportunities
for
research
on
tick–host–pathogen
interactions.
Front
Cell
Infect
Microbiol
2016,
6.
16.
Donohoe
H,
Pennington-Gray
L,
Omodior
O:
Lyme
disease:
current
issues,
implications,
and
recommendations
for
tourism
management.
Tour
Manag
2015,
46:408-418.
17.
Gulia-Nuss
M,
Nuss
AB,
Meyer
JM,
Sonenshine
DE,
Roe
RM,
Waterhouse
RM,
Sattelle
DB,
de
la
Fuente
J,
Ribeiro
JM,
Megy
K
et
al.:
Genomic
insights
into
the
Ixodes
scapularis
tick
vector
of
Lyme
disease.
Nat
Commun
2016,
7:10507.
18.
Hinckley
AF,
Connally
NP,
Meek
JI,
Johnson
BJ,
Kemperman
MM,
Feldman
KA,
White
JL,
Mead
PS:
Lyme
disease
testing
by
large
commercial
laboratories
in
the
United
States.
Clin
Infect
Dis
2014,
59:676-681.
19.
Fang
R,
Blanton
LS,
Walker
DH:
Rickettsiae
as
emerging
infectious
agents.
Clin
Lab
Med
2017,
37:383-400.
Much
attention
is
focused
on
the
role
of
ticks
in
Lyme
disease,
but
there
are
other
tickborne
zoonoses
that
are
emerging,
some
which
have
fatal
outcomes.
While
both
pathogenic
and
nonpathogenic
Rickettsia
species
have
co-evolved
with
arthropod
hosts,
ticks
transmit
the
majority
of
pathogenic
species.
This
paper
provides
an
updated
review
of
rickett-
sioses
and
the
increase
in
the
number
of
incidences
worldwide.
20.
Chen
LH,
Wilson
ME:
Tick-borne
rickettsiosis
in
traveler
returning
from
Honduras.
Emerg
Infect
Dis
2009,
15:1321-1323.
21.
Gonza
´lez-Acun
˜a
D,
Beldome
´nico
PM,
Venzal
JM,
Fabry
M,
Keirans
JE,
Guglielmone
AA:
Reptile
trade
and
the
risk
of
exotic
tick
introductions
into
southern
South
American
countries.
Exp
Appl
Acarol
2005,
35:335-339.
22.
Mansfield
KL,
Jizhou
L,
Phipps
LP,
Johnson
N:
Emerging
tick-
borne
viruses
in
the
twenty-first
century.
Front
Cell
Infect
Microbiol
2017,
7.
23.
Mihalca
AD:
Ticks
imported
to
Europe
with
exotic
reptiles.
Vet
Parasitol
2015,
213:67-71.
24.
Molaei
G,
Andreadis
TG,
Anderson
JF,
Stafford
Iii
KC:
An
exotic
hitchhiker:
a
case
report
of
importation
into
Connecticut
from
Africa
of
the
human
parasitizing
tick,
Hyalomma
truncatum
(Acari:
Ixodidae).
J
Parasitol
2018
http://dx.doi.org/10.1645/18-
13.
25.
Bardosh
KL,
Ryan
S,
Ebi
K,
Welburn
S,
Singer
B:
Addressing
vulnerability,
building
resilience:
community-based
adaptation
to
vector-borne
diseases
in
the
context
of
global
change.
Infect
Dis
Poverty
2017,
6.
26.
Godfrey
ER,
Randolph
SE:
Economic
downturn
results
in
tick-
borne
disease
upsurge.
Parasites
Vectors
2011,
4:35.
27.
Corn
JL,
Mertins
JW,
Hanson
B,
Snow
S:
First
reports
of
ectoparasites
collected
from
wild-caught
exotic
reptiles
in
Florida.
J
Med
Entomol
2011,
48:94-100.
28.
Cohen
EB,
Auckland
LD,
Marra
PP,
Hamer
SA:
Avian
migrants
facilitate
invasions
of
neotropical
ticks
and
tick-borne
pathogens
into
the
United
States.
Appl
Environ
Microbiol
2015,
81:8366-8378.
This
paper
highlights
the
importance
of
global
spread
of
ticks
and
TBD
through
migrating
birds.
The
authors
present
data
on
predominantly
neotropical
birds
migrating
between
Texas,
and
Central
or
South
Amer-
ica,
the
tick
diversity,
and
the
pathogenic
bacteria
that
were
present
in
both
birds
and
ticks.
They
estimate
that
between
4
and
39
million
ticks
are
introduced
each
year
on
migrating
birds.
29.
La
Sorte
FA,
Fink
D,
Blancher
PJ,
Rodewald
AD,
Ruiz-Gutierrez
V,
Rosenberg
KV,
Hochachka
WM,
Verburg
PH,
Kelling
S:
Global
change
and
the
distributional
dynamics
of
migratory
bird
populations
wintering
in
Central
America.
Glob
Change
Biol
2017,
23:5284-5296.
30.
Mukherjee
N,
Beati
L,
Sellers
M,
Burton
L,
Adamson
S,
Robbins
RG,
Moore
F,
Karim
S:
Importation
of
exotic
ticks
and
tick-borne
spotted
fever
group
rickettsiae
into
the
United
States
by
migrating
songbirds.
Ticks
Tick-Borne
Dis
2014,
5:127-134.
31.
Wu
X,
Ro
¨st
G,
Zou
X:
Impact
of
spring
bird
migration
on
the
range
expansion
of
Ixodes
scapularis
tick
population.
Bull
Math
Biol
N
Y
2016,
78:138-168.
32.
Eisen
RJ,
Kugeler
KJ,
Eisen
L,
Beard
CB,
Paddock
CD:
Tick-
borne
zoonoses
in
the
United
States:
persistent
and
emerging
threats
to
human
health.
ILAR
J
2017
http://dx.doi.org/10.1093/
ilar/ilx005.
33.
Merten
HA,
Durden
LA:
A
state-by-state
survey
of
ticks
recorded
from
humans
in
the
United
States.
J
Vector
Ecol
J
Soc
Vector
Ecol
2000,
25:102.
34.
Takken
W,
Knols
BGJ:
Olfaction
in
Vector–Host
Interactions.
Wageningen
Academic
Publ;
2010.
35.
Gaither
M,
Schumacher
M,
Nieto
N,
Corrigan
J,
Murray
H,
Maurer
M:
Where
are
the
ticks?
Solving
the
mystery
of
a
tickborne
relapsing
fever
outbreak
at
a
youth
camp.
J
Environ
Health
Denver
2016,
78:8-11.
36.
Lubelczyk
C,
Cahill
BK,
Hanson
T,
Turmel
J,
Lacombe
E,
Rand
PW,
Elias
SP,
Smith
JRP:
Tick
(Acari:
Ixodidae)
infestation
at
two
rural,
seasonal
camps
in
Maine
and
Vermont.
J
Parasitol
2010,
96:442-443.
37.
Rosenberg
R:
Vital
signs:
trends
in
reported
vectorborne
disease
cases
United
States
and
Territories,
2004–2016.
MMWR
Morb
Mortal
Wkly
Rep
2018,
67.
38.
Steere
AC,
Broderick
TF,
Malawista
SE:
Erythema
chronicum
migrans
and
Lyme
arthritis:
epidemiologic
evidence
for
a
tick
vector.
Am
J
Epidemiol
1978,
108:312-321.
39.
Steere
AC,
Strle
F,
Wormser
GP,
Hu
LT,
Branda
JA,
Hovius
JWR,
Li
X,
Mead
PS:
Lyme
borreliosis.
Nat
Rev
Dis
Primer
2016,
2:16090.
40.
Bouchard
C,
Leighton
PA,
Beauchamp
G,
Nguon
S,
Trudel
L,
Milord
F,
Lindsay
LR,
Be
´langer
D,
Ogden
NH:
Harvested
white-
tailed
deer
as
sentinel
hosts
for
early
establishing
Ixodes
scapularis
populations
and
risk
from
vector-borne
zoonoses
in
southeastern
Canada.
J
Med
Entomol
2013,
50:384-393.
41.
Lieske
DJ,
Lloyd
VK:
Combining
public
participatory
surveillance
and
occupancy
modelling
to
predict
the
distributional
response
of
Ixodes
scapularis
to
climate
change.
Ticks
Tick-Borne
Dis
2018,
9:695-706.
42.
Nelder
MP,
Russell
C,
Lindsay
LR,
Dhar
B,
Patel
SN,
Johnson
S,
Moore
S,
Kristjanson
E,
Li
Y,
Ralevski
F:
Population-based
passive
tick
surveillance
and
detection
of
expanding
foci
of
blacklegged
ticks
Ixodes
scapularis
and
the
Lyme
disease
agent
Borrelia
burgdorferi
in
Ontario,
Canada.
PLOS
ONE
2014,
9:e105358.
43.
Ripoche
M,
Gasmi
S,
Adam-Poupart
A,
Koffi
JK,
Lindsay
LR,
Ludwig
A,
Milord
F,
Ogden
NH,
Thivierge
K,
Leighton
PA:
Passive
tick
surveillance
provides
an
accurate
early
signal
of
emerging
Lyme
disease
risk
and
human
cases
in
Southern
Canada.
J
Med
Entomol
2018
http://dx.doi.org/10.1093/jme/tjy030.
The
authors
present
a
comparative
analysis
of
passive
surveillance,
active
surveillance,
and
reported
human
cases
of
Lyme
disease
in
Canada.
They
found
that
passive
tick
surveillance
was
correlated
with
tick
abundance
(risk
of
tick
encounter),
but
also
a
good
indicator
of
Lyme
disease
risk.
44.
Aenishaenslin
C,
Bouchard
C,
Koffi
JK,
Ogden
NH:
Exposure
and
preventive
behaviours
toward
ticks
and
Lyme
disease
in
Canada:
results
from
a
first
national
survey.
Ticks
Tick-Borne
Dis
2017,
8:112-118.
45.
Kolopack
PA,
Parsons
JA,
Lavery
JV:
What
makes
community
engagement
effective?
Lessons
from
the
eliminate
dengue
program
in
Queensland,
Australia.
PLoS
Negl
Trop
Dis
2015,
9:
e0003713.
Engaging
the
public
about
tick-borne
disease
Sakamoto
87
www.sciencedirect.com
Current
Opinion
in
Insect
Science
2018,
28:81–89
The
authors
describe
how
Eliminate
Dengue
(now
World
Mosquito
Pro-
gram)
was
able
to
successfully
implement
its
strategies
by
engaging
community
members.
46.
Kowalec
M,
Szewczyk
T,
Welc-Fale?ciak
R,
Si
nski
E,
Karbowiak
G,
Bajer
A:
Ticks
and
the
city
are
there
any
differences
between
city
parks
and
natural
forests
in
terms
of
tick
abundance
and
prevalence
of
spirochaetes?
Parasit
Vectors
2017,
10:573.
47.

Jones
EH,
Hinckley
AF,
Hook
SA,
Meek
JI,
Backenson
B,
Kugeler
KJ,
Feldman
KA:
Pet
ownership
increases
human
risk
of
encountering
ticks.
Zoonoses
Public
Health
2018,
65:74-79.
The
authors
present
data
supporting
the
correlation
between
pet
own-
ership
and
likelihood
of
tick
contact
using
data
obtained
through
TickNET
from
2727
households
in
the
USA,
the
multi-state
surveillance
network
established
by
the
CDC.
Given
that
over
70%
of
US
households
have
at
least
one
pet,
veterinary
professionals
can
play
a
significant
role
in
TBD
prevention.
48.
Forrester
JD,
Vakkalanka
JP,
Holstege
CP,
Mead
PS:
Lyme
disease:
what
the
wilderness
provider
needs
to
know.
Wilderness
Environ
Med
2015,
26:555-564.
49.
Li
S,
Juha
´sz-Horva
´th
L,
Tra
´jer
A,
Pinte
´r
L,
Rounsevell
MDA,
Harrison
PA:
Lifestyle,
habitat
and
farmers’
risk
of
exposure
to
tick
bites
in
an
endemic
area
of
tick-borne
diseases
in
Hungary.
Zoonoses
Public
Health
2018,
65:e248-e253.
50.
De
Keukeleire
M,
Vanwambeke
SO,
Somasse
`E,
Kabamba
B,
Luyasu
V,
Robert
A:
Scouts,
forests,
and
ticks:
impact
of
landscapes
on
human-tick
contacts.
Ticks
Tick-Borne
Dis
2015,
6:636.
51.
Stott
RE,
Richards
SL,
Balanay
JAG,
Martin
GL:
Prevention
of
tick
exposure
in
environmental
health
specialists
working
in
the
Piedmont
Region
of
North
Carolina.
J
Environ
Health
Denver
2016,
78:E1-E7.
52.
Rabinowitz
PM,
Natterson-Horowitz
BJ,
Kahn
LH,
Kock
R,
Pappaioanou
M:
Incorporating
one
health
into
medical
education.
BMC
Med
Educ
2017,
17.
53.
Elchos
BN,
Goddard
J:
Implications
of
presumptive
fatal
Rocky
Mountain
spotted
fever
in
two
dogs
and
their
owner.
J
Am
Vet
Med
Assoc
2003,
223:1450-1452.
54.
Gibbs
EPJ:
The
evolution
of
One
Health:
a
decade
of
progress
and
challenges
for
the
future.
Vet
Rec
2014,
174:85-91.
55.
Bombara
CB,
Du
¨rr
S,
Machovsky-Capuska
GE,
Jones
PW,
Ward
MP:
A
preliminary
study
to
estimate
contact
rates
between
free-roaming
domestic
dogs
using
novel
miniature
cameras.
PLOS
ONE
2017,
12.
56.
Davies
S,
Abdullah
S,
Helps
C,
Tasker
S,
Newbury
H,
Wall
R:
Prevalence
of
ticks
and
tick-borne
pathogens:
Babesia
and
Borrelia
species
in
ticks
infesting
cats
of
Great
Britain.
Vet
Parasitol
2017,
244:129-135.
57.
Rodrı
´guez-Vivas RI,
Apanaskevich
DA,
Ojeda-Chi
MM,
Trinidad-
Martı
´nez I,
Reyes-Novelo
E,
Esteve-Gassent
MD,
Pe
´rez
de
Leo
´n
AA:
Ticks
collected
from
humans,
domestic
animals,
and
wildlife
in
Yucatan,
Mexico.
Vet
Parasitol
2016,
215:106-113.
58.
Scott
JD,
Anderson
JF,
Durden
LA,
Smith
ML,
Manord
JM,
Clark
KL:
Prevalence
of
the
Lyme
disease
Spirochete,
Borrelia
burgdorferi,
in
Blacklegged
Ticks,
Ixodes
scapularis
at
Hamilton-Wentworth,
Ontario.
Int
J
Med
Sci
2016,
13:316-324.
59.
Shannon
AB,
Rucinsky
R,
Gaff
HD,