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Climate Change and Vector-Borne Diseases of Public Health Significance
Climate Change and Vector-Borne Diseases of Public Health Significance
Climate Change and Vector-Borne Diseases of Public Health Significance
doi: 10.1093/femsle/fnx186
Advance Access Publication Date: 7 September 2017
Minireview
M I N I R E V I E W – Environmental Microbiology
ABSTRACT
There has been much debate as to whether or not climate change will have, or has had, any significant effect on risk from
vector-borne diseases. The debate on the former has focused on the degree to which occurrence and levels of risk of
vector-borne diseases are determined by climate-dependent or independent factors, while the debate on the latter has
focused on whether changes in disease incidence are due to climate at all, and/or are attributable to recent climate change.
Here I review possible effects of climate change on vector-borne diseases, methods used to predict these effects and the
evidence to date of changes in vector-borne disease risks that can be attributed to recent climate change. Predictions have
both over- and underestimated the effects of climate change. Mostly under-estimations of effects are due to a focus only on
direct effects of climate on disease ecology while more distal effects on society’s capacity to control and prevent
vector-borne disease are ignored. There is increasing evidence for possible impacts of recent climate change on some
vector-borne diseases but for the most part, observed data series are too short (or non-existent), and impacts of
climate-independent factors too great, to confidently attribute changing risk to climate change.
1
2 FEMS Microbiology Letters, 2017, Vol. 364, No. 19
Figure 1. Direct effects of climate and weather on vector populations and vector-borne pathogen transmission illustrated by potential effects on West Nile virus
transmission (from Ogden and Lindsay 2016). Dark and pale blue arrows indicate, respectively, development and host finding, while red arrows indicate pathogen
transmission. Points at which weather and climate (and potentially climate change) may impact the vector’s lifecycle and pathogen transmission cycle are indicated
by the grey-filled boxes in which A = effects on activity, D = effects on inter-stadial development rates, EI = effects on the extrinsic incubation period, Re = effects on
reproduction, and T = effects of temperature, Ra = effects of rainfall and RH = effects of humidity.
wildlife, and their occurrence is intrinsically less determined by of refuges for vector survival during weather extremes, which
man’s control efforts (Ogden et al. 2014c). are particularly important for hard-bodied ticks due to their long
This review has three main sections that aim to briefly de- interstadial development times. Climate and weather impact
scribe, and point the reader to literature on (i) possible effects of transmission cycles of vector-borne pathogens directly by ef-
climate change on vector-borne diseases; (ii) how we can pre- fects of temperature on the duration of the extrinsic incubation
dict these effects to assist decision making on public health period of pathogens in insect vectors, which is a crucial factor
policies and programmes; and (iii) evidence to date for impacts determining whether or not insect-borne diseases can persist or
of climate change on some example vector-borne diseases. I not. Habitat characteristics also determine the communities of
conclude with suggested needs for improving our prepared- vertebrate hosts, and host biodiversity (and biodiversity change)
ness to respond to anticipated changing risk from vector-borne can impact transmission of those vector-borne zoonoses for
diseases. which wildlife are the main reservoirs (Cable et al. 2017).
Predicted climate changes include increasing temperatures,
changes to geographic patterns of rainfall, increasing climate
HOW CAN CLIMATE CHANGE AFFECT THE variability, and increasing frequency and severity of extreme
weather events (Fig. 2; IPCC 2013). All of the above climate-
RISK FROM VECTOR-BORNE DISEASES?
and weather-dependent factors may, therefore, be impacted by
Risk from vector-borne diseases is intrinsically sensitive to a changing climate resulting in changes to where and when
changes in weather and climate. This has been extensively re- environments may be suitable for vectors and vector-borne
viewed (e.g. Medlock and Leach 2015; Parham et al. 2015; Ogden pathogens to thrive. The expected result is changes in ge-
and Lindsay 2016), and I briefly summarise these reviews as fol- ographic and seasonal patterns of vector-borne disease oc-
lows and in Fig. 1. Where, when and how many arthropod vec- currence and levels of their risk. Changing dynamics of host
tors are found directly depend on multiple impacts of weather communities, vectors and pathogens is expected to also drive
and climate including direct effects of low and high tempera- changes in the landscape of fitness of different genetic vari-
tures on vector mortality rates, effects of temperature and hu- ants of microorganisms and vectors. This may alter the fitness
midity on activity and host finding of vectors, effects of temper- and abundance of strains/genetic variants of pathogens and vec-
ature on rates of vector development from one life stage to the tors, and drive ‘adaptive’ emergence of novel strains and species
next and effects of rainfall on availability of breeding habitat for of public health significance (Gortazar et al. 2014). In general,
insect vectors. Climate has also indirect impacts on vector oc- it would be expected that many vector-borne diseases trans-
currence by determining qualities of habitat and availability of mitted by flies would be able to respond quickly to changes in
animal hosts for vector blood meals. Characteristics of habitat weather and climate, because of the short (several weeks long)
are important for vector survival by determining the availability lifecycles of many dipteran vectors, resulting in increasingly
Ogden 3
Figure 3. Possible impacts of climate change on changing risks from vector-borne diseases illustrated using possible impacts on Canada as an example. VBD = vector-
borne disease, WNV = West Nile virus, CSV = California serogroup viruses, RVF = Rift valley fever, JE = Japanese encephalitis, EEE = eastern equine encephalitis, La
Crosse = La Crosse encephalitis, HME = human monocytic ehrlichiosis.
when and where climate change may cause vector-borne dis- actually have indirect impacts on the factors controlling vector
eases to emerge, re-emerge or indeed die out. This foresight in- or pathogen occurrence. Unsurprisingly, when both overpredict-
formation is essential for the development of policies on pre- ing mathematical models and possibly underpredicting pattern-
paredness for vector-borne disease risks that may arise in the matching methods are used for the same vector-borne disease,
more distant future, the design of public health programmes for they can yield starkly different results. This has been the case
more immediate risks and the identification of research gaps for predictions of climate change impacts on malaria (Martens
(Campbell-Lendrum et al. 2015). Predictions involve identifying et al 1995; Rogers and Randolph 2000), and these widely different
climatic limits for vectors and vector-borne pathogen transmis- assessments, compounded by the use of models that are con-
sion, identifying where and when those climatic limits occur at sidered too simplistic (Tanser, Sharp and le Sueur 2003; Reiter
present and then, using global or regional climate models, pro- et al. 2004), have contributed to considerable debate on potential
jecting where and when those same climatic limits, and by in- impacts of climate change and vector-borne diseases (Lafferty
ference the vectors and vector-borne pathogens, will occur in 2009).
the future (Fig. 4). There are two broad ways in which predic- The notion that ‘all models are wrong but some are useful’
tive relationships between climate and vector-borne pathogen applies to those used to predict the effects of climate change
occurrence are obtained. The first is the use of empirical data on on vector-borne diseases. Our confidence in using them to de-
climatic limits often synthesised across the vector lifecycle and velop policies and programmes increases with (i) validation of
pathogen transmission cycle in dynamic mathematical popula- the deduced climate-vector/vector-borne disease relationship
tion models (e.g. Ogden et al. 2005; Ermert et al. 2011). The second using data independent of those employed in calibrating the
is the ‘pattern matching’ use of field data on occurrence of vec- models; (ii) exploration of uncertainty in model predictions aris-
tors and pathogens to find quantitative associations between cli- ing from uncertainty in model parameter estimates (e.g. Parham
mate data and vector/pathogen presence (using ecological niche and Michael 2010; Beale and Lennon 2012); (iii) accounting for
modelling methods: Peterson 2003) or presence/absence (using climate-independent factors in model construction or in simu-
statistical methods: Lorenz et al. 2014). For these methods, cur- lations (Woolhouse 2011; Fox et al. 2012); (iv) exploration of as-
rent climate and climate-independent data are obtained from semblages of climate models that may provide a range of pro-
interpolated ground-level observations or from satellite data, jected future climates that are equally possible (McPherson et al.
which are linked to field observations of vectors and pathogens 2017); and, eventually (v) validation by observed effects of cli-
using geographic information systems (e.g. Gabriele-Rivet et al. mate change (see below).
2017).
In either case, predictions that are made while account-
ing for climate independent factors are those that are, by and WHAT IS THE EVIDENCE TO DATE OF EFFECTS
large, the most useful. Predictions that are made using math- OF CLIMATE CHANGE ON VECTOR-BORNE
ematical models without considering the modifying effects
DISEASES OF PUBLIC HEALTH SIGNIFICANCE?
of climate-independent factors may well overestimate effects
of climate change. Conversely, predictions made by pattern- Clearly, the most powerful driver for public health policy
matching methods on the basis of current distributions of on climate change and vector-borne diseases would be the
vector-borne diseases may well underestimate potential climate presence of empirical evidence. However, amongst the most
change effects if (i) distributions are highly controlled by seem- contentious issues around climate change and vector-borne
ingly climate-independent factors and (ii) if climate change will diseases is whether or not there is evidence to date for effects
Ogden 5
Tick-borne encephalitis (TBE): The possible role of climate over long distances by migratory birds (Ogden, Mechai and Mar-
change in changes in incidence of TBE in Europe has been a gos 2013). Likely for these reasons, at the northern edge of their
source of debate almost as intense as that around malaria (e.g. geographic ranges, northward range expansion of B. burgdor-
Hay 2001; Lindgren and Gustafson 2001; Randolph 2004, 2010). feri has followed that of the tick vectors (Ogden, Lindsay and
This debate has focused on evidence for climate change impacts Leighton 2013). In Canada at least, expansion of the range of the
on increases in incidence of human cases (Hay 2001; Lindgren tick, followed by that of B. burgdorferi, has been accompanied by
and Gustafson 2001), and in particular on alternative explana- an increase in human Lyme disease cases (Ogden et al. 2014a).
tions for observed changes in incidence. Apart from the effects Incursion of tropical/subtropical vector-borne diseases into temper-
of anticipated climate change on the geographic range of the ate zones: A key fear for public health in temperate zone coun-
tick vectors, a warming climate has been predicted to impact tries is that a tropical/subtropical vector-borne disease, that is
whether or not TBE transmission cycles can persist via effects highly transmissible human to human via mosquitoes, will be-
on seasonality of tick activity where Ixodes ricinus is the vector. come established due to effects of climate change. This possi-
The short period of infectivity of rodent hosts means that trans- bility has received much attention in terms of qualitative (e.g.
mission is only efficient when the seasonal activity periods of Rezza 2014; Medlock and Leach 2015; Ebi and Nealon 2016) and
nymphal I. ricinus ticks infecting the rodents, and larval ticks ac- quantitative (or at least data-driven) assessments of the risk
quiring infection from the rodents, are very synchronous (Ran- of endemic/autochthonous transmission of tropical/subtropical
dolph et al. 1999). Projected effects of climate change in central vectors and vector-borne diseases (e.g. Caminade et al. 2012; Og-
and northern Europe are a northward range shift (rather than den et al. 2014b; Ng et al. 2017). There have clearly been invasions
simply expansion) in the early decades of this century, followed of tropical/subtropical vectors and vector-borne diseases into
by an increasingly fragmented occurrence of transmission cy- temperate regions, and these include the invasion and spread of
cles as warming continues (Randolph and Rogers 2000). There West Nile virus in North America (Kilpatrick 2011; Reisen 2013),
are a number of reports that provide some evidence for chang- an outbreak of chikungunya in Italy (Angelini et al. 2007) and
ing geographic patterns of vector ticks and TBE incidence that autochthonous cases of dengue and Leishmaniasis in Europe
may be consistent with climate change (e.g. Daniel et al. 2009; (Naucke et al. 2008; Tomasello and Schlagenhauf 2013; Schaffner
Tokarevich et al. 2011, 2017), and a recent northward range shift and Mathis 2014). However, while we can predict that climate
in Sweden (Lindgren and Gustafson 2001) would be consistent change may increase the probability of these events (via direct
with the projected early effects of climate change (Randolph and impacts on local environmental suitability and indirect effects
Rogers 2000). More recently, analyses of human case surveil- on migration and control efforts in endemic countries), the ex-
lance data have identified (i) changes in altitude of TBE occur- tent to which these events to date have been associated with cli-
rence and (ii) spreading of the pattern of seasonal occurrence mate change is unknown. A range of climate-independent plau-
of TBE cases, as well as changes in incidence, which may all be sible explanations include increased travel and globalisation of
consistent with effects of climate change (Křı́ž et al. 2015). The trade increasing introduction probabilities, adaptation of vec-
authors do not state that these data prove climate change ef- tors and virus to temperate climates, and the occurrence of un-
fects, but they underline that the observed patterns mean that expected suitable niches for exotic vectors (Medlock and Leach
climate change effects are plausible. However, in some parts of 2015).
Europe, recent increases in TBE incidence have most likely been
associated with socioeconomic changes, landscape change and
other factors that have changed rates of contact between the hu- CONCLUSION
man population and infective ticks (Sumilo et al. 2007; Korenberg
Efforts to predict impacts of climate change on vector-borne
2009; Zeman, Pazdiora and Beneš 2010; Zeman and Benes 2013).
diseases must continue to drive the development of public
Lyme disease: Surveillance systems and targeted studies in
health policies and programmes that reduce the impact of
Canada and Sweden have been able to detect recent northward
emerging and re-emerging vector-borne diseases. Ideally such
range expansion of tick vectors of Lyme disease (I. scapularis and
model-based assessments of risk should include consideration
I. ricinus respectively) (Lindgren, Tälleklint and Polfeldt 2000; Og-
of climate-dependent and independent factors that directly af-
den et al. 2010, 2014a; Leighton et al. 2012). Furthermore, there
fect vector-borne disease transmission, and also more distal ef-
is more solid evidence, in the form of geographic patterns and
fects of climate change on vector-borne disease that may arise
timing of expansion related to regional warming, that changes
due to socioeconomic impacts of climate change on our soci-
in the northern limits of these vectors can be attributed to recent
eties. Surveillance for vector-borne diseases needs to be imple-
warming climate (Lindgren, Tälleklint and Polfeldt 2000; Ebi et al.
mented but with intensity of effort tailored towards the im-
2017b). Expansion of the range of I. scapularis is attributed to the
mediate risk level (Murphy, Vaux and Medlock 2013; Kampen
effects of a warming climate on shortening the lifecycle of the
et al. 2015). In many circumstances, this will involve entomo-
tick rather that direct effects of warming temperatures on tick
logical surveillance, or other methods such as sentinel ani-
survival (Ogden 2014), while the precise mechanism of effect on
mal surveillance, that provides an early warning in advance
I. ricinus has not yet been elucidated. Borrelia burgdorferi trans-
of human disease cases and helps to validate and improve
mission cycles are robust, particularly when compared to those
model-based predictions. For attribution of changing vector-
for TBE, because of the long duration of infectivity of infected
borne disease risks to climate change, long-term (i.e. decades)
hosts, and the very wide host range (including birds) for some B.
surveillance programmes would need to be planned for. Lastly,
burgdorferi genospecies (Kurtenbach et al. 2006). Borrelia burgdor-
public health jurisdictions at risk need the prevention and con-
feri transmission cycles are therefore less affected by changes
trol tools to protect the health of the public in response to
in tick seasonality, and, due to the feeding behaviour of the
emerging and re-emerging vector-borne disease, at which point
tick, considerations of climate effects on the extrinsic incuba-
whether or not the underlying cause is climate change is largely
tion period are mostly irrelevant (reviewed in Ogden, Mechai and
irrelevant.
Margos 2013; Ogden and Lindsay 2016). Furthermore, the tick
vectors and some B. burgdorferi genospecies are readily dispersed Conflicts of interest. None declared.
Ogden 7
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