|
|
Interdiscip Perspect Infect Dis. 2009; 2009: 385487. Published online 2009 January 4. doi: 10.1155/2009/385487. | PMCID: PMC2648659 |
Climate Change and Malaria in Canada: A Systems Approach L. Berrang-Ford,1* J. D. MacLean,2 Theresa W. Gyorkos,2, 3, 4 J. D. Ford,1 and N. H. Ogden5 1Department of Geography, McGill University, 805 Sherbrooke Street West, Montreal, QC, Canada H3A 2K6 2McGill University Centre for Tropical Diseases, Montreal General Hospital, Department of Medicine, McGill University, Montreal, QC, Canada H3G 1A4 3Division of Clinical Epidemiology, McGill University Health Centre, Royal Victoria Hospital, V Building, 687 Pine Avenue West, Montreal, QC, Canada H3A 1A1 4Department of Epidemiology, Biostatistics and Occupational Health, McGill University, Montreal, QC, Canada H3A 1A2 5Public Health Agency of Canada and Faculté de médecine vétérinaire, Université de Montréal, CP 5000, Saint Hyacinthe, QC, Canada J2S 7C6 Received January 9, 2008; Accepted March 27, 2008. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. This article examines the potential for changes in imported and autochthonous malaria incidence in Canada as a consequence of climate change. Drawing on a systems framework, we qualitatively characterize and assess the potential direct and indirect impact of climate change on malaria in Canada within the context of other concurrent ecological and social trends. Competent malaria vectors currently exist in southern Canada, including within this range several major urban centres, and conditions here have historically supported endemic malaria transmission. Climate change will increase the occurrence of temperature conditions suitable for malaria transmission in Canada, which, combined with trends in international travel, immigration, drug resistance, and inexperience in both clinical and laboratory diagnosis, may increase malaria incidence in Canada and permit sporadic autochthonous cases. This conclusion challenges the general assumption of negligible malaria risk in Canada with climate change. Canada's climate could support, and has
supported, local malaria transmission in the past. Malaria was introduced to
continental North America in the 16th and 17th
centuries by European colonists and African slaves [ 1]. The disease spread
with settlement until being controlled in the early 1900s and eradicated in the
1950s [ 1]. Extensive debate and research has focused on the potential for
climate change to alter or increase malaria distributions and incidence both
globally and regionally. Global models and research discourse focuses—justifiably—on the impact of climate change on the spread
and magnitude of global endemic malaria in at-risk regions and regions at the
margins of current endemic distributions. Changes in malaria incidence in Canada and similar northern countries are assumed to be negligible. In this paper we
challenge this assumption. The 4th assessment report (FAR)
of the Intergovernmental Panel on Climate Change (IPCC) highlights, with increased confidence, the
projected impact of climatic change on infectious
diseases and human health [ 2]. These projections are
supported by a growing body of literature which has contributed to the
characterization and quantification of climate as a determinant of disease
distributions and incidence [ 3– 10]. The assessment of climate
impacts on infectious diseases, however, is challenged by often complex
interactions of climatic determinants with other ecological, economic, and
social determinants of disease incidence [ 5, 6, 9, 10]. This has led to efforts to
quantify the disease burden that is specifically attributable to climate change
[ 4, 8], but disentangling the causal
contribution of anthropogenic climate change from complex disease systems poses
both analytical and conceptual difficulties. Analytically, it is often
difficult to characterize and quantify causes of disease variation in time and
space, and to quantify these while controlling for variation in nonclimatic
determinants. Furthermore, both the direct and indirect effects of climate
change are likely to impact vector-borne disease occurrence; for example,
extreme weather events (or indeed long-term changes in climate) may result in
population migration and subsequent changes in population health and exposure. Increasing sophistication in transmission
and systems modeling, however, has provided innovative approaches to confront
this challenge [ 5, 7, 9]. The IPCC FAR, for example, does itself
integrate social and ecological determinants of disease [ 3]. Within the climate change and
health literature, there have been parallel developments in the application and
development of systems frameworks for assessing environmental change impacts on
infectious disease [ 6, 10– 13]. These approaches arise from a range of
(inter)disciplinary and pedagogical roots, including environmental health,
social epidemiology, environmental change, and systems theory [ 13]; the emergence of conceptual systems
frameworks has included eco-epidemiology [ 14], ecohealth [ 15, 16], social epidemiology [ 17], and vulnerability science [ 18, 19]. Ecosystem health approaches, for
example, have been widely used to provide new and integrative frameworks for
conceptualizing, understanding, and characterizing complex dynamics within
health systems [ 6, 20– 23]. These approaches draw on general and
complex systems theory [ 24– 27] to conceptualize health problems as
highly integrative systems affected by interacting processes of social and
ecological complexity. The theoretical basis of these approaches is that
understanding complex systems can only be achieved by looking at how different
parts of a system interact together rather than from teasing them apart [ 28]. Climate change, in this context, is one
of several determinants of infectious disease occurrence, whose impact is
superimposed upon, and moderated by, parallel changes in nonclimatic
determinants. The utility of these frameworks is thus not necessarily in
isolating the attributable burden of disease due to climate change, but rather
in explicitly characterizing the cumulative or integrative impact of climate
change within the context of changes in other disease determinants. Such
frameworks are particularly useful for preliminary characterization and
identification of key processes, interactions, scales, and feedbacks—an exercise which can inform and guide
integrative attribution modeling [ 12, 13, 20]. In this paper, we use a
systems approach to begin to assess how climate change, by having multiple
proximal and distal influences on determinants of transmission, might affect
the occurrence of malaria in Canada.
It has been generally concluded that there is negligible risk of malaria in Canada and similar northern countries due to climate change [ 27– 29]. This assessment
has largely been based on the assumption that the importance of malaria in
these countries rests solely on the likelihood of endemic malaria becoming
established. In this paper, we challenge this assumption, drawing on four key
premises. (1) Absence of risk of endemic malaria does not preclude the
potential for changes in incidence due to imported or sporadic autochthonous (i.e., locally acquired) malaria. (2) Even small changes in
malarial incidence or emergence of autochthonous cases in Canada and other nonendemic
countries could have important implications for public health systems. (3)
Current models of climate impacts on malaria are not designed to effectively or
accurately evaluate the potential for changing malaria incidence in peripheral
regions and should not be interpreted as such. (4) Systems approaches provide a
useful framework for conceptually and methodologically integrating social and
biophysical determinants of disease. We begin the paper by describing
the methods used in the study, before reviewing the nature of malaria incidence
in Canada.
We then assess how climate-malaria links have been approached in the literature
in general and argue that assumptions of limited risk in Canada are not supported by
existing climate-malaria research, and merit re-examination in the context of
sporadic incidence and the role of nonclimatic determinants. The paper then
explores how climate change might affect malaria incidence in Canada based on an understanding of
the malaria transmission cycle and its climatic determinants. Using a systems
approach, we assess how nonclimatic determinants of malaria risk may exacerbate
or moderate climate-related changes in malaria incidence. The characterization
presented here represents a preliminary qualitative review and synthesis of existing knowledge and literature and
should therefore be considered descriptive and exploratory. A summary of common
themes and considerations used in systems frameworks was developed to guide
this review ( Table 1). A systems graphic was developed by adapting the malaria
life cycle model to identify and include both proximal and distal transmission determinants.
Key parameters were reviewed and assessed with respect to trends, interactions,
and potential impact on transmission. We performed an integrative review and
analysis of existing literature and data related to malaria transmission and
dynamics, Canadian malariology research, climate change science, projections
for Canadian climate, demographic trends, international travel, and current
models and research related to both global and regional impacts of climate
change on malaria transmission. | Table 1Common factors in systems approaches to environment and health. |
Canadian malaria data were
acquired from the Public Health Agency of Canada Notifiable Diseases registry [ 29]. Distributions of mosquito vectors were
reviewed to identify competent vectors with distributions in Canada and with the highest vector
potential for parasite transmission [ 1, 30– 37]. Existing records of autochthonous
malaria cases were reviewed, recorded, and combined to map autochthonous
malaria in Canada and the United States (1957–2003) [ 1, 38– 45]. These cases were overlaid with key
vector distributions using ArcMap (ArcInfo 9.2, Environmental
Systems Research Institute, Redlands, Calif,
USA). Temperature data were compared
to parasite development thresholds and dynamics using three sources of data: effects
of temperature on the sporogonic cycle of Plasmodium spp. in mosquitoes, Canadian climate data, and downscaled climate change
projections. The effects of temperature on the duration of development of the
parasites in the mosquito were as follows: P.
vivax requires approximately 30 days at 18°C or 20 days at 20°C, while P. falciparum requires approximately 30
days at 20°C. Above 33°C or below 16/18°C (for P. vivax and P. falciparum,
resp.), the cycle cannot be completed and transmission cannot occur [ 1, 46]. Data on the maximum number of consecutive days >18°C in Toronto (1970–2006) were
calculated using archived Environment Canada climate data [ 46]. Data from Toronto were selected since Toronto is the largest Canadian city within the distributional range of a competent
malaria vector. Downscaled climate change projection data were used to
characterize projected temperature changes on transmission potential. The
climate change projections were obtained from interpolation (for Chatham,
Ontario) of output from the CGCM2 (Canadian Coupled Global Climate Model 2) [ 47] that incorporated estimated forcing
calculated in emission scenario forcing “A2” [ 48]. The output was downscaled using LARS-WG
stochastic weather generator. LARS-WG was calibrated with 30 years of daily
weather observations at Chatham (and its predecessors) obtained from the
Environment Canada database. Chatham was
selected because it is the location closest to Toronto for which we already have downscaled
projections. The data and methodology used here are described in detail by Ogden
et al. [ 49]. 3. Malaria in Canada and USA As recently as the 1820–30s, Canada experienced malaria epidemics, including
severe outbreaks during construction of the Rideau Canal in eastern Ontario, and outbreaks in Montreal and the prairies [ 50]. Records
suggest endemic malaria occurred in the mid to late 1800s on the shores of Lake Ontario from Kingston to Hamilton,
along the northern shore of Lake Erie, along the whole St. Lawrence River and its
tributaries, in parts of the western provinces, and sporadically in Quebec City and Halifax
[ 36]. Incidence declined steadily in the early 1900s, and its eradication is
attributed to increased urbanization and improved socioeconomic conditions
which decreased mosquito populations, decreased human contact with mosquitoes,
and improved the speed and effectiveness of case treatment [ 36, 51]. While
current socioeconomic conditions have dramatically reduced the risk of local
malaria transmission, historical incidence supports the potential for
autochthonous malaria in Canada under conditions favouring transmission. For this reason, we evaluate the
potential impact of shifts in the climatic and nonclimatic determinants of
malaria on the balance of transmission potential. For malaria transmission to
occur, three key factors need to coincide: competent vectors, a suitable
climate for transmission cycles (i.e., completion of parasite development in
the vector), and infected, infective humans. The first two factors are present
in some locations in Canada,
and travel and immigration could potentially introduce parasites into local
human populations. However, in recent decades these factors have not been
sustained at levels sufficiently high or for periods sufficiently long, for
transmission cycles to be established, even at a local level. This is because (1)
the numbers of infected and infective humans have been too low (due to high
standards of living and ready access to medical services and antimalarial
chemotherapy) and (2) vector abundance and rates at which mosquitoes could bite
humans have not been sufficiently high (due to a combination of climate, water
management, housing conditions, and mosquito control). Thus, while malaria
transmission occurred in Canada in the 19th century and the requirements for transmission of malaria theoretically
exist in Canada,
transmission potential since 1900 has been too low to permit local transmission
[ 36, 52– 54]. Changes in these and other factors,
directly or indirectly associated with climate change, however, have the
potential to affect this balance. An average of over 500
travel-related cases are reported annually in Canada (1989–2004, ; [ 29, 55]). This number, which likely represents
fewer than half of actual cases [ 55], is comparable to the incidence of West
Nile Virus in Canada in most years (annual average of 459 clinical cases up to
2006 [ 56])—a disease which has generated widespread media
and public health attention in Canada. While the United States records far more
cases ( >1000/year [ 57]), reported malaria incidence per capita
in Canada is at least three times higher than its southern neighbour; the
reasons for this difference remain unclear [ 55, 58]. Nearly, all malaria cases in North
America are imported cases brought into the country by people who have become
infected while visiting, or after arriving from, an endemic country [ 59]. Travel and immigration were also
associated with two of Canada's
most significant recent outbreaks. The first, in 1995–97, involved
Canadians traveling to the Indian Punjab region, which was experiencing a P. vivax outbreak at that time [ 59]. The second involved an outbreak in
Quebec in 2001-2002 in a
population of central and east African refugees recently arrived in Canada from
Tanzanian refugee camps [ 58– 60]. While there are few malaria deaths in
Canada each year, all malaria cases raise significant community and public
health concern [ 55]. While most cases of malaria in
the United States are imported, there have been a number of cases of autocthonous malaria, whereby
people with no history of travel to endemic areas have become infected by
locally infected mosquitoes. Between 1957 and 2003,
there were 156 cases of locally transmitted malaria in US [ 40]. These cases have not been
confined to the southern United States (); locally-transmitted cases,
for example, have been reported in Virginia, New York, and Michigan [ 1, 40]. Locally acquired outbreaks are often
reported near urban centres or airports, where large influxes of travelers and
immigrants are found [ 40]. Increased air travel, increasing drug
resistance, and changing environmental conditions have raised concern over
malaria re-emergence in the United States [ 1]. In Canada, one case of suspected locally-acquired
autochthonous malaria was reported in a Toronto woman in 1997 [ 38, 61] (). An unexplained death due
to falciparum malaria was also
recorded in Quebec in 1974, raising questions of local transmission, although this is unlikely
give that local climate conditions at that time could not have supported
transmission [ 61, 62]. In Canada, there are six species of Anopheles mosquito, of which only two
are potentially important vectors of malaria ( Table 2). An. quadrimaculatus, found in southern Ontario and Quebec, and An. freeborni which occurs in south-western British Columbia (BC) (, Table 2) are considered to be the
most important vectors for potential autochthonous transmission in the northern
United States, and by
extension, Canada [ 1, 30, 32– 34]. Although the regions where these two
mosquito species occur represent only a small proportion of Canada's territory,
they are located in areas where at least half of Canada's population reside and
where the majority of population growth in Canada is occurring [ 62] (Figures -). The
potential population at risk could increase with even small expansions in the
geographic ranges of the vectors themselves, and of the areas climatically
suitable for parasite transmission. Increased mosquito abundance, duration of
seasonal survival, and parasite replication within
existing distribution ranges, however, would likely affect population risk
more than range expansion. There is little information on local or urban
mosquito abundance and biting within these ranges; existing mosquito
distribution data for Canada () are based on rough estimates dating
to the 1970s, with much of the available data more than several decades old [ 30, 31, 35, 37]. Current, updated, and detailed
distributions of competent malaria vectors in Canada remain unknown. | Table 2
Anopheles species of Canada and their potential competence as malarial vectors. |
4. Climate Change and Global Malaria Climatic factors are important
determinants of malaria transmission. The parasite can only be transmitted from
a mosquito to a human once it has completed a complex cycle of development and
multiplication inside the mosquito, called the sporogonic cycle [ 1]. The length of this cycle (often called
the extrinsic incubation period) depends on the parasite species and ambient
temperature [ 1]. Therefore, for mosquitoes to transmit
infection from an infected human to an uninfected human, ambient temperatures
must be sufficiently high, for a sufficiently prolonged period, (1) for mosquitoes
to acquire infection by biting an infected human, (2) for parasites to develop
in the mosquito, and then, (3) for the mosquito to bite another human and
transmit the parasites. The lifespan of the mosquito is related, among other
factors, to air temperature, humidity, and rainfall, which also affect mosquito
abundance and the rate at which mosquitoes bite humans [ 1, 50, 51, 63]. Climate has, therefore, multiple effects
on malaria transmission. Malaria periodicity and
outbreaks have long been recognized to be associated with climate and climate
fluctuations, particularly, on the fringes of global malaria distribution [ 64– 67]. Global malaria outbreaks have been regularly
linked, for example, to heavy rains associated with El-Nino events [ 64– 66]. In the United States, hotter and more
humid weather conditions were a common factor in local outbreaks of malaria,
including a case at a Michigan campsite in 1995 [ 1, 68]. These warmer, wetter conditions can
increase the survival of the mosquito and reduce the required length of the
sporogonic cycle sufficiently to allow the parasite to develop and the mosquito
to become infectious where it otherwise would not. Similar localized outbreaks
in nonendemic northern countries have also been associated with particularly
warm weather [ 69]. Predictions of global climate change
[ 70] have lead to extensive research interest
into its potential impact on malaria incidence [ 32, 71– 79], but how climate change may affect the
incidence and distribution of malaria is much debated [ 80– 82]. Differing opinions generally arise from
differing conceptual and methodological approaches to malaria modeling. Some
research in this area has predicted significant global or regional spread based
on biological models that incorporate some climate-driven variables that
directly affect the basic reproductive number of malaria ( R0) (particularly
parasite replication in the vector); these reflect predictions of extensions in
transmission season and geographic range, where there may be a potential for transmission cycles to occur [ 83, 84]. These models, which focus on transmission potential, can, however, over-predict both
the impact of climate and current disease distributions. More conservative
projections based on statistical approaches, such as that by Rogers and
Randolph [ 85] have suggested negligible change in
global malaria distributions. These are based on current global distributions and statistical estimates of existing
incidence risk. It is difficult to explicitly incorporate nonclimatic factors
such as health care, local habitat, and vector control into global malaria
models; these determinants are therefore generally absent from global
projections, though efforts have been made to integrate and reflect
socioeconomic vulnerability and adaptive capacity into global scenarios in a
general sense [ 9]. Rogers and Randolph, for example,
acknowledge this challenge conceding that the model predictions are less
reliable in marginal areas, where mosquito life-spans barely exceed incubation
periods for the parasite, and acknowledging that nonclimatic factors are
particularly important in determining the balance of transmission in these
areas. Van Lieshout et al. [ 9] note that more accurate integration of socioeconomic
variables in malaria modeling will require research at regional and national
scales. Research has been
conducted on the potential for climate impacts on malaria in northern
countries, particularly, the UK.
Kuhn et al. [ 86], in an analysis of the risk
of malaria re-emergence in Britain, concluded that despite an increase in the
transmission potential due to climate change, the importance of nonclimatic
factors (including medical systems, socioeconomic conditions, and agricultural
changes) are likely to prevent emergence of endemicity. This example raises a
second important point: the focus of climate-malaria models
and assessments on distributions and spread of endemic malaria. While this is certainly justified in the
prioritization of global health priorities and infectious disease burden, it
does not negate the potential for climate impacts on sporadic autochthonous or
imported cases in marginal or peripheral regions. Given the importance of
nonclimatic factors on malaria transmission in marginal regions such as Canada,
and using an assumption that nonendemic malaria incidence is of research and
public health relevance, global climate-malaria models cannot be used to infer
risk in such regions. That is to say that while existing models are rigorously
developed and valuable to global climate-malaria projections, these models are
not designed to predict changing risk in nonendemic areas, where climatic
conditions for transmission are marginal. 5. Climate Change and Malaria in Canada In the case of Canada and other developed regions on the periphery of the climatic range of malaria
transmission, nonclimatic and local factors are important determinants
affecting the balance of transmission potential. For these regions, with our
current information, it is difficult to quantify whether increased climatic
suitability would be sufficient to push the probability of malaria transmission
beyond the threshold at which current localized and social factors become
insufficient to inhibit transmission. Given Canada's northern climate and
well-established social, health and economic systems, Canada is at negligible
risk of experiencing endemic or regular malaria transmission despite the
presence of competent Anopheles vectors
[ 32, 87]. The questions of climate change impacts
on malaria risk in Canada are not so much whether Canada will become an endemically infected country, but more whether changing climate
determinants will have an impact on current incidence, and whether we can
expect to see cases of locally-acquired autochthonous transmission in Canada.
The answers to these questions require simultaneous evaluation of potential
climatic effects as well as trends in nonclimatic determinants of malaria
transmission. Predictions of shorter winters
and increasing spring and summer temperatures, including prolonged summer heat
waves [ 88, 89], could promote mosquito abundance and
parasite replication in the summer in Quebec, Ontario, and British Columbia.
Conversely, predictions of decreased summer rainfall, particularly in southern
BC where there are already summer rainfall deficits [ 88, 89], could reduce mosquito survival. Southern
Quebec and Ontario already have hot, humid summers with extended periods of high temperatures.
Hotter summers, which are predicted by climate change in this region [ 88, 89], may result in a decrease in the number
of consecutive warm days required for the parasite to develop within the
mosquito and for the mosquito to become infectious. Additionally, milder
winters and spring increases in precipitation in Ontario and Quebec [ 88, 89] may promote early mosquito abundance or
increased winter survival of infective mosquitoes. These represent presumed
potential impacts, though a number of descriptive reviews and qualitative
assessments—particularly related to West Nile Virus—have suggested that climate changes will
affect mosquito abundance and distributions in Canada [ 54, 87, 90– 93], no quantitative models or results have
yet been published to more certainly explore the potential impact of climate
change on Canadian mosquito vectors. In recent decades, there have been several years when Toronto has experienced
more than 30 consecutive days above 18°C (), conditions potentially supporting P. vivax development in the vector.
In 2002 and 2005, there were sufficient warm days to allow for two full
replication cycles. The actual time required for parasite development depends
upon an accumulation of “degree-days,” a count of the cumulative number of days
when temperatures exceed the minimum threshold for development, with each
degree above the threshold contributing to an additional degree-day [ 1, 49, 82]. These days do not necessarily need to be
consecutive; some parasite species can survive temperatures below and above the
minimum threshold and continue development once temperatures rise again [ 35], although these relationships are poorly
understood, particularly in northern latitudes. Projected temperatures for
Chatham in southwestern Ontario [ 47, 49] suggest a doubling of the summer period
capable of supporting parasite development (based on a period of 30 days over
18°C) within the next 50–75 years (). Given that many of these days are well over 18°C and the number of days
required for replication decreases at higher temperatures, these estimates can
be considered conservative. This trend may be generalizable within the southern
Ontario region, and while the degree of warming predicted varies among climate
models and emissions scenarios, all model predictions in the IPCC FAR [ 2] and the Canadian National Impacts
Assessment [ 94] indicate a warming trend in the Canadian
regions where competent malaria vectors currently exist. These projections can be
placed within the context of global malaria modeling. Van Lieshout et al. [ 9], for example, suggest that regions where
the transmission season increases from 0 to 1 or 2 months per year may
experience large increases in population at risk. Canada fits within this range, and
may experience increases of up to 3 months per year (). Van Lieshout
et al. [ 9] also note that this transmission will be
unstable (or sporadic) and that absolute risk remains low. Within the context of
a national public health system such as Canada's, however, even low risk of
emerging sporadic malaria is of importance for public health services and
programming. Changes in the variation and
extremes of rainfall and temperature may be as important as trends in average temperature
conditions for transmission potential. Southern Quebec is projected to experience both increases in average summer rainfall as well as
more frequent and extreme rainfall events. Despite predictions of reduced
summer rainfall in southern Ontario,
summer rain is expected to occur as more frequent extreme rainfall events.
Higher temperatures and drought conditions, followed by heavy rainfall, can
provide ideal conditions for increasing mosquito abundance and reducing
predator populations [ 87]. If combined with sufficiently extended
periods of hot weather to support parasite development, these conditions could
further increase transmission potential. Locally transmitted cases of malaria
in Suffolk, New York, for example, occurred after heavy rainfall during a
particularly hot and dry summer in 1999 [ 95]. This scenario is less likely in southern
British Columbia, where increased rainfall is more likely to occur in the
winter rather than the summer [ 88, 89]. Climate change could be
expected, therefore, to increase the potential for locally transmitted,
autochthonous malaria in Canada.
Climate changes, however, are only one of several determinants of malaria
transmission. Endemic malaria transmission occurred in Canada during the 1800s,
for example, when temperatures were cooler than today [ 96]. It is, however, the combination of changes in multiple transmission determinants of sporadic autochthonous malaria that is
of interest. 6. A Systems Approach to Malaria in Canada Drawing on the
guidelines outlined in Table 1,
we can characterize and assess the role of indirect climate impact and
nonclimatic determinants of transmission, as well as their interactions. Systems
frameworks employ a variety of conceptual tools for system characterization.
Here, we adapt the life cycle model of malaria to include the broader
determinants of transmission (). The basic reproductive number ( R0)
of malaria is determined by the biting rates of mosquitoes, and by infection of
mosquitoes and humans, which are constrained by the life cycle of mosquitoes
and parasites [ 97]. R0 represents the
transmission potential of a disease, that is to say, the number of secondary
cases expected to arise from a primary case in a naïve population [ 97]. Empirical malaria modeling is often
restricted to quantification of these inner parameters and their proximate
determinants. The magnitude of these transmission parameters, however, is
influenced by a range of mediating variables (outer circle), many of which vary
at regional/ local scales or are related to sociopolitical rather than
biological systems. As we illustrate, climatic determinants represent only one
set of variables affecting malaria transmission parameters. Of the variables shown in , incidence and parasitemia in the mosquito population are perhaps the most likely
to experience temporal variation in Canada. Given the low incidence of
malaria and current absence of local transmission in Canada, variations in vector
control, personal protection measures, housing, socioeconomic variables,
differential immunity, and local habitat are unlikely to notably influence transmission.
Delays in diagnosis and treatment of malaria in Canada are already a concern [ 59, 98] and would prolong duration of infection
as well as increase transmission potential under conditions of local
transmission. Climate change may have
indirect effects on Canadian malaria incidence by affecting the nonclimatic
determinants of transmission. For example, any increased incidence of malaria
in countries to or from which Canadians travel would affect the magnitude of
imported cases and the risk of introduction of parasites into Canadian mosquito
populations. This would affect incidence and parasitemia levels in the human
population, as well as transmission efficiency (parameters b and c in ).
Indirect climate change impacts on health vulnerability, socioeconomic status,
reduced resources available for vector control measures or health systems, as
well as trends in population growth, other diseases, overall poverty and
health, and drug use or resistance [ 80– 82, 99], though difficult to quantify, are
potentially significant. Similarly, changes in climate such as warmer and
longer summers could result in behavioural shifts—such as increased or extended seasonal use of
parks and backyard BBQs—that could indirectly affect human-vector
exposure and biting rates. Air-conditioning use in southern Canada, which can
be expected to increase with warmer summer temperatures, may provide a
protective effect, reducing transmission by limiting human exposure to vectors [ 100]. Increasing immigration and
increasing international travel [ 58, 60, 101, 102]—particularly
Canadian immigrants returning to visit friends and relatives in malaria-endemic
countries—may increase
the likelihood of imported cases, as well as the potential for introduction of
parasites into the Canadian mosquito population. The proportion of Canadian
immigrants originating from malarial areas has increased significantly in the
past 50 years [ 103] and more Canadians are traveling more
often to malarial destinations in Africa, Asia, and South America [ 104]. Resulting increases in infected and
infectious individuals in Canada may increase the potential for transmission of
parasites to the local mosquito population as well as potential occurrence of
transfusion-transmitted malaria [ 105]. Canada has, in fact, already
recorded malaria cases that may be associated with climate, immigration, and
international travel. A dramatic increase in imported P. vivax cases in 1995–97 was likely attributable
to Canadians of Indian origin who visited the Punjab region of India during a P. vivax outbreak associated with higher
than normal temperatures and precipitation during a strong El Niño year [ 59, 64, 65, 106– 108]. This example demonstrates the potential
for climate impact outside Canada to affect malaria incidence in Canada.
Increased incidence and parasitemia in the human population is likely to be
most pronounced in urban areas, where travel transit and immigration are the highest. The on-going, and sometimes
rapid, emergence of parasite resistance to antimalarials also has the potential
to affect Canadian malaria incidence. Drug resistance has resulted in the
emergence and re-emergence of malaria around the world, and it considered to be
one of the greatest challenges to global malaria control today [ 109]. Antimalarial resistance can increase the
incidence, severity, and cost of travel-related malaria in Canada by decreasing the efficacy
of traveler prophylaxis, complicating selection of prophylaxis and treatment
regimes, and increasing the potential for treatment failure. A summary of key
trends in the determinants of malaria incidence in Canada is provided in Table 3. | Table 3Trends in the determinants of malaria incidence and transmission in Canada. |
Our characterization and
assessment of the changing climatic and nonclimatic determinants of malaria indicates
that Canada may experience increasing imported incidence as well as the potential for
emergence of sporadic cases of autochthonous malaria. Our analysis provides a qualitative and exploratory assessment
of potential climate impacts within the context of other Canadian disease
determinants and trends. Whether these trends and parameters would be quantitatively sufficient to tip the
balance towards sporadic autochthonous transmission is unknown and requires
further study. While well within
the capacity of Canada's
health system to address, the potential for changes in malaria incidence would
require targeted and strategic shifts in health service programming, physician/technologist education and training, travel agent education and travel clinic
referral, education of the public, and surveillance. Targeted research to quantify the sensitivity of potential
local mosquito transmission to key parameter changes would require the
development of process-based models or equivalent empirical models to simulate
sporadic incidence. This is consistent with global research recommendations identifying
the need for further research on malaria modeling at the regional or national
scales and integrating regional environmental and socioeconomic variation [ 9]. While not quantitatively
sufficient to project incidence increase, the results of this review and
characterization qualitatively support the merit of targeted regional research
to quantify projected transmission potential in Canada. Such an endeavour would be
of importance to public health in Canada, but is also of relevance to
broader questions related to the impact of climate change on infectious disease
occurrence. This review, while regional, highlights the utility of systems
frameworks in characterizing potential health risks not readily identified or
addressed by global models or climate attribution modeling. The authors would like to
thank Dr. Robbin Lindsay (Public Health Agency of Canada) for entomological
advice, and Abdel Maarouf (now retired from the Environment Canada) and Fatima
Ramay for downscaled projected temperatures for southern Ontario. 1. Zucker JR. Changing patterns of autochthonous malaria transmission in the United States: a review of recent outbreaks. Emerging Infectious Diseases. 1996;2(1):37–43. [PubMed] 2. Parry M, Canziani O, Palutikof J, van der Linden P, Hanson C, editors. Climate Change 2007: Impacts, Adaptation and Vulnerability. Cambridge, UK: Cambridge University Press; 2007. (Working Group II Contribution to the Fourth Assessment Report of the
Intergovernmental Panel on Climate Change). 3. McMichael AJ, Campbell-Lendrum DH, Corvalán CF, et al., editors. Climate Change and Human Health: Risks and Responses. Geneva, Switzerland: World Health Organization; 2003. 4. McMichael A, Campbell-Lendrum DH, Kovats RS, et al. Climate change. In: Ezzati M, Lopez A, Rodgers A, Vander Hoorn S, Murray C, editors. Comparative Quantification of Health Risks: Global and Regional Burden of
Disease Due to Selected Major Risk Factors. Geneva, Switzerland: World Health Organization; 2004. pp. 1543–1649. 5. McMichael AJ, Woodruff RE, Hales S. Climate change and human health: present and future risks. The Lancet. 2006;367(9513):859–869. 6. Parkes MW, Bienen L, Breilh J, et al. All hands on deck: transdisciplinary approaches to emerging infectious disease. EcoHealth. 2005;2(4):258–272. 7. Patz JA, Balbus JM. Methods for assessing public health vulnerability to global climate change. Climate Research. 1996;6(2):113–125. 8. Stott PA, Stone DA, Allen MR. Human contribution to the European heatwave of 2003. Nature. 2004;432(7017):610–614. [PubMed] 9. van Lieshout M, Kovats RS, Livermore MTJ, Martens P. Climate change and malaria: analysis of the SRES climate and socio-economic scenarios. Global Environmental Change. 2004;14(1):87–99. 10. Wilcox BA, Colwell RR. Emerging and reemerging infectious diseases: biocomplexity as an interdisciplinary paradigm. EcoHealth. 2005;2(4):244–257. 11. McMichael AJ, Woodruff RE. Detecting the health effects of environmental change: scientific and political challenge. EcoHealth. 2005;2(1):1–3. 12. Vanwambeke SO, Lambin EF, Eichhorn MP, et al. Impact of land-use change on dengue and malaria in northern Thailand. EcoHealth. 2007;4(1):37–51. 13. Eisenberg JN, Desai MA, Levy K, et al. Environmental determinants of infectious disease: a framework for tracking causal links and guiding public health research. Environmental Health Perspectives. 2007;115(8):1216–1223. [PubMed] 14. Susser M, Susser E. Choosing a future for epidemiology—II: from black box to Chinese boxes and eco-epidemiology. American Journal of Public Health. 1996;86(5):674–677. [PubMed] 15. Waltner-Toews D. Ecosystem Sustainability and Health: A Practical Approach. Cambridge, UK: Cambridge University Press; 2004. 16. Waltner-Toews D, Kay J. The evolution of an ecosystem approach: the diamond schematic and an adaptive methodology for ecosystem sustainability and health. Ecology and Society. 2005;10(1):p. 38. 17. Krieger N. Theories for social epidemiology in the 21st century: an ecosocial perspective. International Journal of Epidemiology. 2001;30(4):668–677. [PubMed] 18. Few R. Health and climatic hazards: framing social research on vulnerability, response and adaptation. Global Environmental Change. 2007;17(2):281–295. 19. Turner BL, II, Kasperson RE, Matsone PA, et al. A framework for vulnerability analysis in sustainability science. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(14):8074–8079. [PubMed] 20. Berrang-Ford L, Waltner-Toews D, Charron D, Odiit M, McDermott J, Smit B. Sleeping sickness in southeastern Uganda: a systems approach. EcoHealth. 2005;2(3):183–194. 21. Parkes M, Panelli R, Weinstein P. Converging paradigms for environmental health theory and practice. Environmental Health Perspectives. 2003;111(5):669–675. [PubMed] 22. Waltner-Toews D, Kay JJ, Neudoerffer C, Gitau T. Perspective changes everything: managing ecosystems from the inside out. Frontiers in Ecology and the Environment. 2003;1(1):23–30. 23. Wilcox BA, Gubler DJ. Disease ecology and the global emergence of zoonotic pathogens. Environmental Health and Preventive Medicine. 2005;10(5):263–272. 24. Allen T, Starr T. Hierarchy: Perspectives for Ecological Complexity. Chicago, Ill, USA: University of Chicago Press; 1982. 25. Checkland P, Scholes J. Soft Systems Methodology in Action. Chichester, UK: John Wiley & Sons; 1990. 26. Kay JJ, Regier HA, Boyle M, Francis G. An ecosystem approach for sustainability: addressing the challenge of complexity. Futures. 1999;31(7):721–742. 27. Puccia J, Levins R. Qualitative Modeling of Complex Systems. Cambridge, Mass, USA: Harvard University Press; 1985. 28. Waltner-Toews D, Kay J, Murray TP, Neudoerffer C. Adaptive methodology for ecosystem sustainability and health (AMESH): an introduction. In: Midgley G, Ochoa-Arias A, editors. Community Operational Research: Systems Thinking for Community Development. Boston, Mass, USA: Kluwer Academic Publishers; 2004. 29. Public Health Agency of Canada. National Notifiable Diseases Online: Notifiable disease incidence
by year, 1989–2004. 2006. 30. Darsie R, Ward R. Identification and Geographical Distribution of the Mosquitoes: of North America, North of Mexico. Fresno, Calif, USA: American Mosquito Control Association; 1981. 31. Darsie R, Ward R. Identification and Geographical Distribution of the Mosquitoes: of North America, North of Mexico. Gainesville, Fla, USA: University Press of Florida; 2005. 32. Kiszewski A, Mellinger A, Spielman A, Malaney P, Sachs SE, Sachs J. A global index representing the stability of malaria transmission. American Journal of Tropical Medicine and Hygiene. 2004;70(5):486–498. [PubMed] 33. Levine RS, Peterson AT, Benedict MQ. Distribution of members of Anopheles quadrimaculatus Say s.l. (Diptera: Culicidae) and implications for their roles in malaria transmission in the United States. Journal of Medical Entomology. 2004;41(4):607–613. [PubMed] 34. WHO. World Malaria Report. 2005. 35. Horsefall WR. Mosquitoes: Their Bionomics and Relation to Diseases. New York, NY, USA: Ronald Press; 1955. 36. O'Rourke F. Anopheles and the problem of malaria in Canada. Canadian Entomologist. 1959;91(6):346–358. 37. Wood D, Dang P, Ellis R. The Mosquitoes of Canada. Ottawa, Ont, Canada: Canadian Government Publishing Services; 1979. 38. Baqi M, Gamble K, Keystone JS, Kain KC. Malaria: probably locally acquired in Toronto, Ontario. Canadian Journal of Infectious Diseases and Medical Microbiology. 1998;9(3):183–184. 39. Eliades MJ, Shah S, Nguyen-Dinh P, et al. Malaria surveillance—United States, 2003. Morbidity and Mortality Weekly Report. 2005;54(2):25–40. 40. Filler SJ, MacArthur JR, Parise M, et al. Locally acquired mosquito-transmitted malaria: a guide for investigations in the United States. Morbidity and Mortality Weekly Report. 2006;55(R13):1–9. [PubMed] 41. Holtz TH, Kachur SP, MacArthur JR, et al. Malaria surveillance—United States, 1998. Morbidity and Mortality Weekly Report. 2001;50(5):1–20. [PubMed] 42. MacArthur JR, Levin AR, Mungai M, et al. Malaria surveillance—United States, 1997. Morbidity and Mortality Weekly Report. 2001;50(SS01)(1):25–44. 43. Newman RD, Barber AM, Roberts J, Holtz T, Steketee RW, Parise ME. Malaria surveillance—United States, 1999. Morbidity and Mortality Weekly Report. 2002;51(1):15–28. 44. Shah S, Filler S, Causer LM, et al. Malaria surveillance—United States, 2002. Morbidity and Mortality Weekly Report. 2004;53(1):21–34. 45. Williams HA, Roberts J, Kachur SP, et al. Malaria surveillance—United States, 1995. Morbidity and Mortality Weekly Report. 1999;48(1):1–23. 48. Houghton J, Ding Y, Griggs DJ, et al., editors. Climate Change 2001: the Scientific Basis. Cambridge, UK: Cambridge University Press; 2001. (Working Group I Contribution to the Third Assessment Report of the
Intergovernmental Panel on Climate Change). 49. Ogden NH, Maarouf A, Barker IK, et al. Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada. International Journal for Parasitology. 2006;36(1):63–70. [PubMed] 50. Randolph SE, Rogers DJ. Tick-borne disease systems: mapping geographic and phylogenetic space. Advances in Parasitology. 2006;62:263–291. [PubMed] 51. Reiter P. Global-warming and vector-borne disease in temperate regions and at high altitude. The Lancet. 1998;351(9105):839–840. 52. Fisk G. Malaria and the Anopheles mosquito in Canada. Canadian Medical Association Journal. 1931;25(6):679–683. 53. McLintock J, Iverson J. Mosquitoes and human disease in Canada. Canadian Entomologist. 1975;107:695–704. 54. Charron DF. Potential impacts of global warming and climate change on the epidemiology of zoonotic diseases in Canada. Canadian Journal of Public Health. 2002;93(5):334–335. 55. CATMAT. Canadian recommendations for the prevention and treatment of malaria among international travelers. Canadian Communicable Diseases Report. 2004;30(supplement 1):1–62. 56. PHAC. West Nile Virus MONITOR, Human Surveillance 2002–2006. 2007. 57. Stoppacher R, Adams SP. Malaria deaths in the United States: case report and review of deaths, 1979–1998. Journal of Forensic Sciences. 2003;48(2):404–408. [PubMed] 58. Ndao M, Bandyayera E, Kokoskin E, Gyorkos TW, MacLean JD, Ward BJ. Comparison of blood smear, antigen detection, and nested-PCR methods for screening refugees from regions where malaria is endemic after a malaria outbreak in Québec, Canada. Journal of Clinical Microbiology. 2004;42(6):2694–2700. [PubMed] 59. MacLean JD, Demers A-M, Ndao M, Kokoskin E, Ward BJ, Gyorkos TW. Malaria epidemics and surveillance systems in Canada. Emerging Infectious Diseases. 2004;10(7):1195–1201. [PubMed] 60. Ndao M, Bandyayera E, Kokoskin E, et al. Malaria “epidemic” in Québec: diagnosis and response to imported malaria. Canadian Medical Association Journal. 2005;172(1):46–50. [PubMed] 61. Wilton P. Malaria may be on move to “tropical” Canada. Canadian Medical Association Journal. 1998;158(2):p. 160. 62. Statistics Canada. Census of Canada. 2001. 63. Sherman IW, editor. Malaria: Parasite Biology, Pathogenisis, and Protection. Washington, DC, USA: ASM Press; 1998. 64. Bouma MJ, Van der Kaay HJ. Epidemic malaria in India and the El Niño southern oscillation. The Lancet. 1994;344(8937):1638–1639. 65. Bouma MJ, Sondorp HE, van der Kaay HJ. Climate change and periodic epidemic malaria. The Lancet. 1994;343(8910):p. 1440. 66. Kovats RS, Bouma MJ, Hajat S, Worrall E, Haines A. El Niño and health. The Lancet. 2003;362(9394):1481–1489. 67. MacDonald G. The analysis of malaria epidemics. Tropical Disease Bulletin. 1954;50(10):871–892. 68. Sunstrum J, Elliott LJ, Barat LM, Walker ED, Zucker JR. Probable autochthonous Plasmodium vivax malaria transmission in Michigan: case report and epidemiological investigation. American Journal of Tropical Medicine and Hygiene. 2001;65(6):949–953. [PubMed] 69. IPCC . Summary for policymakers. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE, editors. Climate Change 2007: Impacts, Adaptation and Vulnerability. Cambridge, UK: Cambridge University Press; 2007. pp. 7–22. (Working Group II Contribution to the Fourth Assessment Report of the
Intergovernmental Panel on Climate Change). 70. Mantel CF, Klose C, Scheurer S, Vogel R, Wesirow A-L, Bienzle U. Plasmodium falciparum malaria acquired in Berlin, Germany. The Lancet. 1995;346(8970):320–321. 71. Patz JA, Kovats RS. Hotspots in climate change and human health. British Medical Journal. 2002;325(7372):1094–1098. [PubMed] 72. Kovats RS, Campbell-Lendrum DH, McMichael AJ, Woodward A, Cox JSH. Early effects of climate change: do they include changes in vector-borne disease? Philosophical Transactions of the Royal Society B. 2001;356(1411):1057–1068. 73. Martens WJM, Niessen LW, Rotmans J, Jetten TH, McMichael AJ. Potential impact of global climate change on malaria risk. Environmental Health Perspectives. 1995;103(5):458–464. [PubMed] 74. Martens WJ, Jetten TH, Rotmans J, Niessen LW. Climate change and vector-borne diseases: a global modelling perspective. Global Environmental Change. 1995;5(3):195–209. 75. Martens WJM, Jetten TH, Focks DA. Sensitivity of malaria, schistosomiasis and dengue to global warming. Climatic Change. 1997;35(2):145–156. 76. van Lieshout M, Kovats RS, Livermore MTJ, Martens P. Climate change and malaria: analysis of the SRES climate and socio-economic scenarios. Global Environmental Change. 2004;14(1):87–99. 77. Hay SI, Shanks GD, Stern DI, Snow RW, Randolph SE, Rogers DJ. Climate variability and malaria epidemics in the highlands of East Africa. Trends in Parasitology. 2005;21(2):52–53. [PubMed] 78. Githeko A, Ndegwa W. Predicting malaria epidemics in the Kenyan highlands using climate data: a tool for decision makers. Global Change & Human Health. 2001;2(1):54–63. 79. Martens P, Kovats RS, Nijhof S, et al. Climate change and future populations at risk of malaria. Global Environmental Change. 1999;9:S89–S107. 80. Thomas C. Malaria: a changed climate in Africa? Nature. 2004;427(6976):690–691. [PubMed] 81. Thomas CJ, Davies G, Dunn CE. Mixed picture for changes in stable malaria distribution with future climate in Africa. Trends in Parasitology. 2004;20(5):216–220. [PubMed] 82. Small J, Goetz SJ, Hay SI. Climatic suitability for malaria transmission in Africa, 1911–1995. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(26):15341–15345. [PubMed] 83. Martin PH, Lefebvre MG. Malaria and climate: sensitivity of malaria potential transmission to climate. Ambio. 1995;24(4):200–207. 84. Martens WJM, Niessen LW, Rotmans J, Jetten TH, McMichael AJ. Potential impact of global climate change on malaria risk. Environmental Health Perspectives. 1995;103(5):458–464. [PubMed] 85. Rogers DJ, Randolph SE. The global spread of malaria in a future, warmer world. Science. 2000;289(5485):1763–1766. [PubMed] 86. Kuhn KG, Campbell-Lendrum DH, Armstrong B, Davies CR. Malaria in Britain: past, present, and future. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(17):9997–10001. [PubMed] 87. Charron D, Waltner-Toews D, Maarouf A. Sault Ste. Marie, Ont, Canada: Ministry of Natural Resources, Ontario Forest Research Institute; 2003. A synopsis of known and potential diseases and parasites associated with
climate change. Tech. Rep. 154. 90. Epstein PR. West nile virus and the climate. Journal of Urban Health. 2001;78(2):367–371. [PubMed] 91. Epstein PR. Climate change and emerging infectious diseases. Microbes and Infection. 2001;3(9):747–754. [PubMed] 92. Gosselin P, Lebel G, Rivest S, Douville-Fradet M. The integrated system for public health monitoring fo West Nile virus (ISPHM-WNV): a real-time GIS for surviellance and decision-making. International Journal of Health Geographics. 2005;4, article 21:1–12. [PubMed] 93. Health Canada. Canadian Climate Change and Health Vulnerability Assessment. 2007. Government of Canada: Ottawa, Canada. 94. Lemmen D, Warren F, editors. Climate Change Impacts and Adaptation: A Canadian Perspective. Ottawa, Canada: Natural Resources Canada (NR-CAN); 2007. 95. Bradley CB, Zaki MH, Graham DG, et al. Probable locally acquired mosquito transmitted Plasmodium vivax
infection—Suffolk County, New York, 1999. Morbidity and Mortality Weekly Report. 2000;49(22):495–298. [PubMed] 96. Bradley R. Past global changes and their significance for future. Quarternary Science Reviews. 2000;19(1–5):391–402. 97. Smith DL, McKenzie FE, Snow RW, Hay SI. Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Biology. 2007;5(3):531–542. 98. Kain KC, Harrington MA, Tennyson S, Keystone JS. Imported malaria: prospective analysis of problems in diagnosis and management. Clinical Infectious Diseases. 1998;27(1):142–149. [PubMed] 99. Lindsay SW, Martens WJM. Malaria in the African highlands: past, present and future. Bulletin of the World Health Organization. 1998;76(1):33–45. [PubMed] 100. Schoepke A, Steffen R, Gratz N. Effectiveness of personal protection measures against mosquito bites for malaria prophylaxis in travelers. Journal of Travel Medicine. 1998;5(4):188–192. [PubMed] 101. Martens P, Hall L. Malaria on the move: human population movement and malaria transmission. Emerging Infectious Diseases. 2000;6(2):103–109. [PubMed] 102. Muentener P, Schlagenhauf P, Steffen R. Imported malaria (1985–1995): trends and perspectives. Bulletin of the World Health Organization. 1999;77(7):560–566. [PubMed] 104. Statistics Canada. Tourism Statistical Digest. 2001. Catalogue N. 87-403-XIE. 105. Slinger R, Giulivi A, Bodie-Collins M, et al. Transfusion-transmitted malaria in Canada. Canada Communicable Disease Report. 1999;25(6):53–62. [PubMed] 106. Bouma MJ, Dye C, van der Kaay HJ. Falciparum malaria and climate change in the northwest frontier province of Pakistan. American Journal of Tropical Medicine and Hygiene. 1996;55(2):131–137. [PubMed] 108. de Zulueta J, Mujtaba SM, Shah IH. Malaria control and long-term periodicity of the disease in Pakistan. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1980;74(5):624–632. [PubMed]
|
This article has been 
