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Rising temperature and its impact on receptivity to malaria transmission in Europe: A systematic review.

BACKGROUND
Malaria is one of the most life-threatening vector-borne diseases globally. Recent autochthonous cases registered in several European countries have raised awareness regarding the threat of malaria reintroduction to Europe. An increasing number of imported malaria cases today occur due to international travel and migrant flows from malaria-endemic countries. The cumulative factors of the presence of competent vectors, favourable climatic conditions and evidence of increasing temperatures might lead to the re-emergence of malaria in countries where the infection was previously eliminated.


METHODS
We performed a systematic literature review following PRISMA guidelines. We searched for original articles focusing on rising temperature and the receptivity to malaria transmission in Europe. We evaluated the quality of the selected studies using a standardised tool.


RESULTS
The search resulted in 1'999 articles of possible relevance and after screening we included 10 original research papers in the quantitative analysis for the systematic review. With further increasing temperatures studies predicted a northward spread of the occurrence of Anopheles mosquitoes and an extension of seasonality, enabling malaria transmission for annual periods up to 6 months in the years 2051-2080. Highest vector stability and receptivity were predicted in Southern and South-Eastern European areas. Anopheles atroparvus, the main potential malaria vector in Europe, might play an important role under changing conditions favouring malaria transmission.


CONCLUSION
The receptivity of Europe for malaria transmission will increase as a result of rising temperature unless socioeconomic factors remain favourable and appropriate public health measures are implemented. Our systematic review serves as an evidence base for future preventive measures.


Introduction
Malaria is one of the most life-threatening vector-borne diseases and is affecting nearly half of the people worldwide [1]. Malaria is caused by Plasmodia parasites that are spread to humans through the bites of infected female Anopheles mosquitos. Five parasite species cause malaria in humans whereas P. falciparum and P. vivax pose the highest thread. Anopheles are mainly found in tropical and subtropical areas of the world. In 2018 some 228 million cases of malaria were estimated, mainly in sub-Saharan Africa with about 405 0 000 deaths, mostly in children under 5 years of age [2]. In Europe, malaria was endemic until its elimination in the 1970s, with Macedonia being the last endemic area in 1974 [3]. Many factors led to the decline of malaria, including land use and agricultural change, socioeconomic improvements and intervention efforts [4]. However, recent autochthonous cases registered in several European countries have raised awareness regarding the threat of malaria reintroduction to Europe. An increasing number of imported malaria cases are now registered due to international travel and migrant flows from malaria-endemic countries [5,6]. Together with the presence of competent vectors, favourable climatic conditions and evidence of a changing climate this may lead to the re-emergence of malaria in countries where this disease was previously eliminated. Locally transmitted cases have been reported in Germany [7], the Netherlands [8], Spain [9], France [10], Italy [11], Greece [12], and the UK [13]. The dominant Anopheles vector species in Europe are currently An. Atroparvus, An. Labranchiae, An. Messeae, An. Sacharovi, An. Sergentii, and An. Superpictus [14]. The main cause for autochthonous malaria in Europe is the human parasite P. vivax with P. falciparum occurring only sporadically [15].
The risk of malaria spreading depends on the receptivity and vulnerability in a given area. The WHO defines receptivity as a degree to which an ecosystem in a given area at a given time allows for the transmission of Plasmodium spp. From a human to another human through a vector mosquito [16]. The concept encompasses the vectorial capacity of the mosquito, susceptibility of the human population to malaria infection and the strength of the health system, including malaria interventions. Receptivity depends on vector susceptibility to particular species of Plasmodium and is influenced by ecological and climatic factors. Vulnerability of an area is defined as the frequency of influx of infected individuals or groups and/or infective Anopheles mosquitoes and is also referred as the "importation risk" [16]. Since local malaria transmission in Europe is only possible after introduction of a Plasmodium infected individual or mosquito, this systematic review refers to receptivity of Europe for malaria transmission only.
Climatic conditions, such as temperature, rainfall patterns and humidity affect the life cycle and survival of parasites and vectors and therefore highly determine the receptivity for transmission of malaria and other vector-borne diseases [4]. This is of special concern since the world's climate is changing. The Intergovernmental Panel on Climate Change (IPCC) defines climate change as long-term change in the state of the climate that can be identified by changes in the mean or the variability of its properties that persists for an extended period, typically decades or longer [17]. Climate change impacts environmental factors including rise in temperature, precipitation, sea level, ocean acidification and extreme weather events (heat weaves, floods, windstorms). This systematic review focuses on the impact of rising temperature due to climate change. The IPCC stated that human activities have already caused approximately 1.0 � C of global warming since pre-industrial period and warming is likely to reach 1.5 � C between 2030 and 2052 if it continues to increase at the current rate [17]. The IPCC special report from 2018 provides multiple lines of evidence that this rapid global warming has major impacts on organisms and ecosystems, as well as on human systems and well-being and further emphasises that the risk for vector-borne diseases, such as malaria, are projected to increase with a high degree of confidence [17]. Global warming can increase vectorial capacity of malaria mosquitos through the reduction of the Plasmodium extrinsic incubation period, the extension of the mosquito breeding period and an increase in adult population density [18,19]. The aim of this systematic review is therefore, to assess the impact of rising temperature on the receptivity to malaria transmission in Europe and to provide an evidence base for the critical appraisal of the current state of knowledge on which health care guidelines and prevention efforts rely.

Literature extraction
The literature searches for this study were conducted following PRISMA guidelines, providing a set of items for reporting in systematic reviews and meta-analyses [20]. We searched for peer-reviewed articles published before October 21, 2019 in the electronic databases Embase, Medline, Cochrane Library and Scopus. Besides, we identified additional articles through other sources (reference list of identified papers, official reports from Ministries of Health and other surveillance reports, institutional reports from their website).
We used the following search terms in title, abstract and keywords (for full search methods see Appendix 1): Associated keywords: 'climate change' or climat* or 'global warming' or seasonality.
The three concepts have been combined through Boolean operator AND to a search set (n ¼ 1 0 999) and animal studies have been removed (n ¼ 274) (Fig. 1). After duplicate removal in total 1 0 040 studies have been screened for eligibility. Articles in English, French and German were reviewed.

Screening, inclusion and exclusion criteria
Eligibility criteria were original articles focused on rising temperature associated with climate change and transmission of malaria. This systematic review was restricted to malaria in Europe. Europe was defined according to the United Nations geoscheme for Europe, created by the United Nations Statistics Division (for countries see Appendix 2) [21].
We used the following inclusion criteria for selecting studies (in order of importance): websites of interest (WHO, ECDC, IPCC). In addition to the articles extracted from the electronic databases, we added 13 articles identified through other sources (Fig. 1). The selected papers were systematically reviewed and thematically analysed. We excluded non-original research such as opinion pieces and viewpoints or articles referring to geographical areas other than Europe. The selected studies were read in more detail by one author (LF), who also hand-searched reference lists to ensure that no relevant articles are missing in this systematic review. An independent selection among the full-text articles assessed for eligibility was made by two authors (LF, PS) that discussed their choices and consequently agreed upon a final selection. Articles were further excluded for one of the following reasons: area other than Europe, other language, other focus, no original research or duplicate. Finally, a total number of 10 articles were included in the findings table of this systematic review. For documenting the research process a study flow diagram as recommended by the PRISMA statement was performed (Fig. 1). To ensure the quality of the included studies an assessment of the relevance and credibility was performed for each study individually, following a questionnaire from the International Society for Pharmacoeconomics and Outcomes Research (ISPOR), Academy of Managed Care Pharmacy (AMCP) and National Pharmaceutical Council (NPC) Good Practice Task Force Report (Table 1) [22].

Data extraction
References were imported from the electronic databases and managed with the bibliographic software Zotero. For data management a summary of key findings of full-text articles retrieved and identified for qualitative synthesis was listed in a customised Microsoft Excel spread sheet. We used a uniform tool to extract data from eligible papers and recorded data on the journal, title, author, year, place, time period, method, vector species, response type, temperature, key findings, and additional comments. From a total of 10 articles that were included in the final selection, 8 used the occurrence of the Anopheles vector and two the malaria infection as marker of risk (Table 1). We summarized the models used as climate models including climate scenarios (Box 1 and 2) and the vector models (Box 3) found in the articles.

Results
We identified 1 0 999 articles in the electronic database searches, added 13 through other sources and after removal of duplicates and animal studies we screened 1 0 040 articles. We found 59 studies on malaria in Europe to access for eligibility and eventually included 10 articles in the final selection as shown in the PRISMA diagram (Fig. 1).

Modelling trends
We found two approaches for predicting the impact of rising temperature on receptivity to malaria transmission that can be distinguished. First, empirical correlative approaches that use statistical models of relationships between Anopheles mosquitoes and/or malaria  distribution and rising temperature. Second, process-based mathematical models that aim to simulate epidemiological processes between environmental conditions and vectorial performance estimated independently of current distributions. From the 10 articles included in the quantitative analysis of this systematic review, five studies used statistical models to conclude their results, four used projecting mathematical models and one used both methods ( Table 1). The six papers that were found using correlative statistical modelling approaches were based on empirically observed data on Anopheles mosquitoes and/or current/historical malaria distribution as well as climate data. Climate data, including temperature, was found to be either satellite-derived (1) or obtained from national weather stations (4). The five identified papers that used predictive mathematical models included historical and current data while allowing to make projections for the future. In our analyses five different climate models were identified and an overview of the models used can be found in Box 1. The models were either general circulation models (GCM) or regional climate models (RCM) and used different climate scenarios to make projections for future malaria transmission in Europe (Box 2). In addition, four different vector models have been identified that have been used as a measure for the risk prediction of possible transmission and spread of malaria. A summary of the identified malaria vector models can be found in Box 3.

Anopheles mosquitos are still present in Europe
All studies included in this systematic review confirmed that Anopheles mosquitoes transmitting Plasmodium vivax are still present in European countries, although in lower densities compared to the preelimination period. An. Atroparvus was found to be the most widely distributed species in Europe (evaluated in 8 studies) that is capable of transmitting P. vivax malaria. Three studies evaluated An. Labranchiae, An. Messeae, An. Sacharovi, and An. Superpictus respectively, two studies An. Sergentii and one study An. Maculipennis, An. Algeriensis, An. Hyrcanus, and An. Melanoon respectively. Studies on environmental suitability for malaria (8 from 10 studies) further concluded that the present environmental conditions would be suitable for Anopheles mosquito development at high densities and the spatial and temporal patterns closely resemble those registered in the past in endemic regions [25,28].
We found two studies that generated risk maps of the competent Anopheles mosquito species currently present in Europe that can be used as a preliminary step towards predicting future scenarios for receptivity to malaria transmission [18,23]. Receptivity depends on vector susceptibility to particular Plasmodium species and was higher in P. vivax than in P. falciparum. The most widely distributed Anopheles vector belong to the Anopheles maculipennis complex that includes several species with different susceptibility to Plasmodium species due to different behavioural pattern and feeding preferences. The most common species, An. Atroparvus, was found to be widely distributed in Northern and Western Europe, Spain, Portugal, Italy, the Balkans, but not in North Scandinavia, the Alpine regions, and North Africa [18,23,[25][26][27][28][29]. An. Messeae was identified as the second most common Anopheles mosquito and its presence has been mapped in Scandinavia and North-Western Europe, including the Baltic States and Russia [18,23]. An. Labranchiae was found to be the third most common species and restricted to Southern Europe, comprising Italy, the coastal regions of the Balkans, Eastern Spain and North Africa [18,23]. An. Sacharovi was present mainly in South-Eastern Europe, from Eastern Spain along the Alps to the Balkans, Turkey and the Black Sea [18,23]. The distribution of An. Superpictus was mapped similar but less extensive than that of An. Sacharovi and ranges from the Alps to the Balkans, Turkey and North Africa [18,23]. Besides that, one study stated that An. Hyrcanus, and not An. Atroparvus, was reported the main potential malaria vector in Southern France in 2005 [30]. Note: Relevance questions refer to the usefulness of the modelling study to inform the particular health care decision and are finally assessed as Sufficient or Insufficient. The credibility is captured with questions in the following seven domains, Validation, Design, Data, Analysis, Reporting, Interpretation, and Conflict of interest and overall credibility of the modelling study and is judged as Sufficient or Insufficient. The questionnaire consists of 15 questions related to the relevance and credibility of a modelling study and each question is answered with Yes/No/Can't Answer.
a Assessed using a questionnaire to assess the relevance and credibility of a modelling study following an International Society for Pharmacoeconomics and Outcomes Research (ISPOR), Academy of Managed Care Pharmacy (AMCP) and National Pharmaceutical Council (NPC) Good Practice Task Force Report [22].

Northward spread of Anopheles mosquitos
Five studies were found assessing the potential transmission of malaria in the future, of which all modelled increased Anopheles abundance for large parts of Europe under rising temperatures. However, distinct changes in the distribution of the dominant European malaria vectors were predicted. In general, we found that rising temperatures are expected to lead to a northward spread of Anopheles vector occurrence [23]. Most noticeable is the projected spread of An. Atroparvus and An. Messeae to the North until the end of the 21st century. Concurrently, An. Messeae is predicted to decline over the Western parts of Europe. An. Labranchiae, An. Sacharovi and An. Superpictus have been found to be expected to extend northwards, but with a lower probability of occurrence [23]. In contrast, we found that for some Mediterranean areas occurrence probabilities may decline. Most pronounced seems to be the reduction of An. Superpictus, An. Sacharovi and An. Sergentii over the Eastern Mediterranean area and North Africa under future climate conditions. Hertig assumed that these distribution changes are related to the general temperature increase and the strong temperature increase over North-Eastern Europe and the Mediterranean area in spring and autumn, but also to the predicted reduction in precipitation [23]. Moreover, we found a geographically northward decline in malaria transmission stability towards Scandinavia in the predictive modelling studies. The authors stated that the duration of the extrinsic incubation period in the mosquito could also in the future, be still temperature-limited over Northern Europe [23,25]. In addition, we found that the future risk of locally transmitted malaria is considered limited due to low biting rates and the low probability of vectors feeding on a malaria-infected person, as stated in a study on the UK by Lindsay et al. [25].

Lengthening of possible transmission season
The results of our systematic review also show a lengthening of the possible malaria transmission season, which was investigated in four studies. We found one study that has already observed an expansion of the potential malaria transmission window in Spain in 2005, based on data corresponding to a 26-year-period [27]. The authors noted that the favourable transmission period was longer and started two months earlier, in May, and lasting until September in the case of P. falciparum and until October in case of P. vivax, respectively. In addition, we found three predictive modelling studies that suggest an extension of the potential malaria transmission season for regions other than Southern Europe and the Mediterranean area. Changes in the length of Anopheles larva season were expected for Central and Eastern Europe and the North Balkan region [24,29]. Based on the REMO climate model, Tr� ajer and Hammer predicted that the season for An. Maculipennis larvae will increase by one or two months between 2041 and 2070, with April and October showing the most notable changes [24]. We also found an expected prolonged seasonal transmission in An. Atroparvus for Germany, enabling malaria transmissions due to P. vivax up to six months in the period 2051-2080 (REMO, scenario A1B) [26]. Moreover, we identified a widening of the potential malaria transmission window favoured by rising temperature for the UK, where the climate is predicted to be suitable for P. vivax malaria transmission for three to four months by 2030 [25].

Expected risk areas in Europe
In general, all predictive models showed that the areas of potential malaria transmission are increasing where rising temperature favours Anopheles occurrence and also significantly impacts the vectorial capacity. As a result, highest malaria transmission stability was found to be projected for Southern and South-Eastern European areas. The authors stated that a rise in global mean temperature by 2100 of about 4.8 � C compared with pre-industrial levels (RCP8.5 scenario) is predicted to lead to an increased vector stability especially in South and South-Eastern Europe [23]. An increased risk was predicted for the following areas: Spain, France, Italy, Greece, the Central and Eastern European countries Bulgaria, Romania, Macedonia, Serbia, Croatia, Hungary, Ukraine and Russia [23,24,27,29].
A further finding of our analysis is that socioeconomic factors will most likely play a large role in the determination of malaria risk in Europe [18]. Zhao et al. showed that the elimination of malaria in Europe was already in the past mainly related to socioeconomic improvements and only to a limited extent to climatic changes including temperature [4].

Discussion
In its most recent report, the IPCC stated that global warming of 1.5 � C-2 � C compared to pre-industrial levels is expected to have major impacts on vector-borne diseases such as malaria and that their risk is projected to increase with high confidence including potential shifts in their geographic range [17]. This, together with the fact that its former vectors are still distributed across the continent [14], has led us study the effects of rising temperature on the receptivity to malaria transmission in Europe, in order to assess the risk of malaria re-emergence in

Box 1
Climate models used in the publications selected in this review. countries where the disease was previously eliminated. The articles we identified focused on the vector species historically associated with the distribution of endemic malaria in Europe. They confirmed that several Anopheles species capable of transmitting P. vivax caused malaria are still present in Europe, leading to a phenomenon known as "anophelism without malaria". The current and historically most widespread species An. Atroparvus, An. Labranchiae and An. Sacharovi are among the members of the subgroup An. Maculipennis. Malaria vectors of minor importance comprise other members of the subgroup An. Maculipennis (An. Messeae, An. Maculipennis s.s., An. Melanoon), or refer to An. Algeriensis, An. Claviger, An. Hyrcanus, An. Plumbeus, An. Superpictus, and An. Sergentii. Moreover, An atroparvus was found to be the dominant malaria vector in large parts of Europe not only under past and present but also under future climate conditions [23]. An important role is assigned to this vector with regard to the change in potential transmission stability, based on expected increases in length of the transmission season and the extrinsic incubation period.

Impact on malaria by rising temperature
The distribution of European malaria vectors has already in the past frequently been linked with rising temperatures [18]. It has been speculated that rising temperatures associated with climate change may increase the frequency of the Anopheles mosquitos and its bite rates as well as shorten the extrinsic incubation period of the Plasmodium parasites leading to an increased vectorial capacity [18,19]. Moreover, temperature influences the development and survival rate of the mosquito and also of parasites within the mosquito. For P. vivax a minimum temperature of 14.5-15 � C is required to develop inside the mosquito, while P. falciparum requires 16-19 � C [31,32]. For both Plasmodium parasites the optimal temperature for transmission ranges up to 33 � C. However, a recent modelling study from Mordecai et al. [33] suggests an optimal malaria transmission already at 25 � C (6 � C lower than previous models), which makes many more areas vulnerable to possible transmission, also in Europe. This is consistent with one of our identified studies from Portugal, reporting favoured Anopheles abundance at temperatures between 19 and 25 � C [28].
Our assessment of the impact of rising temperature on the receptivity to malaria transmission in Europe showed that large areas of the continent could support malaria transmission today and could extend in the future. In general, potential malaria transmission in Europe is highly seasonal due to temperate climate conditions. Temperature suitability is usually much higher in Southern than in Northern European areas, where the vector development is probably constrained by lower temperatures in winter [18]. Southern Europe and the Mediterranean area, with mild and wet winters and hot and dry summers, was and still is suitable for malaria transmission. Also in the future under the RCP8.5 scenario, projecting a rise in global mean temperature by 2100 of about 4.8 � C compared with the pre-industrial state, large parts of Southern and South-Eastern European areas emerge as regions of high transmission stability [23]. This finding is consistent with previous studies that investigated the impact of climate change on potentially emerging vector-borne diseases in Europe [34,35]. However, extreme temperatures in summer especially in Southern countries may also constrain Anopheles development [28]. A transmission risk currently exists, lasting from May until September (P. falciparum) or October (P. vivax) and an extension of this season is expected in the future [24][25][26][27]. Therefore, if the climate becomes warmer, conditions for malaria transmission in Europe become more favourable and last for longer. Moreover, we found a general northward spread of the Anopheles mosquito occurrence in our analyses, which was already modelled in previous global modelling studies [23]. An assessment of possible future changes of malaria transmission using general circulation models (GCM) and different malaria impact models also showed that until the 2080s a northward shift of the malaria epidemic belt over Central and Northern Europe could occur [15].

Other driving forces
Despite the substantial number of imported malaria cases from travellers and migrant flows from endemic areas that could contribute to an increased infectious parasite reservoir and the documented presence  of Anopheles mosquitos [36][37][38], autochthonous malaria transmission has only rarely been observed in Europe since its elimination in the 1970s [13]. Recent studies have further stated that malaria transmission caused by imported infectious mosquitoes or travellers with parasitaemia does not occur on a large scale, even at Central European airports, and it is unlikely that such transmission could be sustained by native Anopheles mosquitoes [39]. The present situation of "anophelism without malaria" indicates that current socioeconomic and environmental conditions maintain the basic reproduction number (R 0 ) below 1, indicating no spreading of the disease [18]. It should be noted that a temperature increase does not necessarily mean a transmission risk increase if accompanied by a precipitation decrease. The role of precipitation in promoting malaria transmission is mainly through the availability of larval breeding sites [31]. Also in our analysis we found a decrease of malaria transmission stability to the South that was mainly related to the projected rainfall reductions and the resulting decline of vector occurrences due to the drought-induced inhibition of the aquatic life-cycle of the mosquitos [23]. Moreover, we found that changes in land use practices and draining of marshlands for cropping resulted in fewer mosquito breeding sites in the past [4,18], which is consistent with other studies [40][41][42]. Nevertheless, this limitation can, for example, be offset by artificial irrigation of agricultural landscapes as also reported in our identified studies [18,24,27,30]. Hence, areas with high Anopheles vector abundance tend to be related with ecosystems where irrigated agriculture periods coincide with the optimal temperature interval, generally spring and summer [27,28,30].
Furthermore, several authors have reported already in the past that socioeconomic changes such as the increase in Gross Domestic Product (GDP), life expectancy and urbanization were significantly correlated with the decline and elimination of malaria in Europe [4]. Rising temperature associated with climate change is only one component in a complex epidemiologic setting and other aspects such as human activities are therefore probably more important for the determination of malaria spreading as reported previously [43,44].

Future implications
With our systematic review we could determine the receptivity and identify risk areas of potential future malaria disease spreading for Europe due to rising temperature under climate change. Although the potential of malaria spreading is currently considered limited for Europe, mainly owning to socioeconomic conditions, strengthening of disease awareness and maintaining of robust public health care infrastructures for surveillance and vector control are of great importance, especially in the most vulnerable areas such as Southern Europe and the Mediterranean area. Monitoring drivers of malaria and other infectious diseases, such as changes in environmental and climatic conditions, can help predict the threat of malaria re-emergence, as shown in a recent study from Semenza et al. [40] on prototype early warning systems for vector-borne diseases in Europe. Targeted epidemiological surveillance, vector control activities and awareness raising among the general population and health care professionals, in particular in the areas projected environmentally suitable for malaria transmission as also recommended by the WHO [45]. Interestingly, these areas are often those that once supported malaria in the past [25,28]. Adapting existing surveillance practices in Europe will improve preparedness and facilitate public health responses to potentially emerging infectious diseases, including malaria, thereby helping to contain human and economic costs [46].

Strengths and limitations
A strength of our systematic review is the wide range of screened databases and Public Health agency documentation (WHO, ECDC, IPCC) as well as the adherence to the PRISMA guidelines and the quality

Box 3
Vector models used in the publications selected in this review.

Name (Abbreviation) Vector Model
Vector Stability Index (VSI): Global index representing the potential malaria transmission stability. The spatial index includes the most important intrinsic properties of Anopheles mosquitos that interact with climate to determine the vectorial capacity [23]. VSI ¼ P 12 m¼1 a 2 i;m p E i;m = À lnðpi;mÞ m month i vector (Anopheles species) a human-biting proportion p daily survival rate E length of extrinsic incubation period in days Relative monthly larvae abundance value (A rm ): Measure for mosquito larva season [24].
Arm ¼ Nm Na � 100 N m number of the total collected larvae according to a given month N a total number of the collected larvae representing the entire period Basic Reproduction Rate (R 0 ): R0 ¼ ma 2 bp n ÀlnðpÞr Measure used for the risk prognosis of malaria disease spreading [25,26]: if R 0 � 1 risk of a malaria spread if R 0 < 1 no risk of a malaria spread m relative frequency of mosquito a number of blood meals per human and day b ratio of mosquitos in which parasites can develop after ingestion of infected blood p daily survival probability of adult mosquitoes n duration (days) of parasite development in adult mosquitoes r recovery rate of malaria-infected people Gradient Model Risk Index (GMR index): Measure applied to forecast the malaria transmission risk, e.g. along the year. if GMR �116 transmission risk exists (116 is the value required for the development of one Plasmodium generation) [27] GDD growing degree-days R rainfall PET potential evapotranspiration L. Fischer et al. assessment of the included studies. One possible limitation is that we have only included the aspect of temperature as a climate driver, although precipitation patterns and humidity also impact the life cycle of parasites and vectors. Moreover, most studies were based on mathematical models whose quality highly depends on the parameters used. A selection bias may be our inclusion of articles in English, French or German languages only.

Conclusion
Although malaria was officially eliminated in Europe in the 1970s, its former vectors are still distributed across the continent, leading to a phenomenon known as "anophelism without malaria". The current and future climate in large parts of Europe, in particular Southern and South-Eastern Europe, is predicted to be favourable for the receptivity to malaria transmission. As a result of rising temperature, the geographic occurrence of the Anopheles mosquito is expected to spread northwards and the possible season of malaria transmission to be extended. The risk of malaria transmission will therefore increase unless socioeconomic factors remain favourable and appropriate public health and anti-vector measures are implemented and maintained. Our systematic review assessed the impact of rising temperature on the receptivity of Europe for malaria transmission and provided a critical appraisal of transmission predictions. It will serve as an evidence base for future preventive measures.