Climate Changes and Tick-Borne Diseases in Europe

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This entry is adapted from the peer-reviewed paper 10.3390/ijerph19116516

Ticks, which belong to the phyllum Arthropoda, are blood-skin ectoparasitic vectors, characterized by the variety of pathogens they transmit, by their effect on both human and animal health, and by their worldwide socioeconomic involvement. Climate change has influenced the transmission of a wide range of vector-born diseases in Europe, which is a pressing public health change for the coming decades. Numerous theories have been developed in order to explain how tick-borne diseases are associated with cliamte change. These theories include higher poliferation rates, extended transmission season, changes in ecological balances, and climate-related migration of vectors, reservoir hosts, or human populations.Changes of epidemiological pattern have potentially catastrophic consequences, resulting in increasing prevalence of tick-born diseases.

climate change Europe geographical distribution Ixodes ricinus tick-borne diseases temperature

1. Introduction

Ticks, which belong to the phylum Arthropoda, are blood-sucking ectoparasitic vectors, characterized by the variety of pathogens they transmit, by their effect on both human and animal health, and by their worldwide socioeconomic involvement. They are divided into two large families: Argasidae (soft ticks) and Ixodidae (hard ticks). Hard ticks are the largest and medically most significant group. It is necessary to assess the distribution of tick-borne pathogens and identify possible risk areas because of the increase in tick-borne disease frequency throughout the world. In Europe, the most common and significant tick is Ixodes ricinus (castor bean tick), in terms of its wide ecosystem distribution and the diversity of transmitted pathogens ^[1].

Among the pathogens transmitted by I. ricinus, spirochetes of the Borrelia burgdorferi sensu lato (s.l.) complex, the causative agents of human Lyme borreliosis (LB) disease ^[2] and the Western European TBEV subtype (TBEV-Eur) that causes tick-borne encephalitis (TBE), affect human health to a great degree ^[3].

I. ricinus can also harbor and transmit bacteria of the order Rickettsiales that is important in terms of medical and veterinary concern. Rickettsiae of the spotted fever group (SFG) (R. helvetica, R. monacenis) lead to rickettsioses in humans ^[4], Anaplasma phagocytophilum causes granulocytic anaplasmosis in both humans and animals ^[5], while the emerging pathogen “Candidatus Neoehrlichia mikurensis” may lead to neoehrlichiosis, primarily a disease of immunocompromised patients ^[6]. Additionally, I. ricinus can also harbor and transmit protozoans of the genus Babesia, mainly B. microti and B. divergens, causative agents of babesiosis in humans, while B. venatorum pathogenicity to humans is under investigation ^[7]. The role of I. ricinus in transmission of Bartonella species (e.g., B. henselae and B. quintana), which cause bartonellosis in humans, is discussed controversially ^[8]. The Q fever agent Coxiella burnetii and Francisella tularensis, which are causative agents of tularemia, have also been detected in I. ricinus ^[9].

The ixodid ticks undergo the three-host life cycle, whereby the tick leaves the host after the larval and nymphal stages. Moreover, they stay attached to their hosts for up to several days while feeding ^[10]. The life cycles and transmission of the most infectious agents of ticks are inextricably linked to climate. Climate change has already impacted the transmission of a wide range of vector-borne diseases in Europe ^[11]. In fact, the ozone hole, the greenhouse effect, the heat waves, the extreme weather events, changes in rainfall patterns, and biodiversity reduction affect the spatial spread of vector-borne diseases ^[12]^[13]. Furthermore, climate change indirectly influences the ecosystems by redefining the distribution of the fauna. As a result, global warming is one of the most important factors in redistribution of the ticks’ population and the outbreak of tick-borne diseases ^[14]^[15]. In addition, climate change influences the population ecology of Ixodes ticks via its effects on abiotic factors such as vegetation, drought, and humidity. This is reflected in the earlier vegetation onset and the extension of the growing season during the year, the levels of drought and humidity, as well as the potential access to water, which is vital for arthropod vectors ^[16].

During the last decades, the prevalence of tick-borne diseases has increased in Europe, due to several biotic and abiotic factors ^[17]^[18]. In fact, while in the past tick-borne diseases were endemic only in some specific regions, currently they have been redistributed on an impressively larger geographical scale ^[19]. TBE and LB disease are considered the most climate-sensitive diseases. In fact, a systematic literature review from 1997 to 2017 revealed that the most climate-sensitive diseases are transmitted by arthropods (51% of diseases that are sensitive to climatic factors), in which 41% belong to tick-borne diseases ^[16].

Discovering which abiotic factors have an impact on the biology of ticks, as well as evaluating seasonal patterns of activity resulting from several combinations of climatic conditions, could constitute an estimation of “risk” in a climate change scenario ^[20]. Statistical models are useful in order to predict tick distributions by linking their existence to environmental conditions. Therefore, the use of climate and environmental data can help in making spatial predictions of disease distribution ^[21]^[22].

2. How Climate Affects Tick Phenology—The Example of I. ricinus

I. ricinus is widely distributed across Europe. Its existence has been recorded in countries such as the UK, Germany, Sweden, Ukraine, Russia, Italy, France, Spain, Romania, Belgium, Austria, Latvia, and Lithuania ^[20]^[23]^[24]^[25]^[26]^[27]^[28]^[29]^[30]^[31]^[32]^[33]^[34]. It is also found in Greece and particularly in Northwestern Greece and Crete, according to the current ECDC map distribution for Europe in March 2021 ^[35]^[36].

I. ricinus seasonal population dynamics are influenced by both abiotic (climatic) factors acting on the free-living tick stages and biotic (host) responses to the tick as a parasite ^[37]. Also, interaction between abiotic and biotic factors caused by the indirect effects of climate change on the hosts, influence the abundance and the distribution of the tick ^[38].

Since the I. ricinus species complex spends most of its life (~98%) in the external environment, their prevalence is affected by microclimate changes such as temperature, saturation deficit, humidity, and day length (diapause) ^[37]^[39]. High temperature results in a numerical increase of ticks and the extension of the interaction time between ticks and humans ^[40]^[41]. Combined with temperature, humidity is an important limiting factor in I. ricinus survival and activity. Consequently, relative humidity needs to be above 70–80% in order to allow questing tick behavior and survival ^[42].

Τhe initiation and cessation of questing activity of I. ricinus is strongly correlated to the temperature. I. ricinus, in order to start questing, requires a relative humidity over 45% and a temperature of 7–8 °C ^[43]. Observations made mainly in Central Europe revealed that I. ricinus ticks are inactive during the winter (mid-November to mid-February), while they actively look for hosts from March to October. In autumn, nymphs and adult I. ricinus ticks are more sensitive to a temperature drop, entering behavioral diapause at near-ground temperatures greater than those associated with the onset of questing behavior in the spring period ^[44]. Questing is performed when temperatures exceed 5 °C ^[15]^[44], a theory which has been proved experimentally with the research of Gilbert, Aungier, and Tomkins, 2014, in which ticks of the species I. ricinus proceeded to questing in vitro only if the temperature was higher than 6 °C ^[45].

It is noteworthy, however, that for ticks which were collected from colder climate areas, questing start temperatures were lower than the required temperatures for ticks coming from warmer climate areas. This was also observed for the required temperatures of the tick’s metabolic initiation ^[46]^[47]. The lowest temperatures that permit the metabolic function of I. ricinus are between −5 °C and −10 °C. These temperatures are probably close to the temperatures that permit the tick’s survival ^[48].

Many studies reveal that I. ricinus can adapt to climate changes and integrate to local climate conditions ^[45]. In the publication of Gray et al., 2009, it is stated that the questing period in the UK is approximately 10 months per year because of the milder winter climatic conditions in Western Europe. Temperature increases in colder areas affect the winter activity of ticks, leading to the indication that an increase in the activity of I. ricinus throughout the year is induced by global warming. The rising winter temperatures are considered to be a critical factor for host survival ^[49]. On the other hand, an environment that combines a low rate of summer rainfall with summer drought is probably an inhibitor of the growth of I. ricinus because it weakens its activity ^[39].

Low temperatures have a negative effect on the tick’s lipids and water levels, resulting in a later embryogenesis ^[50]. The way that temperature affects the tick’s metabolism needs to be further investigated in order to clarify the potential tick’s population, their phenology, their seasonal behavior, and the transmission of tick-borne pathogens ^[39]^[51]. The results of Alasmari and Wall, 2021, in their study of the temperature’s impact on the metabolic rate and resource depletion for the tick I. ricinus, showed a low rate of reduction in the nymphs’ proteins, sometimes also in low temperatures ^[48].

Climate change influences the latitudinal and altitudinal distribution of I. ricinus ^[38] (Table 1). In Central Sweden, the increase in the population of species is attributed to warmer winters, since today there are more days with temperatures above 7 °C ^[52]^[53]. This expansion is attributed to climate change that has caused the northern spread of fauna and flora in Sweden over the last 30 years and includes the upward (on latitude) extension of I. ricinus ^[54]. In the past, the highest latitude with a presence of I. ricinus was 61° N ^[53]. Today, I. ricinus is located at latitudes up to 66° N, entirely occupying the Baltic Sea coastline, northern river valleys, and large northern lakes. The reduction of exposure to temperatures below −12 °C for long periods in northern areas is the main parameter that allowed the establishment of ticks. The above is confirmed by the fact that this tick can survive after 24 h exposure in the extreme temperature range of −14.4 °C to −18.9 °C. Instead, an exposure of one month at −10 °C is mostly fatal for the unfed nymphs and for the larvae and nymphs in diapause ^[55]. Moreover, if I. ricinus is not fully developed before the winter, where growth is impossible in the range 7–10 °C, it is impossible for it to survive ^[39].

Furthermore, the increasing prevalence of spring and autumn conditions results in the expansion of the days with temperatures higher than 5–8 °C. In Central and Western Sweden, the duration of tick activity is 6 to 8 months per year, whereas for the British Isles, this period is counted as 11 months per year or the whole year ^[39].

At higher altitudes, without optimal temperature, ticks have less time to search for a host. Consequently, the chances of survival are less compared with ticks at lower altitudes ^[56]. The altitude has a negative correlation with the biological integration of ticks, due to the decrease in temperature that limits the period of questing and development ^[37]^[47]^[57]. Low temperatures in spring delay the ticks’ activation of the questing ^[47] as a result of altitude variation ^[57]. Climate change is linked with the increase in tick populations at higher altitudes in Czech Republic (Table 1) and in Scotland, where the mean temperature is increasing ^[56].

Apart from temperature, saturation deficit, indicator of air dryness that depends on temperature and relative humidity, is an important factor influencing the tick population ^[56]. Ιt influences desiccation, and combined with the day length, it affects the relationship of the tick’s diapause, which is defined as the metabolic and developmental hold-up of the tick, caused by environmental changes. Moreover, it is considered to be an essential factor for questing ^[58]. For example, in Sweden, fewer ticks are observed in areas with low altitude and large saturation deficit ^[56].

Table 1. Current and future state of the effect of climate change on I. ricinus prevalence and on tick-borne diseases in some European countries.

	Country	Changes in I. ricinus Prevalence	Current Incidence of Tick-Borne Diseases	Future Incidence of Tick-Borne Diseases (by 2050)	Ref.
Northern Europe	Czech Republic	Has expanded into higher altitudes as a response to increases in average temperatures	Ιncreasing incidence of TBE	Ιncreasing incidence of TBE	^[59]
	Sweden	Longer tick activity seasons Distribution-limit shifted to higher latitude	Ιncreasing incidence of LB	Ιncreasing incidence of tick-borne disease in southern parts of the country	^[60]
	Norway	Distribution-limit shifted to higher latitude	Decreasing incidence of TBE	Ιncreasing incidence of tick-borne disease in southern parts of the country	^[60]
	Finland	Amplifying tick questing activity Prolonging the duration of the tick activity season Distribution-limit shifted to higher altitudes and latitudes	Ιncreasing incidence of LB	Ιncreasing incidence of tick-borne disease in southern parts of the country	^[60]
	Germany	Distribution-limit shifted to higher latitude	Ιncreasing incidence of LB	Ιncreasing incidence of LB	^[61]
Southern Europe	Greece	Has expanded to include areas at higher latitude and/or altitudes	Low incidence of tick-borne diseases	Have reduced areas of high- risk incidence of tick-borne diseases	^[60]
Southern Europe	Italy	Has expanded to include areas at higher latitude and/or altitudes	Low incidence of tick-borne diseases	High-risk incidence of tick-borne diseases	^[60]
	Portugal	Has expanded to include areas at higher latitude and/or altitudes	Low incidence of tick-borne diseases	Have reduced areas of high- risk incidence of tick-borne diseases	^[60]

3. The Effect of Climate Change on the Prevalence of LB and TBE

Climate change plays a causative role in the outbreak of tick-borne diseases (Table 1). Τhe impact of climate change on seasonal outbreaks or recessions of diseases transmitted by vectors in Europe has been described in many studies ^[16]^[22]^[62]. It is characteristic that the increase in temperature causes a significant reduction in the time required for incubation of the pathogen and for the vector’s life cycle, while the risk of the transmission to humans is dramatically increased due to the increase of the vector’s population ^[22].

LB is the most commonly transmitted to humans tick-borne disease in Europe and I. ricinus is the principal tick vector in Europe ^[63].The abundance of the infected I. ricinus nymphs is the best determinant factor that defines the transmission risk to humans and is influenced by the reduction in the altitude, due to the increase of the temperature ^[64]. The change in the hosts and in the habitat is likely to provoke an increase of I. ricinus density and the transmission risk of LB in Northwestern Europe, which is characterized by cold temperate climate and also by more elevated altitudes ^[38].

Humidity, temperature, and saturation deficit are the most important abiotic factors affecting LB vectors ^[56]. The consequences of global climate change converge on the fact that LB is going to remain a major health issue for the future ^[65]. The risk of LB transmission is connected with the increase of the hibernal and summery temperatures and the small alternations in the intraseasonal temperature range ^[66]. Moreover, the highest possibility of infection happens throughout the warmest period of the year, from May until September, with a peak in July ^[65].

The increase in the prevalence of the disease in Europe is noticeable and is attributed synergistically to anthropogenic and climatic factors ^[38]. In the decades 1990–2010, more than 360,000 cases were recorded in Europe ^[67], which represents a 400% increase of the prevalence of LB in endemic regions ^[67]^[68]. Currently, every year, there are estimated 65,000 new cases of the disease ^[22]. However, this number constitutes only an estimation, due to the incomplete recording of the cases in all the European countries ^[65].

In Western Europe, there are recorded 22.05 LB cases per 100,000 people per year ^[69]. Lithuania has one of the highest prevalence rates of the disease per country in Europe, resulting in mandatory registry of the disease in this country. For the years 2011–2018, there were recorded 73.9–100.6 cases per 100,000 people, while from 2014 to 2016, there were recorded 7424 new cases, which is equivalent to an approximate incidence rate of 85.4 ^[65]. The incidence rate is lower for the countries of Northern and Southwest Europe, which are characterized by the lowest and highest temperatures in Europe, respectively ^[70] (Table 2).

Table 2. Incidence rate for LB in Europe.

Region	Incidence Rate (100,000 People per Year)	Reference
Western Europe	22.05 cases	^[69]
France (2009–2017)	53 cases	^[71]
Northern Italy (2000–2015)	12.4 cases	^[72]
United Kingdom	12.1 cases	^[73]
Finland	61 cases	^[74]
Iceland	2 cases	^[75]
Spain	2.5–11.6 cases	^[76]
Lithuania	99.9 cases	^[65]
Germany	400 cases	^[77]
Regions of Slovenia, Austria, Baltic Coastline of Northern Sweden, some Estonian and Finnish Islands	100 cases	^[2]

Νote: the collection of data concerns either an annual rate or a rate for a period of years when this time is mentioned.

4. Climate Models as a Useful Tool in Predicting the Risk of Tick-Borne Diseases

Climate change is considered a crucial factor driving the range expansion of arthropod vectors and the increased incidence of vector-borne diseases. Thus, it is important to determine which abiotic and biotic factors are influencing the abundance of Ixodes ticks in order to predict the risk of tick-borne diseases ^[78]. Mathematical models are widely used. They include fundamental biological mechanisms, enabling predictions regarding the relative impact of climate change. However, in most cases, these models make simplifying assumptions regarding vector or pathogen dynamics, without incorporating data regarding the factors that drive the vector-borne diseases, such as seasonality in vector as well as host and pathogen dynamics. Although the current approaches are focused on understanding and predicting how climate change influences the abundance of vectors mainly in existing endemic areas, there is not a clear view. Moreover, it is necessary to develop and use climatic models that forecast risk in new regions. Consequently, scientists, in order to investigate how climate affects the distribution range of I. ricinus species, knowing the possibility of the shift in the distribution of the species due to climate change ^[38], have to collect data for climate variables that are known to be important for tick ecology (e.g., temperature, relative humidity, saturation deficit, and precipitation). Importantly, climate models that can predict changes in the short and long term have been developed ^[22]^[79].

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