*3.2. Vector-Borne Disease Risk*

The status of vector-borne diseases (i.e., infections transmitted by arthropod vectors) has changed significantly in the UK and Europe over the early 21st century [53]. During the early 20th century outbreaks of dengue and malaria were common in the Mediterranean region. Both malaria and the dengue mosquito vector, *Aedes aegypti*, were largely eradicated later that century so interest in vector-borne disease in Europe waned. However, the discovery in the early 1980s that the bacteria, *Borrelia burgdorferi*, in *Ixodid* ticks, which causes Lyme borreliosis (i.e., 'Lyme disease'), increasingly raised concerns over the role of ticks as disease vectors in Europe. Ticks are also known to be efficient vectors diseases, including the tick-borne encephalitis virus, the Crimean-Congo Haemorrhagic fever virus (rickettsial bacterial infection,) and other pathogens such as *Babesia*, *Anaplasma*, *Neoehrlichia*, and Louping Ill (infectious encephalomyelitis of sheep).

In 2012, dengue fever returned to Europe with >2000 cases in Madeira [54], and each year there are local cases of either dengue and/or chikungunya viruses across the Mediterranean Basin, including >400 cases of chikungunya in Italy in 2017 [55]. This transmission is associated with the importation, establishment, and spread of non-native invasive mosquitoes, *Aedes aegypti* and *Aedes albopictus* [56]. Since the start of the 21st century, West Nile virus has also consistently been reported in Eastern and Southern Europe, and more recently there have been local outbreaks of malaria in Greece and Italy [57]. The large outbreak of Zika virus in the Americas in 2015–2016 has further highlighted the threat posed by imported non-native mosquitoes and the potential for continental and global spread of mosquito-borne arboviruses, thus ensuring that vector-borne diseases will be an ever present public and veterinary health issue in coming years.

*Campylobacter* represents a good case example of an organism to study the effects of climate and weather on human infections in the UK and beyond. This is because the organism has a seasonality which is different from all other pathogens [44], numerous previous studies have been unable to identify the driving factors for this seasonal distribution [45–48], and since chickens appear to be an important source of infection, the association with weather is likely to be multi-factorial and indirect.

The changing status of vector-borne disease risk in the UK and Europe is partly attributable to globalisation and climate change; however, there are also various other environmental change factors that could equally be playing a role, and over a much shorter timescale. The invasive *Aedes* mosquito vectors of dengue, chikungunya and Zika are peri-domestic species, exploiting containers provided by humans, and dispersing in vehicles along highway systems. Thus, they are responsive to water storage and drought, and extreme precipitation, as well as changes in climate that can impact their development and capacity as vectors. In contrast, the habitat suitability of native mosquitoes and of native and non-native ticks are also driven by habitat availability and connectivity, and animal movements, which can be impacted by environmental change [53].

In the UK context in particular, the HPRU in Environmental Change and Health has focused on the sheep/deer tick, *Ixodes ricinus*, as the primary vector of Lyme borreliosis. It is able to feed on a variety of animal hosts during its three active life stages: larva, nymph and adult. This non-specialist feeding behaviour means that they can feed equally on wildlife, companion animals, livestock and humans, depending upon availability. These ticks thrive in the moist mild UK climate; however, their ability to survive off host is primarily determined by habitat structure, as well as animal diversity. Whilst historically it is a tick of upland sheep pasture and lowland woodland, these ticks are now found in lowland grazed grassland and urban green-space. Their dispersal throughout the countryside is contingent on their movement by animals.

It follows therefore that any environmental management of habitats that increase habitat connectivity or coverage, leads to greater dispersal and greater abundance of ticks. Recent published surveillance data by Public Health England (PHE) reported a significant change in the distribution of *Ixodes ricinus* [58], with particular expansion in the southern UK counties. Habitat management that favours ride (path) management in woodland, the creation of field margins, the impact of increased ecotonal habitat (i.e., habitat between two distinct habitats), changes in management of grassland habitat, or urban greenspace, have all been shown to influence the survival and abundance of ticks. In turn, the prevalence of the *Borrelia* bacteria within ticks is also influenced by both habitat and animal diversity [59–61].

This complex interplay between habitat, climate, animal population dynamics, vector density and pathogen prevalence demonstrates remarkable spatial and temporal heterogeneity, even at fine spatial scales. Although any scheme that modifies and enhances habitat structure may impact tick abundance in the UK, there are opportunities for managing these habitats to both maximise biodiversity and minimise human exposure and public health impacts [60], which can be particularly challenging in an urban setting (see Box 2). Further studies to develop empirical data both to inform such interventions and to understand the ecological aspects of disease transmission cycle are now a priority.

### **Box 2.** Urban greenspace and ticks in the city of Bath (UK).

Urban greenspace has been linked to improved human health and well-being, and such spaces are a focal point of the UK government adaptation plans to mitigate the effects of our changing climate. The benefits of urban greenspace and the arguments for increasing and improving access are clear (as discussed later in this paper), but it is important to also investigate the potential risks posed by tick-borne disease. To date, few studies on ticks in urban greenspace have been conducted in the UK. This research aimed to fill these gaps, and helps inform guidance development. Methodology involves identifying a range of urban greenspace habitats such as woodland, woodland edge, meadows, parkland and short grassland. In each habitat and at each site, standard tick collection is conducted using flagging a cloth over vegetation. Ticks are counted and identified, with abundance of ticks calculated for unit area. All ticks are tested for *Borrelia* bacteria using PCR and sequenced to genospecies to inform Lyme risk. Following initial surveys in Salisbury (UK) on the suitability of urban greenspace for ticks and the *Borrelia* bacteria (causing Lyme disease), comparable surveys were commenced in the city of Bath, working closely with Bath and North East Somerset (BANES) local authority. BANES have a network of natural and managed urban greenspace, and this involves the creation of urban meadows. BANES have also led the way in working with Public Health England (PHE) with regard to assessing and mitigating the risks posed by urban ticks. Integrating the findings of academic and public health research on tick and Lyme risk enables better informed assessment of risk and appropriate public health awareness strategies, and this is proving a model that needs to be replicated across local authorities in the UK where urban ticks are being reported.

As part of the HPRU, field sampling of urban greenspace in Bath has taken place over the last two years, and found high suitability for ticks in some areas, mainly in woodland and woodland edge habitat, and the presence of *Borrelia*-infected ticks. So far, based upon preliminary results, prevalence rates appear lower (at 4.5%; unpublished data) than Salisbury (18.1%) [61], and appear restricted to only parts of the city. This work has been integral to enabling BANES to provide accurate tick awareness material, target their interventions, and assess the risks posed to humans by ticks and the impacts of their management. However further evidence is required, and as part of the HPRU in Environment and Human Health research, further sampling is taking place in Bath as well as in other cities such as Bristol and Southampton. Based upon this collective field research, PHE will be in a better position to advise local authorities, and to begin developing guidelines that can be used for management and in targeting tick awareness.

In contrast to tick-borne disease, which currently causes 2000–3000 cases of human Lyme borreliosis each year, the disease threat posed by native UK mosquitoes is currently insignificant; however, this should not lead to complacency. The incidence of several arbovirus diseases in the rest of Europe, together with the facts that malaria was once endemic in the UK and that mosquitoes are still a serious pest in some localities, suggest there is a need to understand how climate and other environmental change might affect future disease risk.

For example, in the UK, there is a large-scale programme for the development of new wetlands. The aims of this programme include: the managed re-alignment of the coasts to create new saltmarsh and mudflat habitat to mitigate coastal flooding and storm surges, as well as creating new protected habitats; the reversion of arable land to flooded grassland, as part of large-scale wetland expansion projects; and the creation of urban wetlands to provide sustainable urban drainage and to create mitigation habitat under the European Habitats Directive [62]. Field studies in the UK in each of these habitats has shown that mosquitoes do exploit newly created habitats, but their ability to colonise is largely dependent upon the design of new wetlands, the management of tidal waters, the flooding regime of wet grassland and the design of ditches, scrapes and sewage treatment reed beds [63–65]. The UK has 36 recorded species of mosquito, three of which have only been detected in the last 5–10 years [66] and one is known to be non-native and very invasive [67].

Although there is no current health risk, a warming climate and changes in animal movement and human interactions with the natural environment, coupled with an increase in the numbers of infected travelling pets, mean that any habitat management strategy that favours mosquito habitat could be significant. As with ticks, research that focusses on the how these vectors may be managed within the environment, particularly in protected habitats, is a key requirement for future contingency planning. Ensuring that we can progress environmental change and increase biodiversity, without the

unexpected negative impact on vector-borne disease risk, is a priority area for PHE and the HPRU in Environmental Change and Health.
