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Climate Variability And Visceral Leishmaniasis In Europe¹

17 Jan 2008

Source: WHO/TDR

Elisabeth Lindgren ¹ , Torsten Naucke ² , Bettina Menne ³

¹Department of Systems Ecology, Stockholm University, Sweden
²Institute for Medical Parasitology, Bonn University, Germany
³Global Change and Health, WHO European Centre for Environment and Health, Via Francesco Crispi 10, Rome 00187, Italy

Working paper for the Scientific Working Group meeting on Leishmaniasis Research, convened by the Special Programme for Research and Training in Tropical Diseases, Geneva, 2–4 February 2004

Full text source: Scientific Working Group, Report on Leishmaniasis, 2–4 February 2004, Geneva, Switzerland, Copyright © World Health Organization on behalf of the Special Programme for Research and Training in Tropical Diseases, 2004, http://www.who.int/tdr/publications/publications/swg_leish.htm

Introduction

A three-year pan-European project entitled Climate change and adaptation strategies for human health (cCASHh), funded under the European Union thematic programme on Energy, Environment and Sustainable Development (EESD-1999), began in 2000. The aim of this project was to provide a scientific basis for the development within the health sector of response strategies to climate variability and change. The project included academic partners in the United Kingdom, Sweden, the Netherlands, Germany, Italy, and the Czech Republic.

This paper reports the findings of a review of impact of climate variability and change on leishmaniasis, and the results of discussions at a meeting on vector-borne diseases and climate change held in Prague, 5–7 May 2003. A literature search was conducted to answer questions about the current distribution of visceral leishmaniasis (VL) in the WHO European Region, the influence of environmental and climatic factors on disease risk, the possible impacts of future climate, and future research needs.

Current distribution and risks

In Europe, VL is considered to be a rare disease, although its incidence increased significantly in the region during the 1990s. This was due in part to the large proportion of Leishmania/HIV co-infections (approximately 25%–70% of adult VL cases are co-infected with HIV) and to better reporting after the establishment of a WHO surveillance network in 1994 [6]. Non-HIV VL incidence rates have increased in Italy and France (including a four-fold increase in Alpes-Maritimes), and new endemic areas have been detected where no previous autochthonous cases had been reported, e.g. in northern Italy, North Croatia, Switzerland and Germany.

The distribution of leishmaniasis worldwide is limited by the distribution of its vector sandfly and by the latter's susceptibility to cold climate, ability to support internal development of specific species of Leishmania, and tendency to take blood from animals or humans only [31]. Populations of Phlebotomus perniciosus, one of the known vectors of Mediterranean VL, have been found as far north as Paris [22], and recently also in Gerweiler in Germany [21]. Table 1 lists the distribution of the different species that may act as vector for L. infantum, the pathogen that causes VL in Europe.

Since the mid-1990s, the worldwide geographical distribution of endemic leishmaniasis has expanded [30]. This spread is probably due to a combination of factors, among them increased monitoring, intensified research, demographic change, land-use/land cover changes that create new habitats and/or changes in microclimate, and changes in seasonal climate. The overlap between geographical areas with high risk of both leishmaniasis and HIV is increasing with the spread of leishmaniasis (typically a rural disease) into urban areas and the increased spread of HIV into rural areas [30].

Within the European Region, cases of VL have been reported from Albania, Bosnia & Herzegovina, Bulgaria, Croatia, France, Greece, Hungary, Italy, Macedonia, Malta, Monaco, Portugal, Romania, Spain, and Yugoslavia. Leishmaniasis is also transmitted in the adjoining countries of Azerbaijan, Cyprus, Georgia, Kazakhstan, Tajikistan, Turkey, Turkmenistan and Uzbekistan. Fig. 1 shows the regional distribution of VL compared to cutaneous leishmaniasis (CL).

Fig. 1

Most cases of co-infection in Europe are reported from the most densely populated areas and provinces and, as shown in Fig. 2, there is a predominance of cases in coastal areas (75%). In south-western Europe, 80% of co-infection cases are from urban areas, the main cities being Lisbon and Porto in Portugal; Barcelona, Granada, Madrid and Seville in Spain; Marseille and Nice in France; and Genoa, Milan and Catania (Sicily) in Italy. This distribution pattern, however, is probably partly related to the current location of the WHO surveillance centres (which specifically monitor Leishmania/HIV co-infections) rather than to other factors. Most of the centres are located near cities like Rome and Catania in Italy; Madrid, Barcelona, Seville, Bilbao, Granada and Palma de Mallorca in Spain; Paris, Marseille, Montpellier and Nice in France; and Lisbon in Portugal.

Fig. 2

Populations at risk include people living in rural and periurban areas where both sandflies and reservoir animals are prevalent. VL used to be found predominately in children but in recent years an increasing proportion of adult cases (non-HIV) has been reported. This change in age distribution is probably caused by several factors, such as changes in human exposure patterns, environmental changes, and improvements in case diagnosis and notification. Improvements in nutritional and general health status in European children have probably played a roll in reducing the characteristic high susceptibility of children to this disease.

The sandfly vector is mainly active during the night, and the highest risk for contracting the disease from sandfly bites is therefore between dusk and dawn.

Urban areas have become high-risk locations of late. High-risk populations in urban environments are people who are HIV-positive. In Europe, 77% of Leishmania/HIV co-infected patients are aged between 31 and 50 years, and 83% of them are men [33]. Another risk group is intravenous drug users who share syringes [1,4,23]. The highest risk for VL is found among HIV-infected intravenous drug users, who account for 71% of co-infection cases [6].

In addition, Leishmania can be transferred through blood transfusion [12]; the trans-placental route of infection is also possible [18].

Leishmania/HIV co-infections accelerate and aggravate both leishmaniasis and AIDS symptoms [6]. Also, relapses of leishmaniasis after treatment are common among persons with HIV co-infection. The mean survival of co-infected patients is only 13 months [31]. The current number of HIV-infected persons in western and eastern Europe (not including the Russian Federation) is approximately 580 000 (WHO, 2001). In the Mediterranean basin, 1.5%–9% of AIDS patients develop VL [30].

Most of the co-infection cases have been reported from France, Italy, Portugal and Spain, but co-infection is prevalent in Albania, Croatia and Greece as well. On average, the number of reported cases of Leishmania/HIV co-infection increased during the late 1990s relative to the number of reported HIV cases in the same period [6]. However, the number of cases of co-infection has recently started to fall in southern Europe owing to the use of new therapeutic methods, i.e. highly active antiretroviral therapies (HAARTs) (Table 2).

Influence of environmental and climatic factors on disease risk

The distribution of VL in Europe is significantly less than the distribution of the sandfly vectors. The occurrence of disease transmission within the range of the vectors depends on vector abundance, vector survival, vector biting rate (i.e. gonotrophic cycle), the extrinsic incubation period, and the length of the transmission season. Each of these parameters is climate dependent, but the precise relationship with climate needs to be further studied and evaluated. Caution is also required in the interpretation of laboratory experiments as sandflies are able to evade extreme weather conditions in the field by their choice of resting site and time of activity.

Temperature and humidity are the two most important climatic factors for sandfly survival, development and activity. Phlebotomus sandflies can survive cold temperatures in diapause (overwintering), which is initiated by a combination of low temperature and reduced daylight and can last 4 to 8 months depending on location. In Europe, the biting activity of sandflies is strongly seasonal, and restricted to the summer months in most areas. Adult activity as well as larval development slows down considerably below 20°C. However, some species are active even at much lower temperatures, e.g. P. neglectus in Greece at 13°C and P. mascittii in Germany at 13.5°C [19,25].

Temperature also affects the parasite itself; evidence indicates that L. infantum is prevalent within the 5–10°C January and 20–30°C July isotherms, usually located below latitude 45 N and below 400–600 m above sea level [14]. The worldwide distribution of sandflies is considered to be confined to areas that have at least one month with a mean temperature of 20°C [28]. However, it has been suggested that the limit of the European distribution of vectors and parasites better corresponds to the 10°C annual isotherm [15]. This is in accordance with recent findings of vectors and isolated autochthonous cases of leishmaniasis in southern Germany, where the July isotherm is 16°C to 18°C. The highest focus of leishmaniasis in Europe is the Guadix focus (Andalusia, Spain), at an altitude of 900 to 950 m above sea level.

Sandflies are sensitive to sudden temperature changes and usually prefer regions with small differences between the maximum and minimum temperature. Sandfly survival can be reduced if the climate gets too hot and dry, even though the flies may rest in cold, humid places during the daytime [17]. The resting sites of adults are known for a few species of sylvatic sandfly; they include tree holes and trunks. Peridomestic species rest on walls and, at hot times of the day, retreat into cracks and crevices [28]. Poroton stone buildings, for example, have the ability to store humidity during the night and evaporate it during the day, producing favourable conditions for adult sandflies to survive the hot, dry summer days.

In addition to the direct association between climate and leishmaniasis transmission, climate has indirect impacts by influencing (1) the distribution of hosts; (2) the local vegetation (important as resting sites and sugar sources); and (3) the patterns of human exposure to sandfly vectors.

Possible impact of future climate risks

With climate change, the distribution range of both the sandfly vector and the pathogen may extend northwards and into higher altitudes (WHO, 1999). In currently endemic areas, higher seasonal temperatures would lead to prolonged activity periods and shorter diapause periods. This could result in an increased number of sandfly generations per year. In addition, higher temperatures are likely to accelerate maturation of the protozoan parasite, thereby increasing the risk of infection [17,24]. However, if the climate becomes too hot and dry for the vector to survive, the disease may disappear from some localities even though the vector may adapt by resting in cool, humid places during the daytime.

Imported infected dogs can contribute to the emergence of leishmaniasis in new locations. They are a potential source of the pathogen if the vector expands its geographical distribution due to change in climate (WHO, 1999). Several imported cases of canine leishmaniasis are, for example, reported from Germany [9] and the Netherlands [27] every year.

In order to develop more sophisticated climate-vector-disease scenario models, increased knowledge is needed on the short- and long-term effects of climate variation on leishmaniasis risk. This can be achieved in several ways: (1) experimental evidence measuring the influence of temperature or humidity (for example) on sandfly or Leishmania biology; (2) field evidence that sandfly biological parameters vary with climate; (3) field evidence that geographic variation in sandfly abundance (including presence vs. absence) or Leishmania infection rate correlates with climatic variables; and (4) field evidence that temporal variation in sandfly abundance or Leishmania infection rate (including seasonal and long-term trends) correlates with climatic variables. As different sandfly species are responsible for Leishmania transmission across Europe, climate change will have different impacts on VL risk in different parts of the region.

Regional climate models for leishmaniasis should therefore be constructed according to the local vector species.

Future research needs

There is a need for further research on visceral leishmaniasis and its vectors in Europe. Better understanding of the current situation would allow more specific risk evaluation and form the basis for predicting change in distribution and endemicity due to environmental and climatic changes in different parts of Europe. Some main issues are to:

• Collate available data on sandfly and parasite distribution, and sandfly seasonality, in relation to information and data on climate and environmental variables.

• Collect new field data on sandfly biological parameters (including activity patterns, seasonality, survival, infection rates) in relation to defined climatic and environmental variables - latitude and altitude transects over full seasons. Develop a network of fieldworkers across Europe able to use standard methodology for measuring these parameters (especially infection rate).

• Collect laboratory data on vectorial competence, including extrinsic incubation period and diapause determinants, of different European vector species.

• Collect new field data on dog prevalence, and set up a network of veterinarians across Europe to use standardized methodology.

• Further analysis of HIV-leishmaniasis data.

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