Malaria Ecotypes and Stratification

CHAPTER

3 Malaria Ecotypes and Stratification Allan Schapira*,† and Konstantina Boutsika*,†

Contents

Abstract

3.1. Introduction 3.2. Methods 3.3. Results 3.3.1. Global studies 3.3.2. Experiences in different geographical regions 3.3.3. Proposed definition, identification and demarcation of malaria ecotypes and their implications in five biogeographic regions 3.4. Discussion 3.4.1. Implications for control programmes 3.4.2. Implications for malaria modelling and field research Acknowledgements References

98 106 108 108 112

137 149 149 153 155 155

To deal with the variability of malaria, control programmes need to stratify their malaria problem into a number of smaller units. Such stratification may be based on the epidemiology of malaria or on its determinants such as ecology. An ecotype classification was developed by the World Health Organization (WHO) around 1990, and it is time to assess its usefulness for current malaria control as well as for malaria modelling on the basis of published research. Journal and grey literature was searched for articles on malaria or Anopheles combined with ecology or stratification.

* Swiss Tropical and Public Health Institute, Basel, Switzerland {

University of Basel, Basel, Switzerland

Advances in Parasitology, Volume 78 ISSN 0065-308X, DOI: 10.1016/B978-0-12-394303-3.00001-3

#

2012 Elsevier Ltd. All rights reserved.

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It was found that all malaria in the world today could be assigned to one or more of the following ecotypes: savanna, plains and valleys; forest and forest fringe; foothill; mountain fringe and northern and southern fringes; desert fringe; coastal and urban. However, some areas are in transitional or mixed zones; furthermore, the implications of any ecotype depend on the biogeographical region, sometimes subregion, and finally, the knowledge on physiography needs to be supplemented by local information on natural, anthropic and health system processes including malaria control. Ecotyping can therefore not be seen as a shortcut to determine control interventions, but rather as a framework to supplement available epidemiological and entomological data so as to assess malaria situations at the local level, think through the particular risks and opportunities and reinforce intersectoral action. With these caveats, it does however emerge that several ecotypic distinctions are well defined and have relatively constant implications for control within certain biogeographic regions. Forest environments in the Indo-malay and the Neotropics are, with a few exceptions, associated with much higher malaria risk than in adjacent areas; the vectors are difficult to control, and the anthropic factors also often converge to impose constraints. Urban malaria in Africa is associated with lower risk than savanna malaria; larval control may be considered though its role is not so far well established. In contrast, urban malaria in the Indian subcontinent is associated with higher risks than most adjacent rural areas, and larval control has a definite, though not exclusive, role. Simulation modelling of cost-effectiveness of malaria control strategies in different scenarios should prioritize ecotypes where malaria control encounters serious technical problems. Further field research on malaria and ecology should be interdisciplinary, especially with geography, and pay more attention to juxtapositions and to anthropic elements, especially migration.

3.1. INTRODUCTION ‘‘Everything about malaria is so moulded and altered by local conditions that it becomes a thousand different diseases and epidemiological puzzles. . . While this has provided a fascinating occupation for the epidemiologist, it has seemed discouraging enough to the health authorities’’ (Hackett, 1937). To deal with such immense variability—and encourage the health authorities—some kind of classification is needed. In fact, most national malaria control programmes stratify their malarial problem into a number of smaller units, usually geographically defined, where different strategies or approaches are applied (Beales and Gilles, 2000; Beales et al., 1988). Classification of malaria situations should also be useful for malaria modelling, which is undergoing a renaissance on the background

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of increased international funding for malaria control, renewed interest in elimination and eradication and technical developments, which now allow for relatively realistic and dynamic assessment of cost-effectiveness of malaria control in a variety of scenarios (Smith et al., 2008). While it is possible in modelling to handle any number of permutations of variables, an evidence-based classification of malaria situations would make it possible to present model outputs within a humanly manageable number of scenarios. This would also support communication between modelling and control programmes. Over the years, various typologies have been proposed with the aim of supporting stratification and decision-making in malaria control as well as the description of malaria and its occurrence. Almost all of them are based on either the epidemiology of malaria or determinants of the disease such as ecology or climate. Among the malariometric classifications, the division based on spleen or parasite rate into hypo-, meso-, hyper- and holoendemic (Metselaar and Van Thiel, 1959; WHO, 1951) is well known and easy to understand, but it has many weaknesses, including the absence of evidence that it has implications for planning control. An alternative is to classify malaria along the spectrum of stability, that is, contrasting stable malaria characterized by highly anthropophilic long-lived vectors in a warm environment, with unstable malaria, where the characteristics are the opposite. This is more attuned to decision-making, but the assessment is affected by the scarcity of data on the longevity of mosquitoes in nature (Kiszewski et al., 2004), and the utility is limited by the broad intermediate range, where the implications of Macdonald’s stability index (the number of bites on man taken by an average mosquito during a normal life-time) (Macdonald, 1957a) are uncertain. Molineaux (1988) proposed using the basic reproductive rate, as a refinement of the stability index, incorporating more relevant factors. However, its estimation is also demanding and hardly possible at a fine enough scale to deal with important variability for a control programme. Recently, it has been proposed to base classification and decision-making on the more readily available measures of parasite prevalence and disease incidence, especially Plasmodium falciparum prevalence. This may seem a throwback to the old endemicity classification, but avoids the arbitrary classes, while proposing further investigation of relationships between malariometrics and chance of elimination (Hay et al., 2008). However, all of these quantitative indicators may be poor predictors of resilience to currently available interventions. For example, stable malaria on the north coast of South America was easily eliminated by spraying in the 1950s (Giglioli et al., 1976), while unstable urban malaria in India has withstood multi-pronged attacks (Saxena, 2001). In classifying malaria situations, it would therefore be desirable to include elements beyond quantitative epidemiological indicators, for

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example, vector bionomics, resistance to biocides and operational determinants of control feasibility. Typologies based on malaria determinants would be useful if they serve as good proxies for several of such important elements. The earliest global scheme based on this principle was probably a climate-based classification (Gill, 1938), but it has never been widely accepted due to the poor correlation between malaria and climate on a global scale and in many regions of the world. In contrast, a malaria map for Africa based on climate suitability has been widely used to illustrate the presumed distribution of malaria in that continent and has at least an approximate congruence with epidemiological data (Craig et al., 1999). Ecological classifications have been promoted, ‘‘because they allow a classification based on common knowledge about ecological characteristics in a given area without collecting extensive information on vectors, parasites, meteorology, human characteristics, etc.’’ (Beljaev, 2002). Ecological characterization of local malaria situations was used in the early twentieth century when anti-larval measures, which require an understanding of local physiography and vector bionomics, dominated vector control options (Bradley, 1994; Takken et al., 1990). The first global classification incorporating environmental determinants was developed in the 1950s by Macdonald, who, referring to Wallace’s six zoogeographical regions (Table 3.1), identified the main vectors and their bionomics in each of 12 zones (Macdonald, 1957b).

TABLE 3.1 Malaria ecotypes and their occurrence in the world according to texts published 1990–2000 Malaria ecotype

Where found

Savanna Plains with traditional agriculture outside Africa Highland fringe

Sub-Saharan Africa, Southwest Pacific South Asia, Central and South America, China Africa, Southeast Asia, Southwest Pacific, South America Sahel, southern Africa, West Asia South and Southeast Asia, South America Africa, South and Southeast Asia, South and Central America Africa, South Asia, South America Superimposed on any of the above ecotypes

Desert fringe and oasis Forest and forest fringe Costal and marshland Urban and peri-urban Agricultural development including irrigation War and socio-political disturbances

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This description helped organize the global diversity of anophelines and provided valuable insights on vector bionomics and control. However, as a classification scheme, it is a hybrid between a geographical division and an ecological typology, and it has very limited control implications. Macdonald’s scheme was criticized by Russian malariologists as being too top down. As an alternative, they promoted landscape epidemiology (Pavlovsky, 1966; Sergiev et al., 2007a), seeking to integrate epidemiology with landscape science (Dyakonov, 2007), examining the interactions between natural and human ecology to convey a comprehensive local picture of the disease and its determinants and thereby stimulate thinking about what could be done about it. For malaria, these principles were applied by Beklemishev from 1940 onwards (Tchesnova, 1998) and further developed by Lysenko, who recommended the recognition of types of foci within each kind of geographical area or landscape and zonation based on a combination of malaria data and ecological type. However, in practice, it was often difficult to differentiate malaria control in vertical programme strategies according to this approach (Lysenko, 1960). Otherwise, during the eradication era from the 1950s to the 1970s, there was little interest in local assessment and classification, given that indoor residual spraying (IRS) is much less site specific than larval control, and those strategies and approaches were highly standardized. However, in tropical Africa, various classification schemes were developed, especially by francophone scientists (Carnevale and Mouchet, 2001; Hamon et al., 1963; Mouchet, 1976). The experiences were crystallized as an approach consisting of (A) Identification of the primary facie`s e´pide´miologique as belonging to one of six major natural regions, namely, (1) equatorial with forest or savanna and perennial transmission; (2) tropical with humid savanna and a transmission season exceeding 6 months; (3) Sahelian with dry savannas or steppes and a transmission season lasting less than 6 months; (4) desert with steppe or desert and short, sometimes missing transmission season; (5) southern corresponding to the plateaux of southern Africa with seasonal transmission, which is interrupted in winter and (6) highland at 1000–2000m altitude, where transmission is highly variable and limited by temperature and surface declination. (B) Identification of secondary factors within each primary facie`s: natural (landform, water bodies, soil characteristics); anthropic factors (modification of vegetation, water bodies, urbanization, habitat of humans and cattle) and dynamic factors (natural disasters, climate change, malaria control, population movement, development of transport networks) (Mouchet et al., 1993a).

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Outside Africa, the failure to eradicate eventually led to renewed interest in ecology-based classification, aiming to incorporate the lessons learnt as well as the local and regional experiences and frameworks referred to above. A global malaria typology was developed, building on the early ecological characterizations and the Russian and francophone ‘schools’ with environmental characteristics as the primary identifier, but trying to relate them to the selection of control interventions (Najera, 1989; Najera et al., 1992), this framework was included in the global malaria control strategy promoted by World Health Organization (WHO) and approved by the Ministerial Conference on Malaria in Amsterdam in 1992 (WHO, 1993). The general principle is to link environmental determinants to associated characteristics of malaria epidemiology, vector bionomics, human ecology and health systems, emphasizing commonalities of particular patterns across the world (Beales and Gilles, 2000; Najera, 1990). Table 3.1 presents the types defined as these texts converged, with some harmonization of nomenclature. Around 1990, the term paradigm was frequently used to denote the need not only for describing particular settings but also to provide examples of successful control adapted to local determinants. In the following years, as it was difficult to identify truly paradigmatic control experiences, this term fell into disuse, and the most commonly used term became ecotypes or eco-epidemiological types. It is proposed here to use the term (malaria) ecotype, because it parallels the use of ecotype in biology (Table 3.2), meaning that the malaria system, which is a biological and social phenomenon, can be studied in the same way as an organism interacting with an environment. The latest of these texts is a report issued by WHO in 2006 reviewing effectiveness and challenges of different vector control measures according to ecotype. This publication includes the first seven of the above ecotypes under ‘steady-state ecosystems’ and the two last as ‘situations of rapid development change’. It notes that IRS and insecticide-treated nets (ITNs) are both almost universally effective for malaria control (though not to the same degree everywhere), and that stratification according to ecotypes would be useful mainly to identify epidemiological patterns, local risk factors, risk groups and feasibility of larval control (WHO, 2006). Given the accessibility of this text, it will not be summarized here, but attention will be given to recent evidence that challenges or supplements it. This typology has not been critically addressed in journal literature and may now be at risk of being perceived as dogma; it is therefore opportune to revisit it to assess its utility in an era when a wide range of vector control interventions are being considered on a background of increased resources and renewed interest in elimination and eradication. Another reason for revisiting ecology-based malaria classification is that

TABLE 3.2 Terms and acronyms used in this review

Annual parasite index (API) Biogeographic regions or realms/ ecozones/zoo-geographical regions

Cold cloud duration (CCD) Ecoregion Ecosystem

Ecotone

A measure of the number of confirmed malaria cases per thousand people per year in a defined geographical area Major geographic divisions of the biosphere according to distribution of fauna. The original zoogeographical regions of Wallace (1876) have recently been modified by the World Wildlife Foundation (Olson et al., 2002) to the following (Fig. 3.1): 1. Palearctic (including most of Eurasia and North Africa) 2. Nearctic (North America) 3. Neotropic (including South and Central America and the Caribbean) 4. Afrotropic (including sub-Saharan Africa, Madagascar and south-western part of Arabian peninsula) 5. Indo-malay (including Indian subcontinent and Southeast Asia) 6. Australasian (including eastern Indonesia and Southwest Pacific) 7. Oceanic 8. Antarctic Note: 7 and 8 are malaria free Remotely sensed data correlating closely with rainfall (Thomson et al., 1997) Regions of relative homogeneity in ecological systems or in relationships among organisms and their environment (Omernik, 1987) An area of any size with an association of physical and biological components so organized so that a change in one component may bring about some corresponding change in other components and in the operation of the whole system (Bailey, 2009) Transition zone between two communities (Bailey, 2009) (continued)

TABLE 3.2

(continued)

Ecotype

Enhanced vegetation index (EVI) Entomological inoculation rate (EIR) Geographic information system (GIS)

Insecticide-treated nets (ITNs) Indoor residual spraying (IRS) Malaria focus

Normalized difference vegetation index (NDVI) Physiography Receptivity

For malaria: a group of malaria foci, which are similar in terms of physical and biological environment and most of the following attributes: malaria epidemiology, vector bionomics, human ecology and health systems (writers’ proposed definition) In biology, ecotype refers to species with wide geographic range that develop locally adapted populations having different limits of tolerance to environmental factors (Bailey, 2009) NDVI (see below) corrected for some distortions The expected number of infectious bites, per person, per unit time (usually a year) Information system for capturing, storing, analyzing, managing and presenting data which are spatially referenced (linked to location) (Bailey, 2009) Also including long-lasting insecticidal nets (LLINs) Indoor residual spraying with insecticides. ITN and IRS are the two main methods of adult vector control in malaria A defined and circumscribed locality situated in a currently or formerly malarious area and containing the continuous or intermittent epidemiological factors necessary for malaria transmission (WHO, 2007) Remotely sensed data based on reflectance factors indicating presence and density of green vegetation or water (Thomson et al., 1997) Landform (including surface geometry and underlying geologic material (Bailey, 2009)) For a malaria-free area: The abundant presence of vector anophelines and the existence of other ecological and climatic factors favouring malaria

Stratification

Vectorial capacity Vulnerability

transmission. Receptivity is a reflection of vectorial capacity of local anophelines during the season most favourable for malaria transmission (WHO, 1978) A process of dividing the malaria problem of a given area, for example, a country, into a limited number of units, which are sufficient homogenous internally and sufficiently different from each other that it is rational to apply different strategies to them The expected number of infectious bites that will arise from all the mosquitoes that bite a single person in 1 day For a malaria-free area: Proximity to malarious areas or liability to the frequent influx of infected individuals or groups and/or of infected anophelines. The level of awareness of the population concerning malaria, and the level of sophistication of the health authorities also have an important bearing (WHO, 1978)

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since the early 1990s, the evidence-base has been strengthened by the availability of geographic information systems (GISs), remote sensing and spatial analysis (Kitron, 1998). General criteria for a malaria typology could be presented as follows, slightly modified from those put forward by Molineaux in 1988 for a typology based on epidemiological criteria: (a) it does not have too many types; (b) it provides only one type for every possible malaria situation; (c) the types are meaningful for control, in terms of what is recommended and feasible in a situation and of achieving the expected impact and (d) the diagnosis of situations and the stratification of geographical areas according to the types are not too expensive or complicated. The purpose of this chapter is not to identify the perfect malaria typology but to assess, review and possibly improve ecological classification for malaria control and modelling, keeping in mind the existing availability of malariometric data. The methodology selected is a qualitative review of published evidence by biogeographic region. This division of the world has direct implications for mosquito fauna, precedes all malaria typologies, has stood the test of time and is used by other disciplines.

3.2. METHODS Pubmed (http://www.ncbi.nlm.nih.gov/sites/entrez) and ISI Web of KnowledgeTM(http://apps.isiknowledge.com/UA_GeneralSearch_input. do? product¼UAandsearch_mode¼GeneralSearch andSID¼Q2A34OLK8A FDBNLGdOD and preferencesSaved¼) were searched without time limitation, using as search terms ‘malaria’ combined with each of the following: ‘ecology’, ‘ecological’, ‘eco-epidemiological’, ‘ecotype’, ‘geography’ and ‘stratification’. In addition, the search term ‘Anopheles’ was combined with ‘ecology’ or ‘interaction’ for the past 20 years. Major textbooks, monographs, WHO publications on malaria and websites of some institutions and malaria control programmes were hand searched for material relevant to the subject. Recent literature on ecology and disease was examined selectively for updates on modelling and concepts. The several thousand references found were scanned by their titles and the number reduced to about 1000. For these, the abstracts were read, and this led to a selection of the 200 articles and texts quoted in this review. The application of ‘eco-epidemiology’ for classifying malaria situations has been examined by biogeographical region (Table 3.2; Fig. 3.1). For each biogeographical region, a brief overview of malaria vector bionomics and any general region-wide classification schemes is followed by a review of research findings related to specified types, with an emphasis on those of the scheme presented in Table 3.1. This is followed by a review

Palearctic Nearctic Oceanic

Indo-malay

Afrotropic Oceanic Neotropic

Australasian Antarctic

Biome TMF: Tropical and subtropical moist broadleaf forests TDF: Tropical and subtropical dry broadleaf forests TCF: Tropical and subtropical coniferous forests TeBF: Temperate broadleaf and mixed forests TeCF: Temperate coniferous forests BF: Boreal forests/taiga TG: Tropical and sub-tropical grasslands, savannas and shrublands TeG: Temperate grasslands, savannas and shrublands FG: Flooded grasslands and savannas

MG: Montane grasslands and shrublands T: Tundra MF: Mediterranean forests, woodlands and scrub D: Deserts and xeric shrublands M: Mangroves Lakes Rock and ice Biogeographic realm Conutry Ecoregions

FIGURE 3.1 The 14 Biomes and Eight Biogeographic Realms of the World as defined by the World Wildlife Foundation. Biomes are coded in colours. Biogeographic realms are named in the figure. Ecoregions are nested within both biomes and realms. Source: United Nations Millennium Ecosystem Assessment, Appendix, Fig. 4.3. Permission to reuse is given at www.millenniumassessment.org/en/GraphicResources. aspx.

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of articles relevant to malaria and ecology at the global level. The findings are summarized in two tables, one describing the general characteristics of six proposed basic ecotypes at the global level, including their definitions and delimitations (addressing Molineaux’s criterion (a)), and the other, the variability of those ecotypes according to biogeographic region. In these two tables, the delimitation of the ecotypes from each other and their implications for control are specifically addressed, in line with Molineaux’s criteria (b) and (c). The key terms used in this review are presented in Table 3.2.

3.3. RESULTS 3.3.1. Global studies The monumental Biodiversite´ du paludisme is a thorough global review of the diversity of malaria epidemiology with emphasis on the vector aspects (Mouchet et al., 2004a). While referring to previous classification schemes, this text avoids any attempt at a global typology but does include a global overview, which can be summarized as follows: The distribution of malaria follows a gradient: from Afrotropic core areas, where malaria is endemic and continuous over vast distances, except where interdicted by climatic factors, with transitional epidemiology in the ecotones; through tropical Southwest Pacific, then tropical Asia and South America, where malaria is focal and highly dependent on ecological determinants, to subtropical and temperate areas, where malaria is sporadic and transmission conditional on a convergence of enabling factors. As may have been noted, the present review draws extensively on the compilations, reviews and syntheses in Biodiversite´. The sequence in which the world’s biogeographic regions have been presented corresponds to the global gradient just described. The interactions between agriculture and malaria have been reviewed by Service (1989), who includes the various possibilities for control and the circumstances under which they are likely to be feasible and effective. A more recent and quantitative review found that most dam building and irrigation in the world takes place in areas with no or little malaria, but that the risks from environmental change are greatest in areas with unstable malaria and that remedial measures should be planned at the design stage (Keiser et al., 2005a). The effectiveness of environmental management for malaria control has been reviewed with reference to an ecological typology with four classes: deep forests, forest fringe and hills; rural malaria attributable to water resources development and management; rural malaria attributable to wetlands, rivers, streams, coasts and non-agricultural man-made

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habitats and urban and peri-urban malaria. Nearly all analyzable studies showed some effect of environmental measures, but most were confounded by concurrent interventions. This review documented that environmental management can be highly effective in certain circumstances and that the practice in the twentieth century, both before and after the eradication era, had been to select such circumstances, largely excluding settings (especially savanna and forest malaria), which were or which were thought to be inappropriate (Keiser et al., 2005a). Yasuoka and Levins reviewed deforestation worldwide and found that the effects depended on the type of environmental change and the species of vector; in particular, sun preference of the vector was associated with increasing vector density as a result of deforestation. In fact, An. darlingi prefers breeding sites exposed to the sun or with only partial shade in contrast to An. dirus in Southeast Asia (Yasuoka and Levins, 2007). Kiszewski mapped a global malaria stability index in order to describe the distribution of the global malaria burden, as it would be without organized malaria control. The index represented the contribution of regionally dominant vectors to the force of transmission in each geographic area and incorporated human blood index, daily survival of the vector, duration of the transmission season and extrinsic incubation period based on temperature. Vegetation indices from remote sensing were used to define areas suitable for vectors with ecological requirements, such as salt marshes or forests, and altitude limits were used to define the ranges of vector species. Comparing the resulting map (Kiszewski et al., 2004) with Fig. 3.1, the congruence between malaria stability and forests in the Neotropic and Indo-malay is clear. The Malaria Atlas Project (MAP) has over some years mapped malaria burdens in the world. An examination comparing several independent definitions of urban areas with reports on malaria parasite prevalence in pairs of urban and rural areas found that the Global Rural Urban Mapping Project (GRUMP) urban extent mask (Center for International Earth Science Information Network, 2004) proved more accurate than other delimitations of urban extent to delimit urban areas with lower malaria burden. However, significantly lower burdens in urban areas were found only in the Afrotropic (Tatem et al., 2008). The latest iteration makes use of nearly 8000 geo-referenced prevalence surveys dating since 1985 and model-based geostatistics to create a global map of P. falciparum endemicity in 2007. Apart from urban and peri-urban areas, it was found that there was no strong relationship with climate or environmental covariates, so these were not included in the model (Hay et al., 2009). Nonetheless, the geographical distribution shows good correspondence with maps based on other methods including reported incidence maps and with forest cover in the Indo-malay and Neotropic biogeographic regions as shown in Fig. 3.2 and Socheat et al. (2003).

Land use in India, 2001 Arable land: yellow Forests: dark green Non-agricultural use of land: dark brown Plantation: light green Scrub and grass: purple Unproductive land: Light brown Source: Environment Atlas of India, Ministry of Environment and Forest. Map data source Central Pollution Control Board(CPCB) and National Atlas and Thematic Mapping Organisation (NATMO) http://www.soeatlas.org/PDF_Map%20Gallery/Landuse.p df accessed 16 September 2009

N E

W

Jammu & Kashmir

N

S

E

W

Jammu & Kashmir

S

Himachal Pradesh Punjab Chandigarh

Himachal Pradesh Punjab Chandigarh

Uttaranchal

Haryana Arunachal Pradesh

Delhi

Delhi

Arunachal Pradesh Sikkim

Uttar Pradesh

Rajasthan

Uttaranchal

Haryana

Sikkim Assam

Nagaland

Bihar Meghalaya Jharkhand

Madhya Pradesh Gujarat

Uttar Pradesh

Rajasthan

Assam

West Bengal

Nagaland

Bihar

Manipur

Meghalaya

Tripura Mizoram

Jharkhand

Madhya Pradesh

Chhattisgarh

Gujarat

Manipur

Tripura West Bengal

Mizoram

Chhattisgarh

Daman & Diu Dadra & Nagar Haveli

Orissa

Daman & Diu

Maharashtra

API - 2001 > 10.00 5.01 - 10.00 2.01 - 5.00 1.01 - 2.00 <= 1.00

Andhra Pradesh Goa Karnataka

Orissa

Dadra & Nagar Haveli Maharashtra

Goa Karnataka

Pondicherry Kerala Lakshadweep

API - 2007 > 10.00 5.01 - 10.00 2.01 - 5.00 1.01 - 2.00 < 1.00

Andhra Pradesh

Pondicherry

Tamil Nadu

Kerala

Andaman & Nicobar Islands

Tamil Nadu

Lakshadweep

Andaman & Nicobar Islands

Malaria incidence in India, 2001 and 2007, as indicated by annual parasite index (API). Source: National Vectorborne Disease Control Programme, India, and WHO

FIGURE 3.2

Comparison of land use and reported malaria incidence in India in 2001 and 2007.

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3.3.2. Experiences in different geographical regions 3.3.2.1. Afrotropic region 3.3.2.1.1. General In nearly all of sub-Saharan Africa, malaria transmission is dominated by a pair of vectors, which are almost ubiquitous and often transmit malaria in tandem across seasons: An. funestus, which breeds in streams and shaded water bodies in rural areas, and the highly ramified and versatile An. gambiae complex, which occupies mainly temporary water bodies, preferably sunlit. An. arabiensis, which belongs to the An. gambiae complex, is common in relatively arid areas; it is often exophilic and zoophilic but is still a very efficient vector. A few vector species are locally important; they include An. moucheti, which is a main vector in some forested areas, and An. nili, which is found in various environments, usually with riverine breeding sites (Carnevale et al., 1992; Mouchet et al., 2004a; Sinka et al., 2010a). Exploiting the entomological homogeneity, the MARA/ARMA project (http://www.mara.org.za/) mapped malaria in sub-Saharan Africa based on climate suitability. A combination of rainfall and temperature was shown to correlate well with the distribution of malaria as shown by parasitological surveys; in most of the continent, low temperature correlated closely with altitude leading to unstable malaria in mountain fringe areas, mainly in Eastern Africa, and low rainfall with desert fringes in the Sahel and south-western Africa. However, in eastern South Africa, low winter temperatures limit the distribution of the malaria vectors, thereby defining a southern fringe related neither to altitude nor to desert climate (Craig et al., 1999). Epidemiologically, this setting has practically the same characteristics as mountain fringe further north on the continent (see below), with risk of epidemics and high population densities. Further investigations for East Africa including remote sensing, human settlement and land-use data at high spatial resolutions found that the best fit was obtained by stratifying the subcontinent into two ecological zones: one corresponding to highland and arid ecotones and the other corresponding to other rural areas. In addition, it was found necessary to distinguish urban areas, where malaria transmission was always lower than in rural areas with similar climate (Omumbo et al., 2005). Thus, this classification, which started out as climate-based, developed into being more physiography-based because of (a) the close correlation between physiography and climate and (b) the need to reckon urban areas as a special class, which is not distinguished by climate. As mentioned in Section 1.1, a typology for Africa has been proposed by Mouchet et al. (1993a); it has a slightly greater degree of differentiation, for example, between an equatorial zone and a tropical zone. The former would correspond to forest malaria and savanna malaria with perennial

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transmission, and the latter to savanna malaria with long seasonal transmission. However, the transition from equatorial to tropical savanna is gradual, as is also the transition from perennial to seasonal malaria. In fact, as reported in the same article, the transmission of malaria in the savanna environment is maintained at a low level during most of the dry season by An. funestus.

3.3.2.1.2. Savanna In the above analysis, the zone of rural areas with intense malaria transmission corresponds to savanna malaria. Depending on geographic region and especially rainfall and vegetation, there may be up to three extremely efficient vectors in savanna areas: An. gambiae s.s., An. arabiensis and An. funestus. Among these, the second is often, and the first sometimes somewhat exophagic and exophilic. Further investigation of such areas in western Kenya revealed a fragmented landscape mainly consisting of agricultural and domestic land uses within which breeding of malaria vectors was associated with certain land cover types, of largely agricultural origin, and close to streams (Mutuku et al., 2009). In arid savanna in Mali, it was found that NDVI correlated well with malaria incidence (Gaudart et al., 2009). It has been assumed that larval control has little potential in the African savanna environment, because the many diverse temporary habitats of An. gambiae are difficult to cover, while the breeding sites of An. funestus are often difficult to find and protect. Yet, a recent study in western Kenya found that the application of bacterial larvicides at a cost of USD 0.9 per inhabitant per year can lead to an epidemiologically significant reduction in biting density; however, the site had lower malaria transmission before intervention than is usually found in the savanna environment (Fillinger and Lindsay, 2006). 3.3.2.1.3. Forest The main vector is An. gambiae s.s., which in some forests is highly endophilic and therefore easy to control (Carnevale and Mouchet, 2001), but in others somewhat exophilic. The density is lower in forests than in savanna areas due to the requirement for sunlight (Mouchet et al., 2004a). Corresponding to earlier findings, for example, in Cameroon (Manga et al., 1997), a direct comparison between forested and deforested adjacent areas in Kenya found that vectorial capacity was higher in the latter, and this was attributed to higher temperatures and humidity levels (Afrane et al., 2008). In West Africa, very intense transmission with exacerbation during the rainy season may characterize the forest-savanna transition zone (Owusu-Agyei et al., 2009). 3.3.2.1.4. Highland fringe The epidemic pattern and temperature and rainfall influence were shown, for example, in Burundi (Gomez-Elipe et al., 2007). Altitude variations were shown to be important predictors

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of malaria transmission intensity in Zimbabwe (Mabaso et al., 2005). In Madagascar, the epidemic, highly unstable malaria on the high plateau at around 1000–1500m above sea level (a.s.l.) is now being controlled by IRS, but a recent investigation drew attention to the very high burden affecting all age groups almost equally in the nearby foothill area at around 900m a.s.l. (Rabarijaona et al., 2009). In Kenyan highland areas, water bodies identified by remote sensing predicted mosquito breeding and proximity to high-order streams the distribution of adult mosquitoes in houses (Li et al., 2008; Mushinzimana et al., 2006). Similarly, proximity to forest and swamps were both strong predictors of malaria in Kenyan highlands (Ernst et al., 2009). It was recently found in an area of moderate transmission intensity in the highlands of western Kenya, where ITNs were also introduced, that larviciding could reduce risk of malarial infection in children by 40%, almost the same as the protection afforded by nets (Fillinger et al., 2009). This is of considerable interest, because larval control has not in the past been considered to have much potential in such an environment, where breeding sites are abundant and diverse in the rainy season. Ethiopia has large populations without the typical markers of genetic resistance to malaria found in most other African populations; the highest population densities are found in highland areas, which are malaria free, but at risk of malaria epidemics. Following epidemics in the highland areas in 2003–2004, which, together with those in Ethiopia in 1959, are the worst malaria epidemics on record anywhere since 1950 (UNICEF, accessed 12 January 2009 http://www.unicef.org/ ethiopia/malaria.html; Fontaine et al., 1961), there has been increasing coverage of IRS and ITN and a steady reduction in reported malaria incidence.

3.3.2.1.5. Desert fringe It is generally assumed that breeding sites are scarce, dependent on rainfall and/or permanent water bodies, and therefore easy to control. In some texts, highland and desert fringe malaria are treated as one; while the epidemiological pattern is often similar with unstable malaria and higher age groups being vulnerable in contrast to the savanna situation, this overlooks important ecological and social differences: Highlands usually have abundant breeding sites, fertile soil and high population density enabling a health service infrastructure. Mosquito nuisance may be very low, and IRS therefore better accepted than ITNs. In contrast, in thinly populated desert fringe areas, the people are more often pastoralists constraining the provision of health care (Sheik-Mohamed and Velema, 1999). The proximity to cattle may lead to considerable insect nuisance and therefore motivation for the use of mosquito nets, but this may be constrained by seasonally or perennially high ambient temperatures, which is one reason for the

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preference for insecticide-treated curtains rather than mosquito nets in trials in Burkina Faso (Procacci et al., 1991). Yet, while it is clear that the Sahel and Namibia are mainly affected by desert fringe malaria and Burundi and Rwanda by mountain fringe malaria, it must be recognized that certain areas of Kenya, Ethiopia and other countries combine highland and desert fringe characteristics (Noor et al., 2009; Zhou et al., 2007). Recent studies in desert fringe areas do not always confirm received wisdom. In southern Somalia, a clear correlation between malaria and rainfall was found, but not between malaria and distance to permanent water bodies; in the country’s north, there were no significant spatial or climatic covariates, presumably because of data scarcity. Arid areas in Somalia are among the few in tropical Africa where larvivorous fish have been tried for malaria control; the intervention led to reduced larval density, but it was not investigated whether this led to lower malaria transmission (Mohamed, 2003). Similarly, a more recent controlled study in Eritrea showed significant reduction in the adult density of An. arabiensis (which, typically for an arid area, was the only vector) following environmental and chemical larval control (Shililu et al., 2007), but epidemiological impact was not assessed. The south-western part of the Arabian Peninsula belongs to the Afrotropic realm. The main vector is An. arabiensis, and most of the malaria in that area is highly unstable and rain dependent and can be classified as desert fringe. Mouchet et al. (1993a) distinguish Sahe´lien from savanna malaria by a duration of the rainy season of less than 5 months and propose a distinction between desert fringe (Sahe´lien) and actual desert malaria, where malaria transmission takes place only in some years. There is merit in this, but it is difficult to define the demarcation climatically or ecologically, and it would seem practical to treat desert malaria (which probably affects very few people) as a subtype under desert fringe malaria.

3.3.2.1.6. Coastal In Africa, the malaria vectors, An. melas and An. merus, which breed in brackish water (and belong to the An. gambiae complex), are less efficient than those typically found in the surrounding rural areas. Incidence may fluctuate widely when seasonal rains reduce salinity, thereby increasing vectorial capacity (Akogbeto et al., 1992). In Senegal in a coastal area, the malaria situation was characterized by seasonality, low level of transmission with all age groups affected and influence of man-made environmental changes (Diop et al., 2006). In the Senegal river delta, An. pharoensis, which is otherwise not considered an important vector outside Egypt, was identified as the main vector, and ITNs were highly effective there (Carrara et al., 1990).

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3.3.2.1.7. Urban Compared to people in savanna areas, urban populations in Africa, generally, have lower malaria transmission intensity with higher age maxima for morbidity and mortality. Generally, access to curative services is better. Using data from a number of studies, it was shown that there is a rising gradient of entomological inoculation rate (EIR) when moving from urban areas, where the value is typically 20 or less infective bites per person per year, over intermediate peri-urban areas to highly endemic rural areas with EIR values of typically 100–200 (Hay et al., 2005; Robert et al., 2003). The high level of heterogeneity of malaria in urban areas has been demonstrated in a number of studies (Machault et al., 2009) and is easily explained by the scarcity of breeding sites and the high population density. In Khartoum, there have been good experiences with larviciding in the first half of the twentieth century and again in recent years (Elkhalifa et al., 2008). The effect of larviciding was demonstrated recently in Dar es Salaam (Geissbuhler et al., 2009), but there are few other demonstrations of the value of larval control in African cities. In many cases, urban malaria in Africa is due to interspersion of areas with urban and savanna characteristics, so breeding may not be technically easier to control than in rural areas. Recently, it has been observed that increased vector breeding in polluted water and artificial containers, earlier biting, and increased exophily could compromise the expected mitigation effect on malaria of urbanization (Saugeon et al., 2009). A tendency of An. gambiae s.l. in Accra to breed in domestic containers and polluted water was noted already in the 1980s, but it was not clear whether this was a genetic adaptation or a partial replacement of An. gambiae s.s. with An. arabiensis (Chinery, 1984). There is clearly a need for longitudinal studies on possible vector adaptation to urbanization and on ways to deal with it. The serious mosquito nuisance in many urban areas (Carnevale and Mouchet, 2001) and the risks of various arthropod-borne diseases should facilitate effective promotion of house screening and mosquito nets. 3.3.2.1.8. Agricultural development Wet-rice cultivation is rapidly increasing in Africa and there has been concern about the potential impact on malaria. In the savanna zone in Coˆte d’Ivoire, rice cultivation induced moderate changes in the seasonality of malaria, but no increase in EIR or morbidity. In northern Tanzania, rice irrigation was associated with less malaria than alternative agricultural practices, despite the high vector productivity in the paddies (Ijumba et al., 2002; Keiser et al., 2002). Even in the semi-arid sub-Saharan environment in Mali, rice cultivation altered transmission from seasonal to perennial but reduced annual incidence more than twofold (Sissoko et al., 2004). In a study investigating the interactions between environment, vectors, human ecology, health system and disease, biannual irrigation rice harvesting, when compared to

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annual, was associated with changing gender roles, lesser availability of cash for women and consequently poorer health seeking behaviour; however, the situation might look different in a drought year, where the biannual rice harvest could improve food security (de Plaen et al., 2004; Henry et al., 2003). In contrast, studies in a highland area in Burundi showed clearly increased risk (Coosemans, 1991) and in Ethiopian highland areas, malaria morbidity was greatly increased near dams (Brewster, 1999). The effect of rice cultivation was also serious in a forest zone, where the vector density is normally low (Briet et al., 2003). Possibly, the most serious negative effects of irrigation in Africa were seen in the arid conditions of Gezira, Sudan, where eventually malaria was controlled by IRS. Subsequently, epidemics followed the relaxation of control and the development of insecticide resistance related to the use of DDT for cotton cultivation and subsequently malaria was controlled again by IRS with newer insecticides; various forms of larval control were attempted but never proved effective (el Gaddal et al., 1985; WHO, 1985). In urban areas, rice cultivation is associated with high anopheline densities, but it is not clear whether it leads to more malaria than there would otherwise be (Dongus et al., 2009; Matthys et al., 2006). Thus, in ecosystems with relatively low transmission intensity in Africa, irrigation usually leads to increased transmission, while in savanna areas, it has little impact on malaria burden although it may be associated with increased vector density and a shift towards greater perennity. This ‘paddies paradox’ is sometimes attributed to conditions favouring less efficient vectors, but it may also be explained by increased biting rates motivating people to use protective measures and by communities near irrigation schemes benefiting from greater wealth and better access to health care (Ijumba and Lindsay, 2001; Keiser et al., 2005b). Modification of water management practices in irrigation schemes may have limited potential in most of Africa, as water is generally scarce. In Mwea in Kenya, where An. arabiensis is the main vector, intermittent irrigation at four-day intervals did not have a significant impact on mosquito densities (Mutero et al., 2000). As An. arabiensis often emerges as the main vector in rice-field areas, it is possible that the potential of zooprophylaxis could be better exploited (Mutero et al., 2004). Generally, the extensive descriptive literature on malaria and irrigation in Africa contrasts with a paucity of trials of larval control. The serious malaria problem at Zambia’s copper mines in the 1920s shared its main characteristics with malaria in agricultural development projects. The well-documented success in reducing it mainly through environmental management 60–80 years ago is a reminder that such methods may play an important role in some settings dominated by African malaria vectors (Utzinger et al., 2001).

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Madagascar has the same main malaria vectors as continental Africa, but their bionomics are different. In the highlands, irrigated rice fields are the main determinant of malaria, with An. funestus as the main vector with the highest densities, when the rice is close to harvest providing shade (Mouchet et al., 2004a). In the southern lowlands, irrigated rice fields in arid zones, which could be classified as desert fringe, also have greatly increased malaria (Laventure et al., 1996).

3.3.2.1.9. War and socio-political disturbance The particular problems of malaria related to war and political disturbance are easily understood, considering the main feature of degradation of health systems. To this may be added housing problems, environmental damage and migration of populations with varying malaria exposure. New approaches and technologies are being developed to deal with these problems (WHO, 2005).

3.3.2.2. Australasian region This region includes the easternmost part of the Indonesian archipelago, New Guinea Island, Solomon Islands, Vanuatu, New Caledonia, Australia and New Zealand. It has a region-specific anopheline fauna in New Guinea, Solomon Islands, Vanuatu and northern Australia; in contrast, the malaria vectors in the eastern part of the Indonesian archipelago are Indo-malay with the exception of Maluku islands (the Molucas) (Mouchet et al., 2004a; Ndoen et al., 2010). New Caledonia and New Zealand have always been malaria free, like Oceania, probably because malaria vectors have never spread there. Malaria has been eliminated from Australia except for the Torres Strait Islands near Papua New Guinea. Malaria in New Guinea differs from typical Afrotropic malaria by generally somewhat lower transmission intensities and the importance of P. vivax along with P. falciparum. The vector system is quite different and exceptionally complex. There are three main vectors, all belonging to the An. punctulatus complex: An. farauti, in itself a species complex, is responsible for coastal malaria. It is sometimes associated with brackish water, sometimes with swamps further inland; in fact, some subspecies of An. farauti and newly recognized species resembling it are important in highland areas. An. koliensis is highly opportunistic and occupies breeding sites in inland plain areas, which could be considered savannas or foothills. An. punctulatus is also widespread and considered the main vector in highlands. Generally, vector density is highly clustered and correlates with proximity to rivers or swamps and man-made environmental disturbances (Hii et al., 1997). However, the ecology and distributions of the sibling species are not well understood, and vector systems may vary considerably from one village to the next and even within villages (Muller et al., 2003).

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Malaria in coastal plains is hyper- to holoendemic with the main burden concentrated in young children. Transmission becomes unstable at altitudes of 1300–1600m and ceases above 1700–1800m. Like in Ethiopia and Madagascar, a large proportion of the population is concentrated above the usual limit of transmission of malaria. At altitudes from 200 to 1200m, the population density is lower than in the coastal plain, and this has been ascribed to the high malaria risk affecting all age groups (Muller et al., 2003). The emergence of malaria in economic development projects, mainly mines and plantations, has been described repeatedly in Papua New Guinea (Pluess et al., 2009; Radford et al., 1976). Usually, these situations are characterized by population movements, where immune parasite carriers encounter non-immunes from non-endemic areas combined with the creation of man-made breeding sites. From New Guinea to Solomon Islands and onwards to Vanuatu, ecological diversity, vector diversity and transmission intensity decrease. Most of the malaria in the eastern parts of this region can be described as coastal, and there are some highly circumscribed examples of environmental management as a supplementary control measure (Schapira, 2002). The particular opportunities and challenges related to malaria control in estuaries, particularly stream rectification, have been discussed by Ford (1949).

3.3.2.3. Indo-malay region 3.3.2.3.1. General This realm stretches from Pakistan to the Philippines and from the Himalayas to Java (Rao, 1984). With subregions separated by seas and mountain chains and precipitation levels varying from 0 to over 3000mm per year, it harbours immense biodiversity (Trung et al., 2004). There is a gradient of increasing rainfall from west to east with major implications for ecosystems, vegetation and malaria vector bionomics. In most of Pakistan and peninsular India, the main vector is An. culicifacies. It is mainly found in agricultural areas, stagnant or flowing water including rice fields, as well as tanks and ponds. In urban areas, it may be sympatric with An. stephensi. In Sri Lanka, it is more specialized, preferring ponds along rivers, causing epidemics mainly in the dry season. It has been considered a zoophilic and inefficient vector, but newer investigations indicate that one subspecies, E, is anthropophilic and potent. Subspecies A and C are also vectors, while B is practically refractory to malaria infection (Barik et al., 2009). A number of species such as An. aconitus, An. annularis, An. maculatus, An. sinensis and An. superpictus are primary or secondary vectors in rural areas, often breeding in rice fields or streams, but rarely pose a major challenge to control efforts (Beales, 1984). An. fluviatilis is the main vector in monsoon forest and hills in eastern India and in the Western Ghats. Its subspecies S is an anthropophilic,

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efficient vector, which is endophagic, but not always endophilic (Rao, 1984), while subspecies T and U are weak, zoophilic vectors. The related An. minimus (Chen et al., 2006) is an important vector in the Indochinese peninsula, southern China, Bangladesh, Nepal and Northeast India, where it is abundant in hilly as well as forested areas, being exophilic to a variable extent. It is sometimes highly zoophilic (especially subspecies C) and then probably unimportant as a vector (Van Bortel et al., 2004). The main vector in forested areas in the Philippines and parts of Indonesia, An. flavirostris, is closely related to An. minimus. The An. leucosphyrus complex includes several species, which are potent, anthropophilic and exophilic vectors, found in the rainforests of Indonesia and Malaysia. The closely related, even more efficient as well as highly exophilic An. dirus species complex is found in rain forests in the Indochinese peninsula, Northeast India, eastern Bangladesh, Yunnan Province in China, but not peninsular India (except subspecies E, which does not transmit human malaria) (Kalra, 1991; Rao, 1984). It breeds in shaded stagnant water collections with density increasing after rains. The An. sundaicus species complex is found in coastal areas from eastern India over the Indochinese peninsula to Indonesia. The vectorial status varies from place to place, but the efficiency is never high (Manguin et al., 2008).

3.3.2.3.2. Plains with traditional agriculture except irrigated rice In rural areas in India and Pakistan, malaria was historically endemic, but focal and unstable with wide exacerbations related mainly to climate and population movements. Nowadays, the recorded malaria incidence in non-forested rural areas is generally below 2 per 1000 per year. In these areas, IRS is now mainly used reactively, while various methods for larval control are used with the intention of minimizing receptivity (Ghosh et al., 2005; Sharma 1999). The transmission that occurs is often related to migrant farm labourers from forested areas in eastern India. In Sri Lanka, rural malaria is related to An. culicifacies breeding in pools along streams. A recent study indicated that an intermittent flush system might deal cost-effectively with the vector breeding, though it would be necessary to be cautious not to create breeding sites for An. varuna, which prefers flowing water (Konradsen et al., 1998). However, An. culicifacies is the only widespread vector in Sri Lanka, which, for the second time in its history, is approaching malaria elimination (WHO, 2008). In Indonesia, a study in a rural area of Java found a distinct association between certain land-use classes and the presence of malaria vectors, as follows: Rice paddy was associated with An. aconitus and An. subpictus, plantation near human settlement with An. maculatus, bush/shrub with An. aconitus, An. maculatus and An. sundaicus and bare land and water

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body land use on the coast with An. sundaicus (Stoops et al., 2008). All these vectors are inefficient in Indonesia and nowadays rarely associated with any transmission. Likewise in the rest of Southeast Asia, malaria is nowadays rare in undisturbed, socially stable plain areas.

3.3.2.3.3. Forest, forest fringe, deforestation, foothills Tropical rain forest is mainly found in the Indochinese peninsula including northeast India, Indonesia, Philippines, southern China and Western Ghats, while monsoon forest with wet and dry seasons of almost equal duration predominates in other parts of India, especially eastern peninsular India. It has been estimated that out of the national total, the following percentages of recorded malaria cases were forest related in 1989: Bangladesh 87%, India 31%, Indonesia 44%, Nepal 49% and Thailand 42% (Sharma et al., 1991). While western India has important malaria burdens in certain rural and especially urban areas (see below), malaria in eastern and Northeast India and Bangladesh is largely dependent on the presence of forest and hill (stream-breeding) vectors. The proportion of the malaria burden including malaria mortality, which is forest related in India, is likely to have risen considerably since 1989 (Fig. 3.2). Throughout South and Southeast Asia, forest malaria is determined by the convergence of several or all of the following factors: High vectorial capacity with vectors often exhibiting exophily, exophagy and early biting; economic rewards of forest activities (logging, fuel wood, gem mining), sometimes at night (smuggling, frog hunting); transmigration, as in eastern Indonesia, where large populations with no previous malaria exposure are settled near forests; low population density associated with poor road access and rudimentary health services. Often the malaria problem is most visible among migrants and to some extent in forest fringe villages, while it may be neglected and more severe in ethnic minority groups in villages surrounded by forest (Erhart et al., 2004; Harijani and Arbani, 1991; Kondrashin et al., 1991; Shrestha et al., 1991). Depending on several factors, especially patterns of mobility and control measures, malaria may be transmitted in the forest and in fringe villages (Trung et al., 2004) or only inside forests (Sanh et al., 2008). The contrast between forest villages and plain areas in eastern peninsular India was measured in Sundergarh district, Orissa, where annual malaria incidence in forest villages was 347.9 per 1000 with mainly children affected against 61.0 in plain villages with all age groups equally affected (Sharma et al., 2004). The following subtypes of forest-related (tribal) malaria have been identified in India: i. Hilly rain forest and tropical rainforest of North-Eastern States, where An. dirus is the main vector.

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ii. Hilly deforested cultivated areas in the Northeast, where An. minimus and An. dirus supplement each other so that the transmission may be more intense and prolonged than inside the forest. iii. Undulating deforested areas with rice cultivation in the Northeast with lower levels of transmission by An. minimus, An. fluviatilis and An. nivipes. iv. Deciduous forest in eastern peninsular India. An. fluviatilis is the main vector, and the seasonal transmission can be controlled if IRS can be implemented. In the rain forests of the western sub-Himalayan Region in Nepal, the short transmission season makes control easier. v. Deforested areas with An. culicifacies and An. fluviatilis. Transmission is more prolonged and control more difficult, as An. culicifacies is often insecticide resistant and bites early (Sharma et al., 1996). Figure 3.2 compares the spatial distribution of malaria and forest cover in India from 2001–2007. While the correlation is obvious, the exceptions to the rule are of particular interest. The severe malaria problem in Rajasthan and to some extent Gujarat in the beginning of the decade in desert fringe areas is now under a degree of control. In the forest belt in the Himalayas, the short-season transmission seems to have been controlled. In the easternmost parts of Northeast India, some forested areas are likewise not highly endemic, because of high altitude, but in others, the health services are constrained by terrain and unrest so that malaria is more underreported than elsewhere. That explanation would not be valid for the forests in Western Ghats in Karnataka and the Tamil Nadu states, which have relatively strong health systems. Possibly, the health services in those states have been able to deal effectively with the malaria problem except for small residual foci; this would give cause for optimism for forest malaria in eastern India, where the vectors are the same. In Thailand, Myanmar, eastern Bangladesh, western Cambodia and southern Laos, more than in India and Vietnam, there is usually a close association between forests and the An. dirus complex. This vector may also be present in fruit orchards, but at lower density than in forests (Obsomer et al., 2007; Oo et al., 2003; Rosenberg and Maheswary, 1982). While GIS has been used as in Fig. 3.2 to illustrate the overlap between malaria, forests and ethnic minority groups (Kidson et al., 1999; Mouchet et al., 2004a), there have been few rigorous spatial studies of malaria and environment in Southeast Asia. A national malaria survey in Cambodia in 2007 was restricted to populations living in forests and within 5km from the forest border. Distance to forest as identified on land-use maps was highly correlated with malaria prevalence, with very low levels of infection in populations living more than 2km from the forest border. A similar pattern was found using MODerate-resolution Imaging

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Spectroradiometer (MODIS) vegetation index data, especially Enhanced Vegetation Index (EVI) and Normalized Difference Vegetation Index (NDVI) to identify forest-covered areas (Cambodia Malaria Survey, 2007). It was found that remote-sensed data may be more useful than landcover maps, as they are continuously updated, have temporal and spatial resolution well suited to national level analysis and are free (J. Cox, personal communication). Also in Cambodia, regression analysis identified adults and males involved in forest activities as high risk groups, with additional risks for children in forest-fringe villages. Villages displaying the highest malaria rates were clustered along roads or tracks penetrating into recently colonized forested areas (Incardona et al., 2007). Similarly, in Bangladesh in the Chittagong Hill Tract, houses located less than 3km from forest had higher malaria risk, while the malaria risk was inversely related to distance to water bodies (Haque et al., 2009). In Vietnam, an analysis of district level data (which is far from ideal for such ecological studies, as districts in that country have populations of about 100,000 and may comprise a variety of landscapes) found significant association between malaria, poverty and percent forest cover, though with substantial residual spatial heterogeneity (Manh et al., 2010). Other studies have explored the determinants of malaria in or near forested areas in greater depth and less quantitative precision. In northern Thailand, land-poor families practice swidden farming inside forests, where they are infected by An. dirus, and carry parasites to their villages in the fringe for transmission by An. minimus. Lack of roads limits access to markets, and rice fields in these upland areas have low productivity, so people diversify agriculture, increasing their exposure in forests. The illegal character of some forest activities creates a further obstacle to access to the health services (Singhanetra-Renard, 1986). There are very few reports of larval control in areas of forest malaria (Singh et al., 1989). An elaborate scheme was successfully applied for protecting a large contingent of soldiers in northeast India during World War II (Afridi, 1962). A more recent study was done under more normal conditions in an area with An. fluviatilis and An. culicifacies, and the environmental control measures were probably effective against the latter (Singh et al., 1989). It is often stated that IRS is ineffective in forest malaria because of the exophily, but there are experiences indicating some effect (Institute for Malariology, Parasitology and Entomology for Central Vietnam, Qui Nhon, Vietnam, unpublished data), which is not surprising, since exophily usually does not mean that all mosquitoes always rest outside houses, and some people living in forests have houses with sprayable walls. When ITNs were introduced, there were high hopes that they would solve the problem of forest malaria. However, the forest malaria problem cannot be reduced to entomology, and even in the best of circumstances, their effect would be constrained by exophagy and early

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biting. A cluster-randomized trial of conventional ITNs in Cambodian forest villages suggested a reduction of around 30% of malaria incidence and prevalence (Sochantha et al., 2006), while an entomological trial of long-lasting insecticidal hammock nets indicated good protection against the bites of An. minimus, but much less against An. dirus (Sochantha et al., 2010). In Vietnam, a community-randomized trial in forest and forest fringe villages found that incidence in villages provided with long-lasting insecticidal hammock nets was reduced twice as much as in villages without this intervention (Thang et al., 2009).

3.3.2.3.4. Deforestation Deforestation in South and Southeast Asia seems to lead to lower malaria risk in most cases. In Orissa, in eastern peninsular India, the highly anthropophilic and efficient vector, An. fluviatilis S, was very rare in deforested riverine villages, but common in forested hilly villages, with higher malaria burden. It was not clear, however, whether the more hot and dry deforested riverine area would have been more malarious if forest cover had been maintained (Nanda et al., 2000). 3.3.2.3.5. Foothills In Assam, in Northeast India, in hilly deforested areas, An. minimus, breeding in perennial seepage streams, may still be an important vector, responsible for indoor transmission in these areas and in tea gardens (Dev et al., 2004). A recent study from Quang Tri Province in Vietnam, where the physiography is more foothill than forest, presented the health system problems impeding control in a remote thinly populated ethnic minority area (Morrow et al., 2009). Such findings suggest that the malaria ecotype previously classified as Indochinese hills malaria (Macdonald, 1956) should be re-instated. 3.3.2.3.6. Highland fringe In much of Southeast Asia, the highest malaria risk is found at altitudes between 300 and 800m a.s.l., where vectors belonging to the An. fluviatilis-minimus and/or dirus-leucosphyrus groups abound depending on the character of the forest. At higher altitudes, the environment is usually less hospitable with very low population density so that relatively few people are exposed to epidemic risk; however, certain areas in Laos and northern Vietnam above 1500m are settled by the Hmong ethnic group, relatively recent immigrants from China, who traditionally fear disease at lower altitudes (Lewis, 1951). In the recent past, forced resettlement of these in endemic foothill areas has led to malaria epidemics (S. Hoyer, personal communication). 3.3.2.3.7. Desert fringe The north-west of India, especially Rajasthan State, and parts of Pakistan are semi-desert. These areas have been known for many years for serious epidemics related to unusually heavy rainfall and to development projects. A study in 2006 found that not only

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was importation of cases the most important determinant of malaria but also excessive rainfall and low cattle-to-human ratio ( Joshi et al., 2006). In some areas, An. stephensi is the most important vector, resting mainly in storage tanks with the implication that IRS may not be ideal, larval control becoming more important (Sharma et al., 1996). Due to the high summer temperatures, it may be very difficult to motivate the population to use mosquito nets (R.K. Das Gupta, personal communication).

3.3.2.3.8. Coast Coastal malaria transmitted by vectors that tolerate brackish water has been important focally in Indonesia, Malaysia, Philippines and Viet Nam, and to a lesser extent, Cambodia, Thailand and India (Poolsuwan, 1995). The main vectors belong to the An. sundaicus complex including An. sundaicus s.s., An. epiroticus in Vietnam and An. litoralis in southern Philippines and Sabah, Malaysia. The optimal levels of salinity corresponding to between 3% and 50% sea water would generally be found in areas with man-made disturbances of the environment (Trung et al., 2004). Coastal malaria in Vietnam is nowadays related to shrimp farming in areas south of Ho Chi Minh City (Erhart et al., 2004). Over the 10-year period from 1992 to 2002, there was a dramatic reduction in malaria transmitted by brackish water breeders in the Vietnamese part of the Mekong Delta. The reductions could be ascribed to high levels of coverage with ITNs and widespread availability of treatment with artemisinin derivatives. Desalination may also have played a role. Between 1992 and 2001, at a cost of 12 billion US dollars, tidal floodgates were installed on the major rivers and canals and secondary canals were dredged in an effort to prevent seawater intrusion into the low-lying Ca Mau Peninsula. The purpose was to improve agricultural productivity (White, 2009); as a side effect, it may have helped reduce the malaria risk. Although the threat of coastal malaria was evident in the Andaman Islands after the tsunami in 2004 (Krishnamoorthy et al., 2005), it has, generally, lost its former importance in Asia. There may be several explanations for this; coastal vectors are not very efficient and they are largely endophilic (the vegetation probably does not provide suitable resting places), so IRS and ITNs should work well; high population density and economic development allow good access to curative care. A consequence of the low burden is that environmental management, which celebrated some of its greatest triumphs in coastal areas in the past (Takken et al., 1990), may now rarely be cost-effective, except when required for other purposes by other sectors. Coastal malaria is still important in the easternmost part of the Indonesian archipelago, for example, in West Timor, where the vectors are An. subpictus, and possibly An. barbirostris and An. maculatus (Ndoen et al., 2010).

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3.3.2.3.9. Urban Urban malaria in Asia is practically restricted to the Indian subcontinent, from Karachi in the west to Kolkata in the east. It is a consequence of the adaptation of An. stephensi and to some extent An. culicifacies to breeding in artificial containers. Already by 1903, malaria was recognized as a serious public health problem in Mumbai; anti-larval measures were associated with near interruption of transmission there in the 1940s, but it was in the 1970s that urban malaria emerged as a major problem in India, the burden often being higher in the cities than in the surrounding countryside (Rao, 1984). Thus, in the region of Mewat in Gurgaon district, Haryana state, the burden was highest in the urban area despite important breeding sites for An. culicifacies in the surrounding areas classified as irrigation, water catchment, mining and flood prone (Srivastava et al., 2004). One of the reasons for the resilience of the problem is that urban An. stephensi, though mainly endophilic, cannot be controlled by IRS because of its tendency to rest on the inside walls of wells and containers and because IRS is not possible in multi-storey buildings with basements, etc. (Hyma et al., 1983). Control must therefore rely mainly on sanitation supported by public works and health education, chemical and biological larviciding and personal protection. Urban malaria in India is currently considered a serious problem in 131 cities with about 10% of the country’s population. Between 2000 and 2007, the number of reported cases in these cities was reduced from 172,000 to 106,000 and urban malaria now accounts for about 7% of all recorded cases in the country. None of the affected Indian cities has become malaria free yet. The challenge is intersectorial and includes also the control of parasite carriers, who move from poverty-stricken rural areas to cities in search of employment. It must be addressed together with other vectorborne diseases and insect nuisance (National Vectorborne Disease Control Programme, 2009). There is no urban malaria problem in the Indochinese peninsula (Oo et al., 2002). The only major environmental difference between Indian and Southeast Asian cities, is to the writer’s knowledge, the higher air humidity in the latter, but it is not clear whether that can explain the important difference in anopheline fauna. 3.3.2.3.10. Agricultural development including plantations Two major types of agricultural development are particularly important: cultivation of irrigation rice and tree plantations. The use of river water for irrigation of rice fields goes back at least 3000–5000 years in East, Southeast and South Asia, and should therefore be considered as traditional agriculture in those regions. In most of Southeast Asia (Philippines, Vietnam, Cambodia, Laos, Thailand and Myanmar), malaria is virtually absent in the heavily populated flood

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plain areas, where rice is harvested from one to four times a year. Rice fields in these countries may harbour various anopheline species, often at high density, but there is hardly any malaria transmission. An. minimus, an important vector in hilly areas in most of the Indochinese peninsula, can be found near rice fields in ditches and canals but rarely transmits malaria in those areas (Meide et al., 2008). Even close to the forest fringe in Thailand, rice field areas seem almost free of malaria (Kondrashin et al., 1991). In Bangladesh and West Bengal in India, land-use changes and increase in population density led to reduced production of An. philippinensis from ponds, tanks and marshland so that malaria more or less disappeared from the plain areas, although An. annularis and An. aconitus emerged as rice field breeders, occasionally causing low-level transmission (Elias, 1996). In Indonesia, irrigated rice has been associated with malaria transmission, with An. aconitus as the main vector, for example, in Java and Bali (Harijani and Arbani, 1991; Konradsen et al., 2004; Worth and Subrahmaniam, 1940), but this is apparently not a problem at present. In India, An. culicifacies breeds more in irrigation canals than in the paddy and has, in some cases, been controlled by flushing (Russell and Knipe, 1942) and intermittent irrigation. In Central India, An. annularis, breeding in irrigation canals, may play a role (Singh and Mishra, 2000), and in Sri Lanka the introduction of irrigation in a dry forest zone led to the emergence of this otherwise insignificant species as an important vector (Ramasamy et al., 1992). In most areas of Sri Lanka, rice-field irrigation is no longer an important source of effective vectors; in contrast, irrigation malaria remains important in the arid north-west India (Kondrashin and Kalra, 1989). It is striking that irrigated rice cultivation is so closely associated with malaria in the western part of the region and not at all in Southeast Asia. Some factors in human ecology could play a role, such as the almost universal use of mosquito nets in Southeast Asia and the traditional habitation on stilts, but the ethnic Vietnamese (Kinh) build their houses on the ground. One important factor in arid areas could be the need for extensive canals, which may be more important as vector breeding sites than the rice fields per se. Also, anophelines in arid areas are advantaged if long lived, able to fly far and to aestivate and/or hibernate. The Southeast Asian counterparts are physiologically adapted to humid conditions having wider spiracles. They cannot fly far (Rao, 1984), but they might be more competitive in the humid ecosystems by investing in large numbers of offspring to the detriment of longevity, and thereby vectorial capacity (A. Kiszewski, personal communication). In hilly areas, rice fields are not always so innocent. Malaria continues to occur in hilly rice-field areas in Java and West Timor in Indonesia. The most common vector species in these areas are An. annularis, An. vagus and An. subpictus, but it is not certain which of them is important in this

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environment (Ndoen et al., 2010). In contrast, there is almost no malaria nowadays in wet-rice areas in hills in Philippines and Vietnam. A number of studies in areas where malaria is associated with agricultural and other development projects, mainly in western India, indicate that ‘bio-environmental control’, that is, larval control through the use of larvivorous fish and/or environmental management, can be very effective (Dua et al., 1988, 1991, 1997; Ghosh et al., 2005; Konradsen et al., 1998). However, proof from randomized controlled trials is absent. In fact, that kind of evaluation is very difficult in such environments, where malaria is focal with characteristics varying from one site to the next (Sharma and Sharma, 1989).

3.3.2.3.11. Tea and tree plantations For more than a century, tea gardens in India have been infamous for malaria, ascribed more to high population mobility and poor health care than to high vectorial capacity (Christophers and Bentley, 1911). In the Indochinese peninsula, rubber, tree and fruit plantations have often been associated with breeding of efficient vectors. In Sarawak in Malaysian Borneo, deforestation and development of an oil palm plantation were associated with a change in fauna and a major reduction of malaria transmission, but then this study was not carried through to the full maturation of the oil palms (Chang et al., 1997). Thus, tree plantations offer opportunities for breeding of the notorious Asian forest vectors depending on the extent to which they imitate their natural environment. Population mobility becomes a major determinant of the malaria burden. Good health services, which would be expected at plantations, can mitigate the problem, but the ample availability of cheap labour is a constraint. One of the writers (AS) was told in a Cambodian rubber plantation in 1995 that workers often avoided approaching the free health service for fear of being recorded as sick and losing income. They preferred to avail themselves of medicine from private pharmacies and toil on with a fever. 3.3.2.3.12. War and socio-political disturbances Several articles were written a few decades ago about the malaria situations among refugees in the Indochinese peninsula (Baker et al., 1987; Meek, 1988; Meek et al., 1986), and presently, the worst malaria situation in that subregion is in Myanmar, which is still affected by chronic conflict in peripheral forested areas (WHO, 2009). In the past, the arid North-West Frontier Province in Pakistan had the lowest malaria incidence in the country, but in 2001, when the area had been affected by warfare and its social and environmental effects for two decades, the highest (Kazmi and Pandit, 2001).

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3.3.2.3.13. Stratification in India and Vietnam India, Thailand and Vietnam are among the countries with the longest continued experience in stratification as a tool for national level planning and replanning of control. For reasons of space, only two of these schemes are summarized here. A description of the Thai scheme, which has similarities with both of them, is easily accessible (Malaria Control Programme in Thailand. Ministry of Public Health of Thailand http://unpan1.un.org/intradoc/ groups/public/documents/APCITY/UNPAN009706.pdf). Since 1935, malaria researchers in Vietnam have proposed five stratification schemes of the country referring to altitude, forest cover, migrations and influence of brackish water. These schemes have illustrated malaria and its determinants, but the data to define the exact geographic confines and the populations of those strata were not available and there were no major control implications (National Malaria Control Programme, 2004; Phan, 1998). In 2003, the national malaria control programme established a classification as follows: 1. Without malaria transmission. 2. Risk of malaria resurgence: Former endemic area without local transmission during past 5 years. 3. Low malaria endemic: Malaria morbidity rate 1–5 per 1000 persons per year. 4. Moderate malaria endemic area: Malaria morbidity rate 5–10 per 1000 persons per year, P. falciparum proportion <70%. 5. High malaria endemic area: Malaria morbidity >10 per 1000 persons per year and P. falciparum proportion >70%. Morbidity rates include confirmed and unconfirmed malaria, where the proportion of confirmed has been increasing in recent years. Each of these classes is further characterized by landscape, altitude, population movement and vector species, and they have clear implications for interventions and surveillance. In category 3, for example, there is no vector control except for promotion of mosquito nets, which are to be insecticide treated, if and only if the area borders an area of higher risk. With morbidity data, the 10 529 communes of the country were classified by this scheme in 2003 allowing a quantification of target populations for interventions, although it was recognized that the size of migrant populations at risk remained uncertain. The framework is meant to be flexible in such a way that the quantitative epidemiological criteria for decision-making are modulated locally by the mentioned contextual factors. In India, the control experiences of the early twentieth century were formulated as typologies during the years of reorientation from eradication to control: urban, irrigation, rural, tea gardens, railway and coal fields

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(Pattanayak et al., 1994), later distilled as: tribal, rural, urban, industrial and border. Responding to an external evaluation in 1985, it was attempted to use 14 variables to divide the country in to seven strata, but it was impossible to collect the data at a fine enough scale, and this approach was abandoned (Sharma et al., 1996). In the 1990s, as the programme experienced a number of setbacks, it was proposed to go back to a simple typology of epidemic-prone, tribal, project and urban and within each of these define epidemiological criteria (annual parasite incidence (API), slide positivity rate, slide P. falciparum rate, epidemics), for control measures, and provide some indication of subtypes and their control implications. For current national- and state-level malaria control planning in India, stratification is in practice based on API, supplemented by some other criteria (slide positivity rate replacing API if the blood examination rate in a given area is low, high P. falciparum proportion, worsening malaria situation and extensive population movement). As a general rule, areas with API above 2 per 1000 are classified as high risk and therefore eligible for full coverage with IRS or (recently) ITNs (Directorate of National Vector Borne Disease Control Programme, 2009).

3.3.2.4. Neotropic and Nearctic regions 3.3.2.4.1. General Malaria is no longer endemic in the Nearctic except for some areas in northern Mexico, where vectors and ecology are no different from further south within the Neotropic realm; there is therefore no separate description of the latter. The most important vectors and their characteristics can be summarized as follows: An. darlingi is efficient, anthropophilic, endophagic and widespread in tropical lowland areas in South America and parts of continental Mesoamerica. It breeds mainly near rivers and is sometimes described as preferring shaded conditions, sometimes as sun loving. In open plain areas, it is mainly endophilic, but in forest areas, highly exophilic. Recently, An. marajoara has emerged as an important lowland vector associated with wetlands, secondary forests and human intervention (Sinka et al., 2010b). An. nuneztovari is also a widespread lowland vector, which is less closely associated with forests. It can be anthropophilic or zoophilic and its importance as a vector is variable. An. albimanus and An. aquasalis are exophilic, zoophilic and relatively ineffecient vectors, which may attain very high densities in coastal plains, the former near the Pacific, the latter mainly by the Atlantic and the Caribbean. An. pseudopunctipennis prefers stagnant, sun-exposed water, especially ponds along rivers with filamentous algae and occurs from low to very high altitude. The subgenus Kerteszia includes a number of vectors associated with bromeliads (see forest malaria below) (Mouchet et al., 2004b; Sinka et al., 2010b).

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Rubio-Palis and Zimmerman, using mainly South American data, explored climatic factors, vegetation, elevation and landform in accordance with Bailey’s ecosystem geography (Bailey, 1996) to describe five malaria vector ecoregions, where homogeneity of these factors could be related to vector density and distribution: coastal, piedmont, savanna, interior lowland forest and high valleys (Rubio-Palis and Zimmerman, 1997). The following review of Neotropic malaria follows this typology (Fig. 3.3).

No transmission API <10 API 10-49 API>=50

FIGURE 3.3 Malaria risk as measured by annual parasite index (API) by municı´pio in Amazonia legal, 2007 (Source: Ministry of Health) http://portal.saude.gov.br/portal/ saude/profissional/area.cfm?id_area¼1526) and vegetation and deforestation in the Brazilian Amazon, 2002 (Source: Human Pressure on the Brazilian Amazon Forests March 2006. World Resources Institute/Imazon http://www.globalforestwatch.org/ common/pdf/Human_Pressure_Final_English.pdf).

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3.3.2.4.2. Savanna Savanna landscapes with seasonal and variable rainfall are found at elevations from less than 100 up to 1500m with variable rainfall, but always a dry season lasting at least 5 months. Malaria is or was localized to the more humid areas and transmitted by An. darlingi or An. nuneztovari. It has now largely been eliminated by IRS from this ecoregion. 3.3.2.4.3. Interior Lowland Forest Forest malaria in South America was aptly described by Giglioli, bringing out the convergence of determinants, which makes this malaria system so resilient: ‘‘. . .The reasons for this failure of our eradication campaign in the remote interior. . .can be easily summarized. 1. The difficulty of locating all camps and habitations in the forest. 2. The habitual and frequent displacements of the Indian population from their permanent settlements to temporary shelters and camps on their farms in the forest. 3. The exophily of An. darlingi and its persistence in semi-inhabited forest. 4. The lack of adequate sprayable surfaces in rudimentary house structures used on the farms and in the bush camps. 5. The difficulty of access, particularly in the wet season, when flooding interrupts lines of communication, and in the dry season, when the upper reaches of many rivers become unnavigable. . .’’ (Giglioli, 1963). An. darlingi is the main vector in nearly all forest areas in Central and South America. It tends to be exophilic in this environment, especially where human dwellings do not have complete walls, as in traditional Amerindian villages (Girod et al., 2008). In Venezuela, the main problem in some areas was exophily and to some extent exophagy of An. nuneztovari (Rubio-Palis and Curtis, 1992). In contrast, in Northeast Brazil, malaria in deforested areas was mainly transmitted by An.marajoara, a vector previously associated mainly with marshes and assumed to play a minimal role (Conn et al., 2002). It is estimated that at least 70% of P. falciparum in the Americas now occurs in the Amazon and Orinoco basins, where it is mainly transmitted by An. darlingi (J. Najera, personal communication). A multifactorial, spatial analysis with remote sensing data found that, in the short term, deforestation in the Amazon forest fringe leads to increased breeding of An. darlingi (de Castro et al., 2006). After a few years of colonization, agriculture reduces breeding sites, housing improves, and the residual malaria problem is related to incursions into the forests (Takken et al., 2005). Similar conclusions were reached by several other groups, applying different methods in this region (Rubio-Palis and Zimmerman, 1997; Vittor et al., 2009). In the Peruvian Amazon, highly focal malaria transmission in forest communities was demonstrated; despite the high levels of precipitation, proximity to rivers was an important determinant (Bautista et al., 2006). Ecological classification was carried to a finer scale in

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the state of Roraima in northern Brazil. Applying different analytical strategies to an ecological niche model based on landscape elements, human occupancy and vector distribution, eight ecoregions of importance for malaria were identified, including five types of dense rainforest and three types of savanna. Unfortunately, this work does not examine how the ecoregions correlate with the spatial distribution of malaria and does not indicate control implications (Rosa-Freitas et al., 2007). Forest malaria emerged as a major concern in Brazil from the 1970s with rapidly increasing deforestation, agricultural colonization and mining in the Amazon (Wallace and Webb, 2007) and especially, when drug resistance spread to the extent that miners could no longer be protected by chemoprophylaxis. Over time, malaria spread to the Amerindians living inside the forests (Mouchet et al., 2004b). Malaria in Brazil is now only endemic in Amazonia legal, that is, those states with 12% of the nation’s population that include areas of the geographic Amazon region. In 2007, 457,831 malaria cases were recorded in the country, of which only 172 (0.04%) were outside that region. However, 24% of cases were found in urban areas located near forest or with encroaching forest (Ministe´rio da Sau´de, 2008). Comparing the distribution of malaria with the distribution of forest cover, it is easy to see the almost perfect congruence between malaria and forest/forest fringe areas including those, which have been deforested recently (Fig. 3.3). On the background of a paucity of research evidence of control methods—contrasting with the rich literature on spatial description—it is encouraging that a controlled trial among forest dwellers in the Amazon Region found that insecticide treatment of hammock nets prevents 56% of new malaria cases, and non-treated nets presumably have no effects (Magris et al., 2007). In the Atlantic rainforests of South America and the Caribbean, especially Brazil, the main vectors, An. (Kerteszia) bellator and An. (Kerteszia) cruzii, breed in the leaf axils of epiphytic bromeliads in the tree canopy. They have been difficult to control because of exophily, early biting and the peculiar breeding site (Gadelha, 1994). However, they are short lived, and more than 90% of the Atlantic rain forest has disappeared, so bromeliad malaria is now a sporadic phenomenon, but one that could increase as a result of reforestation. In the past, bromeliad malaria affected urban areas and cacao plantations in Trinidad (Marrelli et al., 2007) and coffee plantations in Brazil (Mouchet et al., 2004b). Another variant of forest malaria is found in the Lacandon forest in Belize and south-eastern Mexico, where An. vestitipennis seems to be the main vector (Arredondo-Jimenez et al., 1998).

3.3.2.4.4. Piedmont This ecoregion comprises foothills between 200 and 1500m altitude in Mexico and Central America and on the west and east sides of the Andes. The main vectors are the widespread An. nuneztovari

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and An. pseudopunctipennis, with An. albimanus being found especially in the western Andes and An. darlingi in humid lowland areas. P. vivax is predominant, but P. falciparum closely associated with An. darlingi occurs focally. The transmission is only of low to moderate intensity. In western Venezuela, an exophilic An. nuneztovari continues to challenge control and elimination in the Andean foothills (Mouchet et al., 2004b). In Oaxaca, the state in Mexico, which currently has the highest malaria burden after Chiapas, an ecological study found that transmission was associated with elevation between 200 and 500m, temporary streams and larger population size of rural localities. Land use seemed to be of little importance (Hernandez-Avila et al., 2006); An. darlingi does not inhabit this part of Mexico, where the remaining forest is located at high altitudes. The malaria in the state is thus partially coastal, but mainly of piedmont type, with An. pseudopunctipennis as the main vector; removal of algae from breeding sites has been identified as one element in the control strategy (Case Study Mexico, 2009)

3.3.2.4.5. High valley In Andean valleys above 1000m, P. vivax may be transmitted seasonally by An. pseudopunctipennis. Epidemic P. vivax and sometimes P. malariae persist in the sparsely populated, underserved villages in highland areas in Bolivia, Peru and Colombia. In contrast, malaria has largely been sprayed away in Venezuelan highlands (Giglioli, 1963). This epidemic-prone ecoregion clearly corresponds to highland fringe malaria in other parts of the world. 3.3.2.4.6. Coastal The coastal zone as identified by Rubio-Palis and Zimmerman (1997) includes not only areas under salt water influence but also plains up to 550m altitude or about 100km from the ocean. By this definition, the demarcation from piedmont becomes somewhat arbitrary and related to the landform. In the Caribbean, malaria was always found only in coastal areas, transmitted by An. albimanus, which is today the main vector in the island of Hispaniola as well as in the lowlands of central America, both Atlantic and Pacific. In Pacific coastal areas of South America, An. aquasalis is the main vector, but generally, malaria is now a minor problem there. The Pacific coastal environment in Chiapas, Mexico, where An. albimanus is the main vector, was studied by remote sensing; it was found that certain land cover types, salt marsh, mudflat, savanna/woodland and open water, were more productive of this vector than others (Rojas et al., 1992). It was suggested that this would help target malaria control efforts, but it was not clear, if this approach would improve on targeting by conventional epidemiological methods. In the South American coastal plains facing the Caribbean, An. darlingi, breeding in irrigation canals, rice fields and cane fields, was an important

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endophilic vector. IRS interrupted transmission in these coastal areas, but in some places, the disease returned in the 1980s because of neglect of vector control (Pope et al., 1994).

3.3.2.4.7. Urban Urban malaria in South America is, generally, an extension of surrounding rural malaria. As noted above, malaria is now a serious problem in cities in the Amazon region of Brazil, where it should perhaps be considered ‘urban’ from an administrative viewpoint and ‘forest’ entomologically, as it is transmitted by An. darlingi, breeding in man-made sun-exposed water bodies, but not in artificial containers (Cabral et al., 2010). Control by IRS or ITN is difficult due to the exophily, but much could probably be achieved with environmental management (Gil et al., 2007; Gonc¸alves and Alecrim, 2004; Olano et al., 1997). Similarly, certain cities in Colombia have urban malaria transmitted by An. albimanus with less malaria in the cities than in surrounding countryside. 3.3.2.4.8. Agricultural development In many areas, agricultural development, especially in the savanna environment, has been associated with the disappearance of malaria. Yet, there are a number of examples of specific problems arising as a result of agricultural development. Rice-field malaria was a serious problem in Puerto Rico, in Central America, in the piedmont of Venezuela and in dry zones of Peru but has largely been eliminated by IRS (Mouchet et al., 2004b). In Guyana, the elimination of buffaloes in the Demerara river estuary resulting from mechanization led to a resurgence of malaria caused by the zoophilic An. aquasalis (Giglioli, 1963). In Central America, resistance of An. albimanus to several classes of insecticide has been notorious in cotton plantation areas (Georghiou, 1972), but nonetheless, there has been a continued reduction in malaria over the past 30 years (Pan American Health Organization, 2002). When, at the start of the twenty-first century, malaria returned to The Dominican Republic in sugar cane plantations which recruited workers from Haiti, environmental management helped deal with this problem (WHO, 2008). 3.3.2.4.9. Warfare and social instability The importance of long-term conflict is evident especially in Colombia and Peru, where chronic insecurity in highland areas impede the development of services, which could, in principle, easily achieve elimination of the unstable malaria transmitted by the endophilic An. pseudopunctipennis. Conflict may also contribute to the maintenance of high incidence rates in forested areas of countries like Honduras and Guatemala (Pan American Health Organization, 2002).

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3.3.2.5. Palearctic 3.3.2.5.1. General Malaria in the Palearctic occurs only focally. Like the Indo-malay, this region encompasses enormous ecological and climatic variability. Its demarcation from that region is fuzzy, both east and west of the Himalaya. The malaria situations are best described according to geographic location.

3.3.2.5.2. Arabian peninsula Malaria in the south-western part of the peninsula belongs to the Afrotropic region, as noted above. In the eastern part of the peninsula, small foci now remain in Oman, where the vectors are the same as those in the western Indo-malay. The most intense malaria transmission has been in foothill areas, with An. culicifacies breeding seasonally in streams (Delfini, 1987). 3.3.2.5.3. Caucasus, Iraq and Turkey Several Caucasian nations experienced a re-emergence of vivax malaria in the 1990s, with An. sacharovi as the main vector. The valleys and foothills provided a suitable environment for breeding of this species; in some areas, it was enhanced by dams and irrigation, and the situation was aggravated by a degradation of health services following the breakdown of the Soviet Union and population movements related to the armed conflict between Armenia and Azerbaijan (Sergiev et al., 2007b). In Iraq, malaria now remains in Kurdistan, where it is mainly transmitted by An. sacharovi and to some extent An. superpictus and An. maculipennis. In this area, the ecology could partially be classified as foothills, partially as irrigation (Mouchet et al., 2004a). The current malaria focus in eastern Turkey is associated with irrigated agriculture, which started in the 1970s in the C ¸ ukorova plains, and has led to massive increased breeding of An. sacharovi as well as attraction of large numbers of migrant workers (Sergiev et al., 2007a). Social unrest in this area may also have played a role. 3.3.2.5.4. Afghanistan, Central Asia, Iran and Russia The vectors include the Indo-malay An. culicifacies, An. stephensi and An. fluviatilis, and the Palearctic An. pulcherrimus, An. hyrcanus and An. superpictus. Despite considerable progress in the 1960s, malaria was never eliminated in Afghanistan and serious resurgences occurred following conflicts in the 1980s. In Tajikistan, Uzbekistan and Turkmenistan, malaria had been practically eliminated but was reignited by movements of infected people and vectors across the borders from Afghanistan, and the situation further worsened when control capacity was affected by the dissolution of the Soviet Union. In all these countries, the ecological background situation is valleys and foothills with traditional agriculture, on which, in many areas,

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irrigation is superimposed, greatly increasing vector density. Nomadism is a factor hampering control efforts, but the main problem has been the continued violence and instability in Afghanistan (Sergiev et al., 2007b). The main focus of malaria in Russia in recent years has been in and around Moscow over the years 2000–2007, where carriers of P. vivax of diverse origins have encountered high seasonal densities of several Palearctic vectors breeding mainly in water reservoirs (Gordeev et al., 2005). The focus has now been eliminated as a result of better case management, increased surveillance and awareness, larviciding and diminishing population movement (Ivanova et al., 2009). Together with a smaller outbreak in Tashkumyr in Kyrgysztan in 2002 (Usenbaev et al., 2008), this is the first published example of urban malaria in the Palearctic for several decades. It is possible that climate change contributed to the outbreak (Mironova and Ivanova, 2006).

3.3.2.5.5. Central China and the Korean peninsula Vivax malaria continues to be transmitted in a number of foci in central China and the Korean peninsula, all of them related to irrigated rice cultivation (Beales, 1984; Schapira, 2002; Somboon et al., 1994). The main vectors are An. sinensis, a rice-field breeder with zoophilic and exophilic tendencies, and in hilly areas of China, the much more efficient, anthropophilic An. lesteri (formerly considered as An. anthropophagus) (Qunhua et al., 2004). As one would expect, various larval control methods may play a role in the control of the former, while ITN or IRS works well where the latter dominates (Xu et al., 1998). In contrast to other areas of endemic malaria in the Palearctic, conflict is not a determinant of malaria in these foci (which are gradually being eliminated); however, it has been hypothesized that loss of cattle in the 1990s may have increased the vectorial capacity in North Korea.

3.3.3. Proposed definition, identification and demarcation of malaria ecotypes and their implications in five biogeographic regions Across biogeographic regions, there are striking commonalities between the characteristics of malaria associated with particular ecological backgrounds, for example, for forest malaria in the Indo-malay and the Neotropic, and also striking differences, for example, between savanna malaria in Africa and malaria in plains and valleys with traditional agriculture (which include savannas) in nearly all other biogeographic regions. Within biogeographic regions, there are also striking differences between subregions, for example, as regards irrigated rice fields or urban malaria in different parts of the Indo-malay. In any biogeographic region, major environmental differences generally do translate to differences in malaria

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epidemiology, but in many cases, the differences are quantitative and gradual, and they do not always have implications for control. This is particularly so in the Afrotropic, where the main vectors are ubiquitous and versatile. The only global ecological typology attempting to classify all malaria situations in the world remains the one proposed by WHO (Table 3.1); when considering the six steady-state types, it has the great advantage of parsimony. Only two alternative systematically developed typologies have been published, one for the Neotropic and the other for the Afrotropical. Both of these overlap with WHO’s, but there are interesting differences. The approach of Rubio-Palis and Zimmermann (Rubio-Palis and Zimmerman, 1997), aligning malaria typology with mainstream ecological stratification in the Neotropic, has the advantage that a malaria situation, wherever it occurs, can be assigned to a physiographic background. This may be particularly useful, as malaria has, since 1990, re-emerged in ecoregions from where it was thought to have been eliminated, especially in the Palearctic. One ecoregion included in this typology is foothills (piedmont), which is not specified in the classical typology; in fact, the findings in the Afrotropical (Madagascar) (Rabarijaona et al., 2009), Australasian (Muller et al., 2003), Indo-malay (Dev et al., 2004), Neotropic and Palearctic (Sergiev et al., 2007a,b) regions concur in suggesting that foothills merit to delimit an ecotype of malaria, where the defining characteristic would be that the terrain often provides niches for vectors which prefer fast-flowing water, while the temperature is still (almost) as favourable to malaria transmission as that in adjoining plains. At its upper altitude limit, foothills merge into mountain fringes with unstable, temperature-dependent malaria. In many texts, malaria in foothills has implicitly been clubbed with forest malaria; in fact, although the transition may be gradual, there are often important differences in predominant vector species and bionomics, social conditions and amenability to control. The typology for Africa developed by Mouchet et al. starts with major facie`s e´pide´miologiques, which are similar to those of Table 3.1, but with some finer gradations. These gradations have not been shown to be relevant in a programme perspective, and they would not be easily applicable in a global typology. Yet, this typology has great merit in the separation between major ecoregions ( facie`s) as primary factors and a variety of secondary factors or processes, which may be natural or anthropic. This is very much akin to landscape epidemiology and addresses a limitation of the classical typology, which has only two situations of rapid development change: agricultural development including irrigation and war and sociopolitical disturbances, which seems unnecessarily restrictive. The convergence of physiographic changes and population movement, which often is associated with malaria risk in agricultural development projects, may also occur, in relation to, for example, dam building, road- and railway

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building, mining, etc. Similarly, the effects of natural disasters may be not very different from those of wars. This additional level of analysis can be considered an alternative to structuring a typology with sub- and sub-subtypes. Such may be justified at times in national programmes (viz. Indian forest malaria strata). However, fine subdivisions are difficult to memorize, do not capture juxtapositions and may encourage control managers to straitjacket all malaria situations to fit with defined types, instead of locally examining the implications of interactions between climate, biology, physiography and human ecology. The weakness of an approach with several levels of analysis is that the typology abdicates from almost any prescription, becoming rather a framework. Given that published typologies anyway tend to avoid prescriptiveness and that decision-making on control must consider epidemiological data, available resources (in the broadest sense) and technologies, this is probably rational. From these observations, it is proposed that a global typology can be based on a small number of environmental classes, which are represented in nearly all biogeographic regions and would cover all areas, where malaria transmission is not interdicted by climate or biogeography:       

Savanna, plains and valleys Forest, forest fringe Foothill Mountain fringe and northern and southern fringes Desert fringe Coastal Urban

Despite the profound differences in malaria transmission, African savanna is grouped together with savannas, plains and valleys outside Africa for the sake of consistency, and because in any country or region, savanna, plains and valleys are natural candidates for the role of default ecotype. Also, there are other ecotypes that differ greatly, even within biogeographic regions, for example, urban. In addition, it is proposed that the classical typology is modified towards a scheme with three levels: 1. Identification of the biogeographical region, or subregion, which determines, so to say, the menu of vector species from which the physiography will choose. 2. Classification of the physical environment into one of the above classes, recognizing that even a small district may have several environmental types, where sometimes the juxtaposition of certain environments may create particular dynamics. Some situations may be characterized as transitions (ecotones); others rather as mixed

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(mosaic), like forests encroaching on Amazonian cities or combined, as some fringe areas in East Africa combining desert and highland characteristics. 3. Identification of secondary factors, which can be stationary or dynamic, is classified as follows: a. Natural (landform, water bodies, soil characteristics, disasters, climate change); b. Anthropic (habitat and habits, population movement, agriculture (traditional or based on major investments), animal husbandry, other economic activities, deforestation, modification of water bodies, transport infrastructure, war and unrest); c. Health system including malaria control. (This is, of course, anthropic, but by its intentionality so specific that it appears reasonable to consider it separately). Thus, a given malaria situation would, for example, be classified as Afrotropic in a highland fringe environment and with irrigation rice cultivation as the main anthropic process. Another as localized in the Indo-malay region, with physiography being a mixture of plains and monsoon forest with interspersed urban areas and mines attracting large numbers of migrants, as well as some insurgency causing additional unpredictable population movement. The defining characteristics of the seven environmental classes as well as their demarcations are presented in Table 3.3A, and the major variations in relation to malaria epidemiology and control in Table 3.3B. The most useful findings could be summarized as follows. As has been known for a few decades, forest cover is a very strong determinant of malaria risk in the Indo-malay and the Neotropic, except in certain islands, most notably Sri Lanka, where forest vectors have not arrived, and in areas where the temperatures are too low for malaria transmission. Forest-related malaria can be delimited. In Cambodia (Cambodia Malaria Survey, 2007) and Bangladesh (Haque et al., 2009), malaria risk was greatly increased within 2, respectively, 3km from the forest border, which can be identified by land-use data or by EVI or NDVI. Probably, the demarcation is more complex and fuzzy in the Neotropic, given the propensity of An. darling for deforested areas. It is important to note that forest-related malaria in those two biogeographic regions covers a wide spectrum from the viewpoints of vector bionomics, human ecology and control (Table 3.3B). In tropical Africa, the reductions in malaria transmission associated with highland and southern fringes are well known, as are those associated with desert fringes. Outside Africa, in non-forested areas, the low background risk in rural areas may and may not be increased in areas of agricultural development; the risk is higher, the more arid the area.

TABLE 3.3

Malaria ecotypes as based on physiography, with variations in different biogeographic regions

A. General characteristics of the ecotypes

Malaria implications

Morbidity and Control Demography, human Vector bionomics ecology and health and transmission mortality system Default: Not belonging to any Population density Vectors usually Concentrated in Anti-adult methods other ecotype and health service endophilic, but in youngest age constitute primary coverage variable, certain areas and groups in Africa line of vector but usually far seasons exophilic. including adverse control from universal Often zoophilic. If effects on malaria is pregnancy. endemic, Elsewhere, pattern transmission is is variable, usually seasonal, sometimes lasting >5 months concentrated in (Mouchet et al., occupational 1993a) groups EVI or NDVI consistent with Low population Some, but variable Ranging from Limited effect of antiforest. Forest fringe may density; weak degree of exophily African savanna adult methods in extend up to 2–3km from infrastructure; and exophagy; pattern with most subregions of forest margin in Indo-malay, population groups high degree of mainly young Indo-malay and possibly longer in Neotropic, with different anthropophily; children affected Neotropical; antiespecially if deforestation habitats and variable to only certain larval methods habits; various heliophily. occupational rarely feasible. kinds of Transmission only groups Curative service population in tropical areas provision often movement very difficult and must be tailored to local conditions.

Physiography Definition and delimitation

Savanna, plains and valleys

Forest

(continued)

TABLE 3.3

(continued)

Foothill

Highland fringe and northern and southern fringes

Usually, excellent An altitude belt, where Variable population The inclination may Transmission favour vectors that moderate and focal effect of anti-adult transmission is not density; service find niches in may have intense methods if significantly constrained by access often running water. seasonal operational low temperatures, thus constrained by Vectorial capacity variations. constraints can be depending on latitude. 200– terrain. may be high Usually, all age overcome. Larval 1500m a.s.l. in the Andes Agricultural focally groups affected, control may be (Rubio-Palis and development may often with peak feasible in specific Zimmerman, 1997), 200–1200 increase m in Papua New Guinea population disease incidence circumstances (Muller et al., 2003), 200–800 movement, in older children m in Indochinese peninsula increase or (Rabarijaona et al., 2009) (writer’s (AS) obs.) decrease transmission, and provide control opportunities Malaria unstable depends on Population density Vectors usually Highly unstable, Usually good effect temperature variations, varies from high to endophilic, often epidemic. All of anti-adult secondarily also rainfall, very low; sometimes age groups are methods, when environmental disturbances sometimes zoophilic affected. With high feasible, but and population movement. nomadism and population acceptability of Lower altitude limit defined transhumance; density, mortality ITN may be locally, corresponds to upper infrastructure and in epidemics may constrained by low altitude of foothill, for heath system be enormous insect nuisance example, 800–1200m a.s.l. in highly variable. and small most malaria risk areas. Dams and dwellings with Upper limit depends on irrigation may open fires. Larval latitude and local factors greatly increase control may be affecting outdoor and indoor transmission feasible in some

Desert fringe

Coastal

microclimate, 2800m for vivax in Bolivia (Rubio-Palis and Zimmerman, 1997), 2000 m in Africa near equator (Mouchet et al., 1993a), 1600 m in Madagascar (Mouchet et al., 1993b), 1700–1800m in Papua New Guinea (Muller et al., 2003), 1500m in Indochinese peninsula (writer’s obs.) As highland fringe, but rainfall Population density is main determinant, while in low; often some areas, temperatures nomadism or may be so high as to limit transhumance. transmission. Duration of Health system rainy season up to 5 months, often very weak. transmission season <5 Development months (Mouchet et al., projects are rare. 1993a), may overlap with Irrigation may highland fringe, as in East greatly increase Africa transmission

For a clear distinction, coastal Population density malaria should be defined as usually high with malaria in areas, where the relatively good vectors need salinity. infrastructure and However, coastal vectors in health services the Neotropic are catholic in

circumstances as supplement

Vectors usually endophilic, often zoophilic

Usually, all age Usually, good effect groups are affected of anti-adult methods; feasibility of ITN may be better for mobile populations though sometimes constrained by high temperatures. Larval control may be feasible, in specific circumstances as supplement Vectors associated Usually, all age Environmental with brackish groups are management is water with varying affected, possible in some degrees of salinity, sometimes circumstances, but depending on occupational nowadays plays a species; anthropic exposure limited role as part

(continued)

TABLE 3.3

(continued) this respect, so coastal malaria there has been defined as malaria associated with plains stretching far inland (Rubio-Palis and Zimmerman, 1997)

Urban

disturbances often of intentional essential for malaria control, as breeding sites anti-adult methods (Poolsuwan, 1995); are usually vectors usually effective endophilic transmission low to moderate In most cases, urban malaria is Population density Transmission rarely Usually, all age Anti-adult methods, caused by the encroachment high, health intense but often groups are affected especially IRS, of rural/forest landscapes services accessible, highly variable may be difficult to into urban areas. Urban but dominated by over short implement in truly distances urbanized areas. malaria sensu stricto is caused private providers by vectors, which prefer Anti-larval man-made containers. methods not only Delimitation: GRUMP urban feasible in extent in Afrotropic principle but also constrained by operational problems. House screening, crossdisease collaboration and intersectoral work merit more attention

B. Variations of main characteristics by biogeographic region Afrotropic Australasian Intense transmission with Savanna, Intermediate seasonal variation leading to plains and between stable malaria with burden valleys Afrotropic and the with concentrated in young other regions. traditional children, pregnant women Malaria is agriculture and travellers. Control may relatively stable, be difficult in West African but man-made arid savanna, where intense environmental transmission is compounded disturbances by exophily (Molineaux and greatly increase Gramiccia, 1980). the risk Environmental change rarely leads to important alteration in malaria epidemiology, but population movements may be important. Recent studies suggest that both IRS and chemical larviciding can have additional effect when combined with ITN (Fillinger and Lindsay, 2006; Kleinschmidt et al., 2007) Forest Forest malaria manifests as a Seems to have same variant of savanna malaria, characteristics as often with less intense savanna malaria, transmission because of but the diversity of lower vector density. In most, vectors and but not all cases, African limited

Indo-malay Neotropic Palearctic Malaria is unusual, highly focal and unstable and largely limited to areas with anthropic environmental modifications. Irrigated rice fields are associated with increased malaria risk in the Neotropic and Palearctic regions and in the western, relatively arid part of the Indo-malay region, but usually not in Southeast Asia. Man-made rural malaria outside Africa has been seen as one of the main opportunities for environmental management or other forms of larval control. There are examples of this, mainly in older literature; nowadays, larvivorous fish are used widely in India and some other countries. In most of these settings, the vectors are very amenable to adult control. Planning and implementing IRS or ITN are so easy that little attention is paid to targeting or evaluation of larval control

Forest-related malaria has emerged as the Forest malaria plays dominant residual malaria problem. At no role least in Indo-malay, there is evidence for delimitation of forest-related malaria. In Cambodia (Cambodia Malaria Survey, 2007) and Bangladesh (Haque et al., 2009),

(continued)

TABLE 3.3

(continued) forest vectors are relatively endophilic and amenable to adult control

information makes it difficult to generalize the role of forest environment

malaria risk was greatly increased within 2, respectively, 3km from the forest border, which can be identified by landuse data or by EVI or NDVI. It has serious consequences for the directly affected often underserved populations; it seeds malaria foci in environments with lower vectorial capacity and is a source of multidrug resistant falciparum malaria for the world. The effects of deforestation depend on the type of environmental change and the local forest vectors’ heliophily. Variations especially within Indo-malay region are important: The highly exophilic An.dirus may be confined to continental Southeast Asia; related forest vectors in Indonesia and Malaysia are less exophilic and those in peninsular India even less. There are no true forest vectors in Sri Lanka and those in the Philippines (except Palawan) are inefficient and relatively easy to control. In the Neotropic, the risk is generally greater in the deforested fringe than inside the forest. South American forest malaria has a tendency to invade cities, while southeast Asian forest vectors are likely to colonize plantations. Control must be multi-pronged, deal with population movements and overcome geographic, social and societal constraints

Foothill

Highland fringe and southern and northern climate fringes Desert fringe

Foothill malaria usually has similar characteristics as savanna malaria, but recent studies in Madagascar suggest that the disease burden extending to all age groups merit more attention

Mining and infrastructure development in New Guinea have greatly increased malaria problems

Foothill areas often have specific vectors with The residual or rebreeding sites related to streams; the emerging malaria vectorial capacity is often higher than in problems often adjacent plain areas, and the malaria, result from though unstable, is typically not epidemic convergence of like in the highland fringe, while population transmission is less intense and more movement, controllable than in forest areas. Habit of agricultural using mosquito nets is becoming development and increasingly generalized in Southeast degradation of Asia. Generally, foothill vectors are less services on a exophilic than those in deep forest; as foothill landscape found in Mexico, there may be background opportunities for larval control. Cultivation of foothills, even rice-field terraces, usually changes the landscape in a way that reduces malaria transmission or risk Epidemic malaria in highlands related to Occurs sporadically; the human populations Hardly of any meteorological variations is a highly significant affected are small. Evidence is scanty in importance, except problem. Because of the limited mosquito nuisance, South and Southeast Asia, better in South as northern fringe IRS may be more effective than ITN. Recently, larval America in Central Asia control has shown potential in Kenyan highlands (Fillinger et al., 2009)

Important in western Africa, the Does not occur Horn and south-western Africa. Much more neglected than highland malaria. Both major anti-adult methods

Important in restricted populations inhabiting large areas in Pakistan

Does not occur

Of minimal importance. Resurgences in past 20 years have generally not

(continued)

TABLE 3.3

Coastal

Urban

(continued) should be highly effective, but both meet different operational challenges. Like in forest areas, there is a scope for adapting personal protection methods to local culture and human ecology A variant of savanna malaria with less intense, sometimes more seasonal transmission. Environmental management is likely to be feasible and cost-effective only in very specific situations

Increasingly important. Recent results with larval control in Dar es Salaam are encouraging but need to be subjected to costeffectiveness studies (Geissbuhler et al., 2009). More attention to house screening is needed

and North-west India. Control challenges similar to Africa

occurred in desert fringe areas

Remains dominant, Much less common Does not occur Was in most areas especially in than a century ago, wiped out by IRS nowadays Solomon Islands nowadays only except for a few and Vanuatu, important in parts areas, where it has where the effect of of Indonesia and persisted or readult control is southern Vietnam. emerged somewhat The elaborate constrained by environmental early biting and management exophily schemes of the past have almost become history Similar to African Urban malaria is a Has again become Has re-emerged in a situation, but problem only in important in South few foci posing; generally, so far, a the Indian America in areas of controlled by minor problem subcontinent, but forest combined there it has encroachment; no measures aiming presented serious good examples of at mosquito challenges to control published breeding and control (Gil et al., 2007) human carriers (Ivanova et al., 2009)

Note that there are frequent exceptions to the characteristics as described here; that the transitions between ecotypes are gradual (though less so around urban and forest) and that the proposed delimitations are based on expert opinion, not hard evidence. The recommendations about control measures must be considered tentative; in fact, emphasis has been placed on the potential implications of recent research, which challenges older assumptions.

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Foothills are generally associated with higher malaria risk than nonforested plains in all biogeographic regions outside Africa. Much of the recent, highly focal, malaria occurrences in the Palearctic have been associated with foothills and/or agricultural development projects. The urban environment is associated with increased risk in most of the Indian subcontinent, especially the western, arid part; urban malaria is present in the Neotropic when forests encroach on cities and in a few exceptional circumstances urban malaria has re-emerged in the Palearctic. The findings of Tatem et al. (2006) indicate that urban extent as defined by GRUMP, based on night-time light emissions, is adequate to demarcate urban areas with relatively low malaria transmission in Africa. Whether this is also the case outside Africa remains to be further investigated, but there is no a priori reason to assume that this criterion would work less well there. In most of Southeast Asia, there is usually no or very little malaria in either urban areas or adjacent countryside, unless forested. Thus, there is some evidence for geographic demarcation of forest malaria and urban malaria in the biogeographic regions, where these malaria ecotypes are important. For most other types, the transitions between them are gradual, determined by changing altitude, latitude, rainfall and salt-water infiltration. The resulting modification in malaria epidemiology is likewise gradual. The delimitations of these ecotypes presented in the tables are largely based on published expert opinion and in some cases, the writers’ field observations.

3.4. DISCUSSION 3.4.1. Implications for control programmes Knowledge about ecological determinants of malaria could be useful for control programme stratification in a number of ways: firstly, by improving the delimitation of areas and populations at various levels of malaria risk; secondly, by indicating which vector control interventions are most likely to be effective and cost-effective; thirdly, by indicating any other special measures and fourthly, by indicating what effects can be expected from given interventions.

3.4.1.1. Stratification and delimitation of malaria risk The first step in stratification is normally to delimit populations living in areas where malaria cannot be transmitted (no risk), areas without endemic malaria but a risk of outbreaks (epidemic risk) and areas with endemic areas (WHO, 2009). In theory, ecological determinants should be useful mainly for distinguishing between the two former categories

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because malaria cases are absent from both. There are examples of failures of ecological prediction of risk, as in the case of unforeseen convergence of determinants of urban malaria in Russia (see Section 1.3.2.5.4, p. 56). In contrast, it worked in Southeast Asia, where tree plantations have led to the return of forest vectors and transmission (see Section 1.3.2.3.11, p. 43). Thus, for this distinction, the careful use of ecological, climatic and other determinants together with historical malaria data is probably the best that can be done. For delimitation of endemic areas, ecological determinants may be useful as supplement to epidemiological data. As malaria surveillance is still usually not case-based, data are referenced at best to health facilities, and it is assumed that these have coverage areas corresponding to administrative units. As epidemiological data are usually not available at a fine enough level to allow vector control targeting by village, local planners may need to take decisions based on soft knowledge. This soft knowledge may be expressed by local health service providers, who may have experience that most malaria cases come from given localities, or it may be ecological. Overlaying malaria epidemiological data with population data and physiographic data makes it possible to identify underserved populations, which may be assumed to live with endemic malaria. This is in fact done in mature control programmes (see Section 1.3.2.3.13, p. 44), but in practice, the only ecological malaria determinant that is trusted at face value is probably the forest environment in eastern India, most of Southeast Asia and South America, which has a very strong correlation with malaria risk (see Section 1.3.2.3.3, p. 31 and Section 1.3.2.4.3, p. 48). More generally, the certainty and the degree with which a given ecotype will modify malaria risk are highly variable, depending on the biogeographic region, the ecotype in question and the associated processes. Yet, the forest environment in the Indo-malay and Neotropic realms stands out because of its relatively clear delimitation and almost invariably strong association with heightened malaria risk. In tropical Africa, the implications of the various fringes and urbanization are well documented, but the delimitations are not sharp. This has implications for surveillance and assessment of impact rather than for interventions. In contrast, the knowledge that rice irrigation has different effects according to background ecology is relatively new, though not a great surprise (see Section 1.3.2.1.8, p. 24), and this has control implications. As the widespread application of control interventions in Africa changes the epidemiological pattern, these distinctions are becoming blurred, but it remains to be seen to what extent ecological and climatic determinants will be associated with rebounds. As for the other ecotypes, considering the findings in this review, they should normally be used only as indications of what must be looked out for rather than for what must be there.

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3.4.1.2. Implications for vector control A major reason for ecological assessment of local malaria problems has been to determine whether anti-larval methods could be effective to control malaria. Keiser et al. (2005a) have found that in recent times, intentional methods for larval control remain neglected in favour of anti-adult methods. Coastal malaria, which in the past was found highly suitable for larval control in the Indo-malay region, appears to be receding there, probably as a result of general development (better access to health services, higher population density, improved housing and improved environmental hygiene) and the availability of anti-adult methods. Similarly, malaria related to rural development projects is often managed with antiadult methods, because of the ease of planning and implementing them. In contrast, in urban areas, especially in India, anti-adult methods encounter serious constraints, so that larval control has an important role, although that role is in need of stronger, updated evidence and should be enhanced through more research and more advanced intersectoral collaboration. Larvivorous fish and sometimes source reduction (bio-environmental control) are widely promoted and applied in some countries in Asia, especially India, but with little attention to criteria for applying various methods and evaluation (Dev et al., 2008; Sharma, 1999). Generally, it seems that the simplicity of planning and implementing anti-adult methods leaves little room for serious application of larval control in endemic areas of Asia and the Americas. Those areas, in which anti-adult methods are most constrained, are (a) urban malaria in the Indian subcontinent, where larval control can be highly effective and (b) forest-related malaria, where larval control is usually inapplicable (except possibly in deforested and semi-urbanized areas in South America). Anti-adult methods in non-forested areas in India are running into serious problems of multi-insecticide resistance (K. Raghavendra, personal communication); it is therefore important to revisit the range of larval control methods, including insect growth regulators, and conduct well-designed controlled trials guided by competent entomologists and epidemiologists in defined ecological settings. The problems of vector control in forest areas with exophilic vectors have not been solved. There was hope some years ago that insecticide-treated mosquito nets including hammock nets would provide the solution, but the results have so far suggested an effect, which is modest—though present and possibly better in the Amazon than in the most difficult areas of continental Southeast Asia (Magris et al., 2007; Sochantha et al., 2006; Thang et al., 2009). Although the problems of control of forest-related malaria can in no way be reduced to the entomological dimension, there are good reasons to invest in research and development. Recent investigations in Africa also suggest a broader role for larviciding as an adjunct to effective anti-adult intervention. The studies are few

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and may have been done in selected areas with propitious ecological and health system conditions. Nonetheless, they are potentially very important. In savanna malaria settings in Africa, anti-adult methods have good effect (Lim et al., 2011), but this is limited and subject to decay because of waning population immunity, insecticide resistance and operational factors (Trape et al., 2011). ITNs are widely accepted as the basic vector control method. It remains to be seen, whether and where IRS with alternative insecticides or larval control will be the better primary supplement. In summary, current evidence suggests that only two ecotypes have reasonably clear implications for larval control. In urban malaria, especially the Indian type, larval control should be considered. For forest malaria, there is so far no evidence that larval control is potentially useful.

3.4.1.3. Implications for other control interventions Local assessments of ecotypes with their anthropic and natural processes can lead to the identification of special risk groups and risk areas, for which particular strategies and approaches are needed. It is usually not so much a question of what to do as of how to do it, for example, finding ways of providing case management services to populations at high risk, who may be cut of part of the year, engaging with clandestine work forces, mining companies, private pharmacies in urban areas, etc.

3.4.1.4. Implications for expectations of impact Malaria control planning usually mobilizes investments on the basis of expected reductions of morbidity and mortality. With the currently available menu of interventions, it can be expected that the outcomes will be less impressive and more difficult to sustain in the most difficult areas: those where the transmission (indicated by, e.g. parasite rate) is intense and those where technical and operational constraints converge, like forest-related malaria in certain biogeographic regions and subregions, and to some extent, urban malaria in India and desert fringe areas, with major operational challenges. Although it is more and more the accumulating experience at the local level, which informs the assessment of expected impact, stratification based on ecotypes should help generate an overview, stimulate critical thinking and help communicate to other sectors why the problem seems to be resilient in certain areas.

3.4.1.5. General Landscape epidemiology is not as an alternative to, but a supplement to standard epidemiological information. In many countries, its utility in national level planning is limited, while in local, for example, district level planning, it has greater potential, because it is rarely possible to triangulate all the important information for larger geographical units. Even if it is not always possible to pay attention to larval control at the

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national level, it should be possible at the local level to detect, for example, a company that can be advised on how to reduce breeding sites according to what is known about local vector bionomics, or to avoid wasting efforts on trying to find breeding sites to be seeded with larvivorous fish inside a forest area. As noted in Mexico, an ‘ecohealth approach’ is a means of engaging other sectors. Thus, malaria ecotypes could be useful in training local staff to plan beyond the distribution of commodities, to assist in targeting, to adapt interventions to local conditions and to engage communities and other sectors.

3.4.2. Implications for malaria modelling and field research 3.4.2.1. Mapping Hay et al. found that there are no globally valid environmental covariates for mapping of the prevalence of falciparum malaria (Hay et al., 2009). The findings in this review are consistent with this: the geographic variability in vector bionomics is so great that covariates could only be useful at the level of biogeographical regions or subregions. However, within certain regions, certain covariates are extremely important. Thus, future iterations of global malaria mapping should take into consideration the strong correlation found by various methods in the Indo-malay and Neotropic regions between malaria and forest cover. Other findings, which could perhaps be useful for mapping, are that in the Indian subcontinent, from Kolkata and westwards, malaria transmission is generally more intense in urban areas than in the surrounding rural areas, as long as the latter are not forested. And, in areas dominated by river-irrigated ricefield cultivation in continental Southeast Asia (from Myanmar to Vietnam and from Yunnan Province to Malaysia) and in the Philippines, malaria is virtually absent. This can have important implications for burden estimation, as the populations of these areas are large.

3.4.2.2. Simulation modelling of effects of malaria control strategies To aid decision-making, models can be structured so that inputs and outputs are relevant to the needs of the users. One finding of this review is that ecotyping does not provide a classification of all malaria situations into a ‘humanly manageable’ number of categories for modelling. Although there are arguments for working with only six ecotypes, these have, to a large extent, different implications in the five biogeographical regions, which have endemic malaria today; sometimes, there are important differences between subregions, and to this comes a broad spectrum of anthropic processes and effects of health systems and malaria control with profound implications including insecticide and drug resistance and changed vector behaviour.

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Another finding is that a number of ecoregions are affected by malaria, which in most areas is controllable from a technical viewpoint; in most of these areas, malaria transmission persists because of health system problems. This is the case for practically all malaria in the Palearctic and in plains and valleys outside the Afrotropical and Australasian regions. Although malaria control strategies with their operational and systemic constraints can be modelled in these scenarios, it would probably be more rational to prioritize the ecoregions which are posing serious technical problems, namely:  All malaria ecoregions in the Afrotropical, with their variability in



  

intensity of transmission, exophily, seasonality, heterogeneity (especially urban malaria) and health system performance; most malaria in Papua New Guinea can probably be covered by applying the same variations as in Africa although the presence of P. vivax is an added complication. Forest malaria in the Indo-malay and the Neotropic with the variability of intensity of transmission, exophily, length of transmission season and health system performance. Indian urban malaria with its limited applicability of anti-adult interventions, at least IRS. South American forest-related urban malaria. Coastal malaria in the Australasian and the Neotropic with the potential (at least in principle) for source reduction.

Within each of these ecoregions, there is considerable variability related to anthropic, natural and health system factors. It will probably not be fruitful to address all of these in modelling. What can be done is to address the defining variables noted above under each ecotype. There is an increased interest on malaria bionomic databases which compile this information from published literature (Diboulo, 2010).

3.4.2.3. Field research Researchers need to integrate many scientific disciplines if they are to contribute to the understanding of malaria in its broad social and ecological context. Some studies which have combined observation with systems thinking are the reviews of Palearctic malaria, which integrate evolutionary biology, palaeontology, history and epidemiology (Bruce-Chwatt and de Zulueta, 1980; de Zulueta, 1994), the investigations on human geography and malaria in Thailand (Singhanetra-Renard, 1986) and investigations of West African rice-field malaria (de Plaen et al., 2004). The need for better understanding of factors related to human ecology may be even greater. While it is relatively easy to characterize the physiography of an area, it is difficult to obtain data pertaining to human ecological determinants and to formally describe these in a way that can be used for

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modelling. So far, quantitative techniques for studying human migration are in their infancy. Interesting studies on population movement and malaria were published in the 1960s, and fortunately, this thread is now being resumed (Prothero, 1961; Stoddard et al., 2009). In principle, therefore, the geographical classification of malaria requires an ongoing multidisciplinary collaboration between epidemiologists, statisticians, geographers and computing and database specialists to construct geographically explicit models of both local malaria risk and ecology. Ecologic niche modelling has been promoted to address the limitations of empirical spatial statistical analyses (Peterson, 2006), but it is not certain whether it is realistic to try to assemble all the data needed to calibrate such models when the disease is determined not only by its vectors and parasites but also by a myriad of host factors including the health system, which even has important effects on vector and parasite biology. The interactions that result from spatial juxtaposition of differing landscape elements in patterns that vary from place to place are only beginning to be explored (Lambin et al., 2010; McCallum, 2008).

ACKNOWLEDGEMENTS This work was supported by the Malaria Modelling Project #39777.01 funded by the Bill and Melinda Gates Foundation, which also supports KB. We are grateful to Dr. Tom Burkot (CDC-Atlanta), Dr. Jose´ Najera (Crans-sur-Ce´ligny), Dr. Amanda Ross (Swiss TPH) and Professor Tom Smith (Swiss TPH) for their valuable and constructive comments on earlier drafts.

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