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EFFECT OF WATER RESOURCE DEVELOPMENT AND MANAGEMENT ON LYMPHATIC FILARIASIS, AND ESTIMATES OF POPULATIONS AT RISK

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  • 1 Swiss Tropical Institute, Basel, Switzerland; Department of Geography, University of South Carolina, Columbia, South Carolina; Water, Sanitation and Health, World Health Organization, Geneva, Switzerland; Office of Population Research, Princeton University, Princeton, New Jersey

Lymphatic filariasis (LF) is a debilitating disease overwhelmingly caused by Wuchereria bancrofti, which is transmitted by various mosquito species. Here, we present a systematic literature review with the following objectives: (i) to establish global and regional estimates of populations at risk of LF with particular consideration of water resource development projects, and (ii) to assess the effects of water resource development and management on the frequency and transmission dynamics of the disease. We estimate that globally, 2 billion people are at risk of LF. Among them, there are 394.5 million urban dwellers without access to improved sanitation and 213 million rural dwellers living in close proximity to irrigation. Environmental changes due to water resource development and management consistently led to a shift in vector species composition and generally to a strong proliferation of vector populations. For example, in World Health Organization (WHO) subregions 1 and 2, mosquito densities of the Anopheles gambiae complex and Anopheles funestus were up to 25-fold higher in irrigated areas when compared with irrigation-free sites. Although the infection prevalence of LF often increased after the implementation of a water project, there was no clear association with clinical symptoms. Concluding, there is a need to assess and quantify changes of LF transmission parameters and clinical manifestations over the entire course of water resource developments. Where resources allow, integrated vector management should complement mass drug administration, and broad-based monitoring and surveillance of the disease should become an integral part of large-scale waste management and sanitation programs, whose basic rationale lies in a systemic approach to city, district, and regional level health services and disease prevention.

INTRODUCTION

People living in tropical and subtropical countries have long suffered under the yoke of lymphatic filariasis (LF). This chronic parasitic disease is of great public health and socioeconomic significance and is currently endemic in 80 countries/territories of the world.13 LF accounts for serious disfiguration and incapacitation of the extremities and the genitals and causes hidden internal damage to lymphatic and renal systems.46 Disease, disability, and disfiguration are responsible for a loss of worker productivity, significant treatment costs, and social stigma.7,8 At present, the global burden of LF is estimated at 5.78 million disability adjusted life years (DALYs) lost annually.9 Hence, its estimated burden is almost 3.5-fold higher than that of schistosomiasis and approximately one seventh of that of malaria.9 LF is caused by Wuchereria bancrofti, Brugia malayi, and Brugia timori, with > 90% of cases attributable to W. bancrofti.1 Transmission occurs through various mosquito species, primarily Culex (57%), followed by Anopheles (39%), Aedes, Mansonia, and Ochlerotatus. Detailed information on the geographical distribution of the most important LF vectors can be found elsewhere.2 More than 60% of all LF infections are concentrated in Asia and the Pacific region, where Culex is the predominant vector. In Africa, where an estimated 37% of all infections occur, Anopheles is the key vector.2

In 1993, the World Health Organization (WHO) declared LF to be one of six eliminable infectious diseases.10 After several years of preparation and endorsement by the World Health Assembly in 1997, the Global Program to Eliminate Lymphatic Filariasis (GPELF) was initiated in 1998.11 Large-scale operations were launched in 2000, alongside the forging of a worldwide coalition, the Global Alliance to Eliminate Lymphatic Filariasis (GAELF), which is a free and nonrestrictive partnership forum. WHO serves as its secretariat and is being reinforced by an expert technical advisory group.1214 GPELF’s goal is to eliminate the disease as a public health problem by 2020. It mainly relies on mass drug administration using albendazole plus either ivermectin or diethylcarbamazine (DEC). At the end of 2003, approximately 70 million people were treated and 36 countries had an active control program in place.14

Sustained political and financial commitment and rigorous monitoring and surveillance are essential elements of the global program, as otherwise LF could reemerge because a small fraction of the population will continue to carry microfilaria. Furthermore, the vector population is unlikely to be significantly affected by GPELF. Employing a mathematical modeling approach, it was shown that vector control programs, in addition to mass drug administration, would substantially increase the chances of meeting GPELF’s ambitious target.15 Indeed, some of the most successful control programs in the past demonstrate that an integrated approach, readily adapted to specific eco-epidemiologic settings, was a key factor for controlling and even eliminating LF.1619

In rural areas undergoing ecological transformations, particularly due to the construction of irrigation schemes and dams, new breeding sites suitable for filaria vectors are created.16,20 As a consequence, the transmission dynamics of LF is expected to change. In Africa, where Anopheles transmit malaria and filaria, the estimated surface area of 12 million ha under irrigation in 1990 is estimated to increase by one third until 2020.21 Rapid and uncoordinated urbanization often leads to new habitats for filaria vectors.22,23 Especially poor design and lack of maintenance of infrastructures for drainage of sewage and storm water, waste-water management, water storage, and urban subsistence agriculture can facilitate the proliferation of mosquitoes, including those transmitting filaria. Although the proportion of urban dwellers in the least developed countries was only 27% in 1975, it rose to 40% in 2000 and is predicted to further increase. Nearly 50% of the world’s urban population is concentrated in Asia. Currently, the annual growth rate in Asian cities is 2.7%.24 This implies that in the future, an increasing number of habitats with organically polluted water will be available for Culex vectors.

The objectives of the systematic literature review presented in this paper were (i) to assess the current size of the population at risk of LF with particular consideration of water resource development and management, both in rural and urban settings, and (ii) to assess the effect of these ecological transformations on the frequency and transmission dynamics of LF. Our working hypothesis was that environmental changes resulting from water resource development and management adversely affect vector frequencies, filaria transmission, prevalence of infection, and clinical occurrence of LF. These issues are of direct relevance for GPELF and evidence-based policy-making, and for integrated vector management programs and optimal resource allocation for disease control more generally.

MATERIALS AND METHODS

Contextual determinants and estimation of population at risk in endemic countries.

As a first step, we outlined the contextual determinants of LF transmission in a simplified flow chart. For regional estimates of populations at risk of LF, we used the recent classification set forth in the appendices of the annual World Health Report of WHO, which stratifies the world into 14 epidemiologic subregions.9 For estimation of population fractions at risk of LF due to water resource development and management, we adopted setting-specific definitions. Hence, for rural areas we considered those people at risk of LF who live in close proximity to irrigated agro-ecosystems, employing data sources from the Food and Agricultural Organization (FAO; http://www.fao.org). We followed a similar approach as in our preceding work with an emphasis on the malaria burden attributable to water resource development and management.25 In fact, the size of the rural irrigation population was estimated by multiplying the average population density in rural areas by the total area currently under irrigation in LF-endemic countries/territories.

In urban settings, the size of the population at risk of LF was defined by the proportion that currently lacks access to improved sanitation. Country-specific percentages of urban dwellers without access to improved sanitation were taken from the World Health Report 2004.9 Justification for this indicator is derived from the following experiences. First, there is evidence that, besides common water-borne diseases, lack of access to clean water and improved sanitation increases the risk of acquiring vector-borne diseases.23,26,27 As will be shown in our review and has been noted before, LF transmission is spurred by rapid urbanization in the absence of accompanying waste management and sanitation facility programs.2832 Second, a large-scale campaign built around chemotherapy and improved sanitation proved successful to control LF in the Shandong province, People’s Republic of China.33 Third, Durrheim and colleagues recently suggested that chronic parasitic diseases, including LF, could be used as viable health indicators for monitoring poverty alleviation, as the root ecological causes of these health conditions depend on poor sanitation, inadequate water supply and lack of vector control measures.27

Search strategies and selection criteria.

With the aim of identifying all published studies that examined the effect of water resource development and management on the frequency and transmission dynamics of LF, we carried out a systematic literature review. Particular consideration was given to publications that contained specifications on (i) entomological transmission parameters, abundance of vector populations, microfilaria infection prevalence and rates of clinical manifestations as a result of water resource development, and (ii) studies that compared sites where environmental changes occurred with ecologically similar settings where no water resource developments were implemented.

As a first step, we performed computer-aided searches using the National Library of Medicine’s PubMed database, as well as BIOSIS Previews, Cambridge Scientific Abstracts Internet Database Service, and ISI Web of Science. We were interested in citations published as far back as 1945. The following keywords (medical subject headings and technical terms) were used: “lymphatic filariasis” in combination with “water,” “water management,” “reservoir(s),” “irrigation,” “dam(s),” “pool(s),” “sanitation,” “ecological transformation,” and “urbanization.” No restrictions were placed on language of publication.

In a next step, the bibliographies of all recovered articles were hand-searched to obtain additional references. In an iterative process, this approach was continued until no new information was forthcoming.

Dissertation abstracts and unpublished documents (“gray literature”) were also reviewed. Dissertation abstracts were searched in online databases, that is, ProQuest Digital Dissertations and the Unicorn Online Catalogue (WEBCAT) of the London School of Hygiene and Tropical Medicine.

Finally, online databases of international organizations and institutions, namely WHO and FAO of the United Nations, and the World Bank, were scrutinized, adhering to the same search strategy and selection criteria explained above.

RESULTS

Contextual determinants.

The contextual determinants of LF can be subdivided into three broad categories, namely (i) environmental, (ii) biological, and (iii) socioeconomic (Figure 1). They act on different temporal and spatial scales, adding to the complexity of the local LF eco-epidemiology.

In the first category, LF transmission is mainly determined by climatic factors and the formation or disappearance of suitable breeding sites for the vector. Breeding sites can be either natural or man-made, and their productivity exhibits strong heterogeneity, even on a small scale, which in turn governs filarial transmission dynamics.

In rural settings, the most prominent man-made breeding sites are water bodies created by irrigation systems and dams. Here, the weight of environmental determinants is strongly associated with biologic factors, notably vector and parasite species, and various socioeconomic factors such as human migration patterns, access to, and performance of, health systems, and individual protective measures.

In urban areas, artificial breeding sites are often created by waste-water mismanagement, resulting from poor sanitation systems in private dwellings and industrial units, or the absence of them entirely. Here, biological factors shape the epidemiology of LF after environmental changes have occurred, and socioeconomic factors strongly interact with the environmental determinants. The local quality of domestic and industrial wastewater management, access to clean water and improved sanitation, and the construction of roads and buildings depend on the socioeconomic status of specific subpopulations.

Endemic countries/territories.

Table 1 shows estimates of populations at risk of LF for all the countries/territories where the disease is currently endemic. Only politically independent countries were listed (N = 76). Hence, the populations at risk of French Polynesia, New Caledonia, Réunion, and Wallis and Futuna, which belong to France, and American Samoa, which belongs to the United States, were assigned to the geographically closest independent states. Timor-Leste, which recently became independent, is also included. However, no estimates for at-risk populations are currently available for the following LF-endemic countries: Cambodia, Cape Verde, Lao People’s Democratic Republic, Republic of Korea, Solomon Islands, and Sao Tome and Principe. In view of relatively small population sizes living in these countries, neglecting at-risk population of LF there, only marginally influences estimates on regional and global scales.

People at risk of LF at a global and regional scale.

We estimate that approximately half of all people currently living in LF-endemic countries are at risk of the disease, which translates to approximately 2 billion. This is considerably higher than the 1–1.2 billion estimates put forth in the literature.1,2,11 The difference is largely explained by at-risk estimates for China. In urban areas, there are 394.5 million at risk of LF due to lack of access to improved sanitation. This is almost twice the estimated size in rural areas, namely 213 million, which is attributed to living in close proximity to irrigated agriculture. The largest percentages in terms of LF burden, as expressed in DALYs lost (52%), people at risk (29%), size of the population at risk due to proximity to irrigated land (69%), and lack of improved sanitation (33%) are in WHO subregion 12. This subregion includes Bangladesh, India, Maldives, Myanmar, Nepal, and Timor-Leste (Table 2).

Studies identified and qualitative overview.

Overall, 12 studies fulfilled the selection criteria of our literature review. These studies were all published in the peer-reviewed literature, that is, in specialized entomology, parasitology, and/or tropical medicine journals. None of the work retrieved from electronic databases other than PubMed or ISI Web of Science was deemed of sufficient quality to justify study inclusion.

Table 3 summarizes the main findings of the selected studies, stratified by rural and urban settings. As a common theme, LF vector composition frequencies shifted in all settings. Water resource developments favored An. gambiae, An. funestus, An. barbirostris, Culex quinquefasciatus, Cu. pipiens pipiens, Cu. antennatus, and Aedes polynesiensis, but disfavored An. pharoensis, An. melas, An. subpictus, and Ae. samoanus. Transmission parameters were higher in ecosystems altered by water resource projects and clinical disease manifestation rates often elevated.

Vector densities.

In total, seven studies investigated either the shift of LF vector composition frequencies or the change in vector abundance, as shown in Table 4. In two study sites in Ghana and one in the United Republic of Tanzania, composition frequencies of An. gambiae increased in irrigated sites compared with An. funestus.3436 In turn, the relative dominance of An. gambiae was found to be smaller in irrigated areas in the Upper East region of Ghana and in the United Republic of Tanzania.37,38

In absolute numbers (i.e., mosquito counts), changes manifested themselves more prominently. In all settings where water resource developments were implemented, 1.7–24.6 times more An. gambiae were caught when compared with control sites. Similar numbers were found for An. funestus. Another common LF vector in Africa, namely An. melas, could not maintain itself in irrigated areas. Hence, this species disappeared. Most likely, it was replaced by the strongly proliferating An. gambiae s.s. population.35 In Indonesia, An. subpictus was exclusively found in areas without irrigation and An. barbirostris, a typical rice-field breeder, proliferated in villages with irrigated paddies.39

In urban areas on Upolu Island (Samoa), domestic water-storage and waste accumulation provided suitable breeding sites for Ae. polynesiensis, which in turn became the predominant vector in those areas. On the other hand, Ae. samoanus seemed to favor less populated areas where the relative abundance of Ae. polynesiensis was small.30 High numbers of Culex vectors were found in urban areas dominated by waste-water mismanagement and domestic water storage.29,31,32

Transmission parameters.

Table 5 summarizes the five studies that assessed the impact of water resource development and management on transmission parameters. Three studies were carried out in irrigation schemes,36,38,40 one study evaluated the impact of water mismanagement in the face of urbanization,30 and one study was undertaken after a water management control program had been launched.29 Overall, it was found that irrigation, waste-water mismanagement, water storage, or waste accumulation generally lead to increased biting rates, higher transmission potentials, and a higher proportion of vectors infective or infected with microfilaria.

In east Ghana, the annual biting rate (188 versus 299), the annual infective biting rate (0.5 versus 7.7), the annual transmission potential (0.5 versus 13.8), and the percentage of infective An. gambiae (0.3% versus 2.5–3.3%) were notably higher in irrigated villages compared with control villages.38 This study also found a higher percentage of infective An. funestus (0% versus 1.3%) and a higher worm load per infective vector (1.0 versus 1.8) when compared with the nonirrigated villages. A different study that assessed the prevalence of infective filaria in vectors in irrigated villages in southern Ghana recorded even higher fractions of infective An. gambiae (8%) and An. funestus (2%).36 In Sri Lanka, the geometric mean of female Cu. quinquefasciatus per man-hour was 1.6 times higher after the implementation of a large irrigation system.40

An integrated, community-based bancroftian filariasis and malaria control program was carried out in the first half of the 1980s in urban Pondicherry, India, which aimed at transmission reduction by simultaneous implementation of biologic, chemical and physical vector control measures.29 Source reduction by means of environmental management was given high priority. It consisted of draining water-bodies, deweeding, and sealing of tanks and cisterns. Regarding biological control, larvivorous fish were released in permanent water bodies. Larvicides and oil were used as chemical methods, and physical control measures included application of polystyrene expanded beads in wells. Within five years, the annual biting rate for W. bancrofti-transmitting Cu. quinquefasciatus decreased from 26,203 to 3,617, the numer of infective bites per person per year decreased from 225 to 22, and the annual transmission potential decreased from 450 to 77. On the other hand, the worm load increased during the program from 2.0 to 3.5.

The effect of urbanization on transmission parameters of LF has been documented in Samoa. In areas affected by ecosystem transformation, the biting density per man per hour (26 versus 8), the fraction of infected (2.2% versus 1.7%) and infective (0.4% versus 0.3%) Ae. polynesiensis were greater than in areas without ecosystem transformation. On the other hand, biting density per man per hour (67 versus 33) and the percentage of infected (0.5% versus 0.2%) and infective (0.2% versus 0.04%) Ae. samoanus were found to be smaller.30

Filarial prevalence and clinical manifestation rates.

Infection prevalence and clinical manifestations were assessed in seven and two studies, respectively. Table 6 points out that water resource developments had a strong effect on microfilaria infection prevalence. In six settings, prevalence rates were between 0.5% and 19% higher (median: 7%) compared with control areas.

In 2002, Supali and colleagues39 found that in Indonesian villages with irrigated rice agriculture, An. barbirostris was responsible for B. timori transmission. The infection prevalence of B. timori among villagers was 6%, while W. bancrofti infections were not found. As many as 7% of all people were diagnosed with leg elephantiasis, which was associated with brugian filariasis. In irrigation-free villages, the main vector was An. subpictus and human filarial infection prevalence was 12%, but both An. barbirostris vectors and B. timori filaria, were absent. Clinical symptoms appeared as genital lymphedema in 5% of all people.

The most dramatic impact of a water resource development on LF was found in villages of the United Republic of Tanzania a half-century ago. Microfilaria prevalence in two villages with irrigated rice plantations were 11% and 19% higher compared with two nearby villages where no irrigation systems had been constructed.34

In a north Indian area served by irrigation, infection prevalence for W. bancrofti was found to be 0.5% and disease manifestation 1.5% higher compared with a similar setting without irrigation. Close by, in another irrigated plot, but inhabited by people of a different ethnic origin, microfilaria prevalence was 9% greater. Disease manifestations, on the other hand, were almost at the same level (−0.5%).41

Very high W. bancrofti infection prevalence in the population of Leogane, Haiti (39% and 44%), could be attributed to waste-water discharge by factories located in the city. Infection prevalence in control districts without waste-water pools were much lower (27%).31 High prevalence (17%) in a town in the Egyptian Nile delta was due to sewage ponds of public facilities (prevalence of control site: 12%).32 On Samoa, in contrast, in areas affected by human settlements, the prevalence of W. bancrofti infections was 1.1% smaller than in control areas.30

DISCUSSION

Previous studies have shown that the establishment, operation and poor maintenance of water resource development projects, and the process of rapid and uncoordinated urbanization, have a history of facilitating a change in the frequency and transmission dynamics of vector-borne diseases.16,20,22,23 However, detailed analyses on the contextual determinants are sparse.4244 In recent attempts to fill some of these gaps, we systematically reviewed the literature and estimated the current magnitude of urban malaria in Africa45 and examined the effect of irrigation and large dams on the burden of malaria on a global and regional scale.25 Here, we extended our preceding work from malaria to LF, with an emphasis on the effect of water resource development and management, and estimates of at-risk populations.

It is important to note that estimates of populations at risk of LF, as presented in Table 1, differ considerably according to the source of publication. Also, some countries/territories were highly successful in lowering filaria transmission over the past 10–20 years (e.g., China), and therefore care is needed in the interpretation of at-risk population. Our estimate of 2 billion might thus be a significant overestimation.13 The term “at-risk” raises problems with its definition, because in most countries where transmission has been interrupted, the population is still likely to face the risk of reemerging LF epidemics as parasites and vector species continue to be present and environmental conditions are suitable for transmission.

Our population estimates in LF-endemic countries regarding proximity to irrigated areas (i.e., 213 million) are rather conservative. Irrigated areas often attract people, and thus the population density is usually disproportionately high. However, depending on the vector species and the practice of irrigation, the risk profile of LF could also be lower when compared with nonirrigated control areas. For transmission of bancroftian filariasis outside of Africa, it is less the practice of irrigated agriculture per se, but rather the presence of polluted peridomestic man-made breeding sites that are suitable habitats for LF vectors (mostly Culex).

Care should also be exhibited in the interpretation of our at-risk population estimates in urban settings. We used access to improved sanitation as the underlying risk factor to derive our estimates. However, the current definition of access to improved sanitation is primarily constructed by an aggregation of different social and infrastructure determinants rather than setting-specific eco-epidemiologic features. Arguably, this is an oversimplification, as it fails to capture the complex causal webs of the various levels of disease causality, with outcomes shaped by a combination of distal, proximal, and physiologic/pathophysiological causes.46 In fact, settings with access to improved sanitation, as defined by WHO, on the “least improved end” can include highly productive mosquito breeding sites, while mosquito breeding is unlikely to occur in settings on the “most improved end.” Hence, the nature of water-resource development and management in urban areas exhibits strong spatiotemporal heterogeneity, often at very small scales. In addition, the fine-grained detail about waste-water management that would be essential for a precise appraisal of potential vector breeding sites is not available on a scale that would sharply reduce uncertainties in the present report. Nevertheless, the estimates in Table 2 do provide a good approximate indication of the magnitude of the problem. Unfortunately, LF is too far down on virtually all disease priority lists to get serious attention and serve as a basis for establishing the financial resources and political will for water-related improvements in urban areas. It is conceivable that endemic countries could get major LF reductions as a by-product of multifaceted water campaigns that aim to improve overall health in a systemic manner.

The 12 studies we identified through our systematic review can be grouped into two broad categories, namely (i) those that looked at ecosystems influenced by irrigated rural agriculture and (ii) those that investigated urban environments affected by poor design and lack of maintenance of infrastructures for drainage of sewage and storm water. Despite the different nature of these studies, entomological parameters revealed a quite consistent shift in species composition frequencies, and a proliferation of the overall vector population. High abundances were recorded for An. funestus, and especially for An. gambiae, in irrigated agro-ecosystems, particularly in West Africa. Members of the An. gambiae complex are the most anthropophilic filaria vectors.47 In Africa, the fraction of irrigated arable land is still small (8.5%) but is expected to increase significantly in the decades to come.48 Consequently, it is conceivable that implementation of irrigation systems in this region increases transmission of W. bancrofti.49 Achieving the GPELF’s ambitious goal could be of a particular challenge in Africa, where the burden of LF could actually increase.

Regarding the observation of higher counts of vector species following water resource developments, these do not automatically translate into a higher LF burden. Due to the complicated nature of LF pathology and the highly complex transmission dynamics, it is possible that after the implementation of an irrigation system in a highly endemic area, the LF burden could level off after a few years.15,43 The entomological studies carried out in Sri Lanka during the development of the Mahaweli irrigation project in the 1980s revealed that several mosquito species proliferated over the course of project implementation. High densities of Cu. quinquefasciatus, which is the main LF vector in Sri Lanka, were documented, however, filaria transmission could not be confirmed.40,50

It is widely acknowledged that vector species shifts depended on a myriad of factors, i.e., seasonality, temperature, plant succession, irrigation practices, total area under irrigation, water-depth, and water quality.51 In the studies analyzed here, these aspects were not retrievable from the published work. Thus, temporal variations cannot be excluded, rendering study comparison difficult. Future studies should quantify species composition frequencies and vector populations not only between different eco-epidemiologic settings, but also during different seasons and according to different irrigation practices within the same setting.

Once a vector species is replaced by another that transmits a different filaria species, clinical manifestation rates are likely to shift. This was observed in rural Indonesia, where bancroftian filariasis transmitting An. subpictus vectors were replaced by timorian filariasis transmitting An. barbirostris, resulting in a shift from genital lymphedema to elephantiasis.39 In Egypt and Senegal, a similar phenomenon was observed for schistosomiasis. The construction of large dams led to a shift from Schistosoma haematobium to Schistosoma mansoni, most likely because of a shift in intermediate host snails. This was paralleled by a change of clinical manifestation.52,53

Our review only identified two studies that investigated clinical manifestation rates in connection with water projects. Thus, it is difficult to set forth conclusions about whether water resource development projects positively or adversely affect clinical manifestations due to LF. It is delicate to use results on filaria infection prevalence and transmission parameters as proxies, since microfilaremia and clinical symptoms are not implicitly associated. People with clinical manifestations are often amicrofilaremic, while others who are free of symptoms have microfilariae in their blood.54,55 Currently, there is no clear evidence of acquired or innate immunity to filaria infection. Thus, it is uncertain if lower infection rates and clinical manifestation among the local residents could be, at least partially, explained by acquired immunity or innate immunity genes that govern susceptibility to infection and lymphatic pathology.56,57

Another important finding of our systematic literature review is that urbanization, especially in connection with waste-water mismanagement and water-storage, resulted in significant shifts in LF transmission parameters, as demonstrated in Haiti, India, and Samoa. Reverse shifts in the abundance of Ae. samoanus and Ae. polynesiensis, two vectors with varying infectivity rates, indicated that rapid and uncontrolled urbanization impacts differently on various vector species. Decreased transmission parameters of Ae. samoanus in city centers show that urbanization can also marginalize a vector that fails to adapt to the new condition.

We have estimated that > 70% of urban dwellers in LF-endemic areas are currently located in Asia. Cu. quinquefasciatus, the most important LF vector in this region, prefers polluted waters for breeding. The rapid pace at which urbanization continues to build inroads in Asian (and African) countries, often in the face of declining economies, is paralleled by unprecedented pollutions of open waters and sewage systems beyond organic matters. In fact, industrial pollutants and heavy metals transform these water bodies into hostile environments for the living biota, including LF vectors. Therefore, the issue of uncontrolled urbanization and poor waste-water management as a consequence, gains further importance here.

In urban settings, integrated vector management comprising environmental management (e.g., draining) and biological (e.g., introduction of larvivorous fish), chemical (e.g., application of larvicides), and physical (e.g., use of bed nets) control measures can have a significant impact on LF transmission. A prominent example is the community-based integrated control program in Pondicherry, India.29 Despite a somewhat higher worm load 5 years after the control program was launched, transmission parameters dropped significantly. The reason for the increase of the worm load might be due to smaller mosquito populations feeding more exclusively on humans.58 Another example of how an integrated control approach with strong emphasis on environmental management impacts on LF was described by Chernin.28 In Charleston, South Carolina, southern United States, bancroftian filariasis, which was introduced by African slaves, disappeared after the municipal sanitation system had been improved. These measures were initially intended to fight typhoid fever and related infectious diseases. However, they indirectly reduced polluted domestic waters and therefore reduced the available breeding-sites for filaria transmitting Cu. quinquefasciatus.

To further strengthen and expand the current evidence-base of the contextual determinants of LF, additional investigations are warranted. It would be of particular interest to document qualitatively and quantitatively both transmission and disease parameters, coupled with overall changes in key demographic, health, and socioeconomic parameters over the course of major water resource development projects, such as irrigation schemes and large dams. Moreover, it is essential to investigate the role of urban LF, particularly in the light of rapid and uncontrolled urbanization. These investigations are likely to be carried out only if they are incorporated as part of comprehensive waste management and sanitation programs, driven by the need to establish and finance systemic health systems at the city, district, and regional levels. We conclude that integrated vector management, taking into account environmental, biological and socioeconomic determinants, should receive more pointed consideration, as it is a promising approach to complement mass drug administration programs that form the backbone of the GPELF. Without an integrated control approach, the ambitious goal to eliminate LF as a public health problem by 2020 might remain elusive.

Table 1

Estimates of population at risk in all lymphatic filariasis (LF)-endemic countries/territories of the world, stratified into WHO epidemiological subregions (population at risk of LF in thousands)

n.d., no data currently available.
a Except Mauritius, percentages of the population at risk from Lindsay and Thomas,59 recalculated with recent figures from United Nations.60
b Weekly Epidemiological Record.14
c Réunion, French Polynesia, Wallis and Futuna, and New Caledonia belong to France; American Samoa belongs to the United States.
d WHO.61
e For Rwanda the same “at-risk” percentage as for Burundi was taken.
f A significant reduction in prevalence and intensity of microfilaria has recently been recorded in the United Republic of Tanzania, Egypt, Samoa, and Vanuatu.3
g In Brazil, Costa Rica, Suriname, Trinidad and Tobago, and Malaysia, smaller endemic foci have been eliminated.3
h Percentage of people at risk in 1990 taken from Michael and others,62 recalculated with recent figures from United Nations.60
i Pan American Health Organization.63
k Weekly Epidemiological Record.64
l Supali and others.39
m Thailand has recently eliminated filaria transmission.3
n People at risk estimated < 1%.13
o It has been assumed that Brunei Darussalam has the same percentage of people at risk as Malaysia in 1995 as described by Michael and others.62
p Kazura and Bockarie.65
r Korea and the Solomon Islands using diverse control strategies have eliminated transmission.3
Africa
    WHO subregion 1a (24 countries)
        Angola (10,423), Benin (6,736), Burkina Faso (12,963),b Cameroon (9,338), Cape Verde (n.d.), Chad (6,216), Comoros (768),b Equatorial Guinea (89), Gabon (896), Gambia (1,235), Ghana (6,200),b Guinea (8,336), Guinea-Bissau (1,253), Liberia (34), Madagascar including Reunionc (15,841), Mali (11,329), Mauritius (12),d Niger (10,416), Nigeria (121,901), Sao Tome and Principe (n.d.), Senegal (9,247), Seychelles (81), Sierra Leone (890), Togo (1,182)b
    WHO subregion 2a (14 countries)
        Burundi (1,112), Central African Republic (765), Congo (3,396), Côte d’Ivoire (14,253), Democratic Republic of the Congo (22,481), Ethiopia (3,534), Kenya (10,108), Malawi (11,948), Mozambique (15,336), Rwanda (3,355),e Uganda (23,399), United Republic of Tanzaniaf (14,421), Zambia (9,980), Zimbabwe (10,816)
The Americas
    WHO subregion 4 (6 countries)
        Brazilg (3,569),h Costa Ricag (83),h Dominican Republic (1,854),h Guyana (623),h Surinameg (< 4),i Trinidad and Tobagog (< 13)h
    WHO subregion 5 (1 country)
        Haiti (6,078)b
Eastern Mediterranean
    WHO subregion 7 (3 countries)
        Egyptf (2,446),b Sudan (8,302),h Yemen (100)k
Southeast Asia
    WHO subregion 11 (3 countries)
        Indonesia (27,046)h [B. malayi: 27,046, B. timori: 3,900],l Sri Lanka (9,900),b Thailandm (10,116)k [B. malayi: 7,791]k
    WHO subregion 12 (6 countries)
        Bangladesh (93,984),h India (494,374)h [B. malayi: 190,718],h Maldives (< 3),n Myanmar (28,000),b Nepal (1,359),h Timor-Leste (778)i [B. timori: 778]I
Western Pacific
    WHO subregion 13 (1 country)
        Brunei Darussalam (40)o
    WHO subregion 14 (18 countries)
        Cambodia (n.d.), China (925,979)h [B. malayi: 63,906],h Cook Islands including French Polynesiac (248),k Federated States of Micronesia (109),k Fiji including Wallis and Futunac (854),k Kiribati (88),k Lao People’s Democratic Republic (n.d.), Malaysiag (2,736)h [B. malayi: 2,736],h Niue (2),k Papua New Guinea (3,000),p Philippines (23,800)b [B. malayi: 23,800],b Republic of Korear (n.d.), Samoa including American Samoac (248),k Solomon Islandsr (n.d.), Tonga (104),k Tuvalu (11),k Vanuatuf including New Caledoniac (422),k Viet Nam (12,288)h
Table 2

Current global and regional estimates of lymphatic filariasis (LF), including studies identified in our systematic literature review, disability adjusted life years (DALYs), total population, population at risk, population living in proximity to irrigated areas, and urban population without access to improved sanitation

WHO subregionaStudies identifiedDALYs in 2002 caused by LF (× 103)aTotal population in LF-endemic countries (× 103)bPopulation at risk of LF (× 103) (from Table 1)Population in LF-endemic countries living in proximity to irrigated areas (× 103)Urban population in LF-endemic countries without access to improved sanitation (× 103)a
n.d.: no data currently available.
a Source: World Health Report.9
b Source: United Nations Urbanization Prospects—The 2003 Revisions.60
c Without Cap Verde, and Sao Tome and Principe.
d In all countries both endemic for W. bancrofti and B. malayi or B. timori, “population at risk” from the predominant filaria species was taken.
e Without Cambodia, Lao People’s Democratic Republic, Republic of Korea, and Solomon Islands.
f China has considerably reduced LF transmission, therefore those figures are likely to be significantly smaller.
g Without Equatorial Guinea and Seychelles.
h Without Maldives and Timor-Leste.
i Without Cook Islands, Federated States of Micronesia, Kiribati, Niue, Papua New Guinea, Samoa, Solomon Islands, Tonga, Tuvalu, and Vanuatu.
k Without Liberia, Sao Tome and Principe, and Seychelles.
l Without Trinidad and Tobago.
m Without Federated States of Micronesia, Malaysia, Tonga, and Tuvalu.
13976284,551235,382c574g38,445k
221,035312,344144,90330525,956
409193,8926,14730625,570l
5118,3266,078< 11,561
71122125,55110,8471,6462,265
901n.d.n.d.n.d.n.d.
111242302,78147,062d8,26231,212
1232,9771,287,945618,496d147,894h131,157
130035840< 1n.d.
1414111,565,246970,589d,e,f54,034i176,791m
Total125,7774,079,9952,039,548213,021394,511
Table 3

Overview of studies meeting our inclusion criteria that assessed the effect of water resource development and management on changes of lymphatic filariasis (LF), including vector composition, vector abundance, transmission parameters, filaria infection prevalence, and clinical manifestation rates, as stratified by rural and urban settings in different WHO subregions of the world

SettingWHO subregionCountry, year of study (reference)Water resource development and managementVector species (filaria species)Shift in vector compositionVector abundanceTransmission parametersHuman infection prevalenceClinical manifestation
↑: increase in sites where water-related change occurred; ↓: decrease in sites where water-related change occurred; = : no change.
a Genital lymphedema.
b Elephantiasis.
c Except “number of infective larvae per mosquito,” which was decreasing.
Rural1Ghana, 2000 (Appawu and others38)Irrigated agricultureAn. gambae (W. bancrofti)
An. funestus (W. bancrofti)
Cu. quinquefasciatus (none)
An. pharoensis (none)
An. nili, An. rufipens, Ae. aegypti (none)
Rural1Ghana, 1995 (Dzodzomenyo and others36)Irrigated agricultureAn. gambiae s.l. (W. bancrofti)
An. funestus (W. bancrofti)
Cu. quinquefasciatus (none)
An. Pharoensis (W. bancrofti)=
Rural1Ghana, 1993 (Appawu and others35)Rice irrigationAn. gambiae s.s. (W. bancrofti)
An. melas (W. bancrofti)
Rural2United Republic of Tanzania, 1956 (Jordan34)Rice irrigationAn. gambiae (W. bancrofti)
An. funestus (W. bancrofti)
Rural2United Republic of Tanzania, 1951–1953 (Smith37)Rice irrigationAn. gambiae (W. bancrofti)
An. funestus (W. bancrofti)
Rural11Indonesia, 2001 (Supali and others39)Rice irrigationAn. subpictus (W. bancrofti)a
An. barbirostris (B. timori)b
Rural12Sri Lanka, 1986–1987 (Amerasinghe and others40)Rice irrigationCu. Quinquefasciatus (W. bancrofti)
Rural12India, 1957 (Basu41)Irrigation, sullage, storm-water drainsCu. Quinquefasciatus (W. bancrofti, B. malayi)
Urban5Haiti, 1981 (Raccurt and others31)Water storage, waste-water managementCu. Quinquefasciatus (W. bancrofti, B. malayi)
Urban7Egypt, 1986 (Gad and others32)Waste-water poolsCu. pipiens pipiens, Cu. Antennatus (W. bancrofti)
Urban12India, 1987 (Rajagopalan and others29)Waste-water canals, pits, reservoirsCu. Quinquefasciatus (W. bancrofti)c
Urban14Samoa, 1978–1979 (Samarawickrema and others30)Man-made breeding sites, water storageAe. Polynesiensis (W. bancrofti)
Ae. Samoanus (W. bancrofti)
Table 4

Absolute and relative change in abundance of different filaria vectors in areas where water resource development and management (WRDM) occurred compared to similar control-sites without WRDM

Control siteWRDM occurredAbsolute and relative change in abundance
Country, year of study (reference)Type of changeVector speciesNo.%No.%No.Factor
dis.: disappearance of vector after WRDM; ↑: increase; ↓: decrease.
a Not filaria transmitting.
Ghana, 2000 (Appawu and others38)Irrigated agriculture (site 1/site 2)An. gambiae s.l.75687.71,256/1,83181.9/73.1+500/+1,0751.7/2.4
An. funestus485.6254/47116.5/18.8+206/+4235.3/9.8
Cu. quinquefasciatusa515.90/1280/5.1−51/+77dis./2.5
An. pharoensisa20.20/270/1.1−2/+25dis./13.5
An. nili,aAn. rufipens,a and Ae. Aegypti50.624/471.6/1.9+19/+424.8/9.4
Ghana, 1995 (Dzodzomenyo and others36)Irrigated agricultureAn. gambiae s.l.151214177+1269.4
An. funestus101824022−610.4
Cu. quinquefasciatusa5400−5dis.
An. pharoensis323101
Ghana, 1993 (Appawu and others35)Rice irrigation (site 1/site 2)An. gambiae s.s.27/1796/9450100+23/+331.9/2.9
An. melasa1/14/600−1/−1dis.
Sri Lanka, 1986–1987 (Amerasinghe and others40)Rice irrigationCu. quinquefasciatus20948.346779.8+2582.2
Cu. pseudovishnuia22451.711820.2−1060.5
Samoa, 1978–1979 Samarawickrema and others30)Man-made breeding sites, water storageAe. polynesiensis
Ae. samoanus
United Republic of Tanzania, 1956 (Jordan34)Rice irrigationAn. gambiae2996.771499.6+68524.6
An. funestus13.330.4+23
United Republic of Tanzania, 1951–1953 (Smith37)Rice irrigationAn. gambiae2,05799.93,95999.7+1,9021.9
An. funestus20.1290.3+2714.5
Table 5

Transmission parameters of different filaria vectors in areas where water resource development and management (WRDM) occurred compared to control areas without WRDM

Country, year of study (reference)Type of changeTransmission parameters of different filaria vectorsControl siteWRDM occurredRelative change
n.a.: not applicable.
Ghana, 2000 (Appawu and others38)Irrigated agriculture (site 1/site 2)Annual biting rate of An. gambiae and An. Funestus1882991.6
Annual infective biting rate of An. Gambiae and An. Funestus0.57.715.4
Worm load of An. gambiae and An. funestus1.01.81.8
Annual transmission potential of An. Gambiae and An. Funestus0.513.827.6
Infective An. gambiae0.3%3.3%/2.5%11/8.3
Infective An. funestus0%0%/1.3%n.a.
Ghana, 1995 (Dzodzomenyo and others36)Irrigated agricultureInfective An. gambiae8%
Infective An. funestus2%
Infected An. gambiae27%
Infected An. funestus16%
Sri Lanka, 1986–1987 (Amerasinghe and others40)Rice irrigationGeometric mean female Cu. Quinquefasciatus per man-hour4.67.41.6
India, 1979–1985 (Rajagopalan and others29)Vector control programAnnual biting rate of Cu. quinquefasciatus26,2033,6170.1
Annual infective biting rate of Cu. Quinquefasciatus225220.1
Worm load of Cu. quinquefasciatus2.03.51.8
Annual transmission potential of Cu. Quinquefasciatus450775.8
Samoa, 1978–1979 (Samarawickrema and others30)Man-made breeding sites, water storageBiting density per man-hour of Ae. Polynesiensis8263.3
Infected Ae. polynesiensis1.7%2.2%1.3
Infective Ae. polynesiensis0.3%0.4%1.3
Biting density per man-hour of Ae. samoanus67330.5
Infected Ae. samoanus0.5%0.2%0.4
Infective Ae. samoanus0.2%0.04%0.2
Table 6

Filaria prevalence and frequencies of clinical manifestations in areas where water resource development and management (WRDM) occurred compared to similar areas without WRDM

Country, year of study (reference)Type of WRDMFilaria vector or clinical symptomsControl siteWRDM occurredChange in absolute terms
Indonesia, 2001 (Supali and others39)Rice irrigationW. bancrofti12%0%Absence
B. timori0%6%+6%
Genital lymphedema5%0%Absence
Elephantiasis0%7%+7%
Egypt, 1986 (Gad and others32)Areas around large cesspit/small cesspitW. bancrofti12%17%/7%+5%/−5%
Haiti, 1981 (Raccurt and others31)Waste-water area/area with water-storageW. bancrofti27%39%/44%+12%/+17%
Samoa, 1978–1979 (Samarawickrema and others30)Man-made breeding sites, water storageW. bancrofti5.3%4.2%−1.1%
India, 1957 (Basu41)Rice irrigation, sullage, and storm-water drains in 2 sites (site 1/site 2)Mixed infection of B. malayi and W. bancrofti (ratio 74:26)5%/2%5.5%/12%+0.5%/+9%
Genital lymphedema and elephantiasis3.5%/3%5%/2.5%+1.5%/−0.5%
United Republic of Tanzania, 1956 (Jordan34)Rice irrigationW. bancrofti7%26%+19%
United Republic of Tanzania, 1951–1953 (Smith37)Rice irrigationW. bancrofti12%23%+11%
Figure 1.
Figure 1.

Contextual determinants of lymphatic filariasis.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 3; 10.4269/ajtmh.2005.73.523

*

Address correspondence to Jürg Utzinger, Department of Public Health and Epidemiology, Swiss Tropical Institute, CH-4002 Basel, Switzerland. E-mail: juerg.utzinger@unibas.ch

Authors’ addresses: Tobias E. Erlanger, Jennifer Keiser, Marcel Tanner, and Jürg Utzinger, Swiss Tropical Institute, P.O. Box, CH–4002 Basel, Switzerland. Marcia Caldas de Castro, Department of Geography, University of South Carolina, 125 Callcott Hall, Columbia, SC 29208. Robert Bos, Department of Protection of the Human Environment, World Health Organization; 20 Avenue Appia, CH–1211 Geneva 27, Switzerland. Burton H. Singer, Office of Population Research, Princeton University, 245 Wallace Hall, Princeton, NJ 08544.

Acknowledgments: The authors thank Dr. Felix P. Amerashinge, Prof. David H. Molyneux, Dr. Will Parks, Dr. Erling Pedersen, and Dr. Christopher A. Scott for valuable comments on the manuscript. We also thank Jacqueline V. Druery and her team from Stokes Library at Princeton University for help in obtaining a large body of relevant literature.

Financial support: This investigation received financial support from the Water, Sanitation and Health unit and the Protection of the Human Environment (WSH/PHE) at the World Health Organization (WHO ref. Reg. file: E5/445/15). The research of J. Keiser and J. Utzinger is supported by the Swiss National Science Foundation (Projects PMPDB–106221 and PPOOB–102883, respectively). M. C. Castro is grateful to the Office of Population Research and the Centre for Health and Wellbeing at Princeton University.

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Author Notes

Reprint requests: Jürg Utzinger, Department of Public Health and Epidemiology, Swiss Tropical Institute, CH–4002 Basel, Switzerland, Telephone: +41 61 284-8129, Fax: +41 61 284-8105, E-mail: juerg.utzinger@unibas.ch.
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