The Attributable Fraction of the Lymphatic Filariasis Burden to Water
Resource Development and Management
Report prepared for the WHO commissioned study Burden of water-related vector-borne
diseases: An analysis of the fraction attributable to components of water resources development
and management.
Investigators:
Tobias E. Erlanger, Jennifer Keiser, Marcel Tanner, Jürg Utzinger
Swiss Tropical Institute, P.O. Box, CH-4002 Basel, Switzerland
Marcia Caldas de Castro, Burton H. Singer
Office of Population Research, Princeton University, Princeton, NJ 08544, USA
Robert Bos, Jamie Bartram and Laurence Haller
Water, Sanitation and Health (WSH/PHE), World Health Organization, Avenue Appia 20,
CH-1211 Geneva 27, Switzerland
Contents:
Main Objective
page 3
Approach
page 3
Outcomes
page 4
Conclusion
page 5
Outlook and Perspectives
page 5
Appendix 1
Search strategy and selection criteria for the
comprehensive literature review
page 12
Number of hits for lymphatic filariasis combined with
selected keywords in different electronic databases
page 13
Appendix 3
Relevant literature to address the main research objective
page 14
Appendix 4
Published review paper American Journal of
Tropical Medicine and Hygiene
page 15
Table summarising geographical distribution of the three
Filaria species, ecology of their vectors and environmental
changes leading to increased vector densities
page 36
Appendix 2
Appendix 5
Appendices 6.1–6.14 Key information form of all retrieved publications
2
page 37
Main Objective
In order to strengthen the evidence base in support of decision-making on
different intervention options for vector-borne disease prevention and control in the
context of water resources development and management, WHO commissioned
systematic literature reviews on the association between such development and the
burden of four vector-borne diseases.
In accordance with this mandate, the main objective of work reported here was to:
strengthen and expand the current evidence-base of contextual determinants of
lymphatic filariasis (LF) and to assign and quantify attributable fractions of the disease
burden to specific components of water resources development and management.
This implies the need for (i) the definition and characterization of the contextual
determinants of LF; (ii) the compilation of critical LF statistics on a global and regional
scale (stratified according to the 14 WHO sub-regions of the world); (iii) a systematic
literature review; and (iv) preparation of an analytical report, including questions that
remained unanswered and a mapping out of directions for future work.
This report summarises the research approach taken and provides an outlook and
possible perspectives on how to move forward in view of identified research priorities.
The main findings of the systematic review can be found in appendix 4, which contains
the text of the article published in the peer-reviewed literature.
Approach
For the sake of the current report, LF is defined as a communicable parasitic
disease caused by Wuchereria bancrofti, Brugia malayi or Brugia timori that can clinically
manifest itself in the form of lymphedema or elephantiasis. Other diseases caused by
Filarioidea (e.g. onchocerciasis and dracunculiasis) are not considered here.
A systematic literature review was carried out to identify all published studies that
examined the effect of water-related environmental changes on the frequency and
transmission dynamics of LF. Special consideration was given to publications that (i)
presented information on the sequential cause-and-effect relationships between waterrelated environmental change, abundance of vector populations, entomological
transmission parameters, microfilaria infection prevalence and rates of clinical
3
manifestations, and/or (ii) compared .the epidemiological conditions in sites where
ecosystems had been modified by water resources development with those in
ecologically similar settings without such change. The main findings were synthesised
and formatted into a review paper (Appendix 4).
First, a schematic concept of the contextual determinants of LF was developed.
Next, the fraction of the population at risk of LF was estimated in all 76 countries that are
currently endemic for this disease. At-risk populations in rural and urban areas of all
WHO sub-regions were linked with the most recent burden of disease statistics
expressed in disability adjusted life years (DALYs). We employed the recent
classification, as presented in the appendices of the WHO World Health Report 2004,
which stratifies the world into 14 epidemiological sub-regions. At-risk populations in rural
settings were defined by people living in close proximity to irrigated agro-ecosystems in
those sub-regions where rural LF transmission occurs; in urban settings they were
defined as people lacking access to improved sanitation in those sub-regions where
urban LF transmission occurs. In the context of this report, improved sanitation systems
include facilities which are designed and maintained in a way that they do not favour the
proliferation of LF vectors. The size of the rural population was estimated by multiplying
the average population density in rural areas with the total area under irrigation in the LF
endemic countries. Statistics on urban dwellers lacking access to improved sanitation
were taken from the World Health Report 2004.
Outcomes
Appendix 1 summarises the search strategy and selection criteria that we
employed to address this objective. Appendix 2 shows the number of hits for different
key words derived from a set of electronically-available databases that are widely used
for literature reviews. PubMed/Medline was found to be the most comprehensive
database, as it comprised most of the literature cited in the other databases that we
screened. Our extensive literature search pertaining to the main objective of this project
yielded only 14 articles, all of which were published in the peer-reviewed literature
(Appendix 3). Two out of these 14 contain descriptive data and were therefore not
included in the systematic review article that was published in the peer reviewed
literature. The review article (Appendix 4) presents a panel that lists the population at risk
in all 76 countries endemic for LF, a figure that summarises the contextual determinants
of LF and four tables that show the main findings of vector abundance, transmission and
clinical manifestation rates. An estimate of the size of the population at higher risk due to
4
irrigation and inadequate sanitation is also presented in the article. As a general
guidance, a table that shows the geographical distribution and ecology of major LF
vectors was compiled (Appendix 5). Finally, from all selected publications, including the
ones with descriptive data, the key information (KIF) was retrieved and summarised in a
standardised format, which is presented in Appendices 6.1–6.14.
Conclusion
The objective of this study was to strengthen and expand the current evidencebase of contextual determinants of LF, and to assign and quantify attributable fractions of
the disease burden to specific components of water resources development and
management and generally of water-related environmental change. It is part of a larger
investigation examining the effect of water resources development and management on
four vector-borne diseases, the other three being malaria, schistosomiasis and Japanese
encephalitis.
It was intended to quantify the burden of LF attributable to ecosystem change, with
special reference to the changes in local hydrology, through the use of comparative risk
assessment (CRA). Utilising counterfactual analysis, studies were required that examine
alternative scenarios, thereby describing changes in the exposure to risk factors. Hence,
an ideal study would be one that presents data in the initial steady-state (often natural)
environment, e.g. prior to the implementation of a water resources development project.
It would then describe changes that occurred during project implementation and, finally, it
would assess the impact on filarial transmission, prevalence and morbidity several years
after implementation. Unfortunately, not a single study was identified which fulfilled these
criteria. Most studies either simply quantified prevalence rates or entomological
parameters in a specific region (e.g. without differentiating between communities with
and without water resource development) or were carried out after the completion of a
water resource development project. The fact that the majority of publications are lacking
profound environmental, ecological or socio-economic data made it difficult to link
outcome measures with water-related or other risk factors.
It had been suggested that due to scarcity of detailed analyses, the adoption of
indirect methods may be required by calculation of relative risk (RR). Compared with
other diseases (e.g. schistosomiasis), the application of indirect methods to calculate RR
in the case of LF is very delicate. This is explained by the fact that prevalence rates and
morbidity of LF strongly depend on socio-economic, environmental and ecological factors.
5
To date, however, these dynamics have been poorly explored and are far from fully
understood.
A comparison between areas affected by water resources development projects
and areas with similar ecological and epidemiological characteristics but with no water
resource projects might be possible but analysis requires great care. Applying study
results from a specific site to other more distant areas with similar climatic characteristics
is even more arguable, because of small-scale heterogeneities (e.g. prevalence rates
vary between villages while climatic parameters are similar).
In view of the very few high-quality studies and the lack of a good understanding of
basic transmission dynamics of LF in relation to water resources development and
management, we conclude that it is currently not possible to calculate the population
attributable fraction of risk factors or assign and quantify attributable fractions of disease
burdens caused by LF. It was not feasible to derive DALY estimates for the 10 relevant
WHO-designated sub-regions of the world.
Outlook and Perspectives
Undoubtedly, the potential impact of water resources development and
management impact on transmission parameters of LF is considerable, but many critical
questions remain unanswered. Obviously, the dearth of LF-based studies pertaining to
water resources development and management cannot be caught up with within the next
few years.
Here we propose a selection of research priorities in the field of LF, without considering
research pertaining to clinical aspects, drug development, immunology and molecular
parasitology. In our view, some important questions include:
(1) What is the impact of water resources development and management projects on the
frequency and transmission dynamics of LF in different eco-epidemiological settings?
(2) What is the relationship between filaria transmission and infection prevalence or
infection intensity and clinical manifestation rates, particularly in regions with altered
transmission (vector species succession, transmission intensification) due to water
resources projects?
6
(3) What are the specific risk factors, including ecological, epidemiological and socioeconomic, of LF in a certain region?
(4) How big is the impact of rapid urbanisation, accompanied with lack of sufficient
sanitation facilities, water-storage, urban and peri-urban subsistence agriculture or
wastewater mismanagement on the transmission of filariae?
In the following part we further explore these research priorities 1-4 and propose
concrete strategies to tackle these questions.
(1) The fundamental question, whether or not, how and how much water resources
development and management projects impact on the transmission dynamics and
prevalence of LF remains to be answered.
On the basis of our comprehensive literature search and the identification of 14
publications, we were able to carry forward this task. By a meta-analysis of the identified
publications, we reviewed and synthesised the outcomes and produced an article that
has been published in the peer-reviewed literature.
Special attention has been paid to typical agricultural practices currently employed in the
high burden areas of LF and the predicted development of water resources (e.g. irrigated
rice agriculture). The question how water resource development and management
projects impact on LF can, however, only be answered satisfactorily when the
epidemiological parameters in affected communities and control communities are
monitored prior, during and after their implementation. In other words, environmental and
social determinants, transmission indicators and infection and disease prevalences
should be kept under rigorous surveillance for an adequate number of years.
Conceivably, the LF situation could be compared with that of malaria. This is justified on
several grounds: First, in some regions of the world the same vectors transmit both LF
and malaria (e.g. in West Africa Anopheles funestus and Anopheles gambiae). Second,
both diseases depend on similar risk factors, e.g. low socio-economic status, poor
housing conditions, and limited access to health care systems. Third, while the majority
of the global LF disease burden is concentrated in Asia – where the main vectors are
Culex ssp. – the malaria burden is currently concentrated in sub-Saharan Africa.
Importantly, Asia provides suitable environmental conditions for Anopheles species,
harbours more people than any other continent and contains the biggest proportion of
irrigated agriculture. The correct interpretation of this discrepancy will provide further
7
insight into the complex issue of “parasite-vector-environment” relations, both for LF and
malaria.
(2) The relation between transmission, the prevalence of infection and clinical
manifestations, particularly infection intensity (worm load) and LF morbidity is still not
fully understood. In areas where ecological transformations have occurred, e.g. through
the development of irrigation systems, this issue gains in importance. Such
transformations often lead to the creation of breeding sites or they diminish or alter
existing breeding habitats suitable for filaria vectors. As a consequence, the density of
vector populations fluctuates and vector species composition changes. Therefore,
environmental alterations potentially have an impact on filaria transmission. It has to be
assumed that higher filaria transmission gradually increases infection prevalence and the
worm burden. Thus, morbidity and clinical manifestation rates are expected to increase.
In the case of LF, the connection between transmission, infection and morbidity is
complex and often contradictory. Previous studies showed that people with elephantiasis
are often amicrofilaraemic while others have a high grade of infection but show no
clinical signs. The study design already described in (1) could also be applied for
investigating the connection between filaria infection and clinical disease manifestations.
Special attention has to be given to the confounding factors resulting from the fact that
regions with improved water resources facilities attract people. The influx of people from
areas with either low or high LF transmission can bias the outcome of a study.
To tackle these questions, we propose to design a research project of the following kind:
The investigation should be implemented in an area where a water resources
development project is planned. Prior to its implementation, a baseline cross-sectional
survey will assess infection prevalence, clinical manifestation rates and transmission
parameters of all filaria vectors. Further, demographic parameters such as ethnicity,
socio-economic status, and migration patterns of the affected population should be
recorded. At the next phase, designed as a cohort-study, the research will assess
infection prevalence, clinical manifestation rates and transmission parameters of all filaria
vectors during the construction and implementation of the water resources project. After
the project’s completion, the area should be further monitored and all parameters reassessed longitudinally for at least another five years. The outcomes of such a study
holds promise to examine and quantify how transmission parameters, infection
prevalence and clinical manifestation rates are interrelated. Further, it will expand the
8
current evidence base of adverse determinants attributable to water resources
development.
Future water resource development should include in-depth assessment of potential
health impacts, including LF. Indeed, institutionalisation of health impact assessments
(HIAs) for development projects quite generally, analogous to environmental impact
assessments, would lead to information requirements that could fill many of the data
gaps described in this review. In addition, mitigation strategies to alleviate potential
negative health impacts – of which LF might be only one component – would also be part
of the process of implementing new water projects. Introduction of monitoring and
surveillance systems proximal to such water projects would facilitate systematic
evaluation of the impact of these ecosystem interventions over time. This, in turn, would
greatly improve our understanding of the role of dams and irrigation systems in either
promoting or reducing LF transmission.
Shedding light on these dynamics is an essential step towards a complete understanding
of the disease. It will also help sustain the achievements of the Global Alliance to
Eliminate Lymphatic Filariasis (GAELF). This initiative aims to reduce filaria infection
prevalence and clinical manifestation rates to nearly zero by wide-spread chemotherapy.
Complete elimination is, however, not feasible and vector populations will be unaffected
by the GAELF. To prevent resurgence and proliferation of LF in the future, the strategy of
GAELF has to be upgraded to include a vector control component. A better
understanding of the disease is the basis for a sustainable control strategy that also
targets the vector population.
(3) For prevention and sustainable control of LF it is crucial to have a clear perception of
its risk factors. To date, the vast majority of studies focused on transmission rates,
infection prevalence or frequencies of clinical symptoms but did not define risk factors
and other determinants of LF. It is of great importance to investigate the major risk
factors for LF in the context of specific areas. As already mentioned under item (1), the
development of water resources potentially creates several new risks and aggravates
common risk factors. Other determinants also alter key parameters of LF. Taking the
construction of irrigation systems as an example, we here describe what kind of risk
factors and determinants have to be considered and how their magnitude can be
estimated:
9
Socio-economic factors
People in irrigated areas benefit from higher agricultural yields and can improve their
socio-economic status. This translates into potentially better access to health services,
increased means to purchase health services and products, and improved nutritional
status. Alleviation of poverty will, therefore, have an impact on LF morbidity. Irrigation
schemes also attract a work force which may have a different socio-economic status. In
the case of LF, studies should always consider the socio-economic status of an affected
population and differentiate groups with different levels of vulnerability, as well as the
evolution of vulnerability over time.
Population density, immigration
Areas in which irrigated agriculture is practiced or where man-made reservoirs are
created attract people and this results in higher population densities. It significantly alters
the demographic structure around water resources development projects. This may lead
to the creation of several new risk factors, including those linked to wastewater
accumulation, waste mismanagement and poor housing conditions. Furthermore,
immigrants may be more susceptible to LF infections if they come from regions with less
filaria transmission. In turn, immigrants from regions where LF is highly endemic will
introduce filariae and thus change transmission intensity in regions where LF
transmission used to be non-existent or low. Studies are needed to elucidate how higher
population densities and human movement, in connection with water resources
development, affect transmission and morbidity of LF.
Artificial breeding-sites and habitat change
Irrigation creates or changes breeding sites that are suitable for filaria vectors. New
plants and animals or the marginalisation of species can lead to shifts in vector species
composition, and can introduce new vector species. As a consequence, vector
transmission parameters change and eventually the frequency and intensity of clinical
manifestation will also change. To investigate these determinants, transmission
parameters, vector species composition, infection prevalence and clinical manifestation
rates have to be investigated prior, during and after the construction of irrigation systems.
As the transmission can vary from year to year it is crucial to monitor those LF
parameters over a period of several years.
10
Exposure
Exposure is a factor that directly influences vectorial capacity. If the human–vector
contact is altered, this affects prevalence rates as well. The factors described above also
influence
human
exposure
to
filaria-transmitting
mosquitoes.
Socio-economic
improvement can result in better housing conditions or an improved capacity to purchase
insecticide-treated mosquito nets. Migration of labour force, e.g. farmers, into areas
where Culex is active, can be expected to result in an increased exposure to vectors.
Vector species composition shifts can promote mosquitoes whose “time of biting activity”
and host preference is different. We suggest these factors be considered integrally in
future investigations.
(4) Currently, the connection between rapid, uncontrolled urbanisation and the
proliferation of LF is not well understood. This topic is, however, of considerable public
health significance and is expected to further gain in importance, particularly in view of
the rapid pace of urbanisation, notably in areas where LF poses high levels of risk (Asia
and sub-Saharan Africa). In shanty towns, for example, the building of small-scale
irrigation systems, the storage of water for household consumption and the lack of
improved sanitation facilities can influence the frequency and transmission dynamics of
LF. Due to rapid environmental transformation and population growth, peri-urban settings
are considered to be particularly challenging for health research and planning. Our
systematic review underscores the need to assess the importance and magnitude of
urban LF and we suggest this had best be achieved by the following study design:
First, infection prevalence and morbidity of LF can be assessed by means of crosssectional studies carried out in various urban settings, e.g. in shanty towns, areas with
subsistence agriculture and in inner cities. Second, breeding-sites of filaria vectors
should be defined and the mechanics of their creation described. Third, all important risk
factors and determinants should be assessed.
Tackling these three issues will lead to a better understanding of the dynamics and the
contextual determinants of LF in relation to water resources development and
management, infection, morbidity and urbanisation. Findings from these studies will form
an important basis for the design and implementation of LF-control strategies, more
appropriate planning of water resources development and management projects and the
incorporation of effective health safeguards in urban planning and development.
11
Appendix 1: Search strategy and selection criteria for our comprehensive
literature review
First, a literature search with special emphasis on research findings published over the past 25
years was carried out using the National Library of Medicine’s PubMed database, OVID
Technologies (WebSPIRS 5.02), Cambridge Scientific Abstracts Internet Database Service and
Thomson ISI (previously known as Institute for Scientific Information). With special consideration
of potential bias of research findings during the DDT era, we also included published work
between 1945 and 1975.
PubMed/Medline contains citations published mostly from 1966 to the present, whereas
Thomson ISI database dates back to 1945. The following keywords were employed to search the
above-mentioned databases and websites: “lymphatic filariasis” in combination with “malaria”,
“epidemics”, “water”, “sanitation”, “water supply”, “water development”, “irrigation”, “dam(s)”,
“recreation”, “diversion”, “pool(s)”, “drainage”, “water reservoir(s)”, “water management”, “drinking
water”, “downstream”, “upstream”, “sea water”, “environmental management” (“modification”,
“manipulation”), “water storage”, “flood control”, “water purification”, “impoundment”, “barrage”,
“navigation”, “humidity”, “environment” and “environmental”.
Second, this search was complemented with an iterative proceeding in which we consistently
reviewed reference lists of all those publications that were of relevance to address our main
objective. The bibliographies of all these recovered manuscripts were retrieved again and the
searching strategies repeated until no new information was forthcoming.
Third, we also performed computer-aided searches of the websites of the following organisations
and institutions: World Health Organisation (WHO), Food and Agriculture Organisation of the
United Nations (FAO), World Bank, Centers for Disease Control and Prevention (CDC, Atlanta),
online catalogues of the University of Basel and Princeton University. The yields of these
searches were found to be meagre.
Third, dissertation abstracts and unpublished documents (‘grey literature’) were reviewed.
Dissertation abstracts were searched in following databases (accessed on 23.12.2004):
- www.google.com
- ProQuest Digital Dissertations (http://wwwlib.umi.com/dissertations).
- Wageningen Dissertation Abstracts (http://www.agralin.nl/wda/).
- Index of Theses. A comprehensive listing of abstracts by universities in Great Britain and
Ireland (http://www.theses.com/).
- COPAC union online catalogue of the members of the Consortium of University Research
Libraries (CURL) (http://www.copac.ac.uk/).
- Cambridge Scientific Abstracts Internet Database Service:
(http://www.lib.ecu.edu/erdbs/csa.html).
- M25 Consortium of Academic Libraries (http://www.m25lib.ac.uk/).
- The Unicorn Online Catalogue (WEBCAT) of the London School of Hygiene and Tropical
Medicine (http://193.63.251.23/uhtbin/cgisirsi).
- IRIS Interdisciplinary Online-Databases (www.libiris1.ict.ac.uk).
- Library Online Catalogue IDS Basel/Bern (http://aleph.unibas.ch).
- University of Chicago, Center for Research Libraries, Foreign Doctoral
Dissertations (http://wwwcrl.uchicago.edu/content.asp).
- University of Berkeley Digital Library (http://sunsite.berkeley.edu/Libweb/).
For this search we employed the same keywords as described above for the peer-reviewed
literature search. Through these databases no useful additional data could be found.
The peer-review literature and dissertation abstract search made it clear that in this field of
research only a small number of studies were done and even fewer published. Since the “grey
literature” is mostly not listed in any database it cannot be retrieved remotely by electronic
search-engines.
12
Appendix 2. Number of hits for “lymphatic filariasis” combined with selected
keywords in different electronic databases (accessed January 15 2005)
Search term
Database
PubMed
OVID
Web of Cambridge Scientific Abstracts World
MedLine Technologies Science
Internet Database Service
Cat
Environmental Agricola GeoRef
Sciences &
Pollution
Management
Lymphatic filariasis
Lymphatic filariasis and
epidemics
Lymphatic filariasis and water
Lymphatic filariasis and
sanitation
Lymphatic filariasis and water
supply
Lymphatic filariasis and water
development
Lymphatic filariasis and irrigation
Lymphatic filariasis and dam(s)
Lymphatic filariasis and
recreation
Lymphatic filariasis and diversion
Lymphatic filariasis and pool(s)
Lymphatic filariasis and drainage
Lymphatic filariasis and
reservoir(s)
Lymphatic filariasis and
management
Lymphatic filariasis and drinking
Lymphatic filariasis and
downstream
Lymphatic filariasis and
upstream
Lymphatic filariasis and sea
water
Lymphatic filariasis and
environmental management
(modification, manipulation)
Lymphatic filariasis and storage
Lymphatic filariasis and flood
control
Lymphatic filariasis and water
purification
Lymphatic filariasis and
impoundment
Lymphatic filariasis and barrage
Lymphatic filariasis and
navigation
Lymphatic filariasis and humidity
Lymphatic filariasis and
environment
Lymphatic filariasis and
environmental
1584
425
659
1
953
3
8
4
0
77
0
33
13
10
4
15
3
1
0
0
1
0
5
1
1
0
0
0
0
13
4
0
0
0
0
0
6
0 (2)
0
3
0 (1)
0
3
0 (1)
0
0
0
0
0
0
0
0
0
0
0
0
13 (8)
6
9 (14)
0
12 (9)
0
2(2)
0
13 (10)
3
4 (3)
0
0
0
0
0
0
0
0
0
0
0
0
0
0
46
29
26
0
0
0
6
3
0
1
0
2
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
3
0
0
0
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
4
52
3
5
2
11
0
0
0
0
0
0
0
0
29
22
17
0
0
0
0
13
0
0
Appendix 3. Relevant literature to address our main research objective (in inverse
chronological order)
Smith A. The transmission of bancroftian filariasis on Ukara Island, Tanganyika II. The
distribution bancroftian microfilaraemia compared with the distribution hut-haunting
mosquitoes and their breeding-places. Bulletin of Entomology Research. 1955;46:437444.
Jordan P. Filariasis in the lake province of Tanganyika. East African Journal. 1956
Jun;33(6):237-42.
Basu PC. Filariasis in Assam state. Indian Journal of Malariology. 1957;11:293-308.
Partono F, Pribadi PW, Soewarta A. Epidemiological and clinical features of Brugia timori in a
newly established village. Karakuak, West Flores, Indonesia. American Journal of
Tropical Medicine and Hygiene. 1978;27(5):910-5.
Samarawickrema WA, Kimura E, Spears GF, Penaia L, Sone F, Paulson GS, Cummings RF.
Distribution of vectors, transmission indices and microfilaria rates of subperiodic
Wuchereria bancrofti in relation to village ecotypes in Samoa. Transactions of the Royal
Society of Tropical Medicine and Hygiene. 1987;81(1):129-35.
Rajagopalan PK, Panocker KN, Das PK. Control of malaria and filariasis vectors in south
India. Parasitology Today. 1987;3(8):233-40.
Raccurt CP, Lowrie RC Jr, Katz SP, Duverseau YT. Epidemiology of Wuchereria bancrofti in
Leogane, Haiti. Transactions of the Royal Society of Tropical Medicine and Hygiene.
1988;82(5):721-5.
Amerasinghe FP, Ariyasena TG, 1991. Survey of Adult Mosquitos (Diptera, Culicidae) During
Irrigation Development in the Mahaweli Project, Sri-Lanka. J Med Entomol 28: 387-393.
Hunter JM. Elephantiasis: a disease of development in north east Ghana. Social Science and
Medicine. 1992;35(5):627-45; discussion:645-9.
Gad AM, Feinsod FM, Soliman BA, Nelson GO, Gibbs PH, Shoukry A. Exposure variables in
bancroftian filariasis in the Nile Delta. Journal of the Egyptian Society of Parasitology.
1994;24(2):439-55.
Appawu MA, Baffoe-Wilmot A, Afari EA, Nkrumah FK, Petrarca V. Species composition and
inversion polymorphism of the Anopheles gambiae complex in some sites of Ghana,
west Africa. Acta Trop. 1994 Feb;56(1):15-23.
Dzodzomenyo M, Dunyo SK, Ahorlu CK, Coker WZ, Appawu MA, Pedersen EM, Simonsen
PE (1999). Bancroftian filariasis in an irrigation project community in southern Ghana.
Tropical Medicine and International Health. 4(1):13-8.
Appawu MA, Dadzie SK, Baffoe-Wilmot A, Wilson MD. Lymphatic filariasis in Ghana:
entomological investigation of transmission dynamics and intensity in communities
served by irrigation systems in the Upper East Region of Ghana. Tropical Medicine and
International Health.2001;6(7):511-6.
Supali T, Wibowo H, Ruckert P, Fischer K, Ismid IS, Purnomo, Djuardi Y, Fischer P. High
prevalence of Brugia timori infection in the highland of Alor Island, Indonesia. American
Journal of Tropical Medicine and Hygiene. 2002;66(5):560-5.
14
Appendix 4. Review article published in the American Journal of Tropical
Medicine and Hygiene 73(3), 2005, pp. 523-533
EFFECT OF WATER RESOURCE DEVELOPMENT AND MANAGEMENT
ON LYMPHATIC FILARIASIS, AND ESTIMATES OF POPULATIONS AT
RISK
TOBIAS E. ERLANGER1, JENNIFER KEISER1, MARCIA CALDAS DE CASTRO2,
ROBERT BOS3, BURTON H. SINGER4, MARCEL TANNER1 AND JÜRG UTZINGER1
1
Swiss Tropical Institute, Basel, Switzerland
Geography Department, University of South Carolina, Columbia, South Carolina, USA
3
Water, Sanitation and Health, World Health Organization, Geneva, Switzerland
4
Office of Population Research, Princeton University, Princeton, New Jersey, USA
2
ABSTRACT
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) sub-regions 1 and 2 mosquito densities of the
Anopheles gambiae complex and An. 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 sub-tropical countries have long suffered under the
yoke of lymphatic filariasis (LF). This chronic parasitic disease is of great public health
and socio-economic significance and is currently endemic in 80 countries/territories of
the world.1--3 LF accounts for serious disfiguration and incapacitation of the extremities
and the genitals and causes hidden internal damage to lymphatic and renal systems.4--6
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
15
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 B. 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 Programme 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, which is a free and non-restrictive partnership forum. WHO serves
as its secretariat and is being reinforced by an expert technical advisory group.12--14
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 since 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-epidemiological settings, was a key factor for controlling and even
eliminating LF.16--19
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)
16
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 (Figure 1). 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 epidemiological sub-regions.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 agroecosystems, 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.28-32 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 utilized 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
17
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 (‘grey literature’) were also
reviewed. Dissertation abstracts were searched in online databases, i.e., 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 biological factors, notably vector and parasite species, and
various socio-economic 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 socio-economic
factors strongly interact with the environmental determinants. The local quality of
domestic and industrial waste-water management, access to clean water and improved
sanitation, and the construction of roads and buildings depend on the socio-economic
status of specific sub-populations.
18
Figure 1. Contextual determinants of lymphatic filariasis
Environmental changes due to waterresource development and management
Environmental Factors
Climate
Rural
Urban
Agriculture & irrigation
Industrial waste-water (mis)-management
Large hydroelectric dam construction
Domestic water storage
Small dams & barrages for agriculture &
Construction of roads & buildings
domestic use
Local sewerage systems
Water supply & sanitation
Integrated vector
management
Intervention
Mass-treatment
Intervention
with filariacides
MassBiological Factors
treatment with
filariacides
Poverty
alleviation
Socio-economic
Factors
Poverty
alleviation Poverty
Parasite
Mosquito
Human
Population
density
Population
density
Population
density
Species &
strain
Species &
strain
Immigration & emigration
Survival
Insecticide
resistance
Sex, age,
ethnicity &
immunity
Exposure
Knowledge, attitudes & practices
Health systems
Longevity
19
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 of America, 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.
Table 1. Estimates of population at risk in all lymphatic filariasis (LF)-endemic countries/territories of the world,
stratified into WHO epidemiological sub-regions (population at risk of LF in thousands.
Africa
WHO sub-region 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 sub-region 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 sub-region 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 sub-region 5 (1 country)
Haiti (6,078)b
Eastern Mediterranean
WHO sub-region 7 (3 countries)
Egyptf (2,446)b, Sudan (8,302)h, Yemen (100)k
South-East Asia
WHO sub-region 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 sub-region 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 sub-region 13 (1 country)
Brunei Darussalam (40)o
WHO sub-region 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.), Samoaf 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
20
n.d.: no data currently available)
a
Except Mauritius percentages of the population at risk from Lindsay & Thomas (2000),59 re-calculated with
recent figures from United Nations (2004)60
b
Weekly Epidemiological Record (2004)14
c
Réunion, French Polynesia, Wallis and Futuna, and New Caledonia belong to France; American Samoa belongs
to the United States of America
d
WHO (2002)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 Vanuatu3
g
In Brazil, Costa Rica, Suriname, Trinidad and Tobago, and Malaysia smaller endemic foci have been
eliminated3
h
Percentage of people at risk in 1990 taken from Michael et al. (1996),62 re-calculated with recent figures from
United Nations (2004)60
i
Pan American Health Organization (2002)63
k
Weekly Epidemiological Record (2003)64
l
Supali et al. (2002)39
m
Thailand has recently eliminated filaria transmission3
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 et al. (1996)62
p
Kazura & Bockarie (2003)65
r
Korea and the Solomon Islands using diverse control strategies have eliminated transmission3
People at risk of LF at 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 sub-region 12. This sub-region
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 peerreviewed 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.
21
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
(n.d.: no data currently available)
DALYs in 2004
Total population in LF- Population at risk of LF Population in LF-endemic Urban population in LF-endemic
(x 103) (from Table 1) countries living in proximity countries without access to
caused by LF (103)a endemic countries
3 b
improved sanitation (x 103)a
(x 10 )
to irrigated areas (x 103)
c
g
1
3
976
284,551
235,382
574
38,445k
2
2
1,035
312,344
144,903
305
25,956
4
0
9
193,892
6,147
306
25,570l
5
1
1
8,326
6,078
<1
1,561
7
1
122
125,551
10,847
1,646
2,265
9
0
1
n.d.
n.d.
n.d.
n.d.
8,262
31,212
11
1
242
302,781
47,062d
2,977
1,287,945
618,496d
147,894h
131,157
12
3
13
0
0
358
40
<1
n.d.
411
1,565,246
970,589d, e, f
54,034i
176,791m
14
1
Total
12
5,777
4,079,995
2,039,548
213,021
394,511
a
Source: World Health Report 20049
b
Source: United Nations Urbanization Prospects – The 2003 Revisions60
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
WHO sub- Studies
identified
regiona
22
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 sub-regions of the world.
Setting WHO Country, year of study Water resource
Shift in
Vector
Transmission Human
Clinical
sub(reference)
development and Vector species (Filaria species) vector
abundance parameters infection manifestation
region
management
composition
prevalence
Irrigated
An. gambiae (W. bancrofti)
Ghana, 2000
©
©
ª
Rural
1
An. funestus (W. bancrofti)
©
©
(Appawu et al., 200138) agriculture
Cu. quinquefasciatus (none)
©
ª
An. pharoensis (none)
©
ª
An. nili, An. rufipens, Ae.
©
©
aegypti (none)
Irrigated
An. gambiae s.l. (W. bancrofti) ©
1
Ghana, 1995
©
Rural
agriculture
An. funestus (W. bancrofti)
(Dzodzomenyo et al.,
ª
ª
Cu. quinquefasciatus (none)
199936)
ª
ª
An. pharoensis (W. bancrofti) ª
=
1
Ghana,
1993
Rice
irrigation
An.
gambiae
s.s.
(W.
bancrofti)
ª
©
Rural
(Appawu et al., 199435)
An. melas (W. bancrofti)
©
ª
Rice irrigation
An. gambiae (W. bancrofti)
2
United Republic of
©
©
©
Rural
An. funestus (W. bancrofti)
Tanzania, 1956
ª
©
(Jordan, 195634)
Rice irrigation
An. gambiae (W. bancrofti)
2
United Republic of
©
©
©
Rural
An. funestus (W. bancrofti)
Tanzania, 1951-1953
ª
©
(Smith, 195537)
Rice irrigation
An. subpictus (W. bancrofti)
Indonesia, 2001
ªa
ª
ª
ª
Rural 11
An. barbirostris (B. timori)
(Supali et al., 200239)
©b
©
©
©
Cu. quinquefasciatus
Sri Lanka, 1986-1987 Rice irrigation
©
©
Rural 12
(W. bancrofti)
(Amerasinghe et al.,
199140)
Irrigation, sullage, Cu. quinquefasciatus
India, 1957
©
©
©
Rural 12
storm water drains (W. bancrofti, B. malayi)
(Basu, 195741)
Water storage,
Cu. quinquefasciatus
Haiti 1981
©
©
Urban 5
(W. bancrofti)
(Raccurt et al., 198831) waste-water
management
Waste-water pools Cu. pipiens pipiens, Cu.
Egypt, 1986
©
©
Urban 7
antennatus (W. bancrofti)
(Gad et al., 199432)
Waste-water
Cu. quinquefasciatus
India, 1987
©c
©
Urban 12
canals, pits,
(W. bancrofti)
(Rajagopalan et al.,
reservoirs
198729)
23
Urban 14
Man-made
Samoa, 1978-1979
(Samarawickrema et al., breeding sites,
water storage
198730)
Ae. polynesiensis (W.
bancrofti)
Ae. samoanus (W. bancrofti)
©
ª
©
ª
©
ª
-
-
©: increase in sites where water-related change occurred; ª: decrease in sites where water-related change occurred; =: no change
Genital lymphedema
b
Elephantiasis
c
Except “number of infective larvae per mosquito” which was decreasing
a
Table 4. Absolute and relative change in abundance of different filaria vectors in areas where water resources development and management (WRDM) occurred,
compared to similar control sites without WRDM
Country, year of study
Type of
Vector species
Control site
WRDM occurred
Absolute and relative change
(reference)
change
in abundance
Number
%
Number
%
Number
Factor
Ghana, 2000
Irrigated
An. gambiae s.l.
756
87.7
1,256/1,831
81.9/73.1
+500/+1,075 1.7/2.4
(Appawu et al., 200138)
agriculture
An. funestus
48
5.6
254/471
16.5/18.8
+206/+423
5.3/9.8
51
5.9
0/128
0/5.1
-51/+77
dis./2.5
(site 1/site 2)
Cu. quinquefasciatusa
2
0.2
0/27
0/1.1
-2/+25
dis./13.5
An. pharoensisa
5
0.6
24/47
1.6/1.9
+19/+42
4.8/9.4
An. nilia, An. rufipensa and
Ae. aegypti
Ghana, 1995
Irrigated
An. gambiae s.l.
15
12
141
77
+126
9.4
(Dzodzomenyo et al.,
agriculture
An. funestus
101
82
40
22
-61
0.4
199936)
5
4
0
0
-5
dis.
Cu. quinquefasciatusa
An. pharoensis
3
2
3
1
0
1
Rice irrigation An. gambiae s.s.
Ghana, 1993
27/17
96/94
50
100
+23/+33
1.9/2.9
(site 1/site 2)
An. melasa
1/1
4/6
0
0
-1/-1
dis.
(Appawu et al., 199435)
Rice irrigation Cu. quinquefasciatus
Sri Lanka, 1986-1987
209
48.3
467
79.8
+258
2.2
Cu. pseudovishnuia
224
51.7
118
20.2
-106
0.5
(Amerasinghe et al.,
199140)
Man-made
Samoa, 1978-1979
Ae. polynesiensis
–
–
–
–
ª
©
breeding sites, Ae. samoanus
(Samarawickrema et al.,
–
–
–
–
©
ª
water storage
198730)
Rice irrigation An. gambiae
United Republic of
29
96.7
714
99.6
+685
24.6
An. funestus
1
3.3
3
0.4
+2
3
Tanzania, 1956
(Jordan, 195634)
Rice irrigation An. gambiae
United Republic of
2,057
99.9
3,959
99.7
+1,902
1.9
An. funestus
2
0.1
29
0.3
+27
14.5
Tanzania, 1951-1953
(Smith, 195537)
dis.: disappearance of vector after WRDM; ©: increase; ª: decrease
a
not filaria transmitting
24
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 to An. funestus.34--36
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 to 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 wastewater 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, wastewater 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 non-irrigated 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 biological, chemical and
physical vector control measures.29 Source reduction by means of environmental
management was given high priority. It comprised 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
25
beads in wells. Within five years, the annual biting rate for W. bancrofti-transmitting Cu.
quinquefasciatus decreased from 26,203 to 3,617, the number 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 wastewater discharge by factories located in the city.
Infection prevalence in control districts without wastewater 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
26
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 Type of change
(Reference)
Transmission parameters of different filaria vectors
Irrigated agriculture
Ghana, 2000
(Appawu et al., 200138) (site 1/site 2)
Ghana, 1995
(Dzodzomenyo et al.,
199936)
Sri Lanka, 1986-1987
(Amerasinghe et al.,
199140)
India, 1979-1985
(Rajagopalan et al.,
198729)
Samoa, 1978-1979
(Samarawickrema et
al., 198730)
Annual biting rate of An. gambiae and An. funestus
Annual infective biting rate of An. gambiae and An.
funestus
Worm load of An. gambiae and An. funestus
Annual transmission potential of An. gambiae and An.
funestus
Infective An. gambiae
Infective An. funestus
Irrigated agriculture Infective An. gambiae
Infective An. funestus
Infected An. gambiae
Infected An. funestus
Rice irrigation
Geometric mean female Cu. quinquefasciatus
per man-hour
Control site WRDM
occurred
188
0.5
299
7.7
1.0
0.5
1.8
13.8
Relative change
1.6
15.4
1.8
27.6
0.3%
0%
4.6
3.3%/2.5%
0%/1.3%
8%
2%
27%
16%
7.4
11/8.3
n.a.
1.6
Annual biting rate of Cu. quinquefasciatus
26,203
Annual infective biting rate of Cu. quinquefasciatus
225
Worm load of Cu. quinquefasciatus
2.0
Annual transmission potential of Cu. quinquefasciatus
450
Man-made breeding Biting density per man hour of Ae. polynesiensis
8
sites, water storage
Infected Ae. polynesiensis
1.7%
Infective Ae. polynesiensis
0.3%
Biting density per man hour of Ae. samoanus
67
Infected Ae. samoanus
0.5%
Infective Ae. samoanus
0.2%
3,617
22
3.5
77
26
2.2%
0.4%
33
0.2%
0.04%
0.1
0.1
1.8
5.8
3.3
1.3
1.3
0.5
0.4
0.2
Vector control
program
n.a. = not applicable
27
Table 6. Filaria prevalence and frequencies of clinical manifestations in areas where water resources development and management (WRDM) occurred
compared to similar areas without WRDM
Country, year of study (reference)
Type of WRDM
Filaria vector or clinical
Control site
WRDM occurred Change in absolute
symptoms
terms
Rice irrigation
Indonesia, 2001
W. bancrofti
12%
0%
Absence
(Supali et al., 200239)
B. timori
0%
6%
+6%
Genital lymphedema
5%
0%
Absence
Elephantiasis
0%
7%
+7%
Egypt, 1986
Areas around large cesspit /
W. bancrofti
12%
17%/7%
+5%/-5%
(Gad et al., 199432)
small cesspit
Wastewater area/area with
W. bancrofti
27%
39%/44%
+12%/+17%
Haiti 1981
water storage
(Raccurt et al., 198831)
Man-made breeding sites,
W. bancrofti
5.3%
4.2%
-1.1%
Samoa, 1978-1979
water storage
(Samarawickrema et al., 198730
Rice irrigation, sullage and
India, 1957
Mixed infection of B. malayi
5%/2%
5.5%/12%
+0.5%/+9%
storm-water drains in two sites and W. bancrofti (ratio 74:26)
(Basu, 195741)
(site 1/site 2)
Genital lymphedema and
3.5%/3%
5%/2.5%
+1.5%/-0.5%
elephantiasis
Rice irrigation
7%
26%
+19%
United Republic of Tanzania, 1956
(Jordan, 195634)
W. bancrofti
Rice irrigation
12%
23%
+11%
United Republic of Tanzania, 19511953
W. bancrofti
(Smith, 195537)
28
dynamics of vector-borne diseases.16,20,22,23 However, detailed analyses on the
contextual determinants are sparse.42--44 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.1--3 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 to non-irrigated 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 employed 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-epidemiological 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
physiological/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 spatio-temporal heterogeneity, often at
very small scales. In addition, the fine-grained detail about wastewater 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
multi-faceted 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
29
design and 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 dependent 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 ecoepidemiological 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 S. 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 employ 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
30
Another important finding of our systematic literature review is that urbanization,
especially in connection with wastewater 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 centres 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 wastewater 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 mosquito 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 five years after the control program was launched,
transmission parameters dropped significantly. The reason for the increase of the worm
load might be due to larger mosquito populations feeding less 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 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 socio-economic 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 ambious
goal to eliminate LF as a public health problem by 2020 might remain elusive.
31
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Culicidae) during irrigation development in the Mahaweli Project, Sri Lanka. J
Med Entomol 28: 387-393.
Basu PC, 1957. Filariasis in Assam State. Indian J Malariol 11: 293-308.
Patz JA, Graczyk TK, Geller N, Vittor AY, 2000. Effects of environmental change
on emerging parasitic diseases. Int J Parasitol 30: 1395-1405.
Amerasinghe FP, 2003. Irrigation and mosquito-borne diseases. J Parasitol 89
(Suppl.): S14-S22.
Molyneux DH, 2003. Common themes in changing vector-borne disease
scenarios. Trans R Soc Trop Med Hyg 97: 129-132.
Keiser J, Utzinger J, Castro MC, Smith TA, Tanner M, Singer BH, 2004.
Urbanization in sub-saharan Africa and implication for malaria control. Am J Trop
Med Hyg 71 (2 Suppl.): 118-127.
Ezzati M, Utzinger J, Cairncross S, Cohen AJ, Singer BH, 2005. Environmental
risks in the developing world: exposure indicators for evaluating interventions,
programmes, and policies. J Epidemiol Community Health 59: 15-22.
Costantini C, Sagnon N, della Torre A, Coluzzi M, 1999. Mosquito behavioural
aspects of vector-human interactions in the Anopheles gambiae complex.
Parassitologia 41: 209-217.
Keiser J, Utzinger J, Singer BH, 2002. The potential of intermittent irrigation for
increasing rice yields, lowering water consumption, reducing methane emissions,
and controlling malaria in African rice fields. J Am Mosq Control Assoc 18: 329340.
Surtees G, 1970. Effects of irrigation on mosquito populations and mosquitoborne diseases in man, with particular reference to ricefield extension. Int J
Environ Stud 1: 35-42.
Amerasinghe FP, Munasingha NB, 1988. A predevelopment mosquito survey in
the Mahaweli Development Project area, Sri Lanka: adults. J Med Entomol 25:
276-285.
Service MW, 1984. Problems of vector-borne disease and irrigation projects. Ins
Sci Appl 5: 227-231.
Abdel-Wahab MF, Strickland GT, El-Sahly A, El-Kady N, Zakaria S, Ahmed L,
1979. Changing pattern of schistosomiasis in Egypt 1935-79. Lancet 314: 242244.
Southgate VR, 1997. Schistosomiasis in the Senegal River Basin: before and
after the construction of the dams at Diama, Senegal and Manantali, Mali and
future prospects. J Helminthol 71: 125-132.
Kar SK, Mania J, Kar PK, 1993. Humoral immune response during filarial fever in
Bancroftian filariasis. Trans R Soc Trop Med Hyg 87: 230-233.
Ravindran B, 2003. Aping Jane Goodall: insights into human lymphatic filariasis.
Trends Parasitol 19: 105-109.
Hise AG, Hazlett FE, Bockarie MJ, Zimmerman PA, Tisch DJ, Kazura JW, 2003.
Polymorphisms of innate immunity genes and susceptibility to lymphatic filariasis.
Genes Immun 4: 524-527.
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57.
58.
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65.
Stolk WA, Ramaiah KD, van Oortmarssen GJ, Das PK, Habbema JDF, de Vlas
SJ, 2004. Meta-analysis of age-prevalence patterns in lymphatic filariasis: no
decline in microfilaraemia prevalence in older age groups as predicted by models
with acquired immunity. Parasitology 129: 605-612.
Samuel PP, Arunachalam N, Hiriyan J, Thenmozhi V, Gajanana A,
Satyanarayana K, 2004. Host-feeding pattern of Culex quinquefasciatus Say and
Mansonia annulifera (Theobald) (Diptera: Culicidae), the major vectors of filariasis
in a rural area of south India. J Med Entomol 41: 442-446.
Lindsay SW, Thomas CJ, 2000. Mapping and estimating the population at risk
from lymphatic filariasis in Africa. Trans R Soc Trop Med Hyg 94: 37-45.
United Nations, 2004. World Urbanization Prospects. The 2003 Revisions. New
York: Department of Economic and Social Affairs; Population Division of the
United Nations (ESA/P/WP.190).
WHO, 2002. Defining the Roles of Vector Control and Xenomonitoring in the
Global Programme to Eliminate Lymphatic Filariasis. Report of the Informal
Consultation. Geneva: World Health Organization (WHO/CDS/CPE/PVC/2002.3).
Michael E, Bundy DAP, Grenfell BT, 1996. Re-assessing the global prevalence
and distribution of lymphatic filariasis. Parasitology 112: 409-428.
WHO, 2002. Lymphatic filariasis elimination in the Americas. Report of the
regional program-manager's meeting. Port-au-Prince, Haiti: Pan American Health
Organization.
WHO, 2003. Lymphatic filariasis. Wkly Epidemiol Rec 78: 171-179.
Kazura JW, Bockarie MJ, 2003. Lymphatic filariasis in Papua New Guinea:
interdisciplinary research on a national health problem. Trends Parasitol 19: 260263.
Acknowledgments: We 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 in the Protection of the Human Environment Department
(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 No. PMPDB--106221 and PPOOB--102883, respectively). M. C.
Castro is financially supported by the Office of Population Research and the Centre for
Health and Wellbeing at Princeton University.
Authors’ addresses: Tobias E. Erlanger, Jennifer Keiser, Marcel Tanner, Jürg Utzinger,
Swiss Tropical Institute, P.O. Box, CH–4002 Basel, Switzerland; Marcia Caldas de
Castro, Geography Department, University of South Carolina, Callcott Room 125,
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.
35
Appendix 5. Table summarising geographical distribution of the three LF species, the
ecology of their vectors and environmental changes leading to increased vector
densities
Filaria
type
Brugia
timori
Brugia
malayi
Endemic
region
Alor, Flores
and Timor
islands
South Asia
Wuchereria Americas
bancrofti
Major vector species
Anopheles barbirostris
Anopheles barbirostris
Anopheles campestris
Anopheles donaldi
Mansonia uniformis
Mansonia bonneae
Mansonia dives
Mansonia annulata
Mansonia annulifera
Culex quinquefasciatus
Natural
ecology
Fresh water
Fresh water
Fresh water
with aquatic
weeds
Organically
polluted water
Culex quinquefasciatus
Organically
polluted water
Anopheles funestus
Anopheles gambiae
Fresh water
Culex quinquefasciatus
Organically
polluted water
Middle East
Culex pipiens molestus
Culex quinquefasciatus
Organically
polluted water
Far East
Culex quinquefasciatus
Organically
polluted water
Papuan
Anopheles farauti
Anopheles koliensis
Anopheles punctulatus
Ochlerotatus niveus
Ochlerotatus harinasutai
Fresh water
Afrotropical
Nicobar,
Thailand
Polynesia
Fresh water
with moderate
organic
pollution
Small fresh
water
collections
Environmental change
leading to increased
LF vector densities
Dams and irrigation,
fresh water collection,
flood control
Dams and irrigation,
fresh water collection,
flood control
Man-made reservoirs,
drainage canals of
irrigation schemes,
aquatic weed growth
Inadequate waste-water
treatment due to rapid
urbanisation, organic
pollution of fresh water
Inadequate waste-water
treatment due to rapid
urbanisation, organic
pollution of fresh water
Dams and irrigation,
fresh water collections,
flood control
Inadequate waste-water
treatment due to rapid
urbanisation, organic
pollution of fresh water
Inadequate waste-water
treatment due to rapid
urbanisation, organic
pollution of fresh water
Inadequate waste-water
treatment due to rapid
urbanisation, organic
pollution of fresh water
Dams and irrigation,
fresh water collection,
flood control
Domestic water
collections, rain water
canals
Lack of solid and
organic waste
management,
inadequate drinking
water supply
Source: Zagaria & Savioli (2002), Annals of Tropical Medicine and Parasitology, 96(Suppl.):3-13.
Aedes polynesiensis
Aedes samoanus
36
Appendix 6.1. Key information form (Smith-1955-Bull Ent Res)
WHO sub-region 1
Disease
Author
Title
Lymphatic filariasis
Smith A.
The Transmission of Bancroftial Filariasis on Ukara Island Tanganyika. II.
The Distribution of Bancroftial Microfilaraemia Compared with the
Distribution of Hut-Haunting Mosquitoes and their Breeding Places.
Bulletin of Entomology Research. 1955;46:437-444.
Reference
Language
English
Country,
Tanganyika [Tanzania], 1951-53
year of study
Village,
Ukara Island
district,
region
Geographical Lo: 33° 00’ E / La: 01° 50’ S
coordinates
WHO sub- 1
region {1-14}
Abstract
Key
- Microfilaraemia prevalence rate
information
- Number of female Anopheles gambiae and Anopheles funestus
caught
Water
Gravitational irrigation
resource
development
and
management
project
Type
Rice irrigation
Year of
inception
37
Outcome
measures
(e.g.
prevalence,
incidence,
# of cases,
parasites
density
exposed
population,
etc.)
Irrigated areas
Villages
Microfilariae
No. of An.
No. of An.
prevalence (%) gambiae caught funestus caught
Chifule
30
3622
25
Bukungu
20
3891
31
Bwisya
24
-
-
Chigara
23
-
-
Buyembe
26
-
-
Mbule
20
-
-
Bubanja
26
7143
27
Katende
24
1084
33
Nyanguja
16
-
-
Isiba
22
4050
8
Chamhunda
23
-
-
Buyanja
24
3726
30
Bukiko
23
-
-
Nyamanga
25
4194
51
Mean
23.3
3959
29
Non-irrigated areas
Villages
No. of An.
Microfilariae
No. of An.
funestus
prevalence (%) gambiae caught caught
Kome
11
1714
3
Buyombe
7
-
-
Huna
15
3386
3
Bulabi
16
-
-
Lubonwe
9
1277
1
Busere
10
-
-
Bumiro
13
1852
1
Masaka
17
-
-
Mean
12
2057
2
Relative
changes, risk
(RR)
Additional
notes
38
Appendix 6.2. Key information form (Jordan-1956-East Afr Med Jou)
WHO sub-region 1
Disease
Author
Title
Reference
Language
Country, year of study
Village, district, region
Geographical coordinates
WHO sub-region {1-14}
Abstract
Key information
Lymphatic filariasis
Jordan P.
Filariasis in the lake Province of Tanganyika
East African Medical Journal. 1956 Jun;33(6):233-6.
English
Tanganyika (Tanzania), 1956
Babanja, Boyombe
Lo: 33° 02’ E / La: 01° 50’ S
1
- Microfilaraemia in two villages
- Mosquito-catches (An. gambiae, An. funestus) in two villages
Water resource development - Rice cultivation
and management project
- Pits for grass for cattle fodder
Type
- Irrigation
Year of inception
Showing catches of A. gambiae and A. funestus per hut in two
Outcome measures
(e.g. prevalence, incidence, villages, 3 miles apart, with differents microfilaraema rates
# of cases, parasites density
Flit catches per hut
%
exposed population, etc.)
Village
microfilaraemia An. gambiae An. funestus
May July
May July
Babanja
Boyombe
26
7
Before
During
After
Relative changes, risk (RR)
Additional notes
39
714
29
16
6.1
2.7
0.1
3.8
0.1
Appendix 6.3. Key information form (Basu-1954-Ind Jou Malarol)
WHO sub-region 11
Disease
Lymphatic filariasis
Author
Basu PC.
Title
Filariasis in Assam state.
Reference Indian Journal of Malariology. 1957 Jun;11(3):293-308.
Language
English
Country,
India, 1957
year of study
Village,
Bakakhat area, Chabua area:, Assam state, India
district,
region
Geographical Bakakhat: La: 93° 36’ E / Lo: 26° 38’ N; Chabua area: La: 95° 11E / Lo: 27° 29’ N
coordinates
WHO sub- 12
region {1-14}
Abstract
Key
Clinical data, infection rates and entomological data of tea garden and non-tea
information garden dwellers:
- Climatic data
- Clinical data, disease rates, prevalence, filariaemia rates of different villages and
tea gardens in two regions of Assam
- Age distribution of disease and infection
- Mosquito density, dissection, rates of infection
- Endemecity rates of different categories of persons
Water
Irrigation in tea gardens
resource
development
and
management
project
Type
Irrigation
Year of
inception
40
Outcome
measures
(e.g.
prevalence,
incidence,
# of cases,
parasites
density
exposed
population,
etc.)
41
Before
During
After
Relative
changes, risk
(RR)
Additional
notes
42
Appendix 6.4. Key information form (Partono-1978-Am Jou Trop Med)
WHO sub-region 11
Disease
Author
Title
Lymphatic filariasis
Partono F, Pribadi PW, Soewarta A.
Epidemiological and clinical features of Brugia timori in a newly established village,
Karakuak, West Flores, Indonesia.
Reference
American Journal of Tropical Medicine and Hygiene. 1978 Sep;27(5):910-5.
Language
English
Country, year Indonesia, 1977
of study
Village,
Village Karakuak, West Flores, Indonesia
district, region
Geographical Lo: 8° 18’ S / La: 120° 28’ E
coordinates
WHO sub11
region {1-14}
The epidemiological and clinical features of Brugia timori filariasis in a newly
Abstract
established village, Karakuak, West Flores, is described. The microfilarial rate by
finger stick and Nuclepore filtration was 24% and 30%, respectively, and the disease
rate 64%. Infected persons were found in every family and household with no
predominant age or sex preference. Development of elephantiasis in the population
was associated with residence in the new village of Karakuak, where extensive rice
field cultivation was initiated soon after arrival. The irrigated fields provided excellent
breeding sites for the vector, Anopheles barbirostris. People with no previous
exposure to the parasite developed elephantiasis earlier and more frequently than
those originating from other endemic areas.
Key
- Microfilaremia (smear and membrane filtration method) age and sex distributed
information
- Comparison of number (%) of people with microfilaremia, scar and elephantiasis
among endemic and non-endemic filarial areas
- Number (%) of persons with clinical signs and symptoms of Timorian filariasis
- Indoor and outdoor collection of various potential filaria-transmitting mosquitoes
Water
Rice Irrigation
resource
development
and
management
project
Type
Rice
Year of
inception
1962
43
Outcome
measures
(e.g.
prevalence,
incidence,
# of cases,
parasites
density
exposed
population,
etc.)
The detection of microfilaremia by blood smear and membrane filtration; age and sex
distribution
Age
group
Males
Females
Total
20µl
Nucleopore
20µl
Nucleopore
0-4
10/0 (0)*
-
10/2 (20)
-
20/2 (10)
5-9
13/1 (8)
5/0 (0)
16/2 (13)
6/1 (17)
29/4 (14)
10-19
32/7 (22)
22/5 (23)
22/3 (14)
23/3 (13)
54/10 (19)
20-29
14/3 (21)
-
14/1 (7)
-
28/4 (14)
30-39
13/6 (46)
13/6 (46)
13/4 (31)
16/5 (31)
26/10 (38)
40-49
13/6 (46)
-
9/2 (22)
-
22/8 (36)
50+
9/7 (78)
7/7 (100)
12/4 (33)
4/2 (50)
21/12 (57)
Total
104/30 (29)
47/18 (38)
96/18 (19)
49/11 (22)
200/50 (25)
* number examined / number positive (%)
Comparison of number (%) of people with microfilaremia, scar and elephantiasis
among people from endemic and non-endemic filarial areas
Age at
exposure
Non-endemic
Endemic
No
examined
Mf
positive
Scars
0-10
19
3 (16)
6 (32)
4 (21)
11+
32
9 (28)
18 (56)
Total
51
21 (24)
24 (47)
Elephant- No examined
iasis
Mf
positive
Scars
Elephantiasis
19
4 (21)
10 (53)
2 (11)
11 (34)
38
13 (34)
21 (55)
5 (13)
15 (29)
57
17 (30)
31 (54)
7 (12)
44
Number (%) of persons with clinical signs and symptoms of Timorian filariasis
Males
Females
Elephantiasis
Total
filarial
diseases
0
0
1 (10)
3 (19)
5 (31)
1 (6)
7 (44)
22
12 (55)
12
(55)
6 (27)
21 (95)
13 (93)
14
5 (36)
4 (29)
7 (50)
9 (64)
1 (8)
12 (92)
13
8 (62)
5 (38)
3 (23)
9 (69)
7 (54)
2 (15)
9 (69)
9
3 (33)
3 (33)
2 (22)
5 (55)
5 (56)
2 (22)
2 (22)
5 (56)
13
4 (31)
6 (46)
1 (8)
7 (54)
57 (54)
46
(44)
15 (14)
71 (68)
97
36 (37)
35
(36)
20 (21)
59 (61)
Elephantiasis
Total
filarial
diseases
No
examined
0 (8)
0
2 (18)
10
1 (10)
6 (46)
3 (23)
1 (8)
7 (54)
16
32
16 (50)
17
(53)
3 (13)
23 (72)
20-29
14
10 (71) 5 (36)
5 (36)
30-39
13
11 (85)
12
(92)
40-49
13
7 (54)
50
9
Total
105
Adenolymph- Scars
angitis
Age
group
No
examined
0-4
11
2 (18)*
5-9
13
10-19
Adenolymph- Scars
angitis
Mosquito collection
Indoor human bait
Day 1
Species
Outdoor
Indoor
human
resting
bait day
day 3
Total
3
Day 2
8pm- 10pm- 8pm- 10pm- 12pm- 3am10pm 5am 10pm 12pm 3am 6am
2am4am
8pm9pm
Anopheles
barbirostris
3
75
12
18
41
15
250
13
427
Anopheles
sundaicus
31
52
6
20
4
5
6
6
130
Anopheles
aconitus
4
11
0
4
9
2
0
2
30
Anopheles
vagus
7
13
4
7
7
3
14
3
58
Anopheles
subpictus
16
47
2
8
0
2
0
6
81
Anopheles
annularis
4
0
4
4
4
6
0
4
26
Mansonia
uniformis
0
0
0
0
0
0
0
1
1
Culex fuscocephalus
0
0
0
0
0
0
0
4
4
Culex pipiens
fatigas
0
0
0
1
0
0
0
0
1
Culex
0
0
0
0
0
0
0
1
1
45
Before
During
After
Relative
changes, risk
(RR)
Additional
notes
Further publications from island of Flores:
- Partono F.-Trans R Soc Trop Med Hyg. 1989 Nov-Dec;83(6):821-6
- Partono F.-Trans R Soc Trop Med Hyg. 1984;78(3):370-2.
- Hoedojo-Southeast Asian J Trop Med Public Health. 1980 Sep;11(3):399-404.
- Partono F.-Southeast Asian J Trop Med Public Health. 1978 Sep;9(3):338-43.
- Partono F.-J Parasitol. 1977 Jun;63(3):540-6.
- Atmosoedjono S.-J Med Entomol. 1977 Jan 31;13(4-5):611-3.
- Dennis D.T.-Am J Trop Med Hyg. 1976 Nov;25(6):797-802.
- Partono F.-Trans R Soc Trop Med Hyg. 1976;70(4):354-5.
46
Appendix 6.5. Key information form (Rajagopalan-1987-Paras Today)
WHO sub-region 12
Disease
Author
Title
Reference
Language
Country, year of
study
Village, district,
region
Geographical
coordinates
WHO sub-region
{1-14}
Abstract
Lymphatic filariasis
Rajagopalan PK, Panocker KN, Das PK.
Control of malaria and filariasis vectors in south India.
Parasitology Today. 1987; 3(8):233-40.
English
India, 1987
Pondicherry town
La: 11° 56’ N / Lo: 79° 50’ E
12
Key information
- Evaluation of a malaria and filariasis control programme
- Annual Transmission Index for Wuchereria bancrofti
Water resource
- Vector control programme of the “Vector control Research Centre in
development and Pondicherry”
management
project
Type
- Cesspits, cisterns, wells, water drains, storm channels, other water bodies
Year of inception 1981
Outcome
- Including measures of the mosquito control programme: physical,
measures
chemical, biological strategies and environmental management
(e.g. prevalence,
incidence,
# of cases,
parasites density
exposed
population, etc.)
47
Annual transmission index for Wuchereria bancrofti in
Pondicherry during the 5 years of the VCRC vectors control
project
1979-80
(pre1981
control)
1982
1983
1984
1985
3222
1662
3617
Estimated
no. of
mosquitoes
biting a man
in one year
(a)
26 203
8238
3181
Proportion
of
mosquitoes
infective
(from biting
collections
only) (b)
0.0086
0.006
0.004
Estimated
no. of
infective
bites a man
receives in
a year
225
49
13
21
13
22
Number of
infective
larvae per
infective
mosquito (c)
2.0
4.0
2.6
2.9
3.72
3.50
Annual
transmission
index
(a x b x c)
450
197
33
62
49
77
Before
During
After
Relative changes,
risk (RR)
Additional notes
48
0.0066 0.0079 0.0061
Appendix 6.6. Key information form (Samawrickrema- Trans Roy Soc Trop Med Int
Health-1987)
WHO sub-region 5
Disease
Author
Title
Reference
Lymphatic filariasis
Samawrickrema WA, Kimura E, Spears, GFS, Penaia L, Fola Sone, Paulson GS,
Cummings RF.
Distribution of vectors, tansmission indices and microfilaria rates of subperiodic
Wuchereria bancrofti in relation to village ecotypes in Samoa
Transactions of the Royal Society of Tropical Medicine and International
Health. 1987;81, 129-135.
English
Samoa, 1978-79
Language
Country,
year of study
Village,
Upulu and Savaii islands
district,
region
Geographical Lo: 13° 48’ S / La: 172° 08’ W
coordinates
WHO sub- 5
region {1-14}
Aedes polynesiensis and Ae. samoanus biting densities and Wuchereria bancrofti
Abstract
infection and infective rates were studied in 47 villages throughout the islands of
Samoa Upolu, Manono and Savaii during 1978-79, and microfilaria (mf) rates were
surveyed in 28 of the villages. The mf rate was correlated with both infection and
infective rates of Ae. polynesiensis in Upolu, but not of Ae. samoanus. In Upolu, Ae.
polynesiensis was apparently the major vector. It was relatively more abundant in
more cultivated and populated areas, along the northern coast of Upolu, except Apia
town area. In Savaii, Ae. samoanus predominated over Ae. polynesiensis except in
"plantation" villages. Relatively high biting densities and rates of infection and
infectivity indicated that Ae. samoanus was not less important than Ae.
polynesiensis as a vector in Savaii. Ae. samoanus preferred natural vegetation, in
contrast to Ae. polynesiensis which was found near human habitations in cultivated
land. There was no difference between the biting densities of Ae. polynesiensis in
"coastal" and "inland" villages, indicating that crab holes (numerous only in some
coastal villages) may not influence the density of Ae. polynesiensis. Higher mf rates
were associated with villages where Ae. polynesiensis, rather than Ae. samoanus,
was dominant, indicating that Ae. polynesiensis was generally a more efficient
vector. In the former villages, the difference in mf rates between males and females
was smaller than in the latter, probably reflecting a difference in biting habits of the
vectors. Ae. polynesiensis infections were recorded in plantations over 2 km from
any village, suggesting that both habitats were foci of transmission.
Key
- Microfilaremia prevalence rates of humans, biting densities, infection and infective
information rates of Aedes species on Upolu and Savaii island
- Biting frequencies depending on different village ecotypes
Water
Higher human population, urbanization, domestic water storage, accumulation of
resource
junk
development
and
management
project
Type
Various artificial water bodies
49
Year of
inception
Outcome
measures
(e.g.
prevalence,
incidence,
# of cases,
parasites
density
exposed
population,
etc.)
50
Before
During
After
Relative
changes, risk
(RR)
Additional
notes
51
Appendix 6.7. Key information form (Raccurt-1988-Trans Roy Soc Trop Med Hyg)
WHO sub-region 5
Disease
Author
Title
Reference
Lymphatic filariasis
Raccurt CP, Lowrie RC Jr, Katz SP, Duverseau YT.
Epidemiology of Wuchereria bancrofti in Leogane, Haiti.
Transactions of the Royal Society of Tropical Medicine and Hygiene.
1988;82(5):721-5.
English
Haiti, 1981
Language
Country,
year of study
Village,
Leogane
district,
region
Geographical La: 18° 31’ N / Lo: 72° 38’ W
coordinates
WHO sub- 5
region {1-14}
A survey for Wuchereria bancrofti in Leogane, Haiti, revealed that 140 of 421
Abstract
individuals (33%) had a patent infection, of which 40% lived in the suburban outskirts
of the city. The median microfilaria density was 19.1 per 20 mm3 of blood for
suburban dwellers compared with only 8.8 for those living in the city. The vector,
Culex quinquefasciatus (Say), breeds mostly in and around numerous rum distilleries,
located exclusively around the periphery of the city, and this undoubtedly accounts for
the higher prevalence and intensity of infection among suburban dwellers.
Key
- Microfilariae (Mf) rates and Mf densities of 4 spots in and around Leogane.
information - Positive regression lines of cumulative frequency distribution of Wuchereria
bancrofti microfilaria-positive cases.
Water
- Leogane inner city (low risk)
resource
- Dampus suburban area: sugar cane fields and crushing factories (high risk)
development - Chassange: distilleries: sugar waste water discharge in ditches and pits; water
and
storage in concrete vats (very high risk)
management
Ca-Ira:
Mangrove swamps; vector Culicoides furens transmits Mansonella ozzardi
project
(medium to high risk)
Type
Sugarcane
Year of
inception
52
Outcome
measures
(e.g.
prevalence,
incidence,
# of cases,
parasites
density
exposed
population,
etc.)
53
Microfilaria (Mf)-rate of Wuchereria bancrofti of 421 participants
Location
Mf-rate in %
Leogane city
27
Dampus
39
Chassange
44
Ca-Ira
36
- Larvae of Culex quinquefaciatus collected around the distilleries; ~2000 larvae per
dip (475 ml).
- After 5-17d 47% of Culex quinquefaciatus had third stage larvae.
Before
During
After
Relative
changes, risk
(RR)
Additional
notes
54
Appendix 6.8. Key information form (Amerasinghe-1991-Jou Med Entom)
WHO sub-region 12
Disease
Author
Title
Lymphatic filariasis
Amerasinghe F.P.
Survey of adult mosquitoes (Diptera: Culicidae) during irrigation development in the
Mahaweli Project, Sri Lanka
Journal of Medical Entomology. 1991 May; 28(3):387-393.
Reference
Language
English
Country,
Sri Lanka, 1986-1987
year of study
Village,
Block 6, Zone 4, Mahaweli System C, Eastern Sri Lanka
district,
region
Geographical La: 07°20’N / Lo: 81°04’E
coordinates
WHO sub- 12
region {1-14}
Abstract
Key
information
- Entomological survey before during and after an irrigation project.
- 71 mosquito-species collected
- Shift in vector composition and abundance
- Cx. qinquefasciatus counts increased 2.2 times during the completion of the project
- The geometric mean female Cu. quinquefasciatus per man-hour rose from 4.6 to
7.4 (factor: 1.6) during the completion of the project
Canals, medium and small dams, pumps and resettlement of people
Water
resource
development
and
management
project
Type
Rice irrigation
Year of
1988
inception
55
Outcome
measures
(e.g.
prevalence,
incidence, of
cases,
parasites
density
exposed
population,
etc.)
56
Appendix 6.9. Key information form (Hunter-1992-Soc Sci Med)
WHO sub-region 1
Disease
Author
Title
Reference
Lymphatic filariasis
Hunter JM.
Elephantiasis: a disease of development in north east Ghana.
Social Science and Medicine. 1992 Sep;35(5):627-45;
discussion 645-9.
Language
Country, year of study
Village, district, region
Geographical coordinates
WHO sub-region {1-14}
Abstract
English
Ghana, 1989
41 chiefdoms in north east Ghana
La: 10° 30’ – 11° 00’ N / Lo: 0° 00’ – 1° 30’ W
1
A reconnaissance survey for the presence of lymphatic filariasis is
made in 41 chiefdoms of north east Ghana. Four disease levels
are identified culminating in hyperendemic disease foci associated
with two government-introduced rice irrigation projects. Attention
is also drawn to the disease effects of small village dams. Multiple
concurrent infections are noted. Within the most stricken irrigation
villages, aspects of concealment, stigma and marriage are
considered. Failure to control lymphatic filariasis has led to
hospital avoidance and neglect of the disease jointly by patients,
physicians and nurses. Culpability rests with the irrigation
authority and government health services. An outline is given of
possible measures for disease control. A multisectoral policy of
'prevention before development' is strongly advocated.
Key information
- Observation of clinical symptoms of LF and the spatial relation to
irrigation and water storage projects
- Different aspects dealing with (water) development projects in
northern Ghana
- No data available: reconnaissance survey, descriptive
Water resource development - Small dams and irrigation systems in northern Ghana
and management project
- Especially the Vea and Tono irrigation project
Type
- Rice, shorgum, millet, vegetables
- Water for livestock
Year of inception
- Vea: 1965 (start) – 1984 (completion)
- Tono: 1975 (start) – 1985 (completion)
- Construction of various little dams 1958 -1964
Outcome measures
Descriptive:
(e.g. prevalence, incidence, - Distinctive higher prevalence of clinical symptoms in villages
of cases, parasites density within 2 km range of irrigation systems and dams
exposed population, etc.)
- Higher prevalence of clinical symptoms in women than in men
- Absence or low prevalence of clinical symptoms in villages > 2
km from major irrigation systems and dams
Before
- Village chiefs reported an increase both of LF-symptomatic
cases and insect nuisance
During
After
57
Relative changes, risk (RR) Estimated by author (!) to be > 1 in villages within the flight range
of Anopheles gambiae + funestus.(~2 km).
Additional notes
58
Appendix 6.10. Key information form (Gad-1994-Jou Egypt Soc Paras)
WHO-region 7
Disease
Author
Title
Reference
Language
Country, year
of study
Village, district,
region
Geographical
coordinates
WHO subregion {1-14}
Abstract
Lymphatic filariasis
Gad AM, Feinsod FM, Soliman BA, Nelson GO, Gibbs PH, Shoukry A.
Exposure variables in bancroftian filariasis in the Nile Delta
Journal of the Egyptian Society of Parasitology. 1994 Aug;24(2):439-55.
English
Egypt, 1986
El Kashish, Qalubyia District
La: 30° 13’ N / Lo: 31° 18’ E
7
To demonstrate focality of filariasis within endemic rural areas and to define
exposure variables which may influence this phenomenon, the population of an
agrarian endemic village, of 12,500 individuals, in the Nile Delta of Egypt was
censused. A sequential sample of individuals residing in every fifth house was
tested for microfilaremia (239 households with 8.6 +/- 3.5 individuals per
household (HHD). Three areas of the village were tested simultaneously and a
questionnaire was filled out for each sampled HHD with special emphasis given
to the entomological and environmental factors that might affect filarial
infection. One area (area A) had a higher intensity of larvae and biting adults of
the main filarial vector, Culex pipiens, than the other two areas (areas B and
C). Of the 1488 persons who agreed to be tested in the three areas 181
(12.2%) were microfilaremic. Microfilaremia prevalences were the same in
males and females and microfilariae were present in all age groups. Filarial
infection was most prevalent in area "A" (1.16 +/- 0.14 infected people per
HHD) than in area "B" (0.44 +/- 0.11) or "C" (0.72 +/- 0.10) (ANOVA; p =
0.0003). several possible predictor variables were analyzed by logistic
regression with the presence of infection as the response variable. Among
individuals residing around the main Culex pipiens development sites, those
living in houses facing vacant land are exposed to more mosquito bites and
had a greater chance of having filarial infection (relative risk [RR] = 1.5; logistic
regression, P = 0.0089). People residing in large households had a reduced
chance of having filarial infection (RR = 0.87; logistic regression, p = 0.0015).
These data show that the distribution of microfilaremic individuals is uneven
within the study village and suggest that small HHD and houses that bordered
open areas containing mosquito development sites are potential risk factors for
acquiring filarial infection.
59
Key information - Microfilaremia prevalence in the study population according to age and sex
- Comparison of microfilaremia prevalence among individuals
- Variance in prevalence of microfilaremia within households (HHD)
- Comparison of microfilaria prevalence and household (HHD) prevalence
between the 3 study areas A, B and C
- Risk factors associated with microfilaremia
Water resource - Cesspits and cesspools
development
and
management
project
Type
- Wastewater
Year of
inception
Outcome
measures
(e.g.
prevalence,
incidence,
# of cases,
parasites
density
exposed
population,
etc.)
60
Microfilaremia prevalence in the study population according to age and sex
Microfilaremia prevalence
Male
Age group
(years)
N
Female
%
N
Total
%
N
%
<10
227
6
239
7
466
6.65
>10≤20
209
16
141
13
350
14.57
>20≤30
108
7
105
15
213
10.80
>30≤40
83
13
99
18
182
15.93
>40≤50
54
13
55
20
109
16.50
>50≤60
53
19
42
24
95
21.05
>60
41
15
32
9
73
12.33
total
775
11
713
13
1488
12.16
Comparison of microfilaremia prevalence among overall individuals
P-values
Area
N
Prevalence±SE
A
399
0.17±0.019
B
326
0.07±0.015
C
763
0.12±0.012
Area A
Area B
Area C
0.001
0.030
0.024
A: area with a large open cesspool (10mx6m) “very high risk”
B: area with a closed cesspool (1mx1m) “high risk”
C: remainder of the whole study-site (village) “normal risk”
Variance in prevalence of microfilaremia within households (HHD)
P-values
Area
HHD
prevalence
Variance
A
0.19
0.0324
B
0.07
0.0144
C
0.12
0.0361
61
area A
Area B
Area C
0.006
0.707
0.001
Comparison of microfilaria prevalence and household (HHD) prevalence between
the 3 study areas A, B and C
No. of people with
HHD prevalence
microfilaria
ANOVA
Tukey’s
MC test
Area No Mean/HHD±SE P-value A B
A
57
1.16±0.14
B
54
0.44±0.11
C
127
0.72±0.10
0.0003
-
*
C
*
- NS
-
ANOVA
Tukey’s
MC test
Mean/HHD±SE P-value A B
0.19±0.024
0.0006
-
C
*
*
0.07±0.017
NS
0.12±0.017
-
- significant (p<0.05)
Risk factors associated with microfilaremia
Vacant space
HHD size
Distance
Area
p-value
Rel.risk
p-value
Rel.risk
p-value
Rel.risk
A
0.0089**
1.50
0.0016**
0.87
0.6656
0.99
B
0.5543
1.15
0.4425
1.05
0.0973
0.95
C
0.0555
1.25
0.2772
0.96
0.0141**
1.00
* RR=exp (regression coefficient) with risk increased or decreased as the magnitude
relative to 1 (no change of risk)
** significant (p<0.05)
Before
During
After
Relative
changes, risk
(RR)
Additional
notes
Other prevalence studies in the same region:
- Harb M-Bull World Health Organ. 1993;71(1):49-54.
62
Appendix 6.11. Key information form (Appawu-1994-Acta Tropica)
WHO sub-Region 1
Disease
Author
Title
Lymphatic filariasis
Appawu MA, Baffoe-Wilmot A, Afari EA, Nkrumah FK, Petrarca V.
Species composition and inversion polymorphism of the Anopheles
gambiae complex in some sites of Ghana, west Africa.
Acta Tropica. 1994 Feb;56(1):15-23.
Reference
Language
English
Country, year of study
Ghana, 1993
Village, district, region
North-south transect through Ghana
Geographical coordinates WHO sub-region {1-14} 1
Samples of Anopheles gambiae s.l. were collected from eight
Abstract
localities belonging to four of the five main ecological strata of Ghana.
Analysis of ovarian polytene chromosomes revealed the presence of
An. gambiae s.s. in all the sites studied, while An. arabiensis was
detected only in the extreme northern locality of Navrongo and An.
melas in some southern sites. Anopheles arabiensis showed a
degree of inversion polymorphism comparable to the one observed in
other West African countries. The analysis of the chromosomal
polymorphism of An. gambiae s.s. showed the presence of the
FOREST form in the rain forest localities and the SAVANNA form in
the coastal savanna sites. The MOPTI form occurred sympatrically
with the SAVANNA form in the northernmost locality. The possible
influence of the presence of various taxa of the An. gambiae complex
and of their intra-specific variants on malaria vectorial system is
discussed.
Key information
- Species composition (Anopheles gambiae, Anopheles arabiensis,
Anopheles melas) through a transsect in Ghana. Some places have
irrigation. Various ecological zones are represented.
Water resource
- Irrigation in Navrongo, Tachekope and Dawhenya
development and
management project
Type
Rice-irrigation
Year of inception
Outcome measures
(e.g. prevalence,
incidence,
# of cases, parasites
density exposed
population, etc.)
63
Appendix 6.12. Key information form (Dzodzomenyo-1999-Trop Med Int Health)
WHO sub-Region 1
Disease
Author
Lymphatic filariasis
Dzodzomenyo M, Dunyo SK, Ahorlu CK, Coker WZ, Appawu
MA, Pedersen EM, Simonsen PE.
Title
Bancroftian filariasis in an irrigation project community in southern
Ghana.
Reference
Tropical Medicine & International Health. 1999 Jan;4(1):13-8.
Language
English
Country, year of study
Ghana, 1995
Village, district, region
Gomoa Okyereko
Geographical coordinates
La: 5° 25’ N / Lo: 0° 37’ W
WHO sub-region {1-14}
1
Abstract
An epidemiological study to document the endemicity and
transmission characteristics of bancroftian filariasis was
conducted in an irrigation project community in southern Ghana.
In a 50% random sample of the population, the prevalence of
microfilaraemia was 26.4% and the geometric mean microfilarial
intensity among positives was 819 microfilariae/ml of blood.
Hydrocoele was found in 13.8% of the males aged > or =18 years,
and 1.4% of the residents examined, all females, had
lymphoedema/elephantiasis.
Detailed
monitoring
of
the
microfilarial intensity in 8 individuals over a 24-h period confirmed
its nocturnal periodicity with a peak at approximately 0100 hours.
The most important vector was Anopheles gambiae s.l., followed
by Anopheles funestus. The abundance of these mosquitoes and
their relative importance as vectors varied considerably between
the wet and the dry season. Opening of the irrigation canals late
in the dry season resulted in a remarkable increase in the
population of Anopheles gambiae (8.3% of which carried infective
filarial larvae) to levels comparable to those seen during the wet
season, suggesting that the irrigation project is responsible for
increased transmission of lymphatic filariasis in the community.
Key information
- Microfilaremia and clinical manifestations (hydrocele +
elephantiasis)
- Microfilaria periodicity in peripheral blood
- No. (%) of vector species before and after opening of canals
- No. (%) of infected and infective vectors during opened canals
Water resource development Irrigation Okyereko Irrigation Project (OIP)
and management project
Type
Rice
Year of inception
1974
Microfilariae periodicity peak at 2.00 am (8 persons observed)
Outcome measures
(e.g. prevalence, incidence,
# of cases, parasites density
exposed population, etc.)
64
No. mosquitoes caught by human landing catch during the
late dry season (canals opened)
Species
No. collected No. infected
No. infective
(no.
(% infection
(% infectivity
dissected)
rate)
rate)
Anopheles
gambiae s.l.
169 (168)
45 (26.8)
14 (8.3)
Anopheles
funestus
53 (50)
8 (16.0)
1 (2.0)
Anopheles
pharoensis
3 (3)
2 (66.7)
1 (33.3)
Culex
quinquefasciatus
18 (18)
1 (5.6)
0 (0.0)
Mansonella
spec.
17 (17)
1 (5.9)
0 (0.0)
Total
260 (256)
57 (22.3)
16 (6.3)
Wuchereria bancrofti microfilaraemia and clinical
manifestations
Age
No.
No. Geometric No. males
No. of
Mean
with
individuals
group examined with
mf
Intensity in hydrocoele
with
(%)
mf/ml
(%)
elephantiasis
(%)
1-9
87
6
(6.9)
696
0 (0.0)
0 (0.0)
10-19
68
15
(22.1)
1288
2 (4.8)
1 (1.5)
20-39
68
24
(35.3)
999
2 (9.1)
0 (0.0)
40-59
37
19
(51.4)
506
3 (16.7)
3 (8.1)
≤ 60
36
14
(38.9)
737
1 (16.7)
0 (0.0)
Total
296
78
(26.4)
819
8 (5.7)
4 (1.4)
65
Distribution of indoor resting mosquitoes / 1 houses
No. door resting mosquitoes collected (% of
total collected for period
Species
Wet season /
canal closed
Early dry
season /
canal closed
Late dry
season canal
open
Anopheles
gambiae s.l.
113 (61.1)
15 (12.1)
141 (76.6)
Anopheles
funestus
56 (30.3)
101 (81.5)
40 (21.7)
Anopheles
pharoensis
10 (5.4)
3 (2.4)
3 (1.7)
Culex
quinquefasciatus
6 (3.2)
5 (4.0)
0 (0.0)
Mansonella
spec.
0 (0.0)
0 (0.0)
0 (0.0)
Total
185 (100)
124 (100)
184 (100.0)
Before
During
After
Relative changes, risk
(RR)
Additional notes
66
Appendix 6.13. Key information form (Appawu-2001-Trop Med Int Health)
WHO sub-region 1
Disease
Author
Title
Lymphatic filariasis
Appawu MA, Dadzie SK, Baffoe-Wilmot A, Wilson MD.
Lymphatic filariasis in Ghana: entomological investigation of transmission dynamics
and intensity in communities served by irrigation systems in the Upper East Region
of Ghana.
Tropical Medicine & International Health. 2001 Jul;6(7):511-6.
English
Ghana, 2000
Reference
Language
Country,
year of study
Village,
Districts: Kassena Nankana, Bolgatanga, Bawku
district,
region
Geographical Wuru (Kassena Nankana District) La:10° 59’ N / Lo: 1° 34’ W
coordinates Vea (Bolgatanga District) La: 10° 52’ N / Lo: 0° 51’ W
Kongo (Bolgatanga District) La: 10° 50’ N / Lo: 0° 42’ W
WHO sub- 1
region {1-14}
We conducted an entomological study to document the effect of irrigation on the
Abstract
vectors and transmission dynamics of lymphatic filariasis in the Upper East Region
of Ghana. Mosquitoes were collected by indoor spraying of houses in a cluster of
communities located around irrigation projects (Tono and Vea) and others without
reservoirs (Azoka). Anopheles gambiae s.s. was the dominant species and major
vector, followed by Anopheles funestus. Anopheles arabiensis constituted 9-14% of
the Anopheles gambiae complex but none were infective. Culex quinquefasciatus
was also not infective in these communities. Chromosomal examinations showed
that >60% (n=280-386) of the Anopheles gambiae s.s. in irrigated communities were
Mopti forms whilst 73% (n=224) in the non-irrigated area were Savannah forms.
Infectivity rates (2.3-2.8 vs. 0.25), worm load (1.62-2.04 vs. 1.0), annual bites per
person (6.50-8.83 vs. 0.47) and annual transmission potential (13.26-14.30 vs. 0.47)
were significantly higher in irrigated communities.
Key
- No. of different vectors in irrigated and non-irrigated regions
information - No. and distribution of sibling species of the Anopheles gambiae complex in
irrigated and non-irrigated regions
- Frequencies of Mopti and Savannah chromosomal population forms of Anopheles
gambiae s.s. irrigated communities (Tono and Vea) and without irrigation (Azoka)
- Entomological parameters for the transmission of bancroftian filariasis in irrigated
communities (Tono and Vea) and without irrigation (Azoka)
Water
Kassena Nankana: Tono irrigation project
resource
Bolgatana: Vea reservoir
development
and
management
project
Type
Irrigation canals, water storage for livestock
Year of
inception
67
Outcome
measures
(e.g.
prevalence,
incidence,
# of cases,
parasites
density
exposed
population,
etc.)
Mosquitoes collected from irrigated communities (Tono and Vea) and without
irrigation (Azoka)
Tono
Vea
Azoka
Species
no.
%
no.
%
no.
%
Anopheles gambiae
1256
81.9
1831
73.1
756
87.7
Anopheles funestus
254
16.6
471
18.8
48
5.6
Anopheles
pharoensis
0
0
27
1.1
2
0.23
Anopheles nili
0
0
14
0.6
0
0
Anopheles rufipens
24
1.6
0
0
0
0
Culex
quinquefasciatus
0
0
128
5.1
51
5.9
Aedes aegypti
0
0
33
1.3
5
0.6
Total
1534
2504
862
Distribution of sibling species of Anopheles gambiae complex in irrigated
communities (Tono and Vea) and without irrigation (Azoka)
Localitiy
No. examined
No. of Anopheles
gambiae s.s. (%)
No. of Anopheles
arabiensis (%)
Tono
464
402 (86.6)
62 (13.4)
Vea
618
562 (90.9)
56 (9.06)
Azoka
356
306 (85.9)
50 (14.0)
Total
1438
1270 (88.3)
168 (11.7)
Frequencies of Mopti and Savannah chromosomal population forms of Anopheles
gambiae s.s. irrigated communities (Tono and Vea) and without irrigated (Azoka)
Locality
No. examined
No. of Mopti
No. of Savannah
Tono
464
280 (69.79
122 (30.4)
Vea
618
386 (62.5)
176 (37.5)
Azoka
356
82 (26.8)
224 (73.2)
Total
1438
748
320
68
Entomological parameters for the transmission of bancroftian filariasis in irrigated
communities (Tono and Vea) and without irrigated (Azoka)
Locality
Tono
Vea
Azoka
Species
No.
dissected
No.
with
L3
Infective
(%)
Total
of L3
Anopheles
gambiae
s.l.
1256
42
3.34
68
Anopheles
funestus
254
0
0
0
Total
1510
42
2.80
68
Anopheles
gambiae
s.l.
1831
46
2.51
94
Anopheles
funestus
471
6
1.27
12
Total
2302
52
2.30
106
Anopheles
gambiae
s.l.
756
2
0.26
2
Anopheles
funestus
48
0
0
0
Total
804
2
0.25
2
ABR
AIBR
Worm
load
ATP
315
8.83
1.62
14.30
283
6.50
2.04
13.26
188
0.47
1.0
0.47
L3: infective third stag larvae of Wuchereria bancrofti; ABR: annual biting rate; AIBR: annual
infective biting rate; ATP: annual transmission potential.
Before
During
After
Relative
changes, risk
(RR)
Additional
For prevalence rates of this region see:
notes
- Dunyo S.K.-Trans R Soc Trop Med Hyg. 1996 Nov-Dec; 90(6): 634-8.
- Hunter J.M.-1992;35(5):627-45; discussion:645-9.
69
Appendix 6.14: key information form (Supali-2002-Am J Trop Med Hyg)
WHO sub-region 11
Disease
Author
Lymphatic filariasis
Supali T, Wibowo H, Ruckert P, Fischer K, Ismid IS, Purnomo, Djuardi Y, Fischer
P.
High prevalence of Brugia timori infection in the highland of Alor Island, Indonesia.
Title
Reference American Journal of Tropical Medicine and Hygiene. 2002 May;66(5):560-5.
Language
English
Country,
Indonesia, 2001
year of study
Village,
Alor Island
district,
region
Geographical Lo: 124° 30’ E / La: 8° 20’ S
coordinates
WHO sub- 11
region {1-14}
To identify areas endemic for Brugia timori infection, a field survey was carried out
Abstract
in 2001 on Alor, East Nusa Tenggara Timor, Indonesia. Elephantiasis was
reported on this island by villagers as a major health problem. Bancroftian
filariasis was detected in four villages in the coastal area, whereas Brugia timori
was identified in four rice-farming villages. No mixed infections with both species
were found. In the highland village Mainang (elevation = 880 m), 586 individuals
were examined for Brugia timori infection and 157 (27%) microfilaria carriers were
detected. The prevalence of microfilaremic individuals standardized by sex and
age was 25%. The geometric mean microfilarial density of microfilaremic
individuals was 138 microfilariae/ml. Among teenagers and adults, males tended
to have a higher microfilarial prevalence than females. Microfilaria prevalence
increased with age and a maximum was observed in the fifth decade of life. In
infected individuals, the microfilarial density increased rapidly and high levels were
observed in those individuals 11-20 years old. The highest microfilaria density was
found in a 27-year-old woman (6,028 microfilariae/ml). Brugia timori on Alor was
nocturnally periodic, but in patients with high parasite loads, a small number of
microfilariae was also detected in the day blood. The disease rate was high and
many persons reported a history of acute filarial attacks. Seventy-seven (13%)
individuals showed lymphedema of the leg that occasionally presented severe
elephantiasis. No hydrocele or genital lymphedema were observed. This study
showed that Brugia timori infection is not restricted to the lowland and indicated
that it might have a wider distribution in the lesser Sunda archipelago than
previously assumed.
Key
- Prevalence of Wuchereria bancrofti, Brugia malayi and Brugia timori infections
information - Predominance of Wuchereria bancrofti, Brugia timori and Brugia malayi vectors
(Anopheles subpictus complex and Anopheles barbirostris respectively)
Water
Normal agriculture
resource
development
and
management
project
Type
Rice
70
Year of
inception
Outcome
measures
(e.g.
prevalence,
incidence,
# of cases,
parasites
density
exposed
population,
etc.)
71
- Lymphedema and elephantiasis patients were observed almost exclusively in the
rice-farming villages endemic for Brugia timori (no data available)
- Male patients with hydrocele or genital lymphedema were recorded only in
Wuchereria bancrofti endemic areas. In these villages people worked in dry-field
agriculture or as fishermen (no data available)
- Wuchereria bancrofti was endemic only in the coastal, rice-field free areas,
where Brugia timori was found in areas with extensive rice culture. The ecotype
for Brugia timori was characterized as foothills along a riverin valley with irrigated
rice fields
- Anopheles barbirostris is a typical rice field-breeding species as is responsible
for brugian filariasis in many areas in East Asia
- Highland more than 500 m altitude is predominate on Sunda archipelago and it
is likely that Brugia timori occurs in all rice-farming areas in this region where
Anopheles barbirostris is abundant
- No reports of co-endemicity of Brugia timori and Brugia malayi have been
published -> Brugia timori might replace Brugia malayi in this region
Before
During
After
Relative
changes, risk
(RR)
Additional
- For prevalence rates see data in publication.
notes
For further information about the LF situation in the region. see:
- Dennis D.T.-Am J Trop Med Hyg. 1976 Nov; 25(6): 797-802.
- Partono F.- Am J Trop Med Hyg. 1978;27(5):910-5.
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