Strategies and approaches to vector control in nine malaria-eliminating countries: a cross-case study analysis


The review of case studies showed that all countries implemented a range of vector
control interventions, whether they had eliminated (Mauritius, Turkey, Turkmenistan)
or were moving towards elimination (Bhutan, Cape Verde, Malaysia, Namibia, Philippines,
Sri Lanka). The types of intervention used were likely determined by many factors,
including operational constraints, cost, vector density and behaviour, insecticide
resistance levels and epidemiological trends, among others. The vector control tools
used by each country can be found in Table 2.

Table 2. Vector control intervention mix across the nine case study countries

The IVM strategy document was disseminated by WHO in 2004 17]. Most countries that were eliminating or had eliminated had strategies in place that
used components of IVM, in particular the combination of interventions. IRS, insecticide-treated
nets (ITNs) and LLINs were used commonly by most programmes to collectively increase
population coverage, along with larval control. Some countries supplemented these
interventions with environmental management, personal protection and insecticide fogging.
Implementation most typically occurred at the district level, with guidance and strategy
development provided at the national level. Some reports showed outsourcing of vector
control activities to community volunteers or the private sector. There was little
explicit description of the other four components of IVM, such as collaboration in
health and with other sectors; advocacy, social mobilization and legislation; capacity
building; nor development and use of evidence-based decision-making.

The rationale for which tools were used and which were not used was not well-articulated
in the case studies. Moreover, there did not appear to be a clear linkage between
entomological surveillance data, including insecticide resistance data, and parasitological
data, nor was there evidence that either types of data informed intervention choice.
Instead, the availability of funding and cost of interventions appeared to have played
an important role in decision making for vector control interventions. The coverage
and targeting of interventions was also poorly reported in the case studies. Some
case studies included detailed stratification strategies, but not all. Even for those
with a stratification strategy, most case studies did not consistently report on intervention
coverage, and the ways in which coverage was described varied enormously, making comparisons
across time periods and countries difficult. There was little evidence of reported
quality assessment of interventions.

Measurement or evidence of impact of vector control interventions was scant or practically
absent. Many case studies indicated that activities were effective in reducing receptivity
in risk areas, but did not provide evidence or indicators, instead using anecdotal
evidence that was likely based on programme experience.

In the analysis, the targeting, coverage and impact of all vector control measures
were compared across the case study countries and similarities and differences highlighted.
The results are described below for each vector control approach and tool.

Integrated vector management

IVM was adopted by four of nine programmes in the cross-case study analysis, but the
meaning and utility of IVM varied across case studies (Table 3). The strategy of IVM was introduced in 2004 by WHO to increase cost effectiveness
of vector control and to reduce the spread of drug and insecticide resistance 17]. The strategy focused on using a combination of interventions to attack the vector
at different stages of its life cycle. It also requires decisions on which tools to
use to be made based on evidence and that the type of vector control deployed will
change as one approaches elimination and post-elimination (Fig. 1). For some countries (e.g., Turkmenistan) it was used as a way to combine vector
control interventions. In other countries it ensured intersectoral collaboration,
community engagement and integration of services, such as entomological surveillance,
with other diseases (e.g., dengue). In Sri Lanka, IVM combined all of these elements,
and engaged other sectors and communities in developing vector control strategies.
It also ensured the use of a mix of interventions, as well as insecticide rotation
for IRS, in which different types of insecticides were used in bordering districts
with rotation of insecticides across districts over time, in order to lessen the risk
of the development of insecticide resistance.

Table 3. Integrated vector management adoption and definition

The impact of IVM was not articulated in the reports, except for Sri Lanka, where
the use of the approach in agricultural areas was thought to have contributed to a
reduction in malaria incidence. Further research would be valuable to understand the
impact of implementation of IVM as a broad strategy on reducing malaria transmission.

Entomological surveillance

Most countries in the case study series began conducting entomological surveillance
during the GMEP. Entomological surveillance is typically comprised of monitoring of
larval habitats, surveying for adult mosquitoes, conducting insecticide susceptibility
tests, and assessing changes in environmental parameters 4], with the objectives of identifying the level of change in receptivity, and of designing
and monitoring effectiveness of programme vector control strategy and interventions.
The case studies did not outline specific activities that were maintained in the current
elimination periods, instead only providing details and time frame when a new effort
or initiative was undertaken. Even for countries that had more consistent entomological
surveillance, the response component was not articulated in the case studies; it appears
that, for most countries, entomological surveillance data were not analysed and used
for outbreak forecasting or programme strategy, including better targeting of vector
control interventions.

There was variation in the quality and consistency of entomological surveillance across
the case studies. Countries that have reached elimination generally had a more detailed
description of their surveillance programmes. For example, in the years leading up
to elimination in Turkmenistan (2004–10), the programme maintained ‘passports’ for
each water body, and district officials systematically updated a database on vector
bionomics and densities. Entomological officers were recruited to serve on epidemic
response mobile teams. In Turkey, surveillance included mapping of larval habitats
in addition to data collection in sentinel sites. The continuation of this type of
surveillance through the years of POR and post-elimination certification was only
described in detail in the Mauritius report, where the programme maintained weekly
surveillance of breeding areas since elimination in 2008.

The Malaysia and Sri Lanka case studies likewise described strong entomological surveillance
programmes. In both countries, consistent entomological surveillance was one of several
approaches credited by the malaria programmes for the national progress in reducing
incidence, as it was used to guide planning of vector control. Malaysia’s diversity
of vectors was a reason for continual monitoring, and district-level surveillance
tracked larval habitats (conducted by district entomologists and assistant environmental
health officers). Mapping with GPS units captured housing locations and larval habitats.
Sri Lanka’s national and district health offices conducted entomological surveillance
on a monthly basis. In later years, Sri Lanka had a large increase in funding to support
entomological surveillance (from a Global Fund grant), which was conducted by a private
sector organization in some areas. In Bhutan, surveillance was conducted monthly.

In other countries, entomological surveillance was more limited, such as in Cape Verde,
where there was not a consistent programme of monitoring. Surveillance in the Philippines
was limited to semi-annual or annual monitoring in the sporadic and malaria-prone
transmission provinces.

In all case study countries, data collected during surveillance were not consistently
used by programmes. Most case studies did not describe the use of entomological surveillance
data to assess impact of interventions or to inform programme strategy. For example,
because Turkey did not conduct entomological evaluations pre- and post-epidemic (after
1993), the programme was unable to assess effectiveness of the response interventions.
There are some examples of programmes using their entomological data to guide decision-making.
In the Philippines, surveillance data were reviewed during sub-national, provincial
elimination certification, a process that was formalized in 2011. In addition, prior
to the national programme’s devolution, all new strategies were tested through field
research and entomological and parasitological surveys before becoming policy, such
as the shift from IRS alone to combined IRS with ITNs. Bioassay and susceptibility
test results guided changes in insecticide usage. In Malaysia and Mauritius, maps
of larval habitats were used to target vector control interventions. Also in Malaysia,
research was undertaken by district and state officers to measure effectiveness of
management of the larval stage of the vector in reducing receptivity, although the
outcomes of this research were not described in the report.

As entomological surveillance data should be the basis for all response interventions
and programme strategies, consistent and high-quality data are needed. Further action
is required to ensure that entomological surveillance is a priority for elimination
programmes and that data are analysed and inform robust response, including forecasting,
targeting and programme strategy.

Indoor residual spraying

Each of the nine programmes employed IRS, and most countries continued IRS after its
introduction during the GMEP era because IRS historically was found to be effective
in reducing receptivity. IRS targeting strategies varied across the countries, but
generally by the 1990s most countries had transitioned to focal IRS instead of universal
coverage, or blanket spray, operations. This transition may have been in response
to the introduction of the WHO Global Strategy for Malaria Control 18]. As all countries (both eliminating and POR) approached elimination, their programmes
transitioned to targeting IRS for active foci or active transmission areas.

In the case studies there were several instances of premature reduction of coverage
or disbanding of IRS, some of which were linked to subsequent resurgences of malaria
(e.g., Cape Verde, Sri Lanka, Turkey). The reported reasons for reducing IRS operations
varied, but the trend was that scale-down occurred when countries were very close
to eliminating malaria or were firmly in the POR stage. In Sri Lanka, IRS was halted
in eliminated areas, which is thought to have contributed to the epidemic of 1957.
In more recent times, Sri Lanka has shown a decline in IRS coverage as it moved from
full coverage of risk areas to focal IRS (conducted in areas with malaria cases) and
outbreak response, moving from 23 % coverage of total population in 2005 to 6 % in
2010. Even without continued IRS coverage, however, to date Sri Lanka has been able
to maintain low caseload and has not experienced a resurgence, perhaps related to
the continued distribution of LLINs and use of larval control in addition to a strong
surveillance system. In Cape Verde, in contrast, twice in recent history, foci on
Santiago Island were re-activated within 3 years after relaxation of aggressive, bi-annual
IRS operations. IRS was not replaced by another vector control intervention; larval
control (temephos and larvivorous fish) was used after the 1960s in Cape Verde, but
there is no evidence in the case study that it was scaled up when IRS declined, and
coverage data were not available. Cape Verde has since continued its small-scale IRS
operations, mainly outbreak response activities that covered about 5–10 % of Santiago
Island.

Turkey scaled down IRS to residual foci only when it did not achieve elimination during
the GMEP, and in the 1970s and 1990s fell short of coverage of active foci that was
achieved in 1961 (86–88 %) and 1968 (nearly 100 %). In both the 1970s and 1990s, reductions
in IRS coverage were linked to the availability of funding; the malaria service was
under pressure to reduce expenses when it did not reach elimination. Other challenges
included operational constraints, lower quality of implementation, a high rate of
refusals in the target population, and insufficient and inexperienced staff. IRS was
not replaced by another method of vector control at that time, although larviciding
had been used as a complementary measure since the late 1950s. In its latest strategy,
the country reserved IRS for areas with residual or active transmission. Likewise,
Mauritius did not have enough funding to conduct IRS island-wide during its second
elimination attempt, so it was restricted to areas with ongoing transmission. Mauritius
used a combination of interventions (IRS, fogging, larval control, and entomological
surveillance) for areas with transmission that reported more than three cases. Areas
with fewer than three cases did not receive IRS. Coverage was described as 65–80 %
of foci in 1986, although it was not clear in the case study if this was considered
sufficient. In recent years, Mauritius used IRS to prevent establishment of transmission
within a residence of a confirmed case, of which all are imported.

Some countries, particularly those in the early stages of elimination, indicated that
operational constraints, instead of a stratification strategy, led to the scale-down
of IRS. Worker shortages and an inability to mobilize spray teams, inadequate training,
and low morale were all factors described in the case studies. In the 1990s, the Philippines
reduced IRS coverage to 20 % of targeted areas as a result of operational disruptions
during the process of programme decentralization. Even when an increase in funding
boosted coverage to two spray cycles per year with 76 % of target achieved, quality
was considered poor due to delays, lack of training, and an insufficient number of
spraymen. In part because of the operational challenges and in part due to Global
Fund influence, the country focused instead on LLIN distribution. In 2011, ITN and
LLIN coverage in the 40 target provinces was 73 % of the total target population.
In Namibia, rainy conditions, poor roads and worker shortages have prevented completion
of IRS activities. IRS national coverage of at-risk populations ranged from 16 to
41 % from 2001 to 2011, and the country revised its goal to a target of 95 % coverage
in areas of moderate endemicity and 100 % focal coverage in low-endemic regions, prioritizing
the highest burden villages in the event that the spray season was cut short due to
staffing or logistics problems. In Bhutan, political instability in the southern region
in the early 1990s led to difficulties in completing IRS spray campaigns and by 1994
cases were increasing. IRS was halted in 1998 when the programme switched to ITNs
as a primary vector control measure. Focal IRS was re-instated in 2004 and by 2012
the Bhutan programme reported achieving 100 % coverage of its target population (14 %
of the population at risk).

Some countries appear to have maintained a consistent level of coverage. Turkmenistan
employed IRS as an outbreak response measure, covering 91–100 % of targeted areas
during the 1998–2000 period. The programme did not conduct IRS from 2005 because there
were no malaria infections to ‘trigger’ the focal IRS response. The case study on
Malaysia did not report any decline in IRS activities, but it was challenging to understand
the coverage because it was measured as the number of households sprayed of those
targeted, and not by proportion of risk population protected.

Some programmes relied on communities or volunteers for IRS campaigns, such as in
the Philippines. Bhutan also trained community volunteers to conduct IRS, however
the quality and coverage declined so volunteer teams were disbanded. In some private
sector plantations in Sabah State (Borneo) of Malaysia, IRS was implemented (and paid
for) by the plantations, with oversight by the Sabah Malaria Control Programme.

Effectiveness of IRS to reduce receptivity was assumed in the reports, evidenced by
declines in malaria incidence in the 1950s and 1960s that were linked with increases
in IRS coverage. But the picture became more complicated in recent years, as multiple
interventions were employed at the same time. This was the case in Malaysia, where
IRS with ITN distribution (ITN distributed began in 1995) was credited for a decrease
in annual parasite index (API), the number of reported cases per 1000 population per
year, from 3.0 (1995) to 0.5 (2000), in addition to the benefits of replacing DDT
with pyrethroids in 1998. Turkey and Mauritius also attributed malaria case declines
to IRS activities along with active surveillance measures.

Most case study reports did not contain adequate information on recent insecticide
resistance monitoring activities or description of evidence of resistance. Malaysia
and the Philippines described the sentinel sites for monitoring insecticide resistance.
Malaysia, Namibia, and the Philippines reported conducting bioassay and susceptibility
tests on insecticides. In the Philippines, Laguna Province shifted insecticides reportedly
due to a drop in effectiveness after 10 years, and more recently there was pyrethroid
resistance possibly detected in Isabela Province. Sri Lanka implemented insecticide
rotation in 1998, part of IVM, in order to prolong the life and utility of the insecticides
and optimize vector control.

Given the experience of several countries that halted or scaled down IRS and suffered
serious epidemics and resurgences of malaria, further research is needed on the transmission
dynamics in various types of contexts, and the alternative methods, such as larval
source management, that can be put into place to avoid resurgence. Information should
also be shared on the monitoring for insecticide resistance and the programmatic response
to the data collected. For some countries, typically higher endemic areas, logistical
issues or decreases in funding have led to poor quality implementation or disruption
of IRS. Less resource intensive, sustainable methods for vector control must be explored
for some countries.

Space spray

Outdoor space spray with insecticide was reported in the case studies of three programmes:
Mauritius, Sri Lanka and Turkey.

Mauritius used space spray as an epidemic response measure starting in 1975, but by
1981 it was discontinued. Implementation was viewed as costly and ineffective because
it was conducted in the morning when the temperature was too warm. The thermal clines
made the insecticide rise and in addition the mosquitos were not flying at that time.
It was re-instated in 1982 as a response to the outdoor-biting behaviour of Anopheles gambiae s.l., this time conducted in the evening. At that time, coverage was limited to the Port
Louis areas in response to outbreaks only. In Sri Lanka, space spray has been used
during festivals and other large gatherings, but coverage and effectiveness was not
articulated in the case study. Turkey conducted space spray as an outbreak containment
strategy. While the report indicated that epidemics were controlled through a combination
of interventions that included space spray, there are no data on the effectiveness
of space spray alone. More research specifically on the impact on malaria transmission
of space spray in countries that use it would help in developing an evidence base.

Long-lasting insecticidal nets/insecticide-treated nets

Most malaria programmes in the case study series employed ITNs, followed by LLINs
as they became available, as a supplementary vector control measure to IRS. However,
the countries in POR (Mauritius, Turkey, Turkmenistan) never used ITNs or LLINs, as
they had achieved elimination before they were available. One exception is Turkmenistan,
where locally made bed nets were in use since the 1930s and were reportedly widely
used (coverage rates not given) in the 2004–2010 elimination campaign.

Of the six eliminating countries, Cape Verde never employed LLINs or ITNs, although
information on the reasons behind this was not reported. ITNs/LLINs became a primary
vector control tool in the Philippines and Namibia, and replaced IRS for 6 years in
Bhutan (1998–2004), until cases doubled from 1998 to 1999, sparking a programme review
and the introduction of several activities, including focal IRS to supplement ITNs.
The programme had struggled to re-treat ITNs in a timely manner, which may have contributed
to the increase in cases. Malaysia never switched from ITNs to LLINs because the programme
believed that ITNs were sufficient. Malaysia also did not have external funding, such
as a Global Fund grant, which may have contributed to the decision to continue ITN
use. LLINs have been used to protect populations living or working in hard-to-reach
or remote areas, such as parts of Bhutan and in the former conflict zone of Sri Lanka.
NGOs in Sri Lanka that were familiar with the conflict-affected communities in the
east and north distributed LLINs.

Similar to reporting on IRS coverage, comparison of coverage and its definition for
ITNs/LLINs across case studies was challenging. Countries used different estimates,
most based on net ownership rather than any measure of use, including the number of
nets distributed as a proportion of the national total population or national population
at risk. Only the Philippines case study report detailed the assumptions behind the
LLIN coverage indicator. In the Philippines, coverage was defined as two people having
an LLIN for an assumed net lifespan of 3 years. In Sabah, one of the most endemic
areas of Malaysia, 55 % of the high-risk areas were considered covered by ITNs in
2009. The distribution of ITNs then increased, from 56,000 in 2009 to nearly 80,000
in 2011, while continuing re-treatment of older ITNs. In Sri Lanka, LLINs were introduced
in 2004 and by 2005 15 % of the population at risk, approximately 440,000 persons,
was considered to be covered (protected) by a LLIN, climbing to 35 % by 2010. It was
believed that the combination of IRS and LLINs in the country helped to lower receptivity.
The Philippines programme first distributed ITNs in 1990, then LLINs were introduced
in 2005, and by 2011, ITN and LLIN coverage in the 40 provinces that received funding
from the Global Fund was 73 % of the target. In Namibia, ITNs were first distributed
in 1993 and then replaced by LLINs in the mid-2000s. By 2005, coverage ranged from
5 to 10 % of the population at risk, increasing to 50 % in 2009 and 2010, but dropped
down to 30 % in 2011. Mass distribution of nearly 500,000 LLINs in the northern regions
was conducted in 2013.

Other alternatives have also been tested. The Philippines experimented with hammock-type
LLINs for their military but they found the available design to be too difficult to
climb out of so they were not scaled up. Hammock LLINs were found to be an effective
tool for preventing malaria in forested areas of Cambodia, but this may be related
to cultural factors, as villagers and forest workers in the area were used to using
hammocks in the early evening hours 19]. In Sri Lanka, efficacy of insecticide-treated curtains was studied in the late 1990s
but no scale up was reported.

ITNs/LLINs have been a core vector control tool for many countries, in particular
for populations that are harder to reach with IRS. However, coverage estimates are
difficult to compare across countries, and actual use has been difficult to estimate,
thus it has been difficult to estimate the impact of ITNs/LLINs. Routine monitoring
of coverage and impact of LLINs must be enhanced to better estimate their programmatic
impact, especially on a more regular basis, to support locally relevant use of the
nets.

Larval control

Larval control is defined as the use of substances that kill or inhibit the development
of mosquito larvae or the introduction of fish or invertebrates that feed on larvae
20], and has been employed by all countries in the analysis. Larval control can include
either larvivorous fish or larviciding (which includes both chemical and biological
agents in water bodies to kill mosquito larvae).

Most countries started using larval control in the early years of their control programmes
(1930s or 1940s) or during the GMEP campaign. Several of the case studies highlighted
larval control as a strategy for outbreak or epidemic response (e.g., Bhutan, Malaysia,
Mauritius, Turkey, Turkmenistan). In some countries larval control was used as a supplement
to IRS, to cover areas that had low or phased-out IRS coverage (e.g., Cape Verde,
Mauritius, Sri Lanka), or when zero cases had been reached and IRS was discontinued
(Turkey, Turkmenistan). Coverage was typically measured by the number of persons estimated
to be protected by this method but this was not detailed in most of the case study
reports. When coverage was reported, it was measured in a variety of ways.

In the countries that have eliminated malaria (Mauritius, Turkey, Turkmenistan), larval
control has been a continuous and important vector control method and is part of their
POR strategic plans. In Mauritius, use of larvivorous fish was perceived to be useful
when implemented in proximity to the airport (to lower receptivity in an area that
may have imported cases) as well as in deeper rooftop pools and irrigation ponds where
vectors were breeding. For the eliminating countries, there were differences in when
and why larval control was used. In Malaysia, for example, it was used in low-risk
areas throughout the year to keep receptivity at low levels; in contrast, in Namibia
it was used primarily in the dry season, when there were fewer water bodies to treat.
Sri Lanka used chemical larviciding in abandoned gem pits and wells. Difficulties
in implementing larval control were noted throughout the case studies. In Namibia,
perceived risk of poisoning animals impeded its widespread use, as did the cost. Inconsistent
use of larval control (Philippines and Namibia), lack of intervention data reported
to the central level (Cape Verde), lack of breeding site maps (Mauritius), and lack
of entomological surveillance in intervention areas (Mauritius) made it difficult
to assess the impact of larval control on reducing receptivity or malaria incidence.

Effectiveness of larval control has been measured in Mauritius and Turkey. However,
it was conducted in combination with other interventions (in Mauritius alongside IRS
and fogging; in Turkey alongside IRS and environmental management) so it was not possible
to identify the impact of larval control alone. Research on larval control undertaken
in Sri Lanka showed reductions in vector density in the laboratory and in field sites,
such as dams, gem pits, brick-making fields, and cement water tanks 21], 22], but the study did not measure impact on malaria transmission.

Similar to IRS and LLINs, coverage of larval control has been measured in different
ways across programmes. Countries measured larval control by coverage of larval habitats,
hectares, reservoirs, or by the number of people protected, all of which are challenging
to compare or understand the scale, much less the impact of this intervention. In
Turkmenistan, 136 larval habitats and labour camps (in the early 2000s) were covered
by larval control, and (in 2009) six hectares were treated with oil-based larvicides
and 1828 hectares were treated with fish. In Mauritius (1985), nearly 16,000 potential
larval habitats were treated with temephos. In Sri Lanka in 2001 approximately one
million people were estimated to be protected through the distribution of larvivorous
fish, but by 2002 only 40,000 were considered to be protected.

As there are some countries that may rely heavily on larval control in the prevention
of re-introduction stages, such as Sri Lanka, more rigorous monitoring, including
stronger indicators, and measurement of impact is needed to understand the best settings
for its implementation.

Environmental management

Environmental management activities aim to reduce the size of the immature vector
population through habitat modification 20]. Environmental modification activities ranged across the case studies, depending
on the Anopheles species and their preferred larval habitats: cleaning and drainage projects (Bhutan,
some parts of Malaysia, Mauritius), marsh draining (Turkey), cleaning or flushing
of stream or irrigation canals (Philippines, Sri Lanka, Turkey), infilling of unused
reservoirs (Turkmenistan), intermittent drying of reservoirs (Cape Verde), protection
of water tanks (Cape Verde), and filling of unused gem pits (Sri Lanka). Namibia did
not list any of these activities.

Environmental management was used as a major intervention for five programmes (Turkey,
Turkmenistan, Malaysia, Philippines, Sri Lanka) since the early 1900s. In Malaysia
it was mainly used in West Malaysia. It was continued as a supplementary measure to
IRS in Turkey and Malaysia, as an outbreak response measure in Turkmenistan, and part
of the POR strategy in Mauritius. Coverage was not reported in the case studies.

In Mauritius, the large-scale draining/cleaning projects, in addition to other factors
such as improvements to housing structures and urbanization, is credited with decreasing
the level of malaria transmission before the initial malaria elimination campaign
and helped to sustain lower transmission levels during the rest of the 20th Century.
In the Philippines, stream clearing was used as a supplementary vector control measure,
but had limited overall impact on case incidence, which may be in part due to its
inconsistent use.

Similar to larval control, environmental management has been used by many countries
as an ongoing vector control tool, and may become more important in the end stages
towards malaria elimination. However, as with larval control, methods to monitor its
impact on transmission need to be improved.

Personal protection

Four of the case studies reported having a strategy that included use of personal
protection approaches, such as promotion of protective clothing, or insecticide-treated
products and some without a strong evidence base, such as ingesting traditional herbal
medicines. For example, in the Philippines, use of personal protective measures during
evening activities was a recommended strategy, but the specific activities were not
described. Namibia promoted awareness in the community of wearing protective clothing,
and in one region the population traditionally used herbs as personal protection.

Personal protection methods may become more important in settings where outdoor-biting
anophelines play or will begin to play a larger role in transmission, owing partly
to vector replacement dynamics. Additional evidence is needed on the effectiveness
of these tools on transmission reduction at the community level.

Economic development and development projects

Economic development was noted as a main contributor to declining receptivity across
many countries as it catalyzed changes that impeded the breeding, feeding or resting
behaviour of major malaria vectors. Economic development may have led to changes at
individual household level (e.g., housing materials) or larger community level (e.g.,
large-scale construction projects, urbanization, increased access to medical care
and services). Improvements in housing made indoor feeding more difficult, as anophelines
were less able to enter and exit homes pre- and post-feeding. These improvements,
including use of air conditioning by about 50 % of households and villages, were likely
contributors to a reduction in receptivity in Turkmenistan. Similarly, in Bhutan,
electrification of homes and subsequent use of electric fans may have reduced transmission.
Urbanization is another factor, in that it reduced the number and surface area of
anopheline breeding habitats. Water bodies became dry or polluted in some provinces
in the Philippines, leading to a decline in larval habitats, since the primary vectors
require clear, clean, slow flowing water. For many case study countries, in particular
in the Asia Pacific, primary vectors were forest dwelling. Increasing deforestation
reduced vector-breeding habitats, such as in Sabah State of Malaysia, where the decline
in forest habitat was believed to have reduced vector abundance of Anopheles balabacensis. Economic development in Mauritius in the 1950s and 1960s reduced malaria transmission,
leading to the first malaria elimination campaign (1969) and helped to sustain lower
transmission levels for the rest of the Century. Although receptivity may have declined
in some countries, these transitions were also accompanied by increases in population
movement or immigration into receptive areas, elevating the potential risk of transmission.
This increased vulnerability due to risk of importation has affected Bhutan and Malaysia
even while receptivity is declining.

While changes in economic or infrastructure development in some countries led to a
decrease in receptivity, in some areas changes led instead to an increase in receptivity.
Irrigation schemes increased levels of receptivity in several countries, such as in
Turkey and Mauritius. Dam construction was thought to have increased receptivity in
Sri Lanka, Turkmenistan and Bhutan. For example, in Sri Lanka, the 1987 epidemic was
linked to a major dam construction project on the Mahaweli River, in the malaria-endemic
eastern part of the country, which included forest clearing for rice cultivation.
This change in land use resulted in an increase in receptivity, which increased risk
of malaria for the one million settlers who moved there from non-endemic areas.

Cape Verde and the Philippines provide examples of the increase in receptivity due
to human behaviour. In Mauritius, flat rooftops became popular after the 1960s but
because of the pooling of water may have led to an increase in receptivity, as they
provided good larval habitats for Anopheles gambiae. In the Philippines, the benefits of electrification in reducing transmission may
have been offset in remote areas as more people stayed up later in the evening hours
when vector exposure is greatest.

Some changes in development have accelerated malaria transmission or, in contrast,
progress toward elimination. In either case, continuous measurement of receptivity
will alert malaria programmes to changes in transmission dynamics. This measurement
relies upon ongoing, robust entomological surveillance.

Combining vector control strategies

Most programmes rely on a combination of interventions, which together are believed
to have reduced vectorial capacities and receptivity of the risk areas.

IRS was a primary tool for most programmes, along with ITN/LLIN to increase coverage
of vector control and some type of larval control. Some countries credited the combination
of interventions with reducing incidence or receptivity in their countries. In Mauritius,
IRS, space spray and larviciding were used in combination with surveillance in active
foci; non-active foci receive all interventions except for IRS. The programme attributed
success to the control of larval habitats above all other interventions. In the Philippines,
the combination of IRS and LLINs was credited for the significant drop in cases since
the 1990s. In Turkey, the impact of vector control methods was used as a justification
for the setting of a national elimination goal, with the plan to use IRS, larvivorous
fish and ITNs to reduce receptivity and achieve elimination.