Am. J. Trop. Med. Hyg., 77(Suppl 6), 2007, pp. 249–263
Copyright © 2007 by The American Society of Tropical Medicine and Hygiene
Dichlorodiphenyltrichloroethane (DDT) for Indoor Residual Spraying in Africa:
How Can It Be Used for Malaria Control?
Shobha Sadasivaiah,† Yeşim Tozan,† and Joel G. Breman*
Weill Cornell Medical College of Cornell University, Cornell University, New York, New York; Earth Institute, Columbia University,
New York, New York; and Fogarty International Center, National Institutes of Health, Bethesda, Maryland
Abstract. In 2006, the World Health Organization issued a position statement promoting the use of indoor residual
spraying (IRS) with dichlorodiphenyltrichloroethane (DDT) for malaria vector control in epidemic and endemic areas.
Other international organizations concurred because of the great burden of malaria and the relative ineffectiveness of
current treatment and control strategies. Although the Stockholm Convention of 2001 targeted DDT as 1 of 12 persistent
organic pollutants for phase-out and eventual elimination, it allowed a provision for its continued indoor use for disease
vector control. Although DDT is a low-cost antimalarial tool, the possible adverse human health and environmental
effects of exposure through IRS must be carefully weighed against the benefits to malaria control. This article discusses
the controversy surrounding the use of DDT for IRS; its effective implementation in Africa; recommendations for
deployment today, and training, monitoring, and research needs for effective and sustainable implementation. We
consider the costs and cost effectiveness of IRS with DDT, alternative insecticides to DDT, and the importance of
integrated vector control if toxicity, resistance, and other issues restrict its use.
INTRODUCTION
HISTORY
Although malaria has been successfully eradicated in highincome and many middle-income countries, the disease remains a major health problem in poor nations. This disease
wreaks havoc in Africa, where the majority of the global malaria incidence (70% of clinical Plasmodium falciparum cases)
is concentrated.1 It was estimated that 18% of child deaths
were directly attributable to the disease in this region in
2000.2 Malaria is ranked second after human immunodeficiency virus/acquired immunodeficiency syndrome (HIV/
AIDS) and accounts for an estimated 10% of the total disease
burden on this continent3; a recent study showed that coinfection fuels the spread of both diseases and results in excess HIV infections and clinical malaria episodes.4 In addition
to its direct health impact, the disease imposes a huge economic burden on afflicted nations through high healthcare
costs, missed days of work and school, reduced economic productivity and output, and low levels of foreign investment.5
The enormous toll that malaria takes on the world’s poorest and most vulnerable populations require all proven and
cost-effective interventions be deployed to battle this scourge.
Malaria control efforts are driven by the persisting health and
economic burden of the disease. However, restricted impact
on disease transmission of the current patient management
and preventive strategies (e.g., insecticide treated nets
[ITNs]) limits progress toward internationally set malaria
goals and targets and poverty reduction.6 Indoor residual
spraying (IRS) with dichlorodiphenyltrichloroethane (DDT)
is now reentering the armory of malaria endemic countries
and international organizations committed to controlling the
disease. This article reviews the role of IRS with DDT in
malaria vector control, clarifies a place for DDT as a residual
insecticide among alternatives, and raises operational and
technical issues for consideration when using DDT for IRS.
After the discovery of the insecticidal properties of DDT in
1939, further testing of the insecticide was conducted at the
U.S. Department of Agriculture’s laboratory in Orlando,
Florida, in 1942 and 1943.7 The tests confirmed the practical
value of DDT in disease vector control, and the insecticide
was first used by the military personnel in southern Italy in
1944 and in other parts of the world in the final years of
World War II.8 In 1945, DDT was introduced as a vector
control measure in civilian populations in Guyana and Venezuela9,10 and then in 1946 in Cyprus and Sardinia.9 Although
large-scale use of DDT for disease vector control started in
1946,11 the insecticide had been intensively applied for agricultural pest control since 1940.12
The astonishing impact of DDT on mosquito longevity resulted in successful early campaigns against the malaria vector. Calls for the global eradication of malaria followed.13 In
addition, many field studies consistently provided evidence
that the primary effect of DDT is its excito-repellency, deterring entry into or driving mosquitoes out of sprayed houses
and reducing transmission with lower feeding rates and
shorter resting periods.14 There was a marked reduction in
the mean age of mosquito population as measured by the
number of ovarian dilatations and a 86% reduction in the
sporozoite inoculation rate after the introduction of IRS with
DDT in a holoendemic area of Tanzania.15
In 1955, the World Health Organization (WHO) launched
the Global Malaria Eradication Campaign based on the periodic use of IRS with DDT for 3–5 years to interrupt malaria
transmission.16 This time-limited attack phase would have
been followed by active case detection and surveillance to
prevent disease propagation.16 Weak healthcare systems, insufficient administrative, operational, and technical capacity,
and public reaction to spraying were the major factors contributing to the demise of national eradication programs.13
However, it was the development of Anopheline resistance to
DDT that was primarily responsible for the dwindling political and financial support for the global campaign.13 The
eradication period ended in 1969, and the eradication strategy
was replaced by a longer-term disease control strategy as part
of the growing primary healthcare movement of the 1970s.13
† The first two authors contributed equally to this manuscript.
* Address correspondence to Joel G. Breman, Fogarty International
Center, National Institutes of Health, Bethesda, MD. E-mail:
[email protected]
249
250
SADASIVAIAH AND OTHERS
Although the Global Malaria Eradication Campaign did
not achieve its ultimate objective, it was credited with eliminating the risk of disease for about 700 million persons,
mainly in North America, Europe, the former Soviet Union,
all Caribbean islands except Hispaniola, and Taiwan.17 High
socio-economic status, well-organized healthcare systems,
and relatively less intensive or seasonal malaria transmission
were the main factors in attaining the disease elimination goal
in these regions.16 Malaria was effectively suppressed in subtropical and tropical areas of Asia, Latin America, and the
Middle East.17 Notable among those efforts was the near
eradication of malaria in India, where the annual number of
malaria cases was reduced from an estimated 75 million to
about 100,000 in the early 1960s.18 These reductions were not
sustained after the eradication period because limited resources were devoted to malaria control. Because of the perceived intractability of the disease and concerns about infrastructure and sustainability, large swaths of Africa were left
out of the global eradication efforts.13 Yet several African
countries embarked on pilot projects of IRS with DDT and
dieldrin with the assistance of WHO and the United Nations
Children’s Fund from between the 1940s and 1960s.19–21 Although malaria transmission was not interrupted in areas with
intense and stable transmission (holoendemic to mesoendemic zones) with tropical climates, malaria vectors and
prevalence rates were considerably reduced during these
projects (e.g., in Cameroon, Kenya, Liberia, Nigeria, Senegal,
and Tanzania).19–21 In areas with seasonal and unstable transmission (hypoendemic) with subtropical and temperate climates, IRS projects interrupted transmission in vast territories and eliminated the disease at the limits of tropical Africa.20 Malaria eradication programs were implemented on
the islands of Zanzibar and Pemba, and the pilot projects
were scaled up to national level in South Africa, Swaziland,
Zimbabwe, and the islands of Madagascar, Mauritius, and
Réunion.20
With the publication of Silent Spring by Rachel Carson in
1962, the safety of DDT for human health and the environment was challenged. Before DDT was officially banned in
the United States in 1972, it was registered for use in 334
agricultural products.12 Driven by the expansion of commercial agriculture, large areas in India and the Central American
countries were intensively treated with DDT in the 1960s and
1970s where national eradication campaigns were also operational.22 Between 1940 and 1973, estimates indicated that
more than 2 million tons (4 billion pounds) of DDT were used
in the United States, about 80% of them in agriculture, and
some level of resistance was reported in populations of 98
species of economically important insects.12 Because of the
growing environmental concerns, the agricultural use of
DDT diminished rapidly from the 1970s onward, affecting
use of the insecticide for public health. DDT for disease
vector control was never banned but international pressure
restricted its implementation in malarious countries. In the
late 1990s, an intense debate erupted when negotiations for
global elimination of DDT were initiated by the United Nations Environment Program (UNEP) against a background of
an increasing malaria burden.23 In 2001, the Stockholm
Convention on Persistent Organic Pollutants classified
DDT as restricted (Table 1) and allowed a provision for its
continued use for disease vector control following the WHO
guidelines when “locally safe, effective, and affordable alter-
TABLE 1
The 12 persistent organic pollutants targeted by the Stockholm Convention on Persistent Organic Pollutants24*
Compound
Aldrin
Dieldrin
Endrin
Chlordane
Heptachlor
Hexachlorobenzene
Mirex
Toxphene
DDT
Class
Classification under
the Stockholm
Convention
Organochlorine insecticide
Organochlorine insecticide
Organochlorine insecticide
Organochlorine insecticide
Organochlorine insecticide
Organochlorine insecticide
Elimination
Elimination
Elimination
Elimination
Elimination
Elimination
Organochlorine insecticide
Organochlorine insecticide
Organochlorine insecticide
Elimination
Elimination
Restriction for disease vector control
Elimination
Polychlorinated Industrial chemical
biphenyls
Dioxins
Combustion byproduct
Furans
Combustion byproduct
Source reduction
Source reduction
* DDT, dichlorodiphenyltrichloroethane.
natives are not available.”24 This provision was approved
without any objection by approximately 150 national delegations,25 including those from Southeast Asia where the use of
DDT was discontinued in malaria control efforts. Although
used in the Americas and Asia, vector control has been neglected as an intervention strategy against malaria in most of
Africa.
Today, the WHO actively promotes the use of IRS with
DDT (Table 2) and recommends implementation in essentially all epidemiologic settings, including unstable, epidemicprone areas; stable-endemic areas with seasonal transmission;
and stable-hyperendemic areas with seasonal or perennial
transmission.26 In this strategy, DDT is sprayed on the walls
and other surfaces inside dwellings where female Anopheles
mosquitoes land and rest before or after a blood meal. The
WHO currently recommends a standard dosage of 1–2 g active ingredient per m2 every 6 months.27 Sufficient contact
with DDT-sprayed surfaces kills malaria vectors. More importantly, DDT has an excitorepellent effect, deterring entry
into and promoting exit from sprayed dwellings.14 It is argued
that the combined mosquito toxicity and excitorepellent effects of DDT may maintain its continued efficacy in areas
where there is resistance against it.14,25 A recent study from
India assessing the impact of IRS with DDT on malaria transmission corroborated the results of earlier Indian studies reporting marked reductions in vector densities and malaria
incidences although the targeted malaria vector had a reduced susceptibility to DDT.28
The gains resulting from IRS activities in Africa between
the late 1940s and the 1960s had not been widely documented
because most of these projects were viewed as a failure when
assessed against a goal of interruption of malaria transmission.29,30 During the past decade, IRS has been implemented
successfully in southern African countries, and DDT has been
used successfully for IRS in Mozambique, South Africa, and
in parts of Swaziland, Eritrea, Ethiopia, and Madagascar.21,30
Key public health organizations and international development agencies, including the WHO, the United States Agency
for International Development, and the World Bank, have
recently announced plans to support IRS activities in malaria
endemic countries.11
251
DDT FOR INDOOR RESIDUAL SPRAYING IN AFRICA
TABLE 2
Insecticides recommended by the World Health Organization for indoor residual spraying27*
Insecticide
Class
Recommended dosage of
active ingredient (g/m2)
Duration of effective
action (months)
DDT
Fenitrothion
Malathion
Pirimiphos-methyl
Propoxur
Bendiocarb
Alpha-cypermethrin
Cyfluthrin
Deltamethrin
Etofenprox
Lambda-cyhalothrin
Bifenthrin
Organochlorine
Organophosphate
Organophosphate
Organophosphate
Carbamate
Carbamate
Pyrethroid
Pyrethroid
Pyrethroid
Pyrethroid
Pyrethroid
Pyrethroid
1–2
2
2
1–2
1–2
0.1–0.4
0.02–0.03
0.02–0.05
0.02–0.025
0.1–0.3
0.02–0.03
0.025–0.05
>6
3–6
2–3
2–3
3–6
2–6
4–6
3–6
3–6
3–6
3–6
3–6
* DDT, dichlorodiphenyltrichloroethane.
TRENDS IN INSECTICIDE USE FOR
VECTOR CONTROL
Decisions made by the international community regarding
the public health use of insecticides are reflected in insecticide
use data. Organochlorines, largely DDT, and carbamates are
used exclusively for IRS. Synthetic pyrethroids (also used for
IRS in the Americas) are the only approved class of insecticides for impregnation of ITNs, and larvicides used in environmental management projects are generally organophosphates. During 1995–2005, the use of DDT and organophosphates for malaria vector control declined steadily
(Figure 1), as reported to WHO Pesticides Evaluation
Scheme (WHOPES).31–33 However, the insecticide use data
from South Africa are included only from 2003–2005, and the
data from India, where IRS has been the mainstay of vector
control for more than 5 decades, were only reported through
2000.
Table 3 gives the recent use of DDT for vector control, as
reported to WHOPES during 2000–2005. Use of DDT increased substantially among the African nations during this
period. In the Americas, among the 3 nations that reported
DDT spraying for disease vector control, DDT use appears to
have decreased almost to zero after 2000. This period coin-
FIGURE 1. Quantities of commonly used insecticides for malaria
vector control.31–33 DDT ⳱ dichlorodiphenyltrichloroethane; OP ⳱
organophosphate (chlorpyrifos, chlorpyrifos-methyl, fenthion, fenitrothion, malathion, pirimiphos-methyl, temephos); C ⳱ carbamate
(bendiocarb, propoxur); PY ⳱ pyrethroid (alpha-cypermethrin, befenthrin, cyfluthrin, cypermethrin, deltamethrin, etofenprox, lambdacyhalothrin, permethrin, mixture). This figure appears in color at
www.ajtmh.org.
cides with Mexico’s decision to discontinue using DDT for
malaria vector control, replacing it with synthetic pyrethroids;
this followed the signing of the North American Agreement
on Environmental Cooperation, a side accord to the North
American Free Trade Agreement. In 1997, Mexico committed to phasing out DDT use and production over 10 years but
achieved elimination rapidly in 2000.34 Other Latin American
countries were forced to stop using DDT for disease vector
control because of this trade agreement and limited availability of the insecticide.23,25 Lastly, data regarding the use of
DDT in Southeast Asia are limited. Given that India did not
report to WHOPES after the year 2000 and that no data were
available from China, the total use in this region is likely to be
significant.
SAFETY
Because it is highly persistent and lipid soluble, DDT bioaccumulates through the food chain. The half-life of dichlorodiphenyldichloroethylene (DDE), a primary metabolite of
DDT, is about 11 years.35 For these reasons, intensive agricultural use of DDT from the 1940s to the 1970s led to adverse environmental effects, including acute toxicity to
birds.36 Several reproductive effects have been demonstrated
in birds, in particular thinning of egg shells in several species.37 An association between exposure to DDT and a number of health outcomes in humans has also been proposed. It
has been suggested that because of its weak estrogenic activity, DDT exposure is linked to breast cancer; there is no
strong evidence to support this association.38 Nor is there any
indication that DDT has adverse effects on reproductive
health.39 Because of its persistent nature in human adipose
tissue and recorded levels in breast milk, neurodevelopmental
effects are an important concern. One report indicated that
prenatal exposure to DDT was associated with neurodevelopmental delays.40 Earlier studies investigating the effect of
long-term exposure to DDT found no significant excess morbidity among spraymen who worked in eradication programs
in India and Brazil for 5 or more years when compared with
matched control groups.41 More recent studies have also
shown that persons occupationally exposed to DDT have
higher blood levels of DDT and its metabolites, but no ill
effects have been confirmed.42,43 On the contrary, an earlier
study showed that maternal and child health mortality outcomes improved steadily in the coastal areas of Guyana
252
SADASIVAIAH AND OTHERS
TABLE 3
Recent use of DDT for vector control (kg per year)32,33*
Country
2000
2001
2002
2003
2004
2005
Eritrea
Ethiopia
Madagascar
Mauritius
Mozambique
Namibia
South Africa
Swaziland
Zambia
Zimbabwe
Ecuador
Guyana
Venezuela
Bangladesh
India
Myanmar
Thailand
TOTALS
3,034
267,313
18,971
1,187
NR
NR
NR
NR
NR
NR
1,659
NR
476
29,933
2,131,049
8,587
22,044
2,484,253
6,272
273,935
0
1,262
NR
NR
NR
NR
NR
NR
NR
40
0
NR
NR
6,670
3,622
291,801
6,375
298,875
45,113
NR
NR
NR
NR
NR
NR
NR
NR
0
0
NR
NR
578
0
350,941
NR
272,243
45,000
872
NR
52,143
53,610
NR
NR
NR
NR
NR
NR
NR
NR
NR
NR
423,868
6,552
255,163
30,000
899
NR
25,837
62,112
NR
8,648
NR
NR
NR
NR
NR
NR
NR
NR
389,211
10,109
275,195
0
625
307,688
39,611
65,575
7,538
13,308
108,000
NR
NR
NR
NR
NR
NR
NR
827,649
* DDT, dichlorodiphenyltrichloroethane; NR, not reported.
where IRS activities were sustained over 3 decades until the
disease was eliminated.44 The possible adverse consequences
of human exposure to DDT cannot be ignored, even with
limited evidence, and merit further study. The risks to public
health by deployment of DDT or other insecticides must be
carefully weighed against the benefits, in this case the prevention of malaria.
The health and environmental effects of DDT when used
exclusively for IRS are not known. The tendency is to compare DDT use in the 1950s and 1960s with that for IRS today.
During the eradication period, DDT was the main tool for
combating malaria. Approximately 40,000 tons of DDT were
used annually during the malaria eradication period of 1955–
1970, corresponding to only 15% of the global DDT production.45 The rest of the consumption was for agricultural pest
control and domestic purposes. After the malaria eradication
period, DDT use for public health purposes was about 30,000
tons per year during 1978–1982, and no major adverse health
effects were reported in exposed populations.46 Nonetheless,
possible soil and water contamination, effects on wildlife and
the environment, and illicit use of DDT, particularly in agriculture, are real concerns. In India, DDT is known to be
diverted for non-public health use and was banned as an agricultural pesticide in 1996.47 Since then no regulation has
been put in place to ensure that DDT is used exclusively for
disease vector control.48 Residues of DDT and its metabolites
in human blood and the environment are detected even in
areas where IRS is not implemented, suggesting diversion of
DDT to agriculture.25 In contrast, a recent IRS program with
DDT and pyrethroids in two mining towns in Zambia was
conducted under the auspices of the Zambian Environmental
Council in partnership with a private mining company.49 The
challenge is to achieve such intersectoral and interagency cooperation at the national and regional levels to monitor the
environmental impact of DDT when used exclusively for IRS.
INSECTICIDE RESISTANCE: MONITORING
AND MANAGEMENT
The recent WHO position statement on IRS notes that the
choice of insecticide must be informed by the following: (1)
vector susceptibility to insecticides; (2) vector ecology and
behavior; (3) toxicity and safety for humans and the environment, including contamination of agricultural goods; (4) efficacy and cost effectiveness compared with alternative insecticides; and (5) community acceptance.26 Although toxicity
and safety concerns have made the use of DDT a contentious
issue at the international level, the remaining factors (plus the
burden of malaria) weigh heavily in the context of a national
program.
Resistance to the insecticides used is a major operational
concern in vector control efforts. Because monitoring efforts
have been limited, the current spectrum of the insecticide
resistance problem is not known in malaria endemic regions,
particularly in Africa.50 Resistance to DDT was widespread
in the early 1970s because of its intensive use in public health
and agriculture12 and emerged after about 11 years of application.15 Although DDT has been used in limited quantities
for disease vector control during the past 3 decades, there
have been recent reports of resistance in malaria vectors from
African countries.51–54 Pyrethroids and, to a lesser extent,
organophosphates and carbamates are increasingly used for
malaria vector control in endemic countries.12 Resistance
monitoring, however, has concentrated mostly on pyrethroids
because of the emphasis placed on ITNs for malaria prevention.50 Today, pyrethroid resistance is a major concern in west
African countries and is a growing problem in eastern and
southern African countries.55–59 The intensive use of pyrethroids for agricultural pest control is linked to the high levels
of resistance observed in west African countries.60
Research has shown 2 major mechanisms of resistance in
mosquitoes: (1) increased metabolism of insecticides reducing
the effective dose of insecticide available at the target site;
and (2) reduced target site sensitivity leading to ineffective
binding of a given dose of insecticide, also known as knockdown resistance (kdr).61 Each mechanism is complex; a diverse range of genes and enzyme families are involved in
resistance development. Hence, malaria vectors may have
multiple resistance mechanisms, which are field selected under insecticide selection pressure, and may be resistant to one
or more classes of insecticides.61 For instance, kdr resistance,
DDT FOR INDOOR RESIDUAL SPRAYING IN AFRICA
which results from single point mutations in the genes that
encode the voltage-gated sodium channel, is a common target
site resistance mechanism in African malaria vectors that confers broad-spectrum resistance to pyrethroids and crossresistance to DDT.61 Therefore, monitoring of kdr resistance
is particularly important if ITNs and IRS with DDT are deployed simultaneously. On the other hand, resistance to pyrethroids can develop through a less tractable mechanism of
metabolic resistance, which results from alterations in the levels or activities of insecticide-detoxifying enzymes.12 Although the absence of kdr resistance in a pyrethroid-resistant
malaria vector may preserve susceptibility to DDT, the
presence of metabolic resistance may confer cross-resistance
to another class of insecticides, as recently reported for pyrethroid-resistant A. funestus with cross-resistance to the carbamate propoxur in South Africa and Mozambique.52,62 Intensive use of insecticides may also induce behavioral changes
in malaria vectors, such as shifts in biting times and reduced
resting periods, compromising vector control efforts.61
The impact of detected resistance on the efficacy of insecticide-based vector control interventions highlights its operational significance. Several experimental hut trials in West
Africa reported that ITNs reduced biting rates and caused
mortality in local populations of A. gambiae in pyrethroid
resistance areas.63–65 A field study from India revealed
marked reductions in vector densities and malaria cases although the target malaria vector A. culicipacies was found to
be resistant to DDT.28 On the other hand, pyrethroid resistance in A. gambiae interfered with the efficacy of IRS and
led to a switch back to DDT in South Africa.56 The results of
a study from Benin showed that ITNs and IRS with pyrethroids failed to control an A. gambiae population with a high
level of kdr resistance genes.66 The results of this study stood
in contrast with the results of several studies from Cote
d’Ivoire that reported a continued efficacy of ITNs in areas
with a comparable kdr resistance.63–65 Further molecular
studies failed to explain the basis for differing contribution of
kdr to pyrethroid resistance in A. gambiae.66
Baseline assessment and routine monitoring of insecticide
resistance in malaria vectors are crucial to inform vector control strategies. To protect the effectiveness of insecticides in
use, it is important to detect the emergence of resistance at an
early stage and monitor the impact on practical control and
spread of resistance across the geographical range of malaria
vectors through field studies with experimental huts. This
monitoring and surveillance system is important for systematic data collection on vector species, vector behavior and
ecology, and transmission patterns (i.e., entomological inoculation rates), which is currently not a routine practice in most
endemic countries. This system can also serve as a platform to
improve our understanding of the development of different
resistance mechanisms and the potential for cross-resistance
among insecticides—knowledge that is important in designing
resistance management strategies.11 The rotation of insecticides is one of the proposed strategies that is currently under
evaluation.67 However, an earlier modeling study showed that
pre-planned rotation of insecticides did not provide any significant advantage over switching insecticides when resistance
build-up was at an intolerable level.68 For effective action,
susceptibility levels of primary malaria vectors to the various
classes of insecticides should be closely monitored using standard bioassays. Much more important is the effect of resis-
253
tance on malaria transmission as it relates to the effectiveness
of interventions, as has been the case for pyrethroids and
ITNs.59,63,69
Such a program of insecticide resistance monitoring and
surveillance will require training of a large number of competent program managers and technicians in classic and molecular entomology—a huge gap throughout tropical Africa
as reported by the African Network on Vector Resistance
(Figure 2)70—and the establishment of a network of entomological surveillance sites with trained field staff. Underlying
this challenge is the broader and urgent need to strengthen
the managerial and operational capacity of national malaria
control programs with human, technical, and financial resources.
COSTS AND COST EFFECTIVENESS
In African countries and elsewhere where malaria is endemic, IRS is a highly cost-effective intervention (US $9–24
per disability-adjusted life year [DALY] averted).71 A recent
study from Mozambique compared 2 operationally similar
IRS programs implemented in a rural and a peri-urban area;
the cost per person covered using carbamates was US $3.48
and US $2.16, respectively, and using alternative insecticides
ranged between US $1.50–US $4.16 and US $0.74–US $2.70,
respectively.72 The study reported that DDT had the lowest
cost per person covered, followed by Icon威 (lambdacyhalothrin), Ficam威 (bendiocarb), and propoxur.72
Table 4 presents the estimated costs of spraying DDT and
other approved insecticides using the high end of the dosage
range recommended by the WHO in consideration of application on mud surfaces. The estimations considered the duration of residual effect on mud surfaces for a period of 6
months, assuming an average of 200 m2 sprayable surface per
house. Water dispensable powders are used because of their
low cost and longer residual activity on porous surfaces. The
costs of insecticides (US $ per kg active ingredient) are based
on the reports of 80 manufacturers in 20 different countries
and do not include freight, import duties and taxes, and other
external costs.73 Therefore, the reported costs of insecticides
do not necessarily reflect the costs that may be incurred by
the ministries of health in endemic countries. Such operational costs such as labor and transport are also not included
in these estimations. These operational costs are highly variable across and within countries depending on the characteristics of the areas targeted for IRS, the insecticide of choice,
and the spraying activity.74
The cost comparison results show that DDT is the least
expensive insecticide; it costs $1.60 per house for 6 months at
2 g/m2 and requires only 1 spraying round for that period. It
is important to note that DDT has been successfully used in
India at a target dose of 1 g/m2 in areas where the major
vector has shown resistance to this insecticide.28 With a
marked reduction in the cost of deltamethrin from US $2074
to $473 per kg active ingredient in the recent past, the cost of
this insecticide compares well with that of DDT, but deltamethrin requires 2 or more spraying rounds depending on the
duration of the malaria transmission season, adding proportionately to the operational costs of IRS. The two insecticides
are followed by malathion and lambda-cyhalothrin, which
cost about 5 times more than DDT and require 3 and 2
254
SADASIVAIAH AND OTHERS
FIGURE 2. Vector surveillance capacities in national malaria control programs (NMCP) and research institutions in 38 African countries.
Product of the African Network on Vector Resistance: ANVR Newsletter Issue No 1, 2006.
spraying rounds, respectively, to achieve 6 months of residual
activity. Bendiocarb and fenitrothion cost about 9 times
more per house sprayed, and propoxur is the most expensive
insecticide to provide 6 months of control.
In setting priorities for malaria control, a rule of thumb is to
compare the cost effectiveness of IRS using DDT with that of
using alternative insecticides and with that of other vector
control interventions. Table 5 describes the advantages and
disadvantages of key vector control interventions, including
IRS, ITNs, and environmental management.75–78 Figure 3
shows the cost-effectiveness ratios of IRS (using DDT and
lambda-cyhalothrin and considering 1 and 2 spraying rounds
per year) and ITNs (considering nets with insecticide and
insecticide only).79
A review of recent IRS and ITN projects concluded that
the two interventions had comparable effectiveness, but the
outcomes were not as impressive when compared with those
of well-documented spraying projects of the 1950s–1970s.19
Increasing pyrethroid resistance may change these conclusions. Intervention effectiveness is locality specific; it is primarily a function of the extent of detected vector resistance
interfering with practical control and the coverage rate
TABLE 4
Cost comparison of the WHO recommended insecticides for IRS, excluding operational costs and freight and other external costs*
Insecticide
Dosage
(g/m2)
Approximate
duration of
residual effect on
mud surfaces
(months)
Number of
spraying rounds
per 6 months
Total dosage
per 6 months
(g/m2)
DDT
Deltamethrin
Malathion
Lambda-cyhalothrin
Bendiocarb
Fenitrothion
Propoxur
2
0.025
2
0.03
0.4
2
2
6
3
2
3
2
3
3
1
2
3
2
3
2
2
2
0.05
6
0.06
1.2
4
4
* DDT, dichlorodiphenyltrichloroethane; WP, water-dispensable powder.
Formulation
Approximate
amount of
formulated product
required per house
per 6 months
(kg)
Approximate cost of
formulated product73
(US$ per kg)
Cost
per house
per 6 months
(US$)
Cost ratio
(DDT⳱1)
75% WP
2.5% WP
50% WP
10% WP
80% WP
40% WP
80% WP
0.5
0.4
2.4
0.1
0.3
2.0
1.0
3.0
4.0
3.4
72.0
46.0
7.4
18.8
1.6
1.6
8.2
8.6
13.8
14.8
18.8
1.0
1.0
5.1
5.4
8.6
9.3
11.8
255
DDT FOR INDOOR RESIDUAL SPRAYING IN AFRICA
TABLE 5
Advantages and disadvantages of key malaria vector control strategies15,65,75–78*
Indoor residual spraying
Advantages
• Mosquitoes killed and repelled
• Community-wide protective effect
• Once sprayed, no additional
commitment from community
• Residual activity: 3–12 months,
depending on the insecticide
• Proven effectiveness in a variety of
epidemiological settings
• No documented serious adverse
effects on human health and the
environment
Insecticide-treated nets
Environmental management†
Advantages
Advantages
• Mosquitoes killed and repelled
• Community-wide protective effect, if
coverage rate is high, extended to
neighboring communities15
• Rebound effect not observed75
• Individual and community decisions
to use
• Effectively treated nets with sizeable
holes remain effective76
• Proven effectiveness in a variety of
epidemiological settings
• No documented serious adverse
effects on human health and the
environment
Disadvantages
Disadvantages
• Insecticide resistance monitoring and
management
• Ineffective against exophilic malaria
vectors
• Difficult to implement and maintain
because of operational complexity
(e.g., transportation into remote
communities are difficult, labor
intensive) and resource requirements
• Programs require technical capacity
for implementation and vector
surveillance
• Acceptability among community
members
• Required removal of all belongings,
except large pieces of furniture, from
the home
• Health and safety of sprayers and
communities
• Ineffective against exophagic malaria
vectors
• Decreased susceptibility and
increasing resistance to pyrethroids,
but nets may still be a practical means
of personal protection65
• Periodic net retreatment is required
(as long-lasting nets become available,
retreatment will cease to be a
problem)
• Distribution and sustainability
problems, particularly in impoverished
areas when nets are not distributed
free of charge
• Low coverage rates, particularly in
high-risk groups such as children and
pregnant women, when nets are not
distributed free of charge
• Difficult to promote in areas of
unstable transmission
• Individual attitudes and practices
(e.g., ineffective for persons sleeping
outside)
• Prevent mosquito maturation by
eliminating breeding sites
• Community-wide protective effect
• Useful in peri-urban and urban areas
where transmission is focal77
• Useful in economic development sites
where nonimmune populations may
be concentrated
• Sustainable reductions in
transmission, morbidity, and mortality
observed when integrated with other
interventions78
Disadvantages
• Difficult to implement and maintain
because of operational complexity
(e.g., periodic maintenance, labor
intensive)
• Programs require technical capacity
for implementation and vector
surveillance
• High initial costs
• Intersectoral action is required
• Impact difficult to quantify when
integrated wth other interventions
• Some undesirable environmental
impact if activities target wetlands
* ITNs, insecticide-treated nets; IRS, indoor residual spraying.
† Environmental management encompasses draining and filling of breeding habitats, clearance of vegetation, and eliminating pools of stagnant water.
achieved in the target community. Indeed, experience in the
Solomon Islands showed that ITNs permitted a reduction in
DDT spraying, but could not replace it without an increase in
malaria incidence.80 It is also important to sustain interventions to realize their full potential. For these reasons and
others, the studies comparing the cost effectiveness of IRS
and ITNs have produced inconclusive results. In addition, it is
unclear whether a combination of ITNs and IRS would be
cost effective.
Few cost-effectiveness analyses of environmental management programs have been performed. One study of an integrated malaria control program in Zambia centering on environmental management showed that the initial costs per
DALY averted were high because of setup costs, but the costs
per DALY averted decreased substantially in the long term.81
A central question in the debate on the role of DDT in IRS
is its cost compared with that of alternative insecticides. It is
important that the cost advantage of using DDT is well established when compared with alternatives. A number of recent studies have indicated that DDT is the least costly insecticide72,74 and that spraying programs with DDT are
slightly cheaper than programs with other insecticides.72,82
Absolute prices of insecticides for public health purposes are,
however, difficult to assess because they do not reflect the
true cost to a given country, including procurement, transportation, handling and disposal, freight, and other external
costs.73,74
Costs related to the availability and production of DDT is
currently restricted to only a few manufacturers (i.e., in India,
Ethiopia, and China24). Presumably, WHO and other organizations will work toward making DDT and other insecticides available for IRS promptly, at low cost, and in a sustainable manner.
RECENT PROGRAMS FOR INDOOR RESIDUAL
SPRAYING IN AFRICA
A highly effective intervention in epidemic-prone areas,
IRS is now promoted for transmission control in stable endemic areas if implemented in a sustainable manner.26 In such
settings, a persisting level of partial immunity exists in the
256
SADASIVAIAH AND OTHERS
FIGURE 3. Cost effectiveness of malaria vector control interventions.79 The vertical bars indicate the ranges favored in the analyses.
DALY ⳱ disability-adjusted life year; IRS ⳱ indoor residual spraying; DDT ⳱ dichlorodiphenyltrichloroethane.
population and provides relative protection that does not exist in epidemic-prone areas. Epidemics can occur when endemicity is low and a susceptible population is exposed to a
sudden increase in transmission. When such an outbreak occurs, malaria incidence and case fatality rates are high among
all age groups.83 According to WHO, IRS can be effective in
most epidemiologic settings, as follows26:
• In areas with unstable malaria transmission, IRS will prevent seasonal increases in transmission, will prevent and
control epidemics, and can eliminate local transmission of
malaria.
• In areas with stable endemic malaria with moderately intense but seasonal transmission, IRS will prevent seasonal
increases in transmission and reduce malaria prevalence
and seasonal increases in morbidity and mortality.
• In areas with stable-hyperendemic malaria where transmission is intensely seasonal or perennial and without much
seasonal flux, IRS will reduce malaria prevalence, incidence, morbidity, and mortality when applied more frequently than in the above instances.
Many malaria endemic countries have areas with the 2 or 3
levels of endemicity noted above and are loath to deny any
population the benefits of effective malaria control. In areas
where epidemics last only for a few months and do not return
for years, promotion and provision of ITNs prove difficult,
and the “fire brigade” approach with trained and equipped
IRS spraymen seems to be the best precaution. Table 6 lists
selected African countries that have successfully used DDT
for IRS.21,52,84–92 In Madagascar, 7% of the population is at
risk of epidemic malaria,93 especially in the central highlands.
Disease had been controlled in this region during the 1950s
through IRS with DDT, and the main malaria vector Anopheles funestus was nearly eradicated.84 However, the program’s
emphasis on spraying decreased over time, An. funestus reappeared in large numbers, and a severe epidemic resulting in
thousands of deaths occurred during 1985–1990 after a heavy
rainfall.84–86 When DDT was reintroduced through a multiintervention program, Opération de Pulvérisation IntraDomiciliaire, by the government of Madagascar, the incidence of malaria was reduced greatly, albeit late.87
A recent study assessed the impact of the Global Malaria
Programe’s (formerly Roll Back Malaria) 5-year program in
Eritrea, where 67% of the population lives in endemic areas.88 The study showed that the number of ITNs and the
amount of insecticide used for IRS were both significantly
correlated with a reduction in malaria morbidity.88
Malaria had been controlled using IRS with DDT in KwaZulu Natal, an epidemic-prone province in South Africa,
from 1946–1995. During the malaria transmission season of
1991–1992, there were only 600 reported cases of malaria.89
However, because of growing environmental concerns and
the presence of DDT in breast milk, South Africa substituted
synthetic pyrethroids for DDT in 1996.21 An. funestus quickly
reemerged (probably after entering from Mozambique) and
were found to be resistant to pyrethroids without crossresistance to DDT. From 1999–2000, 40,700 cases of malaria
were reported.56,89 After DDT was reintroduced, the number
of reported cases diminished rapidly, with 17,500 reported
cases in 2001 and 3,500 reported cases in 2002.89,90
Table 6 shows that in these 3 countries, IRS with DDT was
not an isolated strategy. Treatment with antimalarial drugs,
including artemisinin-based combination therapies (ACTs),
and prevention were key components of the malaria control
strategy in Madagascar, Eritrea, and South Africa. A comprehensive strategy must include multiple interventions and
disease and vector surveillance, all of which require epidemiologic and entomological capacity within the national programs. Treatment of infected individuals may help to reduce
transmission as ACTs have gametocytocidal properties. Evidence also suggests that successful vector control may help
reduce drug resistance.94
Successful IRS programs with DDT were previously implemented in Botswana, Namibia, Zimbabwe, and Mozambique.21 These countries are currently members of the southern African coalition of malaria endemic countries that embarked on a regional control program in the late 1990s.
Uganda, unlike the central highlands of Madagascar or the
Kwa-Zulu Natal province of South Africa, is characterized by
predominantly stable malaria transmission.95 This is one of
the many countries considering deployment of DDT for IRS,
and the situation illustrates the dilemmas faced by many
countries. Proponents claim that given the financial resources
required for spraying programs with deltamethrin, more
households could be protected by using DDT.96 Opponents
question the environmental and health impact of DDT. In
addition, Ugandan and other government officials are rightfully concerned that if DDT is reintroduced, trade relations
with the European Union (EU) may be endangered. In 2005,
the EU warned Uganda that if DDT were used for malaria
control, stringent measures would have to be taken to ensure
that foodstuffs were not contaminated.97 Even with precautions, a negative perception of Ugandan agricultural products
may have profound economic consequences. Before implementing an IRS program with DDT in these countries, potential barriers to trade must be thoroughly addressed.
IMPLEMENTATION, MONITORING,
AND EVALUATION
Recommendations for IRS with DDT must be evidencebased and consider epidemiologic and entomological, operational, and economic factors (Table 7). The effectiveness of
IRS has been demonstrated in both unstable, epidemic-prone
257
DDT FOR INDOOR RESIDUAL SPRAYING IN AFRICA
TABLE 6
Successful experiences with indoor residual spraying with DDT for malaria control in Africa21,56,84–92*
Place
Context
Date
Control measures
Results
• History of epidemic malaria
in the highlands since the
1800s
• Weakening malaria control
efforts
1949–1960
• IRS with DDT and chloroquine
treatment of infected individuals86
Post-1960
• Spraying with DDT limited to 3
foci; closure of treatment centers86
• Launching of malaria control program, Opération de
Pulvérisation Intra-Domiciliaire (OPID), financed by
the World Bank
1993–1997
• IRS with DDT in highland communities at 1,000–1,500 m in elevation covering 2.3 million inhabitants91
• 1996: Establishment of malaria
surveillance system to record malaria cases at the 536 health centers in the region87
Eritrea
• Implementation of a 5-year
malaria control program
2000–2004
South Africa:
KwaZuluNatal
• Long history of malaria
control with IRS
1946–1996
•
•
•
•
•
•
•
• 1954: disappearance of Anopheles funestus; eradication nearly achieved in
196084
• 1980: 3-fold increase in the number of
malaria cases86
• Reappearance of An. funestus in mid1970s84
• Severe epidemic (1985–1990) with
40,000 deaths85
• 28% decrease in the incidence of malaria in sprayed areas only, with no
change in incidence in unsprayed areas87
• 0.8% and 4.5% prevalence of malaria
parasites in schoolchildren in sprayed
and unsprayed areas, respectively, at
1,000–1,500 m85
• Prevalence of Plasmodium positive
schoolchildren was 23.8% and 0.4%
before and after OPID, respectively,
at 1,000–1,500 m91
• Significant negative correlation between the number of ITNs distributed
and the amount of DDT/malathion
used for IRS with malaria morbidity
• No additional benefit from IRS when
added to ITN vector control88
• 600 reported cases of malaria in the
province in 1991–199289
• Concerns about the environmental effects of DDT
and about DDT found in
breast milk
• Identification of pyrethroidresistant An. funestus
1996–1999
Madagascar
Highlands
2000
ITNs
IRS with DDT
IRS with malathion
Improved patient management
Antimalarial drugs
Environment controls
IRS with DDT began in 1946 with
complete coverage of malarial regions by 195821
• 1996: Synthetic pyrethroids were
substituted for DDT21
• Reintroduction of DDT21
• 2001: Artemether-lumefantrine
became first-line therapy for uncomplicated malaria92
• 1998–1999: reinvasion of An. funestus
and doubling of malaria cases56
• 2000: 40,700 reported cases of malaria79
• About 90% reduction of malaria
cases after reintroduction (2000–2004)
compared with before (1996–1999)90
• 2001: 17,500 reported cases; 2002:
3,500 reported cases89
* DDT, dichlorodiphenyltrichloroethane; IRS, indoor residual spraying; ITNs, insecticide-treated nets.
areas and stable, endemic areas of southern Africa.21,30,49 In
areas of high and moderate transmission, ITNs provide another means of malaria control, and decisions about which of
the 2 interventions is preferable will depend on operational
feasibility and resource availability.98,99 Most importantly, the
two interventions are not mutually exclusive and their implementation depends upon local conditions, population acceptability, costs, sustainability, technical expertise, monitoring
and evaluation, and national policies.
Operational issues pose a significant barrier to successful
implementation and were major impediments to the success
of national eradication programs in the 1950s and 1960s.
These operational issues involve access to an adequate supply
and distribution of quality DDT (when stocks being exported
or donated and when old stocks being used), capacity to effectively plan and manage IRS programs, and ability to assess
the potential impact of a spraying program through monitoring of effective forms of resistance, malaria disease surveillance, and evaluation of any adverse effects of DDT to human
health and the environment. Countries should specify how
they intend to provide supervision on decentralized activities
and train sprayers and raise awareness among spraying per-
sonnel and targeted communities on issues relating to DDT
use. The acute toxicity of DDT to human’s is low and is not
a major concern. The stigma associated with IRS may be
difficult to overcome in general and communities may not
tolerate the often visible residues left by the insecticide on the
wall. It is critical that countries have a plan for storage and
disposal of insecticides and are committed to preventing the
diversion of DDT into agriculture. Lastly, the ability to detect
the emergence and spread of vector resistance to DDT of a
kind that has practical impact on intervention effectiveness
and the susceptibility levels to alternative insecticides are key
in effective management of insecticide resistance and sustainability of IRS activities.
Monitoring and evaluation are crucial to assess the success
of any malaria control program. Monitoring serves to measure outcomes and to assess the effectiveness of interventions.
Several approaches for data collection on malaria outcomes
should be considered. Data from national health information
systems, collected from health facilities, can provide information on cases of severe malaria and case fatality rates. However, such data represent only those facilities that regularly
report cases and measure morbidity and mortality only in
258
SADASIVAIAH AND OTHERS
TABLE 7
Requirements for indoor residual spraying with DDT*
Category
Considerations
Epidemiological and
entomological factors
• Epidemic, seasonal, or year-round
malaria transmission
• Vector that is endophilic
• No demonstrated insecticide resistance of operational importance
• Availability of low cost and quality
supply, including other critical commodities (when stocks are being exported or donated and when old
stocks are being used)
• Ability to train sprayers and supervise
and manage decentralized activities
according to spraying cycles
• Safe handling, transport, storage, and
disposal of insecticides
• Community acceptability and cooperation
• Type of housing and sprayable surfaces and appropriate insecticide formulation
• Monitoring of susceptibility and resistance in vectors and assessment of the
impact of any detected resistance on
intervention effectiveness
• Insecticide resistance management by
timely switches to alternates
• Measures to prevent diversion to agriculture and domestic use
• Measures to prevent environmental
contamination
• Malaria disease surveillance to assess
intervention effectiveness
• Monitoring of adverse health and environmental effects
• IRS/DDT is cost effective (including
the costs of project management,
monitoring and evaluation, and disease surveillance)
• IRS/DDT does not negatively affect
trade relations
Operational factors
Economic concerns
* DDT, dichlorodiphenyltrichloroethane; IRS, indoor residual spraying.
those who access health services.100 Thus, local community
and household surveys, such as Demographic and Health Surveys (http://www.measuredhs.com/) and the Malaria Indicator Survey (https://www.rbm.org.int/merg), can supply information not provided by health information systems. These
surveys are useful for collecting data on all-cause under-5
mortality, use of interventions such as ITNs, and use of antimalarial therapies.6
In addition to disease monitoring, efforts must be made to
assess human and environmental exposure. Levels of DDT
are used as markers of exposure and have been measured in
blood, breast milk, dust, soil, water, sediment, and fish. Methods for extraction and identification of DDT from these media with gas chromatography-mass spectroscopy have been
developed.101,102 Studies of human exposure have assessed
DDT levels in blood and breast milk. In Mexico, studies have
shown that blood levels of DDT and DDE in women living in
areas that were heavily sprayed are higher than in areas
where less DDT had been used.43 In all study areas, sprayers
had the highest levels of exposure.43 A reduction in blood
levels of DDT and DDE in the exposed population was noted
over 2 years after the cessation of spraying programs.43 Breast
milk containing DDT has been identified in women throughout the world, including Swaziland and South Africa.103,104
Continued monitoring of DDT levels in breast milk is important to ensure that the acceptable daily intake for infants is
not exceeded and to assess its clinical importance.
Studies of environmental exposure are also important for
assessing the potential impact of DDT on ecosystems. Concentrations of DDT and its metabolites in indoor and outdoor
soils were significantly higher in areas more highly exposed to
DDT than in less exposed areas in Mexico.105 In China, DDT
has been identified in soil, sediment, and wildlife; concentrations in birds were greater than those in fish, suggesting bioaccumulation of DDT.106 Similar studies assessing contamination of environmental media have been conducted in Brazil107,108 and in KwaZulu-Natal, South Africa, where DDT
was identified in the water, particularly attached to sediment
particles.109 Analyses of DDT in humans and the environment should include measurements of DDT and its 2 main
metabolites, DDE and dichlorodiphenyldichloroethane
(DDD). Before the implementation of spraying programs,
baseline assessments should be conducted so as to establish
any impact of IRS with DDT on human health and the environment.
Article 11 of the Stockholm Convention calls for “research,
development, monitoring and cooperation pertaining to persistent organic pollutants (POPs),” including their “presence,
levels, and trends in humans and the environment” as well as
“effects on human health and the environment.”24 However,
for many developing nations, this will require an overall
strengthening of their scientific and technical capacity. To
establish research and monitoring for the health and environmental effects of DDT, as described in the studies above, it
will require training on laboratory protocols and safety, procurement of necessary equipment, and establishment of databases. The UNEP has already established a Global POPs
Monitoring Program to evaluate the effectiveness of the
Stockholm Convention. With the recent endorsement of IRS
with DDT by the WHO, the work of the Monitoring Program
and of existing laboratories with the capacity to monitor
POPs will become important in training and capacity building
in developing countries.
RESEARCH NEEDS
The use of IRS with DDT has proven effective in controlling malaria transmission in areas where malaria vectors were
susceptible or showed some degree of resistance as indicated
with high frequency of resistance genes and where governments could properly manage such programs with high spray
coverage and proper supervision.28 Several important research questions remain concerning the safety and efficacy of
IRS with DDT. Adverse health effects of DDT when used
exclusively for IRS have not so far been demonstrated. Prospective cohort studies linking exposure data (as described
above) to health outcomes should be conducted. Efforts
should also be made to accurately record the amounts of
DDT used for IRS. Such data will help to correlate DDT
exposure with health and environmental outcomes. Research
should focus on the effects of exposure on children in areas
where DDT is being used and on the development of new
methods for improved monitoring of DDT in various environmental settings.
DDT FOR INDOOR RESIDUAL SPRAYING IN AFRICA
The development and spread of insecticide resistance
are dependent on the volume and frequency of application
of insecticides and the inherent characteristics of the malaria vectors against which they are used.11 All WHOrecommended insecticides for IRS, with the exception of
DDT, are widely used in agriculture today. A detailed understanding is needed of the role of agricultural as well as domestic use of insecticides in the development of resistance.
Knowledge of the genetic structure and dispersal patterns of
malaria vectors is important for predicting the spatial and
temporal spread of resistance through gene flow between vector populations.61 Yet only field studies of mosquito populations can facilitate timely operational responses and a better
understanding of the impact of different resistance mechanisms on the effectiveness of IRS. Further research on the
molecular basis of insecticide resistance is needed for the development of new and safe insecticides.110 The question of
who will finance and develop such insecticides warrants further discussion.
The cost effectiveness of various vector control methods is
important to policy makers when trying to decide how to
allocate resources among competing interventions. In areas
with high and moderate transmission, ITNs have proved
equally effective111 and have been promoted, whereas IRS
has been used mainly to control unstable, epidemic malaria.
The use of IRS with DDT must be studied under different
epidemiologic settings (rural versus urban, high and low endemic versus epidemic transmission) to understand where
and how it is most cost effective. Another important question
to policy makers when trying to develop a multi-component
malaria control strategy is estimating the additional benefits
of introducing IRS in an area where ITNs are widely used.
Lastly, behavioral research on local attitudes and practices
and the social acceptability of IRS is exceedingly important
before and during the time such interventions are deployed
on a large scale in a given area.
DISCUSSION
The low-cost insecticide DDT remains effective against malaria vectors in Africa. The possible adverse health and environmental effects of DDT exposure through IRS are not
known and pose a real concern. Less persistent insecticides
that do not bioaccumulate in adipose tissue would be preferable. However, the development of new insecticides for public health has been slow. Less than 10% of the insecticides
developed since the 1970s have been considered for malaria
vector control through IRS.112 The reality is that all insecticides used in public health are initially developed for the
agriculture market, and it is unlikely that pesticide companies
decide to invest in research and development of insecticides
exclusively for disease vector control. Pesticide companies
must be given incentives for developing new insecticides.
Public–private partnerships between drug companies and
public agencies have been successful in spurring research and
development and developing and providing new drugs to
those in developing nations at a low cost (e.g., the Malaria
Medicines for Malaria Venture and the Drugs for Neglected
Diseases Initiative). Similar partnerships may reduce the cost
of developing and registering new insecticides and may foster
an interest among pesticide companies in expanding their re-
259
search to include public health insecticides. In this respect, the
efforts of the Innovative Vector control Consortium are laudable.113 However, for this to occur, international agencies
must recognize the importance of IRS and other transmission
control interventions in integrated vector control as complementary strategies to increase the effectiveness of control efforts. The renewed position of WHO on IRS is a major step
toward this direction. Tiered pricing, which has been used to
provide vaccines and antiretroviral drugs for HIV/AIDS to
those who are in need in developing countries, may also apply
to public health insecticides. With tiered pricing, developed
nations are charged higher prices as a way to recoup losses
accrued by charging less to poorer nations. In a similar way,
pesticide companies might charge lower prices to non-profit
organizations and governments who intend to use the insecticide for malaria control while maintaining higher prices for
insecticide purchases for agricultural use.
Critics fear that DDT will once again cause widespread
environmental damage. There is also a risk of adverse effects
of DDT and its metabolites to human health. However, the
amount of DDT used in public health does not compare with
the quantities used in agriculture prior to its ban for this
purpose in developed countries. Furthermore, DDT is recommended for spraying indoors today whereas previous public
health application of the insecticide before its detrimental
environmental effects were observed in the early 1960s included aerial spraying of large areas in the United Sates and
other developed countries, primarily focusing on marshes and
swamps and adjacent water bodies.114 With proper regulation
and management of the use of DDT in the public health
sector, its illicit use in agriculture and the potential adverse
effects on human health and the environment can be minimized. Under the Stockholm Convention, the use of DDT for
disease vector control is monitored through records of which
nations are using DDT and in what quantities. These national
records may provide a useful tool for the monitoring of annual DDT production and ensure that only the amount of
DDT that is needed for malaria control is produced each year.
The WHO reports that DDT is the insecticide of choice for
malaria vector control in 10 endemic countries, and many
others are considering its deployment. According to the DDT
register established under the Stockholm Convention, China,
Ethiopia, and India are the only countries where DDT is
being produced today. Interest will increase greatly in its
availability. DDT will need to be imported. Procurement
costs and maintenance of adequate supplies will be a major
issue in endemic countries as observed for other key antimalarial commodities, such as ACTs and ITNs.
African countries have implemented effective IRS programs with DDT and other insecticides. The reconsideration
of IRS with DDT today is primarily driven by the relative
cheapness of DDT compared with alternative insecticides for
IRS. The ineffectiveness of current control strategies has
been another strong motive. There is now global support to
scaling up net coverage in vulnerable groups, particularly
through maternal and child health programs, and the expectation is that more than half a million child deaths will be
averted with the distribution of long-lasting insecticidal nets.
Each country should investigate whether IRS would be a costeffective strategy for malaria control after considering the
intervention efforts already in place, the localized dynamics
of malaria transmission in target areas, and the existing op-
260
SADASIVAIAH AND OTHERS
erational capacity. Training of program managers and technicians in entomology and proper supervision of field staff
during spraying operations, along with routine entomological
and disease surveillance, is key in effective implementation.
From an operational point of view, IRS with DDT will eventually lead to decreased sensitivity and resistance in malaria
vectors. However it should be noted that DDT resistance was
not detected in South Africa from 1946–1995. This is probably
because strict measures were taken to prevent its diversion to
agriculture where Anopheles larvae could develop resistance
if under selection pressure. To ensure sustainability in IRS
activities, the use of alternative insecticides to DDT and
methods to use them must be the focus of the research agenda
on integrated vector control.
Received March 9, 2007. Accepted for publication July 23, 2007.
Acknowledgments: We thank Mortezza Zaim of the WHO Pesticides
Evaluation Scheme, Robert Gwadz of the National Institute of Allergy and Infectious Diseases, Yeya Touré of WHO Special Programme for Research and Training in Tropical Diseases, and the
anonymous reviewers for their constructive comments on the manuscript. We acknowledge the African Network on Vector Resistance
for their assistance on vector surveillance capacity in Africa. We also
thank Kathleen Walker, University of Arizona; Juan Arredondo,
Ministry of Health, Mexico; Gezahegn Tesfaye and Afework
Hailemariam Tekle, Ministry of Health, Ethiopia; Yemi Sofola, Ministry of Health, Nigeria; John Paul Clark, United States Agency for
International Development; Ellis McKenzie and David Smith,
Fogarty International Center, National Institutes of Health; Pierre
Guillet, Global Malaria Programme, WHO; and Robert Novak and
Uriel Kitron, University of Illinois at Urbana Champaign for their
guidance and feedback. The views expressed in this article do not
necessarily reflect the views of those listed above.
Financial support: This work was supported by the Disease Control
Priorities Project, Fogarty International Center, National Institutes of
Health.
Authors’ addresses: Shobha Sadasivaiah, Weill Cornell Medical College of Cornell University, 1300 York Avenue, New York, NY,
10021-5320, Tel: 301-496-0815, Fax: 301-496-8496, E-mail:
[email protected]. Yeşim Tozan, Earth Institute, Columbia
University, B15 Hogan Hall, Mail Code 3277, 2910 Broadway, New
York, NY 10025-7822 and Disease Control Priorities Project, Fogarty
International Center, National Institutes of Health, Building 16,
Room 202, 16 Center Drive, MSC 6705, Bethesda, MD 20892-6705,
Tel: 301-496-0815, Fax: 301-496-8496, E-mail: [email protected].
Joel G. Breman, Disease Control Priorities Project, Fogarty International Center, National Institutes of Health, Building 16, Room 214,
16 Center Drive, MSC 6705, Bethesda, MD 20892-6705, Tel: 301-4960815, Fax: 301-496-8496, E-mail: [email protected].
Reprint requests: Joel G. Breman, Fogarty International Center, National Institutes of Health, Building 16, Room 214, 16 Center Drive,
MSC 6705, Bethesda, MD 20892-6705, Tel: 301-496-0815, Fax: 301496-8496, E-mail: [email protected].
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