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Series

Malaria Elimination 1
Shrinking the malaria map: progress and prospects
Richard G A Feachem, Allison A Phillips, Jimee Hwang, Chris Cotter, Benjamin Wielgosz, Brian M Greenwood, Oliver Sabot, Mario Henry Rodriguez,
Rabindra R Abeyasinghe, Tedros Adhanom Ghebreyesus, Robert W Snow
Lancet 2010; 376: 156678
Published Online
October 29, 2010
DOI:10.1016/S01406736(10)61270-6
See Comment page 1515
and 1517
See Perspectives page 1533
See Online/Comment
DOI:10.1016/S01406736(10)61494-8, and
DOI:10.1016/S01406736(10)61499-7
This is the first in a Series of four
papers about malaria elimination
The Global Health
Group, University of
California, San Fransisco,
San Francisco, CA, USA
(Prof Sir R G A Feachem DSc [Med],
A A Phillips BA, J Hwang MD,
C Cotter MPH); Centers for
Disease Control and Prevention,
Atlanta, GA, USA (J Hwang);
International Food Policy
Research Institute, Washington,
DC, USA (B Wielgosz MA);
London School of Hygiene and

In the past 150 years, roughly half of the countries in the world eliminated malaria. Nowadays, there are 99 endemic
countries67 are controlling malaria and 32 are pursuing an elimination strategy. This four-part Series presents evidence
about the technical, operational, and financial dimensions of malaria elimination. The first paper in this Series reviews
definitions of elimination and the state that precedes it: controlled low-endemic malaria. Feasibility assessments are
described as a crucial step for a country transitioning from controlled low-endemic malaria to elimination. Characteristics
of the 32 malaria-eliminating countries are presented, and contrasted with countries that pursued elimination in the
past. Challenges and risks of elimination are presented, including Plasmodium vivax, resistance in the parasite and
mosquito populations, and potential resurgence if investment and vigilance decrease. The benefits of elimination are
outlined, specifically elimination as a regional and global public good. Priorities for the next decade are described.

Introduction
A three-part strategy to eradicate malaria has been
developed14 and is now widely endorsed:510 (1) aggressive
control in highly endemic countries, to achieve low
transmission and mortality in countries that have the
highest burden of disease and death; (2) progressive
elimination of malaria from the endemic margins, to
shrink the malaria map; and (3) research into vaccines
and improved drugs, diagnostics, insecticides, and other
interventions, and into delivery methods that reach all atrisk populations.
Much eort and investment has rightly been devoted to
part one of this strategy, aggressive control in highly
endemic countries, and has resulted in a massive scale-

Key messages
A three-part strategy is now agreed to move the world to eventual malaria eradication:
aggressive control in the high-burden regions; elimination from the endemic margins
inwards; and research and development into new interventions and technologies.
99 countries have endemic malaria; of these, 67 are controlling malaria and 32 are
pursuing an elimination strategy.
The 32 malaria-eliminating countries span all geographic locations, sizes, and incomes.
Many of them have the prospect of eliminating malaria within the next decade.
Countries contemplating elimination should comprehensively assess the feasibility of
malaria elimination.
25 of the 32 malaria-eliminating countries are solely or mainly fighting a battle against
Plasmodium vivax malaria. New interventions and techniques are urgently needed to
detect and treat this infection.
Although malaria elimination has risks, the alternative of maintaining controlled
low-endemic malaria for a long period also has risks, many of them similar in nature and
magnitude.
The benefits of malaria elimination are not sufficiently understood, but include
substantial positive externalities in the form of benefits to neighbouring countries
(regional public goods) and worldwide (global public goods).
Various overarching challenges exist, including improved methods for diagnosis and
surveillance, multicountry collaboration, and ensuring long-term commitment and
resources to achieve elimination and maintain it for decades thereafter.

1566

up of eective interventions1113 and substantial reductions


in mortality and morbidity from malaria in some endemic
countries.1318 Investment and activity in part three of the
strategy, research into new interventions and delivery
methods, have increased in the past decade, and a
research agenda for malaria eradication has been
developed.6 By contrast, part two of the strategy, shrinking
the malaria map, has received less attention, which has
resulted in a deficit of evidence-based knowledge and
guidance. This four-part Series about malaria elimination
begins to fill this gap.1922

Historical summary
Eorts to control and eliminate malaria on a large scale
date back to the late 19th century, with the discovery of
the plasmodium parasite and its transmission by
anopheline mosquitoes. During the first half of the
20th century, when 178 countries had endemic malaria,
little progress was made, partly because eorts were
disrupted by World Wars 1 and 2. However, from
1945 to 2010, 79 countries eliminated malaria.23,24 Despite
exponential population growth in malaria-endemic areas
during the past 60 years, an estimated 50% of the worlds
population live in malaria-free areas, compared with only
30% in 1950.25,26
With few exceptions, elimination in the northern
hemisphere proceeded systematically from north to
south, and in the southern hemisphere, from south to
north. Thus, the concept of shrinking the malaria map
was born. Most of this progress was achieved in temperate
regions where climatic conditions are not as conducive to
endemic malaria as they are in the tropics. Notable
exceptions to this pattern include elimination on tropical
islands, such as Maldives, Mauritius, Reunion, Taiwan,
and much of the Caribbean, and in rapidly developing
small tropical countries, such as Brunei, Hong Kong,
and Singapore.14,2729
This remarkable success was propelled by the
Global Malaria Eradication Program, launched by WHO
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Series

in all parts of the world apart from Africa in 1955. The


programme relied on vector control, mainly indoor
residual spraying, and systematic detection and treatment
of cases. However, because of administrative, financial,
and technical issues, it was abandoned in 1969.30 Lessons
learned from the Global Malaria Eradication Program
have been well documented, are discussed in this Series,
and are important as the international community once
again focuses on progressive elimination and eventual
eradication of malaria.3133
After the abandonment of the Global Malaria Eradication
Program, most countries that had eliminated malaria
continued to maintain their malaria-free status. Many of
the countries remaining malarious were left with
demotivated programmes, chloroquine and DDT
resistance,34 and insucient local and international
commitment, finance, or guidance.35 Such circumstances
led to substantial increases in malaria worldwide during
the 1970s and 1980s.36 Other causes of malaria resurgence
included changes in political and economic conditions, as
seen in former Soviet republics like Tajikistan, where
malaria endemicity was re-established after the post-Soviet
economic collapse and the deterioration of the public
health system.37 These experiences provide important
lessons about the need to maintain investment and
vigilance during the latter stages of elimination eorts.5,14,21
Despite the setbacks, we have many reasons to be
optimistic. Scale-up of malaria control has resulted in
progress towards elimination in several countries since the
early part of the 21st century,38 driven by large increases in
available finance for malaria3942 and by the widespread use
of longlasting insecticide-treated bednets, artemisininbased combination therapy, and rapid diagnostic tests.

Definition of elimination
The terms elimination, eradication, and control are often
used loosely, which results in misunderstanding.43 The
word eradication has previously been used to describe
what we now call elimination,44 but is used only to mean
the permanent reduction to zero of the worldwide
incidence of infection caused by a specific agent as a
result of deliberate eorts. Interventions are no longer
needed.45 Generally, cessation of malaria transmission
in a defined geographic area, such as an island or an
entire country, is now called elimination. WHO defines
malaria elimination as: interrupting local mosquitoborne malaria transmission in a defined geographical
areaie, zero incidence of locally contracted cases,
although imported cases will continue to occur.
Continued intervention measures are required.31
The WHO definition of elimination, taken literally, is
achieved almost nowhere. Most countries that have
achieved elimination and are maintaining their WHOcertified malaria-free status, such as Italy or the USA,
have occasional, small outbreaks of secondary cases that
are contracted from primary imported cases. For example,
despite 12 outbreaks of malaria in the USA between 1993
www.thelancet.com Vol 376 November 6, 2010

and 2009, and 26 secondary cases,46 no one is suggesting


that the USA has not eliminated malaria. WHO addressed
this issue in 2006 by proposing an operational criterion
of elimination as nationwide per year fewer than three
epidemiologically linked cases of a malaria infection
without an identifiable risk factor other than local
mosquito transmission, for 3 consecutive years.27
Cohen and colleagues47 reviewed the use of the terms
control, elimination, and eradication and proposed a new
definition of elimination as a state where interventions
have interrupted endemic transmission and limited
onward transmission from imported infections below a
threshold at which risk of re-establishment is minimised.
Both capacity and commitment to sustain this state
indefinitely are required.47 This new definition recognises
that maintaining zero incidence of locally contracted
cases31 is not always an achievable target. Furthermore, as
addressed in the third paper20 in this Series, this definition
emphasises the maintenance of a highly functional
surveillance and outbreak response system that is capable
of preventing re-establishment of local transmission.
Although many stages occur between the control and the
elimination of malaria, this Series regards the alternative
to malaria elimination as a state of malaria epidemiology
that is typically achieved before launching an elimination
eort, often referred to as sustained control.1 Definition of
this state is important because a country that decides not to
eliminate is not deciding to do nothing, but is deciding to
continue investments and programmatic activities to
maintain a state of malaria control indefinitely.
WHO defines malaria control as reducing the disease
burden to a level at which it is no longer a public health
problem,31 which allows for a contextual and diseaseoriented endpoint. Cohen and colleagues47 introduced a
new term, controlled low-endemic malaria, which they
define as a state where interventions have reduced
endemic malaria transmission to such low levels that it

Tropical Medicine, London, UK


(Prof B Greenwood MD); Clinton
Health Access Initiative,
Boston, MA, USA (O Sabot BA);
National Institute of Public
Health, Cuernavaca, Mexico
(Prof M H Rodriguez PhD);
Ministry of Health, Colombo,
Sri Lanka (R R Abeyasinghe MD);
Ministry of Health,
Addis Ababa, Ethiopia
(T A Ghebreyesus PhD); Malaria
Public Health and
Epidemiology Group, Centre
for Geographic Medicine,
Kenya Medical Research
Institute, Nairobi, Kenya
(Prof R W Snow FMedSci); and
Centre for Tropical Medicine,
Nuffield Department of Clinical
Medicine, Centre for
Vaccinology and Tropical
Medicine (CCVTM), University
of Oxford, Oxford, UK
(Prof R W Snow)
Correspondence to:
Sir Richard G A Feachem,
Director, Global Health Group,
UCSF Global Health
Sciences, 50 Beale Street,
suite 1200 San Francisco,
CA 94105, USA
feachemr@globalhealth.
ucsf.edu

Panel 1: Definitions used in this Series


Elimination
A state where interventions have interrupted endemic transmission and limited onward
transmission from imported infections below a threshold at which risk of re-establishment is
minimised. Both capacity and commitment to sustain this status indefinitely are required.47
Malaria-eliminating country
A country that has formally declared a national, evidence-based elimination goal, has
assessed its feasibility, and has embarked on a malaria elimination strategy.
A country that is strongly considering an evidence-based national elimination goal, and
that has already made substantial progress in spatially progressive elimination (eg, by
eliminating malaria from specific islands, provinces, or geographic areas) and in greatly
reducing malaria nationwide.
Controlled low-endemic malaria
A state where interventions have reduced endemic malaria transmission to such low levels
that it does not constitute a major public health burden, but at which transmission would
continue to occur even in the absence of importation.47

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Series

See Online for webappendix

1568

does not constitute a major public health burden, but at


which transmission would continue to occur even in the
absence of importation.47 Generally, this term applies to
areas where malaria-specific mortality and severe disease
outcomes are rare and malarias contribution to all-cause
childhood mortality is small.48 These definitions of
elimination and controlled low-endemic malaria from
Cohen and colleagues47 are adopted in this paper and
throughout this Series (panel 1). WHO categorises
countries in four programme phases by use of malaria
slide positivity and incidence rates: control, preelimination, elimination, and prevention of reintroduction. For example, a country in the elimination
phase has an annual parasite incidence of less than one
case per 1000 people at risk.49
This Series builds on WHOs categorisations and other
work.2,3 We propose a new term, a malaria-eliminating
country, which refers to a country in the process of
moving from controlled low-endemic malaria towards
elimination. There are two proposed categories for
malaria-eliminating countries: the first includes countries
that have formally declared a national, evidence-based
elimination goal, have assessed the feasibility of such a
goal, and have embarked on a malaria elimination
strategy; the second includes countries that are strongly
considering an evidence-based national elimination goal,
and that have already made substantial progress in
spatially progressive elimination (eg, by eliminating
malaria from specific islands, provinces, or geographical
areas) and in greatly reducing malaria nationwide.
Ten countries in the WHO elimination phase, eight in
the pre-elimination phase,14 and 14 that may or may not
have met WHOs epidemiological criteria for preelimination or elimination (because data are insucient
or ambiguous, or, in some cases, controversy exists with
respect to data interpretation)such as Cape Verde,
Namibia, and Swaziland (webappendix pp 311)qualify
as malaria-eliminating countries under the first
definition category. Several countries that have not
declared a national elimination goal, but are on a
plausible pathway to elimination, and that are
participating in active scientific, technical, and financial
discussions about how to achieve and sustain elimination
(eg, Bhutan, Costa Rica, Dominican Republic, So Tom
and Prncipe, and South Africa; webappendix pp 311),7,8
qualify as malaria-eliminating countries under the
second definition category. Webappendix pp 311
provides data for each of the 32 malaria-eliminating
countries and clarifies present categorisations.
This categorisation of malaria-eliminating countries is
closely aligned with the geographical distribution of
elimination feasibility that is described in the second
paper of this Series.19 We have identified a third of all
malarious countries as malaria-eliminating countries,
and thus draw attention to the need for greater support,
research, and investment into elimination and the
dicult task of preventing reintroduction.

The definitions and categorisations used in this Series


address all plasmodium species that infect human
beings. However, some countries might choose to set
interim elimination targets by parasite species49 in
recognition of the added challenge of eliminating
Plasmodium vivax malaria. The second paper19 in this
Series, which presents wordwide rankings of malaria
elimination feasibility, underscores this challenge and
does not rank the technical feasibility of P vivax
elimination because of the poor understanding of its
epidemiology and the likely species-specific strategies
and interventions that will be needed.

Elimination
Figure 1 shows a world map with countries categorised
by their epidemiological status: 109 countries are malaria
free, 67 are controlling endemic malaria, and 32 are
malaria-eliminating countries. There are, necessarily,
discretionary judgments to be made with respect to
marginal countries that could be categorised as either
controlling or eliminating malaria. We have been
conservative when making these judgments. For example,
Madagascar and Haiti have both adopted elimination
goals,50,51 but in view of their present malaria burden and
other factors aecting the feasibility of elimination,14 we
do not categorise either country as a malaria-eliminating
country. Country conditions and progress towards
elimination will change with time, and we will continue
to reassess the epidemiological status and revise the
categorisation of each country.
The epidemiological status of the countries shown in
figure 1 are not intended to be prescriptive. We believe,
on the basis of country-specific evidence and policies,
assessments, and judgments made by WHO, national
leaders, and malaria experts, that the countries defined
as malaria-eliminating countries all have a reasonable
prospect of eliminating malaria within the next decade
or so.3 Some countries, such as the Solomon Islands,
will find elimination more dicult than will others,
such as Argentina. Some countries defined as
controlling malaria, especially those in Latin America,
might think that figure 1 is overly conservative and
believe that they too can achieve elimination in the next
decade or so.
For a country to decide to move from controlled lowendemic malaria to elimination will always be a matter of
judgment for national decision makers, and should be
based on a comprehensive understanding of the technical,
operational, financial, and socioeconomic viability of the
task.49,52 Countries should be discouraged from embarking
on elimination programmes on the basis of national
ambitions that are not founded on detailed evidence. All
countries contemplating elimination should comprehensively assess the feasibility of malaria elimination,
as recently done in Zanzibar,53 and make their decision on
the basis of the results. Further work and experience will
clarify the feasibility of elimination in diverse settings. In
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Series

Cape Verde
Maldives
So Tom and Prncipe

Seychelles
Comoros

Solomon Islands
Vanuatu

Mauritius
Reunion

Malaria-free
Eliminating malaria
Controlling malaria

Figure 1: Categorisation of countries as malaria free, eliminating malaria, or controlling malaria, 2010
Source: adapted from reference 2 with permission from authors and publisher.

the second paper in this Series, Tatem and colleagues19


present global rankings of the overall feasibility
(a combination of technical and operational feasibility) of
Plasmodium falciparum elimination, and the operational
feasibility of P vivax elimination. Figure 2 shows the key
factors that determine the technical feasibility of
elimination. There is a close, but not perfect, association
between the designation of malaria-eliminating countries
in this paper and the model-based estimations of
elimination feasibility presented by Tatem and colleagues.19
For example, the data that they present lend support to a
higher level of ambition for some Latin American countries
than we have recognised.

shows that in only seven of the malaria-eliminating


countries (Botswana, Cape Verde, Dominican Republic,
Namibia, So Tom and Prncipe, South Africa, and
Swaziland) the malaria burden is due solely or mainly
to P falciparum. The other 25 malaria-eliminating
countries either have a mix of P vivax and P falciparum,
or have predominantly or solely P vivax malaria. The
prevalence of P falciparum malaria in these countries is
falling at a faster rate than is the prevalence of P vivax
malaria, and, therefore, the proportion of malaria due
to P vivax is increasing. Thus, for countries outside
Africa, the final stages of elimination will be the
elimination of P vivax malaria,54 as was the case for

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Elimination worth
assessing

Elimination
probably not
feasible for the
time being

Elimination
plausible

Elimination worth
assessing

Low

Frequency of malaria importation

Malaria-eliminating countries share three important


characteristics. First, most of them lie at the margins of
malaria-endemic regions (figure 1). For example, Algeria,
China, and Mexico are situated at the most
northern margins of endemic malaria transmission, and
Argentina, South Africa, and Vanuatu are situated at the
most southern margins of endemic malaria transmission.
Second, malaria-eliminating countries already have
substantial malaria-free areas. Third, transmission in
malaria-eliminating countries has typically been greatly
reduced in recent years and incidence is generally low.
These characteristics, for obvious reasons, make the task
of malaria elimination much easier.
P vivax malaria is the dominant challenge across the
malaria-eliminating countries. Figure 3 maps the
proportion of human malaria caused by P falciparum
and P vivax by country. Comparison of figures 1 and 3

High

Characteristics of malaria-eliminating countries

Low

High
Intensity of malaria transmission

Figure 2: Factors that determine technical feasibility of elimination


Source: adapted from reference 3 with permission from authors and publisher.

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Series

Cape Verde

So Tom and Prncipe


Comoros

Solomon Islands
Vanuatu

>90% P falciparum
>90% P vivax
P falciparum and P vivax

Figure 3: Categorisation of countries according to whether human malaria is predominantly caused by Plasmodium falciparum, Plasmodium vivax, or both P falciparum and P vivax, 2010
Source: adapted from reference 3 with permission from authors and publisher.

most countries that have already achieved elimination.29,55


This reality and other challenges have sparked a
renewed interest in P vivax.56,57
The table lists the 32 malaria-eliminating countries,
with their socioeconomic and other defining
characteristics. Generally, small countries with few people
will find elimination easier than will large countries with
large populations, although this association will not
necessarily be the case if the small countries are also poor.
28 of the malaria-eliminating countries are middleincome or high-income countries, in which the gross
national income is greater than US$975 per head per
year.58 The remaining four countries (Kyrgyzstan, North
Korea, Tajikistan, and Uzbekistan) will find the task of
elimination much more challenging.
Life expectancy at birth is a good indicator of a countrys
overall health. Life expectancy in malaria-eliminating
countries ranges from 48 years in Swaziland to 79 years
in Costa Rica and South Korea (table).59 The countries
with the lowest life expectancies are those with high child
mortality, a weak health infrastructure, and a high
prevalence of HIV/AIDS. Such countries have tough
decisions to make about resource allocation amidst
competing disease priorities.
An important issue for many countries embarking on
elimination is whether they are eligible for grants from the
Global Fund to Fight AIDS, Tuberculosis and Malaria; the
US Presidents Malaria Initiative; or the World Banks
International Development Association. 22 of the malariaeliminating countries are Global Fund eligible and ten are
not (table). The countries that are not eligible are
upper-middle-income countries or high-income countries
1570

and should therefore be able to finance malaria elimination


with their domestic resources. The Presidents Malaria
Initiative concentrates on malaria control in 15 highburden African countries60 and also provides support to
So Tom and Prncipe. Eligibility for funding from the
International Development Association is, with some
exceptions for very small countries, based on gross national
income per head. 11 of 32 malaria-eliminating countries
are eligible for funding from the International
Development Association (table) and are therefore
receiving, or can receive, highly concessionary loans for
malaria elimination.
Another key variable is the present total health
expenditure per head per year. If this amount is small,
malaria elimination can constitute a substantial (and
possibly unjustifiable) proportion of all funds available
for health. If the total health expenditure is large, malaria
elimination can be financed without interfering with
other health priorities or the health sector as a whole.
Total health expenditures per head per year of malariaeliminating countries varies from $14 to $1168 (table).61
The economics and financing of elimination is discussed
in greater detail in the fourth paper of this Series.21
The proportion of all private health-care expenditure
(typically paid for out-of-pocket) in malaria-eliminating
countries ranges from 8% to 78%. For countries in which
this proportion is high, it will be especially necessary
to enlist non-governmental health-care providers in the
task of malaria elimination.2 Additionally, the development
of social health insurance and other risk-pooling mechanisms will greatly improve the financial feasibility of
malaria elimination.6264
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Comparison of past and present malariaeliminating countries


Countries that have successfully eliminated malaria tend
to be wealthier than those that are seeking to eliminate.
This finding raises two important questions. When they
were in the process of eliminating malaria, were the
countries that have achieved elimination wealthier than
Population
(millions)

Life
expectancy at
birth (years)

GNI per
head
(US$)*

the countries that are currently trying to eliminate? And,


at the time, did they have stronger health-care systems
than malaria-eliminating countries do at present?
We reviewed the economic situation in the 32 present
malaria-eliminating countries and in 99 countries
that attempted elimination since 1948. Webappendix
p 12 shows methods, data sources, and analysis.

GFATM R10
Private health
Health
expenditure per expenditure (% of total malaria
eligibility (Y/N)
health expenditure)
head (US$)*

PMI
selected
(Y/N)

World Bank
IDA eligible
(Y/N)

Low-income economies
Kyrgyzstan

52

66

740

35

57

North Korea

238

66

14

14

Tajikistan

68

67

600

21

77

Uzbekistan

273

68

910

30

49

Lower-middle-income economies
Azerbaijan

86

68

3830

102

73

Bhutan

07

63

1900

49

27

05

70

3130

112

21

13246

74

2940

94

59

Cape Verde
China
El Salvador

61

72

3480

181

38

Georgia

43

72

2470

147

78

Iran

719

72

3540

215

49

Iraq

307

63

21

N
N

Paraguay
Philippines
So Tom and Prncipe
Solomon Islands
Sri Lanka

62

74

2180

117

61

903

71

1890

52

67

01

61

1020

49

15

05

67

1180

44

201

71

1780

62

52

Swaziland

11

48

2520

155

34

Vanuatu

02

69

2330

67

35

Upper-middle-income economies
Algeria

343

71

4260

148

18

Argentina

398

75

7200

551

54

Botswana

19

56

6470

379

23

Costa Rica

45

79

6060

402

31

N
N

Dominican Republic

99

72

4390

206

63

270

72

6970

259

55

1063

76

9980

527

55

Namibia

21

59

4200

281

33

Panama

34

76

6180

380

31

South Africa

486

54

5820

425

62

Turkey

739

73

9340

352

27

Malaysia
Mexico

High-income economies
Saudi Arabia

246

71

15 500

492

23

South Korea

486

79

21 530

1168

44

Total population

20539

=data not available. GNI=gross national income. GFATM=the Global Fund to Fight AIDS, Tuberculosis and Malaria. PMI=the Presidents Malaria Initiative of the US
Government. IDA=the International Development Association. Y=yes. N=no. All data are from standard internet sources provided by the World Bank, WHO, Central
Intelligence Agency, and the Global Fund to Fight AIDS, Tuberculosis and Malaria. Data are from the most recent year available, mostly 200608. *Atlas method (US dollars):
the Atlas conversion factor is used by the World Bank to facilitate cross-country comparisons of national income and health expenditure. The method uses the 3-year average
of the local currency exchange rate to US dollars, adjusting for inflation. R10 refers to applicant eligibility for Round 10 in 2010. So Tom and Prncipe is not among the
PMI 15 focus countries but is receiving support from the governments of Brazil and the USA for its elimination programme. Adapted from reference 2 and reproduced with
permission of the authors.

Table: Demographic, economic, health, and aid characteristics of the 32 malaria-eliminating countries

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Purchasing-power parity in US dollars (2005) were used


for all comparisons. We identified a strong association
between the wealth of a country and the success of its
elimination programme. However, this association is
confounded by geographic position, with temperate
countries being on average both more wealthy and less
malarious.
Of the 50 countries that successfully eliminated
malaria, only four (8%) had a gross domestic product
(GDP) of less than $2500 per head at the time that they
were declared malaria free: Albania in 1967, Granada and
San Lucia in 1962, and Tunisia in 1979. By comparison,
six (18%) of the 32 malaria-eliminating countries have a
GDP per head of less than $2500. These countries,
especially the Solomon Islands and Tajikistan, which also
face high technical or operational barriers to elimination,19
will probably need substantial and sustained external
finance to achieve and maintain elimination. The average
GDP per head of the 32 present malaria-eliminating
countries ($7634) is very similar to the average GDP of
countries that successfully eliminated malaria in the past
at the time they succeeded in elimination ($7592).
Of the 50 countries that successfully eliminated
malaria, 20% had less than 05 physicians per 1000
people at the time they eliminated. This threshold is
consistent with cross-country estimates of the minimum
number of physicians per head needed for
low-level health services.65 Seven (21%) of the countries
that are trying to eliminate malaria have fewer
physicians per head than this threshold. These countries
with weak and under-resourced health systems will face
unique challenges in the elimination of malaria.
Strengthening of health systems is receiving far more
attention and investment than it did several decades
ago.66 Additionally, partly as a result of widespread
failure in the public health sector, health care delivered
by the private sector has proliferated throughout
developing countries.67 In some countries, elimination
will be achieved only if the private sector is successfully
incorporated into the elimination programme.2

Achieving elimination
A conducive environment, including political, social,
financial, operational, and technical factors, is
imperative for successful elimination. As history has
taught us, a universal approach is ineective, and each
country or region pursuing elimination should
thoroughly assess their situation and develop a strategy
for elimination and prevention of reintroduction. The
second paper19 in this Series outlines the details of
technical considerations, the third paper20 presents
operational considerations, and the fourth paper21
discusses financial considerations.
Most of the activity that a malaria programme must
take on to achieve elimination is similar to the activities
needed to maintain controlled low-endemic malaria, and
should already be well established before the launch of
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an elimination eort. High coverage with appropriate


vector control interventions, and with diagnostic and
case management services should be established and
maintained. Data collection should be well designed and
rigorously undertaken, and a high standard of
programme management is essential. As elimination
approaches, these activities should continue, but will
become more focal as the heterogeneity of malaria
transmission increases.49
Elimination needs a relentless focus on surveillance
and response, and especially on the identification and
rapid elimination of foci of all infections, both
symptomatic and asymptomatic.20,68 In the third paper in
this Series, Moonen and colleagues20 review the specific
operational requirements for elimination programmes.
In addition to the need for sophisticated surveillance and
response systems, they detail the onerous requirements
for active case detection at borders, screening of highrisk migrants, and implementation of cross-border and
regional initiatives. To support these activities at the
necessary level of sensitivity, improved laboratory
facilities, including capacity to undertake PCR testing,
genotyping, and serology, are needed.
A further elimination-specific intervention is mass
drug administration or some form of mass or focused
screening and treatment. Although experience of these
techniques in some parts of the world has been
discouraging,69,70 several countries, including China71 and
Vanuatu,28,72 have successfully used mass drug
administration. A comprehensive review of country
experience with mass drug administration, screening,
and treatment is urgently needed, with a particular focus
on Asia. An improved understanding of past and present
practice and results from such reviews will help in the
development of appropriate recommendations to malariaeliminating countries for the suitability and timing of
these interventions, and for which techniques and
combinations of drugs are most eective.

Challenges of elimination
The specific challenges in elimination of malaria vary
substantially between countries and regions and,
although common agendas exist, some countries and
regions need unique solutions. The long-term research
agenda, as defined by MalERA,6 will enable the
development of new generations of diagnostics, drugs,
vaccines, and insecticides during the next decades. For
the 32 malaria-eliminating countries, most of these new
interventions will come too late to assist their elimination
eorts, although they will be helpful in the long term for
prevention of reintroduction. The research agenda that is
especially relevant to countries trying to eliminate malaria
consists of short-term operational research to improve
the eectiveness of present antimalaria interventions.
The Malaria Elimination Group, the Asia Pacific Malaria
Elimination Network, and the Southern African
Malaria Elimination Research Group, along with other
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Series

organisations, are stimulating and supporting applied


research of this type.7,8,73
For countries in Latin America, the Middle East, and
the Asia Pacific region that are trying to eliminate
malaria, elimination of P vivax poses particular challenges
that require constant emphasis and attention. The
pressing challenges in the fight against P vivax malaria
include the dormant hypnozoite stage; the unavailability
of a quick, point-of-care glucose-6-phosphate dehydrogenase test for those at risk of haemolysis if treated with
primaquine (the only available drug); and the limitations
of primaquine.56,74,75

Risks of elimination
Risks of malaria elimination exist both globally and
nationally. Globally, concern focuses mainly on issues of
finance and resistance. Some are concerned that too
much emphasis on or investment into elimination will
take funds away from the important and life-saving goal
to reduce malaria morbidity and mortality in high-burden
countries.10,76 We agree fully that shifting investments
from part one of the three-part strategy, aggressive control
in highly endemic countries, to part two, shrinking the
malaria map, would not be justified, especially in view of
the high returns on investment achieved by the prevention
of severe illness and deaths from malaria, particularly in
children and pregnant women. At present, only 8% of all
commitments to malaria made by the Global Fund are
directed towards the 32 malaria-eliminating countries.77
For the other major international funder of malaria, the
Presidents Malaria Initiative, this figure is close to zero.
Clearly, only a small amount of international finance is
allocated to elimination. Any increased focus on
elimination should not be at the expense of funding
for high-burden countries.
Another concern globally is that of the rapid spread of
insecticide and drug resistance.76,78 However, with calls
for universal coverage of insecticide-treated nets79 and the
major rollout of highly-subsidised artemisinin combination therapies,80 these risks exist in all countries that are
taking strenuous eorts to either control or eliminate
malaria. Failing to successfully eliminate malaria, or the
abandonment of control measures, could result in a
weaker set of interventions and more resistant parasite
and mosquito populations.81
The biggest concern expressed about elimination
nationally is of rebound or resurgence of disease if
commitment, finance, and eective interventions wane.
For example, in Ethiopia,82 Sri Lanka,83 and the highlands
in Madagascar,84 deadly epidemics have occurred when
elimination measures have been relaxed. The extent to
which the risks of resurgence, especially in adults, dier
between elimination and controlled low-endemic malaria
in various ecological settings is unclear. Most malariaeliminating countries are in Asia, Latin America, and
the Middle East, parts of the world that have large
populations of adults living in previously or currently
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malaria-endemic regions. However, outbreaks with high


adult mortality are rare, perhaps because in lowtransmission areas specific immune responses can be
maintained for many years after a malaria infection.85
More information is needed about whether there are
levels of controlled low-endemic malaria below which
eective antimalaria immunity is not preserved, and
about the length of time after exposure to malaria
infection before immunity is lost completely.

Benefits of elimination
Although the benefits of controlling malaria are well
documented and understood,86 the benefits of eliminating
malaria are understood to a lesser extent, are dicult to
quantify, and need further research. Many dierences
between the benefits of elimination and controlled lowendemic malaria will be negligible. Development of a
standardised set of indicators to help a country measure
and monitor the benefits of elimination will help to gain
and sustain political commitment and community
engagement, and guide countries and donors in their
decision making and long-term strategic planning
processes. The fourth paper21 of this Series discusses the
economic and social benefits that a country might expect
to gain from elimination.
From an operational perspective, a benefit that will
dier noticeably between maintenance of controlled lowendemic malaria and elimination is the system for
detecting, reporting, and responding to any imported
cases and potential outbreaks. For elimination to succeed,
this system will need to be robust, private and public
sector providers will need to work together, and the health
system will need to be well managed.20
Concerns about artemisinin resistance in the Greater
Mekong subregionthe traditional epicentre of
antimalarial resistanceare growing.87,88 Modelling
suggests that the elimination of P falciparum from this
subregion is needed to prevent the spread of artemisininresistant parasites.81 Such eorts are a global public good
and essential to the entire fight against malaria.
3330 years ago, King Tutankhamun died, possibly from
malaria.89 Egypt only recently eliminated malaria.14 One
cannot overlook the benefits of national pride after a
countrys health sector successfully eliminates a disease
that has killed its people and blighted its economy for
thousands of years.
With the appropriate levels of documentation and
assessment, every countrys elimination experience
benefits all countries remaining endemic. Countries
attempting to eliminate malaria use a wide range of
techniques in areas such as surveillance, mass drug
administration, and cross-border collaboration. The
documentation, assessment, and dissemination of these
experiences will inform other countries that will face
similar challenges.90
The regional benefits and positive externalities91 of
malaria elimination are substantial. If a country
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Series

Panel 2: Multicountry elimination efforts


Multicountry approaches to elimination can be incredibly useful to countries considering
or embarking on elimination. Collaborative efforts have many benefits, including
increased joint political support, advocacy and global awareness, alignment of strategies,
collaboration on control and prevention activities, and learning from each others
successes and challenges. Collaboration between malaria-endemic neighbours will be
especially important for countries that share borders, but it also applies to island
countries. Several examples of collaborative efforts are described below.
Asia Pacific Malaria Elimination Network (APMEN)8,95
Countries: Bhutan, China, Indonesia, Malaysia, North Korea, Philippines, Solomon Islands,
South Korea, Sri Lanka, Vanuatu.
APMEN comprises ten countries from the Asia Pacific region that are aiming for
elimination on a national or substantial subnational scale, together with the southeast
Asian and western Pacific regional offices of WHO and regional partners. APMEN supports
elimination within the region through research, collaboration, and knowledge exchange,
with a particular focus on Plasmodium vivax malaria. APMEN is supported by the
Australian Government and has its secretariat in Brisbane and San Francisco. It has held
two meetings, one in Brisbane, Australia (in 2009) and one in Kandy, Sri Lanka (in 2010),
and has launched fellowship and research grant programmes.
Elimination Eight (E8) Regional Initiative96
Front-line countries: Botswana, Namibia, South Africa, Swaziland.
Second-line countries: Angola, Mozambique, Zambia, Zimbabwe.
The E8 is a regional initiative in southern Africa comprised of four front-line malariaeliminating countries, which have collectively set a goal of elimination by 2015, together
with their northern neighbours, the four second-line countries. The E8 have pledged to work
together to eliminate malaria through a spatially progressive approach by achieving
elimination in the front-line four and, subsequently, in the second-line four. For elimination
in southern Africa to succeed, close collaboration between all of the eight countries is crucial.
An inaugural meeting of the E8 was held in Windhoek, Namibia in 2009.
The Tashkent Declaration97
Countries: Armenia, Azerbaijan, Georgia, Kazakhstan, Kyrgyzstan, Tajikistan, Turkey,
Turkmenistan, Uzbekistan.
The Tashkent Declaration is a commitment to action signed by the ministers of health from
nine countries, which reaffirms previous commitments to scale up the response with the
goal of elimination by 2015. These nine countries, with the support of the WHO Regional
Office, have been successful in developing strategies for elimination. Armenia, Kazakhstan,
and Turkmenistan have achieved elimination and are making efforts to prevent
reintroduction. The remaining endemic countries in this region have very low levels of
transmission and, with continued collaborative efforts, are also on the path to elimination.
Saudi-Yemeni Partnership in Combating Malaria98
Countries: Saudi Arabia, Yemen.
In 2001, a partnership to combat malaria between Saudi Arabia and Yemen began with
the goal to free the Arabian Peninsula from malaria by 2020. With most of the endemic
transmission occurring along the border between the two countries, the partnership
provides an opportunity for Saudi Arabia to prevent imported malaria cases and for
Yemen to reduce its burden of disease due to malaria, and, ultimately, to eliminate
malaria on the peninsula.

eliminates malaria, its neighbours are assisted in very


definite ways. Importation of malaria cases from the
country that eliminated malaria to its neighbouring
countries will end. Cross-border collaboration will have
already been established to allow the country to achieve
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elimination, and this collaboration might bring many


benefits to the health sector and other sectors.91,92 Thus,
the elimination of malaria from Botswana, Namibia,
South Africa, and Swaziland, is of tangible benefit to
their four northern neighbours, Angola, Mozambique,
Zambia, and Zimbabwe. This regional public good needs
to be factored into calculations about the benefits of
investment in malaria elimination.93 Such benefits
suggest that regional bodies, such as the Southern
African Development Community, should continue
supporting malaria elimination.94 Panel 2 details several
multicountry elimination eorts.
Spatially progressive elimination during the past
century has brought tangible benefits to millions of
people, and has allowed many countries to take up the
elimination challenge as their neighbouring countries
have completed the task. Shrinking the malaria map
steadily increases the focus of international investments
and attention on a decreasing number of countries that
are fighting malaria, and brings us closer to the last
battles against residual malaria in lowland, high rainfall,
and tropical parts of Africa. Malaria elimination is
unquestionably a high-value global public good92,99,100 that
deserves international investment.

Future strategies
When planning the elimination agenda for the next
decade, the first point to emphasise is that eorts directed
at shrinking the malaria map should in no way detract
from control in highly endemic countries or the
development of new interventions and delivery methods.
However, greater attention to shrinking the malaria map
is crucial for global malaria eradication.
Gaining international consensus on the circumstances
under which a country can regard itself as a malariaeliminating country, and be regarded as such by the
international community, would assist the clarity and
focus of international eorts. We hope that this paper
will contribute to clarification of a reasonable set of
criteria for determination of the categorisation of a
country as malaria eliminating, and that the evidence
presented in this Series will lend support to countries
that are striving to eliminate the disease. Enabling the
development of an international consensus on
elimination is clearly the role of WHO, and the process
should be supported by other partners and
stakeholders.
The first comprehensive elimination feasibility
assessment that included a qualitative and quantitative
approach was recently done in Zanzibar.53 Continued
development of such feasibility assessment so that it can
be applied in a user-friendly way by national malaria
programme leaders would be of great assistance to
countries that are contemplating elimination, but do not
yet have the evidence base to build a fully informed
strategy. This work is being taken forward jointly by,
among other organisations, WHO; the Global Health
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Series

Group at the University of California, San Francisco; and


the Clinton Health Access Initiative.
Comprehensive documentation of experiences with
past and present elimination eorts has shown great
value in providing lessons for malaria-eliminating
countries.7,8,55,101 Country-specific case studies are
completed or are being prepared for Bhutan, Mauritius,
Morocco,55 and Sri Lanka, while more focused studies of
specific aspects of elimination programmes are underway
in Botswana, China, Namibia, Philippines, Solomon
Islands,102,103 Swaziland, Vanuatu,104106 and Zanzibar.
The fourth paper21 in this Series presents what is known
about the financial and economic aspects of elimination;
however, not much is known. The first priority is to gain
a better understanding of the costs of elimination and of
preventing reintroduction, by comparison with the costs
of the maintenance of controlled low-endemic malaria. A
detailed assessment and quantification of the benefits of
elimination to a country, a region, and the world, would
also be very helpful.
Previous interventions have allowed 79 countries to
eliminate malaria since 1945. Present interventions are
allowing for steady, and in some cases rapid, progress
towards elimination in the 32 malaria-eliminating
countries. Improved evidence and guidance about the
most eective use of interventions in an elimination
setting would be very valuable. For example, when and
how should indoor residual spraying be partially
withdrawn or made more focal when infection rates are
low and when transmission is highly localised? What is
the appropriate role of mass drug administration in both
the early and late stages of an elimination programme?
Current interventions are good, but they are not good
enough. Although MalERA sets out a long-term agenda for
research to assist the next generation of malaria-eliminating
countries,6 we urgently need new and improved
interventions that can be applied soon, to assist malariaeliminating countries. Specifically, we now need three
technologies for the diagnosis and treatment of P vivax: an
improved rapid diagnostic test with greater specificity and
sensitivity for P vivax;107 an improved test for glucose-6phosphate dehydrogenase deficiency that can be used
accurately in non-laboratory settings;108 and a treatment for
P vivax that is better and safer than primaquine.109
A pervasive assumption exists that, when it comes to
malaria control and elimination, governments have to
do everything; they have to employ all sta, procure all
products, and deliver all services. This is an unnecessary
shouldering of a heavy burden. Every country has
willing and competent non-governmental partners64,110
whose help should be harnessed through eective
collaborations. For example, the mining industries,
faith-based organisations, and other groups have been
active in many malaria programmes and could do
much more.111,112
With immunisation, the maintenance of an expensive
public health intervention in the absence of disease is
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commonplace and thought to be a cost-eective investment. However, experience in malaria shows that when
the disease falls to low rates and is no longer an obvious
threat, political leadership, support, and investment
diminish and interventions are often discontinued.113,114
New approaches are needed to maintain the necessary
political commitment, community engagement,104 and
investment to eliminate malaria and prevent its
reintroduction.115 Some countries, such as Singapore,
have achieved this aim by responding to malaria through
a broader capacity for other vector-borne diseases,
especially dengue fever.116,117 In 2009, Sri Lanka had
428 cases of malaria and no malaria deaths.118 In the
same year, it had 35 000 cases of dengue fever and
360 deaths.119 Joining forces with eorts to control dengue
fever, which kills wealthy and influential people in urban
areas, can help to maintain political commitment and
investment for both diseases. Integrated vector-borne
disease control eorts need to be documented and
widely disseminated.
The average yearly growth rate of GDP per head in the
32 malaria-eliminating countries from 1998 to 2008 was
33%; during this period, the GDP per head fell in only
three of these countries. This per head growth is causing
landscapes, work patterns, and housing styles to change.
These changes tend to reduce a countrys receptivity to
malaria.120 For example, a study in northeastern South
Africa showed that higher incomes and modern house
construction were strongly associated with a lower risk of
malaria.121 Better data are needed for the eect of
economic growth on malaria.

Conclusion
Deliberate shrinking of the malaria map started over 150
years ago and countries have continued to make
remarkable progress since. As history has taught us, a
decision to pursue elimination needs thoughtful
consideration of the many challenges, risks, and benefits,
and planning for the prevention of reintroduction. With
32 countries working towards elimination, appropriate
recognition and support for their eorts is crucial. This
Series seeks to initiate a process of developing evidence
that will support and inform their eorts, and draws
attention to the gaps in knowledge that need to be filled
to realise the vision of a malaria-free world.
Contributors
All authors participated in the development of the ideas for this paper.
The text was drafted by RGAF, AAP, JH, and CC, with contributions
from all other authors. RWS helped shape the key messages. Data
analysis was done mainly by CC and BW. All authors took part in the
review, preparation, and final approval of the paper.
Conflicts of interest
RGAF, CC, and AAP, work at the Global Health Group of the University
of California, San Francisco, CA, USA. The Global Health Group exists
in part to support countries that are embarked on an evidence-based
pathway towards elimination. RRA, TAG, and MHR play leading roles in
the malaria elimination programmes of Sri Lanka, Ethiopia, and Mexico,
respectively. OS leads the malaria programme at the Clinton Health
Access Initiative which actively supports malaria elimination in southern

1575

Series

Africa. RGAF, AAP, BMG, OS, MHR, RRA, and RWS serve as members
of the Malaria Elimination Group. RWS has received funding from
Novartis for chairing meetings of national control programmes in Africa
and has received a research grant from Pfizer. The findings and
conclusions in this paper are those of the authors and do not necessarily
represent the views of their employing organisations nor of the sources
of funding.

For more on the Malaria


Elimination Group see http://
www.malariaelimination
group.org

Acknowledgments
The work of the Global Health Group on malaria elimination is supported
by grants from the Bill & Melinda Gates Foundation and ExxonMobil.
RWS is a Wellcome Trust Principal Research Fellow (#078925) and
acknowledges the support of the Kenyan Medical Research Institute
(KEMRI). BW is supported by the Consultative Group on International
Agricultural Research, the Bill & Melinda Gates Foundation, United States
Agency for International Development, the German Federal Ministry for
Economic Cooperation and Development, and the World Bank Group.
The authors acknowledge the members of the Malaria Elimination Group
for reinvigorating the science and practice of malaria elimination. We are
grateful to the five anonymous reviewers of this paper for their extremely
helpful comments. We also thank Hyun-Ju Woo for invaluable assistance
in the preparation of the manuscript.
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