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CSU 121/2011: CHANGES IN THE BURDEN OF MALARIA IN SUB-SAHARAN AFRICA

Wednesday, 6th of April 2011

 

 

Sub-Saharan Africa defies generalization. Many islands and archipelagos have made striking progress against malaria. In central Africa, with the exception of Rwanda, progress is scanty or poorly documented. Everywhere, the need for better disease reporting and modern case finding (through RDTs, notably) is evident.

This article, with maps and tables, is best viewed at

http://www.thelancet.com/journals/laninf/article/PIIS1473-3099(10)70096-7/fulltext

Good reading.

BD

 

The Lancet Infectious Diseases, Volume 10, Issue 8,

Pages 545 - 555, August 2010

 

Changes in the burden of malaria in sub-Saharan Africa

 

Original Text

Wendy Prudhomme O'Meara, Judith Nekesa Mangeni, Rick Steketee, Prof Brian Greenwood

Summary

The burden of malaria in countries in sub-Saharan Africa has declined with scaling up of prevention, diagnosis, and treatment. To assess the contribution of specific malaria interventions and other general factors in bringing about these changes, we reviewed studies that have reported recent changes in the incidence or prevalence of malaria in sub-Saharan Africa.

Malaria control in southern Africa (South Africa, Mozambique, and Swaziland) began in the 1980s and has shown substantial, lasting declines linked to scale-up of specific interventions. In The Horn of Africa, Ethiopia and Eritrea have also experienced substantial decreases in the burden of malaria linked to the introduction of malaria control measures. Substantial increases in funding for malaria control and the procurement and distribution of effective means for prevention and treatment are associated with falls in malaria burden. In central Africa, little progress has been documented, possibly because of publication bias. In some countries a decline in malaria incidence began several years before scale-up of malaria control. In other countries, the change from a failing drug (chloroquine) to a more effective drug (sulphadoxine plus pyrimethamine or an artemisinin combination) led to immediate improvements; in others malaria reduction seemed to be associated with the scale-up of insecticide-treated bednets and indoor residual spraying.

 

Introduction

After a period of neglect, the urgent need to control malaria has once again engaged the attention of the international health community. Control of malaria is now on the political agenda of several of the world's wealthiest countries and funds have become available from the Global Fund to Fight

AIDS, Tuberculosis and Malaria, The US President's Malaria Initiative, the

World Bank, and bilateral donors on a scale not seen since the first

attempted malaria eradication campaign in the 1950s and 1960s. The global

fight against malaria is now being coordinated by the Roll Back Malaria

Partnership , and major donor foundations,

such as the Bill and Melinda Gates Foundation, have greatly increased

financial support for malaria research. When compared with the low coverage

of malaria control measures in 1999—2001,1these investments have resulted in an increase in global production,

procurement, distribution, and use of insecticide-treated bednets (ITNs).

Global production more than tripled from 30 million in 2004 to 100 million

in 2008. UNICEF procurement increased roughly 20-fold between 2000 and 2005

and has been stable since.2,

3Ownership and use of ITNs within households, as measured by the number of

children under 5 years of age reported to have used an ITN the previous

night, increased by three to ten times between 2000 and 2008 in many African

countries.2There has also been an increase of about 25 times in the global procurement

of artemisinin combination therapies (ACTs) in the past 5 years.2,

3

 

A renewed focus on elimination (cessation of local transmission of malaria

within a defined geographical region) and eradication (global disappearance

of one or more species of malaria parasite)4has spurred several new initiatives, such as the Malaria

Elimination Group , focusing on

practical components of malaria elimination and the Malaria Eradication

Research Agenda group setting the research

agenda needed to support elimination and eradication.

 

This drive towards elimination has been encouraged by reports from several

malaria endemic areas of declines in incidence of clinical cases and deaths.

These changes have coincided with scale-up of effective prevention with ITNs

and the use of more effective treatments for malaria in endemic areas. In

some areas, additional vector-control measures, including indoor residual

spraying and larval control have been deployed. The situation in Africa as a

whole and how specific interventions have contributed to success stories is

unclear. Therefore, we reviewed the relation between reported changes in the

incidence or prevalence of malaria and the introduction or scale-up of

specific interventions in several countries in sub-Saharan Africa. In this

Review, we aim to identify common patterns and investigate whether factors

other than these specific interventions might have contributed to the

changes in malaria burden that have been reported.

 

13 key papers, which describe recent changes in malaria morbidity in

sub-Saharan Africa were identified by consultation with experts. These

papers were used as a guideline for a search for similar or related

published studies. For each article reported we noted the: country, region,

study period, population size, local endemicity, control measures and other

factors independent of the study that might have affected transmission,

rainfall data (if available), the type of data (ie, outpatient numbers,

inpatient numbers, malaria mortality, prevalence), whether cases were slide

confirmed, and the percentage change and the years of change for each type

of data reported. The total number of malaria outpatients or inpatients for

each reported year and the total number of deaths were also noted, when the

information was available.

 

Changing malaria burden in sub-Saharan Africa

 

We identified studies that recorded trends in malaria indicators over time

from countries in sub-Saharan Africa (figure 1,

table).

Most reports describe a recent decline in the incidence of malaria, the rest

report little or no change.

 

 

 

 

Figure 1 Full-size image(47K)

 

 

Distribution of reports included in the Review

 

 

 

TableTable image

 

 

 

Reports of changes in the pattern of malaria in sub—Saharan African

1999—2009.

 

The Horn of Africa

 

Reports from Ethiopia have documented declines in malaria morbidity across

the country.5,

6Surveillance from 2000—07 demonstrated a 70% reduction in both outpatients

with slide-confirmed malaria and children less than 5 years old admitted to

hospital for malaria. Outpatient malaria cases were already declining at the

beginning of the surveillance period, before mass-distribution of ITNs and

treatment with ACTs were introduced in late 2005. The decline in patients

admitted to hospital with malaria was slower than the decline in outpatient

malaria. The largest drop in morbidity occurred at the same time as in other

parts of east Africa—2005—06.

 

The epidemiology of malaria in Ethiopia differs from that in most of

sub-Saharan Africa. Transmission is heterogeneous and generally lower than

in other countries, and Plasmodium vivax is endemic and causes up to 40%

of clinical cases.5A small study showed a decline in the overall incidence of malaria

accompanied by a shift from predominantly P vivax cases to 73% Plasmodium

falciparum cases.7

 

Reports from Eritrea paint a similar picture. Between 1998 and 2004,

substantial reductions in routinely reported clinical malaria cases were

described following a scale-up of control measures.8—10There was a reduction in both the incidence of presumptive malaria in

outpatient facilities (83% decline) and in the case fatality of malaria

admissions (25% decline overall, but trend inconsistent over the time

period). The largest decline in malaria cases was seen between 1998 and

2000. ITN ownership was 80% in 2004, but only 50% of households, when

surveyed, reported anyone having slept under an ITN the night before. It is

very likely that the massive scale-up of ITNs, indoor residual spraying,

community-based management of fevers, and environmental management of

mosquito breeding sites all contributed to these results. However, the

incidence of malaria was already declining at the beginning of the

surveillance period, before these interventions were introduced. Graves and

colleagues8showed that malaria cases increased between 1996 and 1998 before beginning

to decline in 1999; although the increase in cases could have been due to

improved reporting practices. A time-series analysis by Nyarango and

co-workers10showed that the scale-up of ITNs and indoor residual spraying was associated

with a reduction in malaria cases but not with a decline in case fatality,

whereas an expansion of community health-worker training was temporally

associated with the decline in case fatality but not with the reduction in

malaria cases.

 

East Africa

 

Many reports from east Africa have recorded substantial reductions in

malaria transmission and morbidity in the region. In the coastal area of

Kenya, paediatric malaria admissions declined by as much as 75% between 2003

and 2007.11,

12Since the mid-1990s, parasite prevalence in the Kilifi district has declined

progressively from 35% to less than 1%. Prevalence declined by 30% before

any change in the incidence of malaria admissions was recorded. Although ITN

use has increased concurrently with the decline in paediatric admissions,12

the prevalence of malaria infection declined from 35% to 10% before ITN

coverage reached 25%, and before the introduction of ACTs.11

 

In a district in central Kenya, the proportion of malaria outpatient visits

declined from 40% in 2000 to 0% by the end of 2006, with the largest decline

between 2003 and 2005.13Coverage with ITNs in the area is estimated to be 65%, substantially higher

than that reported on the coast, and 35% of households reported use of some

mosquito reduction method, such as environmental management or repellents.

This study is one of the few in which entomological data were collected

concurrently with longitudinal morbidity data. The entomological inoculation

rate was estimated to be very low: 0—0·03 infectious bites per person per

year in the hospital catchment area.

 

In western Kenya, malaria transmission in the lowland areas around Lake

Victoria has historically been very high, with entomological inoculation

rates estimated to be as high as 250 infectious bites per person per year.

14,

15Between 2003 and 2007, demographic surveillance revealed a 42% reduction in

all-cause mortality among children less than 5 years of age.16A 16% decline in malaria-specific mortality was estimated using verbal

autopsy methods.16Verbal autopsy methods have low specificity,

17and malaria-specific mortality likely declined substantially more than was

suggested by verbal autopsy.

 

Data compiled from paediatric inpatient records of 17 hospitals across Kenya

(including hospitals on the coast and in western Kenya) showed different

temporal trends in malaria admissions between 1999 and 2008.18Only four hospitals had clear, substantial declines in malaria admissions.

Six other sites had small or unstable declines. Only six of ten sites that

reported reductions in malaria admissions also reported reductions in

all-cause admissions, which would suggest a true decline in malaria

admissions, rather than a re-classification because of changing diagnostic

practices. In seven other sites, malaria admissions remained stable or

increased. Across all sites together the number of paediatric malaria

admissions decreased by 49%. However, this average masks the heterogeneity

of the effect of nationwide malaria control.

 

In Rwanda, data from 20 facilities representing every district in the

country showed a decline of more than 50% between 2005 and 2007 in both

inpatient and outpatient slide-confirmed malaria cases.6Before 2005, the number of cases had been increasing annually, but began to

decline shortly before or at the same time as mass distribution of

long-lasting insecticidal bednets and the use of ACTs in 2006—07.

 

In neighbouring Burundi, routine health-facility reporting from the Karuzi

province showed an epidemic peak of clinically diagnosed malaria in 2001,

against a background of low but stable monthly incidence of cases.19Between 2002 and 2005, annual indoor residual spraying interventions in the

province had only a small effect on parasite prevalence.20Prevalence in children less than 9 years old declined from 64% to 40%, but

the latter figure was not always significantly different from the control

group over the 3 years of intervention. No additive benefit of bednets could

be detected, and indoor residual spraying in the lowland areas did not

reduce prevalence of infection in adjacent highlands.20

 

In contrast to the largely encouraging reports from Kenya and Rwanda, data

from a highland and a lowland area in western Uganda showed steadily

increasing numbers of malaria cases and deaths in district hospitals from

1991 to 2000, with a two-fold to four-fold overall increase in the number of

children admitted to hospital with the disease.21A slight decline in the proportion of positive blood films was seen in a

single facility in an area of moderate transmission in Uganda after one

round of indoor residual spraying in 2007.2214 months after indoor residual spraying, the proportion of blood films that

tested positive began to increase, suggesting that trends are easily

reversed if control measures are not sustained.

 

In Muheza district, Tanzania, the number of malaria cases increased between

1994 and 2002, with prevalence among children remaining consistently above

80%.23However, the incidence of malaria has recently declined substantially in

some parts of northeastern Tanzania. In the same district, the incidence of

malaria in children fell rapidly during the early 2000s, reaching such a low

level that a trial of intermittent preventive treatment in infants had to be

stopped in 2005 as there were not enough cases.24In the neighbouring Korogwe district, the prevalence of malaria parasitaemia

among febrile patients fell substantially between 2003 and 2006 from 78% to

24% in lowland areas and from 25% to 7% in highland areas.25These changes were detected by community health workers who treated fevers

presumptively for malaria but collected blood films at the time of

treatment. Improved access to effective treatment through the community

programme probably contributed to the decline. At least four of eight

hospitals included in a review of admission data in southwest Tanzania

showed higher numbers of malaria admissions between 1995 and 2000 than in

the preceding 10 years; the number of malaria admissions declined at only

one of the hospitals.26The current situation in these areas has not been reported. Recent

entomological data from the Kilombero Valley in Tanzania, an area with one

of the highest rates of transmission in the world, reported a 60—70% lower

entomological inoculation rate than previously recorded;27although the effect of that decline on clinical malaria is unknown.

 

In highland areas of east Africa, where malaria transmission is unstable and

prone to epidemics, stable transmission has been reported in areas that have

historically been thought to have only periodic epidemic transmission.28In these areas of stable transmission, adults have functional immunity to

malaria and the age ratio of cases in children to adults is greater than

one. The number of cases in three highland hospitals in western Kenya

gradually increased up to the year 2000, although transmission remains

strongly seasonal. More recent data from a few villages in highland Kenya

show success of government efforts to control malaria. Malaria incidence

declined from roughly 100 cases per 1000 people per year in 2003 to no cases

at all in 2008.29Because ITN coverage was less than 25%, this success is probably

attributable to sequential rounds of indoor residual spraying covering

70—95% of households. By contrast, data from two highland sites in Uganda

show slight increases in slide-confirmed cases from 2002 to 2006.30Anecdotal evidence from Burundi suggests that malaria transmission is

occurring at higher altitudes than ever before.31

 

Central Africa

 

Because of a lack of research initiatives and poor infrastructure to support

routine case reporting data from central Africa are sparse. The limited data

available show little change in the malaria burden from historical levels.

In Brazzaville, Congo, the percentage of paediatric hospital admissions due

to malaria (30%) did not change between 1989 and 2001.32Data from eight malaria reference laboratories in eastern Sudan showed a

slight decline in the proportion of positive smears between 1998 and 2002,

but this decline followed a period of increased malaria infection during

several years of heavy rains33and brought the proportion back to the levels noted before the heavy rains.

Two small cross-sectional studies in Cameroon in 2000 and 2004 showed a

slight decline in parasite prevalence among asymptomatic children, but no

change in prevalence among febrile children.34

 

Southern Africa

 

In South Africa, sustained malaria control over many decades has succeeded

in stopping transmission throughout most of the country, with the exception

of the northeastern border regions adjacent to Mozambique and Swaziland.3530 years of passive and active detection of slide-confirmed malaria cases

from the province of KwaZulu Natal give a comprehensive, long-term picture

of the effect of changing control strategies, climatic factors, and other

variables that have influenced the incidence of malaria over time. Parasites

resistant to both chloroquine and sulphadoxine plus pyrimethamine, a rising

prevalence of HIV, the emergence of mosquitoes resistant to pyrethroid

insecticides used for indoor residual spraying, and increasing cases of

imported malaria contributed to a five-fold increase in malaria cases in the

province between the mid-1990s and 2001.36Climatic factors were shown to explain seasonality and short-term trends,

but not long-term trends.37In 2001, DDT was reintroduced for indoor residual spraying and cases began

to decline almost immediately. Data from sentinel facilities showed an 89%

decline in malaria admissions and deaths and an 85% decline in outpatient

malaria cases in the year after reintroduction of DDT. Replacement of

failing sulphadoxine plus pyrimethamine with an ACT might also have

contributed to the decline. By 2003, cases had declined by 99% from their

peak in 2000.38

 

A related report from the bordering regions of Mozambique, Swaziland, and

South Africa highlights the importance of coordinated regional control.39Although indoor residual spraying has been ongoing in Swaziland since 1981,

malaria remained a significant public health problem. In 2001, when South

Africa reintroduced DDT, Mozambique initiated indoor residual spraying

programmes in the border regions. The prevalence of malaria declined

substantially in regions of Mozambique that were part of the indoor residual

spraying programmes, although it dropped below 20% in only one of five spray

zones. Slide-confirmed inpatient and outpatient malaria cases at a district

hospital in the indoor residual spraying areas showed no consistent trend

between 2003 and 2005, indicating that the incidence of symptomatic cases

might have stabilised.40,

41The incidence of cases reported in the two bordering South African provinces

declined by 80—95% in 4 years. Despite no changes in malaria control

interventions, cases in Swaziland showed a similar decline of 95%,

presumably as a result of activities in neighbouring regions.

 

On the western side of Swaziland, the province of Limpopo in South Africa

also reported reductions in the incidence of malaria cases. Routine

slide-confirmed case reporting data from 1998 to 2007 showed significant

declines in cases from 2001 until the end of the reporting interval.42As in KwaZulu Natal, the main malaria control intervention in Limpopo is

indoor residual spraying, with DDT being reintroduced in 2001. ACTs were

deployed in 2004.

 

The Zambian National Malaria Control Programme has achieved substantial

success in scaling up the use of ITNs, indoor residual spraying, and

intermittent preventive treatment in pregnancy with sulphadoxine plus

pyrimethamine. ITN ownership increased substantially from 22% in 2004, to

38% in 2006, and 62% in 2008.43,

44Between 2006 and 2008, paediatric malaria parasite prevelance declined by

53% and moderate to severe anaemia by 69%.44A report from a single outpatient facility showed a remarkable decline in

the proportion of febrile cases with malaria, from 40% in 2003 and 84% in

2004 to less than 1% in 2008.45

 

In Zimbabwe, data are less encouraging. Reductions in donor funding and

national support are likely to account for the increasing morbidity and

mortality from suspected malaria reported between 2001 and 2003.46

 

West Africa

 

Compelling evidence for a dramatic decline in malaria transmission comes

from The Gambia where surveillance at five health facilities across the

country showed a 50—85% decline in the prevalence of slide-confirmed malaria

among outpatients and a 25—90% decline in malaria-related hospital

admissions.47The trend persisted over 7 years with an apparent contribution from ITN

coverage, which increased three-fold to 49% over the surveillance period.

The observed reductions were before the introduction of ACTs. The number of

outpatient cases declined before the number of inpatient cases did.

 

Apart from The Gambia, other evidence from west Africa comes from a handful

of individual hospitals or villages. An urban hospital in Libreville, Gabon

48reported an 80% decline in the number of children with positive blood smears

in the inpatient and outpatient services. The decline began in 2003 and

persisted until the end of the surveillance period in 2008. The decline

pre-dated both the introduction of ACTs in 2006 and ITN distribution in

2005, the coverage of the latter reaching 50% in 2008. Data from one village

in Senegal showed an increase in the incidence of slide-confirmed malaria

between 1998 and 2001 followed by a slight decline of 20% in 2002, although

the incidence in 2002 was still higher than in 1998.49In Niakhar, Senegal, presumptive malaria (facility surveillance) and malaria

mortality (community-based verbal autopsy) fluctuated considerably between

1992 and 2004, but no consistent trends were observed.50

 

A study from a hospital in Nigeria reported severe malaria accounting for a

steadily increasing proportion of hospital admissions between 2000 and 2005,

with nearly 13% of patients admitted having either severe malarial anaemia

or cerebral malaria by the end of the study.51Reports from Burkina Faso mention a three-fold increase in malaria cases at

health facilities between 2000 and 2007 in at least one district, despite

increasing bednet coverage.52

 

There was only one report that discussed the effect of agricultural

practices on the risk of malaria infection.53Malaria indicators in two villages in Côte d'Ivoire with similar, intense

transmission but different agriculture practices were compared. Both the

number of malaria cases and the entomological inoculation rate temporarily

declined in one village with irrigated rice farming when irrigation was

interrupted for a season. During the same season, the village without

irrigated rice farming had a very slight decline in presumptive malaria

cases, despite an increase in entomological inoculation rate from 230 to 570

infective bite per person per year.

 

African islands

 

Some of the most remarkable successes have been reported from islands,

including Bioko (part of Equatorial Guinea), Zanzibar, and Sao Tome and

Principe. On Zanzibar, an 87% decline in parasite prevalence was mirrored by

a 75% decline in clinically diagnosed malaria outpatient visits and hospital

admissions.54Review of monthly clinical cases of malaria in children less than 5 years of

age showed that the downward trend began about 1 year after the introduction

of ACTs, and before the widespread distribution of ITNs. The number of cases

dropped from more than 1500 per month to fewer than 100 per month before the

initiation of ITN distribution campaigns. Changes in diagnostic practices

might have had an effect on these figures. The timing of the decline (2005

to 2006) is similar to that of other reports from the region.

 

The Bioko Island Malaria Control Project was launched in 2003 and combined

bi-annual indoor residual spraying programmes with the introduction of ACTs

and scale-up of the use of intermittent preventive treatment in pregnancy.

55,

56Distribution of long-lasting insecticidal bednets started much later, in

2007. After 4 years of intensive vector control and improved case

management, sporozoite rates were reduced by ten times, leading to a decline

in cross-sectional prevalence of malaria parasitaemia in children from 42%

to 18%, and a 50% reduction in the prevalence of fever. A remarkable 70%

reduction in all-cause mortality in children age less than 5 years was

reported in this intervention time interval.57

 

On Sao Tome, surveillance data between 1995 and 2007 showed malaria

outpatient consultations and hospital admissions declined by 80—90% in both

adults and children after introduction of indoor residual spraying, ACTs,

and long-lasting insecticidal bednets in 2004.58Indoor residual spraying on Sao Tome resulted in a reduction of paediatric

parasite prevalence from 30% to less than 1%, a greater reduction than

indoor residual spraying programmes in Burundi, where prevalence fell from

50% to 40%, and in Mozambique, where prevalence fell from 65% to 20%.59

 

Discussion

 

The burden of malaria has declined substantially in several areas of

sub-Saharan Africa, particularly in the past 3—5 years, coinciding with

expanding coverage of malaria prevention and treatment in many countries (figure

2).

Country-wide surveillance in Ethiopia and Eritrea reveals a 70% decline in

malaria morbidity, with similar changes documented in parts of Kenya, The

Gambia, Rwanda, and Zambia. Malaria control on islands has been remarkably

successful, even though the approaches used have been diverse. However,

other reports describe a static or deteriorating situation in some

locations. Malaria transmission may be increasing in the highland areas of

east Africa, perhaps as a result of environmental conditions that facilitate

transmission. Several countries in west and central Africa have not yet had

any significant reductions in malaria incidence. The situation in large

parts of Africa is unknown.

 

 

 

 

Figure 2 Full-size image(129K)

 

 

Changes in the malaria burden in different regions of sub-Saharan Africa

 

Malaria “burden” defined as worsening (red) if malaria indicators increased

for 2 years consecutively, unchanged (blue) if malaria indicators decreased

for at least 2 years consecutively, or improving (green) if they did not

change in either direction during the study. Malaria indicators used were

the incidence of inpatient or outpatient cases of malaria, deaths from

malaria in children, or the prevalence of malaria infection.

 

The success stories include countries across the spectrum of transmission

intensity. Progress may have been predominantly made in countries with low

to moderate endemicity, but these countries might have started malaria

control efforts at an early date. In southern Africa (South Africa,

Swaziland, and parts of Mozambique), aggressive control started in the 1970s

and 1980s and is ongoing. In this case, successful control was accelerated

by adopting a regional strategy rather than individual country approaches.

Although expanded control efforts began more recently in Eritrea and

Ethiopia, they have seen early and durable declines. Unfortunately, data are

not available for large parts of sub-Saharan Africa, including countries

with high and often seasonally intense transmission.

 

Many reports attribute decreases in malaria morbidity to specific

interventions, although the causal link between the decline and the

intervention is more convincing in some cases than in others (figure 3).

In several reports, the decline began before the specific intervention was

deployed, or the decline was already underway at the beginning of the study

period, suggesting that factors not investigated contributed to the decline.

This is highlighted in the two reports from the coast of Kenya, one of which

shows an association between ITN distribution and a decline in admissions of

children with malaria to hospital whereas the other shows substantial

changes in prevalence of malaria infection before the decline in admissions

and the distribution of ITNs.11,

12Similarly, in The Gambia and Zanzibar, the decline in malaria began before

ITNs were rolled out. In Eritrea and Ethiopia, a substantial outbreak

occurred from late 2002 to 2005,60thus declines in malaria incidence back to historical levels were already

underway as interventions were introduced in 2005 and 2006. In other

reports, the temporal association with the introduction of specific

interventions is compelling, particularly in the data from the northern

provinces of South Africa and Bioko Island.

 

 

 

 

Figure 3 Full-size image(96K)

 

 

Changes in malaria indicators over time relative to the introduction or

scaling up of control measures in selected countries

 

(A) Number of malaria hospital admissions in Zanzibar.46(B) Number of malaria hospital admissions in Ethiopia.

6(C) Proportion of hospital admissions due to malaria in Fajara, The Gambia.

40(D) Incidence of paediatric malaria hospital admissions (hospitalisations

per 1000 children in the hospital catchment area) in Kilifi, Kenya.11(E) Number of malaria cases in Limpopo, South Africa.

36(F) Number of malaria cases in Sao Tome and Principe.

48(G) All cause mortality in children less than 5 years of age per 1000 births

in Bioko Island, Equitorial Guinea.47ACT=artemisinin combination therapies. LLITNs=long-lasting

insecticide-treated bednets. ITNs=insecticide-treated bednets.

CQ+SP=chloroquine with sulfadoxine plus pyrimethamine. IRS=indoor residual

spraying.

 

Indoor residual spraying, ITNs, and ACTs reduce mortality and morbidity from

malaria when deployed under controlled conditions. Indoor residual spraying

probably had a key role in achieving successful malaria control in South

Africa and on Bioko and Sao Tome islands but its effect seems to have been

smaller in other places. There is strong evidence that ITNs can provide a

substantial degree of protection against mortality and morbidity from

malaria,61especially when used by a high proportion of the population. Widespread

deployment of ACTs, which are partly gametocytocidal, would be expected to

have an effect on transmission of malaria in communities where a high

proportion of infected individuals have symptoms and seek treatment.62,

63Thus, for example, introduction of ACTs might have contributed to the

success of malaria control in South Africa.38ACTs would not be expected to have a major effect on malaria transmission in

communities where only a small proportion of infected individuals are sick

and seek treatment. In Zanzibar, the fall in malaria incidence before the

introduction of ITNs or indoor residual spraying that followed the

introduction of ACTs was, therefore, suprising.54This finding could be explained by the concurrent scale-up of malaria

diagnostics which reduced the number of presumptive cases reported, or by

the high incidence of chloroquine treatment failure at the time of the

switch to ACTs. Similarly, in The Gambia and Kilifi district, Kenya, the

fall in malaria incidence began at roughly the same time as first-line

treatment with chloroquine was changed to treatment with sulphadoxine plus

pyrimethamine or sulphadoxine plus pyrimethamine plus chloroquine.11,

47This change replaced an ineffective drug (chloroquine) with an effective one

(sulphadoxine plus pyrimethamine) and it provided a single-dose treatment

(most likely improving cure rates) and a period of chemoprevention against

new infections that persists for several weeks.64The chemopreventive effect of sulphadoxine-pyrimethamine might be especially

important in areas such as The Gambia where malaria transmission is

restricted to a few months of the year.

 

On the basis of current models of malaria transmission, we would not expect

partial coverage with ITNs and the introduction of ACTs to result in the

substantial changes in malaria incidence seen in areas with moderate

transmission. Alternative explanations for these changes should be

considered. Previous experience in Europe and North America has shown that

malaria declines as social conditions and education improve. However, these

changes (eg, improvements in house construction) are likely to be gradual

and cannot account for the sudden changes seen during the past few years,

although they might have contributed. Malaria transmission is strongly

affected by climate. However, climate has been carefully monitored in

several case studies, and although there have been fluctuations from year to

year, no overall pattern emerges that can explain the remarkable reductions

in malaria cases in some countries. A highly speculative explanation for the

reductions is a change in the parasite or its mosquito vector that has

reduced transmissibility of the infection. Both of these are biological

possibilities, but such a change seems unlikely on the opposite sides of the

continent at the same time. Finally, the transmissibility of P falciparummalaria might not be as high as has been previously thought, making it

easier for any transmission blocking intervention directed at either the

parasite (ACTs) or the vector (ITNs or indoor residual spraying) to reduce

transmission.

 

We must bear in mind the limitations in using published scientific

literature to assess the progress of ongoing malaria control programmes.

Some of the reports in this Review might be biased towards presenting data

that reflect well on the outcome of a control programme (to justify

investments) or even presenting data that suggest the malaria burden is

worsening (to encourage further investment into malaria control);

maintenance of the status quo is unlikely to result in publication in the

scientific literature. For example, three studies from Kenya show exciting

reductions in the burden of malaria, but data from 17 hospitals reveal that

there are many areas where malaria is not declining. Many of the reports we

have reviewed are limited in time and geographic scope, and therefore might

not accurately reflect nation-wide trends. Most of these reports rely on

clinical diagnosis of malaria at a health facility. We cannot account for

the effect of changes in access to care or use of health services on

incidence measured at the facility. More importantly, changes in diagnostic

practices or access to diagnostics over time can greatly affect observed

trends. Despite these limitations, the overall picture that emerges when

these studies are assembled is coherent and encouraging.

 

Conclusions

 

Reports from several countries in sub-Saharan Africa show a substantial,

recent decline in the burden of malaria. Similar changes might have occurred

in some other countries, for example Senegal, but these have not been

reported in peer-reviewed publications. In other countries, there has

probably been little change in the malaria burden. Successful control seems

to have been achieved in several different ways, but it has sometimes proved

difficult to link the timing of an apparent decline in the incidence of

malaria with the introduction of a specific intervention. Whether certain

interventions are more likely to have an effect on different outcome

measures cannot be determined, for example, whether scale-up of effective

treatment has a greater effect on burden of clinical malaria than on

prevalence. Although numbers of clinical cases have declined in many areas,

this does not mean that transmission is being interrupted or that these

areas are approaching elimination.

 

We have restricted our analysis to information presented in peer reviewed

journals and presented at international scientific meetings, and we have

focused on clinical malaria rather than on the prevalence of infection. Many

other relevant datasets likely exist (eg, parasite prevalence data as

presented in the Malaria Atlas Project ), which

would define the changing pattern of malaria in sub-Saharan Africa more

clearly than we have been able to do in this Review. We hope that this

initial attempt to review the changing pattern of malaria in sub-Saharan

Africa and the possible causes will encourage more detailed work in this

important area.

 

Search strategy and selection criteria

 

We searched the National Library of Medicine's Medline database with the

Medical Subject Headings “Africa South of the Sahara”,

“Malaria/epidemiology”, “Malaria/mortality”, “Malaria/prevention and

control”, and “Malaria/transmission”, omitting papers that contained the

keywords “Malaria/immunology”. The search was limited by restricting

retrieval to articles published in the past 10 years. Our last search was

done on March 29, 2010. The search identified 1528 publications. Articles

were included if they reported at least 2 years of data on malaria-specific

indicators (clinical or slide diagnosed case numbers, incidence, prevalence,

or malaria-specific mortality) in a population of more than 1000 people.

Cross-sectional studies reporting a single timepoint, those involving only

pregnant women, intervention studies covering 1 year or less of follow-up,

and entomological studies without any clinical or parasitological components

were excluded. Also excluded were studies published in the selected time

frame but which did not report data from the period 1999—2009. The titles

for each citation were screened and 297 were selected for review of their

abstracts. Screening of the abstracts yielded 82 publications for full

review. After reviewing the full texts, 46 studies that fully met the

inclusion criteria were identified.

 

Contributors

 

WPO and BG conceived the paper. WPO and JMM developed the data search and

extracted the data. All authors contributed to interpretation of the data,

drafting the paper, and developing the figures.

 

Conflict of interests

 

We declare that we have no conflicts of interest.

 

Acknowledgments

 

We thank Geoffrey Targett and F Ellis McKenzie for their helpful comments on

the paper.

 

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aSchool of Public Health and Health Services, George Washington University,

Washington, USA

 

bMoi Teaching and Referral Hospital, Eldoret, Kenya

 

cMalaria Control and Evaluation Partnership in Africa (MACEPA), PATH,

Ferney-Voltaire, France

 

dDepartment of Infectious and Tropical Diseases, London School of Hygiene and

Tropical Medicine, London, UK

 

Correspondence

to: Prof Brian Greenwood, Department of Infectious and Tropical Diseases,

London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E

7HT, UK

 

 

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