SCOPING REVIEW Open Access Scaling up impact of malaria ...Scaling up impact of malaria control...

Tambo et al Infectious Diseases of poverty 2012 17httpwwwidpjournalcomcontent117

SCOPING REVIEW Open Access

Scaling up impact of malaria controlprogrammes a tale of events in Sub-SaharanAfrica and Peoplersquos Republic of ChinaErnest Tambo12 Ahmed Adebowale Adedeji3 Fang Huang1 Jun-Hu Chen1 Shui-Sen Zhou1 and Ling-Hua Tang1

Abstract

This review aims at providing synthetic information with scientific evidence on the trends in the malaria eventsfrom 1960 to 2011 with the hope that it will help policy makers to take informed decisions on public health issuesand intervention designs on malaria control towards elimination in both Sub-Sahara Africa and in the PeoplersquosRepublic of China by highlighting the achievements progress and challenges in research on moving malaria fromepidemic status towards elimination Our findings showed that since 1960 malaria control programmes in mostcountries have been disjointed and not harmonized Interestingly during the last decade the causal factors of theunprecedented and substantial decline in malaria morbidity and mortality rates in most vulnerable groups in theseendemic areas are multifaceted including not only the spread of malaria and its related effects but also politicaland financial willingness commitment and funding by governments and international donors The benefits ofscaling up the impact of malaria coverage interventions improvement of health system approaches and sustainedcommitment of stakeholders are highlighted although considerable efforts are still necessary in Sub-Sahara AfricaFurthermore novel integrated control strategies aiming at moving malaria from epidemic status to control towardselimination require solid research priorities both for sustainability of the most efficient existing tools andintervention coverage and in gaining more insights in the understanding of the epidemiology pathogenesisvector dynamics and socioeconomic aspects of the disease In conclusion political commitment and financialinvestment of stakeholders in sustaining the scaling up impact of malaria control interventions networkingbetween African and Chinese scientists and their Western partners are urgently needed in upholding the recentgains and in translating lessons learnt from the Chinese malaria control achievements and successes into practicalinterventions in malaria endemic countries in Africa and elsewhere

Keywords malaria funding scaling up interventions health system Sub-Sahara Africa Peoplersquos Republic of China

Multilingual abstractsPlease see Additional file 1 for translations of the abstractinto the six official working languages of the United Nations

ReviewThe review highlights malaria events achievements andscaling up impact with scientific evidence in moving

Correspondence tambo0711gmailcom1National Institute of Parasitic Disease Chinese Center for Disease Controland Prevention WHO Collaborating Centre on Malaria Schisostomiasis andFilariasis Key Laboratory of Parasite and Vector Biology Ministry of Health207 Rui Jin Er Rd Shanghai 200025 Peoplersquos Republic of China2School of Medicine amp Pharmacy Houdegbe North American UniversityPK10 Route de Porto-Novo 06 BP 2080 Cotonou Reacutepublique du BeacuteninFull list of author information is available at the end of the article

copy 2012 Tambo et al licensee BioMed CentralCommons Attribution License (httpcreativecreproduction in any medium provided the or

malaria from epidemic status towards sustained controland elimination from 1960ndash2011 The unprecedentedand substantial reduction in malaria incidence and con-sequently mortality rates at varied degrees across Afri-can countries and Peoplersquos Republic of China (PRChina) are very encouraging although the gains are stillfragile Increased political commitment and available fi-nancial resources collectively from governments andvarious stakeholders are paramount in sustaining thescaling up innovative and integrated malaria controlinterventions and health system strengthening to turnthe tide against the malaria public health and its relatedeffects in Sub-Saharan Africa (SS Africa) and elsewhere

Ltd This is an Open Access article distributed under the terms of the Creativeommonsorglicensesby20) which permits unrestricted use distribution andiginal work is properly cited

Tambo et al Infectious Diseases of poverty 2012 17 Page 2 of 15httpwwwidpjournalcomcontent117

BackgroundThere has been improvement in the health situation inmost African countries since 1960 and malaria in par-ticular is decreasing over time in SS Africa where theglobal burden of the disease is significantly approxi-mately 90 and PR China accounts for less than 10The recent statistics showing reductions in malariadeaths are very encouraging but the situation is fragileand malaria should not be allowed to resurge [1-3] Mal-aria is a vector-borne disease caused by protozoan para-sites ie Plasmodium falciparum P vivax P malariaeP ovale or P knowlesi that completes a complex cycleof development alternating between human hosts andmosquitoes of the genus Anopheles [4] The diseaseemerged as a worldwide epidemic in the 1960s whenglobal malaria eradication was abandoned [5 6] Conse-quently the emergence of insecticide resistant and drugresistant parasite strains and vectors were greatly fuelledby poverty poor economy political instability poorhealth infrastructure and equipment deficiencies inhealth systems and policy particularly in Africa [4 7 8]The public burden and impact of this disease on humanhealth productivity loss of work efficiency and time inmalarial regions have been devastating [9]To strengthen the efforts towards the fight against

malaria the World Health Assembly passed a resolutionon controlling malaria in Africa in May 1996 and thiswas closely followed by declarations of the Organizationof African Unity(OAU) on malaria in Harare Zimbabwein 1997 and Ouagadougou Burkina Faso in 1998 [10] In1996 the African Regional Office of the World HealthOrganization (WHO) became increasingly attentive tomalaria and launched the African Initiative for MalariaControl (AIM) The AIM contributed $9 million in 1997and 1998 for accelerated implementation of malariacontrol activities in 10 countries in the region and pro-vided the foundation for the eventual launch of RollBack Malaria (RBM) in 1998 [11] The African Heads ofStates Summit to Roll Back Malaria was held in April2000 in Abuja Nigeria where they set the goal for redu-cing malaria deaths to half by the year 2010 The diversearray of meetings programmes and activities are testi-mony to the growing recognition of the regional andglobal nature of the threat posed by malaria [11-13]Strong political commitment financial support and part-nerships are important to bring about the currentdesired changes Malaria re-emerged as a major inter-national health issue in the 1990s despite the globalmalaria control strategy adopted in 1992 RBM in 1998Abuja Declaration in 2000 and strong political commit-ment and partnership respectively In the face of thesemalaria is still prevalent in 106 countries of the tropicaland sub-tropical world with 51 countries in the Africancontinent bearing the highest burden of cases and deaths

[2 9 14-16] No experts from SS Africa were involved inthe Global Malaria Eradication Program (GMEP) due tothe lack of African expertise at that time the majority ofAfrican countries were driven by representatives of west-ern countries taking decisions on their behalf in inter-national forums in addition to socio-cultural beliefs ahigh degree of malaria endemicity in the region com-bined with lack or weak health policy and infrastruc-tures and others factorsIn PR China mass patriotic health campaigns and

mass mobilization approaches on preventive efforts in1960s led to eradication of cholera plague scarlet fevertyphoid and syphilis with a considerable reduction of theburden of infectious diseases [4 17 18] Within thesame period the Chinese government had implementedbirth control measures and 40-45 of the rural Chinesepopulations were covered by cooperative medical sys-tems Efforts at increasing the acute shortage of medicalpersonnel and facilities during1984 -1986 and the eco-nomic boom of 1987 in PR China led to fundamentalurban and rural healthcare reforms systems throughprovision of preventive and curative interventions [1718] Recently PR China has launched a national malariaelimination campaign (NMEP) as the cornerstone of asuccessful and intense surveillance and monitoring ofvectors foci disease management and potential out-breaks [17]The design and implementation of policies for malaria

control and elimination in tropical and sub-tropicalareas have been mitigated by the consequences of polit-ical and financial agenda and achievements A clearunderstanding of the interrelations between malaria andthe cross-effects of targeting policies and financing onhealth systems are of valuable importance in sustainabil-ity There are several challenges linked with the scalingup of malaria control interventions with no clear con-sensus and road map on how existing tools should be ef-ficiently and continuously deployed in achieving targetedgoals and eventual elimination although several recentpublications have targeting these issues [3 19-22]In this review therefore we aimed at providing syn-

thetic information with scientific evidence of scaling upimpact of malaria control interventions on the trends ofmalaria events from 1960 to 2011 with the hope that itwill help stakeholders and policy-makers to takeinformed decisions on public health issues and interven-tion designs on malaria control towards elimination inSS Africa and PR China

MethodologySearch strategyA systematic search was conducted for articles publishedfrom January 1960 to December 2011 in PubMedMED-LINE (OVID) (Originally Publius Ovidius Naso) Embase


(OVID) Web of Knowledge Scopus and the WHOrsquosWHOLIS and regional office databases and CAB Directdatabases using terms for malaria events and 49 targetcountries (48 African countries and PR China) Thereferences were collated and categorized according tomalaria Plasmodium species and whether they con-tained original or derivative data The search was limitedto studies with PR China and SS Africa medical subjectheadings (MeSH) term involving interventions epide-miologic and studies on malaria trends of events Allrecords resulting from these searches were screenedand full-text articles were assessed if the referenceappeared to describe or allude to a malaria epidemiccontrol towards elimination event

Inclusion criteriaPublications relating to malaria in these countries withinthe time frame of January 1960 to December 2011 wereassessed Randomized controlled surveys controlled be-fore and after uncontrolled before and after interruptedtime series and cohort and case control studies wereincluded We assessed risk of bias for included studiesbut did not exclude studies on this basis Accordinglyany report of an increase or decrease in malaria inci-dence or prevalence in assessed articles was included inanalysis and included those published in English Frenchor Chinese regardless of article type or quality Also na-tional malaria strategic plans malaria programme per-formance reviews and country led successful fundingapplications to the Global Fund to Fight AIDS Tubercu-losis and Malaria (GFMAT) on malaria were reviewed toexplore how incidence and mortality trends socio-economical and health reforms can be used in planningand decision making for malaria control and eliminationin SS Africa and PR China

Evaluation of publicationsPublication type for each article was derived from thePubMedMedline database and articles were categorizedrelevant to malaria research based on these publicationtypes i) political and financial analysis ii) malaria healthsystem reforms iii) malaria incidence and prevalenceand trends in interventions (vector parasite control)Malaria-related papers in which the Plasmodium specieswas not defined were categorized as neither Publica-tions not meeting the inclusion criteria relevance formalaria were excluded

Data analysisData analysis were processed using Excel (Microsoft WAUSA) and SPSS 130 was also used to compute the statis-tical comparisons percentages and corresponding 95confidence intervals (95 CI) were calculated using Wil-sons method The scaling up impact was evaluated as

cumulative reduction in morbidity and mortality ratesand increasing life expectancy in vulnerable groups to theimplemented malaria control interventions over time

ResultsThe database searches returned 2171 articles and 340additional records were identified from hand-searchingreference lists producing a total of 883 (4067) uniquerecords screened after removal of duplicates Overall131 (1483) were published during 1960 to1990 (30years) compared to an increase of approximately 6 times782 (8516) during 1990 to 2011(21 years) Of these 89described the trend of malaria events that were includedand assessed from SS Africa and PR China during1960ndash2011 Our findings showed three increasing areasof interest First the political and financial commitmentand investments through scaling up of malaria interven-tion coverage programmes (indoor residual spraying(IRS) insecticide-treated mosquito nets (ITNs) longlasting insecticides treated nets (LLINs) and intermit-tent preventive treatment during pregnancy (IPTp) Sec-ond prompt and effective malaria case managementwith antimalarial drugs mainly the artemisinin basedcombination therapies (ACTs) Third strengtheninghealth system performance through increasing capacitybuilding and delivery of malaria interventions sustain-ability and universal coverage have brought about a dra-matic health impact with short and long-term benefitsInterestingly a substantial reduction in morbidity rate aswell as on average more than a 20-58 mortality ratedecrease in all vulnerable groups in most of SS Africacountries compared to 978 in PR China during thelast decade

Malaria political and financial achievements fromepidemic to control and eliminationOur findings showed that since the independence of themajority of African countries around the 1960s withlimited capacities in malaria control and in PR Chinapolitical and financial commitments and strategies havepermitted the achievements of essential milestonesmoving malaria from epidemic towards control andelimination [1 14 23-27] In the last two decades con-trol towards malaria elimination has been on the polit-ical agenda of several of the worldrsquos wealthiest countriesand funds have become available from the GFMAT TheUS Presidentrsquos Malaria Initiative (PMI) the World BankWHO and bilateral donors that are all financial sourcesfor the fight against malaria The RBM Partnership co-ordinating the global fight against malaria and majordonor foundations such as the Bill and Melinda GatesFoundation National Institute of Health (NIH) The Co-ordination Rationalization and Integration of antimalar-ial drug discovery and Development (CRIMALDDI) The


Rockefeller Foundation The Wellcome Trust TheExxonMobil Foundation USAID from the AmericanPeople The Coalition of Global Businesses have greatlyincreased financial support for malaria research and de-velopment as well as interventional approachesWhen analyzing on the basis of incidence and preva-

lence rates the African malaria situation from 1960ndash2000is comparable to that of PR China between 1960ndash1980[4-7 9-29] The scaling up of malaria coverage interven-tions across endemic areas testified the political andfinancial commitment of governments and stakeholdersin achieving the millennium development goals (MDGs)Most African countries that have successfully implemen-ted health policies witnessed an improved and sustainednationwide coverage of malaria control measures andconsequently documented a substantial decline in themorbidity and mortality rates amongst the population atrisk for example South Africa Zanzibar Gambia SenegalTanzania Kenya Ghana and Cameroon) [3 22 30-32]

Comparison of the trends of malaria morbidity andmortality rates from 1960ndash2011Our findings showed that both PR China and Africa arelocated in the tropical and sub-tropics with optimal cli-matic and environmental conditions for the reproductionand development of Anopheles species P falciparum andP vivax were shown to be major causative agents of mal-aria respectively having different degrees of virulenceand similar disease pathophysiology P vivax accounts for80-90 of malaria cases in the Middle East Asia and theWestern Pacific tropical regions 10-15 in Central andSouth America and less than 2 in Northern Africancountries [4 16 27 30] Although the overall burden ofmalaria is higher in Africa than in PR China there isincreasing evidence that the overall burden economicimpact and severity of disease have been underestimated[4 15-27 30-33]Malaria public health burden during the 1960s-1970s

was characterized by an upsurge in terms of malaria in-cidence and mortality rate in PR China as a result of in-creasing population demography and lack of adequatehealth infrastructure to cater for massive remotelylocated rural populations Our findings showed that mal-aria publications from Africa from 1980ndash2000 are simi-lar to those from PR China between 1960-1980s whichwere characterized by a high death toll amongst therisky groups including children under the age of 5 yearsold pregnant women and travelers [7-9 34-36] Severalreasons contributed to the huge toll of mortality includ-ing a higher degree of endemicity post-independence in-stability in most African countries lack of healthinfrastructures and resources poor understanding of thedisease and ecology inability of ldquonaiverdquo leaders to

generate income andor to implement efficient health-care reforms policy [9 12-19 28 29]The era of 1970s-1980s was marked by a significant

reduction in the infectious diseases in PR China includ-ing a drastic fall in malaria incidence (5000permil to 500permil)as a result of mass patriotic and mobilization healthcampaigns on prevention and implementation of birthcontrol in the early 1970s The ravage of malaria in Af-rica was increasingly higher with poverty related effectson the households community and African countries[6 18-27 30-37] With the structural adjustment planproposed to African countries and implemented with thefinancial support of the International Monetary Fundand The World Bank part of the funds were allocatedinto the health sector but several factors contributed tothe ineffectiveness of the plans These included lack ofpolitical commitment inadequate management and lackof much needed infrastructure in rural areas and difficultaccessibility and availability of drugs as well as lack ofqualified medical personnel with chronic pressuremounted on a few healthcare community workers hasremained a huge challenge in some countries [25-27 30-38] Most African countries faced the sorrowful periodwith alarming collision between the vicious cycle of mal-aria and poverty and the impact of the StructuralAdjusted Plan of the International Monetary Fund imple-mented in these countries During the period 1980 ndash1986 PR China registered an increase in morbidity rateto 500 permil reduction of life expectancy (less than 4 years)due to malaria resulting from global economic crisisdread shortage of health personnel and a weakenedChinese rural cooperative medical system However fol-lowing by the PR China economic boom after 1987there was a significant sharp drop of malaria incidencefrom 500permil to 92permil in 1990 This was thought to bebrought about by the tremendous fundamental healthsystem reforms characterized by increasing support tocollective welfare systems provision of adequate prevent-ive and curative health intervention packages throughhealthcare decentralization primary healthcare reformsin 2005 and the basic healthcare with insurance schemes[17-27 30-36] On the basis of these analyses of the trendof events we came to the general conclusion that transla-tions of national policy into innovative control strategiesare imperative in strengthening the healthcare systemsand actions to tackle the persistent burden of infectiousdiseases in most endemic countriesAt the same time the public health burden of malaria has

continued to increase in most African countries due topoor coverage and accessibility to the needed population inremote areas weaker health system and importantly theserious threat of increasing antimalarial drug and insecti-cide resistance as well as an uncoordinated approach at na-tional and regional levels since 1985 [35 39-41] The goals


oriented interventions are urgently needed by Africancountries especially learning from those have successfullyhealth policies coupled with the sustained programmesinterventions with significant reduction of the malaria bur-den through national wide coverage of malaria controlmeasures and has been appraised such as South AfricaZanzibar Gambia Senegal Ethiopia Rwanda Tanzania andMozambique [Please see Additional file 2] [1 2 20-27 3031] However the scaling up impact has not been the same

2

1

0

1

2

3

4

196019651970197519801985199019952000

2

1

0

1

2

3

4

1960 1965 1970 1975 1980 1985 1990 1995 20

0

20

40

60

80

100

120

A

B

Figure 1 a Trend in malaria incidence rate Log10 (110000) in selecteSubstantial Scaling Up Impact on malaria incidence in PR China and someincidence in PR China and lowmoderate outcomes in some African counand life expectancy in selected African countries and PR China in 2011 (C

in all African countries such as The Democratic Republicof Congo (DRC) and Nigeria with a persistent burden ofthe disease [Figures 1a amp 1b]The Chinese governmentrsquos commitment and intensive

interventions towards malaria control and elimination havebeen enhanced by the GFMAT Round 1ndash6 and nationalstrategic applications from 2002ndash2012 decentralization ofCenter for Disease Control and Prevention at all levels na-tionwide since 2000 integrated healthcare systems by

200520102011

Rwanda

Senegal

South Africa

Gambia

China

00 2005 2010 2011

Nigeria

CAR

Cameroon

Ghana

China

Impacton Incidence

Reduction in Mortality Rate

Life expectancy

d African countries and PR China from 1960ndash2011 (Figure iAfrican countries and Figure ii Scaling up impact on malariatries) b Overall Scaling up Impact on incidence and mortality rateAR Central Africa Republic)


broadening health financing options improving functional-ity of the National Ministry of Health improving perform-ance strengthening case reporting and surveillance systemsin rural areas use of IRS coupled with environmental man-agement to reduce vectors breeding in localized hotspotssuch as in Tibet Henan Hubei Jiangsu Guizhou and Yun-nan provinces staff incentives and competition and work-ing with multi-stakeholders research institutions andprivate sectors Consequently an unprecedented fall ofprevalence rate from 01910000 in 2000 to 003510000 in2011 with increasing health system decentralization anddelivery capacity building and life expectancy of plus 30years operating through an efficient information systemnetwork nationwide on malaria surveillance reportingcoverage of 974 [14 27 35-42] As a result of scaling upimpact the Chinese government in 2010 launched the Na-tional Action Plan for Malaria Elimination till 2020 with

196

T

N

P

201

0

ransmissi

o transmi

lanning for

1 Tra

on

ssion

r elimination

ansmission

n or elimina

No t

ating

transmissionn

Figure 2 Malaria distribution worldwide 1960 and 2011 1960 (Red sqsquare) Planning for elimination or eliminating 2011 (Red square) TransmiPlanning for elimination or eliminating Source Malaria Elimination Initiative

the National Guidelines on Malaria Surveillance and Epi-demic Response in alliance with efforts in strengtheninghealth system and capacity building in remote areas by im-proving investment for malaria control and elimination aswell as regional collaboration on networks Similarly varieddegrees of laudable achievements have been made in someproactive African countries committed to the scaling up ofmalaria control interventions resulting in a marked reduc-tion of morbidity and mortality rates amongst the riskgroups and malaria transmission being more focal withsome areas being relatively free such as South Africa Zan-zibar Ethiopia Equatorial Guinea Sao-Tomeacute amp PrincipeGambia Senegal Mozambique Rwanda Tanzania andZambia In contrast Angola Cameroon Gabon CongoBenin Cote drsquoIvoire and Somalia which are still having sub-stantial risk of malaria endemicity The DRC and Nigeriahave made little progress with malaria control intervention

Planning for elimination or eliminating

uare) Transmission (Yellow-green square) No transmission (light-bluession (Yellow-green square) No transmission (light-blue square)(2011) UCSF Global Health Group


programmes possibly due to large population size land-scape inadequacies in health system and health policy [1 2][Figure 2]

Interventional approaches to malaria control towardseliminationSince 1960 malaria control strategies have achieved sub-stantial successes and there are confounding challengessuch as the inadequacies in health systems in countieslack of access to simple and reliable early diagnosisemergence and spread of multidrug resistant parasitesAnopheles vector resistance insecticides factors relatedto environment demographic and socio-economic sta-tus Our findings showed that healthcare systems withefficient National Malaria Control Programmes (NMCP)having adequate national and global support on malariacontrol using integrated strategy including existing earlydiagnosis tools and prompt treatment combined withvector control have shown a significant impact on redu-cing malaria morbidity and mortality ratesThe strategic approaches on malaria control towards

elimination varied from country to country and within set-tings and depended greatly on political commitment andfinancial potentials These approaches have evolved (1)modeling through estimation incidence prevalence and togenerate risk maps for all of the worlds malaria endemicregions (2) prevention through the interruption of trans-mission of the parasite from mosquito vector to humans(and from humans to mosquitoes) and prompt case detec-tion and (3) management to reduce the incidence andprevalence of malaria infections including severe cases inhumans Knowing the burden of malaria in any country isan essential component of public health planning and ac-curately estimating the global burden is essential to moni-tor progress towards the United Nations

Modeling approaches to malaria controlEstimates based on mathematical and statistical methodsare used to classify malaria risk into low to high-trans-mission incidence derive the incidence and prevalencerates cost- effectiveness time trends and funding-research requirements from malaria epidemiology orempirical data [42] But each evaluation model has itsstrengths and weaknesses as well as to highlight areasthat need to be improved to provide better assessmentsand accurate epidemiological data for malaria controland elimination [43 44] For example in 2000 it wasestimated that total of 225 million malaria cases in the99 countries malaria endemic countries - the majority ofcases (78) were in African region followed by theSoutheast Asian (15) and Eastern Mediterraneanregions [45] In Africa there were 214 cases per 1000population compared with 23 per 1000 in the EasternMediterranean region and 19 per 1000 in the Southeast

Asia region [46] Sixteen countries accounted for 80 ofall estimated cases globally The estimate of malaria caseincidence for the African region is 176 (110ndash248) mil-lion cases 261 (241ndash301) million P falciparum cases in2007 and 214 million for year 2011 [47 48] Nowadaysthe best assessment of malaria burden and trends mustrely on a combination of surveillance and survey data Inrecent years mathematical and statistical models havebeen used extensively in forecasting of incidence andmortality rates socio-economic implications in both Af-rica and Asia in increasing stakeholder awareness onthe disease burden and in estimating the cost (invest-ments and cost effectiveness) in control interventionsbased on spatio-temporal ecological and climatic riskfactor modeling as well as in assessing the impact ofinterventions and challenges [49-53]

Preventive measures against malaria controlThese are measures involving vector control interven-tions aimed at reducing transmission and thus decreasethe incidence and prevalence of parasite infection andclinical malaria Prevention with intermittent preventivetreatment for pregnant women reduces the impact ofplacental malaria infection and maternal malaria-associated anemia Early and effective case managementof malaria will shorten its duration and prevent compli-cations and most deaths from malaria [54] Over theyears the preventive measures have been very effectivestrategies in protecting the most vulnerable groupsagainst vector contact and progression of the infectionThe two most powerful and most broadly applied inter-ventions are LLINs [55-58] and indoor residual sprays(IRS) [59] At the same time behaviour change interven-tions including information education communication(IEC) campaigns and post-distribution are also stronglyrecommended [31 55 56] These interventions act byreducing the lifespan of female mosquitoes and by redu-cing human-vector contact In some specific settingsand circumstances these core interventions may becomplemented by other appropriate and highly practicaleffective methods such as larval source control includ-ing environmental management However larval controlis appropriate and advisable only in a minority of set-tings where mosquito breeding sites are few fixed andeasy to indentify to map and to treat in other circum-stances it is very difficult to find a sufficiently high pro-portion of the breeding sites within the fight range ofthe vector [60]Malaria vector control with LLIN IRS or other inter-

ventions is reported to be only effective if high coverageis achieved and requires timely sustained programme ofvector control and effective delivery operations at na-tional provincial and district levels [20 22 27 30 31]In addition practical experiences in delivery vector


control interventions require capacity in monitoringvector-related and operational factors that may com-promise the effectiveness of the intervention Howeverthe spread of insecticide resistance especially pyrethroidresistance in Africa is a major threat requiring a sub-stantial intensification of resistance monitoring withincountry and across borders as well as research into novelinsecticides and larvicides [61 62] Moreover malariavector bionomics and vector distribution maps need tobe updated periodically through vector sentinel sites indifferent ecological and epidemiological risk factors Forexample in Kenya the proportion of malaria outpatientvisits declined from 40 in 2000 to 0 by the end of2006 with the largest decline between 2003 and 2005Coverage with ITNs in the area is estimated to be 65higher than that reported on the Africa coast and 35of households reported use of some mosquito reductionmethod such as environmental management or repel-lents [20 22 27 30-63] Similarly in Rwanda data from20 health facilities representing every district in thecountry showed a decline of more than 50 between2005 and 2007 in both inpatient and outpatient slide-confirmed malaria cases Before 2005 the number ofcases had been increasing annually but began to declineshortly before or at the same time as mass distributionof long-lasting insecticidal bed nets and the use of ACTsduring 2006ndash2010 [20-22]For example the Zambian NMCP has achieved substan-

tial success in scaling up the use of ITNs with sulphadox-ine plus pyrimethamine ITN ownership increasedsubstantially from 22 in 2004 to 38 in 2006 and 62in 2008 Between 2006 and 2008 pediatric malaria parasiteprevalence declined by 53 and moderate to severe an-aemia by 69 [22] In Central Africa an urban hospital inLibreville Gabon reported an 80 decline in the numberof children with positive blood smears in the inpatient andoutpatient services [22 64 65] In West Africa Gambiawhere surveillance at five health facilities across the coun-try showed a 50ndash85 decline in the prevalence of slide-confirmed malaria among outpatients and a 25ndash90decline in malaria-related hospital admissions [23 2830ndash48] The trend persisted over 7 years with an apparentcontribution from ITN coverage which increased three-fold to 49 over the surveillance period Studies in Africahave shown that ITNs can reduce deaths among under-fives by up to one-third [2 20 27 30 31] IRS for ex-ample has been a highly effective method of malariavector control particularly useful for achieving a rapidreduction in transmission during epidemics [54 55]Reports from Burkina Faso mentioned a three-fold in-crease in malaria cases at health facilities between 2000and 2010 in different districts despite increasing bednet coverage [1 60 65 66] In PR China the use ofLLINs in vector control interventions were integrated in

the GFMAT activities in Yunnan Hainan and Guizhouprovinces and IRS was used in localized foci of out-breaks in some endemic provinces with a significant re-duction of vectorial density to over one percent by 2010Efforts are now devoted in combating imported malariaresistance monitoring and containment programs in theGreat Mekong region and surveillance along the ThreeGorges areas of PR China [14-28 30-67] The IPTp userswere documented in most countries for pregnant womenliving in a high transmission setting receiving at least 2doses of an appropriate anti-malarial drug during preg-nancy as well as non-immune travelers [68] Other tar-geted approaches to vector control such as larvicidingenvironmental management community education andmobilization are applied wherever appropriate based onscientific evidence Recently the applications and uses ofGeographic Information Systems (GIS) and RemotesSensing (RS) have been applied in mapping of thespatio-temporal risk factors of malaria in order to pre-dict the impact of control interventions possible out-breaks and monitor the vectorial density in any givenareas [69-72]

Management approaches to malaria control towardseliminationEffective case management using both preventive andcurative stage specific antimalarial drugs to all indivi-duals living in malaria-endemic areas through detectionof and response to malaria epidemics through regulardisease surveillance malaria early warning systems andadequate preparedness plans of action to ensure IRSITNs and antimalarial drugs are rapidly deployed whenneeded Case management has been achieved over theyears both through IPTp in pregnancy and infants at riskof P falciparum infection in countries in Sub-SaharanAfrica and radical treatment with stage specific mono-therapy or combination antimalarial drugs Our findingsdocumented that since the early 1960s the deploymentof chloroquine and sulphadoxine-pyrimethamine as drugsof choice in management of uncomplicated cases andquinine in severe cases across SS Africa and PR Chinasignificantly helped in alleviating malaria mortality rate inAfrica and PR China However the emergence andspread of chloroquine and sulphadoxine-pyrimethamineP falciparum resistance across Africa led to The WHOrecommended policy change to ACTs based on provenefficacy of chloroquine and multidrug resistance andtolerability [11 16 30 73-75] With the past trend ofemergence and threat of the spread of antimalarial drugresistance in the Great Mekong region WHO recom-mended that in PR China both chloroquine and Dihy-droartemisinin plus Piperaquine But to also includeanother 3 ACTs recommended in PR Chinarsquos malariacontrol guidelines that are first line effective drugs for


the treatment of uncomplicated P vivax and P falcip-arum malaria which should be combined with a 14-daycourse of primaquine for the treatment of P vivax mal-aria in order to prevent relapses (particularly as a compo-nent of a pre-elimination or an elimination programme)provided the risks of haemolysis in patients with glucose-6-phosphate dehydrogenase (G6PD) deficiency have beenanalyzed respectively [1-12 28 29] Nevertheless chal-lenges in some African countries include inefficient healthsystems poor healthcare service coverage and deliverysystems and drug shortage counter prescriptions selfmedication fake or counterfeit drugs should be dis-couraged through health education pharmaceuticalregulations against the decreasing susceptibility to ACTs[76 77] Hence the impact of the combined approachesand interventions in malaria control since 1960 to date issummarized below [Figure 1 and Figure 3]

Sustainability of malaria interventions through healthsystems strengtheningStrengthening health systems in reaching and maintaininguniversal coverage both require substantial effortsStrengthening health systems is not only a malaria specificissue rather a global development issue deserving the sup-port of the international donor community [55] TheWHO definition of a health system sums up all organiza-tions institutions people and resources whose primarypurpose is to improve health It requires adequate staff

Figure 3 Malaria parasite endemicity in Africa and PR China 2011

funds information supplies transport logistics commu-nication overall guidance and direction Our findingsshowed that most African countries had overstretchedhealth systems across malaria-endemic areas with malariaaccounting for an average of 25-35 of all outpatientclinic visits and 15-35 fatal cases from all hospitaladmissions the post independence till 1990s as result ofpolitical and financial constraints [45] Efforts in improv-ing health system strengthening have been set up in mostcountries in Sub-Saharan Africa and other endemic areasthrough the RBM and GFMAT support in achieving ofMDGs targets Goal 6 and 8 mainly focusing on the mostvulnerable malaria-risk population promoting effectiveand sustainable malaria control through partnership withgovernmentsMoreover health system strengthening in Sub Sahara

Africa require the following components (i) good leader-ship and governance through strong political commitmentbacking malaria efforts clear definition of policy and fi-nancing frameworks leadership and stewardship from na-tional authorities to lead planning efforts and tocoordinate all partners (ii) sustainable financing and socialprotection through accessibility to adequate and timelyresources for activities planned in ways that ensure popu-lations at risk are covered by the required delivery qualita-tive interventions without bearing undue personal cost(iii) efficient and cost effective tools for malaria preventionand case management available for all populations at risk

Tambo et al Infectious Diseases of poverty 2012 17 0 of 15httpwwwidpjournalcomcontent117

(iv) good healthcare services delivery should be effectivesafe to those that need them when and where neededwith minimum waste of resources (v) timely and reliablehealth information dissemination as well as monitoringand evaluation Malaria control provides an importantplatform on which to base additional efforts to strengthenthese systems [2-78] Interestingly the substantial declinein the last decade in Africa has been as a result of RBMGFMAT PMI and other donors supporting monitoringand forecasting service delivery by integrating the NMCPand strategies and strengthening health systems throughbuilding host country managerial and technical capacityprocurement quality control storage distribution of med-icines and private sector health workers and managers[14 79 80] In the case of Chinese health system supportstructure the Chinese cooperative medical scheme (CMS)was first implemented in rural China in the 1950s reach-ing its peak in 1978 by covering 90 of rural residentsThis helped reduce Chinese mortality rate from infectiousdiseases during the 1960s and 1970s With the collapse ofthe collective economy in the early 1980s most villageslost their collective welfare funds counties then begandropping the program and coverage rates fell sharply from90 in 1980 to 5 in 1985 [18-27 30-37] In 2003 to fur-ther strengthen the national malaria control programmesthe Chinese government launched the national consoli-dated medical service (NCMS) aimed at providing healthcoverage for the nationrsquos entire rural population and theNational Insurance schemes by 2010 [37] These effortssubstantially provide clues that government financial sup-port and decentralized healthcare through Center for Dis-ease Control and Prevention at all levels have been veryimportant as well as funding from the GFMAT Round 15 6 and national strategic applications played a vital rolein strengthening building and sustaining health system ef-ficiency and associated successes that can be derived inmalaria control towards elimination Our findings showedthat there is a crucial need for capacity building to the dis-trict and local level and also outside the traditional malariasystem In addition the National Malaria Control Programshould be entrusted with the responsibilities in capacitybuilding through training healthcare personnel strength-ening of infrastructure using the best practices in evaluat-ing malaria laboratory diagnosis and proper clinical casemanagement of fever and malaria in creating a sustainablenetwork of research activities and contribution to malariacontrol and integrated results of research into policy bylinking health workers researchers and policy-makersdeveloping and maintaining a viable pharmacovigilancesystem for anti-malarial drugs and strengthening malariasurveillance activities establishment and maintenance of asentinel site surveillance network for the provision ofquality data on malaria morbidity and mortality and inte-grated management of malaria (IMM) through learning

policy and practice health (including malaria) interven-tions at all levels In PR China this task has been effect-ively carried out through the support of Chinesegovernment and GFMAT Round 15 6 and nationalstrategic applications [81] whereas such training andtechnical know-how are urgently needed in most en-demic areas in SS Africa Hopefully the growing PRChina-Africa Cooperation through the Africa-PR ChinaScience and Technology Partnership program should in-tensify such opportunities by building capacity supportingcross-bridge between Africa and Chinese scientists andinstitutions to gain from lessons learnt from PR Chinaachievements and successes in moving malaria from epi-demic towards malaria elimination [Figure 1a amp 1b]

DiscussionScaling up impact for universal coverage against malariaThe benefits of malaria control initiated by the GlobalAction Plan programme towards reducing the burden ofthe disease was endorsed by RBM with the main object-ive of increasing accessibility availability and affordabil-ity of malaria control interventions to the mostvulnerable and needy populations living in remote en-demic areas and monitoring groups in forest fringe bor-ders areas [30 32 35 40-42]This review documented that dedicated leadership

momentum proven effective malaria control interven-tions and available resources collectively converged toturn the tide against the malaria public health burdenand its related effects These remarkable global achieve-ments in malaria control have been by the dedicatedcommitment of an array of stakeholders Similarlyacross Africa and PR China functional partnerships be-tween government and other key stakeholders includingthe academic and educational sector non-governmentand community-based organizations the private sectorreligious and faith-based organizations and multi-bilat-eral development partners have proved to be instrumen-tal in malaria control and information disseminationBased on proven evidence of the effectiveness of themalaria interventions key determinants of scaling upimpact shaped interventional policies and mechanismsof effective deployment of the full package with measur-able results in targeted areas [1 20 31 40 41 82 83]Our finding revealed that from 1960 to 2000 the mal-

aria situation across African countries suffered from astate of dormancy in malaria political commitment andfinancial support resulting in an intolerable toll of mal-aria morbidity and mortality rates as reported in 1998[62] with some improvements in the course of 2005 and2010 The alarming scourge was worsened by 2000 bythe emergence and spread of P falciparum chloroquineand sulfadoxine-pyrimethamine resistance and An gam-biense resistance to insecticides mainly pyrethroids [55


73 75-84] however substantial improvements in scalingup interventions was accentuated from 2005 ndash 2010[1-40 83] In PR China the malaria incidence worsened in1965 1970 and the early 1980s as a result of severeshortage in health care personnel the collapse of the co-operative medical system and lack of adequate healthpolicy were further complicated by major hazardscaused by concomitant infectious such as human im-munodeficiency virus infectionacquired immunodefi-ciency syndrome (HIVAIDS) tuberculosis andschisostomiasis However the situation was rapidlyaddressed with the post 1987 health reforms through ex-pansion and improvement of medical facilities andpersonnel decollectivization of agriculture rural health-care system provision of adequate and sustained pre-ventive and curative services thus resulting in an abruptdecline in malaria burden nationwide [Figure 1a and 1b]Accordingly 35 countries in both Africa and South-

East Asia are still harboring higher vectorial capacitywith high transmission of P falciparum and P vivaxmalaria which are responsible for the majority of thetotal deaths worldwide The major contributors (NigeriaDRC Uganda Ethiopia and Tanzania) account for 50of global deaths and 47 of cases [1-3] Myanmar LaosCambodia and New Papua Guinea in South East Asia[28] Accordingly the benefits of scaling up interven-tions documented in the last decade as result ofincreased malaria control interventions varied signifi-cantly across Africa including Eritrea Zanzibar ZambiaGambia and South Africa demonstrated high impactpoint by showing a marked decrease in morbidity andmortality rates compared to other countries within theAfrica continent but still remained less significant com-pared to the achievements in PR China [Supplement1]Nigeria Central Africa Republic (CAR) and DRC hadthe lowest scaling up impact calling for the attention ofboth traditional and also non-traditional donors in gov-ernment and the private sector in increasing commit-ment and funding for accessibility and availability ofcontrol interventions to larger populations in remotesareas and addressing the inadequacies in healthcare ser-vice and delivery [Figure 1b] However achieving themost satisfactory results and maximum health benefitsrequires a sustained scaling up of integrated malariacontrol interventions including prompt and effectivecase management use of impregnated mosquito netsandor indoor spraying with insecticides intermittentpresumptive treatment of most vulnerable groupsThe financing provided for malaria control has

enabled endemic countries to greatly increase healthcaresystems and delivery capabilities to ITNs LLINs andcase management The percentage of households owningat least one ITN in sub-Saharan Africa is estimated tohave risen from 3 in 2000 to 50 in 2011 the number

of rapid diagnostic tests (RDTs) and ACTs procured isincreasing from 67 globally in 2005 to 76 in 2010Reductions in reported malaria cases of more than 50have been recorded between 2000 and 2010 in 43 out of99 countries with ongoing transmission while down-ward trends of 25ndash50 were seen in 8 other countries[1-85] There is documented substantial progress in useof IPTp andor ITNs in pregnant women in 28 coun-tries Similarly there is marked scaling up coverage pro-gress and substantial beneficial impact across a diverserange of African countries such as South Africa Swazi-land Zanzibar Mozambique Eritrea Gambia SenegalRwanda Satildeo Tomeacute and Priacutencipe [20 31 35 53-85][Figure 1a amp 1b] Despite this encouraging progress ourfindings showed that there is a high variability and dis-parity in ITNsLLINs coverage across African countriesover time to endemic population mainly the vulnerablegroups thus indicating that more efforts are needed be-fore the target of universal access is attained For ex-ample in Sierra Leone and Togo the percentage ofchildren under five sleeping under bednets has droppedto lt 50 in 2009 after mass distribution campaigns andwas only 25-30 in 2011 [56-65] The decrease in mal-aria prevalence is consistent with findings from othercountries that high coverage of malaria control interven-tions (mainly ITNs and ACTs) certainly contributed im-portantly to the decrease in population infection rateand consequently the threat of malaria The fact in highcoverage areas 72 of households with an ITN had atleast one person using the net the previous night is en-couraging but also showed that there is still room forimprovement A recent study of 15 standardized na-tional surveys across Africa showed that within ITNowning households ITN usage by children increases asthe number of persons per available net decreases not-ably of the 15 countries included in that study [66][Fig-ure 2] It should be noted in achieving maximum impactdue to variations between countries in epidemiology andmalaria control programs the appropriate interventionsdiffer by transmission levels parasite type and vector be-havior and delivery strategies need to be adapted toexisting control programs and integrated with other dis-ease and development programs by continuously im-proving health systems to enable malaria control scalingup and maintaining universal coverage Particular atten-tion is required to ensure that control interventionsreach the most vulnerable populations and that gendersocio-economic status or geographic location are notbarriers to accessibility availability and affordabilityFurthermore the review documented that both African

countries and a few endemic counties in PR China for ex-ample in Yunnan Hainan and Guizhou provinces haverecorded different degrees of scaling up impact (35-90)through the national malaria control interventions thus


reducing the rate of morbidity and mortality in childrenunder five years old and pregnancy related effects By 1959there were an estimated 158 million cases per year Despitetwo major outbreaks in the 1960s and then in the 1970sthe country saw a steady decrease in the number of casesfrom millions of cases per year to only 29039 reportedcases in 2000 prior the GFMAT This very encouraging re-sult recorded highlight the evidence that sustained commit-ment and efforts on preventive interventions and promptcase management are the major driving forces with theresulting benefits of incremental burden reduction of mal-aria control towards elimination and in achieving theMDGs globally [3 20 32 40 41 58 79 82-85] For ex-ample promising results were obtained after expandedcoverage of malaria interventions principally LLINs reach-ing over 60 coverage of populations at risk in both coun-tries and ACTs in Ethiopia and Rwanda malaria cases inRwanda decreased by 64 and deaths by 66 between2005 and 2007 among children under 5 years And in Ethi-opia cases decreased by 60 and deaths by 51 in thesame age group in the health facilities selected for the study[31] [Figure 2]In PR China the benefits of sustained scaling up

interventions on malaria have led to a dramatic reduc-tion of incidence and prevalence rate from 01910000in 2000 to 003510000 in 2011 respectively The im-measurable benefits include improved health status andlife expectancy increasing productivity social well beingand potential future economic development at nationalregional and international levels [28 67 81-86] whilemost countries in SS Africa would need to toe the samepath for a better outcome of investment in controllingmalaria Our findings have also documented that inad-equate health systems are one of the main obstacles inscaling up interventions and in securing better healthoutcomes for malaria often financial educational andcultural issues are barriers that need to be addressed insurmounting universal uptake of healthcare services inlow resources settings Since the Abuja declaration wasfollowed by the Roll Back Malaria programme the Glo-bal action plan has contributed immensely to the recenthealth improvement in African countries with substan-tial evidence of high achievements through malaria con-trol intervention coverage especially with ITNs targetedIRS and use of ACTs to reduce child mortalityThe immense health and economic benefits of scaling

up coverage interventions in Africa and PR China includereducing morbidity and mortality rates increasing prod-uctivity in the households community and nationwidelowering disability adjusted life years increasing life ex-pectancy improving healthcare service and delivery in-creasing accessibility and availability of infrastructure andadequate equipment and antimalarial drugs provides add-itional evidence required to increase long-term national

and global political commitment and financial fundingwith the ultimate goal that malaria control sustainabilityleads to elimination and global health Moreover controland eventual elimination of human parasitic diseases inthe PR China requires novel approaches particularly inthe areas of diagnostics mathematical modeling monitor-ing evaluation surveillance and public health response[87-89] [Figure 3]

Challenges in malaria research progress towardseliminationThis review acknowledges that researchers are aware ofthe constraints in implementing any new program in-cluding political administrative financial operationalsocial ecological and technical considerations Furtheroperational research challenges will involve dealing withdifferent aspects of sustained malaria control with theaim of bringing different disciplines together to generatenew tools and strategies Some important technical con-straints facing malaria include following five approaches1) appropriateness and effectiveness of the controlinterventions against vectors and parasite susceptibility2) modeling of risk factors of vectors dynamics 3)socio-economical and ecological determinants of mal-aria infections 4) applications of high throughput tech-nologies in molecular marker identification geneticdiversity studies and searching of malaria potentialdrugeable target(s) and candidate vaccine(s) using avail-able high throughput technologies and databanks 5)novel methods of genetic manipulation of P falciparumand Pvivax and metabolomics and a real time surveil-lance response system However tools alone will notprovide all the knowledge needed for sustainable malariacontrol Setting malaria control strategies and criteriafor monitoring and evaluation of malaria hotspot focias well as mapping the risk factors associated with dis-ease using GIS will play a potential role in predictingmalaria epidemics and monitoring controlIt is acknowledged that there were likely to have been

imperfections in comparing the whole African continentmade up of different countries with different political con-texts and health systems as well as different parasites andvector predominance and populations with PR Chinaone single country with its own internal and cross borderchallenges and the inability to assess the progress of on-going malaria control programmes Other potential limita-tions may be in selection bias and misclassification asresearch publications are not always an accurate mirror ofresearch activities evaluation and policy making Highlyrelevant operative research may not be published but areof great value for programmes Furthermore the extent towhich an individual country is associated with a particularpublication may vary widely also in assigning publicationswith unspecified Plasmodium species publication to one


country or subject when multiple countries or subjects areinvolved Also search algorithms targeting the title key-words and abstract were used to identify and assign publi-cations to multiple countries and subjects

ConclusionsThe review provides the evidence that supporting na-tional international political commitment and long-termfinancial investment in sustaining malaria control to-wards elimination Innovative and integrated approachesand interventions can result in significant reductions inP falciparum and P vivax malaria transmission and theassociated disease burden in Africa and elsewhere How-ever the effectiveness of malaria control interventionsmay not be uniform across African countries due to theheterogeneous impact on malaria transmission intensityand others related factors Meanwhile real time inte-grated malaria surveillance response system is urgentlyneeded in PR Chinas NMEP against vulnerability andreceptivity of P vivax Moreover African and Chineseresearchers should enhance efficient collaboration andvaluable exchanges preferably with inputs from govern-ments and international institutionspartners in sharingthe lessons learnt from Chinese experiences in shiftingfrom malaria control to elimination and in promotinginstitutions partnerships towards scientific technologicaland economical development of new health models tar-geting the most vulnerable people towards global health

Additional file

Additional file 1 Multilingual abstracts in the six official workinglanguages of the United Nations

Additional file 2 Trends in the incidence of malaria in selectedAfrica countries and PR China from 1960ndash2011

AbbreviationsLLIMN Long-lasting Insecticide-treated Mosquito Nets LLINs Long-lastingInsecticide-treated Nets ACTs Artemisinin-based Combination TherapiesMOH Ministry of Health IRS Indoor residual spraying IPTp IntermittentPreventive Treatment ITNs Insecticide-treated mosquito netsOAU Organization f Africa Unity IMM Integrated Management of MalariaMDGs Millennium Development Goals CCMS Chinese Cooperative MedicalScheme NCMS National Consolidated Medical Service NMCP NationalMalaria Control Program HMIS Health Management Information ServicesGMEP Global Malaria Eradication Program PMI US Presidentrsquos MalariaInitiative GFMAT Global Fund to Fight AIDS Tuberculosis and MalariaWHO World Health Organization RBM Roll Back Malaria MIMTDR Multilateral Initiatives on Malaria Tropical Diseases and ResearchDRC Democratic Republic of Congo EU European Union US United Statesof America OVID Originally Publius Ovidius Naso WHOLIS World HealthOrganizationrsquos MeSH Medical Subject Heading UN United NationsAPMEN Asian Pacific Malaria Elimination Network UNICEF United NationsInternational Childrens Emergency Fund

Competing interestThe authors declare that they have no competing interests

Authorsrsquo contributionsThe review was conceived and designed by ET papers were retrieved andanalyzed by ET HJ FH SSZ LHT provided supportive information andsuggestions ET and AA contributed to drafting the manuscript and allauthors gave approval of the final version

AcknowledgmentThis work was supported by National Institute of Parasitic Disease ChineseCenter for Disease Control and Prevention Shanghai 200025 Ministry ofScience and Technology Ministry of Human Resources and Social Security ofPR China and PR China Postdoctoral Science Foundation PR China-AfricaSciences and Technology Partnership Program 2011 Thanks to the partialsupport of the Chinese National Science and Technology Major Program(2012ZX10004220) Thanks to Prof Xiao-Nong Zhou for the critical review ofthe manuscript

Author details1National Institute of Parasitic Disease Chinese Center for Disease Controland Prevention WHO Collaborating Centre on Malaria Schisostomiasis andFilariasis Key Laboratory of Parasite and Vector Biology Ministry of Health207 Rui Jin Er Rd Shanghai 200025 Peoplersquos Republic of China 2School ofMedicine amp Pharmacy Houdegbe North American University PK10 Route dePorto-Novo 06 BP 2080 Cotonou Reacutepublique du Beacutenin 3Department ofPharmacology and Toxicology Kampala International University WesternCampus POBox 71 Ishaka Bushenyi Uganda

Received 28 August 2012 Accepted 12 October 2012Published 1 November 2012

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17 Ministry of Health The malaria situation in the Peoplersquos Republic of China1990 in Chinese

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22 Flaxman AD Fullman N Otten MW Jr Menon M Cibulskis RE Marie NChristopher JL M Lim SS Rapid scaling up of insecticide-treated bed netcoverage in Africa and its relationship with development assistance forhealth a systematic synthesis of supply distribution and householdsurvey data PLoS Med 2010 7(8)145ndash151

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26 Akachi Y Atun R Effect of Investment in Malaria Control on ChildMortality in Sub-Saharan Africa in 2002ndash2008 PLoS One 2011 6(6)e21309

27 Tang LH Progress in malaria control in PR China Chin Med J 200011569ndash92

28 Ndugwa Robert P Heribert R Olaf M Momodou J Ali S Bocar K Brian GHeiko B Comparison of all-cause and malaria-specific mortality from twoWest African countries with different malaria transmission patternsMalaria J 2008 715

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35 Murray CJ Rosenfeld LC Lim SS Andrews KG Foreman KJ Haring DFullman N Naghavi M Lozano R Lopez AD Global malaria mortalitybetween 1980 and 2010 a systematic analysis Lancet 2012 379413ndash431

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40 OMeara WP Mangeni JN Steketee RW Greenwood B Changes in theburden of malaria in sub-Saharan Africa Lancet Infect Dis 201010545ndash555

41 Kleinschmidt I Schwabe C Benavente L Torrez M Ridl FC Segura JL EhmerP Nchama GN Marked increase in child survival after four years ofintensive malaria control Am J Trop Med Hyg 2009 80882ndash888

42 Liu J Yang B Cheung W Yang GJ Modelling Malaria Diffusion Patterns ANetwork Perspective Inf Dis Poverty 2012 1(1)11

43 Snow RW Craig MH Deichmann U le Sueur D A preliminary continentalrisk map for malaria mortality among African children among childrenaged 0ndash4 years Parasitol Today 1999 399ndash104

44 Smith DL Hay SI Noor AM Snow RW Predicting changing malaria riskafter expanded insecticide-treated net coverage in Africa Trends Parasitol2009 25511ndash516

45 Sharp BL Kleinschmidt I Streat E Maharaj R Barnes KI Durrheim DN RidlFC Morris N Seocharan I Kunene S La Grange JJ Mthembu JD Maartens FMartin CL Barreto A Seven years of regional malaria controlcollaborationndashMozambique South Africa and Swaziland Am J Trop MedHyg 2007 7642ndash47

46 World Health Organisation Malaria disease burden in South East Asia RegionhttpwwwsearowhointENSection10Section21Section340_4018htmaccessed on April 24 2012

47 Cibulskis RE Aregawi M Williams R Otten M Dye C Worldwide Incidenceof Malaria in 2009 Estimates Time Trends and a Critique of MethodsPLoS Med 2011 12e1001142

48 WHO World Malaria Report 2011 httpwwwwhointmalariaworld_malaria_report 2011enindexhtml accessed on April 24 2012

49 Hay SI Guerra CA Tatem AJ Noor AM Snow RW The global distributionand population at risk of malaria past present and future Lancet InfectDis 2004 4327ndash336

50 Griffin JT Hollingsworth TD Okell LC Churcher TS White M Wes H Teun BDrakeley CJ Ferguson NM Mariacutea-Gloria B Ghani AC Reducing Plasmodiumfalciparum malaria transmission in Africa a model-based evaluation ofintervention strategies PLoS Med 2010 7e1000324

51 Fang H Shuisen Z Shaosen Z Hongwei Z Weidong L Meteorologicalfactorsndashbased spatio-temporal mapping and predicting malaria inCentral PR China Am J Trop Med Hyg 2011 85560ndash567

52 Zhou SS Fang H Wang JJ Zhang SS Su YP Tang LH Malaria J Malaria J2010 9337

53 Okell LC Lucy Smith P Jayne W Kara H Jo L From intervention to impactmodelling the potential mortality impact achievable by different longlasting insecticide-treated net delivery strategies Malaria J 2012 11327

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55 Korenromp EL Williams BG Eleanor G Christopher D Snow RWMeasurement of trends in childhood malaria mortality in Africa anassessment of progress toward targets based on verbal autopsy Lancet2003 3349ndash358

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58 Roll Back Malaria Partnership Partnership Malaria funding amp resourceutilization the first decade of Roll Back Malaria Progress amp Impact SeriesVolume 1 2010

59 Snow RW Trape J-F Marsh K The past present and future of childhoodmalaria mortality in Africa Trends Parasitol 2001 17593ndash597

60 MARA Mapping Malaria Risk in Africa [wwwmaraorgzahomeaccessedon April 24 2012]

61 Tour0e YT Oduola AMJ Morel CM The Anopheles gambiae genome nextsteps for malaria vector control Trends Parasitol 2012 20142ndash149

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63 Sachs G An economic analysis indicates that the burden of malaria isgreat In report of the African Summit on Roll Back Malaria Abuja WorldHeath Organization 2000

64 Naacutejera JA Gonzaacutelez-Silva M Alonso PL Some lessons for the future fromthe global malaria eradication programme (1955ndash1969) PLoS Med 20118e1000412

65 WHO Targets for Malaria Control Geneva World Health Organization 2010


66 Noor AM Mutheu JJ Tatem AJ Hay SI Snow RW Insecticide-treated netcoverage in Africamapping progress in 2000ndash07 Lancet 2009 37358ndash67

67 Ministry of Health Malaria Surveillance Project in PR China Beijing 2005 inChinese

68 Steketee RW Eisele TP Is the scale up of malaria intervention coveragealso achieving equity PLoS One 2009 4(12)e8409

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72 Yan Z Qiyong L Rongsheng L Xiaobo L Guangchao Z Jingyi J HongshengL Zhifang L Spatial-temporal analysis of malaria and the effect ofenvironmental factors on its incidence in Yongcheng PR China 2006ndash2010 BMC Public Health 2012 12544

73 Djimde A Ogbobara K Doumbo MD Cortese JF Kayentao K Doumbo SDiourte Y Dicko A Su X Nomura T Fidock DA Wellems T Christopher P Amolecular marker for chloroquine resistant falciparum malaria New Eng JMed 2001 344257ndash263

74 Gbotosho GO Sowunmi A Happi CT Okuboyejo TM Therapeutic efficaciesof artemisinin-based combination therapies in Nigerian children withuncomplicated falciparum malaria during five years of adoption as first-line treatments Am J Trop Med Hyg 2011 84936ndash943

75 The maIERA Consultative Group on Drugs A research agenda for malariaeradication drugs PLoS Med 2011 8e1000402

76 Sibley CH Barnes KI Watkins WM Plowe CV A network to monitorantimalarial drug resistance a plan for moving forward Trends Parasitol2008 24(1)43ndash48

77 Lourens C Watkins WM Barnes KI Sibley CH Guerin PJ White NJLindegardh N Implementation of a reference standard and proficiencytesting programme by the World Wide Antimalarial Resistance Network(WWARN) Malaria J 2010 9375

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79 Otten M Aregawi M Were W Karema C Medin A Bekele W Jima D GausiK Komatsu R Korenromp E Low-Beer D Grabowsky M Initial evidence ofreduction of malaria cases and deaths in Rwanda and Ethiopia due torapid scale-up of malaria prevention and treatment Malaria J 2009 814

80 Webster J Kweku M Dedzo M Tinkorang K Bruce J Lines J ChandramohanD Hanson K Evaluating delivery systems complex evaluations andplausibility inference Am J Trop Med Hyg 2010 82672ndash677

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84 Plowe C Monitoring antimalarial drug resistance making the most ofthe tools at hand J Exp Biol 2003 2063745ndash3752

85 Snow RW Amratia P Kabaria CW Noor AM Marsh K The ChangingLimits and Incidence of Malaria in Africa 1939ndash2009 Adv Parasitol2012 78435ndash446

86 Okell LC Drakeley CJ Bousema T Whitty CJ Ghani AC Modelling theimpact of artemisinin combination therapy and long-acting treatmentson malaria transmission intensity PLoS Med 2008 5e226

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88 Sinka ME Bangs MJ Sylvie M Theeraphap C Patil AP Temperley WHGething PW Iqbal RFE Kabaria CW Harbach RE Hay SI The dominantAnopheles vectors of human malaria in the Asia-Pacific regionoccurrence data distribution maps and bionomic preacutecis Parasit Vectors2011 489

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doi1011862049-9957-1-7Cite this article as Tambo et al Scaling up impact of malaria controlprogrammes a tale of events in Sub-Saharan Africa and PeoplersquosRepublic of China Infectious Diseases of poverty 2012 17

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Abstract

Multilingual abstracts

Review

Background

Methodology

Search strategy

Inclusion criteria

Evaluation of publications

Data analysis

Results

Malaria political and financial achievements from epidemic to control and elimination

Comparison of the trends of malaria morbidity and mortality rates from 1960ampndash2011

Interventional approaches to malaria control towards elimination

Modeling approaches to malaria control

Preventive measures against malaria control

Management approaches to malaria control towards elimination

Sustainability of malaria interventions through health systems strengthening

Discussion

Scaling up impact for universal coverage against malaria

Challenges in malaria research progress towards elimination

Conclusions

Additional file

Abbreviations

Competing interest

Authorsrsquo contributions

Acknowledgment

Author details

References

Tambo et al Infectious Diseases of poverty 2012 17 of 15httpwwwidpjournalcomcontent117

BackgroundThere has been improvement in the health situation inmost African countries since 1960 and malaria in par-ticular is decreasing over time in SS Africa where theglobal burden of the disease is significantly approxi-mately 90 and PR China accounts for less than 10The recent statistics showing reductions in malariadeaths are very encouraging but the situation is fragileand malaria should not be allowed to resurge [1-3] Mal-aria is a vector-borne disease caused by protozoan para-sites ie Plasmodium falciparum P vivax P malariaeP ovale or P knowlesi that completes a complex cycleof development alternating between human hosts andmosquitoes of the genus Anopheles [4] The diseaseemerged as a worldwide epidemic in the 1960s whenglobal malaria eradication was abandoned [5 6] Conse-quently the emergence of insecticide resistant and drugresistant parasite strains and vectors were greatly fuelledby poverty poor economy political instability poorhealth infrastructure and equipment deficiencies inhealth systems and policy particularly in Africa [4 7 8]The public burden and impact of this disease on humanhealth productivity loss of work efficiency and time inmalarial regions have been devastating [9]To strengthen the efforts towards the fight against

malaria the World Health Assembly passed a resolutionon controlling malaria in Africa in May 1996 and thiswas closely followed by declarations of the Organizationof African Unity(OAU) on malaria in Harare Zimbabwein 1997 and Ouagadougou Burkina Faso in 1998 [10] In1996 the African Regional Office of the World HealthOrganization (WHO) became increasingly attentive tomalaria and launched the African Initiative for MalariaControl (AIM) The AIM contributed $9 million in 1997and 1998 for accelerated implementation of malariacontrol activities in 10 countries in the region and pro-vided the foundation for the eventual launch of RollBack Malaria (RBM) in 1998 [11] The African Heads ofStates Summit to Roll Back Malaria was held in April2000 in Abuja Nigeria where they set the goal for redu-cing malaria deaths to half by the year 2010 The diversearray of meetings programmes and activities are testi-mony to the growing recognition of the regional andglobal nature of the threat posed by malaria [11-13]Strong political commitment financial support and part-nerships are important to bring about the currentdesired changes Malaria re-emerged as a major inter-national health issue in the 1990s despite the globalmalaria control strategy adopted in 1992 RBM in 1998Abuja Declaration in 2000 and strong political commit-ment and partnership respectively In the face of thesemalaria is still prevalent in 106 countries of the tropicaland sub-tropical world with 51 countries in the Africancontinent bearing the highest burden of cases and deaths

[2 9 14-16] No experts from SS Africa were involved inthe Global Malaria Eradication Program (GMEP) due tothe lack of African expertise at that time the majority ofAfrican countries were driven by representatives of west-ern countries taking decisions on their behalf in inter-national forums in addition to socio-cultural beliefs ahigh degree of malaria endemicity in the region com-bined with lack or weak health policy and infrastruc-tures and others factorsIn PR China mass patriotic health campaigns and

mass mobilization approaches on preventive efforts in1960s led to eradication of cholera plague scarlet fevertyphoid and syphilis with a considerable reduction of theburden of infectious diseases [4 17 18] Within thesame period the Chinese government had implementedbirth control measures and 40-45 of the rural Chinesepopulations were covered by cooperative medical sys-tems Efforts at increasing the acute shortage of medicalpersonnel and facilities during1984 -1986 and the eco-nomic boom of 1987 in PR China led to fundamentalurban and rural healthcare reforms systems throughprovision of preventive and curative interventions [1718] Recently PR China has launched a national malariaelimination campaign (NMEP) as the cornerstone of asuccessful and intense surveillance and monitoring ofvectors foci disease management and potential out-breaks [17]The design and implementation of policies for malaria

control and elimination in tropical and sub-tropicalareas have been mitigated by the consequences of polit-ical and financial agenda and achievements A clearunderstanding of the interrelations between malaria andthe cross-effects of targeting policies and financing onhealth systems are of valuable importance in sustainabil-ity There are several challenges linked with the scalingup of malaria control interventions with no clear con-sensus and road map on how existing tools should be ef-ficiently and continuously deployed in achieving targetedgoals and eventual elimination although several recentpublications have targeting these issues [3 19-22]In this review therefore we aimed at providing syn-

thetic information with scientific evidence of scaling upimpact of malaria control interventions on the trends ofmalaria events from 1960 to 2011 with the hope that itwill help stakeholders and policy-makers to takeinformed decisions on public health issues and interven-tion designs on malaria control towards elimination inSS Africa and PR China

MethodologySearch strategyA systematic search was conducted for articles publishedfrom January 1960 to December 2011 in PubMedMED-LINE (OVID) (Originally Publius Ovidius Naso) Embase



















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Review

Background

Methodology

Search strategy

Inclusion criteria


Data analysis

Results








Discussion



Conclusions

Additional file

Abbreviations

Competing interest


Acknowledgment

Author details

References



















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Review

Background

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Results








Discussion



Conclusions

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Abbreviations

Competing interest


Acknowledgment

Author details

References



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Review

Background

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Data analysis

Results








Discussion



Conclusions

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Abbreviations

Competing interest


Acknowledgment

Author details

References










































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Background

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Data analysis

Results








Discussion



Conclusions

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Data analysis

Results








Discussion



Conclusions

Additional file

Abbreviations

Competing interest


Acknowledgment

Author details

References

SCOPING REVIEW Open Access Scaling up impact of malaria ...Scaling up impact of malaria control...

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