When they don't bite, we smell money: understanding malaria bednet misuse.

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by  HONJO, KEITA

580
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When they don t bite, we smell money: understanding
malaria bednet misuse
KEITA HONJO1†, LUIS FERNANDO CHAVES1,2*†, AKIKO SATAKE1,
AKIRA KANEKO3,4,5 andNOBORU MINAKAWA5
1GraduateSchoolofEnvironmentalSciences,HokkaidoUniversity,Sapporo060-0810,Japan
2ProgramadeInvestigaciónenEnfermedadesTropicales,EscueladeMedicinaVeterinaria,UniversidadNacional,
Heredia,CostaRica
3IslandMalariaGroup,DepartmentofMicrobiology,TumorandCellBiology,KarolinskaInstitutet,17177Stockholm,
Sweden
4SchoolofMedicine,DepartmentofMedicalZoology,OsakaCityUniversity,Osaka545-8585,Japan
5InstituteofTropicalMedicine(NEKKEN)NagasakiUniversityandGlobalCOEProgram,1-12-4Sakamoto,
Nagasaki852-8523,Japan
(Received10September2012;revised6November2012;accepted7November2012;firstpublishedonline24January2013)
SUMMARY
Insecticide-treated nets (ITNs) are a major tool to control malaria. Over recent years increased ITN coverage has been
associatedwithdecreasedmalariatransmission.However,ITN‘misuse’hasbeenincreasinglyreportedandwhetherthis
emergentbehaviourposesathreattosuccessfulmalariacontrolandeliminationisanopenquestion.Here,weuseagame
theorymathematicalmodeltounderstandthepossiblerolesofpovertyandmalariainfectionprotectionbyindividualand
emerging‘communityeffects’onthe‘misuse’ofmalariabednets.Wecomparemodelpredictionswithdatafromourstudiesin
LakeVictoriaIslands(LVI),KenyaandAneityum,Vanuatu.OurmodelshowsthatalternativeITNuseislikelytoemergein
impoverishedpopulationsandcouldbeexacerbatedifITNsbecomeineffectiveorwhenlarge‘communityeffects’emerge.
OurmodelpredictedpatternsofITNusesimilartotheobservedinLVI,where‘misuse’iscommonandthehighITNusein
Aneityum,morethan20yearsaftermalariaeliminationin1990.WethinkthatobserveddifferencesinITNusemaybeshaped
bydifferentdegreesofeconomicandsocialdevelopment,andeducationalcomponentsoftheAneityumelimination,where
traditional cooperative attitudes were strengthened with the malaria elimination intervention and post-elimination
surveillance.
Keywords:Plasmodium,poverty,Paretoequilibrium,Nashequilibrium,insecticidetreatednets,Kenya,Vanuatu.
INTRODUCTION toobtaintheITNs(Tamietal.2006).Forinstance,
newlydistributedLLINsareoftenpatchedtogether
The Roll Back Malaria initiative (RBM) was
to makea large seine net (Fig. 1A), as old ones with
launched in 1998 to tackle malaria, a disease with
holes are not effective for drying (Fig. 1B) and
3·2 billion people at risk of infection worldwide
capturing fish (Fig. 1C) in fishing villages because
(World Health Organization, 2000). In 2000,
ofthenetstrength(Minakawaetal.2008).Protecting
African countries committed to providing proper
plant crops (Fig. 1D) or granaries (Fig. 1E) with
treatmentandinsecticide-treatednets(ITNs,which
ITNs are becoming increasingly popular. Residents
are primarily bednets) to at least 60% of the highest
arenowawareoftheinsecticidalandrepellanteffects
malaria risk population by 2005, a goal raised to
of ITNs on crop pests. It is unclear how widely
80% by 2010 (RBM-Partnership, 2005). The mass
ITNs are used for other purposes, besides the plain
ITN distribution campaign significantly reduced
misuse, e.g. as a sleeping mat (Fig. 1F), and a
malaria-related morbidity and mortality (Lindblade
question remains as to whether this phenomenon
et al. 2004; Fegan et al. 2007; O’Meara et al. 2008),
hampers the ongoing efforts to reduce malaria
and further scaling up ITN coverage is ongoing.
transmission(Eiseleetal.2011).
However,somestudies(Minakawaetal.2008;Lover
Community effects may reduce transmission risk
etal.2011;O’Mearaetal.2011;Pulfordetal.2011)
for people employing ITNs for purposes other than
havereportedITNmisuseasapotentialexplanation
mosquito bite protection. For example, if some
for partial success to increase net coverage, or the
residents sleep under ITNs, in a proportion large
misuse of means, for example subsidized vouchers,
enoughtosignificantlydecreasemosquitoabundance
(Howardetal.2000;Hawleyetal.2003),thatfraction
* Corresponding author: Graduate School of Environ- of ITNs used for malaria prevention can shield all
mental Sciences, Hokkaido University, Suite A701,
individualsinacommunityindependentlyoftheuse
Kita-10, Nishi-5, Kita-Ku, Sapporo, Hokkai-do, 060-
givenbyanindividualtohis/herpersonal/household
0810Japan.Tel: [phone].Fax: [phone].
E-mail:[email protected] ITN(s). The income generated by alternative
† Theseauthorscontributedequallytothemanuscript. ITN use may further reduce the risk of malaria
Parasitology(2013),140,580–586. ©CambridgeUniversityPress2013.TheonlineversionofthisarticleispublishedwithinanOpen
Access environment subject to the conditions of the Creative Commons Attribution-NonCommercial-ShareAlike licence <http://
creativecommons.org/licenses/by-nc-sa/3.0/>.ThewrittenpermissionofCambridgeUniversityPressmustbeobtainedforcommercialre-use.
doi:10.1017/S0031182012002077
Ismalariabednet‘misuse’irrational? 581
Fig.1. ExamplesofalternativeITNuses.(A)Sewingbednetstocreatelargernets.(B)Dryingfish.(C)Fishing.
(D)Cropprotection.(E)Granaryprotection.(F)Sleepingmat.
transmission or morbidity and mortality if the using/misusing an ITN, i.e. a mathematical set of
income is used for malaria and other infectious formulaethatareanalysedtooptimizetheindividual
disease treatment, housing improvement and socio- (Nash equilibrium) and collective (Pareto equili-
economic mobility, all factors associated with the brium)rewards.Wethenusethemodeltoexplorethe
reductionofmalariarisk(IjumbaandLindsay,2001; economic rationality behind alternative ITN use.
Lindsay and Birley, 2004; Chaves and Koenraadt, Throughthemodelpresentationwewillusetheterm
2010). Game theory, a conceptual framework player to refer to the residents’ use strategy in a
widely used to understand behaviour in economics malaria-endemicareawithfreelyavailableITNs.
(Nash, 1950; Karlin, 1959) and ecological and
evolutionarycontexts(SmithandPrice,1973)offers
Data
modelling tools to understand the emergence of
alternative ITN use by rendering an optimization To test model predictions we used data on parasite
between the benefits and risks of different ITN use. rates (PR) and ITN use for malaria protection
Game models allow the optimization of a player (ITNMP) from Aneityum, Vanuatu and Lake
strategy reward through the derivation of Nash Victoria Islands (LVI), Kenya. For the analysis we
equilibria (Nash, 1950) and also the optimization of used (PR) based on blood slide examination, which
the public welfare by combining the strategies of all were about 1/3 of the estimates with a rapid
playersinParetoequilibria(Karlin,1959).Here,we diagnostic test (RDT). Per cent ITNMP was based
introduce a two-player game to understand the on ITN self-reported usage by residents, corrected
emergence of alternative ITN use. In the game, by the percentage of the population covered with
each of the two players uses or misuses its ITN for ITNs(seeTable1forfurtherdetailsaboutcoverage,
malariapreventiontooptimizeitsownpayoff,which useandPRsusingBSEandRDT).
we measure as an economic reward. In the model
we assume that proper ITN use decreases malaria Ethicalapproval
infection probability, while alternative ITN use
This study was approved by the Vanuatu Depart-
increases labour productivity (e.g. income in US $
ment of Health, the Scientific Steering Committee
percapita).WederivetheNashandParetoequilibria
and National Ethics Review Committee of the
to evaluate the individual and social impact of a
Kenya Medical Research Institute (SSC No. 1310
player strategy. From the distribution of Pareto
and 2131), and the ethics review committee of
efficient Nash equilibria in the ITN use game, we
NagasakiUniversity.
found that alternative ITN use can optimize each
player reward and public welfare simultaneously
which we further illustratewith numerical solutions Expectedpayoffmatrix
toourmodelandfielddatafromKenyaandVanuatu. The expected payoff matrix represents the set of
strategiesandrewards(commonlyreferredaspayoffs
inthegametheoryliterature)thatplayerscanemploy
THEMODEL
regardinga behaviour ina game model.In theITN
In the next lines we define a 2-player (which can game, the 2 players have a common set of strategies
be also understood as a two strategy) ITN use denoted by T and F, which correspond to ITN
game. First we define an expected payoff matrix for malariaprotectionuseandmisuse,respectively.Each
KeitaHonjoandothers 582
Table1. Insecticide-treatednet (ITN)self-reporteduse,coverageandmalariaparasiteratesinAneytium,
Vanuatuandislands(Nghode,Takawiri,Kibougi,Mfangano)inLakeVictoria,Kenya
Parasite
Population rate(per100 ITN ITN
Location Year Month surveyed* individuals)a coverageb usec
Aneityum19 1991 Januaryd 446 23(NA) 0 na
Aneityum19 1991 October/Novembere 773 0·004(NA) 94 90
Aneityum 2010 July 1123 0(0) 100 97
Nghode 2012 February 331 5(17) 81 59
Takawiri 2012 February 601 4(15) 79 65
Kibougi 2012 February 130 9(25) 73 71
Mfangano 2012 February 890 23(49) 78 50
* Allsurveyssampledrepresentativelythedemographicprofileoftheislands.
a Thevalueoutsidetheparenthesesistheestimatebasedonbloodslideexamination,thevalueinsidetheparenthesesisthe
estimatebasedonaRapidDiagnostictest(Paracheck-Pf®)andnaindicatesnotavailable.
b %populationowningabednet.
c %populationusingbednetsindependentofcoverage.
d Pre-eliminationbaselinesurvey.
e Post-eliminationbaselinesurvey.
player chooses a strategy (T or F) based on his/her
malaria infection risk, labour productivity, and
expected payoff. Thus, the ITN game can have
4 profiles, which result from the combination of
thestrategiesbythe2players:(T,T),(T,F),(F,T)
and(F,F).
The relation between the ITN game profiles and
the malaria infection risk can be represented by an
infection probability (IP) matrix (Fig. 2A). In this
matrix we define an IP P, which can take any value
between0and1(i.e.15P50).Pcanbeinterpreted
as the probability of malaria infection by an in-
dividual in the setting where she/he resides. To
maketheconnectionwithepidemiologicalliterature,
Pcouldbeseenasafunctionofmalariainfectionrisk
factors, i.e. the higher the odds of an individual
being infected, the higher the value of P. The use
of an ITN by a player is assumed to reduce the
individualprobabilityofinfectionbyα ,asobserved
1
in numerous studies (Howard et al. 2000; Hawley
etal.2003;Lindbladeetal.2004;Feganetal.2007),
and the use of ITNs by other residents in the
Fig.2. DerivinganexpectedpayoffmatrixfortheITN
community can lead to an emergent ‘community
usegame.(A)Infectionprobability(IP)matrix.Pisthe
effect’ (Howard et al. 2000; Kaneko et al. 2000;
malariainfectionprobabilityoftheplayersintheabsence
Hawley et al. 2003; Fegan et al. 2007; Chaves et al. ofITNs.Theparametersα andα denotetheindividual
2008)thatfurtherreducesPbyafactor(α2)n,wheren andcommunityeffectsofIT1Nuse2formalariaprotection,
isthenumberofplayersthatusetheITNformalaria respectively.Toreadthisandthesubsequentmatrices
prevention. Thus, the ‘community effect’ is null thestrategyofplayer1ispresentedintherows,andof
whennoplayersusebednetsandthemagnitudeofits player2inthecolumns.Thematrixvalueforplayer1is
impactincreasesasmoreindividualsusetheITNsfor thefirstentryinagivencell.(B)Labourproductivity
malaria prevention. The α parameters can take any matrix.Listhelabourproductivity(whichcanbemeasured
valueabove0andbelow1(i.e.0<α <1,i=1,2).We inUS$percapita)oftheplayerswithoutanITN,Lcan
canthendefinealabourproductivityimatrix(Fig.2B) takeanypositivevalue(i.e.L>0).Theparameterβdenotes
theβ-foldincrementofLwhenaplayergivesanalternative
that quantifies the utility of labour in malaria
usetohis/herITN,βisassumedtobelargerthan1
uninfected players, L, and the increased utility β by (i.e.β>1).(C)Expectedpayoffmatrix.Thismatrixisthe
using bednets for alternative purposes to malaria
Hadamardproduct(i.e.matrix-element-wiseproduct)
prevention. Finally, with these two matrices we can ofthecomplementoftheIPmatrix(i.e.1–IPmatrix)
define the expected payoff matrix (Fig. 2C) as the andtheLabourproductivitymatrixforeachplayer.
Ismalariabednet‘misuse’irrational? 583
productoftheprobabilityofnotbeinginfectedwith DistributionofParetoequilibria
malaria (1-probability of malaria infection) and the
A Pareto equilibrium is a combination of player
labour utility. The model assumes a perfect knowl-
payoffsthatisefficientforthepublicwelfare(Karlin,
edgeofthecostsandbenefitsfordifferentITNuses.
1959), in the context of this study meaning it
The 2-player model has the advantage of rendering
conduces to a reduction of malaria infection risk
generalresultsindependentlyofwhethertheimpacts
in a community. To find the Pareto equilibria we
of ITN use for malaria protection are density
solved several inequalities comparing the different
or frequency dependent, since results for small n
profiles of the ITN game (see Supplementary
are independent of density/frequency-dependent
material, online version only, for a detailed and
pathogen transmission (Antonovicsetal. 1995) and,
mathematically rigorous derivation). Our analysis
ingeneral,2-playergames areusefultoolstounder-
showedtheNashequilibriatobeParetoefficientwith
stand the emergence of different behaviours in a
the exception of the equilibria for the profile (F,F),
population(SmithandPrice,1973).
wherearegionwithasocialdilemma(SD),i.e.where
the whole community benefits by a player changing
his/herstrategy,emergeswhen:
DistributionofNashequilibria
β−1
Nash equilibria are the profiles (combination of P∗ = . (5)
L β−α α2
player strategies) from which any player has no 1 2
incentive to deviate, because his/her payoff is Bydefinition,P*<P ,isthedifferencebetweenthese
L L
maximized in response to the other player strategy twothresholdsdefiningtherangeofmalariainfection
(Nash,1950;SmithandPrice,1973).Ourmodelhas probabilityoverwhichaSDemerges,andisexpected
3 Nash equilibria that were derived by establishing to be wider as the number of players increases in a
the conditions when given a profile, none of the community(Nash,1950).
players can increase his/her payoff by changing
his/herstrategy.Forexample,inthecaseoftheprofile
Modelimplications
(T,T), i.e. when both players use their ITNs for
malaria prevention we have that (T,T) is a Nash Our model can be used to illustrate the influence of
equilibriumwhenthefollowinginequalityholds: many factors that may underpin patterns of ITN
(1−α (α )2P)L.(1−α P)βL. (1) misuse. Malaria is a disease entrenched among
1 2 2
the poorest nations in the globe (Chaves and
This implies a higher payoffforany player if he/she
Koenraadt, 2010) and the alternative use of ITNs
uses the ITN for malaria prevention than if he/she could represent a significant increase in a household
chooses to profit from an alternative ITN use. Here
income. Figure 3A illustrates how the range of
itisworthhighlightingthatpayoffsareindependent
malaria infection probability (P) where all players
of labour productivity (L), which cancels out on
prefer to use ITNs for purposes other than malaria
bothsidesofEquation(1).Nevertheless,payoffsare
protection doubles its width when a 20% increase in
proportionaltotheincrease(β)ofLbythealternative
the player income is derived by an alternative ITN
ITNuse.Fromexpression(1)athresholdforIP(PR) use,afigurethatmayberealisticforthepoorestofthe
can be derived which ensures that both players will
poor in many developing nations. This is the case
usetheirITNsformalariapreventionwhenP>P :
R even when assuming that ITN use reduces by 40%
β−1 (i.e. α =0·60, e.g. see Killeen et al. (2007)) the
P = . (2) 1
R α (β−α α ) probability of malaria infection, a value within
2 1 2
the range of observed outcomes for ITN trials
Following a similar procedure, P , an IP threshold
L (Lindblade et al. 2004). The free-rider behaviour is
where (F,F), both players giving alternative uses to
expected to become increasingly common as the
theirITNs,isaNashEquilibriumwhenP<PL,can ‘community effect’ increases (Fig. 3B and C), in an
bederived:
exacerbated manner as the protection level by
P =α P . (3) individual ITN use diminishes (i.e. α increasing
L 2 R 1
towards1,Fig.3C).
Finally, the profiles (T,F) and (F,T) are Nash
equilibriawhenPfollowsthefollowingcondition:
P 4P4P . (4) ITNuseandparasiterates(PR)inVanuatu
L R
andKenyaislands,dotheyfollowthemodel?
Equation (4) implies the emergence of ‘free rider’
Nash equilibria, where a player with the strategy F Table1showsdatafrommalariasurveysmadebefore
benefits from the alternative use of his/her ITN (PRE) and after (POST) the 1991 elimination
and from the ‘community effect’ in malaria protec- intervention, and 2010, in Aneityum (a Vanuatu
tion that emerges by the use of ITNs for malaria island) and from 2012 in several LVI (Ngodhe,
preventionbyaplayerwiththestrategyT. Takawiri,Kibuogi,Mfangano).InAneityum,before
KeitaHonjoandothers 584
(A) thepatternsobservedinVanuatuundertheassump-
tion of β > 1. The situation in LVI reflects a higher
coverage and use of ITNs than that observed in
Aneityumpriortotheeliminationtrials(Table1),yet
misusemaybehigher,sincearound20%oftheITNs
are not being used for malaria protection (Table 1),
andonlyaround50%ofthepopulationuseITNsfor
malaria protection. ITN use patterns in LVI
resembleourmodelpredictionswhenβ>1.
(B)
DISCUSSION
OurmodelclearlyindicatesthatITNuseformalaria
protection can be thwarted in settings of extreme
poverty, where an increase in labour productivity
by an alternative ITN use can offset the perceived
benefitsofavoidingmalariainfection.Themodelalso
shows that alternative ITN uses are expected to
emerge as coverage and concomitant ‘community
(C) effects’ become more common, or if ITNs become
unprotective, for example, by the emergence of
insecticide-resistant mosquitoes (Kawada et al.
2011). We also showed that alternative ITN use is
not necessarily detrimental for an endemic commu-
nity,especiallyforlowandmoderatelevelsofmalaria
infection risk, since those strategies are Pareto
efficient, in the context of this study meaning
that alternative ITN use is not detrimental for the
communityasawhole.Ourmodelalsoshowsthatas
Fig.3. ParetoefficientNashequilibria(PNE)andSocial
malaria risk further decreases, social dilemmas, i.e.
Dilemma(SD).(A)Equilibriaasfunctionoftheinfection
probability,P,thetoppanelillustratesacasewhere situationswhereindividualbehaviourscanimprovea
profitabilityforalternativeITNuseislow(income situation for a community as a whole, are likely to
increasesby10%,i.e.β=1·1),thebottompanelrepresents emerge, especially when the use of ITNs could be
acaseofhigherprofitabilityforthealternativebednetuse crucial to render elimination feasible (Smith et al.
(incomeincreasesby30%,i.e.β=1·3).Inthetwopanels 2009), because they are not optimal from the
thethresholdsPR,PLandPL* areindicated(seethemain perspective of non-cooperative individual residents.
textforanexplanationofthethresholds).Thelegendin However,theonlydatawehaveavailableforacurrent
panelBappliestopanelsA,BandC:All-T(All-F)are
low malaria risk area, formerly hyperendemic, i.e.
theequilibriawhereallplayers(donot)usetheITN
Aneityum island in Vanuatu (Kaneko et al. 2000),
formalariaprotection,FRarethefree-riderequilibria.
suggestthatthenon-cooperativebehaviourassumed
(B)EquilibriaasfunctionofPandindividualbednet
protection(α )inasettingwithalowlevelofadditional in our model is not likely to interfere with ITN
1
protectionviaa‘communityeffect’(5%i.e.α =0·95). use for malaria protection when there is a likely
2
(C)EquilibriaasfunctionofPandindividualbednet smallproportionalincreaseoflabourproductivityby
protection(α )inasettingwithahighlevelofadditional alternative ITN use. In Aneityum ITN use is very
1
malariaprotectionviaacommunityeffect(20%,i.e. high(>95%)wellafterelimination,probablybecause
α2=0·80). oftheeducationalcomponentoftheeliminationtrial
aimed at strengthening cooperative practices and
promoting community participation of residents
the1991eliminationtrial,PRwasslightlyabove20% during the trial and subsequent malaria freedom
andITNcoveragewasnull(Table1).Aspartofthe (Kaneko, 2010). Also, Vanuatu has a moderate level
elimination trial coverage was raised to 94% and use of human development, where economic develop-
wasaround 90%(Kanekoetal.2000), andcurrently ment is more sustainable, socially equitable and
coverageis100%with 97%use.In Vanuatu,current conducive to a higher standard of living (e.g. better
levels of use are in accordance with equation (2) education and access to services) than in most
when the parameter β ? 1, i.e. when there is no sub-Saharan African nations (UNDP, 2011), which
significant increase of labour productivity by an makesunrealisticthescenarioofsignificantincreases
alternativeITNuseandwithatransmissioncloseto to individual labour productivity by using an ITN
0 all playerswill usethe ITN for malaria protection for a purpose other than malaria protection. Thus,
(i.e.P ?0).Nevertheless,ourmodelfailstoexplain highITNuseformalariaprotectioncouldalsoreflect
R
Ismalariabednet‘misuse’irrational? 585
the relative higher well-being of the Vanuatu popu- Chaves,L.F.,Kaneko,A.,Taleo,G.,Pascual,M.andWilson,M.L.
lation when compared with most nations in sub- (2008). Malaria transmission pattern resilience to climatic variability is
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beingashighasitiscurrentlyinLVI(>70%),current 27–55.
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2012 LVI malaria survey, Dr François Feugier and 2580.
Professor Takenori Takada for valuable comments about Lindsay,S.andBirley,M.(2004).Ruraldevelopmentandmalariacontrol
game theory and Mr Gabriel Dida for his valuable insub-SaharanAfrica.EcoHealth1,129–137.
commentsandinsightsonITNuse. Lover, A., Sutton, B., Asy, A. and Wilder-Smith, A. (2011). An
exploratorystudyoftreated-bednetsinTimor-Leste:patternsofintended
andalternativeusage.MalariaJournal10,199.
FINANCIALSUPPORT Minakawa,N.,Dida,G.,Sonye,G.,Futami,K.andKaneko,S.(2008).
Unforeseen misuses of bed nets in fishing villages along Lake Victoria.
This project was supported by Nagasaki University. MalariaJournal7,165.
K.H. and L.F.C. are supported by fellowships from the Nash,J.F.(1950).Equilibriumpointsinn-persongames.Proceedingsofthe
Japan Society for the Promotion of Science. All authors NationalAcademyofSciences,USA36,48–49.
declarenocompetinginterests. O’Meara, W.P., Bejon, P., Mwangi, T.W., Okiro, E.A., Peshu,N.,
Snow,R.W.,Newton,C.R.J.C.andMarsh,K.(2008).Effectofafall
inmalariatransmissiononmorbidityandmortalityinKilifi,Kenya.Lancet
372,1555–1562.
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