Hand hygiene in low- and middle-income countries

Article

Reference

Hand hygiene in low- and middle-income countries

LOFTUS, Michael J, et al.

Abstract

A panel of experts was convened by the International Society for Infectious Diseases (ISID) to overview evidence based strategies to reduce the transmission of pathogens via the hands of healthcare workers and the subsequent incidence of hospital acquired infections with a focus on implementing these strategies in low- and middle-income countries. Existing data suggests that hospital patients in low- and middle-income countries are exposed to rates of healthcare associated infections at least 2-fold higher than in high income countries. In addition to the universal challenges to the implementation of effective hand hygiene strategies, hospitals in low- and middle-income countries face a range of unique barriers, including overcrowding and securing a reliable and sustainable supply of alcohol-based handrub. The WHO Multimodal Hand Hygiene Improvement Strategy and its associated resources represent an evidence-based framework for developing a locally-adapted implementation plan for hand hygiene promotion.

LOFTUS, Michael J, et al . Hand hygiene in low- and middle-income countries. International Journal of Infectious Diseases , 2019, vol. 86, p. 25-30

DOI : 10.1016/j.ijid.2019.06.002 PMID : 31189085

Available at:

http://archive-ouverte.unige.ch/unige:134643

Disclaimer: layout of this document may differ from the published version.

1 / 1

Review

Hand hygiene in low- and middle-income countries

Michael J. Loftus

, Chloe Guitart

, Ermira Tartari

, Andrew J. Stewardson

,

Fatma Amer

, Fernando Bellissimo-Rodrigues

, Yew Fong Lee

, Shaheen Mehtar

, Buyiswa L. Sithole

, Didier Pittet

*

aDepartmentofInfectiousDiseases,AlfredHospitalandCentralClinicalSchool,MonashUniversity,Melbourne,Australia

bInfectionControlProgrammeandWHOCollaboratingCentreonPatientSafety,UniversityofGenevaHospitalsandFacultyofMedicine,Geneva,Switzerland

cDepartmentofMicrobiology,ZagazigUniversity,Zagazig,Egypt

dDepartmentofSocialMedicine,RibeirãoPretoMedicalSchool,UniversityofSãoPaulo,RibeirãoPreto,Brazil

eInstituteofGlobalHealth,FacultyofMedicine,UniversityofGeneva,Geneva,Switzerland

fInfectionControlAfricaNetwork,UnitofIPC,TygerbergHospital,CapeTown,SouthAfrica

ARTICLE INFO

Articlehistory:

Received2June2019 Accepted4June2019

CorrespondingEditor:EskildPetersen,Aar- hus,Denmark

Keywords:

Handhygiene

Infectionpreventionandcontrol Low-andmiddle-incomecountries

ABSTRACT

ApanelofexpertswasconvenedbytheInternationalSocietyforInfectiousDiseases(ISID)tooverview evidencebasedstrategiestoreducethetransmissionofpathogensviathehandsofhealthcareworkers and thesubsequentincidence of hospitalacquiredinfectionswith afocuson implementingthese strategiesinlow-andmiddle-incomecountries.Existingdatasuggeststhathospitalpatientsinlow-and middle-incomecountriesareexposedtoratesofhealthcareassociatedinfectionsatleast2-foldhigher thaninhighincomecountries.Inadditiontotheuniversalchallengestotheimplementationofeffective handhygienestrategies,hospitalsinlow-andmiddle-incomecountriesfacearangeofuniquebarriers, includingovercrowdingandsecuringareliableandsustainablesupplyofalcohol-basedhandrub.The WHO Multimodal HandHygiene Improvement Strategyand itsassociated resources represent an evidence-based frameworkfordevelopingalocally-adapted implementationplanforhand hygiene promotion.

©2019TheAuthors.PublishedbyElsevierLtdonbehalfofInternationalSocietyforInfectiousDiseases.

ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by- nc-nd/4.0/).

Contents

Keyissues ... 26

Knownfacts ... 26

Introduction... 26

Burdenofhealthcare-associatedinfectionsinlow-andmiddle-incomecountries ... 26

Transmissionofpathogensviahealthcareworkers’hands ... 26

Handhygienereduceshealthcare-associatedinfections ... 26

Controversialissues ... 27

Handhygieneinovercrowdedsettings ... 27

Handhygienetechnique ... 27

Culturalandreligiousfactors ... 27

Suggestedpractice ... 27

My5momentsforhandhygiene ... 27

WHOmultimodalhandhygieneimprovementstrategy ... 28

WHOhandhygieneself-assessmentframework ... 28

Localproductionofalcohol-basedhandrub... 28

“TurnAfricaOrange” ... 29

* Correspondingauthorat:InfectionControlProgramandWHOCollaboratingCentreonPatientSafety,UniversityofGenevaHospitalsandFacultyofMedicine, 1211Geneva 14,Switzerland.

E-mailaddress:didier.pittet@hcuge.ch(D.Pittet).

https://doi.org/10.1016/j.ijid.2019.06.002

1201-9712/©2019TheAuthors.PublishedbyElsevierLtdonbehalfofInternationalSocietyforInfectiousDiseases.ThisisanopenaccessarticleundertheCCBY-NC-ND license(http://creativecommons.org/licenses/by-nc-nd/4.0/).

ContentslistsavailableatScienceDirect

International Journal of Infectious Diseases

j o u r n a l h o m ep a g e : w w w . e l s e v i e r . c o m / l o c a te / i j i d

Summary ... 29

Conflictsofinterest ... 29

Fundingsources ... 29

Ethicalapproval ... 29

Acknowledgements ... 29

References ... 29

Keyissues

Theburdenofhealthcare-associatedinfections(HAIs)isgreater in low- and middle-income countries (LMICs) than in high- incomecountries.

Handhygieneisoneofthemosteffectivestrategiestoreduce HAIsandthetransmissionofantimicrobialresistantpathogens.

Severalstudieshavedemonstratedeffectiveimplementationof handhygieneinterventionsinLMICs.

LMICsfaceuniquechallengesrelatedtohandhygiene,suchas procurementofandlocalproductionofalcohol-basedhandrub (ABHR) and application of ‘My 5 Moments’ to overcrowded settings.

WorldHealth Organization’s‘Guidelines onHand Hygiene in Health Care’ (World Health Organization, 2009b) and the accompanyingsuiteofimplementationtoolsarekeyresources forpractitionersinLMICs.

Knownfacts Introduction

Healthcare-associatedinfections(HAIs)representasignificant threat to patient safety, affecting hundreds of millions of individuals worldwide (Allegranzi et al., 2011). HAIs result in increased mortality and morbidity, greater length of stay, and higher healthcare costs (Marchetti and Rossiter, 2013). Hand hygieneamonghealthcareworkers(HCWs)isconsideredoneof themostcriticalstrategiestoreducethefrequencyofHAIs.While mostevidenceisfromhigh-incomecountries(HICs),nowthereis sufficientdatafromLMICstosuggestthathandhygieneisalsoa keyandeffectivestrategyinthiscontext.

Burdenofhealthcare-associatedinfectionsinlow-andmiddle-income countries

TheincidenceofHAIsissignificantlyhigherinLMICscomparedto HICs.However,adetaileddescriptionofHAIsinLMICsisrestrictedby arelativelackofdataandthesmallnumberofhigh-qualitystudies (Damanietal.,2017).AWHOsurveydemonstratedthatonly23/147 (15.6%)LMICsreportedafunctioningnationalsurveillancesystem forHAIs(WorldHealthOrganization,2010a).Barrierstoeffective surveillance include insufficient financial resources, scarcity of training in infection prevention and control (IPC) and hospital epidemiology,limitedmicrobiologicalandradiologicalservices,and otherimportantcompetinghealthcarepriorities.Sustainedinvest- mentstotackleanyofthesebarriers–suchasimprovingthecapacity ofmicrobiology laboratories–can alsohaveflow-on benefits inother relatedareas,suchasimprovingthedetectionandsurveillanceof antimicrobialresistantpathogens.

AsmallnumberofstudieshavequantifiedtheburdenofHAIsin LMICs,whichisestimatedtobe2–20timesgreaterthaninHICs (Allegranzietal.,2011;WorldHealthOrganization,2009b).Ina large systematic review of HAIs in LMICs the overall pooled prevalencewas15.5per100beddays,withthehighestdensityof infections among intensive care unit (ICU) patients – pooled

densityof47.9per1000patient-days(Allegranzietal.,2011).A systematic review focusing on HAIs in Africa highlighted the paucity of high-quality data, yet reported a hospital-wide cumulativeincidenceof2.5%–14.8%,whichwasashighas45.8%

in some surgical wards (Bagheri Nejad et al., 2011). The discrepancy between LMICs and HICs was also found among neonatalsettings,withHAIsbeing3–20timeshigherinresource- limitedsettings(Zaidietal.,2005).

Transmissionofpathogensviahealthcareworkers’hands

The hands of healthcare workers play a central role in transferring microorganisms throughout the clinical environ- ment and,more importantly,topatients(Allegranziand Pittet, 2009;Pittetetal.,1999).Handshavethepotentialtoexchange microorganisms at each hand-to-surface contact, and HCWs’ handstransientlycontaminatedwithnosocomialpathogensare consideredtobetheprimaryrouteoftransmission(Pittetetal., 2006).Performing hand hygiene, most commonlythrough the use of ABHR, leads to a significant reduction in the bacterial countspresentonhandsandthereforereducingthelikelihoodof cross-transmission (Bellissimo-Rodrigues et al., 2017; Salmon etal.,2014).

Handhygienereduceshealthcare-associatedinfections

Overthelastfewdecadestherehasbeenanincreasingbodyof evidencetoshowthatimprovedhandhygiene,withaparticular focusontheuseofABHR,canreduceHAIrates(Allegranziand Pittet,2009;Kingstonetal.,2016);inparticularbloodstreamand surgicalsiteinfections(Stewardsonetal.,2011).LMICsareunder- representedinthesestudies,witha systematicreviewonhand hygienecompliancefindingthatonly2of16high-qualitystudies wereperformedwithinaLMICcontext(Kingstonetal.,2016).

Thereare,however,encouragingexamplesofhospitalsinLMICs implementing strategies to significantly improve hand hygiene compliance, often associated with reductions in HAIs. Most of these studiesreport implementationof theWHO’smultimodal improvementstrategy(WorldHealthOrganization,2009b)–see SuggestedPractice,below.InauniversityteachinghospitalinMali, handhygienecomplianceincreasedfrom8%atbaselineto21.8%

(Allegranzietal., 2010);similarlylargeincreasesfrom34.1% to 68.9%wereachievedina rural,non-referralhospitalinRwanda (Holmenetal.,2016).InColumbianICUs,theimplementationof hand hygieneresulted in a reduction in central line-associated bloodstream infections and the cessation of an Acinetobacter outbreak(Barreraetal.,2011).InaVietnamesetertiaryhospital, handhygienecomplianceincreasedfrom25.7%to57.5%,associat- edwithasignificantreductioninHAIsfrom31.7%to20.3%(ThiAnh Thuetal.,2015).Importantly,thecost-effectivenessofmultimodal handhygieneinterventionsinsuchsettingshasbeendemonstrat- edfrombothmodelling(Luangasanatipetal.,2018)andclinical trialdata(ThiAnhThuetal.,2015).

Despitelimitedresources,organizationssuchastheInfection Control Africa Network (ICAN) made significant progress by supportingcountriesintheirefforts ofputting IPCpoliciesand specificallyhandhygienepoliciesintoplace.Therearecurrently 26 M.J.Loftusetal./InternationalJournalofInfectiousDiseases86(2019)25–30

severalcountriesinAfrica(SouthAfrica, Mozambique,Namibia, Guineaandothers)withspecifichandhygienepolicies.Tanzania andEthiopiaareexamples ofcountriesthathave handhygiene policiesembeddedintheirIPCpolicies.Policiesonlocalproduction of ABHRare now used in South Africa, Cameroon, Mali, Sierra Leone,UgandaandMozambiquewithotherLMICsimplementing thesepoliciesinthenearfuture.

Insummary,whilelessresearchisavailablefromLMICsthan HICs,thereissufficientdatatoindicatehighratesofHAIs,andthat effective interventions such as hand hygiene and other IPC measures are critical to patient safety and the overall better deliveryofcare.

Controversialissues

Handhygieneinovercrowdedsettings

A keycomponent of the WHO’s ‘My5 Momentsfor Hand Hygiene’strategy(seebelow)is thedivisionofthehealthcare environmentintotwozones: thepatientzoneandthehealth- carezone.Thepatientzonecontainsthepatienthim/herselfand his or her immediate surroundinginanimate objects,which is assumedtobe“contaminated”bythatpatient’smicrobiota.The healthcare zone includes all other surfaces (including other patients) and is considered to be “contaminated” by micro- organisms that are foreign to, and potentially harmful to, the patientin question. Thishassubsequent implicationsfor when hand hygiene is indicated to prevent cross-contamination and HAIs(Saxetal.,2009;Saxetal.,2007).

However, in resource-limited settings, overcrowding may challengethisconceptualmodele.g.twoormorepatientssharing thesamebedorhaving insufficientspacing betweenindividual patient beds. The resulting loss of distinct patient zones complicatesapplicationofthe‘My5Moments’approach(Salmon etal.,2015).EffortshavebeenmadewithintheWHOGuidelineson HandHygieneinHealthCare(WorldHealthOrganization,2009b) andsubsequentpublications(Salmonetal.,2015)toadaptthe‘My 5Moments’strategyspecificallyforovercrowdedsettings.Thishas beendonetoprovideclarityontheindicationsforhandhygienein this contextand ensuregeneralisabilityof the‘My5 Moments’ strategy.

Overcrowdingisoftenaccompaniedbyarelativeshortageof nursingstaff.Insuchhealthcarefacilities,familycaregiversmaybe relied on to provide a large proportion of patient care. These caregiversmayberesponsible formore handhygieneopportu- nitiesthanHCWs(Horngetal.,2016),andrepresentanotherkey targetforhandhygieneandIPCeducation(Islametal.,2014).

Handhygienetechnique

TheWHOguidelinescurrentlypromoteasix-steptechniquefor applyingABHRtoensurecompletecoverageofthehands(World HealthOrganization,2009b).However,fullcompliancewiththis techniqueappearstobeaslowas0%–8.5%(Stewardsonetal.,2014;

Tschudin-Sutter et al., 2015), even in the context of good compliancewithhandhygiene indications.A number ofrecent studiessuggestthatashorterandsimplerhandhygienetechnique beas effectivewhile maintainingantibacterialefficacy.Recom- mendedmodificationsinclude‘fingertips-first’(Piresetal.,2017a), shorteningthedurationofrubbinghands(15sinsteadof20–30s) (Krameretal.,2017;Piresetal.,2017b),orperforming‘three-steps’ insteadof‘six-steps’(Tschudin-Sutteretal.,2017;Tschudin-Sutter et al., 2018). It is important to recall however that the latter technique also requires complete coverage of the hands. The majorityofthestudieswereperformedinlaboratoryconditions andfurtherclinicalresearchisneeded.

Culturalandreligiousfactors

Manycultures and religions acknowledge theimportance of handwashing and personal hygiene, with washing activities embedded in their religious practiceor cultural norms (World HealthOrganization,2009b).Aseffortsaremadetopromotehand hygiene globally, it is important to recognise the influence of differentculturalandreligiousfactorsonHCWs’attitudestowards hand hygiene and their subsequent hand hygiene adherence (WorldHealthOrganization,2009b).Suchissues,includingtheuse of alcohol, need tobe carefully and respectfully considered in dialoguewithappropriatestakeholders.Forexamplewhenasked toaddressthequestionofABHR,theMuslimScholars’Boardofthe MuslimWorldLeagueclarifiedthat“alcohol maybeusedasan externalwoundcleanser,tokillgermsandinexternalcreamsand ointments” (Ahmed et al., 2006; World Health Organization, 2009b).Arecentcohortstudydemonstratedthatreligion-relevant, culturally-specificinterventionscouldsignificantlyimprovecom- pliancewithandbeliefsaboutABHRintheUnitedArabEmirates (Ngetal.,2019).

Suggestedpractice

My5momentsforhandhygiene

The WHO ‘My 5 Moments for Hand Hygiene’ defines when healthcareworkersshouldperformhandhygieneduringclinical care (Saxet al., 2007). It is based on theconceptual model of microorganismcross-transmissionandisdesignedtobeusedto teach,audit,andreporthandhygienebehaviour.Thepatientzone isthecentralelementofthe‘My5MomentsforHandHygiene.’The

‘5Moments’are(Figure1):

1)Beforetouchingapatient 2)Beforeclean/asepticprocedures 3)Afterbodyfluidexposure/risk 4)Aftertouchingapatient

5)Aftertouchingpatientsurroundings

ThepreferredmethodforhandhygieneisrubbingwithABHR includingafterremovalof gloves.However,handwashingwith soap and wateris recommended when hands are visibly dirty, soiledwithbloodorbodyfluids,orpotentiallycontaminatedwith spore-formingorganisms(e.g.Clostridiumdifficile).

Figure1.TheMy5MomentsofHandHygiene.

WHOmultimodalhandhygieneimprovementstrategy

Inadditiontooutliningtheevidencebaseforfocusingonhand hygieneimprovementaspartofeffortstoreduceHAIs,theWHO

‘Guidelines on Hand Hygiene in Health Care’ (World Health Organization, 2009b) introduced the Multimodal Strategy for HandHygiene Improvementasa meanstoachieve andsustain optimalhandhygienebehaviour.

In brief,thefivecomponentsofthismultimodalstrategyare (WorldHealthOrganization,2009a):

1)Systemchange: ensuring that healthcare facilities havethe necessary infrastructure to allow HCWs to perform hand hygiene.Thisincludesnotonlythereliableanduninterrupted provisionofABHRatthepointofcare,butalsoacontinuous supply of safe water, soap, towels, and disposable non- powderedgloves.Tohelp ensureoptimaladherencetohand hygienerecommendations,productssuchasABHRandgloves should be proven to be tolerable and acceptable to HCWs (Meneguetietal.,2019;WorldHealthOrganization,2009a).

2)Staffeducationandtraining:HCWsshouldbeeducatedabout theimpactofHAIsandtheroleofhandhygieneinsafepatient care,andtrainedaboutimplementationofthe‘My5Moments forHandHygiene’andcorrecthandhygienetechnique.Staffin healthcarefacilitiescanchangeoften;itisthereforeimportant to repeat this training intermittently, to ensure that newly arrivedstaffareeducated,and that theknowledgeof others remainsup todate.Emphasisinghand hygiene(aspartof a largerIPCtrainingprogramme)intheundergraduatecurricu- lumfor bothclinical andnon clinicalstaffis recommended.

Additional education sessions should also be conducted exclusively for hand hygiene observers – allowing them to learnandpracticetheproposedmethodsofobservation.

3)Evaluation and feedback: regularevaluationofhandhygiene complianceisacrucialbehaviourchangestrategywhencoupled with performance feedback; it ensures that progress can be monitoredovertime.Handhygieneobservationscanbeusedto demonstrate improvements following interventions and help sustainmotivationforgoodpractice.Alternatively,itmayhighlight certainprofessionalcategoriesorindicationsforhandhygienethat havepoorcomplianceandneedimprovement.TheHandHygiene Self Assessment Framework (World Health Organization, 2010c) (see below)isastructuredandconsistentmethodofcollectingsuchdata andsupports“blame-free”evaluationandregularfeedback.

4)Remindersintheworkplace:mostcommonlytakingtheform ofaposter,thesecancontinuallypromptHCWsregardingthe importance of – and the indications for – hand hygiene.

Additionally,theyinformpatientsandtheirvisitorsofthelevel ofcaretheyshouldexpectfromHCWswithregardstohand hygiene.Toincreasetheirefficacy,theseposterscanbeadapted tothelocalcontext,andevaluatedandupdatedonaregular basis.

5)Institutional safety climate: creating an environment that prioritises patient safety and high compliance with hand hygiene.Thiscanoccurat aninstitutional level– withclear messages of public support for hand hygiene from leaders within the institution, setting benchmarks or targets, and havinghandhygienechampions.Equallythiscanoccuratan individual level, with HCWs identifying hand hygiene as a priority that reflects their commitment to do no harm to patients.Partneringwithpatientsandpatientorganizationsto promote hand hygiene mayalso foster a climate of patient safety, but should be undertaken sensitively and in close consultationwithkeystakeholdersincludinghealthcarework- ersand patientrepresentatives(Butenkoetal.,2017;Longtin etal.,2010).

This strategy was created following a review of published literatureandexpertconsensus.Thesecomponentsweresubse- quently validatedin a range of healthcare settings around the world,includingLMICs,toensurethattheycouldbeimplemented in a variety of contexts regardless of the resources available (Allegranzietal.,2013).Tofacilitatebroaduptakeand effective execution of these hand hygiene guidelines, the WHO have published an accompanying Guide to Implementation of the WHO Multimodal Hand Hygiene Improvement Strategy(World HealthOrganization,2009a).

WHOhandhygieneself-assessmentframework

TheHandHygiene Self-AssessmentFramework(HHSAF) isa self-administeredvalidatedquestionnairedesigned toprovidea systematicsituationanalysisofhandhygienestructures,resources, promotionandpracticeswithinahealthcarefacility(Stewardson etal.,2013;WorldHealthOrganization,2010c).Structuredaround the five components of the WHO Multimodal Hand Hygiene Improvement Strategy, the HHSAF assesses interventions being implementedbyhealthcarefacilitiestoensureadherencetohand hygiene action as per WHO recommendations (World Health Organization,2009b).TheHHSAFdirectsuserstodifferenttools developedbytheWHOdependingonthespecificareawarranting attention,andcanthereforebeusedtodevelopanactionplanfor localhandhygienepromotion(Stewardsonetal.,2013).TheWHO hasconductedtwoglobalsurveysusingtheHHSAFin2011and 2015 (Kilpatrick et al., 2018). Overall, HHSAF scores increased significantly (p<0.001) in facilities that participated in both surveys.WhencomparedtootherWHOregions,theAfricaregion scoredlowest,whichcouldbeindicativeofpoorerIPCinfrastruc- ture,resourcesandbasicknowledgeinhandhygieneimplemen- tationandsustainability.

Localproductionofalcohol-basedhandrub

ABHRsarethepreferredmethodforhandhygiene,astheyoffer a broad antimicrobial spectrum, are highly effective, are well toleratedbytheskinandcanbemadeavailableatthepointofcare.

However,theavailabilityoftheseproductsinLMICcountriesisstill limited. To overcome such constraints, in 2005, the WHO developed and tested two ABHR formulations according to Europeannormsforhandantisepsis(WorldHealthOrganization, 2009b,2010b).Inarandomizedcross-overtrial,bothformulations showedexcellentskintolerabilityandacceptabilityamongHCWs (Pittetetal.,2007).Theiractivecomponentiseitherethanol(80%

v/v) or isopropanol (75% v/v). These formulations also contain glycerolasemollienttoprotecthands,andhydrogenperoxideto eliminatesporesfromcomponentsorreusedbottles(WorldHealth Organization,2010b).Since2009,theseformulationsarerecom- mendedforusebytheWHOguidelinesonHandHygieneinHealth Care(WorldHealthOrganization,2009b)togetherwithaspecific methodologyadaptedfortheirlocalproduction,andtestedinpilot sitesmostlylocatedinLMICs(WorldHealthOrganization,2010b).

Since 2014,theseformulations are listed inthe WHOessential medicineslist(WorldHealthOrganization,2017).

Commercially-availableABHRsareproducedmainlyintheUSA, inEuropeandinJapan;theymeetinternationalstandardsrequired formarketintroductionofABHRs andforantimicrobialefficacy (ASTM1174orEN1500standards),andexistreliablyinhealthcare inmosthigh-incomecountries.However,ABHRsarenotavailable in all regions of the world (World Health Organization, 2017).

Whencommercially-producedABHRsarenotavailableorafford- able,localproductionaccordingtothemethodologyproposedby WHO,couldbeanalternative(Allegranzietal.,2013;Allegranzi et al., 2010; World Health Organization, 2010b). Over the past 28 M.J.Loftusetal./InternationalJournalofInfectiousDiseases86(2019)25–30

decade,therehavebeenseveralexamplesoflocalproductionof ABHRaspartofmultimodalapproachestoimprovehandhygiene, fromsinglehospitalpharmacytonationallevel(Allegranzietal., 2013;Allegranzietal.,2010;Bauer-Savageetal.,2013;Hopitaux Universitaires de Genève, 2015; World Health Organization, 2010b). Local production provides a low-cost alternative to commercially-producedABHRs,inparticularinLMICs.However, severalchallengingissueshavebeenreported,includingthelackof expertise,the lack of basic equipment and material needed to assurequalitycontrol,aswellasdifficultiesintheprocurementof rawmaterialsand dispensers(Bauer-Savageet al.,2013; World HealthOrganization,2013).Inmostinstances,alcoholandglycerol can be easily procured from local suppliers. Ethanol could be derivedfromsugarcane,wheat,rice,bananasor manioc,easily available inmostofLMICs (WorldHealthOrganization, 2010b).

However,local sourcing dispensers and hydrogenperoxide can proveproblematicandimportationmightbetheonlysolutionin some instances, thus increasing the overall cost of production (Bauer-Savage et al., 2013; World Health Organization, 2010b).

PossibleadditionaladvantagesoflocalABHRproductioninclude sustainability,economicempowermentandjobcreation,particu- larlyincountrieswithsevereeconomicconstraints(Kama-Kieghe, 2016;SARAYACo.LTD,2019).

Oneemergingsolutionforthedevelopmentofcountry-based capacityinABHRproductionhasbeenpromotedthroughSouth- Northpartnershipmechanisms.In2006,a partnershipbetween European and African countries was developed and organized practicalABHRproductionworkshopswithqualitycontrol(World Health Organization, 2013); toolsare available online for wide replicationintheAfricanregion(Bengalyetal.,2013;Pharm-Ed, 2015),aswellasinLMIC.BasedonsuchNorth-Southpartnership model,aprojectoflocalABHRproductionduringthe2014–2016 Ebola Outbreak in twentyfacilities in West Africa(Guinea and Liberia),demonstratedthefeasibilitytodeveloplocalcapacityin ABHRproductionduringanemergencysituationandinlimited- resourcesettings,whenmaterialsandtrainingareprovided.Inthis case, theimplementationprogram wasa successbut factorsof sustainabilityremaintobeidentified(HopitauxUniversitairesde Genève,2015;JacqueriozBauschetal.,2018).

TherearemanyexamplesofABHRlocalproductionoccurringin hospital pharmacies (Olivier et al., 2015). In some cases, particularlywhenlargervolumesofABHRarerequired,anational production company could be an interesting alternative to production in a hospital pharmacy, improving availability.

Demonstration of successful models based on national ABHR productionthatintegratehandhygieneimprovementeffortsinto regular local and national budget plans to ensure long-term sustainabilitywouldbehighlybeneficialsinceliteratureremains scarce.

“TurnAfricaOrange”

TheWHO global campaignSAVE HANDS: Clean YourHands with the primary objective “to promote best hand hygiene practices globally,at all levelsof health care, asa first step in ensuringhighstandardsofinfectioncontrolandpatientsafety”, hasbeenverysuccessfulwithcountriesworldwidepledgingtheir support to implement hand hygiene and reduce HAI. African countriesparticipation inthe campaignremains low. TheTurn AfricaOrangeprogramme, aninitiative ofthe InfectionControl Africa Network (ICAN), aimed to encourage as many African countries as possible to participate in the global campaign of enlistinghealthcarefacilitiesinsupportofhandhygieneimprove- ment.Thephrasewascoined toencourageAfricancountriesto movefrompaleyellowtodeeporangeonthemap,reflectingthe number ofhealthcare facilities registered on theWHO website

(WHOCollaboratingCentreonPatientSafety,2017).Between2014 and2018anannualsustainedcampaignbyICANsawanincreasein the numberof registered institutionsfrom 757to1272 (World HealthOrganization,2019).

Summary

Existing data suggests that hospital patients in LMICs are exposedtoratesofHAIsatleast2-foldhigherthaninHICs.Hand hygiene is an evidence-based strategy to reduce both the transmission of pathogens via the hands of HCWs and the subsequent incidence of HAIs. In addition to the universal challenges to the implementation of effective hand hygiene strategies, hospitals in LMICs face a range of unique barriers, includingovercrowding and securinga reliableand sustainable supply ofABHR.TheWHOMultimodal HandHygieneImprove- mentStrategyanditsassociatedresourcesrepresentanevidence- basedframeworkfordevelopingalocally-adaptedimplementation planforhandhygienepromotion.

Conflictsofinterest

None.

Fundingsources

None.

Ethicalapproval

Notrequired.

Acknowledgements

AS is supportedbya National Health and Medical Research CouncilEarlyCareerFellowship(APP1141398).MLissupportedby a National Health and Medical Research Council Postgraduate Scholarship (APP1169220). Figure 1 reprinted with permission from ‘My 5 Moments for HandHygiene’, https://www.who.int/

infection-prevention/campaigns/clean-hands/5moments/en/, accessed9January2019.

References

AhmedQA,MemishZA,AllegranziB,PittetD.Muslimhealth-careworkersand alcohol-basedhandrubs.Lancet2006;367:1025–7.

AllegranziB,BagheriNejadS,CombescureC,GraafmansW,AttarH,DonaldsonL, et al. Burden of endemic health-care-associated infection in developing countries:systematicreviewandmeta-analysis.Lancet2011;377:228–41.

AllegranziB,Gayet-AgeronA,DamaniN,BengalyL,McLawsML,MoroML,etal.

GlobalimplementationofWHO’smultimodalstrategyforimprovementof handhygiene:aquasi-experimentalstudy.LancetInfectDis2013;13:843–51.

Allegranzi B,PittetD.Roleofhandhygieneinhealthcare-associatedinfection prevention.JHospInfect2009;73:305–15.

AllegranziB,SaxH,BengalyL,RichetH,MintaDK,ChraitiMN,etal.Successful implementationoftheWorldHealthOrganizationhandhygieneimprovement strategyinareferralhospitalinMali,Africa.InfectControlHospEpidemiol 2010;31:133–41.

BagheriNejadS, AllegranziB,SyedSB,EllisB,PittetD.Health-care-associatedinfection inAfrica:asystematicreview.BullWorldHealthOrgan2011;89:757–65.

BarreraL,ZinggW,MendezF,PittetD.Effectivenessofahandhygienepromotion strategyusingalcohol-basedhandrubin6intensivecareunitsinColombia.Am JInfectControl2011;39:633–9.

Bauer-Savage J, Pittet D, Kim E, Allegranzi B. Local production of WHO- recommendedalcohol-basedhandrubs:feasibility,advantages,barriersand costs.BullWorldHealthOrgan2013;91:963–9.

Bellissimo-RodriguesF,PiresD,SouleH,Gayet-AgeronA,PittetD.Assessingthe likelihoodofhand-to-handcross-transmissionofbacteria:anexperimental study.InfectControlHospEpidemiol2017;38(5):553–8.

BengalyL,HightowerJ,BonnabryP,SyedSJAR,ControlI.P334:Catalysinglocal productionofalcoholbasedhandrubinafricanhospitals:thepowerofsouth- north-southpartnership2013;2:P334.

ButenkoS, Lockwood C, McArthur A. Patient experiences of partneringwith healthcareprofessionalsforhandhygienecompliance:asystematicreview.JBI DatabaseSystemRevImplementRep2017;15(6):1645–70.

DamaniN,MehtarS,AllegranziB.Handhygieneinresource-poorsettings.In:Pittet D, BoyceJ, Allegranzi B, editors. Handhygiene: a handbookfor medical professionals.Chichester,WestSussex:JohnWiley&Sons;2017.p.357–66.

HolmenIC, Seneza C, Nyiranzayisaba B, Nyiringabo V, Bienfait M, SafdarN.

ImprovinghandhygienepracticesinaruralhospitalinSub-SaharanAfrica.

InfectControlHospEpidemiol2016;37:834–9.

HopitauxUniversitairesdeGenève.LocalproductionofWHOhandrubduringand aftertheEbolacrisisinWest-Africa.2015...[Accessed9January2019]https://

www.youtube.com/watch?v=ss_0TZJUuQU&feature=youtu.be.

HorngLM,UnicombL,AlamMU,HalderAK,ShoabAK,GhoshPK,etal.Healthcare workerandfamilycaregiverhandhygieneinBangladeshihealthcarefacilities:

resultsfromtheBangladeshNationalHygieneBaselineSurvey.JHospInfect 2016;94(3):286–94.

IslamMS,LubySP,SultanaR,RimiNA,ZamanRU,UddinM,etal.Familycaregiversin public tertiary care hospitals in Bangladesh: risks and opportunities for infectioncontrol.AmJInfectControl2014;42(3):305–10.

JacqueriozBauschFA,HellerO,BengalyL,Matthey-KhouityB,BonnabryP,ToureY, etal.Buildinglocalcapacityinhand-rubsolutionproductionduringthe2014- 2016ebolaoutbreakdisaster:thecaseofLiberiaandGuinea.PrehospDisaster Med2018;33:660–7.

Kama-KiegheS.Localproductionofalcoholbasedhandrubs(ABHR)inNigeria–the wayofthefuture?InfectionControltips.2016...[Accessed9January2019]

https://infectioncontrol.tips/2016/03/05/abhr/.

KilpatrickC,TartariE,Gayet-AgeronA,StorrJ,TomczykS,AllegranziB,etal.Global hand hygieneimprovement progress: two surveysusing the WHO Hand HygieneSelf-AssessmentFramework.JHospInfect2018;100:202–6.

KingstonL,O’ConnellNH,DunneCP.Handhygiene-relatedclinicaltrialsreported since2010:asystematicreview.JHospInfect2016;92:309–20.

KramerA,PittetD,KlasincR,KrebsS,KoburgerT,FuschC,etal.Shorteningthe applicationtimeofalcohol-basedhandrubsto15secondsmayimprovethe frequencyofhandantisepsisactionsinaneonatalintensivecareunit.Infect ControlHospEpidemiol2017;38:1430–4.

LongtinY,SaxH,LeapeLL,SheridanSE,DonaldsonL,PittetD.Patientparticipation:

currentknowledgeandapplicabilitytopatientsafety.MayoClinicProc2010;85 (1):53–62.

LuangasanatipN,HongsuwanM,LubellY,LimmathurotsakulD,SrisamangP,Day NPJ, etal. Cost-effectivenessofinterventions toimprove handhygienein healthcare workers in middle-income hospital settings: a model-based analysis.JHospInfect2018;100:165–75.

MarchettiA,RossiterR.Economicburdenofhealthcare-associatedinfectioninUS acutecarehospitals:societalperspective.JMedEcon2013;16:1399–404.

MeneguetiMG,CiolMA,AraújoTR,Bellissimo-RodriguesF,Auxiliadora-MartinsM, Basile-FilhoA,etal.Theimpactofreplacingpowderedgloveswithpowder-free gloves on hand hygiene compliance among healthcare workers from an intensive care unit: a quasi-experimental study. Amsterdam: European CongressofClinicalMicrobiology&InfectiousDiseases;2019.

NgWK,ShabanRZ,vandeMortelT.Theeffectofahandhygieneprogramfeaturing tailored religion-relevant interventions on healthcare workers’ hand rubbing complianceandbeliefsintheUnitedArabEmirates:acohortstudy.InfectDis Health2019;,doi:http://dx.doi.org/10.1016/j.idh.2019.01.002[Epubaheadofprint].

OlivierH,TyeeTT,MulbahJ,MassaquoiM,DahnB,BengalyL,etal.Localproduction ofalcoholbasedhandrubsolution(ABHS)inLiberiaduringtheEbolaoutbreak.

AntimicrobResistInfectControl2015;4(Suppl.1):P8.

Pharm-Ed.Tutoriels pourlaproductionlocaledesolutionhydro-alcooliqueen ligne!. 2015Availablefrom:http://pharmacie.g2hp.net/tutoriel-pour-la-pro- duction-locale-de-solution-hydro-alcoolique/.[Accessed8January2019].

PiresD,Bellissimo-RodriguesF,SouleH,Gayet-AgeronA,PittetD.Revisitingthe WHO “Howto Handrub” hand hygienetechnique: fingertipsfirst?.Infect ControlHospEpidemiol2017a;38:230–3.

PiresD,SouleH,Bellissimo-RodriguesF,Gayet-AgeronA,PittetD.Handhygiene withalcohol-basedhandrub:howlongislongenough?.InfectControlHosp Epidemiol2017b;38:547–52.

PittetD, AllegranziB, SaxH,ChraitiMN,GriffithsW, RichetH.Double-blind, randomized,crossovertrialof3handrubformulations:fast-trackevaluationof tolerabilityandacceptability.InfectControlHospEpidemiol2007;28:1344–51.

PittetD,AllegranziB,SaxH,DharanS,Pessoa-SilvaCL,DonaldsonL,etal.Evidence- basedmodelforhandtransmissionduringpatientcareandtheroleofimproved practices.LancetInfectDis2006;6:641–52.

PittetD,DharanS,TouveneauS,SauvanV,PernegerTV.Bacterialcontaminationof the handsof hospitalstaff during routinepatientcare.Arch Intern Med 1999;159:821–6.

SalmonS,PittetD,SaxH,McLawsML.The’Myfivemomentsforhandhygiene’

conceptfortheovercrowdedsettinginresource-limitedhealthcaresystems.J HospInfect2015;91:95–9.

SalmonS,TruongAT,NguyenVH,PittetD,McLawsML.Healthcareworkers’hand contamination levels and antibacterial efficacy of different hand hygiene methodsusedinaVietnamesehospital.AmJInfectControl2014;42(2):178–81. SARAYACo.LTD.100%hospitalhandhygieneprojecthttps://hospital-en.tearai.jp/

[Accessed8January2019].

SaxH,AllegranziB,ChraitiMN,BoyceJ,LarsonE,PittetD.TheWorldHealth Organization hand hygiene observation method. Am J Infect Control 2009;37:827–34.

SaxH,AllegranziB,UckayI,LarsonE,BoyceJ,PittetD.’Myfivemomentsforhand hygiene’:auser-centreddesignapproachtounderstand,train,monitorand reporthandhygiene.JHospInfect2007;67:9–21.

StewardsonA,AllegranziB,SaxH,KilpatrickC,PittetD.Backtothefuture:risingto theSemmelweischallengeinhandhygiene.FutureMicrobiol2011;6:855–76.

StewardsonAJ,AllegranziB,PernegerTV,AttarH,PittetD.TestingtheWHOHand HygieneSelf-AssessmentFrameworkforusabilityandreliability.JHospInfect 2013;83:30–5.

StewardsonAJ,ItenA,CamusV,Gayet-AgeronA,CaulfieldD,LaceyG,etal.Efficacy of a new educational tool to improve Handrubbing technique amongst healthcareworkers:acontrolled,before-afterstudy.PLoSOne2014;9:e105866.

ThiAnhThuL,ThiHongThoaV,ThiVanTrangD,PhucTienN,ThuyVanD,ThiKim AnhL,etal.Cost-effectivenessofahandhygieneprogramonhealthcare- associatedinfectionsinintensivecarepatientsatatertiarycarehospitalin Vietnam.AmJInfectControl2015;43:e93–9.

Tschudin-SutterS,RotterML,FreiR,NogarthD,HausermannP,StrandenA,etal.

SimplifyingtheWHO’howtohandrub’technique:threestepsareaseffectiveas six-resultsfromanexperimentalrandomizedcrossovertrial.ClinMicrobiol Infect2017;23:409.e1–e4.

Tschudin-SutterS,SepulcriD,DangelM,SchuhmacherH,WidmerAF.Compliance withtheWorldHealthOrganizationhandhygienetechnique:aprospective observationalstudy.InfectControlHospEpidemiol2015;36:482–3.

Tschudin-SutterS,SepulcriD,DangelM,UlrichA,FreiR,WidmerAF.Simplifyingthe WHOprotocol:threestepsversussixstepsforperformanceofhandhygiene—a cluster-randomizedtrial.ClinInfectDis2018;[inpress].

WorldHealthOrganizationCollaboratingCentreonPatientSafety.TurnAfrica Orange.2017...[Accessed26March2019]http://tinyurl.com/AfricaOrange.

WorldHealthOrganization.GuitheWHOmultimodalhandhygieneimprovement strategy.Geneva:WorldHealthOrganization;2009.

WorldHealthOrganization.WHOguidelinesonhandhygieneinhealthcare:first globalpatientsafetychallengecleancareissafercare.Geneva:WorldHealth Organization;2009.

World Health Organization. The burden of health care-associated infection worldwide:asummary.Geneva:WorldHealthOrganization;2010.

World Health Organization. Guide to local production: WHO-recommended handrubformulations.Geneva:WorldHealthOrganization;2010.

WorldHealthOrganization.Handhygieneself-assessmentframework.2010... [Accessed 22 December 2018] https://www.who.int/gpsc/country_work/

hhsa_framework_October_2010.pdf?ua=1.

WorldHealthOrganization.Localproductionofalcoholbasedhandrubtraining workshopreport-africanpartnershipsforpatientsafety.2013...[Accessed9 January 2019] https://www.who.int/patientsafety/implementation/apps/

events/ABHR-workshop-report.pdf.

WorldHealthOrganization.WHOmodellistofessentialmedicines.20thed.2017 Geneva.

WorldHealthOrganization.Infectionpreventionandcontrol:registrationupdate- countriesorareas.2019...[Accessed26April2019]https://www.who.int/

infection-prevention/campaigns/clean-hands/registration_update/.

ZaidiAK,HuskinsWC,ThaverD,BhuttaZA,AbbasZ,GoldmannDA.Hospital- acquiredneonatalinfectionsindevelopingcountries.Lancet2005;365:1175–

88.raphy>

30 M.J.Loftusetal./InternationalJournalofInfectiousDiseases86(2019)25–30