Reduced in-hospital mortality after improved management of children under 5 years admitted to hospital with malaria: randomised trial

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Reduced in-hospital mortality after improved management of children under 5 years admitted to hospital with malaria: randomised trial
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  RESEARCH Reduced in-hospital mortality after improved managementof children under 5 years admitted to hospital with malaria:randomised trial Sidu Biai, director of paediatric ward, 1 Amabelia Rodrigues, senior epidemiologist, 1 Melba Gomes, projectsmanager, 2 Isabela Ribeiro, clinical epidemiologist, 2 Morten Sodemann, clinical epidemiologist, 1 Fernanda Alves, clinical epidemiologist, 3 Peter Aaby, professor 1  ABSTRACT Objective  To test whether strict implementation of astandardisedprotocolforthemanagementofmalariaandprovision of a financial incentive for health workersreduced mortality. Design  Randomised controlled intervention trial. Setting   Paediatric ward at the national hospital inGuinea-Bissau. All children admitted to hospital withsevere malaria received free drug kits. Participants  951 children aged 3 months to 5 yearsadmitted to hospital with a diagnosis of malariarandomised to normal or intervention wards. Interventions  Before the start of the study, all personnelweretrainedin theuse ofthestandardisedguidelines for the management of malaria, including strict follow-upprocedures.Nursesanddoctorswererandomisedtoworkon intervention or control wards. Personnel in theintervention ward received a small financial incentive($50 (  £ 25;  € 35)/month for nurses and $160 for doctors)and their compliance with standard case managementwas closely monitored. Main outcome measures  In-hospital mortality andcumulative mortality within 4 weeks of hospitaladmission. Results  In-hospital mortality was 5% for the interventiongroup and 10% in the control group (risk ratio 0.48, 95%confidence interval 0.29 to 0.79). The effect may havebeen stronger in patients with positive malaria slides(0.36, 0.16 to 0.80). Cumulative mortality 4 weeks after discharge was also lower in the intervention group(0.61, 0.40 to 0.95). Conclusions  Supervising healthcareworkersto adhere toa standardised treatment protocol was associated withgreatlyreducedin-hospitalmortality.Financialincentivesmay be important for the dedication and compliance of staff members. Trial registration  Clinical Trials NCT00465777. INTRODUCTION Paediatrichospitalwardsindevelopingcountrieshavefailed to respondadequately to thechallengeof saving severely sick children. 1 Problems have been identifiedin triage and emergency care, in monitoring procedures and follow-up of treatment guidelines,and in the unavailability of drugs. 2 These factors havecontributed to high mortality in hospitals in whichhealth personnel are poorly paid and unmotivated.Stafftrainingaloneisnotasolution,andorganisationaldifficulties and follow-up of patients have beenidentified as important problems. 2 Mortality on the paediatric ward of the nationalhospital Simao Mendes in Guinea-Bissau (northwest Africa) is high. 3 It varies between 12% and 18%, andmalaria specific mortality was 12% in 2004. From1991-6, 56% (376/672) of deaths occurred within24 hours of admission. 3 Similar patterns have been seenin studies from Kenya and Zimbabwe, where 84% and44% of deaths occurred within 24 hours of admission. 45 Community studies of childhood mortality in low income countries have highlighted the poorperformance of local health services and haveemphasised that future health interventions shouldalso be directed towards hospitals. 67 Effective inter-ventions toreduce in-hospitalmortality in lowincomecountries should improve equity and reduce mortalityin the community.Paradoxically,duringacivilwarin1998-9,mortalityin hospital in children under 15 years decreasedsignificantly (odds ratio 0.58, 95% confidence interval0.50 to 0.68), as did mortality after discharge (0.57,0.40 to 0.83). 8 This was not explained by a generaldecline in mortality during the war, and childrenadmitted to hospital during the war did not seem tobe less sick or more advantaged socioeconomically.Mortality in the community increased by 34% during thewar.Thereductioninmortalityduringthewarmayhave been the result of several changes on the ward.Firstly, drugs donated by the emergency aid organisa-tions were available free of charge; secondly, staff attendance on the ward was better, as some membersofstafflivedonthewardandweresupportedwithrelief food from the World Food Programme; thirdly,morale of the staff was higher and they were morededicated.About 70% of children admitted to hospital have a clinicaldiagnosisofmalaria,andaround44%ofchildren 1 Projecto de Sa ú de de Bandim,INDEPTH Network, Bissau Codex1004, Guinea-Bissau 2 World Health Organization,Tropical Disease Research, 1211Geneva 27, Switzerland 3 World Health Organization,Bissau Codex 1011, Guinea-Bissau Correspondence to: S Biaisidubiai@hotmail.com doi:10.1136/bmj.39345.467813.80BMJ |  ONLINE FIRST | bmj.com page 1 of 6  under 5 have parasitologically confirmed malaria. 9 These observations led the National Malaria ControlProgramme and the paediatric ward  —  in collaborationwith the Bandim Health Project (BHP) and the WorldHealth Organization (WHO) country office  —  todemand drug kits for emergency management of children with severe and complicated malaria. Thesekits were funded first by BHP and then by WHO.However, we found no clear reduction in mortalityafter the kits were introduced (1 October 2000 until16 October 2003). Hence, we investigated whetheradherence to existing standardised guidelines for themanagement of malaria and strict monitoring of thepatients could reduce mortality. To make supervisionand corrections more acceptable we decided to offer a smallfinancialincentive.Weevaluatedinarandomisedtrial whether a standardised protocol for themanagement of malaria   —  including the enforcement of strict procedures for monitoring of patients, availabilityof free drugs, and small financial incentives  —  couldreduce mortality on the paediatric ward. MATERIALANDMETHODS Study site This study was carried out on the paediatric ward of thenational hospital. This is the national referral paediatricward,butitservesalsoasaprimaryhealthcarecontactforchildren from Bissau city and suburbs. These childrenmay go straight to the hospital without being referredthrough a health centre. During the study period, thepaediatric ward had 117 beds and there was one doctorfor each 12 beds and one nurse for each 32 beds during duty time. The 15 beds in the intensive care unit werecovered by two nurses from 8 am until 2 pm and onenursefortherestoftheday.Alldoctorsrotateintheout-patient clinic. Every morning, each doctor visits his orher patients and patients are discharged at this stage.Standard procedure is as follows. Children arrive at the outpatient clinic and wait to see a doctor. Very sickchildrenarescreenedbyanurseandsenttothedoctorassoonaspossible.Thedoctorevaluatesthechildanddeci-deswhetherheorsheshouldbeadmitted,remainunderobservation, or be given ambulatory treatment. Thedoctor might ask for a laboratory test. The consultationfeeis$0.5( £ 0.25;  € 0.35)andlaboratorytestsarechargedseparately; for example, a thick film, a total leucocytecount, and a haemoglobin measurement each cost $1.The hospital stay is free of charge. After consultation,the parents are given a prescription and they have tobuy the necessary drugs. Drugs can be bought from thecentral hospital pharmacy or the internal paediatricpharmacy when available, and if the parents can affordthem.Parentsmayhavetogobacktotheirhometoraisemoney. They may also havetovisit a privatepharmacytobuydrugsthatarenotavailableatthehospital.Whenadmitted to hospital, children are treated with whateverdrugs the parents can afford. Study design We conducted a randomised controlled study of theeffect of a composite intervention (improved manage-ment of malaria, free emergency drugs for malaria, andfinancial incentive) on the hospital mortality rate. Onepart of the ward was designated the intervention wardand the other was designated the reference or controlward. Training of staff  Medical staff and nursing staff from both the inter-vention ward and control ward were trained in theuseofthestandardisedprotocolformanagingmalaria. Randomisation of staff  After training, three doctors and eight nurses wererandomly selected for the intervention ward (consist-ing of four rooms), and the remaining personnelcontinued to work on the control ward (again, fourrooms), which was also staffed by three doctors andeight nurses. Outpatient clinic In the outpatient clinic, patients consulted with thedoctorinchargeasusualandthedoctordecidedwhetheror not to admit the child to hospital. All children whowere admitted with a clinical diagnosis of malaria andwho met the criteria for enrolment were invited to Children aged 3 months to 5 years admitted during the study period (n=3122) Enrolment Allocation Randomised (n=951)Children aged 3 months to 5 years admitted during the studyperiod with malaria and accessed for eligibility (n=2035)Excluded (n=1084): Did not meet inclusion criteria (n=1057; 470 lived out of Bissau city and suburbs, and 587 did not meet clinical criteria) Refused to participate (n= 0 ) Other reasons: fled from outpatient department (n=27)Allocated to intervention (n=460)Received allocated intervention (n=460; 48%)Did not receive allocated intervention (n=0)Allocated to no intervention (n=491)Received allocated intervention (n=491; 52%)Did not receive allocated intervention (n=0) Follow-upuntil discharge Analysisatdischarge Fled from the ward (n=3; 1%)Died (n=21; 5%)Alive (n=436; 94%)Fled from the ward (n=14; 3%)Died (n=46; 9%)Alive (n=431; 88%)  Analysisat28 days Analysed (n=422)Excluded from analysis because lost to follow-up (n=17; 4%)Analysed (n=423)Excluded from analysis because lost to follow-up (n=22; 5%) Follow-upat28 days Lost to follow-up because child or house not found (n=17; 4%)Died (n=8; 2%)Alive (n=414; 94%)Lost to follow-up because child or house not found (n=22; 5%)Died (n=4; 1%)Alive (n=419; 94%)Analysed (n=457; 99%)Excluded from analysis because fled from the ward (n=3; 1%)Analysed (n=477; 97%)Excluded from analysis because fled from the ward (n=14; 3%) Study flowchart RESEARCH page 2 of 6  BMJ |  ONLINE FIRST | bmj.com  participate in the study. The doctor completed a formcontaining demographic and clinical information. Alaboratory technician collected thin and thick bloodfilms, which were stained with Giemsa. The films werereadonthewardandtheresultsweregiventothedoctor.The slides were then sent to the BHP, where they wereread again by a researcher. This second set of readingswas used in the study. Enrolment and consent procedures As soon as the doctor decided to admit a child fulfilling the inclusion criteria, a study assistant explained thepurposeofthestudytotheparentsandaskedforconsent to include the child. When informed consent wasobtained, the assistant randomised the child by opening asealedenvelopewhichcontainedtheassignmenttooneof the two groups. All children admitted to the hospitalwith malaria, aged 3 months to 5 years and living inBissau city and surrounding suburbs, were randomlyreferred to the standard ward or the intervention ward.Allchildrenadmittedreceivedtheantimalarialkitfreeof charge. Patients temporarily transferred to the intensivecare unit were transferred back to the ward to which thechild was srcinally assigned. Inclusion criteria Weincludedchildrenaged3monthsto5yearswhohadclinically suspected malaria, defined as axillarytemperature >37.5 ° C or a history of recent fever withno other obvious cause. We also required the presenceofoneormoreofthefollowingconditions:unabletoeat,suck,ordrink;morethanthreevomitingepisodesintheprevious 24 hours; unable to sit or stand; impairedconsciousness (Blantyre coma score 3-4); cerebralmalaria (two or more convulsions over the preceding 24 hours); coma (Blantyre coma score 0-2, at least 30 minutes after a generalised convulsion); or severeanaemia (<50 g/l). We excluded children without theabove conditions or if the parents or carer refused togive consent. Randomisation procedure and masking We generated 1000 randomisation numbers on thecomputer and assigned them a running number. Eachchild ’ s randomisation number was sealed inside anenvelope and the running number written on theoutside. Because the study was not blinded, therunning number helped us ensure that randomisationwas not violated  —  the running numbers on theenvelope should match the sequential number inwhich children were enrolled. We assigned childrenwith an odd number to the intervention group andthose with an even number to the control group. Thesrcinal randomisation list had 483 odd numbers and517 even numbers. Hence, there was a slight imbalance between the two groups. For evident reasons, the study was not masked. Follow-up Childrencametothehospitalforafollow-upvisitafter28 days. Children who could not attend the follow-upvisit were seen by a project nurse in the community. The intervention Peopleworkinginbothwardsweretrainedintheuseof the standard protocol for management of malaria andall patients received the drug kits free of charge. Thesame conditions were present in both wards, whichwere separated by a corridor. Intervention ward All staff working on the intervention ward rigorouslyfollowedtheproceduresrecommendedinthenationalstandardisedguidelinesonthemanagementofmalaria and filled in the case record forms; the doctorsevaluated the nurses ’  quality of work and the studysupervisor systematically controlled the quality of implementation of the recommended procedures.Results of supervision were registered in the form.Nurses and doctors received a small amount of money ($50/month for nurses and $160 for doctors)for the additional forms they had to fill out. This isroughly what they would earn if they did extra part time work and is equivalent to monthly rent in Bissaufor these categories of staff.Children assigned to the intervention ward werere-evaluated by the study doctor on duty until 10 pm.The nurse on duty called one of the study doctors if a seriously sick child was recruited after 10 pm. Thenursesonthiswardcouldmakemanagementdecisionsthemselves when the study doctor was not present. Control ward Inthecontrolward,procedureswerethesameasusual.Thenationalguidelinesonthemanagementofmalaria were supposed to be followed. However, the lack of supervision meant that people could choose whetheror not to follow the recommendations. The doctorswere not obliged to evaluate the nurses ’  work, andthe doctors themselves were not evaluated either. Main outcomes The primary end point was in-hospital mortality. Thesecondary end points were cumulative mortality afterdischarge at day 28 and length of hospital stay. Table1  |  Demographicfactorsatinclusionintrial.Valuesarenumber/totalnumber(%)unlessstatedotherwise  VariableGroupIntervention Control Sex (male) 251/460 (55) 280/491 (57)Median (interquartile range)age in months 24 (13-36) 24 (14-39)Arm circumference <130 mm 54/454(12) 60/489 (12)High transmission season 258/460 (56) 269/491 (55)House withceiling 4/455(0.9) 12/489 (2.5)Impregnated bed net 77/455(17) 89/488 (18)Living inthe BHP study area 139/460 (30) 141/491 (29)Malaria parasite positiveslide 318/460 (69) 338/491 (69) BHP, Bandim health project. RESEARCH BMJ |  ONLINE FIRST | bmj.com page 3 of 6  Content of kit Thenationalmalariapolicyfortreatingseveremalaria recommends intravenous infusion of 20 mg quinine/kg body weight in 5% saline solution (4-10 ml/kg) forfour hours. After that, 10 mg quinine/kg body weight should be given for four hours and repeated everyeight hours until the patient can be treated orally.Thus, the basic kit for severe malaria included two500 ml bags of 5% glucose, one vial of 600 mg of quinine, two intravenous catheters, five 5 ml syringes,twopairsofsurgicalgloves,paracetamolanddrugsforother conditions including one vial of diazepam, threesachets of oral rehydration salt, two 500 ml bottles of ringer lactates, and nasogastric tubes. If the childneeded other drugs to complete the treatment, theparents had to buy them. Sample size calculation We estimated that 474 children were needed in eacharm to observe  —  with 80% power and a 5% signifi-cance level  —  a 50% reduction in mortality (fromaround 10% in the control group to 5% in the inter-vention group). Statistical methods We used Dbase-VI and Stata-8 for data entry andcleaning. Statistical analyses were carried out withStata-8. We calculated risk ratios for in-hospitalmortality and mortality after discharge. The length of hospitalstayindayswascomparedforthetwogroups.Children who fled from the hospital were excluded inthe analysis of in-hospital case fatality; however, if weobtained information from them at the 28 day follow-uptheywereincludedintheanalysisof mortalityafterdischarge. Although most of the children absconding from the ward were alive at the 28 day visit, we alsoconducted an analysis considering lost to follow-up at the hospital as a negative outcome. We compared themean duration of stay on the ward and time todischarge between the two groups using Coxregression.Tocomparemortalityforthesameagegroupbeforethe trial we compared mortality during the year of thetrial with mortality between December 2003 andNovember 2004  —  the 12 months before the start of the trial. Ethics All children enrolled in the study should havebenefited. The children in the control and researchwardsbenefitedfromthefreedrugkitsandtheretrain-ing of the staff. The patients did not pay the fees forlaboratory tests as the BHP provided the materialsand reagents. The children in the research wardwould also have benefited from the personnel being rigorously supervised. A data safety monitoring board has not been established for financial reasons. RESULTS The trial was conducted between 1 December 2004and 16 January 2006. During this time, 3122 childrenbetween 3 months and 5 years were admitted to thehospital.Amongthem,2035wereclinicallydiagnosedwithmalaria;470livedoutsideBissaucity,587didnot meet the inclusion criteria, and 27 fled beforerandomisation. We randomised 951 children:460 (48%) to the intervention group and 491 (52%) tothe control group. At the hospital, three (0.7%)children fled from the intervention group (two seenalive at 28 days, one lost to follow-up), while 14 (3%)fled from the control group (12 seen alive at 28 days,two lost to follow-up) (fig 1). In the whole group thediagnosis was revised to severe anaemia in 172children,bronchopneumoniain78patients,diarrhoea in 32, typhoid fever in nine, and sepsis in four. Of the295 patients with a negative malaria slide, wediagnosed severe anaemia in 45, bronchopneumonia in 26, diarrhoea in 17, sepsis in two, and typhoid feverin one.Background characteristics were similar in the twogroups: 251/460 (55%) were boys in the interventiongroup and 280/491 (57%) in the control group. Themedian age of children admitted was 24 months inboth groups. Randomisation to the groups was similarfor different transmission seasons, and the proportionof patients with positive malaria slides was the same(69%) in both groups. Socioeconomic conditionswere comparable and the same proportion of childrenused impregnated bed nets (table 1).Inthe12monthsbeforethetrial,overallmortalityat the hospital in children aged between 3 months and5 years was 13% (413/3076). During the period of thestudy from December 2004 to January 2006, 3122childrenwereadmittedtothehospital;noinformationon outcome was available for 331 children who left without discharge. Of the remaining 2791 children,mortality was 13% (351/2791). Table2  |  Mortalityinthetwogroupsofchildrenclinicallydiagnosedwithmalaria.Valuesarenumber/totalnumber(%)unlessstatedotherwise  VariableGroupRisk ratio (95% CI) P valueIntervention Control Mortality atdischarge 21/457 (5) 46/477(10) 0.48 (0.29 to 0.79) 0.002 In-hospital mortality Patients from the BHParea 5/138(4) 9/136(7) 0.55 (0.19 to 1.59) 0.26Patients living outside theBHP area16/319 (5) 37/341(11) 0.46 (0.26 to 0.81) 0.005Patients positivefor malariaonmicroscopy8/316(3) 23/329 (7) 0.36 (0.16 to 0.80) 0.008Patients negativefor malariaonmicroscopy13/141 (9) 23/148(16) 0.59 (0.31 to 1.12) 0.10 Mortality after28 days Cumulative 29/443 (7) 50/469(11) 0.61 (0.40 to 0.95) 0.02Patients positivefor malariaonmicroscopy12/307 (4) 26/324 (8) 0.49 (0.25 to 0.95) 0.02Patients negativefor malariaonmicroscopy17/136(13) 24/145(17) 0.76 (0.42 to 1.34) 0.33 BHP, Bandim health project. RESEARCH page 4 of 6  BMJ |  ONLINE FIRST | bmj.com  In-hospital mortality We excluded the 17 children who fled from theanalysis of in-hospital mortality. All patients includedin the trial were clinically diagnosed with malaria. Of the67childrenwhodiedinhospital,36hadadiagnosisof malaria only, 20 had anaemia as a secondarydiagnosis, six had pneumonia, four had diarrhoea,and one had convulsions. In the intervention group,21/457 (5%) patients died and in the control group46/477 (10%) patients died (risk ratio 0.48, 95%confidence interval 0.29 to 0.79, P  = 0.002). The effect wassimilarin boys(10/251(4%) v   26/270(10%);0.41,0.20 to 0.84) and girls (11/206 (5%)  v   20/207 (10%);0.55, 0.27 to 1.12). Children living in or outside theBHP study area had a similar reduction in mortality,although mortality was lower for children from thestudy area (table 2).Mortality was significantly higher in children with-out confirmed malaria (12%) than in those clinicallydiagnosedwithmalaria(5%)(P  = 0.04;table2).Becausetheinclusioncriteriawerebasedonaclinicaldiagnosisof malaria, we looked at the effect of intervention onthe basis of whether malaria was confirmed by micro-scopyor not.Mostof theeffect of theinterventionwasseen in children who had malaria positive slides (0.36,0.16 to 0.80).Fewer patients absconded in the control group thanin the intervention group (3/460 (0.7%)  v   14/491(2.9%); 0.23, 0.07 to 0.79). If lost to follow-up at thehospital was included as a negative outcome, the riskratio for a negative outcome was 0.43 (0.27 to 0.67). Length of hospital stay The mean length of stay on the paediatric ward wasshorter in the intervention group (7 days, standarddeviation 3.2) than in the control group (8 days, 4.2),as the rate of discharge was 35% shorter in the inter-vention group (18% to 55%, P<0.0001). Mortality at 28 days of follow-up At the 28 day visit, we obtained information on 422children in the intervention group  —  17 were lost tofollow-up. In the control group, we obtained informa-tion on 423 children  —  22 were lost to follow-up.Children from the intervention group were twice aslikely to come for the 28 days visit at the hospital thanchildrenfromthecontrolgroup(55% v  25%;2.15,1.79to 2.59, P<0.0001).When we looked at mortality after discharge alone,the intervention group had slightly higher mortalitythan the control group (2.01, 0.61 to 6.64, P  = 0.23).However, overall mortality at day 28 was lower in theintervention group than in controls (7%  v   11%; 0.61,0.40 to 0.95). The effect was strongest for the labora-tory confirmed malaria cases (4%  v   8%; 0.49, 0.25 to0.95; table 2). DISCUSSION We found that a composite intervention  —  including standardised guidelines on the management of malaria,freeemergencydrugsformalaria,andmodest financial incentives to staff   —  reduced in-hospitalmortality for patients with malaria by half. Becauseall staff were trained before the study and randomisedto the intervention or control wards, and all childrenreceived free emergency drugs, neither training norfree drugs alone affected the quality of management and subsequent survival.The inclusion criteria for patients with malaria werebasedonclinicaldiagnosis,asisusuallythecaseinlow incomecountries.The intervention tendedto bemorebeneficial in patients with confirmed malaria. Thissuggests that laboratory tests should be used whendeciding whether or not to treat patients with anti-malarial drugs. The tendency to overdiagnose malaria may mean that less attention is paid to other seriousconditions.Thiscouldcontributetothehighmortalityseen in such patients. 1011 Thestudyaimedtoreducein-hospitalmortality,andthe health staff could have discharged children earlierto avoid deaths in hospital. Children in the inter-vention group had a shorter median length of hospitalstaythanthoseinthecontrolgroup,yettheyhadlowercumulative mortality after one month. The extra careandattentiongiventothepatientsseemedtoinfluencehow well they adhered to the advice of health person-nelandincreasedtheirconfidenceinthehealthsystem,as twice as many children in the intervention groupcame to the hospital for the follow-up visit.Ourstudycouldnotdistinguishbetweentheeffectof supervising the implementation of guidelines and theeffect of the financial incentive in reducing mortality.However,it wouldbedifficult toseparatethesefactorsinoursetting.Tomakethestaffacceptcorrectionsandchangesinbehaviouraftersupervision,theyneedtobeinterested and available, otherwise neither the super-vision nor the training would have any effect.Both the intervention and the control wards weresituated in the same building and the staff communicated with each other. There could havebeen contamination between the staff, from the twowards. However, this would have reduced theestimated effect.Training is one of the main activities of healthprogrammes, but it should be followed up by support andreinforcement.Thesameappliestotheavailabilityof free drugs. With the cost recovery system that isnormally in place patients also pay for urgent drugs,and parents often need to go home to raise themoney. Having to pay for services and drugs in healthfacilities might make certain interventions lesseffective. 12 Free drugs are an important part of ourintervention, but drugs alone are not likely to have a largeeffectonmortalityifthepatient  ’ scareisnotgood.Inresourceconstrainedsettings,hospitalworkersearnvery little, payment is often delayed, and they are not highly motivated to improve performance. Super-vision is lacking or ineffective. Even a small financialincentive and a specific target (such as mortality) canmake workers more likely to adhere to standards andimprove the quality of their work. Targets can divert effort away from other activities, 13 but mortality is the RESEARCH BMJ |  ONLINE FIRST | bmj.com page 5 of 6
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