Analysis of Malaria Incidence using Quasi-Poisson Regression Model: Evidence from Obuasi Municipality, Ghana

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1 Journal of Bology, Agrculture and Healthcare ISSN (Paper) ISSN X (Onlne) Analyss of Malara Incdence usng Quas-Posson Regresson Model: Evdence from Obuas Muncpalty, Ghana Alexander Boateng 1* Maseka Lesaoana 1 Tmotheus Darkwa 1 Abenet Belete 2 Hlengan Sweya 3 1.Department of Statstcs and Operatons Research, Unversty of Lmpopo-Turfloop Campus, P/Bag X1106. SOVENGA, South Afrca Department of Agrcultural Economcs and Anmal Producton, Unversty of Lmpopo-Turfloop Campus, Polokwane, P/Bag X1106. SOVENGA, South Afrca Department of Mathematcs and Appled Mathematcs, Unversty of Lmpopo-Turfloop Campus, P/Bag X1106. SOVENGA, South Afrca * E-mal of the correspondng author: sralexboateng@gmal.com Abstract Death and economc losses assocated wth malara have become a global phenomenon that need urgent attenton. To obtan a better understandng of ncdence of the dsease, a quas-posson regresson model has been appled n ths study to determne the ncdence of malara n Obuas Muncpalty, Ghana. Our results show that the ncdence of malara s more prevalent among ndvduals wthn the ages of 20 to 34 years and those above 50 years, as compared to chldren under 5 years of age. In addton, the study reveals that most ncdence of malara were reported n the last quarter of every year between 2007 and Keywords: Obuas Muncpalty, malara, rsk factors, quas-posson regresson model 1. Introducton Malara has been a protracted lfe-threatenng parastc dsease transmtted by female anopheles mosqutoes. Ths dsease has contrbuted to human mortalty n the world, partcularly among chldren. Malara threatens 2.4 bllon (40%) of the world s populaton lvng n the poorest countres and more than one mllon deaths are attrbutable to the dsease annually (World Health Organzaton 2000). Most of these deaths occur among chldren n hgh-transmsson areas, and account for approxmately one n fve of all chldhood deaths n Afrca (Mufunda et al. 2007). World Malara Report 2013 estmated that n 2012 there were 627,000 malara deaths worldwde, 90% occurrng n sub-saharan Afrca and 77% n chldren under 5 years of age (World Health Organzaton 2014). However, the true burden of malara s dffcult to estmate as many people are treated at home and no proper post-mortem dagnoss s made n the case of death (Mufunda et al. 2007). Snce there s no post-mortem dagnoss, many malara cases go unreported. Malara contnues to be a major threat to health, occurrng n 109 countres worldwde (Malara RB 2014). Varous nsttutons have been establshed to overcome ths problem. The Global Strategy has come up wth three components: malara control; malara elmnaton; and research nto new tools and approaches (Malara RB 2014). Of the 35 countres responsble for the majorty of total deaths worldwde, sx are n Afrca, accountng for 50% global deaths and 47% malara cases. A large number of these 35 countres have hgh transmsson of P. falcparum malara and are located n sub-saharan Afrca (Malara RB 2014). Malara s more prevalent n Afrca south of the Sahara, and among very young chldren and pregnant women. In areas of stable endemc malara transmsson n sub-saharan western Afrca, t has been estmated that n the year 1995 about 1 mllon deaths were drectly attrbutable to malara nfecton (Snow et al. 1999). Of these deaths, about 75% were chldren below the age of 5 years. Accordngly, a World Bank Report of 1993 noted that malara accounts for an estmated 35 mllon dsablty-adjusted lfe years per year lost n Afrca due to ll-health and premature death (Jamson et al. 1993). Greenwood and Pckerng (1993) also argued that malara was the man cause of death among early European vstors to The Gamba. Successful efforts have been acheved through nterventons and research amed towards malara elmnaton. Chyaka et al. (2013) reported that between 1945 and 2010, 79 countres worldwde acheved malara elmnaton and 75 remaned malara free, leadng to the reducton of the global geographcal spread of the dsease. Generally, there has been consderable research pertanng to malara ncdence and rsk factors. For example, Greenwood et al. (1987) measured mortalty and morbdty from malara among 3,000 chldren under the age of 7 years n a rural area of The Gamba usng a post-mortem questonnare technque. From ther study, malara was dentfed as the probable cause of 4% of nfant deaths and 25% of deaths n chldren aged 1 to 4 years n rural areas of The Gamba. Koram et al. (1995) studed soco-economc rsk factors for malara n perurban area of The Gamba. Ther study showed that malara was assocated wth poor qualty housng and crowdng and wth travel to rural areas, where the level of malara transmsson was hgher than n urban centres. No assocaton was found between the rsk of malara and the overall educaton level of parents or guardans of the sampled chldren. 52

2 Journal of Bology, Agrculture and Healthcare ISSN (Paper) ISSN X (Onlne) Stresman (2010) looked beyond temperature and precptaton, and studed ecologcal rsk factors that modfy malara transmsson. The research by Stresman (2010) revealed that temperature and water for breedng habtats were mportant prmary ecologcal factors that mpact the dstrbuton of malara vectors and the rate at whch mosquto and paraste develop. Mendez et al. (2000) studed rsk factors assocated wth malara nfecton n an urban settng, and ther study revealed that malara nfecton was prevalent n areas of the cty wth the hghest ncdence of the dsease. Ther study also assessed the assocaton between some characterstcs of the populaton and the rsk of malara nfecton. The prevalence of malara nfecton was 4.4% among the 1,380 people studed and t decreased wth age, knowledge of dsease and preventve measures drected to the elmnaton of breedng stes. In addton, the nfecton was postvely assocated wth exposure to the forest. Kudom and Mensah (2010) studed the potental role of the educatonal system n addressng the effect of nadequate knowledge of mosqutoes on the use of nsectcde-treated nets n Ghana. They contended that snce 2001, there had been a tremendous ncrease n the number of households protected by Insectcde Treated Nets (ITNs) and Internal Resdual Sprayng (IRS) n Ghana. However, they could not fnd any evdence of a reducton n malara cases as expected, but rather reported deaths were found to have ncreased snce Ther study was meant to get a better understandng of nsghts of malara, knowledge on mosqutoes and the sgnfcance attached to ITNs among secondary and tertary students n the Cape Coast, Ghana. They employed structured questonnares whch were admnstered randomly to collect data on demographc characterstcs of students, knowledge of mosqutoes and ITNs and atttude towards the use of ITN n seven publc hgh schools and four tertary nsttutons n Cape Coast metropols. The study by Ba et al. (2013) revewed clmate change and mosquto-borne dseases n Chna. The objectve of ther study was to summarze what s known about the nfluence of clmate change on the ncdence and prevalence of malara, dengue fever and Japanese encephalts n Chna, and to offer mportant nformaton and trend for adaptaton polcy makng. Ffty-fve (55) papers met the ncluson crtera for ther study. Analyss of the results thereof ndcated that the varablty n temperature, precptaton, wnd and extreme weather events s lnked to transmsson of mosquto-borne dseases n some regons of Chna. However, the fndngs of ther study were nconsstent across geographcal locatons and ths requres strengthenng current evdence for tmely development of adaptve optons. Yewhalaw et al. (2013) undertook a study on the effect of dams and seasons on malara ncdence and anopheles abundance n Ethopa usng a longtudnal cohort study conducted over a perod of two years. The am of ther study was to determne P. falcparum malara ncdence among chldren under 10 years of age lvng near a mega hydropower dam n Ethopa. A total of 2,080 chldren from 16 vllages stuated at dfferent dstances from a hydropower dam were followed-up from the year 2008 to 2010 usng actve detecton of cases based on weekly house-to-house vsts. Ths cohort of chldren comprsed 951 grls and 1,059 boys, wth a medan age of 5 years. Malara vectors were concurrently surveyed n all the 16 vllages. Fralty models were used to explore assocatons between tme-to-malara and potental rsk factors, whereas, mxed-effects Posson regresson models were used to assess the consequence of dfferent covarates on anophelne abundance. Overall, 548 (26.9%) chldren experenced at least one clncal malara epsode durng the follow-up perod wth mean ncdence rate of 14.3 cases per 1,000 chld-months at rsk (95% CI: ). P. falcparum malara ncdence showed no statstcally sgnfcant assocaton wth dstance from the dam reservor (p = 0.32), although t vared sgnfcantly between seasons (p < 0.01). The malara vector, Anopheles arabenss, was however, more abundant n vllages nearer to the dam reservor. The researchers concluded that P. falcparum malara ncdence dynamcs were more nfluenced by seasonal drvers than by the dam reservor tself. Malara s a serous threat, not only for autochthonous or ndgenous nhabtants, but also for nonmmune ndvduals travellng or workng n malara-endemc areas. The study undertaken by Texer et al. 2013, quotes from the 2011 nternatonal travel and health book that approxmately 125 mllon nternatonal travellers vst malara-endemc countres annually, after whch more than 10,000 cases of malara are reported upon returnng to ther home countres. The objectve of ther study was, nter ala, to dentfy, at a country scale (Ivory Coast), the envronmental factors that are assocated wth clncal malara among non-mmune travellers, openng the way for a remote sensng-based counsellng for malara rsk preventon among travellers usng a sample of 87 cohorts, ncludng 4,531 French solders who travelled to Ivory Coast durng approxmately four months, between September 2002 and December Due to the fact that malara s nsect-vector transmtted, the envronment was found to be a key determnant of the spread of nfecton (Texer et al. 2013). Geo-clmatc factors, such as temperature, mosture and water qualty, determne the presence of Anopheles breedng stes, vector denstes, adult mosquto survval rate, longevty and vector capacty. The assocaton between envronmental factors and malara ncdence n autochthonous populaton have been shown n several studes (Klenschmdt et al. 2001; Guthmann et al. 2002; Hakre et al. 2004; Dans-Lozano et al. 2007; Gomez-Elpe et al. 2007; Berrang-Ford et al. 2009; Olvera-Ferrera et al. 2010); Zacaras & Andersson 2010; Grod et al. 2011; Mathanga et al. 2012), yet the assocaton between the ncdence of clncal malara cases among non-mmune travellers and envronmental factors s yet to be evaluated. However, (Texer et al. 2013) analysed the 53

3 Journal of Bology, Agrculture and Healthcare ISSN (Paper) ISSN X (Onlne) assocaton between the ncdence of clncal malara and other factors (ncludng ndvdual, collectve and envronmental factors evaluated by remote sensng methods) n a random effect mxed Posson regresson model to take nto account the samplng desgn. The results of ther study showed that 140 clncal malara cases were recorded durng 572,363 person-days of survey, correspondng to an ncdence densty of 7.4 clncal malara epsodes per 1,000 person-months under survey. The rsk of clncal malara was sgnfcantly assocated wth the cumulatve tme spent n areas wth NDVI > 0.35 (RR = 2,42), a mean temperature hgher than 27 C (RR = 2,4), a longer perod of dryness durng the precedng month (RR = 0,275) and the cumulatve tme spent n urban areas (RR = 0,52). The present results suggest that remotely-sensed envronmental data could be used as good predctors of the rsk of clncal malara among vulnerable ndvduals travellng through Afrcan endemc areas. Kang et al. (2013) nvestgated the causal effect of malara on stuntng. The am of ther study was to estmate the causal effect between malara epsodes and stunted growth by applyng a combnaton of Mendelan randomzaton usng the sckle cell trat, and matchng on a cohort of chldren n the Ashant Regon, Ghana. They establshed that the rsk of stuntng ncreases by 0.32 (P-value: 0.004, 95% CI: 0.09, 1.0) for every malara epsode. The rsk estmate based on Mendelan randomzaton substantally dffers from the multple regresson estmate of 0.02 (P-value: 0.02, 95% CI: 0.003, 0.03). In addton, based on the senstvty analyss, ther results were reasonably nsenstve to unmeasured confounders. Agan, the results from ther study revealed a causal relatonshp between malara and stuntng n young chldren n an area of hgh endemcty, and demonstrated the usefulness of the sckle cell trat as an nstrument for the analyss of condtons that mght be causally related to malara. Ahmed et al. (2013) researched nto the epdemology of symptomatc P. falcparum malara n a specfc area of Bangladesh subsequent to the ntroducton of a natonal malara control program. They carred out survellance for symptomatc malara due to P. falcparum n two demographcally defned unons of the Chttagong Hll Dstrcts n Bangladesh, borderng western Myanmar, between October 2009 and May The relatonshp between soco-demographcs and temporal and clmate factors wth symptomatc P. falcparum nfecton over two years of survellance data, was assessed. Rsk factors for nfecton were determned usng a multvarate regresson model. The results showed 472 cases of symptomatc P. falcparum malara cases whch were dentfed among 23,372 resdents durng the study era. More than 85% of cases occurred durng the rany season from May to October, and were hghly crowded geographcally wthn these two unons wth more than 80% of nfectons occurrng n areas that contan approxmately one-thrd of the total populaton. Rsk factors statstcally assocated wth nfecton n a multvarate logstc regresson model were lvng n the areas of hgh ncdence, were young n age, and ther occupaton ncluded jhum cultvaton and/or daly labour. Use of long lastng nsectcde-treated bed nets was hgh (89.3%), but not assocated wth decreased ncdence of nfecton. The researchers concluded that P. falcparum malara contnues to be hypoendemc n the Chttagong Hll Dstrcts of Bangladesh, s hghly seasonal, and s much more common n certan geographcally lmted hot spots and among certan occupatons. In Ghana, malara caused about 8,200 llness daly and 3,000,000 yearly wth 3,000 deaths n the year 2010 (Natonal Malara Control Programme Annual Report 2010). The most vulnerable groups reman chldren under fve years of age and pregnant women (Asante & Asenso-Okyere 2003). Moreover, 25% of chldren who de before ther ffth brthday are klled by the dsease, whch also clams the lves of many pregnant women. Dagnoss of malara n chldren s dffcult wthout laboratory support because the symptoms and sgns of malara overlap wth those of other febrle llnesses such as pneumona (Olaleye et al. 1998). Malara s caused by the plasmodum parastes whch are transmtted by female anopheles mosquto. Despte consstent efforts to reduce malara epsodes that nclude chemcal sprayng, use of treated mosquto bed nets, clearng bushes, cleanng drans and subsdzed treatments, prevalence rates and malara ncdence, reman hgh. It s probable that the efforts to reduce malara do not specfcally take nto account the rsk factors lkely to aggravate malara dsease. Accordng to Bøgh et al. (2007), understandng local varablty n malara transmsson rsk s crtcally mportant when desgnng nterventon or vaccne trals. Ths study therefore endeavours to analyse the ncdence of malara epsodes usng quas-posson regresson model. The rest of the paper s organzed as follows: Secton 2 descrbes the concept of methods employed n the research and the data source. The emprcal analyss and results are presented n Secton 3. Secton 4 provdes the concludng remarks. 2. Data and Methods The malara data used n ths study was obtaned from the Out Patents Department (OPD) compled by the data management secton of the Obuas Government Hosptal n Ghana, whch provdes health servces to all people wthn the Obuas Muncpalty. The Muncpalty s one of the 27 dstrcts of the Ashant Regon of Ghana and was created as part of the Government effort to decentralse governance. The vegetaton s largely degraded and sem-decduous forest wth Gold mnng as the major occupaton of the natves. The data covers all the reported cases for the perod of January 2007 to December The data also 54

4 Journal of Bology, Agrculture and Healthcare ISSN (Paper) ISSN X (Onlne) establshes cases for males and females, as well as age categores (.e. from nfants to the aged). Snce malara cases are consdered as count data, a quas-posson regresson model was specfed to determne the rsk factors for malara nfectons. The covarates consdered nclude gender, age as well as quarterly tme perod of reported malara ncdence cases between 2007 and Specfcaton of the Model and Estmaton Generalzed Lnear Models The basc count data regresson models can be represented and understood usng the Generalzed Lnear Models (GLMs) framework (Nelder & Weddeburn 1992). GLMs descrbe the dependence of a scalar varable ( 1,..., n) x. The condtonal dstrbuton y = on a vector of regressors y xs a lnear exponental famly wth a probablty functon: y λ b ( λ ) f ( y; λ, φ ) = exp + c ( y, φ ) (1) φ where: λ s the canoncal parameter that depends on the regressors va a lnear predctor; φ s a dsperson parameter that s often known; b (.) and c(.) are known and determne whch member of the famly s used, for example, normal, bnomal or Posson dstrbutons Overdsperson Most count models are often overdspersed. Overdsperson s a stuaton where the varance exceeds the mean. A typcal example s the Posson regresson model whose assumpton of the mean beng equal to the varance s very restrctve and often volated, and hence overdspersed. Models such as Negatve bnomal, quas-posson, etc., relax the assumpton of overdsperson n fttng a model for count data Quas-Posson regresson model An alternatve way of dealng wth overdsperson s to use the mean regresson functon ' " E [ y x ] = µ = b ( y ) and the varance functon VAR[ y x ] =. b ( ) from Posson GLM, but leavng the dsperson parameter φ unrestrcted. Thus, φ s not assumed to be fxed at 1, but t s estmated from the data. Ths strategy leads to the same coeffcents as the standard Posson model, wth the excepton of nferences that are adjusted for overdsperson. Consequently, both models (quas-posson and sandwch-adjusted Posson) adopt the estmaton functon vew of the Posson model and do not correspond to fully specfed lkelhoods. As a result, a quas-posson regresson model shall be used to expound the ncdence of malara usng quarterly data between 2007 and 2010, and gender and age groups as covarates. 3. Emprcal Results and Dscusson Tables 1: Descrptve Statstcs of the Varables ( ) Varable Frequency Percentages Tme Trend Season Quarter Quarter Quarter Quarter Age group (years) Less than and above Gender Female Male The ncdence of malara accordng to the selected background characterstcs s shown n Table 1. Wthn the φ λ 55

5 Journal of Bology, Agrculture and Healthcare ISSN (Paper) ISSN X (Onlne) four-year year study perod, a total of 40,719 malara cases were documented at the hosptal, and t can be seen that there s an ncreasng trend of malara ncdence wheren the fourth year (2010) has about 4 tmes the ncdence n the startng year (2007). Ths means that, the ncdence of malara n the year 2010 ncreased four folds compared to The proporton of malara ncdence was found to be hgh wthn the fourth quarter of every year. Ths hghly reported cases of malara n the fourth quarter,.e. October to December, can be attrbuted to the rany season whch s known for promotng mosquto breedng n areas where water gets stagnant, and also n areas where there are unclean and chocked gutters. Fgure 1: Incdence of malara wth respect to covarates (quarters, age groups and gender) n Wth respect to the varous age groups, the proporton of malara ncdence was found to be hgh among nfants and chldren under 5 years of age as well as among adults aged 20 to 34 years. Moreover, ths hgh proporton of malara ncdence s also found to be hgh among females than males (see Fgure1). 3.1 Quas-Posson Model Specfcaton To analyse the ncdence of malara, the study ftted a quas-posson regresson model to the data avalable. The am was to analyse the ncdence of malara wth respect to age, gender and season (quarters of a year) wthn whch the cases were recorded (2007 and 2010). The model was selected based on lkelhood rato ch-square test, Quas Akake nformaton crteron and the resdual devance. Table 2: Parameter Estmates for Quas-Posson Regresson Model Varable Coeffcent Standard error P-value Confdence Interval (L25.5% - U97.5%) Odds rato Constant Gender Female Reference Male Age group(years) <5 Reference Season Quarter 1 Reference Quarter Quarter Quarter Lkelhood rato ch-square test Table 2 summarzes the maxmum lkelhood estmates of the parameters n the model. The coeffcents for all the varables are estmated relatve to a reference group. To evaluate the fnal model, a lkelhood rato test was performed to test the dfference between the null model,.e. model wthout any predctor and the ftted model. 56

6 Journal of Bology, Agrculture and Healthcare ISSN (Paper) ISSN X (Onlne) Based on the p-value of the lkelhood ch-square test, we rejected the null hypothess that the ftted model s sgnfcantly not dfferent from the null model. Thus, the selected model fts the data better, compared to the model wthout any predctor. From the results of the estmated model presented n Table 2, we observe that malara ncdence s less common among males than females. The estmate was found to be less than females. Gender dfference n malara ncdence s ndeed sgnfcant n the sense that norms and values nfluence dvson of labour, lesure patterns and sleepng arrangements, and eventually leads to dfferent patterns of exposures to mosqutos. When the consequence of age and prevalence of malara was measured, we found that the ncdence of malara was sgnfcantly low among the 10 to 14 year olds as well as 50 year olds and above, compared to chldren under 5 years. Nevertheless, t was sgnfcantly hgh amongst the 15 to 19 year age group compared to chldren under 5 years. The reason for chldren under 5 years of age beng mostly affected s probably because they have not yet developed the defensve mmunty aganst most severe forms of the dsease. Wth respect to the four quarters consdered, t was found that the ncdence of malara s sgnfcantly hgh n quarter four (.e. October to December), wth more than n quarter one. Ths fndng shows that transmsson also depends on clmatc condtons such as ranfall patterns, temperature and humdty - all of whch may affect the survval of mosqutos. In many places, transmsson s seasonal wth the peak durng and just after the rany season, hence accountng for the hgh ncdent rate n the last quarter. 4. Concluson Malara has been a long lfe-threatenng parastc dsease transmtted by female anopheles mosqutoes. Ths paper seeks to analyse the ncdence of malara at Obuas Government Hosptal n Ghana usng a quas-posson regresson model. Regardng the four-year perod, a total of 40,717 malara cases were reported at the hosptal. Agan, wthn the four-year perod, there was an ncreasng trend of malara ncdence wth the current year (2010) beng about 4 tmes the startng year (2007). Ths means that, the ncdence of malara n the year 2010 ncreased nearly 4 tmes compared to From the estmated quas-posson regresson model, the proporton of malara ncdence was found to be hgh wthn the thrd and fourth quarters of every year. Ths hghly reported cases of malara n the last two quarters (.e. July to December), can be attrbuted to the rany season whch promotes mosquto breedng. Wth respect to the varous age groups, the proporton of malara ncdence was found to be hgh among nfants and chldren under 5 years of age as well as adults aged 20 to 34 years. Moreover, ths hgh proporton of malara ncdence was also more common among the female group than the male group. The fndngs of ths research confrm those of Asante and Asenso-Okyere (2003), who establshed that 25% of chldren who de before ther ffth brthday are klled by the malara dsease, whch also clam the lves of many pregnant women. The hgh ncdence cases reported durng the last quarter also confrm the work done by Stresman (2010) whose study looked beyond temperature and precptaton - ecologcal rsk factors that modfy malara transmsson. It was revealed that temperature and water for breedng habtats are mportant prmary ecologcal factors that mpact the dstrbuton of malara vectors and the rate at whch mosquto and paraste develop, hence more cases n the last quarter. References Ahmed, S., Galagan, S., Scobe, H., Khyang, J., Prue, C.S., Khan, W.A.,... & Sack, D.A. (2013). Malara Hotspots Drve Hypoendemc Transmsson n the Chttagong Hll Dstrcts of Bangladesh. PloS one, 8(8), e Asante, F.A. & Asenso-Okyere K. (2003). Economc Burden of Malara n Ghana. Techncal Report Submtted to the World Health Organzaton (WHO), Afrca Regonal Offce (AFRO) Unversty of Ghana, Legon. Ba, L., Morton, L.C. and Lu, Q. (2013). Clmate Change and Mosquto-Borne Dseases n Chna: A Revew. Globalzaton and Health, 9(1), 10. Berrang-Ford, L., MacLean, J.D., Gyorkos, T.W., Ford, J.D. & Ogden, N.H. (2009). Clmate Change and Malara n Canada: A Systems Approach. Interdscplnary Perspectves on Infectous Dseases. Bøgh C., Lndsay S.W., Clarke, S.E., Dean A., Jawara, M., Pnder, M. & Thomas C.J. (2007). Hgh Spatal Resoluton Mappng of Malara Transmsson Rsk n The Gamba, West Afrca, usng LANDSAT TM Satellte Imagery. The Amercan Journal of Tropcal Medcne and Hygene, 76(5), Chyaka, C., Tatem, A.J., Cohen, J.M., Gethng, P.W., Johnston, G., Goslng, R.,... & Smth, D.L. (2013). The Stablty of Malara Elmnaton. Scence, 339(6122), Dans-Lozano, R., Rodríguez, M.H., Betanzos-Reyes, Á.F., Hernández-Avla, J.E., González-Cerón, L., Méndez-Galván, J.F.,... & Tapa-Conyer, R. (2007). Indvdual Rsk Factors for Plasmodum Vvax Infecton n the Resdual Malara Transmsson Focus of Oaxaca, Mexco. Salud Públca de Méxco, 49(3), Grod, R., Roux, E., Berger, F., Stefan, A., Gabort, P., Carnc, R.,... & Dusfour, I. (2011). Unravellng the Relatonshps between Anopheles Darlng (Dptera: Culcdae) Denstes, Envronmental Factors and Malara 57

7 Journal of Bology, Agrculture and Healthcare ISSN (Paper) ISSN X (Onlne) Incdence: Understandng the Varable Patterns of Malara Transmsson n French Guana (South Amerca). Annals of Tropcal Medcne & Parastology, 105(2), Gomez-Elpe, A., Otero, A., Van Herp, M. & Agurre-Jame, A. (2007). Forecastng Malara Incdence Based on Monthly Case Reports and Envronmental Factors n Karuz, Burund, Malara Journal, 6(1), 129. Guthmann, J.P., Llanos Cuentas, A., Palacos, A. & Hall, A.J. (2002). Envronmental Factors as Determnants of Malara Rsk. A Descrptve Study on the Northern Coast of Peru. Tropcal Medcne & Internatonal Health, 7(6), Greenwood, B.M. & Pckerng, H. (1993). A Malara Control Tral usng Insectcde-Treated Bed Nets and Targeted Chemoprophylaxs n a Rural Area of The Gamba, West Afrca: A Revew of the Epdemology and Control of Malara n The Gamba, West Afrca. Transactons of the Royal Socety of Tropcal Medcne and Hygene, 87(Supplement 2), Greenwood, B.M., Bradley, A.K., Greenwood, A.M., Byass, P., Jammeh, K, Marsh, K., Tulloch, S., Oldfeld, S.J. & Hayes, R. (1987). Mortalty and Morbdty from Malara among Chldren n a Rural Area of The Gamba, West Afrca. Transactons of the Royal Socety of Tropcal Medcne and Hygene, 81(3), Hakre, S., Masuoka, P., Vanze, E. & Roberts, D.R. (2004). Spatal Correlatons of Mapped Malara Rates wth Envronmental Factors n Belze, Central Amerca. Internatonal Journal of Health Geographcs, 3(1), 6. Jamson, D., Mosley, W.H., Measham, A. & Bobadlla, J.L. (1993). World Development Report: Investng n Health. Washngton, DC: World Bank. Kang, H., Kreuels, B., Adje, O., Krumkamp, R., May, J. and Small, D.S. (2013). The Causal Effect of Malara on Stuntng: A Mendelan Randomzaton and Matchng Approach. Internatonal Journal of Epdemology; 42: Klenschmdt, I., Sharp, B.L., Clarke, G.P.Y., Curts, B. & Fraser, C. (2001). Use of Generalzed Lnear Mxed Models n the Spatal Analyss of Small-area Malara Incdence Rates n KwaZulu Natal, South Afrca. Amercan Journal of Epdemology, 153(12), Koram, K.A., Bennett, S., Adamah, J.H. & Greenwood, B.M. (1995). Soco-Economc Rsk Factors for Malara n a Per-Urban Area of the Gamba. Transactons of the Royal Socety of Tropcal Medcne and Hygene: 89(2), Kudom, A.A. and Mensah, B.A. (2010). The Potental Role of the Educatonal System n Addressng the Effect of Inadequate Knowledge of Mosqutoes on Use of Insectcde-Treated Nets n Ghana. Malara Journal, 9, 256. Malara, R.B. (2014). The Global Malara Acton Plan-For a Malara-free World. Roll Back Malara Partnershp, Mathanga, D.P., Walker, E.D., Wlson, M.L., Al, D., Taylor, T.E. & Laufer, M.K. (2012). Malara Control n Malaw: Current Status and Drectons for the Future. Acta Tropca, 121(3), Mendez, F., Carrasqulla, G. & Muñoz, A. (2000). Rsk Factors Assocated wth Malara Infecton n an Urban Settng. Transactons of the Royal Socety of Tropcal Medcne and Hygene, 94(4), Mufunda, J., Nyarago, P., Usman, A., Gebremeskel, T., Mebrahtu, G., Ogbamaram, A., & Gebremchael, A. (2007). Roll Back Malara-an Afrcan success story n Ertrea, South Afrcan Medcal Journal, 97(1), Natonal Malara Control Programme Annual Report Republc of Ghana. Nelder J.A. & Weddeburn R.W.M. (1992). Generalsed lnear models. In Breakthroughs n Statstcs, Sprnger New York. Olaleye, B.O., Wllams, L.A., D alessandro, U., Weber, M.M., Mulholland, K., Okore, C., Lengerock, P., Bennett, S. and Greenwood B.M., (1998). Clncal Predctors of Malara n Gamba Chldren wth Fever or Hstory of Fever. Royal Socety of Tropcal Medcne and Hygene, 92(3), Olvera-Ferrera, J., Lacerda, M.V., Brasl, P., Ladslau, J.L., Taul, P.L. & Danel-Rbero, C.T. (2010). Revew Malara n Brazl: An Overvew. Malara Journal, 9, 115. Snow, R.W., Crag, M.H., Dechmann, U. & Le Sueur, D. (1999). A Prelmnary Contnental Rsk Map for Malara Mortalty among Afrcan Chldren. Parastology Today, 15(3), Stresman, G.H. (2010). Beyond Temperature and Precptaton: Ecologcal Rsk Factors that Modfy Malara Transmsson. Acta Tropca, 116(3), Texer, G., Machault, V., Barragt, M., Boutn, J.P. and Roger, C. (2013). Envronmental Determnant of Malara Cases among Travellers. Malara Journal, 12, 87. World Health Organzaton. (2000). World Health 2000-Health Systems: Improvng Performance. World Health Organzaton, Geneva, Swtzerland. World Health Organzaton. (2014). World Malara Report 2013: 286. Yewhalaw, D., Getachew, Y., Tushune, K., Kassahun, W., Duchateau L. & Speybroeck, N. (2013). The Effect of Dams and Seasons on Malara Incdence and Anopheles Abundance n Ethopa. BMC Infectous Dseases, 13(1), 161. Zacaras, O.P. & Andersson, M. (2010). Mappng Malara Incdence Dstrbuton that Accounts for Envronmental Factors n Maputo Provnce-Mozambque. Malara Journal, 9(1),

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