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Systematic Literature Review and Meta-Analysis of the Efficacy Of Saito et al. Malar J (2017) 16:488 https://doi.org/10.1186/s12936-017-2135-y Malaria Journal RESEARCH Open Access Systematic literature review and meta‑analysis of the efcacy of artemisinin‑based and quinine‑based treatments for uncomplicated falciparum malaria in pregnancy: methodological challenges Makoto Saito1,2,3*, Mary Ellen Gilder3, François Nosten2,3, Rose McGready2,3 and Philippe J. Guérin1,2 Abstract Background: There is no agreed standard method to assess the efcacy of anti-malarials for uncomplicated falcipa- rum in pregnancy despite an increased risk of adverse outcomes for the mother and the fetus. The aim of this review is to present the currently available evidence from both observational and interventional cohort studies on anti- malarial efcacy in pregnancy and summarize the variability of assessment and reporting found in the review process. Methods: Efcacy methodology and assessment of artemisinin-based treatments (ABT) and quinine-based treat- ments (QBT) were reviewed systematically using seven databases and two clinical trial registries (protocol registra- tion—PROSPERO: CRD42017054808). Pregnant women in all trimesters with parasitologically confrmed uncompli- cated falciparum malaria were included irrespective of symptoms. This review attempted to re-calculate proportions of treatment success applying the same defnition as the standard WHO methodology for non-pregnant populations. Aggregated data meta-analyses using data from randomized control trials (RCTs) comparing diferent treatments were performed by random efects model. Results: A total of 48 eligible efcacy studies were identifed including 7279 treated Plasmodium falciparum epi- sodes. While polymerase chain reaction (PCR) was used in 24 studies for diferentiating recurrence, the assessment and reporting of treatment efcacy was heterogeneous. When the same defnition could be applied, PCR-corrected treatment failure of 10% at any time points was observed in 3/30 ABT and 3/7 QBT arms. Ten RCTs compared dif- ferent combinations≥ of ABT but there was a maximum of two published RCTs with PCR-corrected outcomes for each comparison. Five RCTs compared ABT and QBT. Overall, the risk of treatment failure was signifcantly lower in ABT than in QBT (risk ratio 0.22, 95% confdence interval 0.07–0.63), although the actual drug combinations and outcome endpoints were diferent. First trimester women were included in 12 studies none of which were RCTs of ABT. Conclusions: Efcacy studies in pregnancy are not only limited in number but use varied methodological assess- ments. In fve RCTs with comparable methodology, ABT resulted in higher efcacy than QBT in the second and third *Correspondence: [email protected] 2 Centre for Tropical Medicine and Global Health, Nufeld Department of Medicine, University of Oxford, Old Road Campus, Roosevelt Drive, Oxford OX3 7FZ, UK Full list of author information is available at the end of the article © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Saito et al. Malar J (2017) 16:488 Page 2 of 17 trimester of pregnancy. Individual patient data meta-analysis can include data from observational cohort studies and could overcome some of the limitations of the current assessment given the paucity of data in this vulnerable group. Keywords: Malaria, Pregnancy, Efcacy, Artemisinin, Quinine, Methodology, Review Background With this in mind, this systematic literature review Approximately 60% of all pregnancies worldwide take aims to update the currently available efcacy data of place in malaria endemic areas, leading to 125 million artemisinin-based treatments (ABT) and QBT from both pregnant women at risk of malaria every year [1]. Malaria observational and interventional cohort studies in all tri- in pregnancy, regardless of whether it is clinically symp- mesters with uncomplicated falciparum malaria. Meth- tomatic or not, has been reported to be associated with odological challenges will also be summarized to improve a higher risk of preterm birth, low birth weight for ges- future efcacy studies in pregnancy. tational age, miscarriage, stillbirth and maternal anaemia [2–5]. Tese adverse outcomes lead to a higher risk of Methods perinatal mortality and maternal mortality in areas with A systematic literature review following PRISMA state- low or declining malaria prevalence compared to high ment [25] was conducted to identify studies measuring transmission areas because of lower levels of premuni- the efcacy of ABT or QBT in pregnant women with tion [6, 7]. parasitologically confrmed uncomplicated falciparum In order to mitigate these adverse efects, efcacious malaria, regardless of trimester or clinical symptoms. treatments need to be clearly identifed for pregnant Seven databases (MEDLINE, Embase, Global Health, women. However, several factors have limited the availa- Cochrane Library, Scopus, Web of Science and LILACS) ble evidence on anti-malarials efcacy during pregnancy. and two clinical trial registries (ICTRP and ClinicalTrial. Pregnant women are usually excluded from randomized gov) were used. Tis review is registered to PROSPERO control trials (RCTs) of new anti-malarials mainly (CRD42017054808), and the search terms and conditions because of concerns about the safety for the fetus. Safety are available in Additional fle 1. concerns were particularly critical for artemisinin deriva- Te search (conducted 9 July 2016–10 January 2017) tives, as fetal resorption was observed in animal studies combined fve components: malaria; pregnancy; treat- [8–13]. Quinine-based treatment (QBT) is still recom- ment or names of anti-malarial drugs; study design mended as the frst-line treatment for uncomplicated (interventional or observational cohort studies); and out- falciparum malaria in the frst trimester [14], despite lim- come types (efcacy) without limitation on publication ited clinical data on its safety in the frst trimester [15, year or language. Two reviewers (MS and MEG) assessed 16]. Quinine’s poor side efect profle and long treatment eligibility independently, and discrepant results were course of 5–7 days make it an undesirable choice for resolved by a second assessment. patients [15–17]. Recently, data from prospective obser- Both interventional and observational cohort studies vational cohort studies suggest that artemisinin use in the were included. Studies without any active follow-up in frst trimester did not increase the risks of stillbirth or the frst 28 days were excluded. Studies with fewer than congenital abnormality compared to quinine [3, 18–21], ten pregnant women were excluded, as they could not bringing the question of comparative efcacy into center be included in further meta-analyses. Systematic reviews stage. on the anti-malarial treatment in pregnancy [15, 26–29] Efcacy of anti-malarial drugs for treating uncompli- were checked for any other possible missing articles that cated malaria in non-pregnant patients has traditionally should be included. been assessed over a fxed follow-up period set by the Uncomplicated Plasmodium falciparum malaria was current World Health Organization (WHO) recommen- defned as malaria infection without features of severe dations at 28–42 days [22]. However, this fxed period malaria [14]. Pregnancy was described by trimesters: does not accommodate the pregnant condition as the the frst as < 13 completed weeks, the second as from placenta may become or remain parasitized (placental 14 weeks to 27 completed weeks, and the third from sequestration) after treatment completion [23]. Tere are 28 weeks until delivery. currently no standard guidelines on parasitological ef- After screening, the following data were extracted: cacy studies in pregnancy [24]. demographic information of study (year, country, study Saito et al. Malar J (2017) 16:488 Page 3 of 17 design, study drugs and eligibility criteria), availability of funnel plots [35]. STATA MP 14.2 (Stata Corp, Texas, of outcome assessment (clinical outcomes, parasitologi- US) was used for the statistical analyses. cal outcomes) and the methodology of assessment of variables (defnition of treatment success and statisti- Results cal method). Information was sought from published A total of 48 study cohorts assessing treatment efcacy articles, clinical trial registry and protocols if available. for uncomplicated falciparum malaria in pregnancy Missing information was supplemented by personal cor- were identifed (see Additional fle 2) evaluating at least respondence to authors of the original studies if possible. 7279 episodes of parasitologically confrmed uncom- Tis review describes the methodology of assessment plicated falciparum. Studies based on the same cohort and reporting, and summarizes the reported efcacy were considered as a single study. Forty-one studies were results. Comparisons were made only if the same or simi- published, fve presented at conferences, and two were lar assessment methods were used. registered on a public trials database but not yet pub- Te WHO recommends
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