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Persistence of Chloroquine Resistance Alleles in Malaria Endemic Countries

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Persistence of Chloroquine Resistance Alleles in Malaria Endemic Countries Ocan et al. Malar J (2019) 18:76 https://doi.org/10.1186/s12936-019-2716-z Malaria Journal RESEARCH Open Access Persistence of chloroquine resistance alleles in malaria endemic countries: a systematic review of burden and risk factors Moses Ocan1,8* , Dickens Akena2,5, Sam Nsobya3, Moses R. Kamya4, Richard Senono5,8, Alison Annet Kinengyere6,8 and Ekwaro A. Obuku7,8,9 Abstract Background: Chloroquine, a previous highly efcacious, easy to use and afordable anti-malarial agent was with- drawn from malaria endemic regions due to high levels of resistance. This review collated evidence from published- reviewed articles to establish prevalence of Pfcrt 76T and Pfmdr-1 86Y alleles in malaria afected countries following ofcial discontinuation of chloroquine use. Methods: A review protocol was developed, registered in PROSPERO (#CRD42018083957) and published in a peer- reviewed journal. Article search was done in PubMed, Scopus, Lilacs/Vhl and Embase databases by two experienced librarians (AK, RS) for the period 1990-to-Febuary 2018. Mesh terms and Boolean operators (AND, OR) were used. Data extraction form was designed in Excel spread sheet 2007. Data extraction was done by three reviewers (NL, BB and MO), discrepancies were resolved by discussion. Random efects analysis was done in Open Meta Analyst software. Heterogeneity was established using I2-statistic. Results: A total of 4721 citations were retrieved from article search (Pubmed 361, Lilac/vhl 28, Science Direct 944, Scopus 3388). Additional targeted search resulted in three (03)= eligible articles.= After removal of duplicates= (n 523) and= screening, 38 articles were included in the fnal review. Average genotyping success rate was 63.6% (18,343/28,820)= for Pfcrt K76T and 93.5% (16,232/17,365) for Pfmdr-1 86Y mutations. Prevalence of Pfcrt 76T was as follows; East Africa 48.9% (2528/5242), Southern Africa 18.6% (373/2163), West Africa 58.3% (3321/6608), Asia 80.2% (1951/2436). Prevalence of Pfmdr-1 86Y was; East Africa 32.4% (1447/5722), Southern Africa 36.1% (544/1640), West Africa 52.2% (1986/4200), Asia 46.4% (1276/2217). Over half, 52.6% (20/38) of included studies reported continued unofcial chloroquine use following policy change. Studies done in Madagascar and Kenya reported re-emergence of chloroquine sensitive parasites (IC50 < 30.9 nM). The average time (years) since discontinuation of chloroquine use to data collection was 8.7 7.4. There was high heterogeneity (I2 > 95%). ± Conclusion: The prevalence of chloroquine resistance alleles among Plasmodium falciparum parasites have steadily declined since discontinuation of chloroquine use. However, Pfcrt K76T and Pfmdr-1 N86Y mutations still persist at moderate frequencies in most malaria afected countries. Keywords: Chloroquine, Re-emergence, Sensitivity, Plasmodium falciparum, Policy *Correspondence: [email protected] 1 Department of Pharmacology & Therapeutics, Makerere University, P.O. Box 7072, Kampala, Uganda Full list of author information is available at the end of the article © The Author(s) 2019. 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. Ocan et al. Malar J (2019) 18:76 Page 2 of 15 Background Search strategy Chloroquine was once an important medicine used in Electronic search malaria treatment especially due to its afordability, ease Electronic search for Pubmed data base is reported in of use and high anti-malarial efcacy. However, due to the published protocol [11]. Te search terms were com- high level of resistance among Plasmodium falciparum bined using Boolean logic ‘OR’ for synonymous terms parasites, chloroquine was withdrawn from malaria and ‘AND’ across elements of PECOS (Population, Expo- treatment in most malaria endemic countries [1]. It is sure, Comparison, Outcome and Study design). estimated that the loss of chloroquine to resistance was Te search terms used included, Chloroquine, ‘Antima- responsible for more than doubling of malaria-associated larial drug’, 4-aminoquinoline, ‘antimalarial agent’, Amo- mortality in sub-Saharan Africa, a region which bears diaquine, piperaquine, ‘Plasmodium falciparum’, ‘malaria over 90% of malaria burden [2, 3]. parasites’, ‘parasite sensitivity’, sensitivity’, ‘susceptibil- Chloroquine resistance reached fxation levels across ity’, ‘parasite susceptibility’, extent, spread, prevalence, malaria endemic countries by late 1990s [4]. As a result occurrence, proportion, frequency, resistance, ‘resistance artemisinin agents and their derivatives were introduced alleles’, ‘resistance mutations’, polymorphisms, ‘resistance in malaria treatment and have since been the frst-line reversal’, ‘Pfcrt K76T’, ‘Pfmdr1 N86Y’, ‘resistance reversal’, anti-malarial agents [3]. Te use of artemisinin-based mutations, ‘1990-to-February 2018’. Te search terms combination therapy (ACT) in malaria treatment, how- were restricted to title and abstract during article search ever, is limited by the high cost, pill burden and currently in each data base. Tere was no language restriction in emerging risk of decreased P. falciparum parasite sensi- article search, articles not published in English were tivity [5–7]. Due to lack of current efective alternative translated using Google translator before screening for agents to ACT, malaria treatment faces uncertain future inclusion or exclusion. which could expose populations most afected by the dis- ease to the risk of increased malaria-associated mortality Additional searches as previously seen with chloroquine [2]. Recent studies have indicated emergence of P. falci- Te reference lists of included articles were screened and parum parasites susceptible to chloroquine following for any reference that could potentially be eligible for cessation of its use [4, 8]. However, considerations to inclusion in the review, a full text article was retrieved. re-introduce chloroquine in malaria treatment is faced In addition, authors of included articles were contacted with the challenge of inadequacy of information on cur- for any relevant publications on the review topic but did rent extent of chloroquine sensitivity and the uncertainty obtain any response. over how this might afect future resistance. Te current review was intended to collate evidence and provide cur- Data management rent evidence on genotypic and phenotypic chloroquine All article citations retrieved from database searches resistance among P. falciparum parasites in malaria were exported into EndNote software version X7 (Tom- afected countries. son Reuters, 2015) and duplicates removed. Te articles were grouped into relevant categories as indicated in the PRISMA fow diagram (Fig. 1). Methods Protocol development A systematic review protocol was developed following Selection of studies in the review STREGA [9] and PRISMA-P [10] guidelines. Te proto- Eligibility criteria col was registered in International Prospective Register Te titles and abstracts were screened using a priori crite- of Systematic Reviews, PROSPERO (#CRD42018083957, ria [11]. Articles that reported on at least one of the chlo- http://www.crd.york.ac.uk/prosp ero) and published in a roquine resistance alleles, Pfcrt K76T or Pfmdr1-N86Y peer-reviewed journal [11]. were considered for inclusion. Articles that reported prevalence of the above chloroquine resistance alleles and genotyped more than 300 P. falciparum DNA sam- Review question ples were included. Studies that reported multiple para- Te review sought to establish the prevalence of Pfcrt site resistance genotype infections among patients were K76T and Pfmdr1 N86Y alleles among Plasmodium fal- included in the review. Studies that assessed prevalence ciparum parasites in malaria afected countries since of resistance alleles (Pfcrt K76T or Pfmdr1-N86Y) fol- ofcial discontinuation of chloroquine use in malaria lowing cessation of chloroquine use in malaria treatment treatment. were included. Te review included studies that assessed Ocan et al. Malar J (2019) 18:76 Page 3 of 15 Records identified through database n searching Additional records identified (PubMed = 361; LILACS/VHL=28; through other sources Science Direct = 944; Scopus=3,388 (n = 03) Idenficao Records excluded (n = 3834) Not molecular CQR = 639 Reviews = 100 Records after duplicates removed Not done in humans = 19 (n = 522) Reports/letter to editor = 43 g Policy/communication = 178 Non-Plasmodium falciparum = 203 Malaria disease = 1, 116 Screenin Other drugs/insecticides = 1, 218 Records screened Other diseases/pathogens = 259 (n = 4,198) Methods/drug development = 59 y Full-text articles assessed Full-text articles excluded (n =326) for eligibility Non Pfcrt/Pfmdr 1 mutations = 12 (n = 364) Eligibilit Other antimalarial agents = 21 Efficacy studies (In vitro/In vivo) = 22 Epidemiological studies = 83 Genetic/Haplotype studies = 31 Articles, few DNA samples (<300) = 136 Data collection year not indicated = 07 CQ use was not yet stopped = 03 d No reported SNPs of interest = 03 Done only prior to CQ policy change = 06 Studies included in Could not retrieve full text = 02
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