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      Perceptions and practices for preventing malaria in pregnancy in a peri-urban setting in south-western Uganda

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          Abstract

          Background

          Malaria in pregnancy contributes greatly to maternal morbidity and mortality in Uganda. Thus it is urgent to identify possible barriers that limit access to existing interventions. The aim of this study was to assess perceptions and practices regarding malaria prevention during pregnancy in a peri-urban area and explore ways to scale-up malaria prevention interventions, since little is known about malaria in peri-urban settings.

          Methods

          A survey was conducted in Kabale municipality south-western Uganda from April–June, 2015. Data was collected using a structured questionnaire targeting pregnant women, who delivered in the study area 1 year prior to the survey. Univariate analyses were performed at assess the level of knowledge and practices on malaria prevention during pregnancy.

          Results

          A total of 800 women was interviewed. The majority of women, 96.1 % knew that malaria was a dangerous disease in pregnancy; 60.3 % knew that it caused anaemia, and 71.3 % associated malaria with general weakness. However, fewer women (44.9 %) knew that malaria in pregnancy caused abortions, while 14.9 % thought it caused stillbirths. Similarly, few women (19 %) attended the recommend four antenatal care visits; less than a half (48.8 %) accessed two doses of sulfadoxine-pyrimethamine (SP) for malaria prevention in pregnancy while 16.3 % received at least three doses of SP, as recommended by the current policy. The main reasons for poor antenatal care attendance were: women felt healthy and did not see a need to go for antenatal care, long distances and long waiting hours at clinics. The reasons given for not taking SP for malaria prevention were: women were not feeling sick; they were not aware of the benefits of SP in pregnancy, they were sleeping under insecticide-treated nets; fear of side effects of SP; and the antenatal care clinics were far.

          Conclusion

          Despite a good knowledge that malaria is a dangerous disease in pregnancy, there was poor access to antenatal care and use of SP for malaria prevention in pregnancy. There is urgent to address existing health system constraints in order to increases access to malaria prevention in pregnancy in this setting.

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          Most cited references20

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          Factors Affecting the Delivery, Access, and Use of Interventions to Prevent Malaria in Pregnancy in Sub-Saharan Africa: A Systematic Review and Meta-Analysis

          Introduction Malaria in pregnancy can have important consequences for the mother, foetus, and newborn child, yet the harmful effects are preventable [1]. The adverse outcomes of malaria in pregnancy can be substantially reduced by interventions that have been available for over two decades [2]–[4] and that are inexpensive and cost-effective [5]. Access to and use of these interventions by pregnant women is, however, extremely low, representing a failure of the public health community. In areas of stable malaria transmission in Africa the World Health Organization (WHO) recommends a package of intermittent preventive treatment in pregnancy (IPTp) with sulphadoxine–pyrimethamine (SP) and use of insecticide-treated nets (ITNs), together with effective case management of clinical malaria and anaemia [6]. IPTp consists of two doses of SP taken 1 mo apart commencing in the second trimester [7],[8]. Both IPTp and ITNs are commonly delivered through antenatal clinics (ANCs) through collaboration between malaria and reproductive health programmes. The Roll Back Malaria Partnership aims to ensure that all pregnant women receive IPTp and at least 80% of people at risk from malaria in areas of high-intensity transmission use ITNs by 2010 [9], with even more ambitious targets of 100% for both interventions by 2015 [10]. Achievement of high coverage of these preventive interventions among pregnant women remains elusive for many countries in sub-Saharan Africa [11],[12]. A recent review of national survey data shows that in 27 countries with survey data between the years 2009 and 2011, the median coverage of two doses of SP was 24.5% (range 7.3%–69.4%), even though the median coverage for at least two ANC visits was 84.6% (range 49.7%–96.9%, 22 countries, 2003–2011) (A. M. van Eijk, personal communication), representing substantial missed opportunities at ANCs. Despite the call for universal ITN coverage [13] and all 45 malaria-endemic countries having a policy of providing ITNs to pregnant women, the median use of an ITN the previous night among pregnant women in 37 countries from survey data for the years 2009–2011 was 35.3% (range 5.2%–75.5%) (A. M. van Eijk, personal communication). According to a Countdown to 2015 report, in 20 countries with data, IPTp and ITNs, together with case management of malaria during pregnancy, have the lowest coverage among all the interventions delivered to pregnant women at ANCs [14]. Evidence on the determinants of coverage and reasons for the failure in delivery and uptake of IPTp and ITNs from qualitative [15] and quantitative studies is currently disparate, in addition to which, many relevant reviews are now outdated [5],[16]–[18]. We therefore undertook a systematic review to update the evidence and to integrate findings from three separate syntheses of studies on (1) barriers to achieving high coverage, (2) determinants of uptake, and (3) interventions to increase coverage. We then explored the extent to which the intervention studies have addressed known barriers and determinants, and identified critical gaps in the knowledge required for the formulation of effective strategies. The review was restricted to sub-Saharan Africa as the only malaria-endemic region with a specific WHO strategy for the prevention of malaria in pregnancy, which includes both IPTp with SP and ITNs. Methods Search Strategy We performed a systematic and comprehensive literature search of electronic databases on 23 April 2013, including the Malaria in Pregnancy Library (http://library.mip-consortium.org; updated 20 April 2013) and the Global Health Database [19], and a search of bibliographies of retrieved articles. The Malaria in Pregnancy Library contains peer-reviewed published and unpublished literature compiled from 40 sources including PubMed, the Global Health Library, Google Scholar, Lilacs (Latin American and Caribbean Health Sciences Literature), Popline, the ProQuest Digital Dissertations and Theses database, Web of Knowledge, WorldCat, and registers of trials and studies [20]. A full account of the search terms used is presented in Table S1. Study Inclusion Criteria and Analysis Strategy Titles and abstracts were reviewed independently by two authors (J. Hill and J. Hoyt/A. M. van Eijk). Studies were eligible for inclusion if they met the following criteria: (1) reported an original research study; (2) addressed barriers to, facilitators of, or determinants of the delivery or uptake of IPTp and/or ITNs in pregnancy, or evaluated the impact of an intervention to increase the coverage of IPTp and/or ITNs in pregnancy; (3) were published between 1 January 1990 and 23 April 2013; and (4) were conducted in sub-Saharan Africa. No restrictions were placed on publication language or study design, i.e., quantitative, qualitative, and mixed methods studies were included, and both peer-reviewed papers and grey literature were included. Studies meeting the inclusion criteria were grouped according to whether their content addressed (1) barriers or facilitators, (2) determinants, and/or (3) evaluation of intervention(s); some studies contributed to more than one of these content groups (Figure 2). Studies with content on barriers or facilitators and/or determinants were then further categorised into studies exploring factors among pregnant women, healthcare providers, or both. Studies with content on delivery interventions were categorised by intervention, i.e., IPTp, ITNs, or both. The kappa statistic was used to measure the chance-adjusted inter-rater agreement for eligibility. Data Extraction Two authors extracted data and appraised the quality and content of included studies. J. Hill and J. Hoyt/A. M. van Eijk extracted quantitative and qualitative data on barriers and facilitators from quantitative, qualitative, and mixed methods studies using pre-existing themes used by the authors of the included studies, which were stratified according to whether the views or perspectives were those of pregnant women or healthcare providers; the views or perspectives mainly comprised self-reported information but also observed data. The barrier and facilitator themes were then divided into four predetermined categories adapted from the literature [21],[22] for pregnant or postpartum women (Box 1) and for healthcare providers (Box 2). Because facilitators uniformly reflected the converse of the barriers, we report only the barriers (Table S4). A. M. van Eijk and J. Hoyt/L. D'Mello-Guyett extracted quantitative data from quantitative and mixed methods studies that explored the determinants of receipt of one or two doses of IPTp and ITN ownership and use, henceforth referred to as “determinants”. J. Hill and J. Hoyt/L. D'Mello-Guyett extracted quantitative, qualitative, and descriptive data from the studies evaluating delivery strategies for IPTp and/or ITNs according to the type of delivery intervention, e.g., promotion, training, or type of delivery mechanism. Box 1. Barriers from the Women's Perspective by Level Individual level: factors related to a woman's knowledge, thoughts, beliefs, actions and behaviour, pregnancy, and health status Social/cultural/household level: factors related to a woman's economic and social position, household factors including gender roles, societal and cultural norms and traditions, and religious practices Environmental level: factors related to seasonality of malaria, weather conditions, physical access, and transportation Healthcare system level: factors related to the various components and quality of the healthcare system, such as staff attitudes or performance, medication, service provision, and user fees Box 2. Barriers from the Healthcare Provider Perspective by Level Individual level: factors related to the knowledge, attitudes, and performance of individual healthcare providers Organisational level: factors related to the operation of the health facility unit, such as management, staff rosters/rotation, and services Healthcare system level: factors that are dependent on higher levels of the healthcare system related to the various components and quality of services, such as supply of drugs or ITNs, development and dissemination of policy guidelines, training and supervision of staff, and imposition of user fees Non-Healthcare system: macro-level factors external to the healthcare system such as media, water supply, side effects of medications, and women's practices Two authors (J. Hill and J. Hoyt/L. D'Mello-Guyett) assessed the quality of reporting of individual studies using a checklist of criteria developed a priori based on criteria and methods described in the literature. For observational quantitative studies the criteria of reporting were randomised sample selection, multivariate analysis, and minimising bias through study design and analysis [23],[24]. For qualitative studies the criteria were the extent to which the authors described the sampling strategy, the effects of reflexivity, and methods to ensure reliability and validity [25],[26]. For mixed methods studies, the following reporting criteria were used: justification of mixed methods, clearly described sampling strategy, clear reporting of methods for the qualitative component, analysis strategy, multivariate analyses, minimising bias, and integration of qualitative and quantitative findings [27],[28]. For intervention studies, reporting criteria were presence/type of control, steps to reduce bias, and the extent to which authors described confounding, loss to follow-up, and external validity [29]. No studies were excluded on the basis of quality. Data Synthesis Barriers and facilitators were described and explored using content analysis and narrative synthesis of qualitative and quantitative data. Data from the pregnant women's perspective were synthesised across four levels (individual, household/social/cultural, healthcare system, and environmental) and assessed in relation to receipt of IPTp, ITN ownership, and ITN use. Similarly, data from the healthcare provider perspective were synthesised across four levels (individual, organisational, healthcare system and non-healthcare system) and assessed in relation to the delivery of IPTp and ITNs in the ANC setting. The intervention studies were grouped into common strategies and explored using a narrative synthesis to summarise each intervention and to compare and contrast findings between studies evaluating similar strategies for scaling up one or both malaria interventions. Statistical Analysis We conducted a meta-analysis of data on determinants using Stata version 12 (StataCorp) and Comprehensive Meta-Analysis (Biostat, http://www.meta-analysis.com/). Summary odds ratios (ORs) were calculated using random effects models based on the approach of DerSimonian and Laird [30]. Data were extracted from studies using the following hierarchy based on availability: raw data (numerators and denominators); computed unadjusted ORs, computed adjusted ORs. The use of adjusted (by multivariate analysis) or cluster-adjusted ORs as provided by the studies is indicated in the meta-analysis forest plots. If studies presented results for both “1+ doses” and “2+ doses” of IPTp, only the data for “2+ doses” was used. We conducted sub-group analysis and considered the following factors for IPTp: number of SP doses (1+ or 2+), location of enrolment (community or clinic), study population (postpartum women, a mixed population of postpartum and pregnant women, or pregnant women only), and study country. The subgroup analysis for ITNs considered location of enrolment (community or health facility), study population (postpartum women, a mixed population of postpartum and pregnant women, or pregnant women only), study country, and—for ITNs—type of net (ITN or untreated net) and definition of net use (last night or during pregnancy). Sensitivity analysis was conducted to assess the potential effect of study quality on the examined associations. We assigned studies a score based on the quality assessment, and studies that failed to report on three or more quality criteria scored as low-to-moderate quality. The I 2 and 95% CI were used to quantify heterogeneity [31]. Synthesis across the Barriers, Determinants, and Intervention Studies We compared identified barriers with the determinants identified in the meta-analysis and aligned them with the intervention studies. The barriers were first collapsed into a limited number of key categories using a coding template, and the implications for intervention for each category of barriers were described. We then matched the proposed interventions derived from the barrier studies against the intervention studies included in the review to assess the extent to which the intervention studies addressed the barriers identified in the observational studies. Results Study Selection and Characteristics The primary search identified 1,780 citations (1,240 from the Malaria in Pregnancy Library, 540 from the Global Health Database, and two from bibliographies and authors), from which 271 duplicates were removed (Figure 1). From the remaining 1,511, 1,280 articles were excluded on the basis of abstracts. Of 231 full-text articles reviewed, 133 were excluded as they did not meet the inclusion criteria, the full text was not available, or they contained duplicate data, leaving 98 included articles. There was close agreement between reviewers on the included studies (kappa score of 0.86). 10.1371/journal.pmed.1001488.g001 Figure 1 Flowchart of studies included in the review. 10.1371/journal.pmed.1001488.g002 Figure 2 Analysis strategy. MiP, malaria in pregnancy. Of the 98 included studies, 81 contributed data on barriers and determinants (Table 1), and 20 studies contributed data on interventions that aimed to increase coverage and uptake of IPTp (Table 2) or ITNs (Table 3). One study did not contain data in a usable format for the meta-analysis [32]. The key characteristics of the barrier and determinant studies and of the intervention studies are provided in Table S2. 10.1371/journal.pmed.1001488.t001 Table 1 Data extracted for barriers and determinants by study. Study IPTp ITN Facility-based surveys Barriers Determinants Barriers Determinants Akaba 2013 [34] √ √ √ √ De Allegri 2013 [82] √ √ Aluko 2012 [71] √ √ Amoran 2012a [35] √ √ Amoran 2012b [72] √ √ Arulogun 2012 [55] √ Bouyou-Akotet 2013 [113] √ Diala 2012 [40] √ Iliyasu 2012 [36] √ √ Mubyazi 2012 [63] √ Mutagonda 2012 [43] √ Namusoke 2012 [59] √ Onoka 2012a [37] √ √ Onoka 2012b [114] √ Onwujekwe 2012 [61] √ d'Almeida 2011 [115] √ Donkor 2011 [48] √ Manirakiza 2011 [116] √ √ Napoleon 2011 [117] √ √ Nduka 2011 [118] √ Okonta 2011 [73] √ √ Olajide 2011 [74] √ √ Tutu 2011 [119] √ Smith Paintain 2011 [64] √ Gross 2011 [33] √ Ambrose 2011 [77] √ Sande 2010 [45] √ √ Antwi 2010 [53] √ √ Mubyazi 2010 [52] √ √ Smith 2010 [47] √ Karunamoorthi 2010 [67] √ √ Wagbatsoma 2010 [120] √ Akinleye 2009 [121] √ Takem 2009 [122] √ Klebi 2009 [123] √ Musa 2009 [69] √ Njoroge 2009 [65] √ √ Adjei 2009 [49] √ √ Mubyazi 2008 [18] √ Pettifor 2008 [76] √ √ Anders 2008 [56] √ Onyeaso 2007 [60] √ √ Mnyika 2006 [124] √ Launiala 2007 [44] √ Brentlinger 2007 [62] √ √ Kweku 2007 [83] √ Van Geertruyden 2005 [78] √ √ Gates Malaria Partnership 2005 [39] √ Mubyazi 2005 [41] √ Nganda 2004 [125] √ √ √ Ashwood-Smith 2002 [54] √ Community-based surveys Hill 2013 [126] √ √ Ankomah 2012 [80] √ √ Ansah-Ofei 2011 [46] √ Auta 2012 [81] √ √ Zere 2012 [127] √ √ √ Faye 2011 [128] √ O'Meara 2011 [85] √ Ndyomugyenyi 2010 [50] √ √ Grietens 2010 [51] √ Sangare 2010a [57] √ √ Mbonye 2010 [129] √ Sangare 2010b [70] √ √ Beiersmann 2010 [84] √ Acquah 2009 [130] √ Brabin 2009 [42] √ Gies 2009 [90] √ Gikandi 2008 [131] √ √ Marchant 2008 [58] √ √ Belay 2008 [79] √ √ Hassan 2008 [132] √ Kiwuwa 2008 [133] √ √ Ouma 2007 [91] √ PSI Burundi 2006 [134] √ PSI Rwanda 2006 [135] √ PSI Zambia 2006 [136] √ Mbonye 2006a [38] √ Mbonye 2006b [66] √ van Eijk 2005 [68] √ √ √ Guyatt 2004 [137] √ √ √ Marchant 2002 [75] √ √ Summary total 38 31 28 27 10.1371/journal.pmed.1001488.t002 Table 2 Evaluation of interventions aimed at increasing coverage of IPTp (six studies). Study/Measure Description (Country) Baseline Point of Evaluation Intervention (Percent) Control (Percent) p-Value Intervention (Percent) Control (Percent) p-Valuea p-Valueb Msyamboza 2009 [86] IPTp delivered by community health workers (Malawi) IPTp 2+ 36/87 (41.4) 47/107 (43.9) 0.77 663/912 (72.7) 412/897 (45.9) 19 y) and married women were the most likely to use an ITN. Women with higher education or greater knowledge of malaria or ITNs were more likely to use ITNs than women with lower education or less knowledge, and women who were employed in a wage-paying job were also more likely to use ITNs during pregnancy than farmers or housewives. Women who had received IPTp were more likely to use ITNs. The effect of education on ITN use showed significant variation by country (p = 0.028; Text S2), and the effect of marital status on ITN use varied significantly by location of enrolment (p = 0.001; Text S2). Sensitivity analysis indicated a stronger association between ITN use and marital status in the low-to-moderate quality studies compared to the better quality studies (Text S2). 10.1371/journal.pmed.1001488.g004 Figure 4 Summary odds ratios of determinants of ITN use assessed in 17 studies with quantitative data. SES, Socio-economic status. Intervention Studies Interventions to increase coverage of IPTp The evidence from four studies that evaluated community-based distribution of IPTp suggests that community resources have the potential to complement the delivery of IPTp through ANCs to increase access to and uptake of IPTp among pregnant women [86]–[89] (Table 2). However, there was evidence that community-based distribution may concurrently reduce women's attendance at ANCs, though this was not consistent across the four studies: two studies showed reduced ANC attendance in the intervention sites [86],[87], and two showed increased ANC attendance [88],[89]. An alternative to delivering IPTp through community-based programmes is to employ community-based resource persons to promote IPTp, while referring women to ANCs to be given SP. This approach had substantial success in Burkina Faso, and resulted not only in higher IPTp coverage (71.8% versus 49.2% in intervention and control groups, respectively; p<0.001) but also in women attending the ANC earlier, in their first or second trimester (81.3% versus 70.4% in intervention and control groups, respectively; p<0.001), and in more women making two or more visits (89.3% versus 75.3% in intervention and control groups, respectively; p<0.001) [90]. One intervention study evaluated strategies to improve healthcare provider knowledge and performance on how to deliver IPTp. The study was undertaken in Kenya, 4 y after the national IPTp policy was adopted, and suggests that retraining of healthcare providers on the delivery, timing, and dosing of IPTp significantly increased coverage of IPTp (36.9% versus 10.9% in intervention and control groups, respectively; p<0.001) [91]. Interventions to increase coverage of ITNs The included intervention studies evaluated two main channels for delivering ITNs to pregnant women: campaign delivery (non-targeted) [89],[92]–[94] and routine delivery to pregnant women through ANC services (targeted), with three alternative mechanisms evaluated at ANCs: distribution of free nets with [95]–[97] or without social marketing [98],[99], and distribution of subsidised vouchers [83],[84],[100]–[102]. One study compared the impact of ANC delivery alone versus ANC delivery plus community-based distribution of subsidised nets in Niger (Table 3). Campaign delivery of ITNs to households with pregnant women [89], households with children under 5 y [94], or poor households [93] had limited impact on increasing coverage among pregnant women with one exception, which was a campaign in Senegal that delivered ITN vouchers to all households with children under 5 y, alongside vitamin A and mebendazole (an anthelmintic) [92] (49.2% versus 28.5% ITN coverage in intervention versus control groups, respectively; no statistical analysis reported). In a comparison study in Tanzania, the Tanzania National Voucher Scheme, which provides a voucher subsidy to pregnant women at ANCs, which is then used to purchase an ITN from a contracted retailer, achieved greater coverage than a 3-d mass campaign targeting ITNs to households with infants, based on the assumption that infants sleep with their mothers, a common practice in this setting, or ITNs sourced from retailers [94]. The voucher scheme was, however, inequitable, with fewer poorer women receiving nets [100]. In a comparison study of routine ANC delivery of ITNs alone and ANC delivery plus community-based distribution, there was no significant difference in ITN use among pregnant women between groups [103]. Routine delivery of ITNs through ANCs, by comparison, appeared to be more successful in reaching pregnant women, with four studies demonstrating an increase in ITN coverage among pregnant women compared to baseline [98],[99],[101],[102]. Programmes that delivered vouchers, as opposed to free nets, to women at ANCs experienced more operational challenges [83], and were dependent on retailers having ITN stock available [84]. Social marketing campaigns have been effective in promoting the use of ITNs in some settings through extensive media and educational campaigns that increase awareness about the benefits and importance of ITN use (especially for pregnant women), coupled with provision of readily available ITNs at low cost. They are, however, comparatively expensive to implement and sustain [104]. Implications for Interventions to Address Barriers We aligned the barriers to uptake of IPTp and ITNs against the findings from the intervention studies to determine the extent to which these interventions addressed known barriers (Tables 4 and 5). There were four key categories of barriers to women receiving IPTp: pregnant women's knowledge of IPTp, access to an ANC, affordability of ANC services, and quality of ANC services. Women's lack of knowledge of IPTp was very common and yet may be improved through relatively simple promotional activities delivered through all available channels, such as community-based resource persons, facility-based counselling and education, and messaging via the media and local leaders. We identified only one relevant intervention study, which evaluated community-based promotion of IPTp in Burkina Faso [90]. Women's access to an ANC was a barrier in remote settings, where community-based distribution or outreach services may be required to supplement ANC services. Four studies evaluating community-based distribution of IPTp were identified in the review, using a combination of existing [87],[88] or new community resource persons [86],[89]. 10.1371/journal.pmed.1001488.t004 Table 4 Synthesis matrix comparing findings from observational studies with those of intervention studies for IPTp. Type of Factor Findings from Observational Studies Findings from Intervention Studies Categories Derived from Barriers Implications for Interventions to Increase Uptake Type of Intervention Evaluated Number of Intervention Studies Pregnant women factors Category 1—pregnant women's knowledge Example barriers• Lack of knowledge of the preventive benefits of IPTp• Belief that use of drugs or SP in pregnancy is unsafe, e.g., could cause abortion• Fear of perceived side effects of SP• Unaware of the dangers of malaria in pregnancy Promotion of IPTp strategy and safety of SP for IPTp through a variety of channels, e.g., community-based, clinic-based, media, local leaders Community-based promotion of IPTp and referral of women to ANC 1 study in Burkina Faso (Gies 2009 [90]) Category 2—access to ANC Example barriers• Poor access to ANC• Direct and indirect costs of accessing ANC• Commitments to farming, employment, or childcare• Unwillingness to reveal pregnancy• Lack of awareness of importance of ANC services Community-based distribution of IPTp in hard-to-reach populations with limited access to ANC, e.g., through community-based volunteers and/or community-based referral systems to increase use of ANC Community-based distribution in settings with poor access to ANC, or community-based distribution in settings with existing drug distribution programmes, e.g., onchocerciasis, or community-based referral of women to ANC 3 studies evaluating community-based distribution of IPTp (Okeibunor 2011 [89], Msyamboza 2009 [86], Mbonye 2007 [87]); 1 study in Uganda (Ndyomugyenyi 2009 [88]); 1 study in Burkina Faso (Gies 2009 [90]) Category 3 –affordability of ANC services Example barriers• ANC registration fees• Laboratory fees• Cost of SP• Unofficial penalties charged by healthcare providers for late ANC attendance See healthcare provider factors Category 4—quality of ANC services Example barriers• Providers do not offer IPTp• SP unavailable• Lack of water or cups for DOT• Poor attitudes of healthcare providers• Lack of information or instructions given by healthcare providers regarding IPTp See healthcare provider factors Healthcare provider factors Category 1—provider knowledge Example barriers• Poor knowledge of IPT strategy, timing and dosage of SP• Imprecise estimation of gestational age• Confusion about when to give IPTp in relation to treatment of malaria, HIV, or other• Perception that women will or should not take SP on empty stomach Training and supervision of healthcare providers Training of healthcare providers 1 study in Kenya (Ouma 2007 [91]) Category 2—provider attitudes Example barriers• Health education not given in local language• Information and instructions on IPTp not given to pregnant women• Providers do not offer IPTp• Providers treat women with lack of respect Training and supervision of healthcare providers on provider–client interactions None None Category 3—health facility organisation Example barriers• Restrictive ANC hours• Lack of cups or drinking water• Frequent provider absence from work• Ineffective staff rosters Reorganisation of staff rosters, opening hours, etc., and better management, supervision, and accountability of staff None None Category 4—inadequate guidance on IPTp Example barriers• Variation in information given to healthcare providers on IPTp• No guidelines available at facility• Lack of supervision and monitoring of IPTp• Lack of recent training on IPTp• Private facilities following different practices• Incompatibilities between delivery of IPTp and other health interventions Provision of consistent, simple guidelines to all health facilities, both public and private sectors, together with training and supervision Modelling the effect of simple guidelines on coverage with IPTp 1 study in Tanzania (Gross 2011 [33]) Category 5—fees for ANC services Example barriers• ANC registration fees• Cost of SP• Unofficial penalties charged by healthcare providers for late ANC attendance Modification or removal of user fees and regulation against imposition of penalties None None Category 6—supply of SP Example barriers• SP unavailable• Poor stock control Timely procurement and distribution systems for SP, and system to prioritise use of funds for SP at health facilities None None 10.1371/journal.pmed.1001488.t005 Table 5 Synthesis matrix comparing findings from observational studies with those of intervention studies for ITNs. Type of Factor Findings from Observational Studies Findings from Intervention Studies Categories Derived from Barriers Implications for Interventions to Increase Uptake Type of Intervention Evaluated Number of Intervention Studies Pregnant women factors Category 1—pregnant women's knowledge Example barriers• Lack of knowledge of benefits of ITNs for mother and child• Discomfort of using ITNs• Lack of habit of using ITNs• Fear of chemicals used on ITNs• Perception that there are no mosquitoes Promotion of ITN strategy and safety of insecticides used to treat nets through a variety of channels, e.g., community-based, clinic-based, media, local leaders Promotional campaigns using a variety of channels, e.g., social marketing, clinic-based, media 3 social marketing studies by PSI in Burundi (2007 [97]), Kenya (2008 [95]), and Madagascar (2009 [96]) Category 2—household or cultural constraints Example barriers• Lack of support from husband and/or community• Lack of cultural habit of using ITNs• Cultural beliefs, e.g., resemblance of ITNs to burial shrouds Promotion of ITN strategy and safety of insecticides used to treat nets through a variety of channels, e.g., community-based, clinic-based, media, local leaders As above As above Category 3—access to ITNs Example barriers• Lack of retailers• Cost of ITNs• Inability to pay top-up fees on vouchers• Direct and indirect costs of accessing ITN distribution points Delivery of free ITNs to pregnant women through ANC or campaigns, or delivery of voucher subsidies through ANC or campaigns, or community-based distribution of subsidised ITNs Delivery of free ITNs to pregnant women through ANC or campaigns, or delivery of voucher subsidies through ANC or campaigns, or community-based distribution of subsidised ITNs 3 studies evaluated free ITNs: 2 studies through ANC (Pettifor 2009 [98], Guyatt 2003 [99]) and 1 study through campaign delivery (Thwing 2011 [92]); 7 studies evaluated voucher subsidies: 2 studies via campaign delivery (Ahmed 2010 [93], Khatib 2008 [94]), 5 studies via ANC (Beiersmann 2010 [84], Marchant 2010 [100], Hanson 2009 [101], Muller 2008 [102], Kweku 2007 [83]); 1 study community-based: Nonaka 2012 [103] Healthcare provider factors Category 1—provider knowledge Example barrier• Lack of knowledge of ITN benefits for mother and child Training and supervision of healthcare providers on ITNs None None Category 2—provider attitudes Example barriers• Providers refuse to offer ITNs to pregnant women• Providers impose eligibility criteria for ITNs or vouchers Better training, management, supervision, and accountability of staff None None Category 3—health facility organisation Example barriers• Vouchers not available at facility• As for IPTp Reorganisation of staff rosters, hours, etc., and better management, supervision, and accountability of staff None None Category 4—fees for ANC services Example barriers• ANC registration fees• Cost of ITNs Removal of user fees and regulation against imposition of penalties None None Category 5—supply of ITNs/vouchers Example barriers• Poor stock control• Stockouts of ITNs• Vouchers not available Timely procurement and distribution systems for ITNs or vouchers None None Six key categories of barriers to healthcare providers delivering IPTp were identified: provider knowledge of IPTp, provider attitudes, health facility organisation, policy and guidance, fees for services, and supply of SP. Poor knowledge and poor administration of IPTp guidelines by healthcare providers appear to be substantial barriers to achieving high coverage, as highlighted in several studies included in this review. Provider knowledge of the IPTp strategy could be improved through retraining and closer supervision by district staff; however, only one study was identified that evaluated the impact of retraining of healthcare providers in Kenya on the delivery, timing, and dosing of IPTp [91]. Simplified policy and guidance on IPTp would be a relatively simple intervention to improve healthcare provider practice in delivering IPTp, and while no relevant intervention study was identified, one study in Tanzania modelled the effect of simplified guidelines on coverage with IPTp, demonstrating that coverage could be increased with simplified guidance [33]. No intervention studies were identified that addressed supply of SP, even though this was one of the commonest barriers identified in the observational studies. Poor healthcare provider attitude is a generic problem often entrenched in resource-constrained healthcare system and public sector settings, and may be difficult to address; no relevant intervention studies were identified. Similarly, user fees at ANCs are a generic barrier to ANC services, and no intervention studies were identified that addressed this. Three key categories of barriers to women receiving and using ITNs were identified: pregnant women's knowledge of ITNs, household or cultural constraints, and access to ITNs. As for IPTp, pregnant women's knowledge of ITNs as well as certain household and cultural constraints could be addressed through promotion of ITNs through a variety of channels. Social marketing using extensive media and educational campaigns has been used in a large number of countries, and three evaluation studies were identified in this review [95]–[97]. Access to ITNs has been a problem for women in terms of direct and indirect costs, ITN availability, and access to distribution points. Three studies evaluated the delivery of free ITNs to pregnant women through ANCs [98],[99] or campaigns [92], one study evaluated community-based delivery of subsidised ITNs [103], and seven studies evaluated voucher subsidies delivered through ANCs [83],[84],[100]–[102] or campaigns [93],[94]. Categories of barriers to healthcare providers delivering ITNs were similar to those for the delivery of IPTp: provider knowledge, provider attitudes, health facility organisation, fees for services, and supply of ITNs. We did not find any relevant studies that evaluated interventions that directly addressed these provider barriers. Discussion To our knowledge this is the first systematic review of the factors affecting the delivery, access, and use of interventions to prevent malaria in pregnant women that uses research findings from quantitative, qualitative, and mixed methods studies, that assesses both user and provider perspectives, and that integrates these findings with intervention studies. This analysis provides a comprehensive basis for identifying key bottlenecks in the delivery and uptake of IPTp and ITNs among pregnant women, and for understanding which scale-up interventions have been effective, in order to prioritise which interventions are most likely to have the greatest impact in the short or medium term. Barriers to the delivery of IPTp and ITNs were found at different levels of implementation, and broadly fall into policy and guidance, healthcare system issues, health facility issues, and healthcare provider performance. Whilst many of the barriers reflected broader weaknesses in the healthcare system, some were specific to the intervention. With regard to IPTp, a key identified barrier to effective delivery was healthcare provider confusion about the timing of the two doses of IPTp and whether IPTp can be given on an empty stomach. This confusion stemmed from a combination of unclear policy and guidance, inadequate training, and lack of information and job aids on IPTp. Several studies reported conflicting national policies with regards to provision of IPTp in relation to management of HIV and other diseases or conditions, and when to give IPTp if women have been treated for malaria, a problem also identified in another review [105]. Also, some studies reported that healthcare providers expressed uncertainty over the effectiveness of SP for IPTp. Clearly there is an urgent need for countries to update national IPTp policy and guidance, and to ensure that this information reaches frontline providers at ANCs and outpatient departments providing treatment to pregnant women for illness, e.g., through directives or memos from the Director of Medical Services, as done in Kenya (M. J. Hamel, personal communication). The recent WHO IPTp policy update recommendation with simplified guidance on IPTp dosing, which also restates the continued effectiveness of IPTp with SP, serves as an important opportunity for national programmes to update and reinvigorate their IPTp strategy [106]. Organisational problems at the facility level were also common, such as lack of privacy and confidentiality in the health encounter [51] and the restriction of hours of ANC services, resulting in high client-to-staff ratios, long waiting times [49],[52], and reduced consultation times, all of which contribute to poor quality of care at ANCs. Absenteeism and high staff rotation at the facility leading to lack of continuity of care and high workload among staff on duty was also reported [62]. Most of these organisational problems present another area for improvement in the short term that does not require additional resources, though it will require better management and accountability by the heads of health facilities. Other barriers were, however, dependent on higher levels of the healthcare system, such as high staff turnover [62], understaffing (particularly in remote areas), poor infrastructure [41], poor supervision, and poor use of data to identify problems and inform decision-making. These problems are inherent in the healthcare systems in some areas in some countries, and will require longer term strategies and increased investment in healthcare system strengthening. Also persistently reported across the studies and dependent on action taken at higher levels were stockouts of both SP for IPTp and ITNs, and lack of water or cups for providing IPTp by DOT. The reviewed studies did not explore the reasons for the stockouts, but they are likely to be a combination of lack of funding at the national level for procurement of commodities (i.e., specific to IPTp and ITNs) and problems in supply chain management. Barrier studies among women highlighted additional healthcare system barriers leading to poor uptake of IPTp and/or ITNs. Having to pay user fees or pay for SP, drinking water for DOT, or ITNs was a common barrier, as were the indirect costs associated with visiting ANCs, such as transport, food, and opportunity costs. This finding was supported by the meta-analysis of determinants of coverage among pregnant women, which showed that socio-economic status and employment status are important predictors of IPTp and ITN coverage, respectively. These inequities may to some extent reflect the determinants of women's access to ANCs, where user fees are routinely applied to registration, consultations, laboratory tests, and drugs, as identified in a review of factors affecting utilisation of antenatal care in developing countries [107]. However, in some instances user fees are also applied to SP (e.g., where women have to purchase SP or water to take IPTp by DOT) and to ITNs [108]. This situation calls for a review of charging policies for IPTp and ITNs across national programmes, and of user fees and charges at ANCs in general. Another common barrier to ANC utilisation was the poor quality of interactions between healthcare providers and pregnant women [38],[41]. Women were generally perceived as passive recipients and were provided with little or no information about the services provided [44], and women with a low social position, such as adolescents [51], and less educated women are most vulnerable. This issue appears to be a problem in some resource-poor settings and is more difficult to tackle. However, educating women about their rights and about the ANC services available to them may go some way to empowering women to be able to demand better services. This finding is supported by the fact that pregnant women's lack of knowledge and understanding of IPTp and ITNs was consistently reported in both the barrier and determinant data as an important factor preventing the uptake and use of IPTp and ITNs. Women who understand the benefits of IPTp and the safety of SP, and how and when to take it, are more likely to take it. However, many women do not receive adequate information about IPTp, and this can result in fears that the drug causes harm, even abortion [15], or women showing preference for an alternative drug. Whilst there are some reports that women experience side effects from IPTp, the severity and extent of these events are not clearly described. There were also reports of women fearing that the chemical used on ITNs would harm the foetus [15]. Whilst knowledge is also an important facilitator of ITN use, barrier studies reveal important deterrents to ITN use such as the inconvenience and discomfort of use [109], especially in the dry season, and the lack of a culture or habit of net use. These findings were consistent with the meta-analysis of determinants in that coverage of both IPTp and ITNs was lower among women with no education and, in some countries, women living in rural areas; these women were less likely to access ANC and/or health education services. The meta-analysis was useful in identifying other important risk groups. Younger or adolescent women, unmarried women, and less educated women were significantly less likely to use ITNs. The barrier studies show that this may be related to lower affordability and in-household access among these women. Adolescents, unmarried women, and less educated women therefore constitute high-risk groups for targeting ITNs. This suggests that ministries of health need to pay more attention to IPTp and ITN promotion and health education, with additional targeting of risk groups, as well as using new innovations for communication of messages, since traditional health education is not offered at all facilities or is not always effective. Women seeking care at ANCs often have to overcome barriers at the household or societal level, and these barriers are more challenging to address. Women have commitments to farming or employers and the responsibility of childcare, and often have to defer to their husbands or in-laws in decision-making over accessing ITNs or use of household income to pay for ANC services. In a review of ANC access, use of ANCs was shown to increase with husband's educational level and was an even stronger predictor than women's education in some settings [107]. Local cultural norms and practices present a considerable barrier to women accessing ANC services in some but not all study countries, with wide variation within countries and between countries, a finding also reported in the review by Pell et al. [15]. In comparison to the observational studies, the review identified comparatively few studies that evaluated interventions to promote scale-up of these interventions, particularly for IPTp. Whilst many of the barriers to IPTp and ITN coverage identified in the observational studies related to healthcare providers and service delivery, very few studies that evaluated interventions to improve service delivery were found. Similarly, very few studies explored the determinants of delivery of either IPTp or ITNs among healthcare providers, or supply-side interventions designed to improve the quality of delivery of IPTp or of ITNs with a chosen strategy, whether it be campaigns or routine delivery through ANCs. Of the six studies that evaluated interventions to increase coverage of IPTp, all but one targeted women's knowledge or access, the last being a healthcare provider intervention. Consideration of the context for employing community-based distribution of IPTp is important; this distribution strategy appears to be an effective additional strategy to boost coverage in areas where there is already a successful community-based distribution programme, as seen in the onchocerciasis control programme in Uganda [88], but may serve to undermine women's attendance at ANCs in areas where ANC attendance is fragile. Community-based promotion, on the other hand, has the potential benefit in some settings of increasing access and uptake of IPTp by providing women with information about the importance and benefits of IPTp, and at the same time reinforcing the message that women should obtain antenatal care from ANCs, where they benefit from the full range of focussed ANC services [90]. While 13 studies were identified that evaluated the effectiveness of alternative delivery strategies to increase ITN coverage among pregnant women, the study objectives and designs were heterogeneous; hence, it was not possible to draw generalisable conclusions. Nevertheless, ANC services appear to be an important source of free ITNs for pregnant women in rural areas, a finding supported in a review of best practices of ITN programmes in sub-Saharan eastern Africa [108]. Strengths and Limitations of the Review The review triangulates data from quantitative, qualitative, and mixed methods studies to increase the content validity and comprehensiveness of the review; it does not, however, attempt a full meta-ethnography of qualitative data, which has been undertaken recently by others [15],[110]. The meta-analysis of determinants was used to explore the range of effects between studies and to provide a pooled analysis to support the findings of the narrative (interpretive) synthesis. Although the use of cluster-unadjusted ORs may have overestimated precision, these were limited to four out of 36 studies. There was considerable heterogeneity among studies included in the meta-analysis, and we explored only a limited number of variables in the subgroup analysis to assess whether these could explain the differences between studies (Text S2). The lack of adjustment for ANC attendance in studies using community-based surveys means that the determinants of IPTp use may be partly driven by determinants of ANC access. However, the differences in the results between studies that enrolled women in the community and those that enrolled women in clinics in the subgroup analysis were not significant (Text S2). Whilst distinguishing between use of SP for treatment versus use for prevention poses an important challenge in interpreting community surveys, this limitation was not measured in the studies included in the meta-analysis. Whilst no restrictions were placed on the language of publication, and no studies were excluded on the basis of language, the focus the Malaria in Pregnancy Library (the primary source of studies) to date has been on the European family of languages and predominantly English. Reviewer bias was limited by the use of two independent reviewers to assess inclusion criteria. Reporting of included studies was assessed for quality, and reporting quality for the majority of studies was assessed to be fair. There were three quantitative studies that met no reporting quality criteria and 13 studies that met only one criterion (10 quantitative and three intervention studies). Findings from the studies with data on barriers were found to be entirely consistent with findings from other studies, and provided no new or surprising themes, and inclusion of these studies did not alter the study findings. Our review includes 98 studies from across sub-Saharan Africa, with 77 of these specifically containing data on barriers and determinants of delivery, access, and use of IPTp and ITNs among healthcare providers and pregnant women; this is a sizeable body of evidence. In summary, the delivery and uptake of IPTp and ITNs by pregnant women is impeded by a wide range of factors among both pregnant women and the healthcare system, each influenced by an array of social, cultural, economic, and institutional factors, with each factor influenced by the others in a complex interchange. There are also geographic variations, with some barriers more prominent in some countries than in others. Notwithstanding this complexity, many of the barriers highlighted in this review are relatively consistent across countries and are surmountable: barriers that programmes can address in the near term with limited additional investment. Delivery of ITNs through ANCs presents a narrower range of problems than delivery of IPTp. Actions to increase coverage of IPTp and ITNs in the short term would be (1) to simplify country policies and guidance to align the updated WHO IPTp policy [106] with the new WHO policy for focused antenatal care, consisting of four visits in the second and third trimesters, and ensure effective dissemination to frontline healthcare providers through training and job aids; (2) to earmark funding for procurement of SP and ITNs; (3) to review ANC fee structures; and (4) to launch targeted promotional campaigns to reach high-risk populations of pregnant women, according to local settings, e.g., rural, poor, or adolescent women. Promotional campaigns will need to reflect the needs of women and offer services they will accept at a price they can afford. Other barriers are more entrenched within the overall healthcare system and will require medium- to long-term strategies to improve the overall quality of antenatal services and encourage the habit of ANC use among women. New multifaceted interventions should be explored, such as quality improvement initiatives that link improvements in delivery of IPTp and ITNs to other core ANC services, management tools for facility-level decision-making, and innovations, such as use of mobile phones for defaulter tracing, supply chain/stock control, reporting of health management information systems data on coverage, and surveillance. Increasing drug resistance means that IPTp with SP will most likely be replaced by more complicated and expensive drug regimens [4],[111], or new strategies, such as intermittent screening and treatment [112]. Intermittent screening and treatment will require adjustments to be made in the ANC setting [47],[64], and will not have the added benefit of IPTp in controlling infections that cannot be detected by rapid diagnostic tests or microscopy. Malaria prevention estimates have increased only modestly between 2007 and 2010 (from 13.6% to 21.5% coverage for IPTp and from 17.0% to 38.8% coverage for ITN use) [138]. Conclusion Our synthesis shows that the key barriers to access, delivery, and use of IPTp and ITNs are relatively consistent across countries. These barriers may be helpful as a checklist for use by country malaria programmes and/or policy-makers to identify factors influencing uptake of these interventions in their specific location or context. The review also highlights the need for multi-country studies that evaluate targeted or multifaceted interventions aimed to improve the delivery and uptake of IPTp and ITNs. More research is also needed to understand and improve the policy change process to facilitate future replacement of SP with alternative drug regimens for IPTp or alternative strategies such as screening and treatment that will present even greater challenges for delivery. Supporting Information Table S1 Search terms and databases used in the review. (DOCX) Click here for additional data file. Table S2 Study characteristics. Table S2.1. Characteristics of studies on determinants, barriers, and facilitators. Table S2.2. Characteristics of intervention studies. (DOCX) Click here for additional data file. Table S3 Checklist for quality of reporting. Table S3.1. Checklist for quality of reporting: quantitative studies. Table S3.2. Checklist for quality of reporting: qualitative studies. Table S3.3. Checklist for quality of reporting: mixed methods studies. Table S3.4. Checklist for quality of reporting: intervention studies. (DOCX) Click here for additional data file. Table S4 Barriers and facilitators to delivery, access, and use of IPTp and ITNs. Table S4.1. Barriers and facilitators to receipt of IPTp from the perspective of pregnant and recently delivered women. Table S4.2. Barriers and facilitators to ITN ownership and use from the perspective of pregnant and recently delivered women. Table S4.3. Barriers and facilitators to the delivery of IPTp from the healthcare provider perspective. Table S4.4. Barriers and facilitators to the delivery and use of ITNs from the healthcare provider perspective. (DOCX) Click here for additional data file. Text S1 PRISMA statement. (DOC) Click here for additional data file. Text S2 Meta-analysis of determinants of IPTp and ITN use in pregnancy. (PDF) Click here for additional data file.
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              Patterns and Predictors of Self-Medication in Northern Uganda

              Self-medication with antimicrobial agents is a common form of self-care among patients globally with the prevalence and nature differing from country to country. Here we assessed the prevalence and predictors of antimicrobial self-medication in post-conflict northern Uganda. A cross-sectional study was carried out using structured interviews on 892 adult (≥18 years) participants. Information on drug name, prescriber, source, cost, quantity of drug obtained, and drug use was collected. Households were randomly selected using multistage cluster sampling method. One respondent who reported having an illness within three months in each household was recruited. In each household, information was obtained from only one adult individual. Data was analyzed using STATA at 95% level of significance. The study found that a high proportion (75.7%) of the respondents practiced antimicrobial self-medication. Fever, headache, lack of appetite and body weakness were the disease symptoms most treated through self-medication (30.3%). The commonly self-medicated antimicrobials were coartem (27.3%), amoxicillin (21.7%), metronidazole (12.3%), and cotrimoxazole (11.6%). Drug use among respondents was mainly initiated by self-prescription (46.5%) and drug shop attendants (57.6%). On average, participants obtained 13.9±8.8 (95%CI: 12.6–13.8) tablets/capsules of antimicrobial drugs from drug shops and drugs were used for an average of 3.7±2.8 days (95%CI: 3.3–3.5). Over half (68.2%) of the respondents would recommend self-medication to another sick person. A high proportion (76%) of respondents reported that antimicrobial self-medication had associated risks such as wastage of money (42.1%), drug resistance (33.2%), and masking symptoms of underlying disease (15.5%). Predictors of self-medication with antimicrobial agents included gender, drug knowledge, drug leaflets, advice from friends, previous experience, long waiting time, and distance to the health facility. Despite knowledge of associated risks, use of self-medication with antimicrobial drugs in management of disease symptoms is a common practice in post-conflict northern Uganda.
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                Author and article information

                Contributors
                vpadmn@infocom.co.ug , akmbonye@yahoo.com
                saedmoalim@gmail.com
                jbagonza@musph.ac.ug
                Journal
                Malar J
                Malar. J
                Malaria Journal
                BioMed Central (London )
                1475-2875
                14 April 2016
                14 April 2016
                2016
                : 15
                : 211
                Affiliations
                [ ]Ministry of Health, Kampala and School of Public Health-College of Health Sciences, Makerere University, Box 7272, Kampala, Uganda
                [ ]School of Public Health, College of Health Sciences, Makerere University, Kampala, Uganda
                Article
                1246
                10.1186/s12936-016-1246-1
                4831145
                27075575
                11dd89ed-24b9-4b5d-9964-c43398251253
                © Mbonye et al. 2016

                Open AccessThis 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.

                History
                : 22 November 2015
                : 30 March 2016
                Categories
                Research
                Custom metadata
                © The Author(s) 2016

                Infectious disease & Microbiology
                malaria in pregnancy,sulphadoxine–pyrimethamine,perceptions,practices,peri-urban,uganda

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