Impact of the use and efficacy of long lasting insecticidal net on malaria infection during the first trimester of pregnancy - a pre-conceptional cohort study in southern Benin

Impact of the use and efficacy of long lasting insecticidal net on malaria infection during the... Background: Malaria in pregnancy is prevalent in Sub-Saharan Africa. The first trimester of pregnancy is a critical period and the best preventive measure is Long Lasting Insecticidal Nets (LLIN). Unfortunately, few studies have been conducted which focuses on the usage and efficacy of LLIN on malaria prevention during the first trimester. Methods: We assessed the use and effectiveness of LLIN in early pregnancy in Benin and its impact on malaria infection risk. We followed-up a cohort of 240 pregnant women from pre-conception to the end of the first trimester of pregnancy in Southern Benin. Parasitological, maternal and LLIN data were actively collected before, at the beginning and end of the first trimester of pregnancy. A Cox regression model was used to determine the relationship between the time to onset of the first malaria infection and the use, physical integrity, and bio-efficacy of the LLIN, adjusted for relevant covariables. Results: The good use, good physical integrity and biological efficacy of LLIN were associated with a decreased risk of occurrence of the first malaria infection in early pregnancy (HRa = 0.38; (0.18–0.80); p < 0.001; HRa = 0.59; (0.29–1.19); p < 0.07; HRa = 0.97; (0.94–1.00); p < 0.04 respectively), after adjustment for other covariates. Primi/secundigravidity and malaria infection before pregnancy were associated with a risk of earlier onset of malaria infection. Conclusion: The classically used LLIN’s indicators of possession and use may not be sufficient to characterize the true protection of pregnant women in the first trimester of pregnancy. Indicators of physical integrity and bio-efficacy should be integrated with those indicators in evaluation studies. Keywords: Gestational malaria, First trimester, Long lasting impregnated nets, Use, Physical integrity indicator, Biological efficacy indicator * Correspondence: nellsmilia@yahoo.fr; gilles.cottrell@ird.fr UMR216-MERIT, French National Research Institute for Sustainable Development (IRD), Université Paris Descartes, 75006 Paris, France Full list of author information is available at the end of the article © The Author(s). 2018 Open Access 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. Hounkonnou et al. BMC Public Health (2018) 18:683 Page 2 of 7 Background screened using Rapid Diagnostic Tests (RDT) and treated Malariainpregnancy resultsinanincreased risk of low with Artemisinin-based Combination Therapies (ACT) birth weight (LBW) [1–3], maternal anemia and perinatal when tested positive for malaria according to the national mortality [1, 4]. World Health Organization (WHO) has guidelines [19]. implemented a prevention policy specific to this vulnerable EVALMOUS study held between 1st June 2015 and 31st population [5, 6], based on sulfadoxine-pyrimethamine (SP) October 2016 and aimed to assess the effectiveness of intermittent preventive treatment in pregnant women mosquito nets used by pregnant women and other mem- (IPTp) and the use of Long Lasting Impregnated Nets bers of their household in preventing malaria. The first (LLIN) from the onset of pregnancy. The IPTp comprises 576 women from the RECIPAL primary cohort who monthly intakes of a curative dose of SP during antenatal agreed to participate were included in EVALMOUS study care visits from the second trimester of pregnancy for all before their pregnancy and the first 240 of them to be- pregnant women (whether infected or not). Numerous come pregnant were followed throughout the first trimes- studieshaveshown theeffectivenessofIPTpin improving ter of pregnancy. Women were visited at three home maternal and child health outcomes [7–10]. However, IPTp visits: a first visit was performed before pregnancy and is contraindicated in the first trimester of pregnancy leaving two visits during the first trimester of pregnancy. During women in the first trimester unprotected by this control these visits, a questionnaire was administered to the tool. Moreover, several studies have shown that the first tri- women in order to evaluate the indicators related to LLIN, mester of pregnancy is a critical period during which mal- namely: possession, use and physical integrity. At the last aria infection is associated with an increased risk of low visit the mosquito net used by the pregnant women was birth weight and maternal anemia [11–13]. LLIN is the only taken for laboratory testing to assess their bio-efficacy and preventive tool available for pregnant women during this replaced by new ones provided by the study. Physical in- period. However, it is known that pregnant women attend tegrity and bio-efficacy of the LLINs were determined by the maternity clinic mostly after the first trimester of preg- the field workers using the standard WHO protocol [20]. nancy in sub-Saharan Africa [14]. Consequently, the first trimester of pregnancy is a period badly covered by the Variables malaria prevention policy. There is evidence for the efficacy Outcome variable of LLIN in preventing malaria infection during pregnancy Malaria infection during the first trimester of pregnancy [15], to improve babies’ birth weight [16]. No study has yet was defined as a positive blood smear and/or a positive focused on the specific protection conferred by LLIN in the RDT before 15 weeks of gestation (estimated by early first trimester of pregnancy. In this work, using data from ultrasound scan). Timing of malaria infection was deter- the follow-up of a pre-conceptional cohort carried out in mined based on gestational age. South-Benin in 2015–1016, we evaluated the association between the indicators of use, physical integrity and bio-efficacy of LLINs used by pregnant women and malaria Independent variables incidence during the first trimester of pregnancy. At each visit during the study (before pregnancy and dur- ing the first trimester of pregnancy), the use of mosquito Methods net was defined as a binary variable, “good” if LLIN was Study design reported to be used every day of the week preceding the EVALMOUS is a cohort study nested in the RECIPAL visit and if it was properly installed after inspection by the project, carried out in South Benin [17]. Between June investigator. 2014 and August 2017, 1214 women of childbearing age The physical integrity of nets was characterized by a and willing to become pregnant (primary cohort) were in- hole index (hi) resulting from the characterization of the cluded in a cohort follow-up. All women were screened holes according to WHO protocol [20]. A mosquito net for malaria using thick blood smear (TBS) at their inclu- with a hi between 0 and 64 was considered as in “good” sion and monitored monthly using a urinary pregnancy condition, a hi between 65 and 642 as in an “acceptable” test until the identification of 411 pregnant women among state and a hi greater than 643 as in a “bad” state. them (secondary cohort). The pregnant women were then Bio-efficacy of LLIN was based on both kd60 (knock-- monitored monthly until delivery at the maternity clinic, down 60 min) and 24 h-death (mortality after 24 h) of where they benefited from a clinical, parasitological (by female Anopheles gambiae “Kisumu strain” 2–5 days TBS), nutritional and ultrasound follow-up. Lambarene after exposure to LLIN through standard WHO cone. A technique was used to quantify parasitaemia and the de- LLIN was declared bio-effective when the kd60 rate tection threshold with this method has been estimated to induced by this LLIN is greater than or equal to 95% or be 5 parasites/μL[18]. In addition, in the event of fever or when the mortality rate induced by it is greater than or symptoms suggestive to malaria, pregnant women were equal to 80% [20]. Hounkonnou et al. BMC Public Health (2018) 18:683 Page 3 of 7 Statistical analysis different number of measures between the women, an First, we did a descriptive analysis of the general charac- offset (the log of the number of visits) has been intro- teristic of the women at baseline (sociodemographic, the duced in the model. characteristics of the LLINs and the malaria before The analyses were carried out with STATA software pregnancy). version 13.1 (STATA Corporation, Texas). Univariable analysis Results We studied the relationship between the time to onset Five hundred and seventy-six pregnant women were of the first malaria infection in the first trimester of included in the EVALMOUS study. Figure 1 shows the pregnancy and each of the independent variables by a flow chart during follow-up of these women. We univariable Cox regression model. For each covariate, included 240 pregnant women. At the end of the eight- the proportional risk hypothesis was verified using the een months of follow-up, the proportion of drop-out, overall “p” of the Schoenfeld residue-based test. For the miscarriages, and refusals was 0.42%; 8.33 and 5% re- continuous covariates, the linearity hypothesis was veri- spectively. The bioassays were carried out in the labora- fied. The comparison between the Kaplan-Meier curves tory on 324 LLINs at the end of the first trimester. of the different categories of qualitative variables was The characteristics of the pregnant women included in carried out by a log rank test. the study are shown in Table 1. Among the 240 women, the prevalence of malaria infection before pregnancy was Multivariable analysis 4.41% and the proportion of infected pregnant women The malaria infection and the LLINs indicators were during the first trimester of pregnancy was 18.33%. All available for 190 pregnant women out of the 240. We women except one had an LLIN. compared the 190 pregnant women included in the mul- During pregnancy, all but one of the women had tivariable analysis and the 50 excluded women according LLINs. Most of pregnant women (83.25%) had used their to the age (t-test), the gestational rank, the residence LLIN properly during the week prior to the visits. About area and the malaria infection before pregnancy. The 60% of the LLINs inspected were in good physical condi- comparison of the age in the two groups was performed tion. On the other hand barely 6% of LLINs tested in the by a t-test whereas the categorical variables were com- laboratory were bio-effective. Table 2 recapitulates the pared using a Chi2 test. characteristics of the LLIN’s indicators inspected. A multivariable Cox regression model was used. Adjust- Table 3 shows the different proportions of malaria in- ment factors were age (in years) of the pregnant women fection during the different visits of the first trimester of (quantitative variable recoded in quartiles); the gestational pregnancy. The median time between onset of malaria rank (less than 3 pregnancies/more than 3 pregnancies; before pregnancy and the beginning of pregnancy was marital status (unmarried/married); pre-pregnancy mal- 7.6 months with an interquartile range of (4.9–8.5). aria infection during the pre-pregnancy visit; ethnicity Figure 2 shows the probability of non-occurrence of (Toffin/other); level of education (literate/illiterate); occu- malaria infection in pregnant women as a function of pational status (employed/unemployed) and residential time during the first trimester of pregnancy. The inci- area (lake area/land area). dence rate of malaria infections was 7.18 cases per 100 First, all covariates were introduced in the model and a person-months (95% CI: 5.36–9.62). backward step-by-step strategy was performed to eliminate The group of women not included in the multivariate non-significant cofactors. At theend oftheanalysis,only analysis did not differ significantly from the included the cofactors associated with the variable to be explained at pregnant women, according to the 4 variables: age, resi- the 5% p-value threshold were retained in the final model dence area, gestational rank and malaria before preg- in addition to the LLIN indicator variables. As we consid- nancy (respective p-values = 0.48; 0.29; 0.24 and 0.58 ered in this study one-sided alternative hypotheses (i.e. bet- respectively). Based on those results, excluding the 50 ter use, better physical integrity and better bio-efficacy women from the multivariable model does not seem to would confer protection against malaria), we used have led to a major selection bias. one-sided p-values with a threshold of significance at 5%. The variables selected in the final multivariate model During the study, six pregnant women had at least 2 respected the proportional hazard asumption assump- malaria infections during the first trimester of preg- tion according to the Schöenfeld residuals method. nancy. In order to assess the determinants of the num- Additional file 1: Table S1 and Table 4 respectively ber of infections, we performed a multivariable Poisson summarize the univariate Cox regression model and the regression model, regressing the same covariates (as in final multivariate Cox model. After adjustment, the use the Cox model) on the number of infections in the first of LLIN by pregnant women was marginally significant, trimester. In addition, in order to take into account the whereas the physical integrity, the LLIN’s quantitative Hounkonnou et al. BMC Public Health (2018) 18:683 Page 4 of 7 Fig. 1 Flow chart of EVALMOUS study, Benin 2015–2016 bio-efficacy and malaria infection in pre-pregnancy were significantly associated with the time to onset of the first Table 1 Characteristics of pregnant women at the inclusion, Sô-Ava and Akassato, Benin 2015–2016 (N = 240) malaria infection in the first trimester of pregnancy. We also performed a Poisson model to study the effect of Characteristics Pre-pregnancy the three indicators of LLIN on the number of malaria in- Total Mean or proportion fections occurring during the first trimester of pregnancy (95% CI) adjusted for the same covariates. In this analysis Age (years) 240 26.61 ± 4.78 (Additional file 2: Table S2), the three indicators of the Gestational rank 240 LLINs (the use, the physical integrity and the quantitative Primigravida 22 9.17 (5.49; 12.84) bio-efficacy) were significantly associated with the incidence Secundigravida 36 15.00 (10.45; 19.55) of malaria infection during the first trimester of pregnancy, (IRRa = 0.40; (0.20–0.78); p < 0.003; IRRa = 0.44; (0.24– Multigravida 182 75.83 (70.38; 81.29) 0.81); p < 0.004; IRRa = 0.98; (0.95–0.99); p <0.02 respect- Ethnic Group 240 ively), confirming the results of the Cox model. Toffin 156 65.00 (58.92; 71.08) Others 84 35.00 (28.92; 41.08) Discussion Education level 240 The peculiarity of our study was the ability to have Illiterate 161 67.08 (61.09; 73.07) followed the women from the pre-conceptional period Literate 79 32.92 (26.93; 38.90) until the end of the first trimester of pregnancy. This Occupational status 240 study identified two sets of essential results, i) the re- Employed 221 92.08 (88.64; 95.52) fined characterization of the protection given to the Unemployed 19 7.92 (4.48; 11.36) pregnant women by the LLIN against malaria infection during the first trimester of pregnancy and ii) new im- Marital status 240 portant elements in the reflection on the different indi- Cohabitation 11 4.58 (1.92; 7.25) cators of LLIN’s efficiency that characterize properly the Married (monogamy) 159 66.25 (60.22; 72.27) real protection of pregnant women against malaria dur- Married (polygamy) 70 29.17 (23.37; 34.96) ing this critical period. Residence area 240 We observed a general high possession and good use Lake area 156 65.00 (58.92; 71.08) of LLIN by the study pregnant women. This is probably an indication of the success of the LLIN mass distribu- Land area 84 35.00 (28.92; 41.08) tion campaigns carried out previously in Benin in 2011 Pre-pregnancy malaria 227 and 2014. In all, the Cox model confirmed our working Yes 10 4.41 (1.72; 7.10) hypothesis that the different indicators were significantly No 217 95.59 (92.90; 98.28) related to the delay in malaria infection. Precisely, good Hounkonnou et al. BMC Public Health (2018) 18:683 Page 5 of 7 Table 2 Indicators of possession, use, physical integrity and chemical efficacy of LLINs inspected during follow-up, Sô-Ava and Akassato, Benin 2015–2016 (N = 240) Characteristics Pre-pregnancy Pregnancy visit 1 Pregnancy visit 2 Total Mean or proportion Total Mean or proportion Total Mean or proportion (95% CI) (95% CI) (95% CI) Possession of at least one LLIN/household 240 240 203 Yes 237 98.75 (96.17; 97.60) 239 99.53 (97.06; 99.94) 202 99.51 (96.53; 99.93) No 3 1.25 (0.40; 3.83) 1 0.42 (0.06; 2.94) 1 0.49 (0.07; 3.47) Possession of LLIN according to WHO standards (1 237 239 202 LLIN/2 people) Yes 178 75.11 (69.16; 80.23) 185 77.41 (71.63; 82.30) 164 81.19 (75.14; 86.03) No 59 24.89 (19.77; 30.84) 54 22.59 (17.70; 28.37) 38 18.81 (13.96; 24.85) Use of LLIN by pregnant women 237 239 202 Yes 199 83.97 (78.69; 89.13) 203 84.94 (79.78; 88.96) 178 88.12 (82.83; 91.93) No 38 16.03 (11.86; 21.31) 36 15.06 (11.04; 20.22) 24 11.88 (8.06; 17.17) Physical integrity of pregnant woman’s LLIN 237 239 202 Good 156 65.82 (59.51; 71.62) 145 60.67 (54.29; 66.70) 115 56.93 (49.95; 63.64) Bad 81 34.18 (28.38; 40.49) 94 39.33 (33.30; 45.71) 87 43.07 (36.36; 50.05) Physical integrity of household’s LLIN 169 195 164 Good 101 59.76 (52.12; 66.96) 117 60.00 (52.91; 66.70) 96 58.54 (50.77; 77.90) Bad 68 40.24 (33.04; 47.88) 78 40.00 (33.30; 47.09) 68 41.46 (34.10; 49.23) Bio-efficacy of pregnant women’s LLIN 198 Yes –– 12 6.06 (3.46; 10.41) No –– 186 Bio-efficacy of household’s LLIN 126 Yes –– 7 5.56 (2.64; 11.30) No –– 119 94.44 (88.70; 97.36) use, good physical integrity and the quantitative limit of the two classical indicators of ownership and re- bio-efficacy of the LLIN were found to be associated ported LLIN use the previous night to characterize ad- with a later occurrence of the first malarial infection equately the optimal protection of the pregnant woman during the first trimester of pregnancy. In this model the against the occurrence of a malaria infection. All these physical integrity of the LLIN was associated only mar- elements point out the need to consider, in addition to ginally significantly with the delay of the first malaria in- the classical ownership and reported use indicators, the fection but showed significant associations in the physical integrity and bio-efficacy indicators should be Poisson regression model. Five pregnant women had taken into account in evaluation studies of LLIN effi- malaria infection twice in our study. Two studies did not ciency to reduce the malaria burden in pregnant women. find any association between LLIN usage by pregnant In our study, the high proportions of good use and women and the risk of malaria infection [21, 22]. Since LLINs with good physical integrity are in favor of a good the effectiveness of LLIN to reduce the malaria burden physical barrier conferred by LLIN to the pregnant has been extensively established [23] including in preg- women during the first trimester of pregnancy. Never- nant women [15, 24–28], those result show probably the theless, a more worrying result was the small minority of Table 3 Proportion of pregnant women infected during the first trimester of pregnancy, Sô-Ava and Akassato, Benin 2015–2016 Malaria Pre-pregnancy visit Visit 1 Visit 2 Visit 3 infection n % (95% CI) n % (95% CI) n % (95% CI) n % (95% CI) Total 227 234 199 180 Yes 10 4.41 (2.37; 8.03) 14 5.98 (3.56; 9.88) 10 5.02 (2.71; 9.13) 17 9.44 (5.92; 14.73) A total of 239 pregnant women were followed during 626.63 person-months, with a median follow-up time of 88 days (Interquartile interval: 65–95) Hounkonnou et al. BMC Public Health (2018) 18:683 Page 6 of 7 A strengthof our studyisthatfor thefirst time in amal- aria cohort, the women were seen at a pre-conceptional stage which allowed to follow them on the very beginning of their pregnancy. This is an important strenght compared to non preconcepional studies. Although our results indi- cate minimal selection bias, the moderate size of our sam- ple and the particular facies of the study area (lake zone) impose some caution on the representativeness of the results. Conclusion Our study demonstrated for the first time an overall good physical protection against the malaria vector con- ferred by LLIN in pregnant women in their first trimes- ter of pregnancy, but low chemical protection in our Fig. 2 Probability of non-occurrence of malaria infection in women study area. An important conclusion is that, in addition during the first trimester of pregnancy, Sô-ava and Akassato, to the traditional indicator of possession of LLINs by Benin, 2015–2016 pregnant women, it is essential to take into account other indicators such as actual use, physical integrity LLIN reaching the bio-efficacy threshold set by the and bio-efficiency of LLIN, since all these indicators re- WHO recommendations. This raises the highly import- flect independently from each other the real protection ant question of the duration of the LLINs bio-efficacy in against malaria of this population. Further studies are field conditions. Given that optimal protection by the then needed to assess the generalizability of our results LLIN is provided by the combination of its physical bar- and also to control the duration of the chemical effect- rier and chemical efficacy, we can conclude that the ex- iveness of the LLIN distributed on the territory. treme majority of women in the study were not optimally protected against malaria in the first trimester Additional files of their pregnancy by the LLIN they used. This import- ant conclusion would have been missed if only based on Additional file 1: Table S1. Factors associated with delay in the first malaria infection during the first trimester of pregnancy, univariate Cox the ownership and usage classical indicators. analysis (N = 240); Sô-ava and Akassato, Benin 2015–2016. (DOCX 23 kb) Additional file 2: Table S2. Factors associated with the number of Table 4 Factors associated with the time to onset of the first malaria infections during the first trimester of pregnancy (multivariate malaria infection during the first trimester of pregnancy Poisson regression model, N = 194 pregnant women); Sô-ava and Akassato, Benin 2015–2016. (DOCX 16 kb) (multivariate Cox model, N = 190 pregnant women); Sô-Ava and Akassato, Benin 2015–2016 Abbreviations Variables (terms) Multivariatble Cox model ACT: Artemisinin Combined Therapy; CER-ISBA: Ethics Committee of the N HRa CI 95% pvalue Institute of Applied Biomedical Sciences; HRa: Hazard Ratio adjusted; Use of LLIN by the woman 190 IPTp: Intermittent Preventive Treatment in Pregnant women; IRRa: Incidence the week before the visit Rate Ratio adjusted; LBW: Low Birth Weight; LLIN: Long Lasting Insecticidal Nets; RDT: Rapid Diagnostic Tests; SP: Sulfadoxine - Pyrimethamine; No 36 1 TBS: Thick Blood Smear; WHO: World Health Organization Yes 154 0.38 (0.18–0.80) < 0.001 Acknowledgements Physical integrity of the pregnant 190 We acknowledge all the pregnant women, health center and field workers woman’s LLIN and the local authorities of Sô-Ava and Akassato Districts who participated in the EVALMOUS study. Bad 78 1 Good 112 0.59 (0.29–1.19) 0.07 Funding This work was supported by “Expertise France –Initiative 5%” (Mission n° Quantitative bio-efficacy of 190 0.97 (0.94–1.00) 0.04 15SANIN110), “Fondation Simone Beer” under the aegis of “Fondation de the pregnant woman’s LLIN France” and the French “Agence Nationale de la Recherche” (ANR-13JSV1–004-01). Malaria before pregnancy 190 Availability of data and materials Yes 9 1 The datasets used and/or analysed during the current study are available No 181 0.27 (0.09–0.74) 0.01 from the corresponding author on reasonable request. N Total, HRa Hazard ratio adjusted, CI 95% Confidence Interval at 95%, LLIN Authors’ contributions Long Lasting Impregnated bedNets, pvalue one-sided pvalue Quantitative bio-efficacy is defined as the proportion of female anopheles Project management: CH, AD, VB and GC (Principal Investigator). Field, who died 24 h after exposure to the LLIN Epidemiology and data collection: CH, AD, MA, EY and GC. Biology and Hounkonnou et al. BMC Public Health (2018) 18:683 Page 7 of 7 molecular analyses: NF LLIN’s laboratory tests: AB, CS and AD. Mapping: SE, relation to the risk of low birth weight, anaemia and perinatal mortality in CH and GC. Statistical analysis: CH, AD, PH and GC. Manuscript writing: CH, Burkina Faso. Malar J. 2012;11:71. AD, SE, PH, AB, CS, NF, MA, EY, VB and GC. All authors read and approved 12. Huynh B-T, Fievet N, Gbaguidi G, Dechavanne S, Borgella S, Guézo-Mévo B, the final manuscript. et al. Influence of the timing of malaria infection during pregnancy on birth weight and on maternal anemia in Benin. Am J Trop Med Hyg. 2011;85(2): 214–20. Ethics approval and consent to participate 13. Cottrell G, Mary J-Y, Barro D, Cot M. The importance of the period of The RECIPAL and EVALMOUS studies have received the ethical approval from malarial infection during pregnancy on birth weight in tropical africa. 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The efficacy of antimalarial regimens containing Sulfadoxine-Pyrimethamine and/or chloroquine in preventing peripheral and placental plasmodium falciparum infection among pregnant women in Malawi. Am J Trop Med Hyg. 1994;51(5):515–22. 11. Valea I, Tinto H, Drabo MK, Huybregts L, Sorgho H, Ouedraogo J-B, et al. An analysis of timing and frequency of malaria infection during pregnancy in http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Public Health Springer Journals

Impact of the use and efficacy of long lasting insecticidal net on malaria infection during the first trimester of pregnancy - a pre-conceptional cohort study in southern Benin

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Medicine & Public Health; Public Health; Medicine/Public Health, general; Epidemiology; Environmental Health; Biostatistics; Vaccine
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Abstract

Background: Malaria in pregnancy is prevalent in Sub-Saharan Africa. The first trimester of pregnancy is a critical period and the best preventive measure is Long Lasting Insecticidal Nets (LLIN). Unfortunately, few studies have been conducted which focuses on the usage and efficacy of LLIN on malaria prevention during the first trimester. Methods: We assessed the use and effectiveness of LLIN in early pregnancy in Benin and its impact on malaria infection risk. We followed-up a cohort of 240 pregnant women from pre-conception to the end of the first trimester of pregnancy in Southern Benin. Parasitological, maternal and LLIN data were actively collected before, at the beginning and end of the first trimester of pregnancy. A Cox regression model was used to determine the relationship between the time to onset of the first malaria infection and the use, physical integrity, and bio-efficacy of the LLIN, adjusted for relevant covariables. Results: The good use, good physical integrity and biological efficacy of LLIN were associated with a decreased risk of occurrence of the first malaria infection in early pregnancy (HRa = 0.38; (0.18–0.80); p < 0.001; HRa = 0.59; (0.29–1.19); p < 0.07; HRa = 0.97; (0.94–1.00); p < 0.04 respectively), after adjustment for other covariates. Primi/secundigravidity and malaria infection before pregnancy were associated with a risk of earlier onset of malaria infection. Conclusion: The classically used LLIN’s indicators of possession and use may not be sufficient to characterize the true protection of pregnant women in the first trimester of pregnancy. Indicators of physical integrity and bio-efficacy should be integrated with those indicators in evaluation studies. Keywords: Gestational malaria, First trimester, Long lasting impregnated nets, Use, Physical integrity indicator, Biological efficacy indicator * Correspondence: nellsmilia@yahoo.fr; gilles.cottrell@ird.fr UMR216-MERIT, French National Research Institute for Sustainable Development (IRD), Université Paris Descartes, 75006 Paris, France Full list of author information is available at the end of the article © The Author(s). 2018 Open Access 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. Hounkonnou et al. BMC Public Health (2018) 18:683 Page 2 of 7 Background screened using Rapid Diagnostic Tests (RDT) and treated Malariainpregnancy resultsinanincreased risk of low with Artemisinin-based Combination Therapies (ACT) birth weight (LBW) [1–3], maternal anemia and perinatal when tested positive for malaria according to the national mortality [1, 4]. World Health Organization (WHO) has guidelines [19]. implemented a prevention policy specific to this vulnerable EVALMOUS study held between 1st June 2015 and 31st population [5, 6], based on sulfadoxine-pyrimethamine (SP) October 2016 and aimed to assess the effectiveness of intermittent preventive treatment in pregnant women mosquito nets used by pregnant women and other mem- (IPTp) and the use of Long Lasting Impregnated Nets bers of their household in preventing malaria. The first (LLIN) from the onset of pregnancy. The IPTp comprises 576 women from the RECIPAL primary cohort who monthly intakes of a curative dose of SP during antenatal agreed to participate were included in EVALMOUS study care visits from the second trimester of pregnancy for all before their pregnancy and the first 240 of them to be- pregnant women (whether infected or not). Numerous come pregnant were followed throughout the first trimes- studieshaveshown theeffectivenessofIPTpin improving ter of pregnancy. Women were visited at three home maternal and child health outcomes [7–10]. However, IPTp visits: a first visit was performed before pregnancy and is contraindicated in the first trimester of pregnancy leaving two visits during the first trimester of pregnancy. During women in the first trimester unprotected by this control these visits, a questionnaire was administered to the tool. Moreover, several studies have shown that the first tri- women in order to evaluate the indicators related to LLIN, mester of pregnancy is a critical period during which mal- namely: possession, use and physical integrity. At the last aria infection is associated with an increased risk of low visit the mosquito net used by the pregnant women was birth weight and maternal anemia [11–13]. LLIN is the only taken for laboratory testing to assess their bio-efficacy and preventive tool available for pregnant women during this replaced by new ones provided by the study. Physical in- period. However, it is known that pregnant women attend tegrity and bio-efficacy of the LLINs were determined by the maternity clinic mostly after the first trimester of preg- the field workers using the standard WHO protocol [20]. nancy in sub-Saharan Africa [14]. Consequently, the first trimester of pregnancy is a period badly covered by the Variables malaria prevention policy. There is evidence for the efficacy Outcome variable of LLIN in preventing malaria infection during pregnancy Malaria infection during the first trimester of pregnancy [15], to improve babies’ birth weight [16]. No study has yet was defined as a positive blood smear and/or a positive focused on the specific protection conferred by LLIN in the RDT before 15 weeks of gestation (estimated by early first trimester of pregnancy. In this work, using data from ultrasound scan). Timing of malaria infection was deter- the follow-up of a pre-conceptional cohort carried out in mined based on gestational age. South-Benin in 2015–1016, we evaluated the association between the indicators of use, physical integrity and bio-efficacy of LLINs used by pregnant women and malaria Independent variables incidence during the first trimester of pregnancy. At each visit during the study (before pregnancy and dur- ing the first trimester of pregnancy), the use of mosquito Methods net was defined as a binary variable, “good” if LLIN was Study design reported to be used every day of the week preceding the EVALMOUS is a cohort study nested in the RECIPAL visit and if it was properly installed after inspection by the project, carried out in South Benin [17]. Between June investigator. 2014 and August 2017, 1214 women of childbearing age The physical integrity of nets was characterized by a and willing to become pregnant (primary cohort) were in- hole index (hi) resulting from the characterization of the cluded in a cohort follow-up. All women were screened holes according to WHO protocol [20]. A mosquito net for malaria using thick blood smear (TBS) at their inclu- with a hi between 0 and 64 was considered as in “good” sion and monitored monthly using a urinary pregnancy condition, a hi between 65 and 642 as in an “acceptable” test until the identification of 411 pregnant women among state and a hi greater than 643 as in a “bad” state. them (secondary cohort). The pregnant women were then Bio-efficacy of LLIN was based on both kd60 (knock-- monitored monthly until delivery at the maternity clinic, down 60 min) and 24 h-death (mortality after 24 h) of where they benefited from a clinical, parasitological (by female Anopheles gambiae “Kisumu strain” 2–5 days TBS), nutritional and ultrasound follow-up. Lambarene after exposure to LLIN through standard WHO cone. A technique was used to quantify parasitaemia and the de- LLIN was declared bio-effective when the kd60 rate tection threshold with this method has been estimated to induced by this LLIN is greater than or equal to 95% or be 5 parasites/μL[18]. In addition, in the event of fever or when the mortality rate induced by it is greater than or symptoms suggestive to malaria, pregnant women were equal to 80% [20]. Hounkonnou et al. BMC Public Health (2018) 18:683 Page 3 of 7 Statistical analysis different number of measures between the women, an First, we did a descriptive analysis of the general charac- offset (the log of the number of visits) has been intro- teristic of the women at baseline (sociodemographic, the duced in the model. characteristics of the LLINs and the malaria before The analyses were carried out with STATA software pregnancy). version 13.1 (STATA Corporation, Texas). Univariable analysis Results We studied the relationship between the time to onset Five hundred and seventy-six pregnant women were of the first malaria infection in the first trimester of included in the EVALMOUS study. Figure 1 shows the pregnancy and each of the independent variables by a flow chart during follow-up of these women. We univariable Cox regression model. For each covariate, included 240 pregnant women. At the end of the eight- the proportional risk hypothesis was verified using the een months of follow-up, the proportion of drop-out, overall “p” of the Schoenfeld residue-based test. For the miscarriages, and refusals was 0.42%; 8.33 and 5% re- continuous covariates, the linearity hypothesis was veri- spectively. The bioassays were carried out in the labora- fied. The comparison between the Kaplan-Meier curves tory on 324 LLINs at the end of the first trimester. of the different categories of qualitative variables was The characteristics of the pregnant women included in carried out by a log rank test. the study are shown in Table 1. Among the 240 women, the prevalence of malaria infection before pregnancy was Multivariable analysis 4.41% and the proportion of infected pregnant women The malaria infection and the LLINs indicators were during the first trimester of pregnancy was 18.33%. All available for 190 pregnant women out of the 240. We women except one had an LLIN. compared the 190 pregnant women included in the mul- During pregnancy, all but one of the women had tivariable analysis and the 50 excluded women according LLINs. Most of pregnant women (83.25%) had used their to the age (t-test), the gestational rank, the residence LLIN properly during the week prior to the visits. About area and the malaria infection before pregnancy. The 60% of the LLINs inspected were in good physical condi- comparison of the age in the two groups was performed tion. On the other hand barely 6% of LLINs tested in the by a t-test whereas the categorical variables were com- laboratory were bio-effective. Table 2 recapitulates the pared using a Chi2 test. characteristics of the LLIN’s indicators inspected. A multivariable Cox regression model was used. Adjust- Table 3 shows the different proportions of malaria in- ment factors were age (in years) of the pregnant women fection during the different visits of the first trimester of (quantitative variable recoded in quartiles); the gestational pregnancy. The median time between onset of malaria rank (less than 3 pregnancies/more than 3 pregnancies; before pregnancy and the beginning of pregnancy was marital status (unmarried/married); pre-pregnancy mal- 7.6 months with an interquartile range of (4.9–8.5). aria infection during the pre-pregnancy visit; ethnicity Figure 2 shows the probability of non-occurrence of (Toffin/other); level of education (literate/illiterate); occu- malaria infection in pregnant women as a function of pational status (employed/unemployed) and residential time during the first trimester of pregnancy. The inci- area (lake area/land area). dence rate of malaria infections was 7.18 cases per 100 First, all covariates were introduced in the model and a person-months (95% CI: 5.36–9.62). backward step-by-step strategy was performed to eliminate The group of women not included in the multivariate non-significant cofactors. At theend oftheanalysis,only analysis did not differ significantly from the included the cofactors associated with the variable to be explained at pregnant women, according to the 4 variables: age, resi- the 5% p-value threshold were retained in the final model dence area, gestational rank and malaria before preg- in addition to the LLIN indicator variables. As we consid- nancy (respective p-values = 0.48; 0.29; 0.24 and 0.58 ered in this study one-sided alternative hypotheses (i.e. bet- respectively). Based on those results, excluding the 50 ter use, better physical integrity and better bio-efficacy women from the multivariable model does not seem to would confer protection against malaria), we used have led to a major selection bias. one-sided p-values with a threshold of significance at 5%. The variables selected in the final multivariate model During the study, six pregnant women had at least 2 respected the proportional hazard asumption assump- malaria infections during the first trimester of preg- tion according to the Schöenfeld residuals method. nancy. In order to assess the determinants of the num- Additional file 1: Table S1 and Table 4 respectively ber of infections, we performed a multivariable Poisson summarize the univariate Cox regression model and the regression model, regressing the same covariates (as in final multivariate Cox model. After adjustment, the use the Cox model) on the number of infections in the first of LLIN by pregnant women was marginally significant, trimester. In addition, in order to take into account the whereas the physical integrity, the LLIN’s quantitative Hounkonnou et al. BMC Public Health (2018) 18:683 Page 4 of 7 Fig. 1 Flow chart of EVALMOUS study, Benin 2015–2016 bio-efficacy and malaria infection in pre-pregnancy were significantly associated with the time to onset of the first Table 1 Characteristics of pregnant women at the inclusion, Sô-Ava and Akassato, Benin 2015–2016 (N = 240) malaria infection in the first trimester of pregnancy. We also performed a Poisson model to study the effect of Characteristics Pre-pregnancy the three indicators of LLIN on the number of malaria in- Total Mean or proportion fections occurring during the first trimester of pregnancy (95% CI) adjusted for the same covariates. In this analysis Age (years) 240 26.61 ± 4.78 (Additional file 2: Table S2), the three indicators of the Gestational rank 240 LLINs (the use, the physical integrity and the quantitative Primigravida 22 9.17 (5.49; 12.84) bio-efficacy) were significantly associated with the incidence Secundigravida 36 15.00 (10.45; 19.55) of malaria infection during the first trimester of pregnancy, (IRRa = 0.40; (0.20–0.78); p < 0.003; IRRa = 0.44; (0.24– Multigravida 182 75.83 (70.38; 81.29) 0.81); p < 0.004; IRRa = 0.98; (0.95–0.99); p <0.02 respect- Ethnic Group 240 ively), confirming the results of the Cox model. Toffin 156 65.00 (58.92; 71.08) Others 84 35.00 (28.92; 41.08) Discussion Education level 240 The peculiarity of our study was the ability to have Illiterate 161 67.08 (61.09; 73.07) followed the women from the pre-conceptional period Literate 79 32.92 (26.93; 38.90) until the end of the first trimester of pregnancy. This Occupational status 240 study identified two sets of essential results, i) the re- Employed 221 92.08 (88.64; 95.52) fined characterization of the protection given to the Unemployed 19 7.92 (4.48; 11.36) pregnant women by the LLIN against malaria infection during the first trimester of pregnancy and ii) new im- Marital status 240 portant elements in the reflection on the different indi- Cohabitation 11 4.58 (1.92; 7.25) cators of LLIN’s efficiency that characterize properly the Married (monogamy) 159 66.25 (60.22; 72.27) real protection of pregnant women against malaria dur- Married (polygamy) 70 29.17 (23.37; 34.96) ing this critical period. Residence area 240 We observed a general high possession and good use Lake area 156 65.00 (58.92; 71.08) of LLIN by the study pregnant women. This is probably an indication of the success of the LLIN mass distribu- Land area 84 35.00 (28.92; 41.08) tion campaigns carried out previously in Benin in 2011 Pre-pregnancy malaria 227 and 2014. In all, the Cox model confirmed our working Yes 10 4.41 (1.72; 7.10) hypothesis that the different indicators were significantly No 217 95.59 (92.90; 98.28) related to the delay in malaria infection. Precisely, good Hounkonnou et al. BMC Public Health (2018) 18:683 Page 5 of 7 Table 2 Indicators of possession, use, physical integrity and chemical efficacy of LLINs inspected during follow-up, Sô-Ava and Akassato, Benin 2015–2016 (N = 240) Characteristics Pre-pregnancy Pregnancy visit 1 Pregnancy visit 2 Total Mean or proportion Total Mean or proportion Total Mean or proportion (95% CI) (95% CI) (95% CI) Possession of at least one LLIN/household 240 240 203 Yes 237 98.75 (96.17; 97.60) 239 99.53 (97.06; 99.94) 202 99.51 (96.53; 99.93) No 3 1.25 (0.40; 3.83) 1 0.42 (0.06; 2.94) 1 0.49 (0.07; 3.47) Possession of LLIN according to WHO standards (1 237 239 202 LLIN/2 people) Yes 178 75.11 (69.16; 80.23) 185 77.41 (71.63; 82.30) 164 81.19 (75.14; 86.03) No 59 24.89 (19.77; 30.84) 54 22.59 (17.70; 28.37) 38 18.81 (13.96; 24.85) Use of LLIN by pregnant women 237 239 202 Yes 199 83.97 (78.69; 89.13) 203 84.94 (79.78; 88.96) 178 88.12 (82.83; 91.93) No 38 16.03 (11.86; 21.31) 36 15.06 (11.04; 20.22) 24 11.88 (8.06; 17.17) Physical integrity of pregnant woman’s LLIN 237 239 202 Good 156 65.82 (59.51; 71.62) 145 60.67 (54.29; 66.70) 115 56.93 (49.95; 63.64) Bad 81 34.18 (28.38; 40.49) 94 39.33 (33.30; 45.71) 87 43.07 (36.36; 50.05) Physical integrity of household’s LLIN 169 195 164 Good 101 59.76 (52.12; 66.96) 117 60.00 (52.91; 66.70) 96 58.54 (50.77; 77.90) Bad 68 40.24 (33.04; 47.88) 78 40.00 (33.30; 47.09) 68 41.46 (34.10; 49.23) Bio-efficacy of pregnant women’s LLIN 198 Yes –– 12 6.06 (3.46; 10.41) No –– 186 Bio-efficacy of household’s LLIN 126 Yes –– 7 5.56 (2.64; 11.30) No –– 119 94.44 (88.70; 97.36) use, good physical integrity and the quantitative limit of the two classical indicators of ownership and re- bio-efficacy of the LLIN were found to be associated ported LLIN use the previous night to characterize ad- with a later occurrence of the first malarial infection equately the optimal protection of the pregnant woman during the first trimester of pregnancy. In this model the against the occurrence of a malaria infection. All these physical integrity of the LLIN was associated only mar- elements point out the need to consider, in addition to ginally significantly with the delay of the first malaria in- the classical ownership and reported use indicators, the fection but showed significant associations in the physical integrity and bio-efficacy indicators should be Poisson regression model. Five pregnant women had taken into account in evaluation studies of LLIN effi- malaria infection twice in our study. Two studies did not ciency to reduce the malaria burden in pregnant women. find any association between LLIN usage by pregnant In our study, the high proportions of good use and women and the risk of malaria infection [21, 22]. Since LLINs with good physical integrity are in favor of a good the effectiveness of LLIN to reduce the malaria burden physical barrier conferred by LLIN to the pregnant has been extensively established [23] including in preg- women during the first trimester of pregnancy. Never- nant women [15, 24–28], those result show probably the theless, a more worrying result was the small minority of Table 3 Proportion of pregnant women infected during the first trimester of pregnancy, Sô-Ava and Akassato, Benin 2015–2016 Malaria Pre-pregnancy visit Visit 1 Visit 2 Visit 3 infection n % (95% CI) n % (95% CI) n % (95% CI) n % (95% CI) Total 227 234 199 180 Yes 10 4.41 (2.37; 8.03) 14 5.98 (3.56; 9.88) 10 5.02 (2.71; 9.13) 17 9.44 (5.92; 14.73) A total of 239 pregnant women were followed during 626.63 person-months, with a median follow-up time of 88 days (Interquartile interval: 65–95) Hounkonnou et al. BMC Public Health (2018) 18:683 Page 6 of 7 A strengthof our studyisthatfor thefirst time in amal- aria cohort, the women were seen at a pre-conceptional stage which allowed to follow them on the very beginning of their pregnancy. This is an important strenght compared to non preconcepional studies. Although our results indi- cate minimal selection bias, the moderate size of our sam- ple and the particular facies of the study area (lake zone) impose some caution on the representativeness of the results. Conclusion Our study demonstrated for the first time an overall good physical protection against the malaria vector con- ferred by LLIN in pregnant women in their first trimes- ter of pregnancy, but low chemical protection in our Fig. 2 Probability of non-occurrence of malaria infection in women study area. An important conclusion is that, in addition during the first trimester of pregnancy, Sô-ava and Akassato, to the traditional indicator of possession of LLINs by Benin, 2015–2016 pregnant women, it is essential to take into account other indicators such as actual use, physical integrity LLIN reaching the bio-efficacy threshold set by the and bio-efficiency of LLIN, since all these indicators re- WHO recommendations. This raises the highly import- flect independently from each other the real protection ant question of the duration of the LLINs bio-efficacy in against malaria of this population. Further studies are field conditions. Given that optimal protection by the then needed to assess the generalizability of our results LLIN is provided by the combination of its physical bar- and also to control the duration of the chemical effect- rier and chemical efficacy, we can conclude that the ex- iveness of the LLIN distributed on the territory. treme majority of women in the study were not optimally protected against malaria in the first trimester Additional files of their pregnancy by the LLIN they used. This import- ant conclusion would have been missed if only based on Additional file 1: Table S1. Factors associated with delay in the first malaria infection during the first trimester of pregnancy, univariate Cox the ownership and usage classical indicators. analysis (N = 240); Sô-ava and Akassato, Benin 2015–2016. (DOCX 23 kb) Additional file 2: Table S2. Factors associated with the number of Table 4 Factors associated with the time to onset of the first malaria infections during the first trimester of pregnancy (multivariate malaria infection during the first trimester of pregnancy Poisson regression model, N = 194 pregnant women); Sô-ava and Akassato, Benin 2015–2016. (DOCX 16 kb) (multivariate Cox model, N = 190 pregnant women); Sô-Ava and Akassato, Benin 2015–2016 Abbreviations Variables (terms) Multivariatble Cox model ACT: Artemisinin Combined Therapy; CER-ISBA: Ethics Committee of the N HRa CI 95% pvalue Institute of Applied Biomedical Sciences; HRa: Hazard Ratio adjusted; Use of LLIN by the woman 190 IPTp: Intermittent Preventive Treatment in Pregnant women; IRRa: Incidence the week before the visit Rate Ratio adjusted; LBW: Low Birth Weight; LLIN: Long Lasting Insecticidal Nets; RDT: Rapid Diagnostic Tests; SP: Sulfadoxine - Pyrimethamine; No 36 1 TBS: Thick Blood Smear; WHO: World Health Organization Yes 154 0.38 (0.18–0.80) < 0.001 Acknowledgements Physical integrity of the pregnant 190 We acknowledge all the pregnant women, health center and field workers woman’s LLIN and the local authorities of Sô-Ava and Akassato Districts who participated in the EVALMOUS study. Bad 78 1 Good 112 0.59 (0.29–1.19) 0.07 Funding This work was supported by “Expertise France –Initiative 5%” (Mission n° Quantitative bio-efficacy of 190 0.97 (0.94–1.00) 0.04 15SANIN110), “Fondation Simone Beer” under the aegis of “Fondation de the pregnant woman’s LLIN France” and the French “Agence Nationale de la Recherche” (ANR-13JSV1–004-01). Malaria before pregnancy 190 Availability of data and materials Yes 9 1 The datasets used and/or analysed during the current study are available No 181 0.27 (0.09–0.74) 0.01 from the corresponding author on reasonable request. N Total, HRa Hazard ratio adjusted, CI 95% Confidence Interval at 95%, LLIN Authors’ contributions Long Lasting Impregnated bedNets, pvalue one-sided pvalue Quantitative bio-efficacy is defined as the proportion of female anopheles Project management: CH, AD, VB and GC (Principal Investigator). Field, who died 24 h after exposure to the LLIN Epidemiology and data collection: CH, AD, MA, EY and GC. Biology and Hounkonnou et al. BMC Public Health (2018) 18:683 Page 7 of 7 molecular analyses: NF LLIN’s laboratory tests: AB, CS and AD. Mapping: SE, relation to the risk of low birth weight, anaemia and perinatal mortality in CH and GC. Statistical analysis: CH, AD, PH and GC. Manuscript writing: CH, Burkina Faso. Malar J. 2012;11:71. AD, SE, PH, AB, CS, NF, MA, EY, VB and GC. All authors read and approved 12. Huynh B-T, Fievet N, Gbaguidi G, Dechavanne S, Borgella S, Guézo-Mévo B, the final manuscript. et al. Influence of the timing of malaria infection during pregnancy on birth weight and on maternal anemia in Benin. Am J Trop Med Hyg. 2011;85(2): 214–20. Ethics approval and consent to participate 13. Cottrell G, Mary J-Y, Barro D, Cot M. The importance of the period of The RECIPAL and EVALMOUS studies have received the ethical approval from malarial infection during pregnancy on birth weight in tropical africa. Am J the Ethics Committee of the Institute of Applied Biomedical Sciences (CER- Trop Med Hyg. 2007;76(5):849–54. ISBA: n° 60 of the 06/01/2015) and the Ministry of Health in Benin as well as 14. Ouédraogo S, Koura GK, Accrombessi MM, Bodeau-Livinec F, Massougbodji from the Comité Consultatif de Déontologie et d’Ethique (CCDE) from IRD in A, Cot M. Maternal anemia at first antenatal visit: prevalence and risk factors France. Before any inclusion in the study, free and informed consent was in a malaria-endemic area in Benin. Am J Trop Med Hyg. 2012;87(3):418–24. obtained from each woman after the study had been presented to her in 15. Gamble C, Ekwaru PJ, Garner P, ter Kuile FO. Insecticide-treated nets for the the local language. prevention of malaria in pregnancy: a systematic review of randomised controlled trials. PLoS Med. 2007;4(3):e107. Consent for publication 16. Bennett A, Smith SJ, Yambasu S, Jambai A, Alemu W, Kabano A, et al. Not Applicable. 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BMC Public HealthSpringer Journals

Published: Jun 1, 2018

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