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Background: The widespread use of artemisinin-based combination therapy (ACT ) and long-lasting insecticide- treated nets (LLINs) has led to an impressive decrease of malaria burden these recent years in Africa. However, some new challenges about the future of malaria control and elimination efforts have appeared. Among these challenges, the loss and—or—the only partial acquisition of anti-Plasmodium immunity among exposed populations lead to an increase of the age at risk of malaria. Indeed, older children and adults may become more vulnerable to malaria. Studies about malaria among adults seemed, therefore, important. This study investigated the evolution of malaria morbidity in adults of Dielmo (Senegal) before and after the implementation of LLINs. Methods: From August 2007 to July 2015, a longitudinal study involving adults above 15 years old was carried out in Dielmo, where ACT was introduced in June 2006 and LLINs in July 2008. In July 2011 and August 2014, all LLINs were renewed. The presence of each person in the village was monitored daily. Thick smears associated lately with rapid diagnosis test (RDT ) and quantitative polymerase chain reaction methods were performed for all cases of fever. To assess malaria prevalence, thick smears and RDT were performed quarterly in all individuals. Malaria risks factors were assessed using negative binomial regression mixed-model based on person-trimester observations. Results: Malaria morbidity among adults has decreased significantly since the implementation of LLINs in Dielmo. However, malaria resurgences have occurred twice during the 7 years of LLINs use. During these malaria resurgences, the overall incidence of malaria among adults was similar to the incidence during the year before the implementation of LLINs (adjusted incidence rate ratio [95% CI] aIRR = 1.04 [0.66–1.64], p = 0.88 and aIRR = 1.16 [0.74–1.80], p = 0.52 during the first and the second malaria resurgence period, respectively). Younger adults were most vulnerable during these malaria upsurges as the incidence of malaria increased significantly among them (χ = 5.2; p = 0.02). Conclusion: Malaria among adults especially younger adults should deserve more attention in the areas where malaria was previously endemic as they became vulnerable probably because of the partial acquisition and—or—the loss of anti-Plasmodium relative immunity and the non regular use of LLINs. Keywords: Malaria morbidity, Malaria resurgences, Adults, LLINs, Dielmo, Senegal *Correspondence: amele-nyedzie.wotodjo@ird.fr UMR VITROME ( Vecteurs-Infections Tropicales et Méditerranéennes) Campus International IRD-UCAD, Dakar, Senegal Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/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://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Wotodjo et al. Malar J (2018) 17:384 Page 2 of 9 region of central Senegal, 280 km south-east of Dakar Background on the marshy bank of the Nema, a small stream which Malaria burden decreased significantly in recent years in allowed the persistence of anopheline breeding sites year- Africa through the widespread use of Artemisinin-based round. Since June 1990, a long-term malaria research combination therapy (ACT) and long-lasting insecticide- project has been conducted among the population of treated nets (LLINs) associated with a combination of Dielmo. Malaria transmission was continuous over control interventions [1–3]. In the children < 5 years of the years from the beginning of the project until 2009, age, and the pregnant women, that represent the popula- when transmission became seasonal. The epidemiology tion at risk, the prevalence and the incidence of the dis- of malaria has changed significantly in this village, from ease have collapsed dramatically compared to the period holoendemic in 1990 to hypoendemic since 2010 [15]. In before the introduction of LLINs and ACT as first-line 2014, there were 45 concessions with approximately 450 treatment of malaria. These considerable advances sug - inhabitants, including 245 adults aged at least 15 years. gest the possibility of eliminating malaria in endemic countries [4]. However, this situation is changing the dis- ease epidemiology, as suggested by an increase of the age Participants and procedures at risk of malaria events [5]. Indeed, in former malaria The inhabitants of Dielmo willing to participate at the endemic areas, older children and adults are becom- project were involved in a longitudinal follow-up includ- ing more vulnerable to malaria [2, 6, 7]. Several reasons ing: (i) monitoring of all episodes of fever, and, (ii) may explain the increase of the age at risk. The compli - repeated quarterly cross-sectional surveys to document ance to LLINs use among older children and adults, and malaria prevalence and LLIN use. Written informed their behaviour during Anopheles biting time, have been consent was obtained from all participants. The study incriminated [2, 7–9]. Further, the decrease of human was approved by the Ministry of Health of Senegal, the exposure to malaria parasites due to the use of LLINs is assembled village population and the National Ethics reducing anti-Plasmodium immunity both in children Committee of Senegal. and adults [5, 10–12]. The increase of the age at risk of malaria could maintain malaria residual transmission and Medical surveillance of fever episodes generate serious concerns about the future of malaria Body temperature was systematically recorded in adults elimination efforts [2, 7]. This is all the more important in case of suspected fever or fever-related symptoms. In if consider that malaria controls and preventive measures case of fever, patients were referred to the project health have most often targeted children and pregnant women centre, which was open 24 h/day, 7 days/week. Thick [13]. smears stained with Giemsa were performed to deter- Because of these concerns, it seemed important to mine the presence of the malaria parasite by using light study malaria among adults in order to assess and adapt microscopy. Episodes of fever were attributable to Plas- the current control tools. Studies of malaria in adults modium falciparum malaria clinical attacks, when para- remain scarce, and new data on this topic are needed in site density was higher than an age-dependent threshold the current context of the fall of malaria in some areas [16]. Malaria clinical attacks were treated with the com- [1]. Therefore, an active monitoring of the population at bination artesunate plus amodiaquine since June 2006. risk is important in order to avoid malaria resurgences From 2011 onwards, the diagnostic and treatment policy and to assess eventual new risk factors. The aim of this were modified to maximize efforts to limit malaria trans - study was to investigate the evolution of malaria morbid- mission. The RDT and PCR were then combined with ity among adults of Dielmo (Senegal) between August the thick smear to improve disease diagnosis. Artesu- 2007 and July 2015, after ACT was introduced in the vil- nate plus amodiaquine were systematically given to all lage in June 2006 and LLINs were offered to all villagers patients with fever associated with malaria parasites, in July 2008 and then renewed in July 2011 and August detected by at least one of these three diagnostic tools 2014. This study describes and analyses the change in regardless of age and parasite density. malaria morbidity, prevalence and identifies the disease All participating households were visited daily. The risks factors among adults aged at least 15 years old after presence or absence in the village of each enrolled house- the implementation of LLINs in the village of Dielmo. hold member was monitored and the location of the absent member was reported. Malaria morbidity was then assessed by the estimation of the incidence rate. For Methods each period of the study, the malaria clinical attack inci- Setting: Dielmo site dence rate was calculated as the ratio of the number of The Dielmo research site has been described in detail clinical malaria attack recorded, divided by the number elsewhere [14]. The village is located in a Sudan-savannah of person-days of follow-up during a given period. Wotodjo et al. Malar J (2018) 17:384 Page 3 of 9 Malaria prevalence cross‑sectional surveys Rainfall was also measured each month of the study To assess asymptomatic carriage and malaria preva- period. The following variables were analysed: (i) lence each year, cross-sectional surveys were conducted age group (15–19 years, 20–29 years, 30–44 years, quarterly, with two surveys during the dry season and 45–59 years and 60 years and older); (ii) rainfall; (iii) two in the rainy season. Thick smears and RDT (since sex; (iv) pregnancy; (v) being quarterly resident (hav- May 2011) were performed in all individuals enrolled in ing spent at least 75% of the trimester’s days in Dielmo); the Dielmo project who were present in the village dur- (vi) being born in Dielmo; and (vii) the year of the use ing the survey. of LLINs. Each variable was analysed separately using bivari- ate analysis to assess the association with malaria risk. Quarterly LLINs repeat cross‑sectional surveys Random-effect negative binomial regression models LLINs (Permanet 2.0) were introduced for the first were used to analyse clinical malaria episodes and ran- time in the village in July 2008 and have been offered dom-effect Poisson model was used to analyse the risk of to all villagers. In July 2011 and August 2014, all LLINs malaria according to age group, taking into account the were renewed. In Dielmo, nets were distributed freely interdependence of successive observations in the same by sleeping place and the coverage is 100% with the slo- individuals. The days of monitoring for each person per gan “one bed, one net”. quarter were controlled as the exposure variable. Varia- Simultaneously with the introduction of LLINs, bles that were p < 0.2 in bivariate analyses were integrated repeat home-based surveys have been carried out to in multivariate analyses [17]. The significance level was assess their use. Each participating household was vis- fixed at p = 0.05 in the final model. The χ test for inci- ited quarterly, in the morning by two technicians, who dence rates was used to compare the incidence rate for verified ownership of nets and recorded whether the each year. Analyses were performed using Stata Software, nets were hung above the bed the preceding night. They version 11.0 (College Station, Texas, USA). also administered a short questionnaire to household members about LLINs use. Individuals were asked if they had used nets the night preceding the visit, and Results whether they always or sometimes or never, used nets. Description of participants Net ownership and it use were assessed per inhabitant There were 187 and 243 adults enrolled in the pro - of Dielmo present during the survey. All collected data ject who had spent at least 1 month in the trimester in were entered into the 4D software version 2004.5. Dielmo during the first (August–October 2007) and the last quarter (May–July 2015) of the study respectively. A total of 6558 person-trimester observations (551,650 Study population person-days) corresponding to 347 individuals aged from This study focused on person-trimester observations 15 to 103 years old with a mean of 38 years old and a pro- covering the period before and after LLINs implemen- portion of 58% of women were analysed. Among these tation, from August 2007 to July 2015. All adults of observations, 168 malaria clinical attacks were noted Dielmo who were enrolled in the project during this from whom 164 (2.5% of 6558 persons) were related to period and who had spent at least 30 days in the quar- individuals who had at least one malaria attack per quar- ter in Dielmo were included in the analysis. ter during the study period and 6394 (97.5%) observa- tions were related to adults who had no malaria attacks. Outcome and independent variables definition The number of malaria clinical attacks varied from 1 to 3 The study was conducted in a period of 8 years from attacks per adult per quarter. August 2007 to July 2015 and was divided in two peri- ods: (i) a first period of 1 year (August 2007 to July Incidence of malaria clinical attacks over the study period 2008) corresponding to the time before LLINs imple- Malaria decreased consequently after the implemen- mentation in Dielmo, which is used as a year of control; tation of LLINs in Dielmo. However, adults became (ii) a second period of 7 years from August 2008 to July more vulnerable to malaria since the implementation 2015 corresponding to the time of LLINs use in Dielmo. of LLINs especially during malaria resurgence periods. Malaria clinical attacks were grouped into 32 quar- Indeed, during the year before nets implementation, ters over 8 years (August–October, November–January, only 34% (0.20 attacks per person per year among adults February–April and May–July of each year, previously compared with 0.58 in the Dielmo population, adults defined). The analysis was thus based on person-tri - representing approximately 54% of the study popula- mester observations. The outcome variable was the tion) of malaria incidence rate and only 18% (34/189) of number of malaria attacks per adult per quarter. malaria cases occurred among adults, whereas since the Wotodjo et al. Malar J (2018) 17:384 Page 4 of 9 implementation of nets, approximately the same malaria attacks per adult per year during the malaria decreased incidence was observed among adults and children (0.06 periods when nets were implemented, and was 0.24 dur- attacks per person per year among adults and children ing malaria upsurge periods and was 0.20 during the year during the fourth and fifth years of LLINs implementa - before nets implementation. tion) (Fig. 1). A rise of malaria has occurred at the third year of Malaria incidence according to age groups of adults nets use, and the malaria incidence increased from 0.02 Comparing with the year before nets implementation, attacks per adult per year during the second years of malaria incidence has increased significantly among nets implementation to 0.22 attacks per adult per year. age group 15–19 years during malaria upsurge periods In response to the increase in malaria, all the LLINs (χ = 5.2; p = 0.02) (Fig. 1). Among the individuals aged were renewed in July 2011. Following that, malaria con- 15–19 years, the incidence of malaria was 0.17 attacks sequently decreased from 0.22 attacks per adult per year per person per year during the year before nets imple- recorded during the upsurge to 0.04 and 0.06 attacks per mentation, whereas during malaria upsurges period, adult per year during the fourth and the fifth year of nets malaria incidence increased to 0.43 and 0.52 attacks per implementation respectively (p < 0.001). person per year the first and the second malaria upsurge A second upsurge occurred during the sixth year of the periods respectively. Among older adults, no significant nets implementation corresponding to the third year of difference was observed during malaria upsurge periods the renewal of LLINs, and the malaria incidence shifted comparing with the year before nets implementation to 0.24 attacks per adult per year (p < 0.001). This led to (Fig. 1). a second renewal of all LLINs in Dielmo in August 2014 During the year before net implementation, no dif- and the malaria attack decreased again to 0.08 attacks ference of malaria incidence was observed according to per adult per year in the following year correspond- age groups (compared to adults aged 15–19 years, inci- ing to the 8 year of the nets implementation (p < 0.001) dence rate ratio [95% CI] IRR = 1.85 [0.63; 5.44] p = 0.27; (Fig. 1). Overall, the mean incidence of malaria was 0.08 IRR = 1.31 [0.45; 3.86] p = 0.62; IRR = 0.53 [0.12; 2.27] 15-19 years 20-29 years 30-44 years 45-59 years 0.7 ≥60 years global incidence in the populaon global incidence in adults 0.6 0.5 0.4 0.3 0.2 0.1 Aug. 07- Aug. 08- Aug. 09- Aug. 10- Aug. 11- Aug. 12- Aug.13- Jul. Aug. 14- Jul.08 Jul. 09 Jul. 10 Jul. 11 Jul. 12 Jul. 13 14 Jul. 15 Study periods Fig. 1 Incidence of malaria clinical attacks over the study period among adults in Dielmo Number of P. falciparum malaria aacks per person year Wotodjo et al. Malar J (2018) 17:384 Page 5 of 9 Malaria prevalence p = 0.39, IRR = 1.11 [0.29; 4.27] p = 0.88 respectively for Since the implementation of the nets, the prevalence of adults aged 20–29 years 30–44 years, 45–59 years and malaria among adults has decreased significantly from 60 years and older) whereas during malaria upsurge peri- 23% in 2007 (before LLIN) to 0.9% in 2014. During ods, younger adults were more vulnerable to malaria the upsurge periods, the prevalence did not increase than the oldest (compared to younger adults aged and was 2.5% and 0.2% in 2010 and 2013, respectively. 15–19 years, IRR = 0.44 [0.25; 0.78] p = 0.005; IRR = 0.43 According to the age group, the prevalence was how- [0.25; 0.73] p = 0.002; IRR = 0.28 [0.14; 0.56] p < 0.001, ever slightly higher in youngest adults than oldest over IRR = 0.22 [0.08; 0.55] p = 0.001 respectively for adults the study period (Fig. 2). Indeed, during 2008 and 2009, aged 20–29 years 30–44 years, 45–59 years and 60 years the mean of malaria prevalence was 11.7% among indi- and older). viduals aged 15–29 years and 2.9% among those aged 30 years and over. During the upsurge period in 2010, Factors associated with the risk of malaria clinical attacks the mean prevalence was 3.6% among individuals aged Table 1 describes both characteristics according to 15–29 years and 2.0% among those aged 30 years and malaria attacks and the results of the bivariate and mul- over. tivariate analyses. In bivariate analysis, compared with the year before nets implementation, the risk of malaria attacks among adults was the same during the third (the Entomological inoculation rate (EIR) first malaria upsurge period) and sixth year (the second The EIR decreased from 96.1 infective bites per person malaria upsurge period) after the nets implementation per year in 2008 to only 45.6 infective bites per person (IRR = 1.09 [0.69; 1.73] p = 0.71; IRR = 1.25 [0.81; 1.95] per year in 2009. However, it increased in 2010 during p = 0.32 respectively). Older adults had fewer clini- the first upsurge period to 88.7 infective bites per person cal malaria attacks compared with younger adults aged per year. In 2013, during the second malaria upsurge, the 15–19 years (IRR = 0.59 [0.39; 0.89] p = 0.013; IRR = 0.44 EIR increased from 7.6 infective bites per person per year [0.29; 0.66] p < 0.001; IRR = 0.32 [0.20; 0.53] p < 0.001, in 2012 to 43.1 infective bites per person per year. In 2014 IRR = 0.34 [0.18; 0.62] p < 0.001, respectively for adults and 2015, the EIR remained low and was 18.2 and 2.8 aged 20–29 years 30–44 years, 45–59 years and 60 years infective bites per person per year, respectively. and older). Being born at Dielmo, being quarterly resi- dent of Dielmo, rainfall and the sex were not significantly associated with malaria risk. Pregnancy was associated Net use with malaria risk [(IRR = 2.70 [1.43; 5.12] p = 0.02]. The overall use of nets was slightly higher among older After adjusting for potential covariates such as age, adults than young adults aged 15–29 years except 2008 sex, rainfall and days of monitoring of each person per (Fig. 3). During the first malaria upsurge period in 2010, quarter, no difference in malaria risk was found dur - the use of nets was significantly low among young adults ing the third year (the first malaria upsurge period) and aged 15–29 years and adults aged 45–59 years compared sixth year (the second malaria upsurge period) after nets with adults aged 30–44 years old (OR = 0.07[0.02; 0.25] implementation compared with the year before nets p < 0.001; OR = 0.06[0.02; 0.24] p < 0.001; OR = 0.23[0.06; implementation indicating that the risk of malaria during 0.85] p = 0.027 respectively for adults aged 15–19 years; these years (third and sixth year) of nets implementation 20–29 years and 45–59 years). During the second equal the risk of malaria before nets implementation in malaria resurgence period in 2013, older adults aged Dielmo (aIRR = 1.04 [0.66; 1.64], p = 0.88 and aIRR = 1.16 30–44 years used frequently their nets than young adults [0.74; 1.80], p = 0.52, respectively for the third and aged 15–29 years (OR = 0.15[0.004; 0.61] p < 0.001 and sixth year after nets implementation). The malaria risk OR = 0.09[0.02; 0.31] p < 0.001, respectively for adults remained lower among older adults compared to younger aged 15–19 years and 20–29 years compared with adults adults aged 15–19 old except for age group 20–29 years aged 30–44 years). for whom no significant difference of malaria risk was Except 2008, the first year of the implementation observed (aIRR = 0.68 [0.45; 1.03] p = 0.07; aIRR = 0.45 of nets, where the use of nets was the highest (81%), [0.30; 0.69] p < 0.001; aIRR = 0.33 [0.20; 0.54] p < 0.001; no significant difference was noted for the use of nets aIRR = 0.33 [0.18; 0.62] p < 0.001, respectively for adults according to the year of nets use. The use of nets has aged 20–29 years, 30–44 years, 45–59 years and 60 years then decreased from 81% in 2008 to its lowest in 2013 and older). Rainfall remained not significantly associ - with only 53% of nets use (Fig. 3). During the periods of ated with a risk of having malaria (aIRR = 1.0002 [0.9997; malaria upsurge, the use of nets was 57% and 53% in 2010 1.0007], p = 0.45). and 2013, respectively. However, the use of nets during Wotodjo et al. Malar J (2018) 17:384 Page 6 of 9 Table 1 Socio-demographic and other characteristics according to malaria attacks and results of random-effect negative binomial regression models exploring factors associated with malaria clinical cases (n = 6558) Characteristics Subcategory Number Malaria cases Bivariate analysis Multivariate analysis of observations No, n = 6394 Yes, n = 164 IRR (95% CI) P value aIRR (95% CI) P-value n = 6558 n (%) n (%) n (%) Socio-demographic characteristics Age group 15–19 years (ref ) 1227 (18.71) 1170 (18.30) 57 (34.76) 1 1 20–29 years 1363 (20.78) 1326 (20.74) 37 (22.56) 0.59 (0.39–0.89) 0.013 0.68 (0.45–1.03) 0.07 30–44 years 1771 (27.01) 1735 (27.13) 36 (21.95) 0.44 (0.29–0.66) < 0.001 0.45 (0.30–0.69) < 0.001 45–59 years 1378 (21.01) 1357 (21.22) 21 (12.80) 0.32 (0.20–0.53) < 0.001 0.33 (0.20–0.54) < 0.001 60 years and over 819 (12.49) 806 (12.61) 13 (7.93) 0.34 (0.18–0.62) < 0.001 0.33 (0.18–0.22) < 0.001 Sex Male (ref ) 2780 (42.39) 2699 (42.21) 81 (49.39) 1 1 Female 3778 (57.61) 3695 (57.79) 83 (50.61) 0.76 (0.55–1.05) 0.09 0.89 (0.65–1.22) 0.47 Resident/quarter No (ref ) 770 (11.74) 753 (11.78) 17 (10.37) 1 Yes 5788 (88.26) 5641 (88.22) 147 (89.63) 1.17 (0.71–1.95) 0.53 Born at Dielmo No (ref ) 1969 (30.02) 1923 (30.08) 46 (28.05) 1 Yes 6558 (69.98) 4471 (69.92) 118 (71.95) 1.11 (0.78–1.58) 0.56 Pregnancy No (ref ) 3567 (94.42) 3495 (94.59) 72 (86.75) 1 Yes 211 (5.58) 200 (5.41) 11 (13.25) 2.70 (1.43–5.12) 0.002 Year of the use of LLINs (1) Year before nets 756 (11.53) 724 (11.32) 32 (19.51) 1 1 implementa- tion (ref ) First year of the 771 (11.76) 766 (11.98) 5 (3.05) 0.14 (0.06–0.37) < 0.001 0.14 (0.05–0.35) < 0.001 use of LLINs Second year 818 (12.47) 815 (12.75) 3 (1.83) 0.08 (0.02–0.27) < 0.001 0.08 (0.02–0.25) < 0.001 of the use of LLINs Third year of the 829 (12.64) 788 (12.32) 41 (25) 1.09 (0.69–1.73) 0.71 1.04 (0.66–1.64) 0.88 use of LLINs Fourth year of 808 (12.32) 800 (12.51) 8 (4.88) 0.22 (0.10–0.47) < 0.001 0.21 (0.09–0.44) < 0.001 the use of LLINs Fifth year of the 839 (12.79) 828 (12.95) 11 (6.71) 0.29 (0.14–0.57) < 0.001 0.27 (0.14–0.56) < 0.001 use of LLINs Sixth year of the 873 (13.13) 828 (12.90) 48 (29.27) 1.25 (0.81–1.95) 0.32 1.16 (0.74–1.80) 0.52 use of LLINs Seventh year 864 (13.17) 848 (13.26) 16 (9.76) 0.41 (0.22–0.74) 0.003 0.39 (0.21–0.70) 0.002 of the use of LLINs Rainfall 1.0001 (0.9996– 0.60 1.0002 (0.9997– 0.57 1.0007) 1.0007) these upsurge periods was not significantly different from year of net implementation. The ownership of net other years of nets use except in 2008. reached its lowest level in 2013 with 71.6% of net own- The ownership of net was also the highest in 2008 ership. Over the study period, no important difference with 97.5%; it decreased slightly to 83.5% the second in net ownership was observed except in 2008 (Fig. 3). Wotodjo et al. Malar J (2018) 17:384 Page 7 of 9 60% 15-19 years 20-29 years 30-44 years 45-59 years ≥60 years 50% 40% 30% 20% 10% 0% 2007 2008 2009 2010 2011 2012 2013 2014 2015 Years Fig. 2 Malaria prevalence among adults in Dielmo from 2007 to 2015 15-19 years 20-29 years 30-44 years 45-59 years ≥60 years Net use (all Adults) Net ownership (all adults) 100 100 90 90 80 80 70 70 60 60 50 50 40 40 30 30 10 10 2008 2009 2010 2011 2012 2013 2014 2015 Years Fig. 3 LLINs ownership and its use according to the year among adults by age groups Discussion Unfortunately, two malaria resurgences occurred dur- This study has shown the evolution of clinical malaria ing 7 years of nets universal coverage in Dielmo and among adults before and after the introduction of LLINs the disease incidence has increased significantly among in the village of Dielmo. The efficacy of ACT together younger adults when comparing with the period before with LLINs to reduce malaria incidence was observed the implementation of LLINs. This observation under - in this study after nets implementation in Dielmo in July lines the fragility of current malaria control strategies 2008. This result is in line with the trend observed in based mainly on LLINs use. The relaxation of the popu - many endemic areas [18, 19]. lation to the regular use of LLINs constitutes one of the Net use (%) Malaria prevalence (%) Net ownership (%) Wotodjo et al. Malar J (2018) 17:384 Page 8 of 9 barriers to the effectiveness of this tool [19, 20]. Indeed, decreased recently with the introduction of nets [10, 12], despite LLIN implementation at the Dielmo village level, especially in younger adults. This situation was observed malaria resurgences were observed in young adults who in other areas [5, 6, 24]. Studies in Kenya showed that the represent the population at risk during these upsurges. mean age of people with clinical attacks increased stead- This situation was probably due to the low level of LLINs ily as exposure to mosquito declined [5], indicating a use in younger adults (15–19 years) compared to the rest probable loss of immunity against malaria and the shift of the population. in the age of malaria risk. Despite the probable loss or The non-regular use of nets among younger adults late acquisition of anti-Plasmodium immunity, no severe could be due to their behaviour as they tended to stay malaria was observed during the study period, perhaps much longer outside at night. This outdoor behaviour because of the close monitoring of the population. has been shown previously in some studies as malaria The important reduction of malaria in Dielmo after risk factor [2, 8]. In Dielmo after the implementation of the implementation of LLINs was spoiled by the occur- LLINs, the residual vector populations of Anopheles gam- rence of two malaria resurgences. During these malaria biae sensu lato and Anopheles funestus had an increased resurgences, the overall incidence of malaria equals preference to bite outdoors [21]; thus, spending time out the incidence of malaria before the implementation of lately at night remained malaria risk factor in this vil- nets among adults while malaria increased significantly lage [9]. Another explanation of the shift of malaria risk among younger adults. Before the implementation of age was that children often slept under LLINs with their nets, the portion of malaria attacks among adults was mother, while adult men specially slept later and not only 18%, and since 2010, this portion has been approx- often used their nets [22]. Some studies in Asia explained imately 50%. This observation underlines the fragility the increase of malaria attacks in adult men by forestry of malaria elimination efforts among adults and then and farmings activities and outdoor sleeping behaviour their vulnerability. The current prevention methods for crops protection; thus raising their level of exposure target mostly the children under five and pregnant to vector bites, compared to others groups of the popula- women and tend to reduce the incidence of malaria in tion [2, 7]. In South Africa and Swaziland, where malaria these risk groups and to shift the burden of the disease has decreased drastically, the incidence of malaria was to older children and adults [2]. During the time of net highest among men and this was associated with their use, except for malaria resurgence periods in adults, the outdoor activities [8, 23]. According to gender, no differ - overall malaria incidence remained significantly low in ence in malaria risk was noted in this study. Dielmo [26]. The vulnerability of adults especially the youngest could also be explained by a poor acquired immunity against malaria. One year before the implementation Conclusions of nets in Dielmo, all adults were almost at same risk of These results highlight the need to take into account malaria, whereas after the implementation of nets espe- adults in the fight against malaria, and possible elimina - cially during malaria upsurge periods, younger adults tion. Malaria in adults, especially young adults, should became more vulnerable to malaria. It has to be noted deserve more attention in the areas where malaria was that these younger adults were almost children when nets previously endemic, as adults become vulnerable prob- were implemented in the village. They were conceivably ably because of the reduced acquisition and/or the loss less susceptible to develop an immunity against malaria of anti-Plasmodium immunity and the non-regular during their adulthood, since LLINs act by reducing use of their nets. Awareness campaign and monitor- human-vector contact, and thereby reducing their expo- ing of the use of nets remained crucial to avoid malaria sure to Plasmodium parasites. Nets use could decrease resurgences. immunity against malaria among population who have Authors’ contributions often used LLINs [24, 25]. It was demonstrated by pre- CS and ANW designed the study and supervised the data collection. ANW vious studies that the decrease of malaria transmission analysed the data with the contribution of SD and JG. ANW and SD wrote the manuscript with the contribution of JG and ND. FDS, ND, CS and PP con- could shifted the age risk of malaria and thus increase the tributed to the design and the monitoring of the study. All authors read and age of immunity against malaria [5, 10]. During the study approved the final manuscript. period, malaria prevalence decreased greatly, showing Author details the scarcity of asymptomatic cases because of the prob- UMR VITROME ( Vecteurs-Infections Tropicales et Méditerranéennes) able non-acquired and or loss of immunity [10–12] as 2 Campus International IRD-UCAD, Dakar, Senegal. Aix Marseille Univ, IRD, almost all new infections became symptomatic. Adults of AP-HM, SSA, VITROME, IHU-Méditerranée Infection, Marseille, France. Unité d’Épidémiologie des maladies Infectieuses, Institut Pasteur de Dakar, Dakar, Dielmo were highly protected in the past against malaria Senegal. Aix Marseille Univ, IRD, INSERM, AP-HM, SESSTIM, BioSTIC, Marseille, because of their acquired immunity; this immunity has France. Wotodjo et al. Malar J (2018) 17:384 Page 9 of 9 Acknowledgements October and November of 2013: a case-control study. Am J Trop Med We are grateful to Dielmo villagers for their participation to the project. We Hyg. 2015;92:565–8. thank all the staff of IRD and Pasteur Institutes of Dakar who contributed to 10. Diop F, Richard V, Diouf B, Sokhna C, Diagne N, Trape JF, et al. Dramatic the design, healthcare and data collection during the project. declines in seropositivity as determined with crude extracts of Plasmo- dium falciparum schizonts between 2000 and 2010 in Dielmo and Ndiop, Competing interests Senegal. Malar J. 2014;13:83. The authors declare that they have no competing interests. 11. Trape JF, Tall A, Diagne N, Ndiath O, Ly AB, Faye J, et al. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated Availability of data and materials bednets and artemisinin-based combination therapies: a longitudinal Data can be made available upon request to the corresponding author. study. Lancet Infect Dis. 2011;11:925–32. 12. Niang M, Niass O, Diagne N, Sarr FD, Faye MM, Diop F, et al. Temporal Consent for publication analysis of IgG antibody responses to Plasmodium falciparum antigens All authors read and approved the final manuscript and agree to its in relation to changing malaria epidemiology in a West African setting. submission. Malar J. 2017;16:283. 13. Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI. The global distribu- Ethics approval and consent to participate tion of clinical episodes of Plasmodium falciparum malaria. Nature. Written informed consent was obtained from all participants. The study was 2005;434:214–7. approved by the Ministry of Health of Senegal, the assembled village popula- 14. Trape JF, Rogier C, Konate L, Diagne N, Bouganali H, Canque B, et al. The tion and the National Ethics Committee of Senegal. Dielmo project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoen- Funding demic area of Senegal. 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Malaria Journal – Springer Journals
Published: Oct 25, 2018
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