On-going malaria transmission in The Gambia despite high coverage of control interventions: a nationwide cross-sectional survey
© Mwesigwa et al. 2015
Received: 30 March 2015
Accepted: 3 August 2015
Published: 14 August 2015
As indicators of burden of malaria have substantially decreased in The Gambia, reaching a pre-elimination status may be attainable. Achieving this goal requires in-depth understanding of the current burden of Plasmodium falciparum infection.
A nationwide cross-sectional survey was conducted in 2012 to determine the prevalence of P. falciparum infection, and to describe its heterogeneity and associated risk factors. Finger-prick blood samples were collected for microscopy, species-specific PCR and haemoglobin measurement.
A total of 9,094 participants were included and median age was 11.9 years (IQR 5, 28). Overall prevalence of P. falciparum was 16.01 % with marked heterogeneity between sites (4.32–36.75 %) and within villages in each site (1.63–49.13 %). Across all sites, 51.17 % (745/1,456) of infections were asymptomatic and 35.61 % (448/1,258) were sub-microscopic. The odds of P. falciparum infection were higher in older children; 5–15 years (OR = 1.90; 95 % CI 1.60–2.26), adults (OR = 1.48; 95 % CI 1.24–1.78) and participants with moderate anaemia (OR = 1.62; 95 % CI 1.32–1.99).
The current malaria control interventions are not sufficient to interrupt transmission in The Gambia as malaria prevalence is still relatively high in the eastern part of the country. New interventions aiming at interrupting transmission are needed and should be urgently evaluated.
The last decade has witnessed major progress in the fight against malaria as the burden has substantially reduced, even in sub-Saharan Africa, although malaria still contributes significantly to both morbidity and mortality [1, 2]. The Gambia is one of the African countries where a substantial decline has been observed [3, 4]. This decline resulted from the scaling-up of malaria control intervention , which includes: increased availability and access to long-lasting insecticide bed nets (LLINs), integrated vector control interventions such as indoor residual spraying (IRS), strengthened case management with rapid diagnostic tests (RDTs), and artemisinin combination therapy (ACT). Despite the scaling-up of these interventions, malaria transmission, which is highly seasonal, has not been interrupted. Earlier studies in schoolchildren [6, 7] showed marked heterogeneity in malaria prevalence across the country and significant seasonal variation . In addition, high resistance to DDT and pyrethroids observed in some areas raises concerns about the impact of current vector control interventions [9, 10].
As the country aims for pre-elimination status, gaining a detailed understanding of the current distribution of malaria infection, characterizing its heterogeneity across the country and further identifying asymptomatic carriers is critical as these are important elements for disease surveillance and targeting control efforts. Whereas health facility data have previously been used to describe malaria morbidity trends , this information is greatly limited by incompleteness, differing malaria case definitions and the lack of data on asymptomatic carrier status. This cross-sectional survey was, therefore, conducted to better characterize the dynamics of malaria transmission in The Gambia and to identify the determinants of its heterogeneity.
Each participant was allocated a unique study ID code and individual interviews were conducted for older children (12–17 years) and adults, while parents/guardians completed the questionnaire for younger children (6 months–11 years). Individual participant information on demographic and general health indicators such as history of fever, sleeping habits (including outdoor or out in the field) and travel outside the village in the past month and IRS were collected using a structured questionnaire. Individual participants were asked if their house had received IRS in the last 1 year and in addition if they had slept under a LLIN the previous night. Axillary temperature was measured using a digital thermometer. A finger-prick blood sample was collected from each participant on a blood slide for microscopy and spotted on filter paper (Whatman 3 Corporation, Florham Park, NJ, USA) for molecular analysis. Haemoglobin (Hb) was measured with the HaemoCue 301 machine (Ängelholm, Sweden) following the manufacturer’s instructions.
To determine parasite density, microscopy was read on all samples that tested positive by PCR. Slides were stained with 2.5 % buffered Giemsa (pH 7.2) for 30 min and double read by trained microscopists who were blinded to the survey data of the participants. Slide smears were declared negative if no parasite was seen after examining 200 high power fields (HPF). If positive, parasites were counted against 500 white blood cells (WBCs and parasite densities were calculated assuming 8,000 WBC per μl of blood. A 20 % error check was used to identify discrepancies between slide readers. All discordant results were read by a senior microscopist who was also blinded to participant survey data and these results were taken as the final read.
For diagnostic PCR, three 6-mm dried filter-paper blood spots (DBS) were punched into a 96-well plate. DNA extraction was carried out using the automated QIAxtractor robot (Qiagen). Negative and positive (3D7) controls were included to control for cross contamination and DNA extraction efficiency, respectively. The DBS were lysed by incubating them in tissue digest buffer at 60 °C for 1 h and digested eluates were applied onto capture plates, washed, and the DNA eluted into 80 µl. The extracted DNA (4 µl) was used in a nested PCR, amplifying the multicopy Plasmodium ribosomal RNA gene sequences using genus and species specific primers . All PCR products were run using the QIAxcel capillary electrophoresis system (Qiagen), using the screening cartridge and 15-1,000 bp-alignment marker. Results were exported and double scored using both the QIAxcel binary scoring function and manually by visualization of the gel images and discrepancies were scored by a third independent reader. All readers were blinded to participant survey data.
The sample size was based on the desired precision of the prevalence of infection by village; 300 individuals allowed an estimation of the prevalence with the following precision: 1 % (95 % CI 0.2–3 %); 5 % (3–8 %); 12 % (8–16 %), and 20 % (16–25 %). Data from questionnaires were verified for completeness and all data were double entered and verified using Microsoft Access database (Microsoft Corp., Redmond, USA). Errors in data entry were detected by running consistency checks before exportation to STATA 13.0 (StataCorp, College Station, Texas, USA) for analysis. Age groups were categorized into <5 years, ≥5 to ≤15 years and >15 years [13, 14]; anaemia was defined according to the WHO Haemoglobin concentration for diagnosis of anaemia and assessment of severity; as severe (<8.0 g/dl), moderate (8.0–10.9 g/dl), or mild (11.0–12.9 g/dl) and no anaemia (≥12.9 g/dl) . Carriage of Plasmodium falciparum infection was defined as parasitaemia detected by PCR at screening . LLIN coverage was reported as the proportion of the population that slept under an LLIN the previous night.
Descriptive statistics are presented for continuous variables (median and interquartile range), and proportions for categorical variables and all point estimates presented with 95 % confidence intervals calculated using the Wilson score method with continuity correction. Uni- and multi-variable logistic regression analyses were performed to determine the independent predictors of P. falciparum infection. To account for missing data, complete case analyses were presented along with multiple imputation models (50 iterations), which allowed for the inclusion of partially observed cases. For multiple imputation analysis, a fully conditional model specification [17, 18] was adopted in which a logistic model was used for binary variables (gender, slept under a LLIN the previous night, sleep outdoors at night, IRS, sleep in the fields, and used artemether-lumefantrine the previous week) and an ordinal logistic model was performed for age and anaemia categorical variables. There was an allowance for clustering between and within the six sites in the uni-multivariable models. For age and anaemia, categorical variables, tests for trend and significance of the associations were performed in the multivariable models and, a goodness of fit test performed for the final model. For the analysis of microscopy, the median asexual and sexual parasite densities were calculated and the proportions of parasitaemia determined. The geolocations and P. falciparum prevalence data of each village were imported from Microsoft access and transferred separately onto a layer containing the base map of The Gambia generated using Quantum GIS 2.0.1 (QGIS 2.0.1). The village GPS points with the corresponding variable attributes were then displayed on the new layer and the maps were exported as jpeg, 800dpi file format (Fig. 1).
This study was approved by the Gambia Government/MRC Joint Ethics Committee (SCC1318). Verbal consent for participation was first obtained during the village sensitization meetings. Written informed consent was obtained for all participants, with parents/guardians providing written consent for children less than 12 years. Assent was also obtained from children aged between 12 and 17 years.
Demographic and clinical profiles of the study population
Age (N = 9,079)
Gender (N = 9,094)
Anaemia (N = 8,991)
No anaemia (>12.9 g/dl)
Mild (11.0–12.9 g/dl)
Moderate (8.0–10.9 g/dl)
Severe (<8.0 g/dl)
Has received indoor residual spraying in past 1 year (N = 9,094)
Has slept under a LLIN the previous night (N = 8,621)
Has slept outdoors at night (N = 9,064)
Has used an LLIN outdoors at night (N = 3,689)
Has history of fever in the last 24 h (N = 9,094)
Presence of fever (axillary temperature ≥37.5 °C) (N = 9,094)
Has taken artemether-lumefantrine in past 2 weeks (N = 9,094)
Plasmodium falciparum prevalence and risk factors by site (%)
North bank region
Plasmodium falciparum prevalence
Age, median (IQR)
15 (5, 36)
11 (5, 25)
12 (5, 30)
10 (5, 27)
12 (5, 30)
11 (5, 24)
N = 1,226
N = 1,329
N = 1,357
N = 1,674
N = 1,721
N = 1,684
Has slept under a LLIN last night
Has slept outdoors
Indoor residual spraying
The proportion of participants that reported sleeping under an LLIN the previous night was high [95.63 % (8,244/8,621); 95 % CI 95.17–96.04 %] across all sites while [78.84 % (7,170/9,094); 95 % CI 77.99–79.68 %] of the participants reported having received IRS in their households the previous year. A relatively high proportion of individuals [42.0 % (3,807/9,064); 95 % CI 40.98–43.03 %] slept out doors at night; this was more frequent in the eastern part of the country, i.e., URR-north bank [63.60 % (1,071/1,684); 95 % CI 61.24–65.89 %], CRR-north bank [58.27 % (976/1,675); 95 % CI 55.86–60.64 %] and URR-south bank [44.61 % (769/1,724); 95 % CI 42.24–46.99 %] (Table 2). Few individuals [3.19 % (291/9,094); 95 % CI 2.85–3.59 %] reported travelling outside their village or sleeping in the fields during this period. Although [46.13 % (4,195/9,094) 95 % CI 45.10–47.16 %] of the participants reported a history of fever in the preceding 24 h at the time of the survey, only [5.48 % (498/9,094); 95 % CI 5.02–5.97 %] had a documented fever (axillary temperature ≥37.5 °C). Only 1.9 % of participants [(174/9,094); 95 % CI 1.65–2.22 %] reported having taken artemether-lumefantrine, the first-line anti-malarial treatment at the time of the survey (Table 1). Of the 865 slides read by microscopy, the median (IQR) asexual P. falciparum density was 2,000 µl (192, 12,720) and the median (IQR) gametocyte density (N = 225) was 80 µl (32,224).
Prevalence of Plasmodium falciparum as determined by PCR by site and village
Plasmodium falciparum prevalence
Risk factors for Plasmodium falciparum infection (uni- and multi-variable analysis, complete case and multiple imputation analyses, multilevel logistic model)
Multivariable analysis (full model, complete case analysis) (n = 8,362)
Multivariable analysis (full model, multiple imputation analysis) (n = 9,094, 50 imputations)
OR (95 % CI)
OR (95 % CI)
OR (95 % CI)
≤5 years (N = 2,477)
5–14.9 years (N = 2,811)
≥15 years (N = 3,791)
Male (N = 5,417)
Female (N = 3,670)
No anaemia (N = 2,198)
Mild (N = 3,783)
Moderate (N = 2,671)
Severe (N = 137)
Has slept under a LLIN last night
No (N = 377)
Yes (N = 8,244)
Has slept out doors
No (N = 5,257)
Yes (N = 3,807)
Indoor residual spraying
No (N = 1,883)
Yes (N = 7,170)
Has slept out in the fields
No (N = 8,727)
Yes (N = 321)
Used Artemether-lumefantrine in past week
No (N = 8,881)
Yes (N = 174)
Whereas the burden of malaria in The Gambia has decreased significantly over the last 10 years [3, 4], probably because of the moderately high coverage of preventive interventions (LLINs and IRS) and free access to ACT, malaria transmission is ongoing. The prevalence of P. falciparum infection in villages in the NBR (site 2) was similar to that reported from community-based surveys in 2009 , implying that despite a substantial reduction, malaria transmission is still ongoing. The observed prevalence of infection close to 50 % in some villages in the eastern part of the country is comparable to the prevalence reported from high transmission areas in Tanzania , Gabon  or Burkina Faso . In the rest of the country, prevalence was much lower and heterogeneous, with a five- to eight-fold difference between neighbouring villages. Although the selection of villages for this survey was done according to documented high prevalence of anti-malarial antibodies in school children, the results reported are likely to be a fair representative of the malaria transmission in The Gambia as geographical representation was taken into account.
The difference in transmission between the eastern part and the rest of the country cannot be explained by different coverage of LLINs, as their reported use is relatively high throughout the country and LLIN use reduced odds infection of P. falciparum infection. However, the high resistance to DDT and pyrethroids observed in eastern Gambia [9, 10] and in Senegal  could be responsible for the higher malaria prevalence. Other factors to consider are increased outdoor biting of the local vectors in response to environmental changes as has been reported previously [22, 23], the differences in vector composition across the regions could also contribute to the higher prevalence of P. falciparum in the eastern region. A. gambiae s.s and A. arabiensis are the predominant and in general most efficient vectors in the east, while other areas of the country have less efficient vectors, such as A. melas and A. coluzzii. In addition, this region has more difficult access to health care and prompt treatment. For the latter, the eastern part of The Gambia, where the highest malaria prevalence has been observed, is the least developed and the farthest from the capital.
The low malaria prevalence observed in the western part of the country is consistent with earlier reports in 2008  indicating that 4 years later and despite high coverage of preventive interventions, the human reservoir of infection has not decreased substantially. A significant proportion of infections in this region were also sub-microscopic, implying that they would be missed by routinely used diagnostic tools and would therefore go untreated, hence contributing to maintain the human reservoir of infection and transmission. Conversely in the URR-south bank and NBR, whereas the majority of infections were detected by microscopy, a significant proportion of the participants were asymptomatic and thus unlikely to attend health facilities. Such individuals could therefore remain parasitaemic in the community and maintain residual transmission as well.
Identifying individuals who constitute this reservoir of infection would be extremely important for the identification of ‘hot spots’ in these villages, and designing and targeting interventions aimed at further decreasing malaria transmission. Assuming such carriers are mostly the same individuals from one transmission season to the other, because of environmental factors, such as higher exposure to infectious bites, residing in households near breeding sites, or genetic factors , targeting them for treatment could interrupt transmission. An intense follow-up of some villages included in this survey and covering several transmission seasons is currently ongoing and should be able to prove or disprove this hypothesis.
As previously reported [25, 26], about 36 % of PCR-positive samples were negative by microscopy and thus had sub-microscopic infections. The role of such infections in maintaining transmission remains unclear and urgently needs to be addressed . Sub-microscopic infections may be important in maintaining transmission; an increasing body of evidence indicates that a large proportion of gametocyte carriers remain undetected by microscopy, and gametocytes may actually be present in the majority of infections, albeit at low densities . When considering that the association between gametocyte density and mosquito infection rate is not very strong and is most variable at low gametocyte concentrations , the contribution of the carriers identified within this survey to the maintenance of malaria transmission is plausible. The challenge is to identify and treat them in the most efficient way. Active case detection strategies are increasingly popular across a number of countries although there is little evidence of their effectiveness . Their main limitation is the sensitivity of the diagnostic screening tools used, which would miss an important proportion of sub-microscopic carriers unless field-adapted molecular diagnostic methods are used [30, 31]. Other chemoprevention approaches, such as seasonal chemoprevention in children less than 5 years of age recently implemented in some regions of The Gambia and mass drug administration aimed at eliminating the reservoir of infection should be considered as additional interventions, especially in areas where transmission has not declined significantly.
The prevalence of asymptomatic parasitaemia was significantly higher in the older children and adults, possibly the result of stronger immunity, making them able to tolerate  but not eliminate a malaria infection. Therefore, infections acquired among older children and adults during the current transmission season may remain asymptomatic and untreated, resulting in the higher prevalence observed in these age groups. Nevertheless, such infections are not without consequences as infected individuals had a significantly higher risk of anaemia. This suggests that even if not associated with acute symptoms, malaria infections do have a deleterious effect on the health of infected individuals. A similar association was described in Ghana , Cameroon  and Tanzania  but not among Ugandan schoolchildren .
When considering the distribution of malaria infection across The Gambia, two main strata can be identified: the eastern part where transmission is still relatively intense, with villages in which a third to a half of the population infected, and the western part with low prevalence. Within each stratum, there is considerable heterogeneity between villages. It is remarkable to notice that even in the low endemicity stratum and despite high coverage of preventive and curative interventions, transmission has been maintained over the years. Obviously, current interventions are not sufficient to interrupt transmission in the current context of modified human and vector behaviour and new approaches need to be urgently evaluated. The low endemicity stratum in The Gambia offers an ideal setting to test new interventions aiming at interrupting malaria transmission.
JM conducted the study, analysed the data and wrote the manuscript; JO participated in coordinating the study and reviewed the final version of manuscript; MA supervised the molecular diagnostic analysis, microscopy reads and reviewed the final version of the manuscript; DN reviewed the final version of the manuscript; GLD performed the data analysis and reviewed the draft manuscripts and final version of the manuscript; OJ conducted the diagnostic PCR and reviewed the final version of the manuscript; KOO created the figure legends and reviewed the final version of the manuscript; KP reviewed the final version of the manuscript; JA reviewed the results, wrote the manuscript and reviewed the final version manuscript; UD conceived the study, reviewed the results, the draft manuscripts with JM and JA, and the final version of the manuscript for publication. All authors read and approved the final manuscript.
The study team is grateful to the village leaders and study participants who gave tremendous support and willingly allowed us to collect the data and samples. We are grateful to Mr Archibald Worwui for his support on the data management. The tireless effort of our field teams (assistants and nurses) is greatly appreciated. We acknowledge the tremendous support received from The Gambia Ministry of Health and Social Welfare and National Malaria Control Programme.
This work is funded Medical Research Council (MRC), UK and the Department for International Development (DFID), UK, under the MRC/DFID Concordat Agreement. Grant number MC_EX_MR/J002364/1.
Compliance with ethical guidelines
Competing interests The authors declare that they have no competing interests.
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.
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