Characteristics of Asymptomatic Plasmodium Spp
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Owusu et al. Malar J (2016) 15:38 DOI 10.1186/s12936-015-1066-8 Malaria Journal RESEARCH Open Access Characteristics of asymptomatic Plasmodium spp. parasitaemia in Kwahu‑Mpraeso, a malaria endemic mountainous district in Ghana, West Africa Ewurama D. A. Owusu1,2,7*, Vincent Buabeng3, Samuel Dadzie4, Charles A. Brown2, Martin P. Grobusch1,5,6 and Petra Mens1,7 Abstract Background: Malaria control efforts in Ghana have reduced the countrywide average malaria prevalence from 71 % in 2000 to about 51 % in 2012; however, its main focus is on symptomatic malaria. If further progress is to be made, parasite reservoirs in asymptomatic carriers need to be moved into focus. This study profiles asymptomatic Plasmo- dium spp. parasitaemia amongst residents of mountainous Kwahu-Mpraeso in the Eastern region of Ghana. Methods: A cross-sectional study of 360 residents was carried out from October to December 2013. This included recording demographics, malaria testing of asymptomatic residents, and gathering of their malaria history. Assess- ment of malaria transmission was done with molecular identification of vectors, determination of sporozoite rate, insecticide resistance status and biting pattern. Univariate and multivariate analysis were used to establish risk determinants. Results: In Mpraeso, in the Kwahu highland of Eastern Region, children were at higher risk of asymptomatic parasi- taemia, thereby contributing to the parasite reservoir and hence sustained malaria transmission. As well, findings sug- gested Hb AC genotype influenced susceptibility to asymptomatic malaria with 8.03-fold increase in odds (univariate) and 11.92-fold higher odds (multivariate) than the normal Hb AA. The mosquito vector predominant in the area was Anopheles gambiae sensu stricto of the homozygous pyrethroid resistant form (RR); with biting mainly occurring indoors. Conclusion: For an effective malaria control in this area, interventions should be formulated and implemented to target asymptomatic parasite reservoirs; especially in children and people with Hb AC. The dominant vector species An. gambiae s.s. and its feeding patterns of biting indoors should also be considered. Keywords: Asymptomatic malaria, Plasmodium parasitaemia, Highland, Ghana, Sickle cell trait, Anopheles gambiae Background The entire population of 25.9 million people is at risk of Ghana, a malaria endemic country, is actively fighting malaria [1, 2]; even though transmission is more intense against this deadly disease which still killed about 2500 in the rural areas, relative to the urban areas [2, 3]. The people out of 1,639,451 confirmed cases in 2013 [1]. focus of malaria control in Ghana is on preventive meas- ures such as use of long-lasting insecticidal nets (LLIN) and timely diagnosis and treatment in order to reduce the *Correspondence: [email protected] burden of disease [2, 4]. This has resulted in a noteworthy 2 Department of Medical Laboratory Sciences, School of Biomedical decline in national malaria prevalence over the years [2] and Allied Health Sciences, College of Health Sciences, University of Ghana, Accra, Ghana from 71 % in 2000 [5] to about 51 % in 2012 [4]. Full list of author information is available at the end of the article © 2015 Owusu et al. 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. Owusu et al. Malar J (2016) 15:38 Page 2 of 10 It seems that a blanket approach of interventions by currently approved pyrethroid, used in indoor spraying the Ministry of Health and the Ghana Malaria Control and insecticide-treated nets [30]. In addition, mosquitoes Programme, such as roll-out of LLIN, indoor residual are adapting their feeding behaviour in response to the spraying (IRS), change of first-line treatment to arte- use of preventive measures, such as LLIN [31, 32]. How misinin-based combination therapy (ACT), shift from these characteristics are expressed in the highlands of presumptive treatment to diagnostic + treatment and forest ecological zones in Ghana is unknown and needs availability of WHO pre-qualified malaria rapid diag- to be assessed, if situation-specific, well-adapted malaria nostic test kits (RDT), has worked in Ghana to reduce control policies are to be formulated. malaria cases and deaths [4]. Currently, studies are focus- In order to maintain this momentum of progress and to ing on elements that are essential in formulating tailor- assess what interventions may help to reduce the malaria made interventions for the different populations, such as burden further; more information is needed on the above parasite presence in humans and resistance to drugs [6– mentioned aspects. Therefore, this study set out to pro- 8], resistance of Anopheles vectors to insecticides [9–13], spectively assess the asymptomatic malaria parasite knowledge and health-seeking behaviour of the popula- burden in a rural population in the Kwahu highland of tion affected [14–16], and the burden that malaria poses Eastern Region of Ghana, the influence of SCD, and some on specific risk groups like pregnant women [17–19]. vector characteristics in this area. However, a lot more needs to be done in these areas. Next to symptomatic malaria patients that visit health Methods clinics for treatment, asymptomatic carriers of malaria Study sites and population parasites need to be appropriately treated as well in order Kwahu-South is one of the districts of the Eastern region to reduce or even interrupt transmission. Studies have of Ghana, and Mpraeso is its capital. The district is 1876 shown that in areas of intense malaria transmission, sq km in size and located between latitude 06°35′36″N such as Ghana, asymptomatic children are major carriers and longitude 00°44′05″W. Mpraeso is divided into six of Plasmodium falciparum [20, 21] and, therefore, con- clusters: Ntuntuagya, Akropong, Plot su, Lion House, tribute to the parasite reservoir [22, 23]. Other patient Nsuase and Kwasifori and has an approximate total popu- groups that may need a more specific, rather than a one- lation of 11,500 (Kassim Basit, personal communication). size-fits-all, approach are individuals with haemoglobi- It lies in the tropical rain forest malaria-epidemiolog- nopathies, such as sickle cell disease (SCD). The sickle ical zone [33] and has many streams and marshy areas. cell trait (Hb AS) is known to grant a certain degree of Kwahu, like other parts of the southern half of Ghana, has protection against severe malaria whilst heterozygosity two main rainy seasons: major rainy season from May to worsens the course of disease [24, 25]. June and minor rainy season from September to October. Ghana is known to have up to 18.8 % of its population In general, malaria occurs all year round, as is the case harbouring the HbS allele [26], with about 2 % of new- everywhere in Ghana [11, 34]. It is the commercial hub of borns having SCD [27]. Haemoglobin C is also relatively the rural mountain peak (788.21 m). For this reason only common in West Africa [25, 28, 29], Ghana included residents who had lived there for a minimum of 6 months [29]. In both Hb S and Hb C mutations occur in the 6th were included in the study. Individuals of all ages were position in the beta-globin amino acid sequence (β-6) considered in this study, unless the required number for such that glutamic acid is substituted with lysine (Hb a particular age-group reached its limit. C) or valine (Hb S) [28]. Some work has been done on the influence of haemoglobin S and C in asymptomatic Study design and participant selection Plasmodium spp. carriers in the northern part of Ghana This cross-sectional survey was done between Octo- [20, 24], where an increased risk for Plasmodium malar- ber and December of 2013 to obtain baseline data of the iae and P. falciparum infections was observed in people malaria situation in the Mpraeso area. The study com- who were homozygous HbCC [20]. It was also shown prised of two parts: a questionnaire-laboratory survey that although Hb AS offered better protection against and an entomological survey. Permission was sought malaria, Hb AC reduced the risk of severe malaria [24]. from the District Health Directorate and household In order to effectively control malaria in Ghana, there is heads before commencement. Each cluster was strati- a need to better understand the complexities of asympto- fied into age groups (0–5, 6–10, 11–15, 16–20, 21–40 matic malaria, including its interaction with SCD. and over 40 years) for which systematic selection from Next to control in humans, many programmes also every 8th household was done. Sixty participants in each intervene at the vector level. However, this is being ham- cluster were recruited. All the members of each house- pered by the emergence of resistant mosquitoes to the hold visited were encouraged to enrol in the study. Each Owusu et al. Malar J (2016) 15:38 Page 3 of 10 data collector was rigorously trained in questionnaire Entomological study administration and sample-taking. The questionnaires, The human landing catch method was used to catch which requested demographic information (e.g. sex, age mosquitoes each night for a total of 24 man nights, from and education), malaria prevention measures (ITN, coil two selected households at the beginning and end of and spray usage), exposure to mosquitoes (sleeping and each cluster area. This study was done in November– waking times), recent use of anti-malarials, as well as December, which is just after the September–October fever management practices, were pre-tested prior to minor rainy season.