Amhara, Ethiopia Woyneshet G
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Yalew et al. Malar J (2017) 16:242 DOI 10.1186/s12936-017-1884-y Malaria Journal RESEARCH Open Access Current and cumulative malaria infections in a setting embarking on elimination: Amhara, Ethiopia Woyneshet G. Yalew1, Sampa Pal2, Pooja Bansil2, Rebecca Dabbs3, Kevin Tetteh3, Caterina Guinovart2, Michael Kalnoky2, Belendia A. Serda2, Berhane H. Tesfay2, Belay B. Beyene1, Catherine Seneviratne2, Megan Littrell2, Lindsay Yokobe2, Gregory S. Noland4, Gonzalo J. Domingo2, Asefaw Getachew2, Chris Drakeley3 and Richard W. Steketee2* Abstract Background: Since 2005, Ethiopia has aggressively scaled up malaria prevention and case management. As a result, the number of malaria cases and deaths has signifcantly declined. In order to track progress towards the elimina- tion of malaria in Amhara Region, coverage of malaria control tools and current malaria transmission need to be documented. Methods: A cross-sectional household survey oversampling children under 5 years of age was conducted during the dry season in 2013. A bivalent rapid diagnostic test (RDT) detecting both Plasmodium falciparum and Plasmodium vivax and serology assays using merozoite antigens from both these species were used to assess the prevalence of malaria infections and exposure to malaria parasites in 16 woredas (districts) in Amhara Region. Results: 7878 participants were included, with a mean age of 16.8 years (range 0.5–102.8 years) and 42.0% being children under 5 years of age. The age-adjusted RDT-positivity for P. falciparum and P. vivax infection was 1.5 and 0.4%, respectively, of which 0.05% presented as co-infections. Overall age-adjusted seroprevalence was 30.0% for P. falciparum, 21.8% for P. vivax, and seroprevalence for any malaria species was 39.4%. The prevalence of RDT-positive infections varied by woreda, ranging from 0.0 to 8.3% and by altitude with rates of 3.2, 0.7, and 0.4% at under 2000, 2000–2500, and >2500 m, respectively. Serological analysis showed heterogeneity in transmission intensity by area and altitude and evidence for a change in the force of infection in the mid-2000s. Conclusions: Current and historic malaria transmission across Amhara Region show substantial variation by age and altitude with some settings showing very low or near-zero transmission. Plasmodium vivax infections appear to be lower but relatively more stable across geography and altitude, while P. falciparum is the dominant infection in the higher transmission, low-altitude areas. Age-dependent seroprevalence analyses indicates a drop in transmission occurred in the mid-2000s, coinciding with malaria control scale-up eforts. As malaria parasitaemia rates get very low with elimination eforts, serological evaluation may help track progress to elimination. Keywords: Malaria, Plasmodium falciparum, Plasmodium vivax, Seroconversion, Seroprevalence, Malaria transmission Background [1]. Malaria epidemiology in Ethiopia is relatively unique Malaria is a major public health challenge in Ethiopia, in Africa in that both Plasmodium falciparum and Plas- accounting for approximately 12 million cases each year modium vivax are present and malaria transmission is generally unstable, with focal, seasonal outbreaks and *Correspondence: [email protected] occasional epidemics [1]. 2 PATH, 2201 Westlake Avenue, Suite 200, Seattle, WA 98121, USA During the last decade, significant scale-up of inter- Full list of author information is available at the end of the article ventions—including population-wide distribution of © The Author(s) 2017. 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. Yalew et al. Malar J (2017) 16:242 Page 2 of 11 free, long-lasting insecticide-treated nets (LLINs), Methods indoor residual spraying (IRS), nationwide roll-out of Study area rapid diagnostic tests (RDTs) and artemisinin-based Tis study was conducted in Ethiopia’s Amhara Region, combination treatments—to reduce malaria transmis- which has a population of approximately 20 million peo- sion was implemented throughout the country [2]. ple. In 2012, the reported annual incidence of malaria This resulted in a significant reduction in the preva- in the Amhara Region was 60 cases per 1000 popula- lence of the malarial infection and illness and its con- tion, accounting for 19% of the national malaria burden sequences [3–6]. It is estimated that, if these activities [15, 16]. Te Amhara Region has signifcant variations are continued and sustained in the coming 5 years, 50 in altitude, temperature, and annual rainfall resulting in million malaria cases will be averted and $39 million in areas of difering malaria risk and transmission for both costs associated with patient care and treatment will P. falciparum and P. vivax. Malaria transmission is sea- be saved [7]. It is in this context that there is a renewed sonal, with the major malaria transmission season being commitment to advance toward malaria elimination in between September and December. For the purpose of Ethiopia. this study, woredas (districts) of Amhara were divided To facilitate malaria elimination in geographical areas into four eco-epidemiological zones (very low, very with historically low transmission [8], it is imperative to low to low, low, and low to moderate) based on weekly frst document the current levels of malaria transmission malaria incidence data from 2012. A total of 16 woredas and to provide the necessary evidence to extend efec- from these four unique eco-epidemiological zones were tive malaria elimination activities. Measuring malaria selected (Fig. 1a, b). transmission in low transmission areas is challenging, as microscopy and/or RDT results both underestimate Ethical considerations infections and typically present a narrow dynamic range Tis research protocol was reviewed and approved by of malaria prevalence estimates, which require large sam- ethical review committees at Amhara National Regional ple sizes [9–11]. While molecular diagnostic tests such as State (Amhara Research Ethics Review Committee), PCR are more sensitive and may capture a more accurate PATH, and Emory University. representation of infection prevalence, they are currently impractical in terms of complexity and cost, and in the Study design and data collection case of P. vivax, require a larger specimen volume [12, A cross-sectional household survey was conducted in 13]. Serological markers measuring cumulative exposure March–April 2013 during the dry, low-transmission can be a more practical and cost efective alternative, and season to provide estimates of malaria burden and cov- may provide improved discrimination of transmission erage of malaria control tools at woreda level in 16 tar- rates in the low to medium transmission areas by com- get woredas. Woreda-stratifed sampling was used to paring seroprevalence and seroconversion rates. A recent draw a sample from each woreda that was proportional study based on school surveys from the Oromia Regional to the woreda population. Within each woreda, enu- State of Ethiopia, demonstrate the value of serological meration areas (EAs) were selected with probability pro- marker-based indicators in low transmission areas (sero- portional to size. A total of 278 EAs were selected from prevalence of 0–12.7% for P. falciparum and 0–4.5% for P. woreda listings of all EAs developed by the Central Sta- vivax) [14]. tistical Agency for the 2007 census. In each selected EA, A collaborative efort between the Federal Ministry 25 households were selected using simple random sam- of Health and Amhara National Regional State Health pling from a sampling frame of all households created by Bureau (ANRSHB); the Malaria Control and Elimination EA mapping. EAs were mapped using personal digital Partnership in Africa (MACEPA), a programme at PATH; assistants (PDAs). Within each sampled household, all and Te Carter Center (TCC) was established to develop, children aged 6 months to 4 years old were eligible for implement, and evaluate a comprehensive malaria elimi- malaria testing. Household members over 5 years of age nation strategy in selected areas of Amhara Region, Ethi- were eligible in one out of every four households. Indi- opia. Before the implementation of activities, this study viduals were invited to participate and were included was conducted to estimate 2013 baseline rates of: (1) core after verbal informed consent was obtained. malaria interventions including LLIN ownership and use, A standardized questionnaire to collect information on and IRS coverage; and (2) current and cumulative malaria socio-demographic characteristics, knowledge and atti- infections due to P. falciparum and/or P. vivax using a tudes about malaria, and use of malaria control tools was population-based survey with malaria RDTs and malaria administered to each participant. Data were collected serology. using PDAs. Finger-prick blood samples were collected Yalew et al. Malar J (2017) 16:242 Page 3 of 11 Fig. 1 a Amhara Region, Ethiopia, b survey areas (woredas) selected for the Malaria Elimination, colour-coded light to dark from lowest to highest for altitude, c Plasmodium falciparum RDT prevalence, d Plasmodium vivax RDT prevalence, e Plasmodium falciparum seroprevalence, and f Plasmo- dium vivax seroprevalence Yalew et al. Malar J (2017) 16:242 Page 4 of 11 from consenting participants to perform an RDT (biva- and compared with a model with a single force of infec- lent SD Bioline Malaria Ag P.f./P.v. HRP-2/pLDH POCT) tion using log-likelihood tests [10]. and prepare dried blood spots (DBS) on flter paper. Par- Logistic regression was employed to determine the ticipants with a positive RDT result received antima- likelihood of being RDT-positive for P. vivax and/or P. larial treatment per national guidelines.