BackgroundMalaria control interventions have been scaled-up in Zambia in conjunction with a malaria surveillance system. Although substantial progress has been achieved in reducing morbidity and mortality, national and local information demonstrated marked heterogeneity in the impact of malaria control across the country. This study reports the high burden of malaria in Nchelenge District, Luapula Province, Zambia from 2006 to 2012 after seven years of control measures.MethodsYearly aggregated information on cases of malaria, malaria deaths, use of malaria diagnostics, and malaria control interventions from 2006 to 2012 were obtained from the Nchelenge District Health Office. Trends in the number of malaria cases, methods of diagnosis, malaria positivity rate among pregnant women, and intervention coverage were analysed using descriptive statistics.ResultsMalaria prevalence remained high, increasing from 38% in 2006 to 53% in 2012. Increasing numbers of cases of severe malaria were reported until 2010. Intense seasonal malaria transmission was observed with seasonal declines in the number of cases between April and August, although malaria transmission continued throughout the year. Clinical diagnosis without accompanying confirmation declined from 95% in 2006 to 35% in 2012. Intervention coverage with long-lasting insecticide-treated nets and indoor residual spraying increased from 2006 to 2012.ConclusionsDespite high coverage with vector control interventions, the burden of malaria in Nchelenge District, Zambia remained high. The high parasite prevalence could accurately reflect the true burden, perhaps in part as a consequence of population movement, or improved access to care and case reporting. Quality information at fine spatial scales will be critical for targeting effective interventions and measurement of progress.

BackgroundDespite large reductions in malaria burden across Zambia, some regions continue to experience extremely high malaria transmission. In Nchelenge District, Luapula Province, northern Zambia, almost half the human population carries parasites. Intervention coverage has increased substantially over the past decade, but comprehensive district-wide entomological studies to guide delivery of vector control measures are lacking. This study describes the bionomics and spatio-temporal patterns of malaria vectors in Nchelenge over a two and a half year period, investigates what household factors are associated with high vector densities and determines why vector control may not have been effective in the past to better guide future control efforts.MethodsBetween April 2012 and September 2014, twenty-seven households from across Nchelenge District were randomly selected for monthly light trap collections of mosquitoes. Anopheline mosquitoes were identified morphologically and molecularly to species. Foraging rates were estimated and sporozoite rates were determined by circumsporozoite ELISAs to calculate annual entomological inoculation rates. Blood feeding rates and host preference were determined by PCR. Zero-inflated negative binomial models measured environmental and household factors associated with mosquito abundance at study households such as season, proximity to the lake, and use of vector control measures.ResultsThe dominant species in Nchelenge was An. funestus (s.s.) with An. gambiae (s.s.) as a secondary vector. Both vectors were found together in large numbers across the district and the combined EIRs of the two vectors exceeded 80 infectious bites per person per annum. An. funestus household densities increased in the dry season whilst An. gambiae surged during the rains. Presence of insecticide treated nets (ITNs) and closed eaves in the houses were found to be associated with fewer numbers of An. gambiae but not An. funestus. There was no association with indoor residual spraying (IRS).ConclusionIn Nchelenge, the co-existence of two highly anthropophagic vectors, present throughout the year, is likely to be driving the high malaria transmission evident in the district. The vectors here have been shown to be highly resistant to pyrethroids used for IRS during the study. Vector control interventions in this area would have to be multifaceted and district-wide for effective control of malaria.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1786-9) contains supplementary material, which is available to authorized users.

BackgroundThe scale-up of malaria control interventions has resulted in substantial declines in transmission in some but not all regions of sub-Saharan Africa. Understanding factors associated with persistent malaria transmission despite control efforts may guide targeted interventions to high-risk areas and populations.MethodsHousehold malaria surveys were conducted in Nchelenge District, Luapula Province, in northern Zambia. Structures that appeared to be households were enumerated from a high-resolution satellite image and randomly sampled for enrollment. Households were enrolled into cross-sectional (single visit) or longitudinal (visits every other month) cohorts but analyses were restricted to cross-sectional visits and the first visit to longitudinal households. During study visits, a questionnaire was administered to adults and caretakers of children and a blood sample was collected for a malaria rapid diagnostic test (RDT) from all household residents. Characteristics associated with RDT positivity were analyzed using multi-level models.ResultsA total of 2,486 individuals residing within 742 households were enrolled between April 2012 and July 2015. Over this period, 51% of participants were RDT positive. Forty-three percent of all RDT positive individuals were between the ages of 5 and 17 years although this age group comprised only 30% of study participants. In a multivariable model, the odds being RDT positive were highest in 5–17 year olds and did not vary by season. Children 5–17 years of age had 8.83 higher odds of being RDT positive compared with those >18 years of age (95% CI: 6.13, 12.71); there was an interaction between age and report of symptoms, with an almost 50% increased odds of report of symptoms with decreasing age category (OR = 1.49; 95% CI 1.11, 2.00).ConclusionsChildren and adolescents between the ages of 5 and 17 were at the highest risk of malaria infection throughout the year. School-based programs may be effective at targeting this high-risk group.

Malaria transmission in northern Zambia has increased in the past decade, despite malaria control activities. Evidence-based intervention strategies are needed to effectively reduce malaria transmission. Zambia’s National Malaria Control Centre conducted targeted indoor residual spraying (IRS) in Nchelenge District, Luapula Province, from 2014 to 2016 using the organophosphate insecticide pirimiphos-methyl. An evaluation of the IRS campaign was conducted by the Southern Africa International Centers of Excellence for Malaria Research using actively detected malaria cases in bimonthly household surveys carried out from April 2012 to July 2017. Changes in malaria parasite prevalence after IRS were assessed by season using Poisson regression models with robust standard errors, controlling for clustering of participants in households and demographic, geographical, and climatological covariates. In targeted areas, parasite prevalence declined approximately 25% during the rainy season following IRS with pirimiphos-methyl but did not decline during the dry season or in the overall study area. Within targeted areas, parasite prevalence declined in unsprayed households, suggesting both direct and indirect effects of IRS. The moderate decrease in parasite prevalence within sprayed areas indicates that IRS with pirimiphos-methyl is an effective malaria control measure, but a more comprehensive package of interventions is needed to effectively reduce the malaria burden in this setting.

Abstract. Nchelenge District in Luapula Province, northern Zambia, experiences holoendemic malaria despite implementation of vector control programs. The major Anopheles vectors that contribute to Plasmodium falciparum transmission in this area had not previously been well defined. Three collections performed during the 2012 wet and dry seasons and the 2013 wet season revealed Anopheles funestus sensu stricto and Anopheles gambiae sensu stricto as the main vectors, where 80-85% of each collection was composed of An. funestus. Both vectors were found to be highly anthropophilic, and An. funestus has higher sporozoite infection rates (SIRs) and entomological inoculation rates (EIRs) year-round compared with An. gambiae: SIRs of 1.8-3.0% and 0-2.5%, respectively, and EIRs of 3.7-41.5 infectious bites per 6-month period (ib/p/6mo) and 0-5.9 ib/p/6mo, respectively. Spatial and temporal changes in each vector's dynamics and bionomics were also observed. Anopheles funestus was the predominant vector in the villages near Kenani Stream in both wet and dry seasons, whereas An. gambiae was found to be the main vector in areas near Lake Mweru during the wet season. The vector data illustrate the need for broader temporal and spatial sampling in Nchelenge and present unique opportunities to further our understanding of malarial transmission and implications for malarial control in high-risk areas.

BackgroundTwo mitochondrial DNA clades have been described in Anopheles funestus populations from southern Africa. Clade I is common across the continent while clade II is known only from Mozambique and Madagascar. The specific biological status of these clades is at present unknown. We investigated the possible role that each clade might play in the transmission of Plasmodium falciparum and the insecticide resistance status of An. funestus from Zimbabwe and Zambia.MethodsMosquitoes were collected inside houses from Nchelenge District, Zambia and Honde Valley, Zimbabwe in 2013 and 2014. WHO susceptibility tests, synergist assays and resistance intensity tests were conducted on wild females and progeny of wild females. ELISA was used to detect Plasmodium falciparum circumsporozoite protein. Specimens were identified to species and mtDNA clades using standard molecular methods.ResultsThe Zimbabwean samples were all clade I while the Zambian population comprised 80% clade I and 20% clade II in both years of collection. ELISA tests gave an overall infection rate of 2.3% and 2.1% in 2013, and 3.5% and 9.2% in 2014 for Zimbabwe and Zambia respectively. No significant difference was observed between the clades. All populations were resistant to pyrethroids and carbamates but susceptible to organochlorines and organophosphates. Synergist assays indicated that pyrethroid resistance is mediated by cytochrome P450 mono-oxygenases. Resistance intensity tests showed high survival rates after 8-hrs continuous exposure to pyrethroids but exposure to bendiocarb gave the same results as the susceptible control.ConclusionsThis is the first record of An. funestus mtDNA clade II occurring in Zambia. No evidence was found to suggest that the clades are markers of biologically separate populations. The ability of An. funestus to withstand prolonged exposure to pyrethroids has serious implications for the use of these insecticides, either through LLINs or IRS, in southern Africa in general and resistance management strategies should be urgently implemented.

This is the first record of An. funestus mtDNA clade II occurring in Zambia. No evidence was found to suggest that the clades are markers of biologically separate populations. The ability of An. funestus to withstand prolonged exposure to pyrethroids has serious implications for the use of these insecticides, either through LLINs or IRS, in southern Africa in general and resistance management strategies should be urgently implemented.

BackgroundInsecticide use via indoor residual spraying (IRS) or treated nets is the primary method for controlling malaria vector populations. The incidence of insecticide resistance in vector populations is burgeoning globally making resistance management key to the design of effective malaria control and elimination strategies. Vector populations can be assessed for insecticide resistance using a binary (susceptible or resistant) classification based on the use of the standard WHO insecticide susceptibility assay for adult anopheline mosquitoes. However, the recent scaling up of vector control activities has necessitated a revision of the WHO bioassay protocol to include the production of information that not only diagnoses resistance but also gives information on the intensity of expression of resistance phenotypes detected. This revised protocol is expected to inform on the range of resistance phenotypes in a target vector population using discriminating/diagnostic insecticide concentrations (DC) as well as their potential operational significance using 5× DC and 10× DC assays. The aim of this project was to use the revised protocol to assess the intensity of pyrethroid resistance in a range of insecticide resistant Anopheles strains with known resistance mechanisms and for which there is evidence of operational significance in the field setting from which these colonies were derived.MethodsDiagnostic concentration (DC) bioassays followed by 5× DC and 10× DC assays using the pyrethroid insecticides permethrin and deltamethrin were conducted according to the standard WHO bioassay method against pyrethroid resistant laboratory strains of Anopheles funestus, An. arabiensis and An. gambiae.ResultsLow to moderate resistance intensities were recorded for the An. arabiensis and An. gambiae strains while moderate to high intensities were recorded for the An. funestus strains.ConclusionsIt is evident that resistance intensity assays can add predictive value to the decision making process in vector control settings, although more so in an IRS setting and especially when bench-marked against resistance phenotypes of known operational significance.