Estimating malaria transmission risk through surveillance of human-vector interactions in northern Ghana.

BACKGROUND: Vector bionomics are important aspects of vector-borne disease control programs. Mosquito-biting risks are affected by environmental, mosquito behavior and human factors, which are important for assessing exposure risk and intervention impacts. This study estimated malaria transmission risk based on vector-human interactions in northern Ghana, where indoor residual spraying (IRS) and insecticide-treated nets (ITNs) have been deployed. METHODS: Indoor and outdoor human biting rates (HBRs) were measured using monthly human landing catches (HLCs) from June 2017 to April 2019. Mosquitoes collected were identified to species level, and Anopheles gambiae sensu lato (An. gambiae s.l.) samples were examined for parity and infectivity. The HBRs were adjusted using mosquito parity and human behavioral observations. RESULTS: Anopheles gambiae was the main vector species in the IRS (81%) and control (83%) communities. Indoor and outdoor HBRs were similar in both the IRS intervention (10.6 vs. 11.3 bites per person per night [b/p/n]; z = -0.33, P = 0.745) and control communities (18.8 vs. 16.4 b/p/n; z = 1.57, P = 0.115). The mean proportion of parous An. gambiae s.l. was lower in IRS communities (44.6%) than in control communities (71.7%). After adjusting for human behavior observations and parity, the combined effect of IRS and ITN utilization (IRS: 37.8%; control: 57.3%) on reducing malaria transmission risk was 58% in IRS + ITN communities and 27% in control communities with ITNs alone (z = -4.07, P < 0.001). However, this also revealed that about 41% and 31% of outdoor adjusted bites in IRS and control communities respectively, occurred before bed time (10:00 pm). The mean directly measured annual entomologic inoculation rates (EIRs) during the study were 6.1 infective bites per person per year (ib/p/yr) for IRS communities and 16.3 ib/p/yr for control communities. After considering vector survival and observed human behavior, the estimated EIR for IRS communities was 1.8 ib/p/yr, which represents about a 70% overestimation of risk compared to the directly measured EIR; for control communities, it was 13.6 ib/p/yr (16% overestimation). CONCLUSION: Indoor residual spraying significantly impacted entomological indicators of malaria transmission. The results of this study indicate that vector bionomics alone do not provide an accurate assessment of malaria transmission exposure risk. By accounting for human behavior parameters, we found that high coverage of ITNs alone had less impact on malaria transmission indices than combining ITNs with IRS, likely due to observed low net use. Reinforcing effective communication for behavioral change in net use and IRS could further reduce malaria transmission.

Partial indoor residual spraying with pirimiphos-methyl as an effective and cost-saving measure for the control of Anopheles gambiae s.l. in northern Ghana.

The scale up of indoor residual spraying (IRS) and insecticide treated nets have contributed significantly to global reductions in malaria prevalence over the last two decades. However, widespread pyrethroid resistance has necessitated the use of new and more expensive insecticides for IRS. Partial IRS with pirimiphos-methyl in experimental huts and houses in a village-wide trial was evaluated against Anopheles gambiae s.l. in northern Ghana. Four different scenarios in which either only the top or bottom half of the walls of experimental huts were sprayed, with or without also spraying the ceiling were compared. Mortality of An. gambiae s.l. on partially sprayed walls was compared with the standard procedures in which all walls and ceiling surfaces are sprayed. A small-scale trial was then conducted to assess the effectiveness, feasibility, and cost of spraying only the upper walls and ceiling as compared to full IRS and no spraying in northern Ghana. Human landing catches were conducted to estimate entomological indices and determine the effectiveness of partial IRS. An established transmission dynamics model was parameterized by an analysis of the experimental hut data and used to predict the epidemiological impact and cost effectiveness of partial IRS for malaria control in northern Ghana. In the experimental huts, partial IRS of the top (IRR 0.89, p = 0.13) or bottom (IRR 0.90, p = 0.15) half of walls and the ceiling was not significantly less effective than full IRS in terms of mosquito mortality. In the village trial, the annual entomological inoculation rate was higher for the unsprayed control (217 infective bites/person/year (ib/p/yr)) compared with the fully and partially sprayed sites, with 28 and 38 ib/p/yr, respectively. The transmission model predicts that the efficacy of partial IRS against all-age prevalence of malaria after six months would be broadly equivalent to a full IRS campaign in which 40% reduction is expected relative to no spray campaign. At scale, partial IRS in northern Ghana would have resulted in a 33% cost savings ($496,426) that would enable spraying of 36,000 additional rooms. These findings suggest that partial IRS is an effective, feasible, and cost saving approach to IRS that could be adopted to sustain and expand implementation of this key malaria control intervention.

Identification of main malaria vectors and their insecticide resistance profile in internally displaced and indigenous communities in Eastern Democratic Republic of the Congo (DRC).

BACKGROUND: Malaria remains a major public health concern in the Democratic Republic of the Congo (DRC) and its control is affected by recurrent conflicts. Médecins Sans Frontières (MSF) initiated several studies to better understand the unprecedented incidence of malaria to effectively target and implement interventions in emergency settings. The current study evaluated the main vector species involved in malaria transmission and their resistance to insecticides, with the aim to propose the most effective tools and strategies for control of local malaria vectors. METHODS: This study was performed in 52 households in Shamwana (Katanga, 2014), 168 households in Baraka (South Kivu, 2015) and 269 households in Kashuga (North Kivu, 2017). Anopheles vectors were collected and subjected to standardized Word Health Organization (WHO) and Center for Disease Control (CDC) insecticide susceptibility bioassays. Mosquito species determination was done using PCR and Plasmodium falciparum infection in mosquitoes was assessed by ELISA targeting circumsporozoite protein. RESULTS: Of 3517 Anopheles spp. mosquitoes collected, Anopheles gambiae sensu lato (s.l.) (29.6%) and Anopheles funestus (69.1%) were the main malaria vectors. Plasmodium falciparum infection rates for An. gambiae s.l. were 1.0, 2.1 and 13.9% for Shamwana, Baraka and Kashuga, respectively. Anopheles funestus showed positivity rates of 1.6% in Shamwana and 4.4% in Baraka. No An. funestus were collected in Kashuga. Insecticide susceptibility tests showed resistance development towards pyrethroids in all locations. Exposure to bendiocarb, malathion and pirimiphos-methyl still resulted in high mosquito mortality. CONCLUSIONS: This is one of only few studies from these conflict areas in DRC to report insecticide resistance in local malaria vectors. The data suggest that current malaria prevention methods in these populations are only partially effective, and require additional tools and strategies. Importantly, the results triggered MSF to consider the selection of a new insecticide for indoor residual spraying (IRS) and a new long-lasting insecticide-treated net (LLIN). The reinforcement of correct usage of LLINs and the introduction of targeted larviciding were also included as additional vector control tools as a result of the studies.

Longitudinal estimation of Plasmodium falciparum prevalence in relation to malaria prevention measures in six sub-Saharan African countries.

BACKGROUND: Plasmodium falciparum prevalence (PfPR) is a widely used metric for assessing malaria transmission intensity. This study was carried out concurrently with the RTS,S/AS01 candidate malaria vaccine Phase III trial and estimated PfPR over ≤ 4 standardized cross-sectional surveys. METHODS: This epidemiology study (NCT01190202) was conducted in 8 sites from 6 countries (Burkina Faso, Gabon, Ghana, Kenya, Malawi, and Tanzania), between March 2011 and December 2013. Participants were enrolled in a 2:1:1 ratio according to age category: 6 months-4 years, 5-19 years, and ≥ 20 years, respectively, per year and per centre. All sites carried out surveys 1-3 while survey 4 was conducted only in 3 sites. Surveys were usually performed during the peak malaria parasite transmission season, in one home visit, when medical history and malaria risk factors/prevention measures were collected, and a blood sample taken for rapid diagnostic test, microscopy, and haemoglobin measurement. PfPR was estimated by site and age category. RESULTS: Overall, 6401 (survey 1), 6411 (survey 2), 6400 (survey 3), and 2399 (survey 4) individuals were included in the analyses. In the 6 months-4 years age group, the lowest prevalence (assessed using microscopy) was observed in 2 Tanzanian centres (4.6% for Korogwe and 9.95% for Bagamoyo) and Lambaréné, Gabon (6.0%), while the highest PfPR was recorded for Nanoro, Burkina Faso (52.5%). PfPR significantly decreased over the 3 years in Agogo (Ghana), Kombewa (Kenya), Lilongwe (Malawi), and Bagamoyo (Tanzania), and a trend for increased PfPR was observed over the 4 surveys for Kintampo, Ghana. Over the 4 surveys, for all sites, PfPR was predominantly higher in the 5-19 years group than in the other age categories. Occurrence of fever and anaemia was associated with high P. falciparum parasitaemia. Univariate analyses showed a significant association of anti-malarial treatment in 4 surveys (odds ratios [ORs]: 0.52, 0.52, 0.68, 0.41) and bed net use in 2 surveys (ORs: 0.63, 0.68, 1.03, 1.78) with lower risk of malaria infection. CONCLUSION: Local PfPR differed substantially between sites and age groups. In children 6 months-4 years old, a significant decrease in prevalence over the 3 years was observed in 4 out of the 8 study sites. Trial registration Clinical Trials.gov identifier: NCT01190202:NCT. GSK Study ID numbers: 114001.

Baseline malaria vector transmission dynamics in communities in Ahafo mining area in Ghana.

BACKGROUND: Malaria vector dynamics are relevant prior to commencement of mining activities. A baseline entomology survey was conducted in Asutifi and Tano (referred to as Ahafo) in the Brong-Ahafo geo-political region of Ghana during preparatory stages for mining by Newmont Ghana Gold Limited. METHODS: Between November 2006 and August 2007, eight Centre for Disease Control light traps were set daily (Monday-Friday) to collect mosquitoes. Traps were hanged in rooms that were selected from a pool of 1,100 randomly selected houses. Types of materials used in construction of houses were recorded and mosquito prevention measures were assessed from occupants. RESULTS: A total of 5,393 mosquitoes were caught that comprised Anopheles gambiae (64.8%), Anopheles funestus (4.2%), as well as Culicines, comprising of Culex (30.4%) and Aedes species (0.6%). The entomological inoculation rate in Asutifi (279 infective bites/person/month) and Tano (487 infective bites/person/month) demonstrate relatively high malaria transmission in Ahafo. The presence or absence of Anopheles vectors in rooms was influenced by the type of roofing material (OR 2.33, 95%CI: 1.29-4.22, p = 0.01) as well as the presence of eaves gaps (OR 1.80, 95%CI: 1.37-2.37, p < 0.01). It was also associated with bed net availability in the room (OR 1.39, 95%CI: 1.08-1.80, p = 0.01). Over 80% of the houses were roofed with corrugated zinc sheets. Over 60% of the houses in Ahafo had no eaves gaps to give access to mosquito entry and exit into rooms and mosquito bed net coverage was over 50%. Other measures used in preventing mosquito bites included; coil (22.1%), insecticide spray (9.4%), repellent cream (4.0%) and smoky fires (1.1%), contributed minimally to individual mosquito preventive measures in impact areas. Similarly, levels of protection; coil (16.9%), insecticide spray (2.8%) and repellent cream (0.3%) for the non-impact areas, depict low individual prevention measures. CONCLUSIONS: The survey identified areas where intensified vector control activities would be beneficial. It also demonstrates that transmission in Asutifi and Tano is high even before the commencement of mining operations. This study serves as baseline information to assess impact of mining activities in relation to future vector control interventions.

Trends in multiplicity of Plasmodium falciparum infections among asymptomatic residents in the middle belt of Ghana.

BACKGROUND: Malaria is the most important cause of mortality and morbidity in children living in the Kintampo districts in the middle part of Ghana. This study has investigated the multiplicity of infection (MOI) within asymptomatic residents of the Kintampo districts, and the influence of age and seasonality on MOI, by studying the distribution of the polymorphic Plasmodium falciparum antigen merozoite surface protein 2 (MSP2). METHODS: DNA was extracted from an asymptomatic cohort of children and adults infected with P. falciparum during the period November 2003 to October 2004. Polymerase chain reaction was carried out and multiplicity of infection (MOI) was determined. RESULTS: Children under 10 years of age had an average MOI of 2.3 while adults 18 years and above had an average MOI of 1.4. Children below five years had high and low average MOIs of 2.8 in the March/April survey and 0.9 in the May/June survey respectively. A similar trend in the monthly distribution of MOI was observed for the entire cohort. IC/3D7 strains outnumbered the FC27 strains throughout the year by a ratio of about 4:1 with the difference between the prevalence of the two strains being least marked in the March/April survey, at the beginning of the rainy season. MOI was not linked to the level of malaria transmission as measured by the entomological inoculation rate. DISCUSSION/CONCLUSION: The impact of interventions, introduced since this baseline study was carried out on the parasite diversity of asymptomatic residents will be the subject of further investigations.

Malaria epidemiology in the Ahafo area of Ghana.

BACKGROUND: Plasmodium falciparum malaria remains endemic in sub-Saharan Africa including Ghana. The epidemiology of malaria in special areas, such as mining areas needs to be monitored and controlled. Newmont Ghana Gold Limited is conducting mining activities in the Brong Ahafo Region of Ghana that may have an impact on the diseases such as malaria in the mining area. METHODS: Prior to the start of mining activities, a cross-sectional survey was conducted in 2006/2007 to determine malaria epidemiology, including malaria parasitaemia and anaemia among children < 5 years and monthly malaria transmission in a mining area of Ghana. RESULTS: A total of 1,671 households with a child less than five years were selected. About 50% of the household heads were males. The prevalence of any malaria parasitaemia was 22.8% (95% CI 20.8-24.9). Plasmodium falciparum represented 98.1% (95% CI 96.2-99.2) of parasitaemia. The geometric mean P. falciparum asexual parasite count was 1,602 (95% CI 1,140-2,252) and 1,195 (95% CI 985-1,449) among children < 24 months and ≥ 24 months respectively. Health insurance membership (OR 0.60, 95% CI 0.45-0.80, p = 0.001) and the least poor (OR 0.57, 95% CI 0.37-0.90, p = 0.001) were protected against malaria parasitaemia. The prevalence of anaemia was high among children < 24 months compared to children ≥ 24 months (44.1% (95% CI 40.0-48.3) and 23.8% (95% CI 21.2-26.5) respectively. About 69% (95% CI 66.3-70.9) of households own at least one ITN. The highest EIRs were record in May 2007 (669 ib/p/m) and June 2007 (826 ib/p/m). The EIR of Anopheles gambiae were generally higher than Anopheles funestus. CONCLUSION: The baseline malaria epidemiology suggests a high malaria transmission in the mining area prior to the start of mining activities. Efforts at controlling malaria in this mining area have been intensified but could be enhanced with increased resources and partnerships between the government and the private sector.

Patterns and seasonality of malaria transmission in the forest-savannah transitional zones of Ghana.

BACKGROUND: Knowledge of the local pattern of malaria transmission and the effect of season on transmission is essential for the planning and evaluation of malaria interventions. Therefore, entomological surveys were carried out in the forest-savannah transitional belt of Ghana (Kintampo) from November 2003 to November 2005 in preparation for drug and vaccine trials. RESULTS: A total of 23,406 mosquitoes were caught from 919 traps over the two-year period (November 2003 to November 2005): 54.3% were Culicines, 36.2% Anopheles funestus, and 9.4% Anopheles gambiae. Infection rates with Plasmodium falciparum were 4.7% and 1.5% for Anopheles gambiae and Anopheles funestus, respectively. Entomological inoculation rates (EIRs) were 269 infective bites per person per year in the first year (November 2003-October 2004) and 231 the following year (November 2004-November 2005). Polymerase Chain Reaction (PCR) analysis detected only Anopheles gambiae s.s. Nineteen mosquitoes were tested by PCR in the wet season; 16 were S-molecular form, 2 M-molecular form and 1 hybrid (S/M). In the dry season, sixteen mosquitoes were tested; 11 S-molecular form, 2 M-molecular form and 3 S/M hybrids. The frequency of knock down resistance (kdr) genotypes F(R) was 0.60. CONCLUSION: The dynamics and seasonal abundance of malaria vectors in the Kintampo area was influenced by micro-ecology, rainfall and temperature patterns. Transmission patterns did not differ significantly between the two years (2004 and 2005) and both Anopheles gambiae and Anopheles funestus were identified as effective vectors. EIR estimates in 2004/2005 were between 231 and 269 infective bites per person per year. The information provided by the study will help in planning intensified malaria control activities as well as evaluating the impact of malaria interventions in the middle belt of Ghana.

Epidemiology of malaria in the forest-savanna transitional zone of Ghana.

BACKGROUND: Information on the epidemiology of malaria is essential for designing and interpreting results of clinical trials of drugs, vaccines and other interventions. As a background to the establishment of a site for anti-malarial drugs and vaccine trials, the epidemiology of malaria in a rural site in central Ghana was investigated. METHODS: Active surveillance of clinical malaria was carried out in a cohort of children below five years of age (n = 335) and the prevalence of malaria was estimated in a cohort of subjects of all ages (n = 1484) over a 12-month period. Participants were sampled from clusters drawn around sixteen index houses randomly selected from a total of about 22,000 houses within the study area. The child cohort was visited thrice weekly to screen for any illness and a blood slide was taken if a child had a history of fever or a temperature greater than or equal to 37.5 degree Celsius. The all-age cohort was screened for malaria once every eight weeks over a 12-month period. Estimation of Entomological Inoculation Rate (EIR) and characterization of Anopheline malaria vectors in the study area were also carried out. RESULTS: The average parasite prevalence in the all age cohort was 58% (95% CI: 56.9, 59.4). In children below five years of age, the average prevalence was 64% (95% CI: 61.9, 66.0). Geometric mean parasite densities decreased significantly with increasing age. More than 50% of all children less than 10 years of age were anaemic. Children less than 5 years of age had as many as seven malaria attacks per child per year. The attack rates decreased significantly with increasing cut-offs of parasite density. The average Multiplicity of Infection (MOI) was of 6.1. All three pyrimethamine resistance mutant alleles of the Plasmodium falciparum dhfr gene were prevalent in this population and 25% of infections had a fourth mutant of pfdhps-A437G. The main vectors were Anopheles funestus and Anopheles gambiae and the EIR was 269 infective bites per person per year. CONCLUSION: The transmission of malaria in the forest-savanna region of central Ghana is high and perennial and this is an appropriate site for conducting clinical trials of anti-malarial drugs and vaccines.

Insecticide resistance profiles for malaria vectors in the Kassena-Nankana district of Ghana.

BACKGROUND: Malaria is a major public health problem in Ghana. The current strategy of the National Malaria Control Programme is based on effective case management and the use of insecticide treated bed nets among vulnerable groups such as children under-five years of age and pregnant women. Resistance to pyrethroids by Anopheles gambiae s.l. and Anopheles funestus has been reported in several African countries including neighbouring Burkina Faso. METHODS: Indoor resting Anopheles mosquitoes were collected. Blood-fed and gravid females were allowed to oviposit, eggs hatched and larvae reared to 1-3 days old adults and tested against permethrin 0.75%, deltamethrin 0.05%, cyfluthrin 0.15%, lambdacyhalothrin 0.1% and DDT 4%, based on WHO methodology. PCR analyses were carried out on a sub-sample of 192 of the An. gambiae for sibling species complex determination. Resistance to pyrethroids and DDT was determined by genotyping the knock-down resistance kdr gene mutations in the study area. RESULTS: A total of 9,749 1-3 days-old F1 female Anopheles mosquitoes were exposed to the insecticides. Among the pyrethroids, permethrin, 0.75% had the least knockdown effect, whilst cyfluthrin 0.15%, had the highest knock-down effect. Overall, no difference in susceptibility between An. gambiae 93.3% (95% CI: 92.5-94.1) and An. funestus 94.5% (95% CI: 93.7-95.3) was observed when exposed to the pyrethroids. Similarly, there was no difference in susceptibility between the two vector species (An. gambiae = 79.1% (95% CI: 76.6-81.8) and An. funestus = 83.5% (95% CI: 80.2-86.4) when exposed to DDT. Overall susceptibility to the insecticides was between 80% and 98%, suggesting that there is some level of resistance, except for cyfluthrin 0.15%. The kdr PCR assay however, did not reveal any kdr mutations. The analysis also revealed only the molecular M (Mopti) form. CONCLUSION: The findings in this study show that An. gambiae and An. funestus, the main malaria vector mosquitoes in the Kassena-Nankana district are susceptible to the insecticides being used in the treatment of bed nets in the malaria control programme. There is however, the need for continuous monitoring of the pyrethroids as the efficacy is not very high.