How much does malaria vector control quality matter: The epidemiological impact of holed nets and inadequate indoor residual spraying

Background: Insecticide treated nets (ITN) and indoor residual spraying (IRS) are the two pillars of malaria vector control in Africa, but both interventions are beset by quality and coverage concerns. Data from three control programs were used to investigate the impact of: 1) the physical deterioration of ITNs, and 2) inadequate IRS spray coverage, on their respective protective effectiveness. Methods: Malaria indicator surveys were carried out in 2009 and 2010 in Bioko Island, mainland Equatorial Guinea and Malawi to monitor infection with P.falciparum in children, mosquito net use, net condition and spray status of houses. Nets were classified by their condition. The association between infection and quality and coverage of interventions was investigated. Results: There was reduced odds of infection with P.falciparum in children sleeping under ITNs that were intact (Odds ratio (OR): 0.65, 95% CI: 0.55-0.77 and OR: 0.81, 95% CI: 0.56-1.18 in Equatorial Guinea and in Malawi respectively), but the protective effect became less with increasingly worse condition of the net. There was evidence for a linear trend in infection per category increase in deterioration of nets. In Equatorial Guinea IRS offered protection to those in sprayed and unsprayed houses alike when neighbourhood spray coverage was high (≥80%) compared to those living in areas of low IRS coverage (<20%), regardless of whether the house they lived in was sprayed or not (adjusted OR = 0.54, 95% CI 0.33-0.89). ITNs provided only personal protection, offering no protection to non users. Although similar effects were seen in Malawi, the evidence was much weaker than in Equatorial Guinea. Conclusions: Universal coverage strategies should consider policies for repair and replacement of holed nets and promote the care of nets by their owners. IRS programs should ensure high spray coverage since inadequate coverage gives little or no protection at all. © 2011 Rehman et al. Bioko is the main island of Equatorial Guinea, situated approximately 30 miles off the coast of Cameroon, with a population of about 200,000. Malaria has historically been hyperendemic in Bioko with year round transmission. Annual entomological inoculation rates (EIR) of over 250 and 750 infectious bites per person per year by An.gambiae and An.funestus respectively were recorded before intensive malaria control was introduced [12]. The Bioko Island Malaria Control Project (BIMCP) was launched in 2004 in collaboration with the government of Equatorial Guinea. IRS was introduced in February 2004 using the pyrethroid deltamethrin (K-othrine WDG, Bayer Crop Science, Isando, South Africa), followed by biannual spraying with the carbamate bendiocarb (Ficam™, Bayer) from 2005. Strengthening of diagnosis through training in microscopy and the introduction of rapid diagnostic tests (RDT), the introduction and training of health facility staff in case management using Artemisinin Combination Therapy (ACT), expanding access to Intermittent Preventative Treatment for pregnant women (IPTp), and extensive information education and communication activities were started in 2005. Mass door-to-door distribution of the long lasting insecticidal net (LLIN) PermaNet 2.0 (Vestergaard Frandsen, Lausanne, Switzerland) was carried out in November and December 2007, supplying and assisting in hanging one net per sleeping area at an average of three nets per household. Entomological surveillance was carried out continuously and Malaria indicator surveys were undertaken annually in 18 sentinel areas to evaluate the impact of the control measures as reported previously [13], [14], [15]. The second five year phase of the BIMCP began in 2009. The study we are describing is based in part on data from the first two BIMCP annual surveys (of the second five year phase) which were carried out from August to September 2009 and 2010. One spray locality (areas used to carry out house spraying) was randomly selected with probability proportional to size in each sentinel area. A fixed number of houses (400 in each urban and 100 in each rural site) were selected by systematic sampling. Mainland Equatorial Guinea has a number of malaria vectors, which have been described in detail elsewhere [16]. The main vector is An.gambiae. The Equatorial Guinea Malaria Control Initiative (EGMCI), which is linked to the BIMCP, initiated malaria control measures in mainland Equatorial Guinea (EG) from 2007, similar to interventions carried out in Bioko, except that every province was designated to receive either IRS or LLINs by mass distribution. Centro Sur and Wele Nzas provinces received PermaNet 2.0 (Vestergaard Frandsen) LLINs in August to September 2007 and 2008 respectively. In Litoral province houses were sprayed semi-annually from August 2007 through September 2009 with the pyrethroid insecticide Alpha Cypermethrin (Fendona™, Avima/BASF, South Africa and HI Kara, India), in January 2010 with the carbamate insecticide bendiocarb (Ficam™, Bayer, South Africa), and from July 2010 with the pyrethroid insecticide deltamethrin (K-Orthrin™, Bayer, South Africa). In Kie Ntem province IRS was carried out semi-annually with Alpha Cypermethrin from July 2008, with Deltamethrin™ from January 2010 and with bendiocarb in July 2010. In addition, villages not covered by IRS in Litoral (seven in Mbini and 33 in Cogo) received LLINs in February 2009. Other malaria control measures were similar to those in Bioko. Programme monitoring and evaluation was also along the lines of that carried out on Bioko, including household MIS between April and June each year. In 2007 household listings were compiled in 17 sentinel sites from which households were randomly sampled each year for participation in the survey. We are using data from two MIS carried out in 2009 and 2010. Malaria is endemic in Malawi with the main transmission season between October and April. The predominant malaria vectors are An. arabiensis and An. funestus. The Malaria Decision Support System, as part of the Innovative Vector Control Consortium [17] (IVCC), conducted continuous entomological monitoring since 2007 and malaria indicator surveys in April 2009 and 2010 at 14 sentinel sites in Nkhota Khota district in Malawi. Vector control has primarily been via ITNs, with distribution campaigns in 2006 and 2008 to the most vulnerable groups. Continuous distribution of ITNs has been through antenatal clinics. In 2008, supported by the Presidents Malaria Initiative, annual IRS operations, with the pyrethroid lambda-cyhalothrin™ (ICON, Syngenta, Switzerland) began as a pilot of 25,000 households in Nkhota Khota district. In 2009 four sites (Makoka, Mazanduwa, Kalungama and Kamtekeke) received IRS and with the scale up of activities a fifth site (Ambali) was sprayed in 2009. Households for the MIS were selected from strata formed by dividing sentinel sites into quadrants from which households were systematically selected, to ensure the greatest geographical spread within the site. The data from the two household surveys were used in the study we are reporting. All data were collected using Personal Digital Assistants (PDA). Children less than 15 years of age were tested for P.falciparum using ICT™ Malaria Combo Cassette Test (ML02, R&R, Cape Town, South Africa) in Bioko, mainland Equatorial Guinea and in Malawi. Children under one year old were excluded from analysis a priori because maternal antibodies could provide protection against infection. Adherence to malaria control measures for each child were derived from the questionnaires; whether the child slept under an ITN the night before the survey; the condition of the net and whether the house in which the child lived had been sprayed during a reference period. Nets were classified into categories based on whether they were LLIN, treated or untreated nets, whether they were intact and if holed, the size of the largest hole to generate a net condition variable (see table 1 for details). Small holes were defined as being smaller than a D sized torch battery. Big holes were defined as at least one hole that could fit a D sized torch battery. Net condition was classified by the size of the largest hole only, not by the number of holes. In a small number of nets (2% of all nets, n = 204) the condition of the net was unknown. Using an untreated net with holes was included in the category of worst condition as there was no evidence of a statistical difference between this category and those not using a net (p>0.2). In Equatorial Guinea where malaria transmission is year round and spraying is carried out every six months, IRS coverage was assessed over the reference period of six months prior to the survey, whereas in Malawi where IRS is carried out annually, IRS coverage was assessed over the reference period of 12 months prior to the survey. Socio economic status (SES) was generated for each household using the first principal component score based on asset ownership and household characteristics [18], and converted to tertiles for analysis (See supporting information file S1 for further details). Logistic regression was used to estimates risk of malarial infection of an individual in relation to whether they had slept under a net the night before the survey (as a proxy measure for net use in general), the category of condition of the net, whether the house had been sprayed in the reference period, the spray coverage of the neighbourhood (site), net usage of the neighbourhood, SES tertile, and age group. Due to differences in transmission patterns, health service provision and vector ecology between Equatorial Guinea and Malawi, separate models were fitted for the two countries. In Equatorial Guinea an indicator was used to distinguish between Bioko Island and the mainland, and in Malawi an indicator was used to distinguish between lakeside and non lakeside sites. Standard errors were adjusted to account for the survey design [19]. The primary sampling unit (PSU) was set to be the sentinel site. All analyses were carried out in the STATA 11.1 software package [20]. The Equatorial Guinea continental region and Bioko studies were approved by the ethics committees of the Ministry of Health and Social Welfare in Equatorial Guinea and the London School of Hygiene and Tropical Medicine. The Malawi study was approved by the Malawi College of Medicine Ethics Committee (COMREC). The parents or caregivers of all children who participated in the surveys were asked for informed written consent. Respondents were informed of the purpose of the survey, the procedure for obtaining information and blood samples, the risks and benefits in participation, confidentiality of information collected, and their right to refuse. Individuals who tested positive for malarial parasites were referred to a local clinic for appropriate treatment according to national treatment policy. No individuals or communities were randomly allocated to different treatments.