Microbial larvicide application by a large-scale, community-based program reduces malaria infection prevalence in urban Dar es Salaam, Tanzania

Abstract

Background: Malaria control in Africa is most tractable in urban settlements yet most research has focused on rural settings. Elimination of malaria transmission from urban areas may require larval control strategies that complement adult mosquito control using insecticide-treated nets or houses, particularly where vectors feed outdoors.

Methods and findings: Microbial larvicide (Bacillus thuringiensis var. israelensis (Bti)) was applied weekly through programmatic, non-randomized community-based, but vertically managed, delivery systems in urban Dar es Salaam, Tanzania. Continuous, randomized cluster sampling of malaria infection prevalence and non-random programmatic surveillance of entomological inoculation rate (EIR) respectively constituted the primary and secondary outcomes surveyed within a population of approximately 612,000 residents in 15 fully urban wards covering 55 km(2). Bti application for one year in 3 of those wards (17 km(2) with 128,000 residents) reduced crude annual transmission estimates (Relative EIR [95% Confidence Interval] = 0.683 [0.491-0.952], P = 0.024) but program effectiveness peaked between July and September (Relative EIR [CI] = 0.354 [0.193 to 0.650], P = 0.001) when 45% (9/20) of directly observed transmission events occurred. Larviciding reduced malaria infection risk among children < or =5 years of age (OR [CI] = 0.284 [0.101 to 0.801], P = 0.017) and provided protection at least as good as personal use of an insecticide treated net (OR [CI] = 0.764 [0.614-0.951], P = 0.016).

Conclusions: In this context, larviciding reduced malaria prevalence and complemented existing protection provided by insecticide-treated nets. Larviciding may represent a useful option for integrated vector management in Africa, particularly in its rapidly growing urban centres.

Figure 1. A map of the study area in central Dar es Salaam, Tanzania.

Wards included in the study area of the Dar es Salaam Urban Malaria Control Program (UMCP) are outlined, specifying those targeted for larviciding from March 2006 onwards (intervention) and those which did receive any larviciding over the course of the study (non-intervention wards).

Figure 2. Schematic representation of the timeline of activities described in this study.

The study is divided into years of programmatic activity as follows: Year 1: April 2004 till March 2005 was the first year, during which household surveys were initiated and systems for mapping and monitoring larval habitats were developed , . Year 2 spans the period April 2005 to March 2006 and was also defined as a pre-intervention year because no larviciding was implemented. In year 2 household surveys were complemented with entomological baseline data (larval and adult surveys) allowing subsequent rational implementation and evaluation of larviciding. Year 3 is the subsequent intervention year during which systematic larviciding was introduced to the three selected wards and spanned the period of April 2006 to March 2007.

Figure 3. Study area, population, experimental design and sample sizes.

Figure 4. Longitudinal trends in overall malaria prevalence and its environmental determinants in Dar es Salaam, Tanzania.

Monthly variations in rainfall, temperature (A), mosquito biting densities (B–E) and malaria prevalence (F) in the intervention and non-intervention areas over the first three years of the urban malaria control program (UMCP). Climatic and prevalence data was available from May 2004 till March 2007 whereas mosquito data was only collected from April 2005 till March 2007. Meteorological data was derived from meteorological station at Nyerere International Airport and assumed representative of both intervention and non-intervention areas.

Figure 5. Seasonal patterns of malaria transmission in Dar es Salaam, Tanzania.

Seasonal patterns of rainfall and temperature (A), seasonal distribution of mosquito biting densities (B–D) and sporozoite-infected mosquitoes in the non-intervention areas (G), as well as relative biting rates in the pre-intervention and the intervention year (E, F). Relative biting densities were aggregated over pre-intervention year 2 (E: April 2004 till March 2005) and intervention year 3 (F: April 2005 till March 2006)) while direct observations of transmission in the non-intervention areas (G) were summed over both years to consolidate the limited numbers of observations in a qualitatively useful manner.

Figure 6. Crude prevalence of malaria infection amongst children of five years or less in intervention and non-intervention wards over each year of the study.

Error bars represent 95% confidence intervals with the significance of the differences between intervention and non-intervention wards estimated by χ² analysis (n = 1908, 1983 and 1910 for non-intervention and 414, 456 and 456 for intervention wards in years 1, 2 and 3, respectively).