Steve W. Lindsay

Climate change and vector-borne diseases: a regional analysis

Current evidence suggests that inter-annual and inter-decadal climate variability have a direct influence on the epidemiology of vector-borne diseases. This evidence has been assessed at the continental level in order to determine the possible consequences of the expected future climate change. By 2100 it is estimated that average global temperatures will have risen by 1.0-3.5 degrees C, increasing the likelihood of many vector-borne diseases in new areas. The greatest effect of climate change on transmission is likely to be observed at the extremes of the range of temperatures at which transmission occurs. For many diseases these lie in the range 14-18 degrees C at the lower end and about 35-40 degrees C at the upper end. Malaria and dengue fever are among the most important vector-borne diseases in the tropics and subtropics; Lyme disease is the most common vector-borne disease in the USA and Europe. Encephalitis is also becoming a public health concern. Health risks due to climatic changes will differ between countries that have developed health infrastructures and those that do not. Human settlement patterns in the different regions will influence disease trends. While 70% of the population in South America is urbanized, the proportion in sub-Saharan Africa is less than 45%. Climatic anomalies associated with the El Niño-Southern Oscillation phenomenon and resulting in drought and floods are expected to increase in frequency and intensity. They have been linked to outbreaks of malaria in Africa, Asia and South America. Climate change has far-reaching consequences and touches on all life-support systems. It is therefore a factor that should be placed high among those that affect human health and survival.

Effect of pregnancy on exposure to malaria mosquitoes

Pregnant women attracted twice the number of Anopheles gambiae complex--the predominant African malaria-carrying mosquito--than did their non-pregnant counterparts. We postulate that physiological and behavioural changes that occur during pregnancy are responsible for increased attractiveness, which could be important in intervention strategies aimed at protecting this high-risk group against malaria.

Effect of fly control on trachoma and diar rhoea

BACKGROUND Domestic flies are accepted vectors of diarrhoea, but their role in trachoma transmission has never been quantified and no study has shown that fly control decreases the prevalence of trachoma. We assessed the effect of fly control on public health in a pilot study in Gambian villages. METHODS We studied two pairs of villages--one pair in the 1997 wet season, and one pair in the 1998 dry season. For each pair, deltamethrin was sprayed for 3 months to control flies in one village whilst the other was used as a control. Fly populations were monitored with traps. We surveyed trachoma at baseline and at 3 months, and collected daily data on diarrhoea in children aged between 3 months and 5 years. FINDINGS Fly control decreased numbers of muscid flies by around 75% in the intervention villages compared with controls. Trachoma prevalence was similar at baseline (wet season, prevalence in intervention village 8.8% vs control 12.2%; dry season, 18.0% vs 16.0%), but after 3 months of fly control there were 75% fewer new cases of trachoma in the intervention villages (wet season 3.7% vs 13.7%; dry season 10.0% vs 18.9%; rate ratio and relative risk of pooled data 0.25 [adjusted 95% CI 0.09-0.64], p=0.003). There was 22% less childhood diarrhoea in the wet season (14% vs 19%, period prevalence ratio 0.78 [0.64-0.95], p=0.01), and 26% less diarrhoea in the dry season (6% vs 8%; 0.74 [0.34-1.59], p=0.60) compared with controls. INTERPRETATION Muscid flies are important vectors of trachoma and childhood diarrhoea in The Gambia. Deltamethrin spray is effective for fly control and may be useful for reducing trachoma and diarrhoea in some situations, but further research on sustainable fly-control methods is needed.

Role of flies and provision of latrines in trachoma control : cluster-randomised controlled trial.

BACKGROUND Eye-seeking flies have received much attention as possible trachoma vectors, but this remains unproved. We aimed to assess the role of eye-seeking flies as vectors of trachoma and to test provision of simple pit latrines, without additional health education, as a sustainable method of fly control. METHODS In a community-based, cluster-randomised controlled trial, we recruited seven sets of three village clusters and randomly assigned them to either an intervention group that received regular insecticide spraying or provision of pit latrines (without additional health education) to each household, or to a control group with no intervention. Our primary outcomes were fly-eye contact and prevalence of active trachoma. Frequency of child fly-eye contact was monitored fortnightly. Whole communities were screened for clinical signs of trachoma at baseline and after 6 months. Analysis was per protocol. FINDINGS Of 7080 people recruited, 6087 (86%) were screened at follow-up. Baseline community prevalence of active trachoma was 6%. The number of Musca sorbens flies caught from childrens eyes was reduced by 88% (95% CI 64-100; p<0.0001) by insecticide spraying and by 30% (7-52; p=0.04) by latrine provision by comparison with controls. Analysis of age-standardised trachoma prevalence rates at the cluster level (n=14) showed that spraying was associated with a mean reduction in trachoma prevalence of 56% (19-93; p=0.01) and 30% with latrines (-81 to 22; p=0.210) by comparison with the mean rate change in the controls. INTERPRETATION Fly control with insecticide is effective at reducing the number of flies caught from childrens eyes and is associated with substantially lower trachoma prevalence compared with controls. Such a finding is consistent with flies being important vectors of trachoma. Since latrine provision without health education was associated with a significant reduction in fly-eye contact by M sorbens, studies of their effect when combined with other trachoma control measures are warranted.

Reducing malaria by mosquito-proofing houses

Sometimes, valuable lessons from history are forgotten, remain unknown, or worse, are ignored. This article reminds us of the pioneering work of Angelo Celli at the end of the 19th century, who demonstrated that people could be protected from malaria by screening their homes against mosquitoes. Since then, public health scientists have continued to show that simple changes in house design have the potential for protecting people against this life-threatening disease. Yet today, this type of intervention remains virtually ignored. The literature reviewed here demonstrates the enormous potential of these methods to reduce malaria, in the hope that it will stimulate scientific debate and further research.

Effect of two different house screening interventions on exposure to malaria vectors and on anaemia in children in The Gambia: a randomised controlled trial.

BACKGROUND House screening should protect people against malaria. We assessed whether two types of house screening--full screening of windows, doors, and closing eaves, or installation of screened ceilings--could reduce house entry of malaria vectors and frequency of anaemia in children in an area of seasonal malaria transmission. METHODS During 2006 and 2007, 500 occupied houses in and near Farafenni town in The Gambia, an area with low use of insecticide-treated bednets, were randomly assigned to receive full screening, screened ceilings, or no screening (control). Randomisation was done by computer-generated list, in permuted blocks of five houses in the ratio 2:2:1. Screening was not treated with insecticide. Exposure to mosquitoes indoors was assessed by fortnightly light trap collections during the transmission season. Primary endpoints included the number of female Anopheles gambiae sensu lato mosquitoes collected per trap per night. Secondary endpoints included frequency of anaemia (haemoglobin concentration <80 g/L) and parasitaemia at the end of the transmission season in children (aged 6 months to 10 years) who were living in the study houses. Analysis was by modified intention to treat (ITT), including all randomised houses for which there were some outcome data and all children from those houses who were sampled for haemoglobin and parasitaemia. This study is registered as an International Standard Randomised Controlled Trial, number ISRCTN51184253. FINDINGS 462 houses were included in the modified ITT analysis (full screening, n=188; screened ceilings, n=178; control, n=96). The mean number of A gambiae caught in houses without screening was 37.5 per trap per night (95% CI 31.6-43.3), compared with 15.2 (12.9-17.4) in houses with full screening (ratio of means 0.41, 95% CI 0.31-0.54; p<0.0001) and 19.1 (16.1-22.1) in houses with screened ceilings (ratio 0.53, 0.40-0.70; p<0.0001). 755 children completed the study, of whom 731 had complete clinical and covariate data and were used in the analysis of clinical outcomes. 30 (19%) of 158 children from control houses had anaemia, compared with 38 (12%) of 309 from houses with full screening (adjusted odds ratio [OR] 0.53, 95% CI 0.29-0.97; p=0.04), and 31 (12%) of 264 from houses with screened ceilings (OR 0.51, 0.27-0.96; p=0.04). Frequency of parasitaemia did not differ between intervention and control groups. INTERPRETATION House screening substantially reduced the number of mosquitoes inside houses and could contribute to prevention of anaemia in children. FUNDING Medical Research Council.

THE IMPORTANCE OF MOSQUITO BEHAVIOURAL ADAPTATIONS TO MALARIA CONTROL IN AFRICA

Over the past decade the use of long‐lasting insecticidal nets (LLINs), in combination with improved drug therapies, indoor residual spraying (IRS), and better health infrastructure, has helped reduce malaria in many African countries for the first time in a generation. However, insecticide resistance in the vector is an evolving threat to these gains. We review emerging and historical data on behavioral resistance in response to LLINs and IRS. Overall the current literature suggests behavioral and species changes may be emerging, but the data are sparse and, at times unconvincing. However, preliminary modeling has demonstrated that behavioral resistance could have significant impacts on the effectiveness of malaria control. We propose seven recommendations to improve understanding of resistance in malaria vectors. Determining the public health impact of physiological and behavioral insecticide resistance is an urgent priority if we are to maintain the significant gains made in reducing malaria morbidity and mortality.

Do untreated bednets protect against malaria

Bednets are thought to offer little, if any, protection against malaria, unless treated with insecticide. There is also concern that the use of untreated nets will cause people sleeping without nets to receive more mosquito bites, and thus increase the malaria risk for other community members. Regular retreatment of nets is therefore viewed as critical for malaria control. However, despite good uptake of nets, many control programmes in Africa have reported low re-treatment rates. We investigated whether untreated bednets had any protective benefit (in October and November 1996) in The Gambia where nets, although widely used, are mostly untreated. Cross-sectional prevalence surveys were carried out in 48 villages and the risk of malaria parasitaemia was compared in young children sleeping with or without nets. Use of an untreated bednet in good condition was associated with a significantly lower prevalence of Plasmodium falciparum infection (51% protection [95% CI 34-64%], P < 0.001). This finding was only partly explained by differences in wealth between households, and children in the poorest households benefited most from sleeping under an untreated net (62% protection [14-83%], P = 0.018). There was no evidence that mosquitoes were diverted to feed on children sleeping without nets. These findings suggest that an untreated net, provided it is in relatively good condition, can protect against malaria. Control programmes should target the poorest households as they may have the most to gain from using nets.

Spatial repellents: from discovery and development to evidence-based validation

International public health workers are challenged by a burden of arthropod-borne disease that remains elevated despite best efforts in control programmes. With this challenge comes the opportunity to develop novel vector control paradigms to guide product development and programme implementation. The role of vector behaviour modification in disease control was first highlighted several decades ago but has received limited attention within the public health community. This paper presents current evidence highlighting the value of sub-lethal agents, specifically spatial repellents, and their use in global health, and identifies the primary challenges towards establishing a clearly defined and recommended role for spatial repellent products in disease control.

Can source reduction of mosquito larval habitat reduce malaria transmission in Tigray, Ethiopia?

The development of irrigation schemes by dam construction has led to an increased risk of malaria in Tigray, Ethiopia. We carried out a pilot study near a microdam to assess whether environmental management could reduce malaria transmission by Anopheles arabiensis, the main vector in Ethiopia. The study took place in Deba village, close to a dam; Maisheru village, situated 3–4 km away from the dam, acted as a control. Baseline entomological and clinical data were collected in both villages during the first 12 months. Source reduction, involving filling, draining and shading of potential mosquito‐breeding habitats was carried out by the community of Deba in the second year and routine surveillance continued in both villages during the second year. Anopheles arabiensis was highly anthropophilic (Human Blood Index = 0.73), biting early in the night before people went to bed. The major breeding habitats associated with the dam were areas of seepage at the dam base (28%), leaking irrigation canals (16%), pools that formed along the bed of streams from the dam (13%), and man‐made pools (12%). In the pre‐intervention year, 5.9–7.2 times more adult vectors were found in the dam village compared with the control village. There was a 3.1% higher prevalence of an enlarged spleen in children under 10 years in the dam village than in the control village during the pre‐intervention period, but no statistically significant difference was found in the incidence of falciparum malaria between the two villages during the same period. Source reduction was associated with a 49% (95% CI = 46.6–50.0) relative reduction in An. arabiensis adults in the dam village compared with the pre‐intervention period. There were very few cases of malaria during the intervention period in both villages making it impossible to judge whether malaria incidence had been reduced. These preliminary findings suggest that in areas of low intensity transmission community‐led larval control may be a cheap and effective method of controlling malaria. Further, large‐scale studies are needed to confirm these findings.