Is staying overnight in a farming hut a risk factor for malaria infection in a setting with insecticide-treated bed nets in rural Laos?

Laos is located in Southeast Asia, where malaria transmission is intensive in and on the fringes of forests [1]. With 70% of the population at risk, malaria is the leading cause of morbidity and mortality in the country [2]. Most of the population lives in rural areas and 84% of the households are engaged in rice farming [3]. The National Malaria Control Programme has emphasized the promotion of insecticide-treated bed nets (ITNs), early diagnosis, and prompt treatment as the principal malaria control strategies [4].

During the rice farming season, farmers and their family members often move from their village to a farm, where they stay in a temporary shelter (farming hut). Likewise, in Thailand, movements entailing overnight stays on farms occur throughout the year for rice cultivation, and peaked between June and September [5]. A study in Tanzania showed that most of the studied population stayed overnight in huts for weeding in February and harvesting rice in May [6].

These seasonal movements in relation to agricultural activities have been identified as risk factors associated with malaria infection [5, 7‐11]. In Thailand, the relative risk of infection for people who slept in farm huts was three times higher than that of people staying in residential villages [5]. In Vietnam, farmers who regularly slept in plot huts in the forest were approximately three times more likely to be infected with malaria than those involved in other work [7].

Two environmental factors for higher risk of malaria infection have been identified among those who stayed overnight in farm huts. First, malaria transmission is more intense in the farm huts than in the village settlements. Second, farm huts are poorly constructed with fewer barriers against mosquitoes [5]. In addition to these environmental factors, social factors were also noted. A shortage of nets leads people to keep their valued nets in their village houses, which are more secure and it may be cumbersome for people to carry and set up their nets in their farm huts [12].

Recently, the Global Fund to Fight AIDS, Tuberculosis and Malaria and other global efforts rapidly increased the coverage of ITNs in many malaria endemic countries. In Laos, ITN coverage reached 77.5% of the target population in 2003 [13]. Furthermore, 1,672,500 ITNs, including long-lasting ITNs, were distributed amongst the population of five million between 2004 and 2007 [14]. With the assumption that two people use a net together, this covered 67% of the total population.

Although the coverage has been increased in many countries, few studies have documented the association between malaria infection risk and overnight stay in a farming hut in a setting of high ITN coverage. Most of the previous studies about overnight stay provided little information on whether ITNs or any nets were used among their target populations [5, 7‐9], and others were conducted in the settings where no use or use of untreated bed nets was more common than use of ITNs [10, 11]. Thus, this study sought to assess whether staying overnight in a farming hut is associated with malaria infection among farmers and their family members in a rural district of Laos.

The primary finding was that overnight stays in farming huts was not associated with the risk of malaria infection in either the dry or rainy seasons in the study site in Laos, where ITNs were widely used both in permanent residences and farming huts.

This finding suggests that previously reported associations might be due partly to insufficient coverage or improper use of ITNs in the farming huts. This finding was in line with that of the Tanzania study that reported no association between overnight stays in the farming huts and incidence of febrile illness episodes in the malaria endemic area of the country [6]. In that study, 97.9% of the people who stayed overnight in farming huts reported that they used a bed net and nearly 60% of the nets were ITNs.

The finding is important not only because overnight stays in farming huts are reported in malaria endemic countries other than Laos, but because overnight stays in farming huts are not confined to adult population. As shown both in the present study and by Hetzel et al[6], children under five years of age, those most vulnerable to malaria infection, were taken to the farming huts by their parents. Although the coverage of ITNs is high in Laos, it remains low in many malaria endemic countries [13]. Efforts should be made to increase ITN coverage to protect this vulnerable group.

The second important finding was that using one family type net with five or more people significantly increased the odds of malaria infection risk. In the study site, almost all the nets were family type, which are usually designed to cover up to three adult people. Thus, sharing one family type net with five or more people quite obviously exceeds its capacity. The finding is in line with a study from Vietnam that reported that people sharing one net with four to six people were more likely to have malaria than those who shared with up to three people [19]. However, their results were not adjusted for potential confounding variables. Results of the present study showed that the association was found even after adjustment for age, the number of household members, and insecticide-treatment status.

The importance of health education regarding the proper use of nets has been recognized in malaria control [20, 21]. However, such education does not necessarily cover how many people can share a net [22, 23]. Additionally, Roll Back Malaria indicators, which are often used to assess progresses of malaria control efforts, focus only on whether people sleep under a net or not and pay little attention to proper net use [24]. Thus, this study suggests that number of people sharing one net should be emphasized in health education and be included as an indicator to assess the proper use of nets.

An interesting finding was that although the association between the number of people sharing the same family type net and malaria infection was statistically significant in the March survey, no association was found in the August survey. This difference might be related to the decreased repellent effects of ITNs. In the study site, the National Malaria Control Programme annually provides net treatment around April, and people have little chance to treat their nets with insecticide except the programme-led treatment exercise. Although the repellent effect on mosquitoes is strongest soon after treatment, the effect gradually decreases as time passes [25]. Thus, the reason for the lack of association in the August survey might be due to the effects from insecticide remaining on the nets. Alternatively, the finding could be due to the results of increased number of ITNs and its use. In the August survey, ITNs accounted for 93.6% of the total nets, while 83.5% in the March survey.

The results suggest that people who practice seasonal movements may need a greater number of nets than those who do not. In March, 25.7% of the total bed nets were placed in the farming huts even though the study respondents reported that they rarely stayed at the huts overnight. There were two possible reasons for this: first, the nets may be used for nuisance protection during the day, as was reported in a number of studies [26, 27]; second, the difficulty involved with frequently carrying a net between the main residences and farming huts [12]. Programme planners need to take the extra nets used in farming huts into account when they decide how many nets are required for distribution.

In this study, blood examinations were performed with Paracheck, which is based on the detection of histidine-rich protein-2 produced by falciparum parasites. Because this protein can remain in blood for several weeks even after successful treatment, some of the study participants who tested positive might not have had parasitaemia (false-positive). However, it is unlikely that many of them resulted from false-positives; studies that assessed the performance of Paracheck among asymptomatic population in Asian settings showed that sensitivity, specificity, positive predictive value, and negative predictive value were 92.3%, 97.2%, 83.7%, and 98.8% in Thailand (prevalence: 15.0%), and 94.4%, 89.0%, 70.3%, and 98.3% in India (prevalence: 24.4%), respectively [28, 29].

This study asked people's behaviors regarding overnight stay in farming huts in the past two weeks. The use of the two weeks duration is reasonable to minimize the potential recall bias associated with self-report, but may not be enough to assess an association between sleeping in farming hut and malaria infection, particularly when the extended period of persistence of histidine-rich protein-2 is considered. However, it is likely that the study population who frequently slept in farming huts for the past two weeks were more likely to choose to sleep in farming huts around the survey period, compared to those who never slept in farming huts.

In this study there were five major limitations. First, nearly 30% of the people did not participate in blood examinations. Logistic regression analysis was conducted using data from those who participated. Thus, results are not free from selection bias. Those who did not participate in blood examinations were more likely to sleep in huts for five days or more compared to those who participated in March (10.7% vs. 5.9%) and in August (52.1% vs. 48.7%). It suggests that one reason for non-participation might be due to people working in the farms and that the association between malaria infection and frequency of overnight stays might be underestimated. In a future study, performing blood examinations at the time of interview is recommended to avoid potential loss due to non-response. Second, because any entomological surveys were not conducted, it is unclear how intensive transmissions were in permanent residences and farming huts. Third, because the data collection was limited to only one health zone in the district, the samples of this study might not reflect the entire population of the district. However, as other health zones have the similar ecological setting and the same ethnic group (Lao Thueng), differences in malaria epidemiology and people's behaviors seem to be small. Fourth, the association might be somewhat underestimated in case sleeping in farming huts was associated with low-level parasitaemia. Finally, although the estimated minimum sample size was multiplied by 1.5, the increase might be insufficient to fully address the design effect of the sampling strategies used in this study. The estimated sample size should have been multiplied with consideration to design effect related to cluster surveys.

This study showed that staying overnight in farming huts was not associated with an increased risk of malaria infection in the setting where ITNs were widely used in farming huts. It suggests that malaria infection during overnight stays in farming huts might be preventable if ITNs are properly used in rural Laos.