PLoS Neglected Tropical Diseases
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Source reduction with a purpose: Mosquito ecology and community perspectives offer insights for improving household mosquito management in coastal Kenya
DOI 10.1371/journal.pntd.0008239, Volume: 14, Issue: 5,

Table of Contents

Highlights

Notes

Abstract

Because Ae. aegypti mosquitoes bite during the day, bednets are not protective. Moreover, Ae. aegypti mosquitoes are ‘anthropophilic container breeders’ primarily breeding in containers outside people’s homes. Therefore, vector control efforts that reduce the abundance of containers and other potential mosquito breeding habitats should be prioritized. This research aimed to identify productive Ae. aegypti mosquito breeding habitats in coastal Kenya and to understand household mosquito management behaviors and their behavioral determinants. We found that more than half of all immature mosquitoes were in containers with no intended purpose that had unintentionally filled with rainwater. Residents had limited awareness of day-time biting, container-breeding, Aedes mosquitoes. Consequently, households prioritized sleeping under bednets as a primary protection against mosquito-borne disease. Our findings inform the design of vector control efforts; encouraging community trash clean-up events and targeting the reduction or re-use of unused containers.

Forsyth, Mutuku, Kibe, Mwashee, Bongo, Egemba, Ardoin, LaBeaud, and Barrera: Source reduction with a purpose: Mosquito ecology and community perspectives offer insights for improving household mosquito management in coastal Kenya

Introduction

Emerging arthropod-borne viruses (arboviruses), which are spread by the Aedes aegypti mosquito, pose a substantial threat to global public health [1]. Unlike the night-time biting Anopheles mosquito that transmits malaria, Ae. aegypti bites during the day and transmits multiple arboviruses, including dengue, chikungunya, Zika, and yellow fever viruses. Individuals with these diseases can range from being asymptomatic to suffering from life-threatening encephalitis and hemorrhage, or debilitating arthritis that can persist for years [2]. Arboviral disease outbreaks have been unpredictable and increasing in frequency over the past two decades [3]. Kenya and other African countries have experienced a number of outbreaks in the past 5 years, despite little attention to the issue from government and community organizations [4]. In this context, outbreaks are often underreported and infections misdiagnosed as malaria [57].

Since there is no antiviral therapy and bednets are not protective against the day-time biting Ae. aegypti mosquitoes, it is imperative to focus vector control efforts on reducing the number of available Ae. aegypti breeding sites (source reduction). Individuals in the community play a crucial role in control efforts because Ae. aegypti mosquitoes are ‘anthropophilic container breeders’ primarily breeding in outdoor water containers such as buckets located immediately outside people’s homes [8]. In Kenya, adult Ae. aegypti mosquitoes have been found to bite during circumscribed times of the day [9].

Source reduction may include tasks like covering containers, discarding containers, or cleaning outdoor environments. These behaviors can be numerous, complex, and difficult to perform, let alone sustain, by household members [10, 11]. Despite these challenges, community-based interventions promoting source reduction have effectively reduced mosquito indices in other countries by engaging women, who are often involved with water-related activities like fetching and storage [12], and children, who may be willing to engage with new ideas, more flexible in taking up behaviors early in life, and acting as agents of change in communities [13]. Studies in South America and Asia have demonstrated reductions in mosquito indices from women and children’s involvement in comprehensive source reduction of all potential mosquito habitats as well as targeted source reduction of containers previously identified as having the highest mosquito larval and pupal densities [11, 12].

The objectives of this study conducted in ten villages in Kwale County, coastal Kenya, were to identify productive mosquito breeding habitats outside homes and explore household mosquito management behaviors and their behavioral determinants among female caregivers and children. Together, this information could be used to develop community-based source reduction interventions that aim to target the most productive container habitats.

Methods

Study sites

This study was conducted in coastal rural villages near the town of Msambweni in Kwale County, Kenya, located approximately 60 kilometers south of Mombasa and 50 kilometers north of the Kenya-Tanzania border (4°28′0.0114″S, 39°28′0.12″E).

The annual mean temperatures range from 23–34°C with average relative humidity between 60–80%. Precipitation varies throughout the year: February is the driest month, with an average of 18 mm of rain, and May is the wettest with an average of 347 mm. The seasons are classified based on precipitation levels with the long dry season between January-March, the long rainy season between April-June, the short dry season between July-September, and the short rainy season between October-December. With low population densities of 460 people/km2 , central water systems transporting piped water to households are lacking. As a result, residents obtain water for domestic purposes from rainfall in the wet months and wells and boreholes in the dry months. Fishing and subsistence farming are the primary livelihoods among residents. Islam is the dominant religion. [8, 14]

Entomological surveys

We aimed to conduct entomological surveys in 500 households to understand container productivity profiles. We conducted these surveys primarily during the short rainy season between September and December 2016. Fifty houses with children in grades 5 and 6 (approximately ages 11 to 16) were randomly selected from 10 different primary school rosters. Outside each house, all potential larval habitats in the outdoor domestic environment of every house were inspected for mosquito larvae and pupae. We excluded the indoor environment because a prior study conducted by our team in the same region indicated that indoor habitats accounted for only 5.2% of the positive containers and were therefore deemed a lower priority than outdoor containers [8]. The larval habitats were classified into different habitat types (as described by [8]. All pupae and a sample of larvae (3rd and 4th instars) from positive larval habitats were collected with the aid of pipettes and ladles [15], counted and recorded on field-data forms. Technicians from the Msambweni Hospital Vector-borne Disease Control Unit reared the larvae and pupae to adult mosquitoes for species identification. Rearing conditions were kept stable in the laboratory at an average temperature of 28°C and relative humidity of 80%. Larvae and pupae were kept in 200 ml plastic cups and fed TetraMinbaby® fish food (Tetra Werke, Melle, Germany). Standard taxonomic keys were used to distinguish Ae. aegypti species [16]. Characteristics were reported for each observed habitat, including the presence or absence of water, habitat type, size, purpose, water source, and frequency of filling and emptying. Purpose was identified in consultation with the female head of household who was asked an open-ended question about how the family was currently using each container or if the container had no immediate purpose.

Entomology survey data were analyzed using descriptive statistics of the number of habitats and number of productive habitats according to their type, purpose, and water source. Standard entomological indices were also calculated including the container index (percent of water-holding containers with larvae or pupae), Breteau index (number of positive containers per 100 houses), and house index (percent of houses with positive containers).

Semi-structured interviews

A pilot entomological survey among 100 of the 500 households was conducted between May and July 2016. From the results of this pilot survey, 40 households were selected for semi-structured in-depth interviews based on approximated risk levels for mosquito-borne disease. The 20 ‘highest risk’ households were selected because they had the most total containers and had the most mosquito larvae or pupae in containers. Conversely, the 20 ‘lowest risk’ households were selected because had the fewest number of containers and they had no mosquito larvae or pupae in containers. Research assistants collected demographic data for 40 female caregivers and conducted 35 semi-structured in-depth interviews with these women lasting approximately 45 minutes. In addition to female caregivers, research assistants conducted semi-structured interviews with 37 of the women’s children in grades 5–6 (ages 11–16).

The overarching goals of the interviews were to explore household mosquito management behaviors and their behavioral determinants. Research assistants were trained to be neutral and probe in a consistent manner (see S1 Text, S2 Text, S3 Text and S4 Text for English and Swahili versions of the interview protocol). To the extent possible, research assistants asked open-ended questions such as, “What do you know about mosquitoes?” The research assistants showed participants a video of mosquito larvae and pupae to elicit discussion around respondents’ understanding about the mosquito life cycle.

Interviews were conducted in Kiswahili or Kidigo, depending on participant preference, and audio-recorded. Research assistants then transcribed and translated the interviews into English. Two coders who did not conduct the interviews analyzed the transcripts for themes. They used an a priori (deductive) and emergent (inductive) coding processes guided by our interest in mosquito-borne disease risk perception, and motivation to engage in source reduction and other protective behaviors. They identified themes in the interviews and analyzed data by reporting frequency of mentioning those themes by respondents.

Ethics statement

We obtained written informed consent and assent from all study participants. The study protocol was reviewed and approved by the ethical review committee at the Kenyatta National Hospital/University of Nairobi (protocol # 241/03/2016) and the Institutional Review Board (IRB) of Stanford University (protocol #35504).

Results

Entomological surveys

A total of 2,452 container mosquito habitats were identified outside 444 houses across 10 villages. Among the 1,786 containers filled with water, 34 were positive (container index: 1.9%; Breteau index: 7.7). A total of 436 early instars, 641 late instars, and 390 pupae were identified. 82% were Aedes aegypti, and 18% were Culex species.

Positive containers were found outside 24 houses (house index: 5.4%), located in 5 of the 10 villages. More than one-third of the positive containers were found outside houses in 1 of the 10 villages. Among the 24 houses with positive containers, the average number of water-holding containers was 6.2 (±3.1 S.D.), nearly 3 times higher than the average for all houses: 2.2 (±1.8 S.D.). Water-holding containers varied in size from small domestic containers and bottles (<5L) to large drums and tanks (>25L), though most containers were buckets and jerrycans (10-25L) (Fig 1).

Examples of productive mosquito habitats: a) tires with no immediate purpose, b) bucket and small container for sanitation, c) small domestic containers with no immediate purpose, and d) buckets and jerrycans for laundry or with no immediate purpose.
Fig 1
Examples of productive mosquito habitats: a) tires with no immediate purpose, b) bucket and small container for sanitation, c) small domestic containers with no immediate purpose, and d) buckets and jerrycans for laundry or with no immediate purpose.

More than half of all immature mosquitoes (55.2%) were found in tires, buckets, and small domestic containers with no immediate purpose. Buckets for laundry were the next most productive, containing 37.4% of immature mosquitoes. Although tires accounted for less than 1% of all containers, they contained 28.0% of immature mosquitoes. Containers used for all other purposes were minimally productive even though they were more abundant. The majority of positive containers, and the most highly productive containers, held rainwater. These accounted for 95.8% of immature mosquitoes. (Table 1, Table 2, Table 3, Table 4, S1 Table and S2 Table)

Table 1
Percentage of total habitats are shown in parentheses across type and purpose categories. Percent of total immature mosquitoes (both larvae (early and late instars) and pupae) are reported within the cells of the table with shaded color highlighting with green, yellow, orange, and red representing 0%, 0–5%, 5–20%, and >20% of larval abundance, respectively. Habitat type according to size: 1) small domestic containers, vases, and cooking vessels (<5L), 2) tires, buckets, jerrycans, and basins (10-25L), and 3) drums and tanks (>25L).
Table of mosquito habitats by type and purpose among 444 entomological surveys in Kwale County, Kenya, between September-December 2016.
  Habitat type (% of habitats) 
  Bucket (48.1)Tire (0.7)Small containers (9.2)1Basin (6.5)Drum (2.9)Jerrycan (28.8)Other (3.8)2Total
Purpose
(% habitats)
No immediate purpose (3.4)13.828.013.40.00.00.00.055.2
Laundry (34.4)37.40.00.01.00.02.90.041.3
Sanitation (12.5)1.90.00.10.10.00.00.02.2
Animals (2.3)0.00.00.70.00.00.00.00.7
Plants (0.3)0.00.00.40.00.00.00.00.4
Other (47.1)30.00.00.00.00.20.00.00.2
 Total53.128.014.71.20.22.90.0100.0
1Food containers, bottles, vases
2Tanks and cooking vessels
3Bathing, drinking, cooking, and multiple functions
Table 2
Larval and pupal productivity profiles based on habitat type.
Habitat typeNo. of containersNo. of containers filled with water% filled with rainwaterNo. of positive containers% of positive containers filled with rainwaterNo. of early instarsNo. of late instarsNo. of pupae
Buckets109686016.31275.0206348225
Jerrycan68351415.84100.061818
Small containers32016423.2862.51224746
Basin17411622.4366.70611
Drum565238.510.0030
Tire291291.76100.010221990
Other936835.300.0000
Table 3
Larval and pupal productivity profiles based on water source (among the 1,786 containers filled with water).
Water sourceNo. of containersNo. of positive containersNo. of early instarsNo. of late instarsNo. of pupae
Rain34025429598379
Borehole46140227
Well58143214
Tap3931400
Dam110000
River/stream00000
Table 4
Larval and pupal productivity profiles based on container purpose (among the 1,786 containers filled with water).
Container purposeNo. of containersNo. of positive containersNo. of early instarsNo. of late instarsNo. of pupae
Bathing1800000
Drinking921030
Cooking770000
Animals4110100
Plants51051
No immediate purpose6014268400142
Laundry61412161202243
Sanitation22557214
Other/multiple functions4970000

Semi-structured interviews

The average age of the female caregivers was 37.2 (±9.2) with an average of 4.7 (±3.6) years of education. Most women engaged in farming or small business-related activities. All but one were Muslim, which explains the need for sanitation water used for cleansing. Shared boreholes and wells were the predominant water sources (Table 5).

Table 5
Demographic characteristics of 40 female caregivers participating in in-depth interviews and structured observations in Kwale County, Kenya, July-August 2016.
CharacteristicFrequency (%)
Age (years)137.2 (9.2)
Education (years)14.7 (3.6)
Religion
    Muslim39 (97.5)
    Christian1 (2.5)
Marital status
    Unmarried1 (2.5)
    Married35 (87.5)
    Divorced/separated1 (2.5)
    Widowed3 (7.5)
Occupation
    Farmer24 (60.0)
    Business owner7 (17.5)
    Teacher1 (2.5)
    House help1 (2.5)
    Housewife7 (17.5)
Children (number)12.2 (1.9)
Household residence (years)114.9 (9.7)
Water source
    Borehole19 (47.5)
    Well15 (37.5)
    Public tap3 (7.5)
    River1 (2.5)
    Dam1 (2.5)
1Mean (standard deviation) reported for continuous variables.

Most respondents expressed greatest concern about mosquitoes that bite at night and cause malaria. The respondent’s risk category did not impact household mosquito management or disease prevention behaviors. Several women and children distinguished between mosquitoes that bite during the day and those that bite at night; mentioning that day-biting mosquitoes are present but harmless. One woman stated that mosquitoes do not bite during the day at all. On the other hand, two women stated that mosquitoes only affect them during the day (Table 6).

Table 6
Coding themes and illustrative quotes from semi-structured in-depth interviews with 35 female caregivers and 37 children in Kwale County, Kenya, July-August 2016.
ThemeSub-themeFemale caregiver frequency (%)1Child frequency (%)2Quotes and examples
Risk perception of mosquito typesNight-timing biting mosquitoes affect us most30 (86)30 (81)“The night mosquito is the one that hurts, the night one. Egheee, there are those that I have told you they come at 2 or 1 at night, and then there are the daytime ones. Mmmmmh, the night one is the one which disturbs, always ndyeeee [making the noise that mosquitoes make when they fly] but the daytime one doesn’t disturb.” (V02001)
“They bite more at night especially starting from midnight. That’s when the dangerous mosquitoes bite and cause malaria.” (V01005)
“Mosquitoes also bite during the day but those that bite during the day are not harmful at all… harmful mosquitoes are available at night." (V01040)
Only night-time biting mosquitoes (not day-time) cause harm4 (11)N/A
Mosquito-borne diseasesMalaria35 (100)37 (100) 
Filariasis4 (11)1 (3) 
Chikungunya3 (9)0 (0) 
Bilharzia0 (0)3 (8) 
Scabies2 (6)0 (0) 
Cholera0 (0)1 (3) 
Typhoid2 (6)0 (0) 
Pneumonia2 (6)0 (0) 
Others4 (11)4 (11)Umbilical cord enlargement, headache, dizziness, diarrhea, stomach or blood vessel disease
Knowledge of larvae and pupaeAppear in _____ weeks…   
Unknown13 (37)8 (22) 
< 116 (46)14 (38) 
1–25 (14)5 (14) 
>21 (3)1 (3) 
Are young mosquitoes8 (23)6 (19)"It's only you… when you came and you sieved them and called them mosquitoes… [now] I also call them mosquitoes." (V02045)
“[I] thought they were water insects but some KEMRI researchers came and told me they were mosquitoes.” (V01014)
Have a negative effect if ingested29 (83)22 (59) 
Cause stomach issues19 (54)11 (30)“You’ll just feel it in your stomach, if you want a disease then drink them.” (V02003)
"They scare me when I see them. They have effects. . . for example when they go inside someone's stomach. It is diseases." (V01036)
Descriptions ranged from general stomach infections to diarrhea, or parasitic worms like bilharzia.
Cause mosquito problems5 (14)3 (8)Some mentioned that swallowing the larvae and pupae caused malaria while others mentioned that they would become adult mosquitoes.
If found in my water I will…“As for me, I have a well nearby. I'll just pour the water down and then fetch some new ones. But for those who get their water from a distance because also me before we dug that well I used to get my water very far. So it's not good to pour the water. I used to sieve the water. Or when there is no sieve I take a clean cloth and use it to sieve the water from the insects.” (V01014)
Pour my water out19 (54)9 (24)
Only use the water for washing/bathing but never drinking or cooking8 (23)3 (8)
Drink the water as normal/do nothing1 (3)7 (19)
Treat the water or otherwise remove them7 (20)4 (11)
Protective behaviorsSleeping under bed nets31 (89)32 (86)“The nets don’t cover the beds properly, the nets can only cover a school or a hospital bed, but if it’s a family size bed where by two to three children sleep together… the nets are small.” (V01014)
Deterring or killing adult mosquitoes10 (29)12 (32)Mosquito coils, fire, killing mosquitoes or wearing long sleeve shirts and pants.
Cleaning the environment17 (49)23 (62)"…. if you are sleeping under nets and yet your environment is not clean, that won’t help." (V01012)
Sweeping and clearing bushes or grasses.
Source reduction10 (29)6 (16)Collecting/burning coconut shells, covering containers, turning containers upside down or removing stagnant water.
1Thirty-five female caregivers responded
2Thirty-seven children responded

All of the women and children interviewed stated that mosquitoes primarily cause malaria and that at least one person in each family had been severely affected by malaria. Several respondents described other mosquito-borne diseases accurately (filariasis, chikungunya, and bilharzia), while others stated that non-mosquito-borne diseases are caused by mosquito bites (e.g., scabies, typhoid, cholera, and pneumonia) (Table 6).

Respondents demonstrated limited knowledge about the mosquito life cycle. Few mentioned household containers as primary breeding habitats because they are considered relatively clean. One woman described how mosquitoes preferentially breed in dirty water in coconut shells, saying: “[The water] stays today, tomorrow, and the third day is when they [mosquitoes] get in there…. They normally wait until they get some bad smell from the water inside the shell” (Table 6).

When researchers showed a video depicting larvae and pupae, less than one quarter of respondents recognized them as immature mosquitoes. Most considered the larvae and pupae to be a type of “unclean” organism, such as bacteria, parasites, or worms that could cause stomach infections and diarrheal disease. They did not recognize that the larvae and pupae would transform into a flying adult mosquito. Local names for the immature mosquitoes ranged widely: mwamtibwiri, mwamchibwiri, and vitikutiku (Kidigo words describing the wriggling movement); vimelea (algae); sungusungu (ants); jiggers (chigoe fleas); and vidudu (a Kiswahili term for bacteria or bugs), or maggots. (Table 6)

When researchers asked if respondents would do anything if they saw immature mosquitoes in their water, more women than children described the importance of pouring out the water or at least not drinking the larvae or pupae. One woman emphasized this point stating, “You see them [immature mosquitoes] do this [using her finger to demonstrate the wriggling movement]; then you won't drink that water. You just take the water and pour it down, because a young kid will just get the water without knowing that those things can cause disease. Or if you have dirty clothes, then you just use the water to clean them.

One respondent described the importance of not knowingly ingesting the contaminated water even though it happens accidentally: "I just clean it and pour the water, but if you haven’t seen them because it’s at night you’ll just drink them, just only one of it… you get a stomach ache". Then when asked why she wouldn’t fetch water more frequently to avoid “bugs” from entering her water, she said, "Where is the time to fetch water?! I want to go to the shamba (field for farming)… I’m tired. Several women echoed this sentiment and drew the connection between water scarcity and mosquito breeding. They specifically bemoaned the lack of piped-water access, which necessitates storing water for long periods of time and results in wriggling worms, bacteria, and generally unclean water (Table 6).

Women and children mostly reported mosquito avoidance measures, such as sleeping under bednets, as the most effective way to minimize mosquito-borne diseases. About one-third of respondents reported learning about bednets from doctors while being treated for malaria and other diseases at hospitals and school-based community clinics. Three women mentioned that they learned by experience, witnessing cause and effect. If they lit a fire, for example, they noticed how mosquitoes fled and they did not get bitten.

Few respondents knew about, let alone practiced, source reduction as a way to prevent Ae. aegypti mosquito breeding. Covering water, for example, was a measure that women took to avoid contaminating water for drinking and cooking, but was not an intentional source reduction action.

Discussion

This study combines entomological surveys that identify the most productive mosquito breeding habitats with qualitative interviews that explore behaviors related to source reduction. Our results provide a deeper understanding of the social ecological context and allow us to recommend vector control strategies. The combination of low entomological infestation, low perceived risk of daytime mosquitoes, and limited awareness about mosquito breeding in man-made containers, suggests that interventions in this part of coastal Kenya should be targeted so as to require minimal effort and align with existing incentives.

To the extent possible, vector control strategies should aim to identify and target high-risk households. In the study region, Ae. aegypti larvae and pupae were over-dispersed, meaning that immature mosquitoes were concentrated in relatively few containers at a small number of households [17]. This highlights the potential utility of tools like the Premises Condition Index (PCI) that have been developed from predictive models to identify high-risk households for targeted vector control [18, 19]. The PCI, originally developed in Australia and further tested in Central America and South Asia, aims to rapidly assess the cleanliness of an area and the degree of shade in order to predict the risk of Ae. aegypti infestation [1921]. This or a similar tool could be further honed and adapted for the study region and other Sub-Saharan African countries.

Because only a few habitat types predominated, source reduction should target highly productive habitat types. Many interventions encourage targeted source reduction based on container type (e.g., buckets, drums, tanks, and tires,) but fewer consider container purpose [22]. From a behavioral standpoint, considering purpose when targeting productive habitat types would reduce the number of containers of concern dramatically and would also increase the impact of any efforts [23]. The most productive habitat types can be grouped into three categories based on purpose: 1) containers with an immediate purpose or with a potential future purpose (e.g., buckets), 2) containers with no immediate purpose but with repurposing value (e.g., tires) and 2) containers with no immediate purpose and limited repurposing value (e.g., small domestic containers and bottles).

Buckets used for laundry or those kept around for some future use could be covered if covers were easy to retain. Covering containers is a commonly recommended source reduction tactic and has been found to significantly reduce the odds of a container having immature mosquitoes by more than 80% [17]. Given the irregularity of laundry bucket use, covering with nylon net could allow for the continued use of containers without removing the cover. Nylon net covers have reduced mosquito abundance elsewhere, despite some long-term maintenance needed to patch any holes that the form in the net [24]. In this context, residents would need to be convinced that it would be worth their time to cover buckets used for purposes other than drinking and cooking since respondents did not see a reason to cover water that wasn’t being ingested. One challenge with covering buckets is related to the number of buckets in circulation. Although targeting buckets would reduce mosquito breeding by half in this study region, with more than 1,000 buckets, it would be time intensive to manage and sustain.

Tires, on the other hand, were highly productive and yet few in number, making them an attractive source reduction target. Consistent with the evidence from this study, tires have been found to be highly productive habitats elsewhere in Kenya and other countries in sub-Saharan Africa [8, 2527], as well as across the world, in the US, Caribbean, South and Southeast Asia [20, 2830]. Part of the reason tires may be so productive is due to the fact that they sit for long periods of time undisturbed, as we noted in this study. Other factors could include the water temperature and detritus that tends to collect in tires, making them ideal breeding sites for numerous Aedes and Culex species [20].

Tires in this study context had no immediate purpose but considerable value. Since covers are unlikely to be applicable to tires that are not intended to hold water, we recommend different actions. Some tires remain outside residences because they are informally used as seats. Cutting and turning over these tires could ensure that they don’t collect water. Others could be collected and re-purposed to make recycled goods such as toys or shoes.

For small domestic containers, food tins, and plastic bottles with no purpose at all, we recommend community clean-ups and efforts to improve solid waste management. In the short-term, households could consolidate trash under a shaded storage place away from rain. Periodic community-led trash clean-ups may be more appropriate than household-level actions since they would not require a change in habits. Since the respondents already expressed interest in maintaining their compounds, any additional benefit or income that they could generate from collecting, recycling, or re-using no-purpose containers would add even more incentive. At a larger scale, improving centralized solid waste management and access to piped water would have benefits for long-term vector control as well as the prevention of other diseases [31]. However, governmental provision and maintenance of these services will take time, and coverage is likely to be patchy and inconsistent, especially in informal and rural settlements [32].

Our source reduction recommendations are specific to the study region. Given the low mosquito infestation indices, our data suggest that Ae. aegypti-specific control measures like targeted source reduction may be easy to implement but a lower priority than Anopheles control. By only sampling outdoors, we may have underestimated the abundance of Ae. aegypti immatures. However, the effect of this is likely to be minimal given the evidence that Ae. aegypti primarily breed in outdoor containers across the study region [8].

Future research should consider urban areas of coastal Kenya where Ae. aegypti mosquitoes have been found to be three times more abundant than nearby rural areas [8, 9]. Numerous outbreaks of chikungunya have occurred in cities along Kenya’s coast within the past decade [33, 34]. Although disease risk is likely to be higher in urban areas, these communities tend to be more informal and less cohesive. Therefore, source reduction recommendations may benefit less from collaborative community clean-ups and necessitate vector control strategies tailored to the unique social and ecological characteristics of those urban settings.

Acknowledgements

The authors appreciate remarkable field data collection support from Julius Kamoni, Robin Bundi, Hussein Kitsongo, Rashid Mtowa. Finally, the authors acknowledge the study participants in Kwale County.

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    W Tun‐Lin, A Lenhart, VS Nam, E Rebollar‐Téllez, A Morrison, P Barbazan, et al. Reducing costs and operational constraints of dengue vector control by targeting productive breeding places: a multi‐country non‐inferiority cluster randomized trial. Tropical Medicine & International Health. 2009;14(9):, pp.1143–53.

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    D Getachew, H Tekie, T Gebre-Michael, M Balkew, A Mesfin. . Breeding sites of Aedes aegypti: potential dengue vectors in Dire Dawa, East Ethiopia. Interdisciplinary perspectives on infectious diseases. 2015;2015.

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    J Midega, J Nzovu, S Kahindi, R Sang, C Mbogo. . Application of the pupal/demographic-survey methodology to identify the key container habitats of Aedes aegypti (L.) in Malindi district, Kenya. Annals of Tropical Medicine & Parasitology. 2006;100(sup1):, pp.61–72.

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    A Philbert, JN Ijumba. . Preferred breeding habitats of Aedes aegypti (Diptera Culicidae) mosquito and its public health implications in Dares Salaam. Journal of Environmental Research and Management. 2013;4(10):, pp.344–51.

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    A Krystosik, G Njoroge, L Odhiambo, JE Forsyth, F Mutuku, AD LaBeaud. . Solid Wastes Provide Breeding Sites, Burrows, and Food for Biological Disease Vectors, and Urban Zoonotic Reservoirs: A Call to Action for Solutions-Based Research. Frontiers in Public Health. 2020;7(405). , doi: 10.3389/fpubh.2019.00405

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    H Zeller, W Van Bortel, B Sudre. . Chikungunya: Its History in Africa and Asia and Its Spread to New Regions in 2013–2014. The Journal of Infectious Diseases. 2016;214(suppl_5):, pp.S436–S40. , doi: 10.1093/infdis/jiw391

14 Jan 2020

Dear Dr. Forsyth:

Thank you very much for submitting your manuscript "Source reduction with a purpose: mosquito ecology and community perspectives offer insights for improving household mosquito management in coastal Kenya" (#PNTD-D-19-01882) for review by PLOS Neglected Tropical Diseases. Your manuscript was fully evaluated at the editorial level and by independent peer reviewers. The reviewers appreciated the attention to an important problem, but raised some substantial concerns about the manuscript as it currently stands. These issues must be addressed before we would be willing to consider a revised version of your study. We cannot, of course, promise publication at that time.

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PLOS Neglected Tropical Diseases

Eric Dumonteil

Deputy Editor

PLOS Neglected Tropical Diseases

***********************

Reviewer's Responses to Questions

Key Review Criteria Required for Acceptance?

As you describe the new analyses required for acceptance, please consider the following:

Methods

-Are the objectives of the study clearly articulated with a clear testable hypothesis stated?

-Is the study design appropriate to address the stated objectives?

-Is the population clearly described and appropriate for the hypothesis being tested?

-Is the sample size sufficient to ensure adequate power to address the hypothesis being tested?

-Were correct statistical analysis used to support conclusions?

-Are there concerns about ethical or regulatory requirements being met?

Reviewer #1: This is an interesting study, backed with clear objectives and well designed to address the insights for improving household mosquito management in coastal Kenya. There is a clear statement on the sample size used for entomological and interviews components.

HOWEVER,

a) In the abstract- Looking at Methodology/ Principal Methodology: these two items could be more clear if separated!

b) Lines - 33-34: “The field team conducted entomological surveys in 34 444 households in Kwale County, coastal Kenya, between May and December 2016.” The abstract does not include the interviews— was that deliberately or an oversight?

Main Document

Methodology

Sampling approach applied to obtain households both for entomological and Interviews need to be presented in a more straightway style.

Ref. Lines 152-154: While it is clearly written that “Fifty houses with children in 152 grades 5 and 6 (approximately ages 11 to 16) were randomly selected from 10 different primary school rosters” . Readers at Ref Lines No. 168-172: will question “How were these 40 households selected?”

Reviewer #2: The authors are investigating the productive mosquito breeding habitats and explore the existing knowledge, attitudes and behaviour of the community participants in relation to source reduction. They used mixed methods approach that combines entomological surveys and interviews to female caregivers and children. This approach proves better as it provides a deeper understanding of the social ecological context towards vector control strategies. This is a well written manuscript which I think should be published without delay.

Introduction/Background: The background information is good, well written and the research question is easily identifiable.

Materials & Methods: The methodologies applied are appropriate and adequately described. The study design is appropriate and the data analysis is also adequately described.

Reviewer #3: A major method (how purpose of containers was defined and studied) needs to be better described.

The population wasn't necessarily the best choice given the low infestation indices found, but this did not affect my recommendation.

My recommendation is based on the need to describe that method better as well as make correct use of the numerous references, and shorten and sharpen the results and discussion.

All other aspects of study design are appropriate.

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Results

-Does the analysis presented match the analysis plan?

-Are the results clearly and completely presented?

-Are the figures (Tables, Images) of sufficient quality for clarity?

Reviewer #1: The manuscript contains quantitative and qualitative results. However, the Authors there is no description on Data analysis. Hence, The authors are expected to address this gap!

Reviewer #2: Results, Discussion and conclusion:The results and discussions are coherently described. The Tables and supporting information provided are of sufficient quality and well presented. The discussion highlights the different aspects of the findings and are neatly discussed in relation to the current literature.

Reviewer #3: The analysis presented matches the analysis plan.

The results are presented in a repetitive way at times. I suggest in my comments how to shorten.

The figures are of sufficient quality for clarity and don't require that much more text as the volume currently provided.

--------------------

Conclusions

-Are the conclusions supported by the data presented?

-Are the limitations of analysis clearly described?

-Do the authors discuss how these data can be helpful to advance our understanding of the topic under study?

-Is public health relevance addressed?

Reviewer #1: Conclusions: This is missing in the main document while abstract prepares readers to see it!

Reviewer #2: The conclusions are clear and logical and are supported by data presented.

Reviewer #3: The conclusions are supported by the data presented, but they are currently presented in a vague manner.

There is no limitations section and I recommend one in my comments.

All other aspects of conclusions are appropriate.

--------------------

Editorial and Data Presentation Modifications?

Use this section for editorial suggestions as well as relatively minor modifications of existing data that would enhance clarity. If the only modifications needed are minor and/or editorial, you may wish to recommend “Minor Revision” or “Accept”.

Reviewer #1: "Minor Revision"

Reviewer #2: N/A

Reviewer #3: 10. Various other comments throughout:

1. Water “holding” might be a better term than water “storage” containers, to better capture the fact that in this setting the water collection in the containers without immediate purpose was not intentional.

2. Lines 73-75. Consider this editing: “Individuals with these diseases can range from asymptomatic to… suffering from life-threatening encephalitis and hemorrhage, to… debilitating arthritis that can persist for years (Murray et al. 2013).

3. Line 87. “Adult mosquitoes typically venture less than 100 meters from their hatch site” – true if they hatch in and around people’s homes because they do not need to travel far for a blood meal. Not true if they hatch at a tire dump or car graveyard with few or no humans around. Consider qualifying statement.

4. Line 88 re biting during circumscribed times of the day – qualify that this finding pertains to Kenya.

5. Lines 90-93. Statement is true about any setting.

6. Line 98 “easier” tasks vs. easy tasks because covering containers is not easy if you actually try it…

7. Lines 117-118. “Most interventions do not target specific habitat types, possibly because mosquito habitats are numerous and vary by season.” All the interventions that you cite target specific habitat types. The point you want to make, not here – in the discussion, is that interventions should target containers by purpose.

8. Line 126. If you only looked at containers outside homes without checking inside homes, you cannot claim that the important containers were only found outside. In fact this point will fit well in a study limitation section.

9. Line 143. “Mosquitoes are least abundant during the long dry season.” This may be true for Anopheles. Is there any evidence for Aedes? Better off to delete. Or qualify which mosquitoes you refer to.

10. Lines 211-214. Specify if the containers found had water or not. If they were dry, it was no surprise that they didn’t have immature mosquitoes.

11. Line 404. “For example, instead of non-targeted source reduction, requiring households to consider 2,452 containers…” A reason to target dry but useful containers would be to protect them from the rain. Rephrase.

13. Lines 409-411: “While there were only 29 tires, these accounted for up to 30% of immature mosquitoes, so targeting tires would be less behaviorally intensive than buckets, but not as effective as considering purpose along with habitat type.” You didn’t find any tires with a purpose (Table 1) so it would be just as effective to target those 29 tires. A more important problem is that tires are kept for future use, and those without any purpose at all have nowhere to go - no services exist...

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Summary and General Comments

Use this section to provide overall comments, discuss strengths/weaknesses of the study, novelty, significance, general execution and scholarship. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. If requesting major revision, please articulate the new experiments that are needed.

Reviewer #1: This manuscript is generally well written, with relevant materials in its field of study. It is publishable upon addressing the minor revisions as suggested.

Reviewer #2: The paper is well written and appropriate for the journal

Reviewer #3: The manuscript incudes an excellent title and well written abstract, both of which raise the reader’s expectations for a very good piece of research with important intervention insights. However some key but fixable weaknesses need to be addressed before the manuscript can bring its point across to the reader.

1. Purpose takes a central focus on the title, abstract and throughout the manuscript. However, there is no information on how purpose was identified. This is a major weakness of the manuscript. In the methods section, please, provide explicit information on how the purpose of each container studied was defined. Include who reported the purpose, and how was the question asked (open ended/closed). The meaning of “no purpose” may well be “no immediate purpose, but we keep the container for future use.” Indeed, it takes the reader until page 26 of the manuscript to find out that indeed this was the case for the larger containers. The cut tire e.g. in Fig 1a may not have had a purpose at the moment of the survey, but the way it is cut is characteristic of tires used as animal drinking dishes. This reviewer therefore suggests that “no purpose” is replaced with “no immediate purpose” throughout the manuscript and tables, and to explain this in the methods and take it out of page 26.

2. The current use of citations in the text, especially in the introduction raises serious concerns. The manuscript should not be accepted before the authors go over each citation and check that it is used correctly to make the point that it is intended to make. This is another major weakness of the manuscript. Examples include:

1. Gubler 2002 does not mention child development. Rephrase

2. Lines 84-86. Harrington 2005 does not seem an appropriate reference because it talks about release and recapture of adult mosquitoes in Puerto Rico and Thailand – not where they breed.

3. Ngugi found key containers outdoors in the western region of Kenya and indoors in the coastal region. Drums, buckets and pots that Ngugi found were purposeful water storage containers. It should not be taken for granted that the important containers are found only outdoors. This may vary by setting. A similarly inaccurate statement about Ngugi is made in lines 119-121.

4. Lines 95-97, re Keating reference: when the goal is to prevent malaria, bed nets will be effective but source reduction of containers around the home will not be effective, because Anopheles doesn’t breed in containers around the home like Aedes. So this reference here doesn’t apply and malaria control programs should not bring reduction of water containers in the home into the mix! Same goes for Kibe reference – larvae found in and around homes are not anopheles larvae and controlling them will not control malaria. The point to make here instead is that the overwhelming focus has been in malaria control and the Aedes larvae found in and around the home are allowed to complete their life cycle undetected. But this means that education efforts should distinguish between mosquito larvae and adults and specifically mention which behavior will control which type of mosquito larvae.

5. Lines 100-102. Neither Andersson nor Winch say that households often perceive source reduction labor intensive or ineffective. In fact in Andersson, households had a positive attitude toward source reduction. Andersson et al perceive that “We do not, however, expect community participation in dengue control [via source reduction] to be easy or easily sustainable.” Winch et al perceive that source reduction behaviors are complex in nature, large in number and difficult to perform by households; that entomologists are concerned that voluntary source reduction may be ineffective because of the high level of coverage required. Rephrase or delete.

6. Line 103. The intervention by Arunachalam 2012 was targeted but definitely not simple - covers had to be made in three different sizes and promoted through community actors, clean-up campaigns had to be organized, and dissemination of dengue information given through schoolchildren. The point to make here is that good covering interventions exist and could be leveraged for your study site. The point with its reference is better suited for the discussion.

7. Lines 104-107. In Bowman 2016, “house screening significantly reduced dengue risk, OR 0.22 (95% CI 0.05–0.93, p = 0.04), as did combining community-based environmental management and water container covers, OR 0.22 (95% CI 0.15–0.32, p<0.0001).” Refrain from singling out covers.

8. Lines 121-124. Prochaska 2008, in contrast to what the authors state, provides a rationale and need for multiple health behavior change interventions, and reviews a series of theoretical and methodological issues that need to be resolved in order to implement such multiple health behavior changes interventions successfully. In addition all the successful source reduction interventions that the authors cite earlier consist of implementing multiple health behaviors at a time. Rephrase.

9. Lines 364-367: “The implication of over-dispersed larval and pupal distributions on vector control is that an intervention must obtain good geographic coverage in order to reduce breeding enough to disrupt disease transmission (Irvine et al. 2018).” This statement doesn’t make sense in the context of overdispersal. Overdispersal calls for finding the heavily infested households and concentrating on those. Besides, the Irvine reference is on a totally different mosquito with very different larval habitats not studied in your paper. Irvine studies biting behavior instead. The statement can go.

10. Line 376. “Consistent with other studies, tires, buckets and small domestic containers were the most productive habitat types.” In the Focks and Chadee 1997 study cited to defend this point, tires, buckets and small domestic containers were equally important as water storage drums and tanks. In that setting (Trinidad) water storage drums and tanks are much larger in volume (55 US gallons, 1 US gallon equals 3.78 litres). Therefore this is not a good comparison. And the Ndenga and Ngugi studies also found important indoor containers. You are better off eliminating that point altogether.

11. Kathomi 2013. Complete reference or delete

3. In the abstract, methods and other places, knowledge and attitudes are mentioned as behavioral determinants studied in the manuscript. However, the reviewer could not identify any data pointing to attitudes. Knowledge, yes, as well as a number of other determinants are described, such as people’s previous lived experience with mosquitoes (felt night biting, noticed night mosquito nuisance, felt effectiveness of bednets); the purpose of the water held in the containers is a major behavioral determinant in the study; lack of access to adequate covers for their containers, and lack of access to waste collection services are mentioned in the discussion. This reviewer therefore suggests replacing knowledge, attitudes and behaviors with, say, exploration of household mosquito management behaviors and their behavioral determinants, or similar.

4. The study is described as combining mixed methods. This reviewer suggests stating combining entomological surveys with qualitative methods, wherever mixed methods are currently mentioned.

5. The results section text is often repetitive, as well as repeats what is stated in the tables. Please go through and shorten. Examples include: Lines 247-269, lines 277-279, Text repeating much of Table 6.

6. A glaring finding of the study is the low entomological infestation indices, making any intervention easier to implement, especially due to the documented overdispersal that calls for targeting certain households rather than everyone, but at the same time not a highly prioritized site for Aedes aegypti control. The manuscript will benefit from commenting on this in the discussion, or in a separate study limitation section.

7. In abstract, author summary and discussion, qualify conclusions as appropriate for the specific study setting, therefore recommendations applying to that setting, not necessarily generally, because in many studies cited in the manuscript, the purposeful containers are more problematic than or as problematic as the accidental ones.

8. Please shorten and sharpen the discussion. No need to repeat results. Limit and sharpen recommendations to the specific study site; e.g. instead of mentioning covering in general, state what type of covers would serve buckets of various sizes. Limit each recommendation to one or two sentences. The reader is exhausted by the time we reach the discussion!

9. In line with an earlier comment, separate out the household mosquito management recommendations in the discussion, for containers with no purpose at all vs. those with no immediate purpose, from the start.

--------------------

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Reviewer #1: Yes: Adiel K. Mushi

Reviewer #2: No

Reviewer #3: No

Submitted filename: Manuscript_ Review-Source reduction with a purpose- Jena e et al.docx

14 Mar 2020

Submitted filename: Forsyth et al. reviewer responsev2.docx

20 Mar 2020

Dear Dr. Forsyth,

We are pleased to inform you that your manuscript 'Source reduction with a purpose: mosquito ecology and community perspectives offer insights for improving household mosquito management in coastal Kenya' has been provisionally accepted for publication in PLOS Neglected Tropical Diseases.

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Thank you again for supporting Open Access publishing; we are looking forward to publishing your work in PLOS Neglected Tropical Diseases.

Best regards,

Roberto Barrera, Ph.D.

Associate Editor

PLOS Neglected Tropical Diseases

Eric Dumonteil

Deputy Editor

PLOS Neglected Tropical Diseases

***********************************************************


4 May 2020

Dear Dr. Forsyth,

We are delighted to inform you that your manuscript, "Source reduction with a purpose: mosquito ecology and community perspectives offer insights for improving household mosquito management in coastal Kenya," has been formally accepted for publication in PLOS Neglected Tropical Diseases.

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Thank you again for supporting open-access publishing; we are looking forward to publishing your work in PLOS Neglected Tropical Diseases.

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PLOS Neglected Tropical Diseases

Shaden Kamhawi

Editor-in-Chief

PLOS Neglected Tropical Diseases

https://www.researchpad.co/tools/openurl?pubtype=article&doi=10.1371/journal.pntd.0008239&title=Source reduction with a purpose: Mosquito ecology and community perspectives offer insights for improving household mosquito management in coastal Kenya&author=Jenna E. Forsyth,Francis M. Mutuku,Lydiah Kibe,Luti Mwashee,Joyce Bongo,Chika Egemba,Nicole M. Ardoin,A. Desiree LaBeaud,Roberto Barrera,Eric Dumonteil,Roberto Barrera,Eric Dumonteil,Roberto Barrera,Eric Dumonteil,Roberto Barrera,&keyword=&subject=Research Article,Medicine and Health Sciences,Infectious Diseases,Disease Vectors,Insect Vectors,Mosquitoes,Biology and Life Sciences,Species Interactions,Disease Vectors,Insect Vectors,Mosquitoes,Biology and Life Sciences,Organisms,Eukaryota,Animals,Invertebrates,Arthropoda,Insects,Mosquitoes,Biology and Life Sciences,Developmental Biology,Life Cycles,Pupae,Biology and Life Sciences,Developmental Biology,Life Cycles,Larvae,Biology and Life Sciences,Psychology,Behavior,Social Sciences,Psychology,Behavior,Medicine and Health Sciences,Infectious Diseases,Disease Vectors,Insect Vectors,Mosquitoes,Aedes Aegypti,Biology and Life Sciences,Species Interactions,Disease Vectors,Insect Vectors,Mosquitoes,Aedes Aegypti,Biology and Life Sciences,Organisms,Eukaryota,Animals,Invertebrates,Arthropoda,Insects,Mosquitoes,Aedes Aegypti,Biology and Life Sciences,Zoology,Entomology,Biology and Life Sciences,Psychology,Behavior,Animal Behavior,Animal Sexual Behavior,Social Sciences,Psychology,Behavior,Animal Behavior,Animal Sexual Behavior,Biology and Life Sciences,Zoology,Animal Behavior,Animal Sexual Behavior,Medicine and Health Sciences,Infectious Diseases,Infectious Disease Control,