Measuring and characterizing night time human behaviour as it relates to residual malaria transmission in sub-Saharan Africa: a review of the published literature

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malaria 104 Title: Malaria JournalMeasuring and characterizing night time human behaviour as it relates to residual malaria transmission in sub-Saharan Africa: a review of the published literatureApril MonroeSarah MooreHannah
malaria 698 interventions, namely insecticide-treated nets or indoor residual spraying, poses a significant challenge to malaria elimination efforts. To understand when and where remaining transmission is occurring, it is necessary
malaria 929 and human behaviour, and where they overlap. To date, a review of human behaviour related to residual malaria transmission has not been conducted.MethodsStudies were identified through PubMed and Google Scholar.
malaria 1267 to English language articles published between 2000 and 2017. Publications with primary data from a malaria endemic setting in sub-Saharan Africa and a description of night time human behaviours were included.ResultsTwenty-six
malaria 1534 inclusion criteria. Study results fit into two broad categories: when and where people are exposed to malaria vectors and what people are doing at night that may increase their contact with malaria vectors. Among
malaria 1622 exposed to malaria vectors and what people are doing at night that may increase their contact with malaria vectors. Among studies that quantified human-vector interaction, a majority of exposure occurred indoors
malaria 2433 is well-established, relatively few studies have included human behaviour when measuring exposure to malaria vectors. Broader application of a standardized approach to measuring human-vector interaction could
malaria 2690 settings and over time. In-depth understanding of night time activities that occur during times when malaria vectors are active and barriers to prevention practices in different contexts should also be considered.
malaria 3036 prevention tools.BackgroundSubstantial and sustained global efforts have led to a significant decrease in malaria burden over the last 15 years, with a 41% decrease in incidence rates and 62% decrease in mortality
malaria 3539 estimated 68% of the decrease in infections can be attributed to ITNs, making this the most effective malaria prevention tool currently available [[1], [3]]. Combined, the core vector control interventions, ITNs
malaria 3710 core vector control interventions, ITNs and IRS, account for an estimated three quarters of clinical malaria cases averted [[1]].Despite the contribution of ITNs and IRS to vector control, malaria persists, with
malaria 3798 of clinical malaria cases averted [[1]].Despite the contribution of ITNs and IRS to vector control, malaria persists, with a disproportionate impact on sub-Saharan Africa. In 2016, sub-Saharan Africa accounted
malaria 3923 disproportionate impact on sub-Saharan Africa. In 2016, sub-Saharan Africa accounted for 90% of all malaria cases and 91% of all malaria deaths [[4]]. Residual malaria transmission, defined by the World Health
malaria 3952 sub-Saharan Africa. In 2016, sub-Saharan Africa accounted for 90% of all malaria cases and 91% of all malaria deaths [[4]]. Residual malaria transmission, defined by the World Health Organization as ‘persistence
malaria 3983 sub-Saharan Africa accounted for 90% of all malaria cases and 91% of all malaria deaths [[4]]. Residual malaria transmission, defined by the World Health Organization as ‘persistence of parasite transmission even
malaria 4261 well as in situations where ITN use or IRS are not practical’, represents a critical challenge for malaria control and elimination efforts [[5]–[8]].As indoor-focused interventions, there are limitations to
malaria 4675 Significant research has been done to understand mosquito feeding and resting behaviour. The dominant malaria vectors in Africa are Anopheles gambiae sensu lato (s.l.) (including An. gambiae sensu stricto, Anopheles
malaria 5421 and rest outside. In addition, in recent years shifts in vector behaviour following introduction of malaria control interventions in certain locations have been observed [[9]–[13], [18], [19]]. These changes
malaria 5824 successful vector control, there is an urgent need to understand when and where people remain at risk for malaria transmission to effectively target specific places, groups, and activities. This information is critical
malaria 5949 effectively target specific places, groups, and activities. This information is critical for guiding malaria control and elimination efforts. To understand when and where remaining transmission is occurring, it
malaria 6670 The review focuses on human behaviour in sub-Saharan Africa based on the disproportionate burden of malaria in these countries.MethodsA literature review of published research findings was carried out using electronic
malaria 7524 01/01/2000-12/31/2017Number of articles screenedAfrica[MeSH Terms] AND human AND (behavior OR behaviour) AND malaria 1361Africa[MeSH Terms] AND “Human Activities” [MeSH Terms] AND malaria732Outdoor OR outside OR residual
malaria 7598 AND (behavior OR behaviour) AND malaria1361Africa[MeSH Terms] AND “Human Activities” [MeSH Terms] AND malaria 732Outdoor OR outside OR residual AND malaria AND (behavior OR behaviour)307Malaria AND (outdoor OR residual)
malaria 7643 malaria1361Africa[MeSH Terms] AND “Human Activities” [MeSH Terms] AND malaria732Outdoor OR outside OR residual AND malaria AND (behavior OR behaviour)307Malaria AND (outdoor OR residual) AND behavior217Human AND location AND
malaria 7753 AND (behavior OR behaviour)307Malaria AND (outdoor OR residual) AND behavior217Human AND location AND malaria 119(“Human behavior” or “human behaviour”) AND malaria 45“Human activities”[Mesh] and malaria
malaria 7815 AND behavior217Human AND location AND malaria119(“Human behavior” or “human behaviour”) AND malaria 45“Human activities”[Mesh] and malaria and (outdoor OR residual)23Anthropology OR anthropologic
malaria 7859 malaria119(“Human behavior” or “human behaviour”) AND malaria 45“Human activities”[Mesh] and malaria and (outdoor OR residual)23Anthropology OR anthropologic AND malaria exposure 17Outdoor AND human AND
malaria 7928 malaria 45“Human activities”[Mesh] and malaria and (outdoor OR residual)23Anthropology OR anthropologic AND malaria exposure 17Outdoor AND human AND behavior AND night AND Africa21Outdoor AND malaria AND (“human
malaria 8013 anthropologic AND malaria exposure 17Outdoor AND human AND behavior AND night AND Africa21Outdoor AND malaria AND (“human behaviour” OR “human behavior”)6Africa[MeSH Terms] AND “human exposure” AND
malaria 8122 AND (“human behaviour” OR “human behavior”)6Africa[MeSH Terms] AND “human exposure” AND malaria 35Africa[MeSH Terms] AND “Human Activities” [MeSH Terms] AND night time4Africa[MeSH Terms] AND human
malaria 8381 time12Studies were included in the review if they involved investigation of human behaviours in relation to malaria exposure. Specifically, studies needed to include a malaria endemic setting in sub-Saharan Africa and
malaria 8441 investigation of human behaviours in relation to malaria exposure. Specifically, studies needed to include a malaria endemic setting in sub-Saharan Africa and a description of human behaviours occurring during times when
malaria 8553 endemic setting in sub-Saharan Africa and a description of human behaviours occurring during times when malaria transmission can occur, i.e. when malaria transmitting vectors are active. Behaviour is defined by PubMed
malaria 8595 description of human behaviours occurring during times when malaria transmission can occur, i.e. when malaria transmitting vectors are active. Behaviour is defined by PubMed as, “the observable response of a
malaria 9179 full-text was evaluated and grouped by categories of human activities occurring during times when local malaria vectors are active, methods for capturing human behaviour, and presence and type of entomology data
malaria 9688 key areas of interest: when (time of night) and where (indoors versus outdoors) people are exposed to malaria vectors and characterization of night time activities occurring during hours when malaria vectors are
malaria 9778 exposed to malaria vectors and characterization of night time activities occurring during hours when malaria vectors are active.Human exposure to malaria vectorsTen studies integrated human behavioural and entomological
malaria 9823 characterization of night time activities occurring during hours when malaria vectors are active.Human exposure to malaria vectorsTen studies integrated human behavioural and entomological data to provide a quantitative estimate
malaria 10248 collectedEntomological methodsTiming of entomology and human behaviour data collectionHuman exposure to malaria vectorsKilleen et al. (2006) [[20]]TanzaniaSurveyUsual bed time and wake-up timeIndoor and outdoor HLC,
malaria 14618 asleep)Protective efficacy of an ITN:51%Bradley et al. (2015) [[28]]Equatorial Guinea-Bioko IslandAnnual malaria indicator surveyTime household members entered the house the night before, any other time spent outside
malaria 17907 4:00 a.m. to 6:00 a.m. in selected sites in Tanzania and Burkina Faso, and self-reported survey data from malaria indicator surveys in Zambia and Kenya. The two methods were not compared to one another. Bradley et
malaria 18063 methods were not compared to one another. Bradley et al. also used data from questions included in a malaria indicator survey [[28]]. Other studies used self-reported survey data to gather similar information
malaria 18730 common human-vector indicators presented in the studies reviewed included proportion of exposure to malaria vectors occurring indoors for an unprotected individual, exposure to malaria vectors occurring indoors
malaria 18807 proportion of exposure to malaria vectors occurring indoors for an unprotected individual, exposure to malaria vectors occurring indoors during sleeping hours for an unprotected individual, exposure occurring indoors
malaria 19153 across all studies integrating human and vector data.Across settings, a majority of human exposure to malaria vectors for non-users of ITNs was found indoors, largely during sleeping hours. However, variation was
malaria 19773 [23]–[27]]. However, Cooke et al. found that use of an ITN could prevent only about half of exposure to malaria vectors despite predominantly endophagic primary vectors, likely due to high levels of indoor exposure
malaria 20326 (indoor/outdoor) of exposure across time. Russell et al. found significant changes in indoor human exposure to malaria vectors for both An. gambiae s.l. and An. funestus as ITN use increased [[22]]. In 1997, over 90% of
malaria 20977 species, namely An. arabiensis [[20], [21], [26], [27]].Association between night time location and malaria riskSeven studies were identified that linked night time location with malaria risk. Four of the six
malaria 21056 night time location and malaria riskSeven studies were identified that linked night time location with malaria risk. Four of the six studies specifically looked at whether time spent outdoors at night was associated
malaria 21195 specifically looked at whether time spent outdoors at night was associated with an increased risk of malaria infection. A case control study in South-West Kenya by Githinji et al. assessed micro-ecological and
malaria 21367 et al. assessed micro-ecological and human behavioural factors associated with an increased risk of malaria infection. Human behaviour was assessed through a standardized survey [[31]]. No detail on the content
malaria 21654 section. Results showed participants who spent time outside at night were more likely to be infected with malaria . Spending time outside at night was binary and did not specify length of time or time of the night.
malaria 22255 section.In two studies, Bradley et al. investigated the association between time spent outdoors and malaria infection on Bioko Island, Equatorial Guinea. In a 2012 publication, Bradley analysed data from an annual
malaria 22369 infection on Bioko Island, Equatorial Guinea. In a 2012 publication, Bradley analysed data from an annual malaria indicator survey, which includes a question asking whether a child spent time outside between 10 p.m.
malaria 22912 publication, Bradley et al. conducted a survey to measure the association between time spent outdoors and malaria infection as measured by RDT, in addition to measuring exposure to malaria vectors [[28]]. Malaria infection
malaria 22987 time spent outdoors and malaria infection as measured by RDT, in addition to measuring exposure to malaria vectors [[28]]. Malaria infection was not significantly higher in individuals who reported spending
malaria 23648 household members. Outdoor sleeping varied by season and was associated with a significantly higher risk of malaria infection.Hetzel et al. carried out a longitudinal study looking at time spent at shamba (farm houses)
malaria 25092 household compound during peak vector biting hours. Time spent in high or low risk areas, identified by a malaria risk map, depended on the level of risk for the area in which a participant’s compound was located.
malaria 26219 months. While presented together, the data were not integrated to provide an estimate of exposure to malaria vectors.Characterization of night time activitiesA total of 10 studies included some description of
malaria 26383 of 10 studies included some description of night time activities occurring during times when local malaria vectors are active (Table 3). These studies identified activities taking place in the peri-domestic
malaria 30222 often looked at specific night time activities, as well as the impact of these activities on use of malaria prevention tools.The level of detail provided on night time activities and sleeping patterns varied
malaria 30594 patterns in response to livelihood practices and socio-cultural events, and how these could impact malaria exposure and prevention practices in rural Tanzania [[38]]. The study documented changes in daily and
malaria 31186 Uganda, spending time away from home at night emerged as an important theme for understanding potential malaria exposure and prevention practices [[39]]. Social events, livelihood activities, and "times of difficulty”
malaria 32961 of routine household chores, social activities, and large-scale events that may impact exposure to malaria vectors and use of prevention tools. Large-scale socio-cultural events and outdoor sleeping were the
malaria 34174 work, funerals, parties, and other gatherings as activities that could increase risk of exposure to malaria . Mosquito collections were carried out in bars but were not linked with human behavioural data.Dlamini
malaria 34425 semi-structured interviews, focus group discussions, and observations to identify behaviours that might impact malaria control interventions. Group socialization outside late into the evening at soccer games, friends’
malaria 36104 al. used in-depth interviews and focus group discussions to better understand community knowledge of malaria transmission. The study described time spent outdoors, primarily during the early evening hours. During
malaria 38936 The first relates to when (time of night) and where (indoors versus outdoors) people are exposed to malaria vectors. The second is what people are doing at night that may increase their contact with malaria vectors.
malaria 39035 malaria vectors. The second is what people are doing at night that may increase their contact with malaria vectors. This understanding of human behaviour is crucial for targeting context-appropriate vector control
malaria 39364 study design and methods, the results of the studies in this review suggest a majority of exposure to malaria vectors continues to occur indoors during sleeping hours for unprotected individuals. This is true even
malaria 39744 settings, signalling a gap in protection. One of the most relevant indicators for understanding residual malaria transmission is the protective efficacy of ITNs, defined as the proportion of human exposure to malaria
malaria 39848 malaria transmission is the protective efficacy of ITNs, defined as the proportion of human exposure to malaria vectors prevented by ITN use out of total exposure i.e. compared to a non-user. Protective efficacy,
malaria 40142 was as low as 50% in some settings, with even lower estimates of protection for primarily exophagic malaria vectors. The fraction of exposure occurring indoors during non-sleeping hours and outdoors can pose
malaria 40262 fraction of exposure occurring indoors during non-sleeping hours and outdoors can pose a threat to malaria control and elimination efforts [[10]].While the review focused on studies published between 2000 and
malaria 41225 understanding of human behaviour is as important as vector behaviour for understanding when and where malaria transmission occurs and that the presence of humans must be considered when calculating risk of infective
malaria 41411 calculating risk of infective bites [[47]].Despite the importance of human behaviour to understanding malaria transmission dynamics, relatively few studies were identified that included it. Further, differences
malaria 42373 small set of survey questions with uniform phraseology would allow for comparison of human exposure to malaria vectors across settings and over time on a large scale, as well as the evaluation of vector control
malaria 42760 integrated with indoor and outdoor biting rates to calculate a weighted estimate of human exposure to malaria vectors indoors and outdoors. Information on the proportion of the population under an ITN and sleeping
malaria 42890 outdoors. Information on the proportion of the population under an ITN and sleeping during times when malaria vectors are active can provide higher-resolution information on exposure by accounting for ITN use.
malaria 43051 information on exposure by accounting for ITN use. These data can be used to quantify human exposure to malaria vectors occurring indoors and outdoors, exposure prevented by current ITN use practices, potential gains
malaria 45452 behavioural research to better understand night time activities and sleeping patterns as they relate to malaria risk. Moving forward, entomological studies should include parallel human behavioural research. A standardized

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