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Impact of duration of structured observations on measurement of handwashing behavior at critical times

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      Abstract

      Background

      Structured observation is frequently used to measure handwashing at critical events, such as after fecal contact and before eating, but it is time-consuming. We aimed to assess the impact of reducing the duration of structured observation on the number and type of critical events observed.

      Methods

      The study recruited 100 randomly selected households, 50 for short 90-minute observations and 50 for long 5-hour observations, in six rural Bangladeshi villages. Based on the first 90 minutes in the long observation households, we estimated the number of critical events for handwashing expected, and compared the expected number to the number of events actually observed in the short observation households. In long observation households, we compared soap use at critical events observed during the first 90 minutes to soap use at events observed during the latter 210 minutes of the 5-hour duration.

      Results

      In short 90-minute observation households, the mean number of events observed was lower than the number of events expected: before eating (observed 0.25, expected 0.45, p < 0.05) and after defecation (observed 0.0, expected 0.03, p = 0.06). However, the mean number observed was higher than the expected for food preparation, food serving, and child feeding events. In long 5-hour observation households, soap was used more frequently at critical events observed in the first 90 minutes than in the remaining 210 minutes, but this difference was not significant (p = 0.29).

      Conclusions

      Decreasing the duration of handwashing significantly reduced the observation of critical events of interest to evaluators of handwashing programs. Researchers seeking to measure observed handwashing behavior should continue with prolonged duration of structured observation. Future research should develop and evaluate novel models to reduce reactivity to observation and improve the measurement of handwashing behavior.

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      Most cited references 9

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      Effect of handwashing on child health: a randomised controlled trial.

      More than 3.5 million children aged less than 5 years die from diarrhoea and acute lower respiratory-tract infection every year. We undertook a randomised controlled trial to assess the effect of handwashing promotion with soap on the incidence of acute respiratory infection, impetigo, and diarrhoea. In adjoining squatter settlements in Karachi, Pakistan, we randomly assigned 25 neighbourhoods to handwashing promotion; 11 neighbourhoods (306 households) were randomised as controls. In neighbourhoods with handwashing promotion, 300 households each were assigned to antibacterial soap containing 1.2% triclocarban and to plain soap. Fieldworkers visited households weekly for 1 year to encourage handwashing by residents in soap households and to record symptoms in all households. Primary study outcomes were diarrhoea, impetigo, and acute respiratory-tract infections (ie, the number of new episodes of illness per person-weeks at risk). Pneumonia was defined according to the WHO clinical case definition. Analysis was by intention to treat. Children younger than 5 years in households that received plain soap and handwashing promotion had a 50% lower incidence of pneumonia than controls (95% CI (-65% to -34%). Also compared with controls, children younger than 15 years in households with plain soap had a 53% lower incidence of diarrhoea (-65% to -41%) and a 34% lower incidence of impetigo (-52% to -16%). Incidence of disease did not differ significantly between households given plain soap compared with those given antibacterial soap. Handwashing with soap prevents the two clinical syndromes that cause the largest number of childhood deaths globally-namely, diarrhoea and acute lower respiratory infections. Handwashing with daily bathing also prevents impetigo.
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        Effect of washing hands with soap on diarrhoea risk in the community: a systematic review

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          The Effect of Handwashing at Recommended Times with Water Alone and With Soap on Child Diarrhea in Rural Bangladesh: An Observational Study

          Introduction Intervention trials promoting handwashing with soap in communities with high child mortality consistently report a reduction in childhood diarrheal disease [1]. Bolstered by these data, public health programs serving low-income populations commonly promote handwashing with soap. Across a wide range of low-income countries, however, handwashing with soap is uncommon. In a review of structured observations in 11 countries mothers of young children washed their hands with soap on average only 17% of the time after using the toilet [2]. Barriers to washing hands with soap in low-income communities include the high cost of soap relative to household income, the risk that soap left out in a convenient place would be wasted by children playing with it or stolen, and the time required and inconvenience of fetching soap [3],[4]. In contrast to the low frequency of handwashing with soap, handwashing with water alone is more commonly practiced. In the same 11 countries study, mothers washed their hands with water alone 45% of the time after toileting [2]. Because intervention trials of handwashing with soap consistently demonstrated a health benefit, handwashing promotion interventions focus almost exclusively on handwashing with soap [5]. A second common characteristic of handwashing promotion programs is a focus on five “key times” for handwashing. These include handwashing after defecation, after handling child feces or cleaning a child's anus who had defecated, before preparing food, before feeding a child, and before eating [5],[6]. Asking mothers of young children to wash their hands with soap after each of these critical times would typically translate into requesting busy impoverished mothers to wash their hands with soap more than ten times a day. If mothers also follow recommendations to wash hands after touching domestic animals, animal dung, potentially contaminated raw food, and after coughing or sneezing [7], the number of recommended times for handwashing with soap would often exceed 20 times per day. In low-income households, soap is used judiciously to preserve money for food and other essentials [8]. Washing hands with soap this frequently, especially if practiced by all family members, would affect household finances. In order to preserve the household supply of soap, families commonly store soap away from the most convenient place to wash hands [3]. Washing hands with soap 10 or more times per day also takes a lot of time, time that mothers in low-income settings do not have in abundance [9]. The time required for handwashing with soap is especially onerous if lathering is continued for the full recommended 20 seconds [10] and soap is not kept at the most convenient place to wash hands. A third barrier to promoting handwashing at five different key times is the complexity of the message. A critical review of health communication interventions in low-income countries concluded that interventions that focus on a few messages were more effective than communication interventions targeting many behaviors [11]. Two steps that might improve the effectiveness of handwashing promotion interventions would be to encourage handwashing only at the most critical times for interrupting pathogen transmission and clarifying whether handwashing with water alone, a behavior that is apparently much easier for people to practice, should be encouraged. There are however, few data available to guide more focused recommendations. In 2007, the Government of Bangladesh Department of Public Health Engineering in collaboration with UNICEF and with support from the Department for International Development (DFID) of the British Government launched a program, Sanitation, Hygiene Education and Water supply-Bangladesh (SHEWA-B) that is among the largest intensive handwashing, hygiene/sanitation, and water quality improvement programs ever attempted in a low-income country. The intervention targeted 20 million people in rural Bangladesh. As part of the assessment of the program's impact, fieldworkers conducted household structured observations at baseline in 50 randomly selected villages that served as nonintervention control households to compare with outcomes to communities receiving the SHEWA-B program. Community monitors assessed the frequency of diarrhea in control households each month for the subsequent 2 y. We analyzed the relationship between handwashing behavior as observed at baseline and the subsequent experience of child diarrhea in these households. The objective of this analysis was to identify which specific handwashing behaviors were associated with less diarrhea. Methods Ethics Statement UNICEF publicly requested bids for the evaluation of the SHEWA-B program. The International Centre for Diarrhoeal Disease Research, Bangladesh (ICDDR,B) was selected through a competitive process and signed a contract with UNICEF for the evaluation. From UNICEF's perspective, and the perspective of the Government of Bangladesh, this was not a research contract. It was a contract to evaluate a US$90 million program targeting 20 million people across rural Bangladesh. The Government of Bangladesh separately contracted with 58 organizations to implement the intervention across 68 rural subdistricts on an aggressive launch schedule. The program evaluation required a preintervention baseline survey. If the evaluation team postponed field work for the 12- or more wk process that is characteristic for local human study participant protocol review and approval, ICDDR,B would have been unable to provide a preintervention measurement. This would have reduced the ability of ICDDR,B to assess the program, and would represent a failure to meet contractual obligations. We received ICCDR,B administrative approval to classify this activity as a nonresearch program evaluation that did not require independent human study participant review because the primary goal of this activity, particularly from the sponsor's perspective, was program evaluation and not generation of new generalizable knowledge. The plan for the evaluation was reviewed by UNICEF and the Government of Bangladesh Department of Public Health Engineering, but was not reviewed by an independent human study participant committee. Each field worker received formal training in taking informed consent. As part of the consent process the field worker clarified how much time we were requesting from prospective participants. Field workers explained that there was no individual benefit or compensation for participation, that there would be questions about use of water, toilet facilities, and handwashing, and noted that these topics may be uncomfortable or that it may be uncomfortable to have a stranger in their home observing household activities. Twice during the consent process the field workers specified that participation was voluntary. They explained that even if the participant originally provided consent, he or she could withdraw consent at any time. Field workers secured written informed consent from each participant. Fields workers provided participants with contact information for the study coordinator and the research administration office of ICDDR,B if they had any questions. All collected information was kept in locked rooms. Only staff whose responsibilities included working with the data had access to the data. Study supervisors made unannounced visits to field teams to ensure that field workers properly implemented the enrollment and consent process. Study Population The SHEWA-B program targeted 68 subdistricts (upazilas) in 19 districts. The government and UNICEF selected the specific intervention upazilas because of the perceived need and the absence of other active programs addressing water, sanitation, and hygiene in these communities. Upazilas are further subdivided into unions. We listed all of the unions and their populations in the 68 targeted subdistricts and randomly selected 50 unions with the probability of selection proportional to the size of the union. For each SHEWA-B intervention upazila where a union was chosen for evaluation we selected a control upazila that had similar geography, hydrogeology, infrastructure, agricultural productivity, and household construction, and where the government confirmed that no other major water-sanitation-hygiene programs were ongoing. We selected unions for evaluation in the control upazilas using the same probability of selection proportional to size used to select unions for evaluation in the intervention upazilas. Within each selected union we listed all village names, and used a random number generator to select the evaluation village. Fieldworkers asked residents of the selected village to identify the village center. Fieldworkers identified the household closest to the village center that had a child 1 child <5 y of age at home 9,897 3,615 (37) 377 (10.4) 1.18 0.93–1.51 0.177 Structured Observation Before preparing food Did not wash hands 8,023 2,957 (37) 370 (12.5) — — — Washed one hand with water only 8,023 2,187 (27) 182 (8.3) 0.79 0.59–1.07 0.133 Washed both hands with water only 8,023 2,797 (35) 192 (6.9) 0.70 0.52–0.94 0.0170 Washed at least one hand with soap 8,023 82 (1) 3 (3.7) 0.32 0.23–0.44 <0.001 Following handwashing optimal hand drying observedd 5,066 589 (12) 32 (5.4) 0.92 0.58–1.47 0.735 Before feeding a child Did not wash hands 8,093 4,070 (50) 416 (10.3) — — — Washed one hand with water only 8,093 3,102 (38) 302 (9.7) 0.86 0.69–1.08 0.192 Washed both hands with water only 8,093 685 (8) 62 (9.1) 1.19 0.85–1.68 0.314 Washed at least one hand with soap 8,093 236 (3) 19 (8.1) 0.63 0.20–1.31 0.221 Following handwashing optimal hand drying observedd 4,023 301 (7.5) 20 (6.6) 0.75 0.46–1.22 0.246 Before eating Did not wash hands 9,801 516 (5) 36 (7.0) — — — Washed one hand with water only 9,801 6,956 (75) 711 (10.2) 1.12 0.60–2.10 0.719 Washed both hands with water only 9,801 2,016 (22) 172 (8.5) 0.99 0.52–1.87 0.967 Washed at least one hand with soap 9,801 313 (3) 20 (6.4) 1.23 0.61–2.49 0.569 Following handwashing optimal hand drying observedd 9,285 312 (3) 18 (6) 0.77 0.48–1.23 0.273 After cleaning child's anus who had defecated Did not wash hands 3,913 273 (7) 37 (13.6) — — — Washed one hand with water only 3,913 1,186 (30) 110 (9.3) 1.32 0.59–2.92 0.497 Washed both hands with water only 3,913 1,165 (30) 135 (11.6) 1.65 0.73–3.77 0.231 Washed at least one hand ash/mud 3,913 305 (8) 20 (6.6) 1.14 0.45–2.89 0.779 Washed at least one hand with soap 3,913 984 (25) 102 (10.4) 1.58 0.56–4.42 0.383 Following handwashing optimal hand drying observedd 3,640 619 (17) 60 (9.7) 0.85 0.49–1.46 0.546 After defecation Did not wash hands 2,976 24 (1) 0 (0) — — — Washed one hand with water onlye 2,976 1,029 (35) 135 (13) — — — Washed both hands with water only 2,976 711 (24) 76 (10.7) 0.77 0.46–1.29 0.321 Washed at least one hand ash/mud 2,976 431 (14) 30 (7.0) 0.62 0.34–1.14 0.124 Washed at least one hand with soap 2,976 781 (26) 47 (6.0) 0.45 0.26–0.77 0.003 Following handwashing optimal hand drying observedd 2,952 253 (9) 18 (7.1) 0.68 0.44–1.08 0.100 a When multiple handwash opportunities were observed in the same household, the household's handwashing behavior was classified on the basis of the most thorough handwashing behavior observed. b Adjusted for repeated measures of the same child and village clustering. c There were 24 fewer observations in the analysis with fathers' education, because there data were missing for one of the households. d Optimal hand drying (air drying or drying with a clean towel) was compared with hands not dried or dried on dirty towel or clothing; this analysis was restricted to episodes where handwashing was observed. e Washed one hand with water only was selected as the baseline category because too few people did not wash their hands at all to permit robust statistical evaluation. Mothers reported at least some breast-feeding of their <1-y-old children in the preceding 24 h in 93% of monthly visits and reported exclusive breastfeeding of their <6-mo-old children in the preceding 24 h in 55% of monthly visits. Young children were both more likely to be breastfed and more likely to have diarrhea. After adjustment for age, neither any reported breastfeeding nor exclusive breast-feeding was associated with significantly less diarrhea. Fieldworkers observed at least one opportunity to wash hands before preparing food in 281 (81%) of the households during structured observation. Handwashing before preparing food was associated with less diarrhea in the subsequent 2 y of follow-up (Table 3). In households where food was prepared without washing hands, children had diarrhea in 12.5% of monthly assessments compared with 8.3% in households where one hand was washed with water only, 6.9% where both hands were washed with water only, and 3.7% where at least one hand was washed with soap (Table 3). Food preparers commonly washed one or both hands with water only, but fieldworkers observed food preparers washing at least one hand with soap in only three households (1%). Fieldworkers observed at least one opportunity to wash hands after defecation in 102 (29%) of the households during structured observation. Fieldworkers observed only a single household where residents never washed their hands after defecation. Handwashing with soap was much more common after defecation than before food preparation. In 25% of households, at least one household resident washed at least one hand with soap after defecation. Among the 27 observed episodes of handwashing with soap after defecation, in eight (30%) both hands were washed with soap. Children who lived in households where fieldworkers observed at least one hand washed with soap after defecation experienced substantially less diarrhea in the subsequent 2 y of follow-up compared with children who lived in households where only one hand was washed with water after defecation (Table 3). The fieldworkers' observations of handwashing before feeding a child, before eating, and after cleaning a child's anus who had defecated were not associated with subsequent diarrhea (Table 3). Among household residents observed washing hands, fieldworkers observed optimal hand drying, either allowing hands to air dry or drying hands on a clean towel, uncommonly, ranging from 3% before eating to 17% after cleaning a child's anus who had defecated. Children who lived in households where optimal hand drying was observed had somewhat less diarrhea than other children, but none of the observed differences were statistically significant. In the multivariate analysis of structured observations before preparing food, washing both hands with water only and washing at least one hand with soap were both independently associated with significantly less diarrhea morbidity during 7,999 subsequent monthly assessments for diarrhea (Table 4). The number of months since initiating surveillance, child age less than 24 mo, father's education, and household ownership of a mobile phone were also independently associated with diarrhea, but the odds ratios for the structured observation of handwashing before preparing food in the multivariate analysis were nearly identical to the bivariate odds ratios. 10.1371/journal.pmed.1001052.t004 Table 4 Multivariate analysis of observed handwashing behavior and subsequent diarrhea. Characteristic Adjusted Odds Ratio (95% Confidence Limit)a p-Value Structured observation before preparing food (n = 7,999) Before preparing food  Did not wash hands – baseline — —  Washed one hand with water only 0.78 (0.57–1.05) 0.105  Washed both hands with water only 0.67 (0.51–0.889) 0.004  Washed at least one hand with soap 0.30 (0.19–0.47) <0.001 Number of months since initiating surveillance 0.96 (0.94–0.98) <0.001 Child age less than 24 mo 1.25 (1.01–1.55) 0.040 Father having education above primary level 0.72 (0.52–1.00) 0.052 Household owns a mobile phone 0.74 (0.57–0.97) 0.028 Structured observation after defecation (n = 2,952) After defecation  Washed one hand with water only—baseline — —  Washed both hands with water only 0.79 (0.46–1.35) 0.389  Washed at least one hand ash/mud 0.63 (0.34–1.16) 0.135  Washed at least one hand with soap 0.45 (0.26–0.77) 0.004 Month since initiating surveillance 0.96 (0.94–0.98) <0.001 a Odds ratio was calculated using a general estimated equations model that accounted for neighborhood clustering and repeated household sampling using a nested correlation structure. In the multivariate analysis of structured observations after defecation, washing at least one hand with soap was independently associated with significantly less diarrhea in the 2,952 subsequent monthly assessments (Table 4). With a smaller sample size, the month since initiating surveillance was the only other factor independently associated with diarrhea. The odds ratios for the structured observation of handwashing after defecation in the multivariate analysis were nearly identical to the bivariate odds ratios. Discussion In 50 villages across rural Bangladesh where fecal environmental contamination, undernutrition, and diarrhea are common, in those households where fieldworkers observed food preparers washing their hands before handling food, children under the age of 5 y experienced less diarrhea over the next 2 y compared with children living in households where food preparers did not wash their hands before preparing food. This observation suggests that before preparing food may be a particularly important time to promote handwashing [16]. Tomatoes, cucumbers, carrots, and various seasonal vegetables and greens are common components of meals in rural Bangladesh. Some of these vegetables are served raw but most are boiled and made into a curry that is commonly served with rice, the primary staple of the Bangladeshi diet. Many foods that are not further cooked, for example boiled root vegetables, fruits including bananas, and dried fish are often mashed and mixed by hand with spices and other ingredients during food preparation. Raw vegetables are commonly contaminated with pathogens and are a common vehicle for gastrointestinal pathogen transmission. Numerous outbreaks of gastroenteritis from a variety of pathogens have been traced to raw vegetables [17],[18]. The surface of raw cut lettuce and tomatoes is a hospitable environment for the growth of Shigella and Salmonella [19]–[21]. Similarly, there is considerable microbiological and epidemiological evidence that implicates cross-contamination of food as an important pathway for gastrointestinal pathogen transmission [22],[23]. Food that is inoculated with bacterial pathogens from contaminated hands may provide a nutrient rich environment that permits exponential growth for numerous pathogens [24]–[27]. The risk of diarrhea for many bacterial pathogens is proportional to the dose of the pathogens ingested [28],[29]. In several outbreaks of bacterial gastroenteritis, food that was contaminated several hours before serving was associated with high attack rates of gastroenteritis among persons who consumed it [30]. If persons preparing food did not wash their pathogen-contaminated hands before touching raw vegetables and rice, these foods may have become contaminated with gastrointestinal pathogens, which could subsequently multiply in a conducive growth environment before consumption. However, if the vegetables were cooked at a high enough temperature for a long enough time the pathogens would not survive and would not be transmitted. In future research, it would be useful to have fieldworkers specifically code the context of the handwashing opportunity around food preparation, so that the association between handwashing before handling raw vegetables and other foods that were subsequently cooked, handwashing before handling foods that were eaten raw, and handwashing before cross contaminating food that was not further cooked could be separately assessed. In contrast to standard recommendations for handwashing that stress the central importance of using soap and specify detailed techniques for washing underneath fingernails, continuing lathering for over 20 s, and using either a clean towel or air drying to ensure effective handwashing [10], in this observational study, children who lived in households where food preparers practiced suboptimal handwashing (including briefly washing their hands with water alone) experienced significantly less diarrhea than children living in households where the food preparer did not wash hands at all. Fieldworkers did not directly measure the duration of handwashing with soap in this study, but in another study that used structured observation in urban Bangladesh to assess handwashing behavior and timed the duration of handwashing with soap with a stopwatch, the baseline mean duration of handwashing with soap was 5 s before preparing food and 11 s after defecation [31]. Although the benefits of handwashing with water alone observed in this evaluation conflict with standard recommendations, they are consistent with an older randomized controlled intervention study from urban Bangladesh. Stanton and Clemens used structured observation to observe handwashing behavior and noted an association between washing hands with or without soap and reported childhood diarrhea in a case control study in low-income urban communities in Dhaka Bangladesh [32]. In a subsequent intervention study in households that received the intervention, food preparers were significantly more likely to wash their hands with or without soap compared with food preparers in nonintervention households (49% versus 33%) [32]. Intervention households reported 26% less diarrhea than nonintervention households. Microbiological studies demonstrate that washing hands with water alone reduces the concentration of various bacteria on hands [4],[33]–[35]. The reduction in these bacteria is generally less than the reduction in hand contamination following handwashing with soap [4],[33]–[36]. Field workers did not record the source of water used to wash hands, but the most common source of household water in rural Bangladesh is shallow tube wells. In other studies approximately 40% of water samples directly collected from shallow tube wells in Bangladesh were contaminated with fecal bacteria, though generally at a low-level of contamination [37],[38]. The present evaluation suggests that even the modest reduction in hand contamination achieved by washing with water alone reduces the risk of pathogen transmission at least during food preparation, albeit to a lesser degree than handwashing with soap. The low proportion of households that followed recommended hand drying procedures suggests that substantial efforts would be required to change community habits to conform with hand drying recommendations. Since children living in households that practiced recommended hand drying behavior did not have significantly less diarrhea than other households, these data suggest that efforts to promote improved hand hygiene would be better focused on behaviors more strongly associated with child health, for example on handwashing before preparing food and after defecation, than on prescribing specific hand drying behavior. People wash their hands more frequently when they know they are being observed [39]–[42]. In a previous study in rural Bangladesh that placed accelerometers within bars of soap to detect soap motion, the presence of an observer increased the frequency of soap motions consistent with handwashing by 35% [43]. Since Bangladeshi culture views adult feces as impure [8], social desirability bias may have increased observed handwashing with soap, especially after defecation. In the Bangladesh motion sensor study, residents of households with more education and who owned a mobile phone or watch were more likely to increase handwashing in the presence of an observer, and in the present study households with more education and those that owned mobile phones or televisions had less diarrhea [43]. Thus, an alternative interpretation of these observations is that the association between washing hands and subsequent childhood diarrhea is not causal. Rather, the observed reactive handwashing behavior might be an indicator of broader hygiene awareness that identified a subset of households that practiced a number of behaviors that contributed to less childhood diarrhea. But there are two difficulties with this alternative interpretation. First, the strong association of handwashing with water alone before preparing food with diarrhea is less likely to result from social desirability bias, because there is no strong cultural norm for handwashing before preparing food. Indeed, only 1% of households washed hands with soap before preparing food. If household residents washed hands before preparing food because of social desirability bias that was then linked to other behaviors associated with less diarrhea, then we would also expect to find a significant association of diarrhea with handwashing before eating, before feeding a child, and after cleaning a child who defecated, associations that were not significant in this analysis. A second difficulty with attributing the observed associations to a theoretical unknown, unnamed, and unmeasured confounder is that the analysis implies that such a causal pathway for reduced diarrhea was independent of education, wealth, exclusive breastfeeding, and other evaluated household characteristics. An unmeasured personal or household characteristic that is so powerful that it dominates the relationship between handwashing and diarrhea, but is so elusive that we cannot even name it, seems a less likely explanation than pathogen contaminated hands and food, a biologically plausible explanation that invokes a pathway of gastrointestinal pathogen transmission repeatedly demonstrated in other contexts. The observation in this evaluation that children living in households where residents washed their hands with soap after defecation had less diarrhea compared with children living in households where handwashing after defecation was less thorough is consistent with findings of previous intervention studies [1] and with handwashing interrupting the transmission of pathogens from the gastrointestinal tracts of household members to a susceptible child. The lack of a significant association of diarrhea with handwashing after cleaning a child's anus who defecated or handwashing before feeding a child or before eating also have plausible microbiological explanations. A child's gastrointestinal tract and immune system has already been exposed to the organisms in his/her own feces. Further exposure to these organisms is unlikely to cause clinical illness in the child. Unwashed hands can transmit pathogens to food, but when contaminated hands contact food at the time of eating or feeding, the dose of ingested pathogen is limited to the number of organisms that are passively transferred from hand to food. In contrast, when pathogens are transmitted to food items that are stored and not further cooked, bacterial pathogen populations may reproduce exponentially, resulting in a much higher dose of pathogen and a greater risk of diarrhea. An important limitation of this study is that measuring handwashing on a single day risks misclassifying exposure. Among mothers in Burkina Faso, observed handwashing behavior after cleaning a child who had defecated was concordant with observations on a different day between 57% and 73% of the time [44]. This imperfect repeatability of handwashing assessments risks misclassifying exposure, which reduces the statistical power to identify associations. Such misclassification could explain why handwashing at some key times was not associated with less child diarrhea in this evaluation. However, handwashing in this evaluation was not classified on the basis of a single observation, but on the basis of the best behavior observed among multiple observations within the household (Table 2). Handwashing is a habitual behavior [2]. For example, in the Burkina Faso study, not washing hands on one occasion was significantly associated with subsequent behavior [44]. Importantly, even with reduced power from misclassification, the Bangladesh evaluation presented in this article identified associations between handwashing at two biologically plausible occasions with reduced prevalence of subsequent diarrhea. A second limitation is that fieldworkers observed an opportunity to wash hands after defecation in only 29% of households. The resulting limited statistical power precluded a thorough assessment of the utility of washing hands after defecation with water only or with ash/mud, the contribution of other determinants of diarrhea, or a combined model that included both handwashing before preparing food and handwashing after defecation. However, even with limited power there was a strong association between handwashing with soap and less subsequent diarrhea, and the point estimates of the odds ratios are suggestive of less diarrhea for handwashing with water alone. A third limitation is that different gastrointestinal pathogens have different routes of transmission within different contexts, which might limit the generalizability of this study. It is possible that transmission of gastrointestinal pathogens from hands to food during preparation is a less important route of transmission in other settings. Additionally, in settings where water to wash hands is more heavily contaminated with feces than available water in rural Bangladesh, washing hands with water alone may be less protective. However this evaluation was conducted in 50 rural villages in 26 districts across Bangladesh and Bangladesh is the eighth most populous country in the world, so the analysis is not identifying a highly isolated phenomenon. In an assessment of hygiene indicators in rural Nicaragua, washing hands before preparing food was the single hygiene indicator most strongly associated with child diarrhea [16]. Nevertheless, it would be useful to conduct similar evaluations in other contexts. A fourth limitation is that the program evaluation was not designed to evaluate the hypothesis that observed handwashing behavior was associated with a change in the prevalence of subsequent diarrhea. Because this is a secondary analysis of the data, there is some risk of data mining to identify an interesting but ultimately not robust finding. However, we planned these data analyses at the time we designed the program evaluation. There was a dose effect between thoroughness of handwashing before preparing food and subsequent observed diarrhea and the associated p-values were <0.005. An important flaw in this evaluation was that we did not have the protocol reviewed by an independent human study participant committee. The amount of time we asked from participants, the intensity of the interaction with the field team, and the use of these data to draw generalizable insights to improve global scientific understanding mean that the activity had substantial research components and should have been reviewed by an independent human study participant committee. The study team did implement standard procedures to minimize risks and harms to evaluation participants, but similar future evaluations should be reviewed by human study participant committees. Rigorous evaluations of large public health programs provide insights that can translate into improved programs that save lives and improve community health. However large public health programs in low-income countries often have extremely tight implementation schedules. Human study participant committees in low-resource settings may need to develop additional capacities to provide appropriate independent review more promptly for these type of evaluations. Most people living in low-income settings have apparently concluded that following recommendations that require them to wash hands with soap ten, 20, or more times per day is not feasible [2]. The observations from this program evaluation suggest that to prevent childhood diarrhea the most important occasions for handwashing and the technique for effective handwashing differ from standard recommendations. Specifically, handwashing promotion programs in rural Bangladesh should not attempt to modify handwashing behavior at all five key times, but should focus primarily on handwashing after defecation and before food preparation. Because handwashing before food preparation is such a different context than after defecation, developing and evaluating strategies to promote handwashing before food preparation is an important area for future research. The lower prevalence of childhood diarrhea seen in this evaluation among children living in households where residents washed hands with soap are consistent with the many intervention trials that demonstrate less childhood diarrhea in households where residents are encouraged to wash hands with soap [1]. The findings from this study, that children living in households where field workers observed food preparers washing their hands with water alone before preparing food had less diarrhea compared with children living in households where fieldworkers observed that food preparers did not wash their hands, suggest that promoting handwashing exclusively with soap may be unwarranted. Handwashing with water alone might be seen as a step on the handwashing ladder: handwashing with water is good; handwashing with soap is better. Additional controlled trials evaluating the effect on child health of interventions that include encouraging handwashing either with water alone or with soap and water would be particularly helpful to guide public health programs. More generally, research to develop and evaluate handwashing messages that account for the limited time and soap supplies available for low-income families, and are focused on those behaviors where there is the strongest evidence for a health benefit could help identify more effective strategies.
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            Author and article information

            Affiliations
            [1 ]International Centre for Diarrheal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh
            [2 ]Millennium Challenge Corporation, 875 Fifteenth Street NW, Washington DC, USA
            [3 ]Stanford University, 473 Via Ortega, Stanford, CA, USA
            [4 ]University at Buffalo, 3435 Main Street, Buffalo, NY, USA
            Contributors
            Journal
            BMC Public Health
            BMC Public Health
            BMC Public Health
            BioMed Central
            1471-2458
            2013
            2 August 2013
            : 13
            : 705
            23915098
            3750651
            1471-2458-13-705
            10.1186/1471-2458-13-705
            Copyright © 2013 Halder et al.; licensee BioMed Central Ltd.

            This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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