Occupational exposure to pesticides and neurobehavioral outcomes. Impact of different original and recalled exposure measures on the associations.

BACKGROUND: Several measures of occupational exposure to pesticides have been used to study associations between exposure to pesticides and neurobehavioral outcomes. This study assessed the impact of different exposure measures for glyphosate and mancozeb on the association with neurobehavioral outcomes based on original and recalled self-reported data with 246 smallholder farmers in Uganda. METHODS: The association between the 6 exposure measures and 6 selected neurobehavioral test scores was investigated using linear multivariable regression models. Exposure measures included original exposure measures for the previous year in 2017: (i) application status (yes/no), (ii) number of application days, (iii) average exposure-intensity scores (EIS) of an application and (iv) number of EIS-weighted application days. Two additional measures were collected in 2019: (v) recalled application status and (vi) recalled EIS for the respective periods in 2017. RESULTS: Recalled applicator status and EIS were between 1.2 and 1.4 times more frequent and higher for both pesticides than the original application status and EIS. Adverse associations between the different original measures of exposure to glyphosate and 4 neurobehavioral tests were observed. Glyphosate exposure based on recalled information and all mancozeb exposure measures were not associated with the neurobehavioral outcomes. CONCLUSIONS: The relation between the different original self-reported glyphosate exposure measures and neurobehavioral test scores appeared to be robust. When based on recalled exposure measures, associations observed with the original exposure measures were no longer present. Therefore, future epidemiological studies on self-reported exposure should critically evaluate the potential bias towards the null in observed exposure-response associations.

Evaluating and Enhancing an Educational Intervention to Reduce Smallholder Farmers' Exposure to Pesticides in Uganda Through a Digital, Systematic Approach to Behavior Change: Protocol for a Cluster-Randomized Controlled Trial.

BACKGROUND: Smallholder farmers receive educational interventions on safe pesticide handling by governmental agencies, industries, or nongovernmental organizations to reduce exposure risks. However, existing educational interventions have limited effects on changing behaviors. Targeting psychosocial determinants of behavior change in educational interventions through theory- and evidence-based approaches may enhance their effectiveness. OBJECTIVE: We aim at describing the intervention development and study design of a 3-arm cluster-randomized controlled trial to assess the effects in improving safe pesticide handling and reducing pesticide exposure of (1) an existing educational intervention and (2) a newly developed SMS text messaging intervention based on the Risks, Attitudes, Norms, Abilities, and Self-regulation (RANAS) behavior change approach. METHODS: We enrolled 539 Ugandan smallholder farmers in 12 clusters (subcounties). The clusters, each with 45 farmers, were randomly allocated to one of the three arms: (1) educational intervention, (2) educational intervention+RANAS-based SMS text messages, or (3) control group. The educational intervention comprised a 2-day workshop that targeted multiple aspects of safe pesticide handling, whereas the SMS text messages targeted the use of personal protective equipment (PPE) and were based on the RANAS approach. For intervention development in this study, this approach includes identifying psychosocial determinants of PPE use at baseline and selecting behavior change techniques to target them in SMS text messages. The primary outcomes of the study are (1) pesticide knowledge, attitude, and practice scores indicating performance throughout the educational intervention; and (2) frequency of PPE use. Secondary outcomes are the RANAS-based behavioral determinants of PPE use, the frequency of glove use, algorithm-based pesticide exposure intensity scores, and signs and symptoms of pesticide poisoning. The outcomes were assessed in structured interviews before the intervention (baseline) and at the 12-month follow-up. The effect of the interventions among the arms will be analyzed using the intervention arms and baseline measures as predictors and the follow-up measures as outcomes in linear multivariable mixed models including the clusters as random effects. The mediating psychosocial determinants of the interventions will be assessed in multiple mediation models. RESULTS: The study was conducted from 2020 to 2021-baseline interviews were conducted in October 2020, and the educational intervention was delivered in November 2020. The RANAS-based SMS text messages were developed based on the baseline data for relevant behavioral determinants of PPE use and sent between February 2021 and September 2021. Follow-up interviews were conducted in October 2021. Overall, 539 farmers were enrolled in the study at baseline; 8.3% (45/539) were lost to follow-up by the end of the study. CONCLUSIONS: This study will contribute to a better understanding of the effectiveness and behavior change mechanisms of educational interventions by using an experimental, cluster-randomized study design to improve pesticide handling among smallholder farmers. TRIAL REGISTRATION: International Standard Randomised Controlled Trial Number (ISRCTN) 18237656; https://doi.org/10.1186/ISRCTN18237656. INTERNATIONAL REGISTERED REPORT IDENTIFIER (IRRID): DERR1-10.2196/55238.

Factors influencing occupational exposure to pyrethroids and glyphosate: An analysis of urinary biomarkers in Malaysia, Uganda and the United Kingdom.

BACKGROUND: Long-term exposure to pesticides is often assessed using semi-quantitative models. To improve these models, a better understanding of how occupational factors determine exposure (e.g., as estimated by biomonitoring) would be valuable. METHODS: Urine samples were collected from pesticide applicators in Malaysia, Uganda, and the UK during mixing/application days (and also during non-application days in Uganda). Samples were collected pre- and post-activity on the same day and analysed for biomarkers of active ingredients (AIs), including synthetic pyrethroids (via the metabolite 3-phenoxybenzoic acid [3-PBA]) and glyphosate, as well as creatinine. We performed multilevel Tobit regression models for each study to assess the relationship between exposure modifying factors (e.g., mixing/application of AI, duration of activity, personal protective equipment [PPE]) and urinary biomarkers of exposure. RESULTS: From the Malaysia, Uganda, and UK studies, 81, 84, and 106 study participants provided 162, 384 and 212 urine samples, respectively. Pyrethroid use on the sampling day was most common in Malaysia (n = 38; 47%), and glyphosate use was most prevalent in the UK (n = 93; 88%). Median pre- and post-activity 3-PBA concentrations were similar, with higher median concentrations post-compared to pre-activity for glyphosate samples in the UK (1.7 to 0.5 µg/L) and Uganda (7.6 to 0.8 µg/L) (glyphosate was not used in the Malaysia study). There was evidence from individual studies that higher urinary biomarker concentrations were associated with mixing/application of the AI on the day of urine sampling, longer duration of mixing/application, lower PPE protection, and less education/literacy, but no factor was consistently associated with exposure across biomarkers in the three studies. CONCLUSIONS: Our results suggest a need for AI-specific interpretation of exposure modifying factors as the relevance of exposure routes, levels of detection, and farming systems/practices may be very context and AI-specific.

Consumer risk perception towards pesticide-stained tomatoes in Uganda.

BACKGROUND: Tomatoes are consumed daily. Unfortunately, abuse of pesticide application by vegetable growers in Uganda increases risks of pesticide residue exposure among consumers, as they may be above Maximum Residue Limits (European Union Maximum Residue Limits used as a standard in Uganda). This study aimed to determine consumer attitudes and risk perceptions towards pesticide-stained tomatoes in Uganda to support interventions that could be used to reduce pesticide residue exposures in food. METHODS: A mixed methods cross-sectional study sampled 468 household consumers in four regions of Uganda, selecting one district (interventional project area) per region. In each district, about 60 household members were randomly selected from a total of three Sub Counties and interviewed. In addition, 9 tomato handlers (three tomato farmers, three tomato retailers, and three tomato wholesalers) participated in Focus Group Discussions (FGDs) per district. Collected data were entered into MS-Excel 13 and exported into Stata version 14.0 for cleaning and analysis at a 5% level of significance and 95% Confidence Intervals (CI). The proportion of risk perceptions and attitudes were computed and presented as percentages, while factors associated with risk perception were determined using Fisher exact test. Qualitative data collected under a traditional theory were analyzed using thematic content analysis. RESULTS: More than half, 54.2% (253/468), of the respondents were females, mean age was 37 years (SD = 13.13, ranging from 18 to 88 years). Half of the respondents, 50.9% (238/467), were farmers by occupation, and 40.3% (188/468) had completed upper primary education. Only 5.0% (20/396) of consumers reported a high-risk perception towards tomatoes stained with pesticide residues, the rest, 95.0% (376/396), were buying pesticide-stained tomatoes despite their awareness of the possible health effects. The main reason for buying the pesticide-stained tomatoes was that a majority, 59.0% (230/390), lacked an alternative to stained tomatoes like organically grown tomatoes. However, consumers generally had a negative attitude towards pesticide-stained tomatoes, with 67.0% (313/468) of the consumers disagreeing with the statement that tomatoes sold on the market are safe. Consumer risk perception was significantly associated with their awareness about residues in the tomatoes; where the proportion of consumers who were aware of the risk of pesticide-stained tomatoes was 42.8 times more likely not to buy stained tomatoes compared to the proportion of those who were not aware. OR, 42.8 (95% CI: 10.76-170.28). However, after Fisher-Exact tests analysis, level of education P(0.975), gender P(0.581), and age group P(0.680) were not associated with consumer risk perception (95% CI and 5% level of significance). CONCLUSION: Although the consumers had a negative attitude towards the pesticide-stained tomatoes, their risk perception towards them ranked low, with most consumers buying tomatoes stained with pesticide residues due to a lack of an alternative. Ministry of Agriculture extension service efforts should promote and emphasize community to start household-based organic kitchen gardens as the efforts for the establishment of a national pesticide residue monitoring center awaits.

Self-reported and urinary biomarker-based measures of exposure to glyphosate and mancozeb and sleep problems among smallholder farmers in Uganda.

OBJECTIVE: We aim to showcase the impact of applying eight different self-reported and urinary biomarker-based exposure measures for glyphosate and mancozeb on the association with sleep problems in a study among 253 smallholder farmers in Uganda. METHODS: The questionnaire-based exposure measures included: (1) the number of application days of any pesticide in the last 7 days (never, 1-2; >2 days) and six glyphosate and mancozeb-specific measures: (2) application status over the last 12 months (yes/no), (3) recent application status (never, last 7 days and last 12 months), (4) the number of application days last 12 months, (5) average exposure-intensity scores (EIS) and (6) EIS-weighted number of application days in last 12 months. Based on 384 repeated urinary biomarker concentrations of ethylene thiourea (ETU) and glyphosate from 84 farmers, we also estimated (7) average biomarker concentrations for all 253 farmers. Also in the 84 farmers the measured pre-work and post-work biomarker concentrations were used (8). Multivariable logistic regression models were used to assess the association between the exposure measures and selected Medical Outcomes Study Sleep Scale (MOS-SS) indices (6-item, sleep inadequacy and snoring). RESULTS: We observed positive associations between (1) any pesticide application in the last 7 days with all three MOS-SS indices. Glyphosate application in the last 7 days (3) and mancozeb application in the last 12 months (3) were associated with the 6-item sleep problem index. The estimated average urinary glyphosate concentrations showed an exposure-response association with the 6-item sleep problem index and sleep inadequacy in the same direction as based on self-reported glyphosate application in the last 7 days. In the analysis with the subset of 84 farmers, both measured and modelled post-work urinary glyphosate concentration showed an association with snoring. CONCLUSIONS: Self-reported, estimated average biomarker concentrations and measured urinary biomarker exposure measures of glyphosate and mancozeb showed similar exposure-response associations with sleep outcomes.

Pesticides monitoring in surface water of a subsistence agricultural catchment in Uganda using passive samplers.

Pesticides are intensely used in the agricultural sector worldwide including smallholder farming. Poor pesticide use practices in this agronomic setting are well documented and may impair the quality of water resources. However, empirical data on pesticide occurrence in water bodies of tropical smallholder agriculture is scarce. Many available data are focusing on apolar organochlorine compounds which are globally banned. We address this gap by studying the occurrence of a broad range of more modern pesticides in an agricultural watershed in Uganda. During 2.5 months of the rainy season in 2017, three passive sampler systems were deployed at five locations in River Mayanja to collect 14 days of composite samples. Grab samples were taken from drinking water resources. In these samples, 27 compounds out of 265 organic pesticides including 60 transformation products were detected. In the drinking water resources, we detected eight pesticides and two insecticide transformation products in low concentrations between 1 and 50 ng/L. Also, in the small streams and open fetch ponds, detected concentrations were generally low with a few exceptions for the herbicide 2,4-D and the fungicide carbendazim exceeding 1 ug/L. The widespread occurrence of chlorpyrifos posed the largest risk for macroinvertebrates. The extensive detection of this compound and its transformation product 3,4,5-trichloro-2-pyridinol was unexpected and called for a better understanding of the use and fate of this pesticide.

Interventions to Reduce Pesticide Exposure from the Agricultural Sector in Africa: A Workshop Report.

Despite the fact that several cases of unsafe pesticide use among farmers in different parts of Africa have been documented, there is limited evidence regarding which specific interventions are effective in reducing pesticide exposure and associated risks to human health and ecology. The overall goal of the African Pesticide Intervention Project (APsent) study is to better understand ongoing research and public health activities related to interventions in Africa through the implementation of suitable target-specific situations or use contexts. A systematic review of the scientific literature on pesticide intervention studies with a focus on Africa was conducted. This was followed by a qualitative survey among stakeholders involved in pesticide research or management in the African region to learn about barriers to and promoters of successful interventions. The project was concluded with an international workshop in November 2021, where a broad range of topics relevant to occupational and environmental health risks were discussed such as acute poisoning, street pesticides, switching to alternatives, or disposal of empty pesticide containers. Key areas of improvement identified were training on pesticide usage techniques, research on the effectiveness of interventions targeted at exposure reduction and/or behavioral changes, awareness raising, implementation of adequate policies, and enforcement of regulations and processes.

Evaluation of two-year recall of self-reported pesticide exposure among Ugandan smallholder farmers.

OBJECTIVES: To evaluate smallholder farmers' recall of pesticide use and exposure determinants over a two-year period in a low-income country context. METHODS: The Pesticide Use in Tropical Settings (PESTROP) study in Uganda consists of 302 smallholder farmers who were interviewed in 2017. In the same season in 2019, these farmers were re-questioned concerning pesticide use (e.g., use of active ingredients) and exposure information (e.g., crops, personal protective equipment [PPE], hygienic behaviours) they had previously provided. The extent of recall bias was assessed by comparing responses at follow-up in 2019 with practices and behaviours reported from the baseline interview in 2017. RESULTS: An 84% (n = 255) follow-up response rate was attained. We found instances of better recall (e.g., overall agreement >70% and Area Under the Curve (AUC) values > 0.7) for the use of some active ingredients, commonly used PPE items, and washing clothes after application, whereas only 13.3% could correctly recall their three major crops. We observed a trend where more individuals reported the use of active ingredients, while fewer reported the use of PPE items, two years later. In general, we found better agreement in the recall of years working with pesticides compared to hours per day or days per week in the field, with no apparent systematic over or under reporting by demographic characteristics. CONCLUSIONS: While some of these findings provide consistency with those from high-income countries, more research is needed on recall in poorly educated agriculture communities in low- and middle-income settings to confirm these results.

Recent pesticide exposure affects sleep: A cross-sectional study among smallholder farmers in Uganda.

BACKGROUND: Poorly educated smallholder farmers in low-income countries are highly exposed to pesticides. This can result in adverse mental health issues, of which sleep problems might be an underlying indicator. We aim to examine the association between sleep problems and pesticide exposure among smallholder farmers in Uganda. METHODS: A cross-sectional survey with 253 smallholder farmers was conducted between October and December 2019. Sleep problems were assessed during the week before the visit using the Medical Outcomes Study Sleep Scale (MOS-SS). Exposure to pesticides was assessed as application days of any pesticide and as use of 2,4-D, glyphosate, mancozeb, organophosphates & carbamates, pyrethroids and other pesticides during the week and year prior to the visit. Associations were assessed using adjusted multivariable logistic regression models. RESULTS: Increased odds ratio (OR) for the sleep problem index 6-items (OR [95% Confidence Interval] 1.99 [1.04; 3.84] and 3.21 [1.33; 7.82]), sleep inadequacy (1.94 [1.04; 3.66] and 2.49 [1.05-6.22]) and snoring (3.17 [1.12; 9.41] and 4.07 [1.04; 15.14]) were observed for farmers who respectively applied pesticides up to two days and three or more days in the past week compared to farmers who did not apply during the past week. Gender-stratified analyses showed a higher OR for female applicators (4.27 [1.76-11.16]) than for male applicators (1.82 [0.91-3.79]) for the association between the sleep problem index 6-items and pesticide use in the week before the visit. Increased ORs were also observed for the association between the sleep problem index 6-item and mancozeb exposure during the past year 2.28 [1.12-4.71] and past week 2.51 [0.86-7.55] and glyphosate exposure during the past week 3.75 [1.24-11.8] compared to non-applicators. DISCUSSION: Our findings suggest an increased risk of sleep problems among smallholder farmers in a pesticide-exposure-dependent way in a low-income context. Further gender-stratified, longitudinal investigations are warranted to confirm these findings.

Exposure to multiple pesticides and neurobehavioral outcomes among smallholder farmers in Uganda.

BACKGROUND: Multiple epidemiological studies have shown that exposure to single pesticide active ingredients or chemical groups is associated with adverse neurobehavioral outcomes in farmers. In agriculture, exposure to multiple pesticide active ingredients is the rule, rather than exception. Therefore, occupational studies on neurobehavioral effects of pesticides should account for potential co-exposure confounding. METHODS: We conducted a cross-sectional study of 288 Ugandan smallholder farmers between September and December 2017. We collected data on self-reported use of pesticide products during the 12 months prior to survey and estimated yearly exposure-intensity scores for 14 pesticide active ingredients using a semi-quantitative exposure algorithm. We administered 11 neurobehavioral tests to assess five neurobehavioral domains. We implemented a Bayesian Model-Averaging (BMA) approach to examine the association between exposure to multiple pesticides and neurobehavioral outcomes, while accounting for multiple testing. We applied two levels of inference to determine (1) which neurobehavioral outcomes were associated with overall pesticide exposure (marginal inclusion probability (MIP) for covariate-only models <0.5) and (2) which specific pesticide active ingredients were associated with these outcomes (MIP for models where active ingredient was included >0.5). RESULTS: Seventy-two percent of farmers reported use of pesticide products that contained at least one of 14 active ingredients, while the applicators used in median three different active ingredients (interquartile range (IQR) 4) in the 12 months prior to the study. The most widely used active ingredients were glyphosate (79%), cypermethrin (60%), and mancozeb (55%). We found that overall pesticide exposure was associated with impaired visual memory (Benton Visual Retention Test (BVRT)), language (semantic verbal fluency test), perceptual-motor function (Finger tapping test), and complex attention problems (Trail making A test and digit symbol test). However, when we looked at the associations for individual active ingredients, we only observed a positive association between glyphosate exposure and impaired visual memory (-0.103 [95% Bayesian Credible Interval (BCI)] [-0.24, 0] units in BVRT scores per interquartile range (IQR) increase in annual exposure to glyphosate, relative to a median [IQR] of 6 [3] units in BVRT across the entire study population). CONCLUSIONS: We found that overall pesticide exposure was associated with several neurobehavioral outcome variables. However, when we examined individual pesticide active ingredients, we observed predominantly null associations, except for a positive association between glyphosate exposure and impaired visual memory. Additional epidemiologic studies are needed to evaluate glyphosate's neurotoxicity, while accounting for co-pollutant confounding.

Pesticide Research on Environmental and Human Exposure and Risks in Sub-Saharan Africa: A Systematic Literature Review.

On the African continent, ongoing agriculture intensification is accompanied by the increasing use of pesticides, associated with environmental and public health concerns. Using a systematic literature review, we aimed to map current geographical research hotspots and gaps around environmental and public health risks research of agriculture pesticides in Sub-Saharan Africa (SSA). Studies were included that collected primary data on past and current-used agricultural pesticides and assessed their environmental occurrence, related knowledge, attitude and practice, human exposure, and environmental or public health risks between 2006 and 2021. We identified 391 articles covering 469 study sites in 37 countries in SSA. Five geographical research hotspots were identified: two in South Africa, two in East Africa, and one in West Africa. Despite its ban for agricultural use, organochlorine was the most studied pesticide group (60%; 86% of studies included DDT). Current-used pesticides in agriculture were studied in 54% of the study sites (including insecticides (92%), herbicides (44%), and fungicides (35%)). Environmental samples were collected in 67% of the studies (e.g., water, aquatic species, sediment, agricultural produce, and air). In 38% of the studies, human subjects were investigated. Only few studies had a longitudinal design or assessed pesticide's environmental risks; human biomarkers; dose-response in human subjects, including children and women; and interventions to reduce pesticide exposure. We established a research database that can help stakeholders to address research gaps, foster research collaboration between environmental and health dimensions, and work towards sustainable and safe agriculture systems in SSA.

Comparative Analysis of Pesticide Use Determinants Among Smallholder Farmers From Costa Rica and Uganda.

Pesticides are used globally in agriculture and pose a threat to the health of farmers, communities, and the environment. Smallholder farmers in low- and middle-income countries have generally a low socio-economic status and educational level. Consequently, they are particularly vulnerable to negative impacts of pesticides on their health, yields, or land. In a Knowledge, Attitude, and Practices study, we compared the pest management practices between a market-oriented farming system in Zarcero County, Costa Rica, and a subsistence-based farming system in Wakiso District, Uganda. We conducted a cross-sectional survey among smallholder farmers from Costa Rica (n = 300) in 2016 and from Uganda (n = 302) in 2017. We enrolled conventional and organic farmers, but also farmers with mixed practices and non-applicators of any pest management strategy. We found that the majority of pesticides used in both case studies are classified as highly hazardous by the World Health Organization. While more than 90% of smallholder farmers from both countries were aware of the negative health effects of pesticide exposure, <11% in Costa Rica and <2% in Uganda reported using personal protective equipment every time they handled or applied pesticides. Hygiene and other safe use practices were not adopted by all farmers (<61%), especially among farmers applying more hazardous pesticides. Conventional farmers from Costa Rica (14%) and Uganda (19%) reported disposing pesticide residuals into rivers. Using a logistic regression we found that organic farmers were more likely to having been trained on safe pesticide use practices. Using a robust regression, we observed that smallholder household income was primarily driven by education and not directly by the use of synthetic pesticides. Our results suggest that negative effects of pesticides can be managed over the whole life cycle, from purchase, via storage and application to residual and waste management by fostering professionalization of farmers. We advise future safe use and handling interventions to consider the pesticide use-related socioeconomic and demographic findings highlighted in this paper.

Assessment of Dithiocarbamate Residues on Tomatoes Conventionally Grown in Uganda and the Effect of Simple Washing to Reduce Exposure Risk to Consumers.

Pesticide misuse by farmers poses health risks to consumers. This study assessed the level of dithiocarbamate residues in tomatoes acquired from 20 farmers and 25 market vendors in Wakiso District, how simple washing affects these residues, and the potential chronic health risk for Ugandans eating such tomatoes. Results revealed that mancozeb was the only reported dithiocarbamate, and 47.4% and 14% of farm and market samples, respectively, had dithiocarbamate residues exceeding the Codex alimentarius maximum residue limit of 2 mgCS2/kg. Mixing concentration had a positive significant effect on dithiocarbamate residue levels (P = 0.004). Washing reduced dithiocarbamate residues by a factor of 0.3. Dietary risk assessment revealed no chronic health risk to both children and general population when a national daily per capita consumption of 1.0 g is considered. This study recommends comprehensive research into Uganda's food production and consumption patterns and establishment of a national pesticide residue surveillance program.

Effect of Integrated Pest Management Training on Ugandan Small-Scale Farmers.

Small-scale farmers in developing countries use hazardous pesticides taking few or no safety measures. Farmer field schools (FFSs) teaching integrated pest management (IPM) have been shown to reduce pesticide use among trained farmers. This cross-sectional study compares pesticide-related knowledge, attitude, practice (KAP), potential exposure, and self-reported poisoning symptoms among 35 FFS farmers, 44 neighboring farmers, and 35 control farmers after an IPM intervention in Uganda (2011-2012). The FFS farmers were encouraged to teach their neighboring farmers. Data were based on standardized interviews and were analyzed using a linear trend test and logistic regression. The results showed that FFS and neighboring farmers used significantly fewer pesticide applications (P = .021) and used more safety measures. No differences were found on the hazardousness of pesticides used or self-reported symptoms. The study supports IPM as a method to reduce pesticide use and potential exposure and to improve pesticide-related KAP among small-scale farmers in developing countries.