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      Reducing Occurrence of Giardia duodenalis in Children Living in Semiarid Regions: Impact of a Large Scale Rainwater Harvesting Initiative

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          Abstract

          Background

          In Brazil, about two million people living in rural semiarid regions were benefited with the construction of rainwater cement cisterns, as an initiative from the program “One Million Cisterns” (P1MC). Nevertheless, few epidemiological studies have been conducted to assess health risks or protection effects associated with consumption of this water source. The aim of this study was to evaluate whether access to rainwater harvesting cisterns is associated with the decrease in the occurrence of Giardia duodenalis infections in children, compared to other children living in households supplied by other water sources.

          Methodology/Principal Findings

          A quasi-experimental study with two concurrent cohorts was developed in two rural municipalities of the semiarid region of Brazil. A sample of 664 children, aged between 4 months and 5 years old, was followed up, of which 332 had access to rainwater cisterns (cistern group) and 332 did not, having water supplied from alternative sources (comparison group). In a period of approximately one year (2010) intestinal parasites were investigated in feces three times. The prevalence of G. duodenalis in children from the cistern group ranged from 4.8 to 10.5%, while the prevalence in the comparison group ranged from 7.6 to 16.7%. Multivariate analysis (GEE) showed a higher risk of G. duodenalis infection in children who did not have access to rainwater cisterns, when compared to children who did (OR 1.72; 95% CI 1.14–2.59). The other variables associated with G. duodenalis infection were: number of rooms per house (OR 0.89; 95% CI 0.80–0.99); family income (OR0.48; 95% CI 0.26–0.88); birth order (OR 1.72; 95% CI 1.17–2.51); preterm children (OR 1.70; 95% CI 1.19–2.43); and improper hand hygiene prior to food preparation (OR 4.78; 95% CI 1.95–11.76).

          Conclusions/Significance

          Ownership of a rainwater cistern is associated with a lower prevalence of G. duodenalis infection in children after adjustment for environmental and family-related factors. Nevertheless, the study suggests the necessity to complement physical interventions with actions related to personal and domestic hygiene to enable further reductions in parasite infections affecting mainly the underprivileged populations.

          Author Summary

          Currently, rainwater harvesting cisterns built up through the “One Million Cisterns” Program, coordinated by the Brazilian Government, represents the most important public policy for water supply in the rural semiarid region of Brazil. Despite the extensive use of this water provision, few studies have been performed to assess the associated health impact. To assess such impact, this study investigated factors associated with the occurrence of Giardia duodenalis (protozoan closely related to the ingestion of contaminated water) in children aged between 4 months and five years old. Two distinct groups of children, one with access to rainwater cisterns (cistern group) and the other without cisterns, with water supplied from alternative sources, including rivers, springs or dams (comparison group) were followed up for approximately one year. It was observed that the risk occurrence of G. duodenalis prevalence was greater in children from the comparison group, when compared with those from the cistern group, indicating that the odds of infection by this parasite were 1.72 times greater for comparison group children. In conclusion, the study showed health benefits related to rainwater cisterns, but also identified that other complementary sanitation interventions are needed to minimize the risk of disease in populations with limited access to drinking water.

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          Most cited references25

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          Health risk from the use of roof-harvested rainwater in Southeast Queensland, Australia, as potable or nonpotable water, determined using quantitative microbial risk assessment.

          A total of 214 rainwater samples from 82 tanks were collected in urban Southeast Queensland (SEQ) in Australia and analyzed for the presence and numbers of zoonotic bacterial and protozoal pathogens using binary PCR and quantitative PCR (qPCR). Quantitative microbial risk assessment (QMRA) analysis was used to quantify the risk of infection associated with the exposure to potential pathogens from roof-harvested rainwater used as potable or nonpotable water. Of the 214 samples tested, 10.7%, 9.8%, 5.6%, and 0.4% were positive for the Salmonella invA, Giardia lamblia β-giardin, Legionella pneumophila mip, and Campylobacter jejuni mapA genes, respectively. Cryptosporidium parvum oocyst wall protein (COWP) could not be detected. The estimated numbers of Salmonella, G. lamblia, and L. pneumophila organisms ranged from 6.5 × 10¹ to 3.8 × 10² cells, 0.6 × 10⁰ to 3.6 × 10⁰ cysts, and 6.0 × 10¹ to 1.7 × 10² cells per 1,000 ml of water, respectively. Six risk scenarios were considered for exposure to Salmonella spp., G. lamblia, and L. pneumophila. For Salmonella spp. and G. lamblia, these scenarios were (i) liquid ingestion due to drinking of rainwater on a daily basis, (ii) accidental liquid ingestion due to hosing twice a week, (iii) aerosol ingestion due to showering on a daily basis, and (iv) aerosol ingestion due to hosing twice a week. For L. pneumophila, these scenarios were (i) aerosol inhalation due to showering on a daily basis and (ii) aerosol inhalation due to hosing twice a week. The risk of infection from Salmonella spp., G. lamblia, and L. pneumophila associated with the use of rainwater for showering and garden hosing was calculated to be well below the threshold value of one extra infection per 10,000 persons per year in urban SEQ. However, the risk of infection from ingesting Salmonella spp. and G. lamblia via drinking exceeded this threshold value and indicated that if undisinfected rainwater is ingested by drinking, then the incidences of the gastrointestinal diseases salmonellosis and giardiasis are expected to range from 9.8 × 10° to 5.4 × 10¹ (with a mean of 1.2 × 10¹ from Monte Carlo analysis) and from 1.0 × 10¹ to 6.5 × 10¹ cases (with a mean of 1.6 × 10¹ from Monte Carlo analysis) per 10,000 persons per year, respectively, in urban SEQ. Since this health risk seems higher than that expected from the reported incidences of gastroenteritis, the assumptions used to estimate these infection risks are critically examined. Nonetheless, it would seem prudent to disinfect rainwater for use as potable water.
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            Real-time PCR detection of pathogenic microorganisms in roof-harvested rainwater in Southeast Queensland, Australia.

            In this study, the microbiological quality of roof-harvested rainwater was assessed by monitoring the concentrations of Escherichia coli, enterococci, Clostridium perfringens, and Bacteroides spp. in rainwater obtained from tanks in Southeast Queensland, Australia. Samples were also tested using real-time PCR (with SYBR Green I dye) for the presence of potential pathogenic microorganisms. Of the 27 rainwater samples tested, 17 (63%), 21 (78%), 13 (48%), and 24 (89%) were positive for E. coli, enterococci, C. perfringens, and Bacteroides spp., respectively. Of the 27 samples, 11 (41%), 7 (26%), 4 (15%), 3 (11%), and 1 (4%) were PCR positive for the Campylobacter coli ceuE gene, the Legionella pneumophila mip gene, the Aeromonas hydrophila lip gene, the Salmonella invA gene, and the Campylobacter jejuni mapA gene. Of the 21 samples tested, 4 (19%) were positive for the Giardia lamblia beta-giardin gene. The binary logistic regression model indicated a positive correlation (P < 0.02) between the presence/absence of enterococci and A. hydrophila. In contrast, the presence/absence of the remaining potential pathogens did not correlate with traditional fecal indicators. The poor correlation between fecal indicators and potential pathogens suggested that fecal indicators may not be adequate to assess the microbiological quality of rainwater and consequent health risk.
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              A comparative study of the TF-Test®, Kato-Katz, Hoffman-Pons-Janer, Willis and Baermann-Moraes coprologic methods for the detection of human parasitosis

              This study compares the diagnostic accuracy of the TF-Test® (TFT) for human parasitosis with results obtained using the traditional Kato-Katz (KK), Hoffman-Pons-Janer (HPJ), Willis and Baermann-Moraes (BM) techniques. Overall, four stool samples were taken from each individual; three alternate-day TFT stool samples and another sample that was collected in a universal container. Stool samples were taken from 331 inhabitants of the community of Quilombola Santa Cruz. The gold standard (GS) for protozoa detection was defined as the combined results for TFT, HPJ and Willis coproscopic techniques; for helminth detection, GS was defined as the combined results for all five coproscopic techniques (TFT, KK, HPJ, Willis and BM). The positivity rate of each method was compared using the McNemar test. While the TFT exhibited similar positivity rates to the GS for Entamoeba histolytica/dispar (82.4%) and Giardia duodenalis (90%), HPJ and Willis techniques exhibited significantly lower positivity rates for these protozoa. All tests exhibited significantly lower positivity rates compared with GS for the diagnosis of helminths. The KK technique had the highest positivity rate for diagnosing Schistosoma mansoni (74.6%), while the TFT had the highest positivity rates for Ascaris lumbricoides (58.1%) and hookworm (75%); HPJ technique had the highest positivity rate for Strongyloides stercoralis (50%). Although a combination of tests is the most accurate method for the diagnosis of enteral parasites, the TFT reliably estimates the prevalence of protozoa and selected helminths, such as A. lumbricoides and hookworm. Further studies are needed to evaluate the detection accuracy of the TFT in samples with varying numbers of parasites.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                June 2014
                19 June 2014
                : 8
                : 6
                : e2943
                Affiliations
                [1 ]School of Engineering; Department of Sanitary and Environmental Engineering – Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
                [2 ]Department of Parasitology; Institute of Biological Sciences and Graduate Program in Health Sciences: Infectious Diseases and Tropical Medicine – Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
                [3 ]Department of Statistics; Institute of Mathematical Sciences – Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
                [4 ]Laboratory of Parasitology – Universidade Presidente Antônio Carlos, Teófilo Otoni, Minas Gerais, Brazil
                [5 ]London School of Hygiene and Tropical Medicine, London, United Kingdom
                Emory University, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: LH MC. Performed the experiments: JEF JLP. Analyzed the data: JEF EAC AGFCdC NBdS. Contributed reagents/materials/analysis tools: LEM. Wrote the paper: JEF MC LH JLP SC.

                Article
                PNTD-D-13-00434
                10.1371/journal.pntd.0002943
                4063750
                24945928
                6374769e-d8c6-4932-859f-ba27d5c9667e
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 24 March 2013
                : 1 May 2014
                Page count
                Pages: 10
                Funding
                This work was supported by the National Council for Scientific and Technological Development (CNPq Brazil). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Engineering and Technology
                Environmental Engineering
                Water Management
                Sanitary Engineering
                Medicine and Health Sciences
                Epidemiology
                Environmental Epidemiology
                Infectious Disease Epidemiology
                Health Care
                Environmental Health
                Pediatrics
                Child Health
                Public and Occupational Health

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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