Microbiological contamination of young children’s hands in rural Bangladesh: Associations with child age and observed hand cleanliness as proxy


Autoři: Sarker Masud Parvez aff001;  Rashidul Azad aff001;  Amy J. Pickering aff002;  Laura H. Kwong aff003;  Benjamin F. Arnold aff004;  Musarrat Jabeen Rahman aff001;  Md. Zahidur Rahman aff001;  Mahfuja Alam aff001;  Debashis Sen aff001;  Sharmin Islam aff001;  Mahbubur Rahman aff001;  John M. Colford, Jr. aff004;  Stephen P. Luby aff003;  Leanne Unicomb aff001;  Ayse Ercumen aff004
Působiště autorů: International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh aff001;  School of Engineering, Tufts University, Medford, MA, United States of America aff002;  Stanford University, Stanford, CA, United States of America aff003;  Division of Epidemiology and Biostatistics, School of Public Health, University of California, Berkeley, CA, United States of America aff004;  North Carolina State University, Raleigh, NC, United States of America aff005
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222355

Souhrn

Background

Hands are a route of transmission for fecal-oral pathogens. This analysis aimed to assess associations between hand E. coli contamination and child age and determine if observed hand cleanliness can serve as a proxy for E. coli contamination on young children’s hands.

Methods

Trained field workers collected hand rinse samples from children aged 1–14 months in 584 households in rural Bangladesh and assessed the visual cleanliness of child hands (fingernails, finger pads and palms). Samples were analyzed using the IDEXX most probable number (MPN) methodto enumerate E. coli. We assessed if child age (immobile children aged 1–4 months vs. mobile children aged 5–14 months) is associated with log10 E. coli counts on hands using generalized estimating equations (GEE). We estimated the log10 difference in hand E. coli counts associated with the cleanliness of different hand parts using a multivariable GEE model.We calculated the sensitivity, specificity, positive predictive value (PPV) and negative predictive value (NPV) for dirty fingernails, fingerpads, palms and overall hands (the three observed parts combined) against binary E. coli presence on hands.

Results

E. coli was detected on 43% of child hands. Children in the mobile age range had 0.17 log10 MPN higher E. coli on hands than those in the immobile age range (Δlog10 = 0.17, 95% CI = 0.02, 0.32, p = 0.03). Children with visible dirt particles on finger pads had 0.46 log10 MPN higher E. coli on hands than those with clean finger pads (Δlog10 = 0.46, 95% CI = 0.05, 0.87, p = 0.03). Dirty fingernails indicated binary E. coli presence with 81% sensitivity and 26% specificity while dirty fingerpads and palms indicated E. coli presence with 29% sensitivity and 75–77% specificity. The PPV was 45–48% and NPV 59–65% for all three types of observations.

Conclusion

Hand contamination with E. coli was prevalent among young children in rural Bangladesh, with higher levels of contamination among mobile children. Studies should assess if strategies to remove animal feces from the courtyard, provide designated hygienic play spaces for children and deliver targeted messaging to mothers to wipe or wash children’s hands after contact with animals and animal feces reduce child hand contamination. Visible hand cleanliness was a poor predictor of E. coli presence on young children’s hands so other low-cost field measurements are needed to accurately detect fecal contamination on hands.

Klíčová slova:

Biology and life sciences – Anatomy – Musculoskeletal system – Body limbs – Fingers – Microbiology – Medical microbiology – Microbial pathogens – Bacterial pathogens – Organisms – Eukaryota – Animals – Animal types – Domestic animals – Zoology – Medicine and health sciences – Arms – Health care – Environmental health – Sanitation – Public and occupational health – Hygiene – Pathology and laboratory medicine – Pathogens – People and places – Population groupings – Age groups – Children – Families – Geographical locations – Asia – Bangladesh


Zdroje

1. Eisenberg JN, Scott JC, Porco T. Integrating disease control strategies: balancing water sanitation and hygiene interventions to reduce diarrheal disease burden. American Journal of Public Health. 2007; 97 (5):846–52. doi: 10.2105/AJPH.2006.086207 17267712

2. Kawata K. Water and other environmental interventions—the minimum investment concept. The American journal of clinical nutrition. 1978; 31(11):2114–23. doi: 10.1093/ajcn/31.11.2114 102181

3. Aiello AE, Larson EL. What is the evidence for a causal link between hygiene and infections? The Lancet infectious diseases. 2002; 2(2):103–10. https://doi.org/10.1016/S1473-3099(02)00184-6. 11901641

4. Pickering AJ, Davis J, Walters SP, Horak HM, Keymer DP, Mushi D, et al. Hands, water, and health: fecal contamination in Tanzanian communities with improved, non-networked water supplies. Environmental science & technology. 2010; 44 (9):3267–72. 10.1021/es903524m 20222746

5. Schriewer A, Odagiri M, Wuertz S, Misra PR, Panigrahi P, Clasen T, et al. Human and animal fecal contamination of community water sources, stored drinking water and hands in rural India measured with validated microbial source tracking assays. The American journal of tropical medicine and hygiene. 2015;93(3):509–16. 10.4269/ajtmh.14-0824 26149868

6. Utsi L, Smith S, Chalmers R, Padfield S. Cryptosporidiosis outbreak in visitors of a UK industry-compliant petting farm caused by a rare Cryptosporidium parvum subtype: a case-control study. Epidemiology & Infection. 2016;144(5):1000–9. 10.1017/S0950268815002319 26424385

7. Khanum H, Islam MR, Parvin S. Occurrences of eggs and larvae of gastrointestinal nematodes in nails of street inhabitants in Dhaka City. Journal of Life and Earth Science. 2010;5:75–9. https://doi.org/10.3329/jles.v5i0.7354.

8. Ansari S, Sattar S, Springthorpe V, Wells G, Tostowaryk W. Rotavirus survival on human hands and transfer of infectious virus to animate and nonporous inanimate surfaces. Journal of clinical microbiology. 1988;26(8):1513–8.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC266652/pdf/jcm00080-0089.pdf 2844846

9. Kwong LH, Ercumen A, Pickering AJ, Unicomb L, Davis J, Luby SP. Hand-and object-mouthing of rural Bangladeshi children 3–18 months old. International journal of environmental research and public health. 2016;13(6):563. 10.3390/ijerph13060563 27271651

10. Parvez SM, Kwong L, Rahman MJ, Ercumen A, Pickering AJ, Ghosh PK, et al. Escherichia coli contamination of child complementary foods and association with domestic hygiene in rural Bangladesh. Tropical Medicine & International Health. 2017. 10.1111/tmi.12849 28164415

11. George CM, Oldja L, Biswas S, Perin J, Lee GO, Kosek M, et al. Geophagy is associated with environmental enteropathy and stunting in children in rural Bangladesh. The American journal of tropical medicine and hygiene. 2015;92(6):1117–24. 10.4269/ajtmh.14-0672 25918214

12. Ercumen A, Pickering AJ, Kwong LH, Arnold B, Parvez SM, Alam M, et al. Animal feces contribute to domestic fecal contamination: Evidence from E. coli measured in water, hands, food, flies and soil in Bangladesh. Environmental Science & Technology. 2017. 10.1021/acs.est.7b01710 28686435

13. Harris AR, Pickering AJ, Harris M, Doza S, Islam MS, Unicomb L, et al. Ruminants contribute fecal contamination to the urban household environment in Dhaka, Bangladesh. Environmental science & technology. 2016;50(9):4642–9. 10.1021/acs.est.5b06282 27045990

14. Julian TR. Environmental transmission of diarrheal pathogens in low and middle income countries. Environmental Science: Processes & Impacts. 2016;18(8):944–55. 10.1039/c6em00222f 27384220

15. Rusin P, Maxwell S, Gerba C. Comparative surface‐to‐hand and fingertip‐to‐mouth transfer efficiency of gram‐positive bacteria, gram‐negative bacteria, and phage. Journal of Applied Microbiology. 2002;93(4):585–92.http://login.research4life.org/tacsgr1doi_org/10.1046/j.1365-2672.2002.01734.x 12234341

16. Aiello AE, Coulborn RM, Perez V, Larson EL. Effect of hand hygiene on infectious disease risk in the community setting: a meta-analysis. American journal of public health. 2008;98(8):1372–81. 10.2105/AJPH.2007.124610 18556606

17. Freeman MC, Stocks ME, Cumming O, Jeandron A, Higgins J, Wolf J, et al. Systematic review: hygiene and health: systematic review of handwashing practices worldwide and update of health effects. Tropical Medicine & International Health. 2014;19(8):906–16. 10.1111/tmi.12339 24889816

18. Ram P. Practical guidance for measuring handwashing behavior. Washington, DC: Water and Sanitation Program. 2010.https://openknowledge.worldbank.org/bitstream/handle/10986/19005/596450WP0Pract101public10BOX353742B.pdf?sequence=1&isAllowed=y

19. Halder AK, Tronchet C, Akhter S, Bhuiya A, Johnston R, Luby SP. Observed hand cleanliness and other measures of handwashing behavior in rural Bangladesh. BMC Public Health. 2010;10. 10.1186/1471-2458-10-545 20828412

20. Morrill VN, de Aceituno AMF, Bartz FE, Heredia N, Garcia S, Shumaker DJ, et al. Visible Soil as an Indicator of Bacteria Concentration on Farmworkers’ Hands. Food Protection Trends. 2018;38(2):122–8.

21. Onis M. WHO Motor Development Study: windows of achievement for six gross motor development milestones. Acta paediatrica. 2006;95(S450):86–95. 10.1080/08035320500495563

22. Fujioka R, Sian‐Denton C, Borja M, Castro J, Morphew K. Soil: the environmental source of Escherichia coli and enterococci in Guam's streams. Journal of applied microbiology. 1998;85(S1). 10.1111/j.1365-2672.1998.tb05286.x 21182696

23. Hardina C, Fujioka R. Soil: the environmental source of Escherichia coli and enterococci in Hawaii's streams. Environmental toxicology and water quality. 1991;6(2):185–95. https://doi.org/10.1002/tox.2530060208

24. Soller JA, Schoen ME, Bartrand T, Ravenscroft JE, Ashbolt NJ. Estimated human health risks from exposure to recreational waters impacted by human and non-human sources of faecal contamination. Water Research. 2010;44(16):4674–91. 10.1016/j.watres.2010.06.049 20656314

25. Pickering AJ, Ercumen A, Arnold BF, Kwong LH, Parvez SM, Alam M, et al. Fecal indicator bacteria along multiple environmental transmission pathways (water, hands, food, soil, flies) and subsequent child diarrhea in rural Bangladesh. Environmental science & technology. 2018. 10.1021/acs.est.8b00928 29902374

26. Arnold BF, Null C, Luby SP, Unicomb L, Stewart CP, Dewey KG, et al. Cluster-randomised controlled trials of individual and combined water, sanitation, hygiene and nutritional interventions in rural Bangladesh and Kenya: the WASH Benefits study design and rationale. BMJ Open. 2013;3. 10.1136/bmjopen-2013003476

27. Pickering AJ, Boehm AB, Mwanjali M, Davis J. Efficacy of waterless hand hygiene compared with handwashing with soap: a field study in Dar es Salaam, Tanzania. The American journal of tropical medicine and hygiene. 2010;82(2):270–8. 10.4269/ajtmh.2010.09-0220 20134005

28. Julian TR, Islam MA, Pickering AJ, Roy S, Fuhrmeister ER, Ercumen A, et al. Genotypic and phenotypic characterization of Escherichia coli isolates from feces, hands, and soils in rural Bangladesh via the Colilert Quanti-tray System. Applied and environmental microbiology. 2015;81(5):1735–43. 10.1128/AEM.03214-14 25548044

29. Kwong LH, Ercumen A, Pickering AJ, Unicomb L, Davis J, Luby SP. Age-related changes to environmental exposure: variation in the frequency that young children place hands and objects in their mouths. Journal of Exposure Science & Environmental Epidemiology. 2019:1. https://doi.org/10.1038/s41370-019-0115-8

30. Nizame FA, Leontsini E, Luby SP, Nuruzzaman M, Parveen S, Winch PJ, et al. Hygiene practices during food preparation in rural Bangladesh: opportunities to improve the impact of Handwashing interventions. The American journal of tropical medicine and hygiene. 2016;95(2):288–97. 10.4269/ajtmh.15-0377 27296388

31. Aini I. Indigenous chicken production in South-east Asia. World's Poultry Science Journal. 1990;46(1):51–7. https://doi.org/10.1079/WPS19900010.

32. UNICEF/MICS/DHS. The latest available MICS/DHS survey with data for each country: 2014 update. https://www.unicef.org/statistics/index_24302.html

33. Sultana R, Mondal UK, Rimi NA, Unicomb L, Winch PJ, Nahar N, et al. An improved tool for household faeces management in rural Bangladeshi communities. Tropical Medicine & International Health. 2013;18(7):854–60. 10.1111/tmi.12103 23557125

34. Ercumen A, Pickering AJ, Kwong LH, Mertens A, Arnold BF, Benjamin-Chung J, et al. Do Sanitation Improvements Reduce Fecal Contamination of Water, Hands, Food, Soil, and Flies? Evidence from a Cluster-Randomized Controlled Trial in Rural Bangladesh. Environmental science & technology. 2018;52(21):12089–97. 10.1021/acs.est.8b02988 30256095

35. Reid B, Seu R, Orgle J, Roy K, Pongolani C, Chileshe M, et al. A Community-Designed Play-Yard Intervention to Prevent Microbial Ingestion: A Baby Water, Sanitation, and Hygiene Pilot Study in Rural Zambia. The American journal of tropical medicine and hygiene. 2018;99(2):513–25. https://doi.org/10.4269/ajtmh.17-0780 10.4269/ajtmh.17-0780 29869596

36. Callaghan J, Hyder AA, Khan R, Blum L, Arifeen S, Baqui AH. Child supervision practices for drowning prevention in rural Bangladesh: A pilot study of supervision tools. Journal of Epidemiology & Community Health. 2010;64(7):645–7. http://dx.doi.org/10.1136/jech.2008.080903

37. Humphrey JH, Mbuya MN, Ntozini R, Moulton LH, Stoltzfus RJ, Tavengwa NV, et al. Independent and combined effects of improved water, sanitation, and hygiene, and improved complementary feeding, on child stunting and anaemia in rural Zimbabwe: a cluster-randomised trial. The Lancet Global Health. 2019;7(1):e132–e47. https://doi.org/10.1093/cid/civ844. 10.1016/S2214-109X(18)30374-7 30554749

38. Ram PK, Jahid I, Halder AK, Nygren B, Islam MS, Granger SP, et al. Variability in hand contamination based on serial measurements: implications for assessment of hand-cleansing behavior and disease risk. The American journal of tropical medicine and hygiene. 2011;84(4):510–6. 10.4269/ajtmh.2011.10-0299 21460002

39. Pickering AJ, Julian TR, Mamuya S, Boehm AB, Davis J. Bacterial hand contamination among Tanzanian mothers varies temporally and following household activities. Tropical Medicine & International Health. 2011;16(2):233–9. 10.1111/j.1365-3156.2010.02677.x 21091858

40. Wu J, Long S, Das D, Dorner S. Are microbial indicators and pathogens correlated? A statistical analysis of 40 years of research. Journal of water and health. 2011;9(2):265–78. 10.2166/wh.2011.117 21942192

41. Gruber JS, Ercumen A, Colford JM Jr. Coliform bacteria as indicators of diarrheal risk in household drinking water: systematic review and meta-analysis. PloS one. 2014;9(9):e107429. 10.1371/journal.pone.0107429 25250662

42. Ram P. Practical guidance for measuring handwashing behavior: 2013 update. Washington, DC: Water and Sanitation Program. 2013. https://www.wsp.org/sites/wsp/files/publications/WSP-Practical-Guidance-Measuring-Handwashing-Behavior-2013-Update.pdf

43. Fuller C, Besser S, Cookson BD, Fragaszy E, Gardiner J, McAteer J, et al. Assessment of blinding of hand hygiene observers in randomized controlled trials of hand hygiene interventions. American journal of infection control. 2010;38(4):332–4. 10.1016/j.ajic.2009.10.005 20189686

44. Arnold BF, Khush RS, Ramaswamy P, Rajkumar P, Durairaj N, Ramaprabha P, et al. Reactivity in rapidly collected hygiene and toilet spot check measurements: a cautionary note for longitudinal studies. The American journal of tropical medicine and hygiene. 2015;92(1):159–62. 10.4269/ajtmh.14-0306 25385856


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