Volume 94, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Poor sanitation could pose greater risk for enteric pathogen transmission at higher human population densities because of greater potential for pathogens to infect new hosts through environmentally mediated and person-to-person transmission. We hypothesized that incidence and prevalence of diarrhea, enteric protozoans, and soil-transmitted helminth infections would be higher in high-population-density areas compared with low-population-density areas, and that poor sanitation would pose greater risk for these enteric infections at high density compared with low density. We tested our hypotheses using 6 years of clinic-based diarrhea surveillance (2007–2013) including 4,360 geolocated diarrhea cases tested for 13 pathogens and a 2010 cross-sectional survey that measured environmental exposures from 204 households (920 people) and tested 701 stool specimens for enteric parasites. We found that population density was not a key determinant of enteric infection nor a strong effect modifier of risk posed by poor household sanitation in this setting.

[open-access] 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.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Eisenberg JNS, Trostle J, Sorensen RJD, Shields KF, , 2012. Toward a systems approach to enteric pathogen transmission: from individual independence to community interdependence. Annu Rev Public Health 33: 239257.[Crossref] [Google Scholar]
  2. Sedgwick WT, MacNutt JS, , 1910. On the Mills-Reincke phenomenon and Hazen's theorem concerning the decrease in mortality from diseases other than typhoid fever following the purification of public water-supplies. J Infect Dis 7: 489564.[Crossref] [Google Scholar]
  3. Cutler D, Miller G, , 2005. The role of public health improvements in health advances: the twentieth-century United States. Demography 42: 122.[Crossref] [Google Scholar]
  4. McMichael AJ, , 2000. The urban environment and health in a world of increasing globalization: issues for developing countries. Bull World Health Organ 78: 11171126. [Google Scholar]
  5. Mara D, Lane J, Scott B, Trouba D, , 2010. Sanitation and health. PLoS Med 7: e1000363.[Crossref] [Google Scholar]
  6. Norman G, Pedley S, Takkouche B, , 2010. Effects of sewerage on diarrhoea and enteric infections: a systematic review and meta-analysis. Lancet Infect Dis 10: 536544.[Crossref] [Google Scholar]
  7. Clasen TF, Bostoen K, Schmidt W-P, Boisson S, Fung IC-H, Jenkins MW, Scott B, Sugden S, Cairncross S, , 2010. Interventions to improve disposal of human excreta for preventing diarrhoea. Cochrane Database Syst Rev 6: CD007180. [Google Scholar]
  8. Ziegelbauer K, Speich B, Mäusezahl D, Bos R, Keiser J, Utzinger J, , 2012. Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis. PLoS Med 9: e1001162.[Crossref] [Google Scholar]
  9. Arnold BF, Khush RS, Ramaswamy P, London AG, Rajkumar P, Ramaprabha P, Durairaj N, Hubbard AE, Balakrishnan K, Colford JM, , 2010. Causal inference methods to study nonrandomized, preexisting development interventions. Proc Natl Acad Sci USA 107: 2260522610.[Crossref] [Google Scholar]
  10. Patil SR, Arnold BF, Salvatore AL, Briceno B, Ganguly S, Colford JM, Jr Gertler PJ, , 2014. The effect of India's total sanitation campaign on defecation behaviors and child health in rural Madhya Pradesh: a cluster randomized controlled trial. PLoS Med 11: e1001709.[Crossref] [Google Scholar]
  11. Clasen T, Boisson S, Routray P, Torondel B, Bell M, Cumming O, Ensink J, Freeman M, Jenkins M, Odagiri M, Ray S, Sinha A, Suar M, Schmidt W-P, , 2014. Effectiveness of a rural sanitation programme on diarrhoea, soil-transmitted helminth infection, and child malnutrition in Odisha, India: a cluster-randomised trial. Lancet Glob Health 2: e645e653.[Crossref] [Google Scholar]
  12. Anderson RM, May RM, , 1985. Helminth infections of humans: mathematical models, population dynamics, and control. Adv Parasitol 24: 1101.[Crossref] [Google Scholar]
  13. Halpenny CM, Koski KG, Valdés VE, Scott ME, , 2012. Prediction of child health by household density and asset-based indices in impoverished indigenous villages in rural Panama. Am J Trop Med Hyg 86: 280291.[Crossref] [Google Scholar]
  14. Halpenny CM, Paller C, Koski KG, Valdés VE, Scott ME, , 2013. Regional, household and individual factors that influence soil transmitted helminth reinfection dynamics in preschool children from rural indigenous Panamá. PLoS Negl Trop Dis 7: e2070.[Crossref] [Google Scholar]
  15. Bates SJ, Trostle J, Cevallos WT, Hubbard A, Eisenberg JNS, , 2007. Relating diarrheal disease to social networks and the geographic configuration of communities in rural Ecuador. Am J Epidemiol 166: 10881095.[Crossref] [Google Scholar]
  16. Cairncross S, Feachem R, , 1999. Environmental Health Engineering in the Tropics. West Sussex, England: John Wiley & Sons. [Google Scholar]
  17. Cortes J, Arvelo W, Lopez B, Reyes L, Kerin T, Gautam R, Patel M, Parashar U, Lindblade KA, , 2012. Rotavirus disease burden among children <5 years of age–Santa Rosa, Guatemala, 2007–2009. Trop Med Int Health 17: 254259.[Crossref] [Google Scholar]
  18. Estévez A, Arvelo W, Hall AJ, López MR, López B, Reyes L, Moir JC, Gregoricus N, Vinjé J, Parashar UD, Lindblade KA, , 2013. Prevalence and genetic diversity of norovirus among patients with acute diarrhea in Guatemala. J Med Virol 85: 12931298.[Crossref] [Google Scholar]
  19. Benoit SR, Lopez B, Arvelo W, Henao O, Parsons MB, Reyes L, Moir JC, Lindblade K, , 2014. Burden of laboratory-confirmed Campylobacter infections in Guatemala 2008–2012: results from a facility-based surveillance system. J Epidemiol Glob Health 4: 5159.[Crossref] [Google Scholar]
  20. Baqui AH, Black RE, Yunus M, Hoque AR, Chowdhury HR, Sack RB, , 1991. Methodological issues in diarrhoeal diseases epidemiology: definition of diarrhoeal episodes. Int J Epidemiol 20: 10571063.[Crossref] [Google Scholar]
  21. Schmidt W-P, Arnold BF, Boisson S, Genser B, Luby SP, Barreto ML, Clasen T, Cairncross S, , 2011. Epidemiological methods in diarrhoea studies—an update. Int J Epidemiol 40: 16781692.[Crossref] [Google Scholar]
  22. Arnold BF, Galiani S, Ram PK, Hubbard AE, Briceño B, Gertler PJ, Colford JM, Jr, 2013. Optimal recall period for caregiver-reported illness in risk factor and intervention studies: a multicountry study. Am J Epidemiol 177: 361370.[Crossref] [Google Scholar]
  23. U.S. Centers for Disease Control and Prevention, 2009. DPDx: Laboratory Identification of Parasites of Public Health Concern—Stool Specimens: Microscopic Examination. Available at: http://www.cdc.gov/dpdx/diagnosticProcedures/stool/microexam.html. Accessed October 31, 2014. [Google Scholar]
  24. Standards Unit, Microbiology Services, Public Health England, 2014. UK Standards for Microbiology Investigations, B 30 Investigation of Faecal Specimens for Enteric Pathogens. Available at: https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/423601/ID_16i4.pdf. Accessed January 30, 2016. [Google Scholar]
  25. Tornieporth NG, John J, Salgado K, de Jesus P, Latham E, Melo MC, Gunzburg ST, Riley LW, , 1995. Differentiation of pathogenic Escherichia coli strains in Brazilian children by PCR. J Clin Microbiol 33: 13711374. [Google Scholar]
  26. Trujillo AA, McCaustland KA, Zheng D-P, Hadley LA, Vaughn G, Adams SM, Ando T, Glass RI, Monroe SS, , 2006. Use of TaqMan real-time reverse transcription-PCR for rapid detection, quantification, and typing of norovirus. J Clin Microbiol 44: 14051412.[Crossref] [Google Scholar]
  27. Barreto ML, Genser B, Strina A, Teixeira MG, Cairncross S, Assis AM, Rego RF, Teles CA, Prado MS, Matos SM, Santos DN, dos Santos LA, , 2007. Effect of city-wide sanitation programme on reduction in rate of childhood diarrhoea in northeast Brazil: assessment by two cohort studies. Lancet 370: 16221628.[Crossref] [Google Scholar]
  28. Santamaria J, Toranzos GA, , 2003. Enteric pathogens and soil: a short review. Int Microbiol 6: 59. [Google Scholar]
  29. Escamilla V, Knappett PSK, Yunus M, Streatfield PK, Emch M, , 2013. Influence of latrine proximity and type on tubewell water quality and diarrheal disease in Bangladesh. Ann Assoc Am Geogr 103: 299308.[Crossref] [Google Scholar]
  30. UNICEF, WHO, 2012. World Health Organization and United Nations Children's Fund Joint Monitoring Programme for Water Supply and Sanitation (JMP). Progress on Drinking Water and Sanitation: 2012 Update. New York and Geneva: UNICEF and WHO. [Google Scholar]
  31. Rothman KJ, Greenland S, Lash TL, , 2008. Modern Epidemiology, 3rd edition. Philadelphia, PA: Lippincott Williams and Wilkins. [Google Scholar]
  32. VanderWeele TJ, Knol MJ, , 2014. A tutorial on interaction. Epidemiol Methods 3: 3372. [Google Scholar]
  33. Black RE, Lopez de Romaña G, Brown KH, Bravo N, Bazalar OG, Kanashiro HC, , 1989. Incidence and etiology of infantile diarrhea and major routes of transmission in Huascar, Peru. Am J Epidemiol 129: 785799.[Crossref] [Google Scholar]
  34. Hotez P, , 2000. The other intestinal protozoa: enteric infections caused by Blastocystis hominis, Entamoeba coli, and Dientamoeba fragilis . Semin Pediatr Infect Dis 11: 178181.[Crossref] [Google Scholar]
  35. Islam N, Angeles G, Mahbub AQM, Lance P, Nazem NI, , 2006. Slums of Urban Bangladesh: Mapping and Census, 2005. Center for Urban Studies, MEASURE Evaluation, National Institute of Population Research and Training. Available at: http://www.cpc.unc.edu/measure/publications/tr-06-35. Accessed November 25, 2014. [Google Scholar]
  36. Hathi P, Haque S, Pant L, Coffey D, Spears D, , 2014. Place and Child Health: The Interaction of Population Density and Sanitation in Developing Countries. World Bank Policy Research Working Paper WPS7124.[Crossref] [Google Scholar]
  37. Brown J, Cumming O, Bartram J, Cairncross S, Ensink J, Holcomb D, Knee J, Kolsky P, Liang K, Liang S, Nala R, Norman G, Rheingans R, Stewart J, Zavale O, Zuin V, Schmidt W-P, , 2015. A controlled, before-and-after trial of an urban sanitation intervention to reduce enteric infections in children: research protocol for the Maputo Sanitation (MapSan) study, Mozambique. BMJ Open 5: e008215.[Crossref] [Google Scholar]
  38. Langford M, Unwin DJ, , 1994. Generating and mapping population density surfaces within a geographical information system. Cartogr J 31: 2126.[Crossref] [Google Scholar]
  39. VanderWeele T, , 2012. Sample size and power calculations for additive interactions. Epidemiol Methods 1: 159188. [Google Scholar]

Data & Media loading...

Supplementary PDF

  • Received : 30 Jul 2015
  • Accepted : 03 Jan 2016
  • Published online : 06 Apr 2016

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error