• 1.

    World Health Organization, 2016. Soil-Transmitted Helminth Infections Fact Sheet. Geneva, Switzerland: World Health Organization.

  • 2.

    Kelly P, 2014. Intestinal protozoa. Farrar J, ed. Manson's Tropical Diseases. Philadelphia, PA: Saunders.

  • 3.

    Fikresilasie S, 2015. Status of soil-transmitted helminths infection in Ethiopia. Am Jf Health Res 3: 170–176.

  • 4.

    Abera B, Alem G, Yimer M, Herrador Z, 2013. Epidemiology of soil-transmitted helminths, Schistosoma mansoni, and haematocrit values among schoolchildren in Ethiopia. J Infect Dev Ctries 7: 253–260.

    • Search Google Scholar
    • Export Citation
  • 5.

    Tadesse Z, Hailemariam A, Kolaczinski JH, 2008. Potential for integrated control of neglected tropical diseases in Ethiopia. Trans R Soc Trop Med Hyg 102: 213–214.

    • Search Google Scholar
    • Export Citation
  • 6.

    Zerdo Z, Yohanes T, Tariku B, 2016. Soil-transmitted helminth reinfection and associated risk factors among school-age children in Chencha District, southern Ethiopia: a cross-sectional study. J Parasitol Res 2016: 4737891.

    • Search Google Scholar
    • Export Citation
  • 7.

    King JD, Endeshaw T, Escher E, Alemtaye G, Melaku S, Gelaye W, Worku A, Adugna M, Melak B, Teferi T, 2013. Intestinal parasite prevalence in an area of Ethiopia after implementing the SAFE strategy, enhanced outreach services, and health extension program. PLoS Negl Trop Dis 7: e2223.

    • Search Google Scholar
    • Export Citation
  • 8.

    Victora CG, de Onis M, Hallal PC, Blössner M, Shrimpton R, 2010. Worldwide timing of growth faltering: revisiting implications for interventions. Pediatrics 125: e473–80.

    • Search Google Scholar
    • Export Citation
  • 9.

    Gebre T, Ayele B, Zerihun M, Genet A, Stoller NE, Zhou Z, House JI, Yu SN, Ray KJ, Emerson PM, Keenan JD, Porco TC, Lietman TM, Gaynor BD, 2012. Comparison of annual versus twice-yearly mass azithromycin treatment for hyperendemic trachoma in Ethiopia: a cluster-randomised trial. Lancet 379: 143–151.

    • Search Google Scholar
    • Export Citation
  • 10.

    Aiemjoy K, Stoller NE, Gebresillasie S, Shiferaw A, Tadesse Z, Sewnet T, Ayele B, Chanyalew M, Callahan K, Stewart A, Emerson PM, Lietman TM, Keenan JD, Oldenburg CE, 2016. ‘If an eye is washed properly, it means it would see clearly’: a mixed methods study of face washing knowledge, attitudes, and behaviors in rural Ethiopia. PLoS Negl Trop Dis 10: e0005099.

    • Search Google Scholar
    • Export Citation
  • 11.

    Aiemjoy K, Stoller NE, Gebresillasie S, Shiferaw A, Tadesse Z, Sewent T, Ayele B, Chanyalew M, Aragie S, Callahan K, Stewart A, Emerson PM, Lietman TM, Keenan JD, Oldenburg CE, 2016. Is using a latrine “a strange thing to do”? A mixed-methods study of sanitation preference and behaviors in rural Ethiopia. Am J Trop Med Hyg 96: 65–73.

    • Search Google Scholar
    • Export Citation
  • 12.

    Utzinger J, Botero-Kleiven S, Castelli F, Chiodini P, Edwards H, Köhler N, Gulletta M, Lebbad M, Manser M, Matthys B, N'Goran EK, Tannich E, Vounatsou P, Marti H, 2010. Microscopic diagnosis of sodium acetate-acetic acid-formalin-fixed stool samples for helminths and intestinal protozoa: a comparison among European reference laboratories. Clin Microbiol Infect 16: 267–273.

    • Search Google Scholar
    • Export Citation
  • 13.

    WHO Expert Committee, 2002. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organ Tech Rep Ser 912: i–vi, 1–57.

    • Search Google Scholar
    • Export Citation
  • 14.

    Gonin P, Trudel L, 2003. Detection and differentiation of Entamoeba histolytica and Entamoeba dispar isolates in clinical samples by PCR and enzyme-linked immunosorbent assay. J Clin Microbiol 41: 237–241.

    • Search Google Scholar
    • Export Citation
  • 15.

    de Onis M, Onyango AW, Van den Broeck J, Chumlea CW, Martorell R, 2004. Measurement and standardization protocols for anthropometry used in the construction of a new international growth reference. Food Nutr Bull 25: S27–S36.

    • Search Google Scholar
    • Export Citation
  • 16.

    World Health Organization, 1995. Physical Status: The Use and Interpretation of Anthropometry. Report of a WHO Expert Committee. Technical Report Series No. 854. Geneva, Switzerland: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 17.

    Ayele B, Aemere A, Gebre T, Tadesse Z, Stoller NE, See CW, Sun NY, Gaynor BD, McCulloch CE, Porco TC, Emerson PM, Lietman TM, Keenan JD, 2012. Reliability of measurements performed by community-drawn anthropometrists from rural Ethiopia. PLoS One 7: e30345.

    • Search Google Scholar
    • Export Citation
  • 18.

    Leroy J, 2011. ZSCORE06: Stata Module to Calculate Anthropometric Z-Scores Using the 2006 WHO Child Growth Standards. Chestnut Hill, MA: Boston College.

    • Search Google Scholar
    • Export Citation
  • 19.

    Cummings P, 2011. Estimating adjusted risk ratios for matched and unmatched data: an update. Stata J 11: 290–298.

  • 20.

    Casapía MW, Joseph SA, Núnez C, Rahme E, Gyorkos TW, 2007. Parasite and maternal risk factors for malnutrition in preschool-age children in Belen, Peru using the new WHO Child Growth Standards. Br J Nutr 98: 1259–1266.

    • Search Google Scholar
    • Export Citation
  • 21.

    Heymann DL, 2008. Control of Communicable Diseases Manual. Washington, DC: American Public Health Association.

  • 22.

    Prado M, Cairncross S, Strina A, Barreto ML, Oliveira-Assis A, Rego S, 2005. Asymptomatic giardiasis and growth in young children; a longitudinal study in Salvador, Brazil. Parasitology 131: 51–56.

    • Search Google Scholar
    • Export Citation
  • 23.

    Nematian J, Gholamrezanezhad A, Nematian E, 2008. Giardiasis and other intestinal parasitic infections in relation to anthropometric indicators of malnutrition: a large, population-based survey of schoolchildren in Tehran. Ann Trop Med Parasitol 102: 209–214.

    • Search Google Scholar
    • Export Citation
  • 24.

    Bartelt LA, Roche J, Kolling G, Bolick D, Noronha F, Naylor C, Hoffman P, Warren C, Singer S, Guerrant R, 2013. Persistent G. lamblia impairs growth in a murine malnutrition model. J Clin Invest 123: 2672–2684.

    • Search Google Scholar
    • Export Citation
  • 25.

    Hall A, Hewitt G, Tuffrey V, De Silva N, 2008. A review and meta-analysis of the impact of intestinal worms on child growth and nutrition. Matern Child Nutr 4: 118–236.

    • Search Google Scholar
    • Export Citation
  • 26.

    Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque ASG, Zaidi AKM, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O'Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM, 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382: 209–222.

    • Search Google Scholar
    • Export Citation
  • 27.

    McCormick B, 2014. Frequent Symptomatic or Asymptomatic Infections May Have Long-Term Consequences on Growth and Cognitive Development. Old Herborn University Seminar Monographs. Herborn, Germany: Institute for Microbiology und Biochemistry, 23–39.

    • Search Google Scholar
    • Export Citation
  • 28.

    Petri WA, Miller M, Binder HJ, Levine MM, Dillingham R, Guerrant RL, 2008. Enteric infections, diarrhea, and their impact on function and development. J Clin Invest 118: 1277–1290.

    • Search Google Scholar
    • Export Citation
  • 29.

    De Vlas S, Gryseels B, 1992. Underestimation of Schistosoma mansoni prevalences. Parasitol Today 8: 274–277.

  • 30.

    Knopp S, Mgeni AF, Khamis IS, Steinmann P, Stothard JR, Rollinson D, Marti H, Utzinger J, 2008. Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Negl Trop Dis 2: e331.

    • Search Google Scholar
    • Export Citation
  • 31.

    Glinz D, Silué KD, Knopp S, Lohourignon LK, Yao KP, Steinmann P, Rinaldi L, Cringoli G, N'Goran EK, Utzinger J, 2010. Comparing diagnostic accuracy of Kato-Katz, Koga agar plate, ether-concentration, and FLOTAC for Schistosoma mansoni and soil-transmitted helminths. PLoS Negl Trop Dis 4: e754.

    • Search Google Scholar
    • Export Citation
  • 32.

    Marti H, Escher E, 1990. SAF: an alternative fixation solution for parasitological stool specimens [in German]. Schweiz Med Wochenschr 120: 1473–1476.

    • Search Google Scholar
    • Export Citation

 

 

 

 

Epidemiology of Soil-Transmitted Helminth and Intestinal Protozoan Infections in Preschool-Aged Children in the Amhara Region of Ethiopia

View More View Less
  • 1 Proctor Foundation, University of California San Francisco, San Francisco, California.
  • 2 The Carter Center, Atlanta, Georgia.
  • 3 Amhara Regional Health Bureau, Bahir-Dar, Ethiopia.

Intestinal parasites are important contributors to global morbidity and mortality and are the second most common cause of outpatient morbidity in Ethiopia. This cross-sectional survey describes the prevalence of soil-transmitted helminths and intestinal protozoa in preschool children 0–5 years of age in seven communities in the Amhara region of Ethiopia, and investigates associations between infection, household water and sanitation characteristics, and child growth. Stool samples were collected from children 0–5 years of age, 1 g of sample was preserved in sodium acetate–acetic acid–formalin, and examined for intestinal helminth eggs and protozoa cysts ether-concentration method. A total of 212 samples were collected from 255 randomly selected children. The prevalence of Ascaris lumbricoides, Trichuris trichiura, and hookworm were 10.8% (95% confidence interval [CI] 6.6–15.1), 1.4% (95% CI = 0–3.0), and 0% (95% CI = 0–1.7), respectively. The prevalence of the pathogenic intestinal protozoa Giardia lamblia and Entamoeba histolytica/dispar were 10.4% (95% CI = 6.2–14.6) and 3.3% (95% CI = 0.09–5.7), respectively. Children with A. lumbricoides infections had lower height-for-age z-scores compared with those without, but were not more likely to have stunting. Compared with those without G. lamblia, children with G. lamblia infections had lower weight-for-age and weight-for-height z-scores and were more than five times as likely to meet the z-score definition for wasting (prevalence ratio = 5.42, 95% CI = 2.97–9.89). This article adds to a growing body of research on child growth and intestinal parasitic infections and has implications for their treatment and prevention in preschool-aged children.

Author Notes

* Address correspondence to Kristen Aiemjoy, Proctor Foundation, University of California San Francisco, 513 Parnassus Avenue, MedSci S309, Box 0412, San Francisco, CA 94143. E-mail: kristen.aiemjoy@ucsf.edu

Financial support: This study was supported by the National Institutes of Health—National Eye Institute (U10 EY016214), That Man May See, and the Sara and Evan Williams Foundation (San Francisco, CA).

Authors' addresses: Kristen Aiemjoy, Nicole E. Stoller, and Jeremy D. Keenan, Proctor Foundation, University of California San Francisco, San Francisco, CA, E-mails: kristen.aiemjoy@ucsf.edu, nicole.stoller@ucsf.edu, and jeremy.keenan@ucsf.edu. Sintayehu Gebresillasie, Ayalew Shiferaw, Zerihun Tadesse, Solomon Aragie, and Kelly Callahan, The Carter Center, Atlanta, GA, E-mails: sintayehugs@gmail.com, ayalewsisu2003@gmail.com, zerihun.tadesse@cartercenter.org, solomon.aragie@cartercenter.org, and kelly.callahan@cartercenter.org. Melsew Chanyalew, Amhara Regional Health Bureau, Bahir-Dar, Ethiopia, E-mail: yeshiwork97@yahoo.com.

Save