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Prevalence and associated risk factors of Giardia duodenalis infection among school-going children in Nepal

Abstract

This study aimed to determine the prevalence of intestinal parasites and its associated risk factors among school-going children in Kathmandu, Nepal. Between August and September 2016, a total of 333 stool samples were collected from children at five public schools. The collected samples were subjected to formol-ether concentration, followed by conventional microscopic examination for intestinal parasites. The overall prevalence of intestinal parasites was 24.3% (81/333), with Giardia spp. showing the highest prevalence of 18.9% (63/333). Samples positive for Giardia spp. by microscopy were further subjected to quantitative polymerase chain reaction (qPCR) for G. duodenalis, resulting in a positive ratio of 100%. The positive ratio of Giardia spp. was considerably high among children consuming tanker water (27.3%), jar water (21.0%), and tap water (17.5%). Our results demonstrated that G. duodenalis remains predominant in school-going children in Nepal.

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References

  1. Alkhalife IS (2006) Retrospective analysis of intestinal parasitic infections diagnosed at a University Hospital in Central, Saudi Arabia. Saudi Med J 27:1714–1718

  2. Amar CFL, Dear PH, McLauchlin J (2003) Detection and genotyping by real-time PCR/RFLP analyses of Giardia duodenalis from human faeces. J Med Microbiol 52(8):681–683. https://doi.org/10.1099/jmm.0.05193-0

  3. Anim-Baidoo I, Narh CA, Oddei D, Brown CA, Enweronu-Laryea C, Bandoh B, Sampane-Donkor E, Armah G, Adjei AA, Adjei DN, Ayeh-Kumi PF, Gyan BA (2016) Giardia lamblia infections in children in Ghana. Pan Afr Med J 24:217. https://doi.org/10.11604/pamj.2016.24.217.8012

  4. Bertrand I, Gantzer C, Chesnot T, Schwartzbrod J (2004) Improved specificity for Giardia lamblia cyst quantification in wastewater by development of a real-time PCR method. J Microbiol Methods 57(1):41–53. https://doi.org/10.1016/j.mimet.2003.11.016

  5. Buret AG (2008) Pathophysiology of enteric infections with Giardia duodenalius. Parasite 15(3):261–265. https://doi.org/10.1051/parasite/2008153261

  6. Cama VA, Mathison BA (2015) Infections by intestinal coccidia and Giardia duodenalis. Clin Lab Med 35(2):423–444. https://doi.org/10.1016/j.cll.2015.02.010

  7. Choy SH, Al-Mekhlafi HM, Mahdy MAK, Nasr NN, Sulaiman M, Lim YAL, Surin J (2014) Prevalence and associated risk factors of Giardia infection among indigenous communities in rural Malaysia. Sci Rep 4:1–9. https://doi.org/10.1038/srep06909

  8. Delialioglu N, Aslan G, Sozen M, Babur C, Kanik A, Emekdas G (2004) Detection of Entamoeba histolytica/Entamoeba dispar in stool specimens by using enzyme-linked immunosorbent assay. Mem Inst Oswaldo Cruz 99(7):769–772. https://doi.org/10.1590/S0074-02762004000700019

  9. Haramoto E, Yamada K, Nishida K (2011) Prevalence of protozoa, viruses, coliphages and indicator bacteria in groundwater and river water in the Kathmandu Valley, Nepal. Trans R Soc Trop Med Hyg 105(12):711–716. https://doi.org/10.1016/j.trstmh.2011.08.004

  10. Heyworth MF (2016) Giardia duodenalis genetic assemblages and hosts. Parasite 23:13. https://doi.org/10.1051/parasite/2016013

  11. Ignatius R, Lehmann M, Miksits K, Regnath T, Arvand M, Engelmann E, Futh U, Hahn H, Wagner J (1997) A new acid-fast trichrome stain for simultaneous detection of Cryptosporidium parvum and microsporidial species in stool specimens. J Clin Microbiol 35(2):446–449

  12. Khadka KS, Kaphle HP, Gurung K, Shah Y, Sigdel M (2013) Study of intestinal parasitosis among school going children in Pokhara, Nepal. J Health Allied Sci 3:47–50

  13. Kunwar R, Acharya L, Karki S (2016) Decreasing prevalence of intestinal parasitic infections among school-aged children in Nepal: a systematic review and meta-analysis. Trans R Soc Trop Med Hyg 110(6):324–332. https://doi.org/10.1093/trstmh/trw033

  14. Maas L, Dorigo-Zetsma JW, de Groot CJ, Bouter S, Plötz FB, van Ewijk BE (2014) Detection of intestinal protozoa in paediatric patients with gastrointestinal symptoms by multiplex real-time PCR. Clin Microbiol Infect 20(6):545–550. https://doi.org/10.1111/1469-0691.12386

  15. Malla B, Ghaju Shrestha R, Bhandari D, Tandukar S, Shrestha S, Yoshinaga H, Inoue D, Sei K, Nishida K, Tanaka Y, Sherchand JB, Haramoto E (2015) Detection of Cryptosporidium, Giardia, fecal indicator bacteria, and total bacteria in commercial jar water in the Kathmandu Valley, Nepal. J Inst Med 37(2):10–15

  16. Mank TG, Zaat JOM, Deelder AM, van Eijk JTM, Polderman AM (1997) Sensitivity of microscopy versus enzyme immunoassay in the laboratory diagnosis of giardiasis. Eur J Clin Microbiol Infect Dis 16(8):615–619. https://doi.org/10.1007/BF02447929

  17. Ministry of Urban Development (2006) National drinking water quality standard implementation guideline, 2062. Kathmandu, Nepal

  18. Molina N, Pezzani B, Ciarmela M, Orden A, Rosa D, Apezteguía M, Basualdo J, Minvielle M (2011) Intestinal parasites and genotypes of Giardia intestinalis in school children from Berisso, Argentina. J Infect Dev Ctries 5(7):527–534. https://doi.org/10.3855/jidc.1660

  19. Morrone FB, Carneiro JA, dos Reis C, Cardozo CM, Ubal C, De Carli GA (2004) Study of enteroparasites infection frequency and chemotherapeutic agents used in pediatric patients in a community living in Porto Alegre, RS, Brazil. Rev Inst Med Trop S Paulo 46(2):77–80. https://doi.org/10.1590/S0036-46652004000200004

  20. Pant ND, Poudyal N, Bhattacharya SK (2016) Bacteriological quality of bottled drinking water versus municipal tap water in Dharan municipality, Nepal. J Health Popul Nutr 35(1):17. https://doi.org/10.1186/s41043-016-0054-0

  21. Pradhan P, Bhandary S, Shakya PR, Acharya T, Shrestha A (2014) Prevalence of intestinal parasitic infections among public school children in rural village of Kathmandu Valley Nepal. Nepal Med Coll J 16(1):50–53

  22. Sahagun J, Clavel A, Goni P, Seral C, Llorente MT, Castillo FJ, Capilla S, Arias A, Gomez-Lus R (2008) Correlation between the presence of symptoms and the Giardia duodenalis genotype. Eur J Clin Microbiol Infect Dis 27(1):81–83. https://doi.org/10.1007/s10096-007-0404-3

  23. Schuurman T, Lankamp P, van Belkum A, Kooistra-Smid M, van Zwet A (2007) Comparison of microscopy, real-time PCR and a rapid immunoassay for the detection of Giardia lamblia in human stool specimens. Clin Microbiol Infect 13(12):1186–1191. https://doi.org/10.1111/j.1469-0691.2007.01836.x

  24. Scott TM, Rose JB, Jenkins TM, Farrah SR, Lukasik J (2002) Microbial source tracking: current methodology and future directions. Appl Environ Microbiol 68(12):5796–5803. https://doi.org/10.1128/AEM.68.12.5796-5803.2002

  25. Shrestha S, Aihara Y, Bhattarai AP, Bista N, Rajbhandari S, Kondo N, Kazama F, Nishida K, Shindo J (2017) Dynamics of domestic water consumption in the urban area of the Kathmandu Valley: situation analysis pre and post 2015 Gorkha Earthquake. Water 9(3):222. https://doi.org/10.3390/w9030222

  26. Shrestha S, Haramoto E, Sherchand JB, Hada S, Rajbhandari S, Shindo J (2016) Prevalence of protozoa and indicator bacteria in wastewater irrigation sources in Kathmandu Valley, Nepal: cases from Kirtipur, Bhaktapur, and Madhyapur Thimi municipalities. J Water Environ Technol 14(3):149–157. https://doi.org/10.2965/jwet.15-047

  27. Supram HS, Koirala B, Rani A, Gokhale S, Bhatta DR (2015) Prevalence of intestinal parasitic infections in a tertiary care center at western Nepal: five years retrospective study. J Pharm Biomed Sci 5:154–159

  28. Tandukar S, Ansari S, Adhikari N, Shrestha A, Gautam J, Sharma B, Rajbhandari D, Gautam S, Nepal HP, Sherchand JB (2013) Intestinal parasitosis in school children of Lalitpur district of Nepal. BMC Res Notes 6:449. https://doi.org/10.1186/1756-0500-6-449

  29. Thompson RCA (2004) The zoonotic significance and molecular epidemiology of Giardia and giardiasis. Vet Parasitol 126(1–2):15–35. https://doi.org/10.1016/j.vetpar.2004.09.008

  30. Uga S, Rai SK, Kimura K, Rai G, Kimura D, Wakasugi M, Miyake Y, Ishiyama S, Rajbhandari TP (2004) Parasites detected from diarrheal stool samples collected in Nepal. Southeast Asian J Trop Med Public Health 35(1):19–23

  31. Valones MAA, Guimarães RL, Brandão LAC, de Souza PRE, Carvalho AAT, Crovela S (2009) Principles and applications of polymerase chain reaction in medical diagnostic fields: a review. Braz J Microbiol 40(1):1–11. https://doi.org/10.1590/S1517-83822009000100001

  32. Verweij JJ, Schinkel J, Laeijendecker D, van Rooyen MAA, van Lieshout L, Polderman AM (2003) Real-time PCR for the detection of Giardia lamblia. Mol Cell Probes 17(5):223–225. https://doi.org/10.1016/S0890-8508(03)00057-4

  33. Wafa AI, Megrin AL (2015) Assessment the prevalence of intestinal parasitic and associated risk factors among preschool children in Riyadh, Saudi Arabia. Res J Parasitol 10(1):31–41. https://doi.org/10.3923/jp.2015.31.41

  34. World Health Organization (1994) Bench aids for the diagnosis of intestinal parasites. World Health Organization, Geneva, Switzerland

  35. World Health Organization (2004) How to add deworming to vitamin A distribution. World Health Organization, Geneva, Switzerland

  36. World Health Organization (2008) Generic protocol for monitoring impact of rotavirus vaccination on gastroenteritis disease burden and viral strains. World Health Organization, Geneva, Switzerland

  37. Xiao L, Singh A, Limor J, Graczyk TK, Gradus S, Lal A (2001) Molecular characterization of Cryptosporidium oocysts in samples of raw surface water and wastewater. Appl Environ Microbiol 67(3):1097–1101. https://doi.org/10.1128/AEM.67.3.1097-1101.2001

  38. Yakob L, Williams GM, Gray DJ, Halton K, Solon JA, Clements ACA (2013) Slaving and release in co-infection control. Parasit Vectors 6:157. https://doi.org/10.1186/1756-3305-6-157

  39. Yaoyu F, Xiao L (2011) Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev 24(1):110–140. https://doi.org/10.1128/CMR.00033-10

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Acknowledgments

The authors would like to thank participants for their cooperation during the study. We are also grateful to the technical staff of the Public Health Research Laboratory, Tribhuvan University, Nepal; Tulane University, USA; Sadhana Shrestha; and Bijay Man Shakya (University of Yamanashi, Japan) for their technical support and guidance.

Author information

Correspondence to Eiji Haramoto.

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Tandukar, S., Sherchand, J.B., Xue, J. et al. Prevalence and associated risk factors of Giardia duodenalis infection among school-going children in Nepal. Parasitol Res 117, 287–293 (2018). https://doi.org/10.1007/s00436-017-5706-5

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Keywords

  • Giardia duodenalis
  • Nepal
  • Quantitative polymerase chain reaction
  • School-going children
  • Stool