Helicobacter pylori and enteric parasites co-infection among diarrheic and non-diarrheic Egyptian children: seasonality, estimated risks, and predictive factors

  • Asmaa Ibrahim
  • Yasser B. M. Ali
  • Amal Abdel-Aziz
  • Ayman A. El-Badry
Original Article


Helicobacter pylori (H. pylori) and intestinal parasites are known for their high prevalence in children. Both of them infect the gastrointestinal tract with overlapping clinical pictures. This study was conducted to determine H. pylori prevalence and its association with intestinal parasites in children, moreover to estimate risk and predictive factors for their detection in stool samples. Single fecal samples were collected from 226 Egyptian pediatric patients (125 diarrheic and 101 non-diarrheic) attending gastroenterology outpatients’ clinics, from February 2016 to June 2017. All stool specimens were microscopically examined to search for ova and parasites. Copro-DNAs detection of H. pylori and Cryptosporidium were performed using nested-PCR assays. H. pylori was detected molecularly in 36.8% of the total study population, with a higher prevalence in diarrheic than in non-diarrheic children. Intestinal parasites were detected in 27.4% of the total study populations, of these, 43.9% had co-existence with H. pylori colonized patients and was significantly associated with Cryptosporidium spp. and G. intestinalis. Estimated risk of the presence of H. pylori was in January. Our data provide a better understanding of the epidemiology of H. pylori infection when associated with intestinal parasites. H. pylori co-existence with G. intestinals and Cryptosporidium may suggest the association of H. pylori infection with markers of fecal exposure. Whether H. pylori provides favorable conditions for intestinal parasitosis or vice versa, still further investigations are needed with an emphasis upon determining correlation with gut microbiomes.


Helicobacter pylori Intestinal parasites Risk factors Diarrhea Children Egypt 


Authors contribution

AI: corresponding author, participate in all stages from study design to manuscript writing and revision, YBMA: participate in study design and manuscript revision); AA-A provide technical help; AAE-B: participated in Study design, supervised the lab work, analysis and interpretation of data and involved in drafting the manuscript.


This research was self-funded and did not receive any grants from any funding agency.

Compliance with ethical standards

Conflict of interest

The authors have declared that no competing interest exists.

Ethical approval

Ethical board of University of Sadat City, Genetic Engineering, and Biotechnology Research Institute, Egypt approved the study. Parents of all the children included in the study were verbally informed about the study’s aims, and collection of the specimens was done after their consent was obtained.


  1. Abd El Kader NM, Blanco MA, Ali-Tammam M, El Ghaffar Abd, Ael R, Osman A, El Sheikh N, Rubio JM, de Fuentes I (2012) Detection of Cryptosporidium parvum and Cryptosporidium hominis in human patients in Cairo, Egypt. Parasitol Res 110:161–166CrossRefGoogle Scholar
  2. Bhan MK, Bahl R, Sazawal S, Sinha A, Kumar R, Mahalanabis D, Clemens JD (2000) Association between Helicobacter pylori infection and increased risk of typhoid fever. J Infect Dis 186(12):1857–1860CrossRefGoogle Scholar
  3. Bhutta ZA, Das JK, Walker N, Rizvi A, Campbell H, Rudan I, Black RE (2013) Interventions to address deaths from childhood pneumonia and diarrhoea equitably: what works and at what cost? Lancet 381:1417–1429CrossRefGoogle Scholar
  4. Brooker S, Kabatereine NB, Smith JL, Mupfasoni D, Mwanje MT, Ndayishimiye O, Lwambo NJ, Mbotha D, Karanja P, Mwandawiro C, Muchiri E, Clements AC, Bundy DA, Snow RW (2009) An updated atlas of human helminth infections: the example of East Africa. Int J Health Geogr 8:42CrossRefGoogle Scholar
  5. Chen TL, Chan CC, Chen HP, Fung CP, Lin CP, Chan WL, Liu CY (2003) Clinical characteristics and endoscopic findings associated with Blastocystis hominis in healthy adults. Am J Trop Med Hyg 69:213–216CrossRefGoogle Scholar
  6. Cheng H, Hu F, Zhang L, Yang G, Ma J, Hu J, Wang W, Gao W, Dong X (2009) Prevalence of Helicobacter pylori infection and identification of risk factors in rural and urban Beijing, China. Helicobacter 14:128–133CrossRefGoogle Scholar
  7. Cheesbrough M (2006) District laboratory practices in tropical countries. Part London Cambridge University Press, Cambridge, pp 184–215CrossRefGoogle Scholar
  8. David TJ, William AP (2006) Markell and Voge’s medical parasitology. 9th edn. Saunders Elsevier, New YorkGoogle Scholar
  9. Einarsson E, Ma’ayeh S, Svard SG (2016) An up-date on giardia and giardiasis. Curr Opin Microbiol 34:47–52. PMID:27501461 CrossRefPubMedGoogle Scholar
  10. El-Badry AA, Al-Antably AS, Hassan MA, Hanafy NA, Abu-Sarea EY (2015) Molecular seasonal, age and gender distributions of Cryptosporidium in diarrhoeic Egyptians: distinct endemicity. Eur J Clin Microbiol Infect Dis 34:2447–2453CrossRefGoogle Scholar
  11. Escobar-Pardo ML, de Godoy AP, Machado RS, Rodrigues D, Fagundes Neto U, Kawakami E (2011) Prevalence of Helicobacter pylori infection and intestinal parasitosis in children of the Xingu Indian Reservation. J Pediatria 11:87–105Google Scholar
  12. Frenck RW Jr, Clemens J (2003) Helicobacter in the developing world. Microbes Infect 5:705–713CrossRefGoogle Scholar
  13. Frenck RW Jr, Fathy HM, Sherif M, Mohran Z, El Mohammedy H, Francis W, Rockabrand D, Mounir BI, Rozmajzl P, Frierson HF (2006) Sensitivity and specificity of various tests for the diagnosis of Helicobacter pylori in Egyptian children. Pediatrics 118:1195–1202CrossRefGoogle Scholar
  14. Gallo N, Zambon CF, Navaglia F, Basso D, Guariso G, Grazia Piva M, Greco E, Mazza S, Fogar P, Rugge M, Di Mario F, Plebani M (2003) Helicobacter pylori infection in children and adults: a single pathogen but a different pathology. Helicobacter 8(1):21–28CrossRefGoogle Scholar
  15. Garcia LS, Bruckner DA, Brewer TC, Shimizu RY (1983) Techniques for the recovery and identification of Cryptosporidium oocysts from stool specimens. J Clin Microbiol 18:185–190PubMedPubMedCentralGoogle Scholar
  16. Helmy YA, Krucken J, Nockler K, von Samson-Himmelstjerna G, Zessin KH (2013) Molecular epidemiology of Cryptosporidium in livestock animals and humans in the Ismailia province of Egypt. Vet Parasitol 193(15–24):2Google Scholar
  17. Jacoby EB, Porter KB (1999) Helicobacter pylori infection and persistent hyperemesis gravidarum. Am J Perinatol 16:85–88CrossRefGoogle Scholar
  18. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, 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(9888):209–222. CrossRefPubMedGoogle Scholar
  19. Lal A, Hales S, French N, Baker MG (2012) Seasonality in human zoo-notic enteric diseases: a systematic review. PLoS ONE 7(4):e31883CrossRefGoogle Scholar
  20. Mansour-Ghanaei F, Taefeh N, Joukar F, Besharati S, Naghipour M, Nassiri R (2010) Recurrence of Helicobacter pylori infection 1 year after successful eradication: a prospective study in Northern Iran. Med Sci Monitor 16(3):CR144–CR148Google Scholar
  21. Marini E, Maldonado-Contreras AL, Cabras S, Hidalgo G, Buffa R, Marin A, Floris G, Racugno W, Pericchi LR, Castellanos ME, Gröschl M, Blaser MJ, Domínguez-Bello MG (2007) Helicobacter pylori and intestinal parasites are not detrimental to the nutritional status of Amerindians. Am J Trop Med Hyg 76:534–540CrossRefGoogle Scholar
  22. Mehmood A, Akram M, Shahab-uddin AA, Usmanghani K, Hannan A, Mohiuddin E, Asif M (2010) Helicobacter pylori: an introduction. Int J Appl Biol Pharm Technol 1(3):1337–1351Google Scholar
  23. Moayyedi P, Anthony TR, Feltbower R, Duffett S, Crocombe W, Braunholtz D, Richards ID, Dowell AC, Forman D, Leeds HELP Study Group (2002) Relation of adult lifestyle and socioeconomic factors to the prevalence of Helicobacter pylori infection. Int J Epidemiol 31:624–631CrossRefGoogle Scholar
  24. Moreira ED Jr, Nassri VB, Santos RS, Matos JF, de Carvalho WA, Silvani CS, Santana e Sant’ana C (2005) Association of Helicobacter pylori infection and giardiasis: results from a study of surrogate markers for fecal exposure among children. World J Gastroenterol 11:2759–2763CrossRefGoogle Scholar
  25. Pedraza-Díaz S, Amar C, Nichols GL, McLauchlin J (2001) Nested polymerase chain reaction for amplification of the Cryptosporidiumoocyst wall protein gene. Emerg Infect Dis 7:49–56CrossRefGoogle Scholar
  26. Rafeey M, Ghotaslou R, Nikvash S, Hafez AA (2007) Primary resistance in Helicobacter pylori isolated in children from Iran. J Infect Chemother 13:291–295 PMID: 17982716 CrossRefGoogle Scholar
  27. Rajindrajith S, Devanarayana NM, de Silva HJ (2009) Helicobacter pylori infection in children. Saudi J Gastroenterol 15(2):86–94CrossRefGoogle Scholar
  28. Raschka C, Schorr W, Koch HJ (1999) Is there seasonal periodicity in the prevalence of Helicobacter pylori? Chronobiol Int 16(6):811–819CrossRefGoogle Scholar
  29. Rodrigues MN, Queiroz DM, Bezerra Filho JG, Pontes LK, Rodrigues RT, Braga LL (2004) Prevalence of Helicobacter pylori infection in children from an urban community in north-east Brazil and risk factors for infection. Eur J Gastroenterol Hepatol 16(2):201–205CrossRefGoogle Scholar
  30. Rodriguez OL, Ortiz-Princz D, Cavazza ME, López E, Hagel I (2011) Evaluation of the possible association between the presence of intestinal parasites and Helicobacter pylori in children of ethnic Warao Venezuela. Bol Mal Salud Amb 11:41–50Google Scholar
  31. Sabah AA, Gneidy MR, Saleh NM (2015) Prevalence of Helicobacter pylori infection among adult patients with different gastrointestinal parasites in Tanta City district. J Egypt Soc Parasitol 45:101–106CrossRefGoogle Scholar
  32. Salih BA (2009) Helicobacter pylori infection in developing countries: the burden for how long? Saudi J Gastroenterol 15(3):201–207CrossRefGoogle Scholar
  33. Sasaki K, Tajiri Y, Sata M, Fujii Y, Matsubara F, Zhao M, Shimizu S, Toyonaga A, Tanikawa K (1999) Helicobacter pylori in the natural environment. Scand J Infect Dis 31:275–279CrossRefGoogle Scholar
  34. Savarino V, Mela GS, Zentilin P, Lapertosa G, Cutela P, Mele MR, Mansi C, Dallorto E, Vassallo A, Celle G (1992) Are duodenal ulcer seasonal fluctuations paralleled by seasonal changes in 24-hour gastric acidity and Helicobacter pylori infection? J Clin Gastroenterol 22(3):178–181CrossRefGoogle Scholar
  35. Sethi A, Chaudhuri M, Kelly L, Hopman W (2013) Prevalence of Helicobacter pylori in a first nations population in northwestern Ontario. Can Fam Physician 59(4):e182–187PubMedPubMedCentralGoogle Scholar
  36. Shahinian ML, Passaro DJ, Swerdlow DL, Mintz ED, Rodriguez M, Parsonnet J (2000) Helicobacter pylori and epidemic Vibrio cholerae O1 infection in Peru. Lancet 355:377–378CrossRefGoogle Scholar
  37. Sow SO, Muhsen K, Nasrin D, Blackwelder WC, Wu Y, Farag TH, Panchalingam S, Sur D, Zaidi AK, Faruque AS, Saha D, Adegbola R, Alonso PL, Breiman RF, Bassat Q, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ahmed S, Qureshi S, Quadri F, Hossain A, Das SK, Antonio M, Hossain MJ, Mandomando I, Nhampossa T, Acácio S, Omore R, Oundo JO, Ochieng JB, Mintz ED, O’Reilly CE, Berkeley LY, Livio S, Tennant SM, Sommerfelt H, Nataro JP, Ziv-Baran T, Robins-Browne RM, Mishcherkin V, Zhang J, Liu J, Houpt ER, Kotloff KL, Levine MM (2016) The burden of cryptosporidium diarrhoeal disease among children < 24 months of age in moderate/high mortality regions of Sub-Saharan Africa and South Asia, utilizing data from the global enteric multicenter study (GEMS). PLoS Negl Trop Dis 10(5):e0004729CrossRefGoogle Scholar
  38. Spano F, Putignani L, McLauchlin J, Casemore DP, Crisanti A (1997) PCR-RFLP analysis of the Cryptosporidium oocysts wall protein (COWP) gene discriminates between C. wrairi and C. parvum, and between C. parvum isolates of human and animal origin. FEMS Microbiol Lett 150:209–217CrossRefGoogle Scholar
  39. Striepen B (2013) Parasitic infections: time to tackle cryptosporidiosis. Nature 503:189–191CrossRefGoogle Scholar
  40. Suerbaum S, Michetti P (2002) Helicobacter pylori infection. N Engl J Med 347(15):1175–1186CrossRefGoogle Scholar
  41. Tanih NF, Ndip RN (2013) A South African perspective on Helicobacter pylori: prevalence, epidemiology and antimicrobial chemotherapy. Review article. Afr J Microbiol Res 7(21):2430–2437CrossRefGoogle Scholar
  42. Thompson RCA, Ash A (2016) Molecular epidemiology of Giardia and Cryptosporidium infections. Infect Genet Evol 40:315–323CrossRefGoogle Scholar
  43. Torres J, Perez GP, Ximenez C, Muñoz L, Camorlinga-Ponce M, Ramos F, Gomez A, Muñoz O (2003) The association of intestinal parasitosis and Helicobacter pylori infection in children and adults from a Mexican community with high prevalence of parasitosis. Helicobacter 8:179–185CrossRefGoogle Scholar
  44. Vale FF, Vitor JM (2010) Transmission pathway of Helicobacter pylori: does food play a role in rural and urban areas? Int J Food Microbiol 138:1–12CrossRefGoogle Scholar
  45. Vos T, Allen C, Arora M, Barber RM, Bhutta ZA, Brown A, Carter A, Casey DC, Charlson FJ, Chen AZ, Coggeshall M, Cornaby L (2016) Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 388(10053):1545–1602CrossRefGoogle Scholar
  46. Whary MT, Taylor NS, Feng Y, Ge Z, Muthupalani S, Versalovic J, Fox JG (2011) Lactobacillus reuteri promotes Helicobacte hepaticus-associated typhlocolitis in gnotobiotic B6.129P2-IL10(tm1Cgn) (IL-10(−/−)) mice. Immunology 133:165–178CrossRefGoogle Scholar
  47. Whitney AE, Guarner J, Hutwagner L, Gold BD (2000) Helicobacter Pylori gastritis in children and adults: comparative histopathologic study. Ann Diagn Pathol 4(5):279–285CrossRefGoogle Scholar
  48. World Gastroenterology Organisation (WGO) (2012) World gastroenterology organisation global guidelines: acute diarrhoea in adults and children: a global perspective. WGO, MilwaukeeGoogle Scholar
  49. World Health Organization (WHO) (2017) Diarrhoeal diseases: WHO fact sheet on diarrhoeal diseases. Accessed 15 Sept 2018
  50. Yakoob J, Jafari W, Abid S, Tafari N, Hamid S, Shah HA, Rizvi L, Islam M, Shaikh H (2005) Giardiasis in patient with dyspeptic symptoms. World J Gastroenterol 11(42):6667–66705CrossRefGoogle Scholar
  51. Zamani M, Ebrahimtabar F, Miller WH, Alizadeh-Navaei R, Shokri-Shirvani J, Derakhshan MH (2018) Review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther 47:868–876CrossRefGoogle Scholar
  52. Zeyrek D, Zeyrek F, Cakmak A, Cekin A (2008) Association of Helicobacter pylori and giardiasis in children with recurrent abdominal pain. Turkiye Parazitol Derg 32:4–7PubMedGoogle Scholar

Copyright information

© Indian Society for Parasitology 2019

Authors and Affiliations

  1. 1.Diagnostic and Research Unit of Parasitic Diseases (DRUP), Department of Medical Parasitology, Kasr Al-Ainy Faculty of MedicineCairo UniversityCairoEgypt
  2. 2.Genetic Engineering and Biotechnology Research InstituteUniversity of Sadat CitySadat CityEgypt
  3. 3.Department of Microbiology, Faculty of MedicineImam Abdulrahman Bin Faisal UniversityDammamSaudi Arabia

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