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The hidden impact of different Blastocystis genotypes on C-3 and IgE serum levels: a matter of debate in asthmatic Egyptian children

  • Enas A. El SaftawyEmail author
  • Noha M. Amin
  • Dina H. Hamed
  • Aly Elkazazz
  • Sherihan Adel
Original Article
  • 39 Downloads

Abstract

Blastocystis hominis is highly prevalent with respiratory allergies among Egyptian children. Yet, little is known about the possible immunological relationship. Aims of this study were to measure complement-3 (C-3), total and specific IgE to intestinal allergens in patients’ serum regarding the identified B. hominis genotypes. In a cross-sectional study, three hundred children (150 asthmatics and 150 non asthmatics) participated in the study from both sexes, mean age 7.5 ± SD (3–4) years after a questionnaire administration. PCR-based genotyping of B. hominis selective in vitro cultivation was performed. C-3, total and specific IgE were all measured in patients’ serum utilizing ELISA. Blastocystosis was detected in 100 out of 300 children, 65 (43.3%) out of 150 asthmatics and 35 (23.3%) out of 150 non-asthmatics. Vacuolar forms were the most prevalent in both direct wet mount and stool cultures. Forty (61.5%) out 65 asthmatics and 5 (14.2%) out of 35 non-asthmatics were ≥ 5 organisms/HPF. Sex and irritable bowel disease were statistically insignificant (p value < 0.05). Urticaria was coincided in 15.4% of asthmatics and 8.6% of non-asthmatics. Of 100 cases of blastocystosis, eighty-four were genotype-3 and sixteen were genotype-4. Out of these, 55 cases of genotype-3 and 6 cases of genotype-4 were asthmatics. Positive C-3 serum levels were in 46 (54.81%) of genotype-3 and 2 (12.5%) of genotype-4. High total IgE levels in 30 (35.7%) out of 84 cases of genotype-3 and 4 (25%) out of 16 cases of genotype-4. Positive specific IgE was in 25 (29.8%) of genotype-3 and 3 (18.75%) of genotype-4. Genotype-3 was of higher infection intensity (p value = 0.0001). In conclusion, B. hominis possess a hidden allergy triggering impact that can be obscured by simultaneous high (total and specific) IgE levels towards specific common intestinal allergens. Blastocystosis induces allergy by increasing C-3 serum levels in a genotype-dependent manner being higher in genotype-3. Virulence of genotype-3 seems to stand beyond increased parasite intensity and wide absorption of intestinal allergens that indirectly elevate IgE serum levels.

Keywords

Blastocystis hominis Allergies Genotype-3 Genotype-4 C-3 IgE 

Notes

Acknowledgements

The authors thank the whole pediatrician team at chest clinics located in the Outpatient’s Department of Abou El-Reesh Teaching Pediatrics Hospital, Cairo University for supplying the research team with all required data. Also authors thank Dr. Hamida A. Gohar, Professor of Medical Microbiology Department, School of Medicine, Cairo University, and Dr. Samar Almogy, MD. Medical Microbiology, and DR Marwa Tarek, lecturer of Medical Biochemistry and Molecular Biology Department, College of Medicine, Ain Shams University for their consultations. The authors feel grateful to Dr. Moussa Abdelgawad, Professor of Parasitology and Head of Diagnostic and Research Unite of Parasitology, School of Medicine, Cairo University. The funding was provided by Authors of the papers (Grant Number 9000).

Author’s contribution

EAE and NMA contributed together in data collection using questionnaire, stool and serum samples collection, parasitological examination and performance of Blastocystis hominis culture, PCR and genotyping of the extracted isolates. EAE performed the ELISA for C3 and total and specific IgE. NMA performed the special bacteriological examinations. DHH and AE supplied the research with the clinical data and referred children to the Medical Parasitology Department. SA was incorporated in the molecular study of the parasite.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights

All procedures performed in the study involving human participants were in accordance with the ethical standards of the National Research Committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Permission to conduct this study and ethical approval was received from the Deanship of Higher Education and Scientific Researches, Faculty of Medicine, Cairo University. The present study was conducted only on stool and serum samples of the selected cases.

Informed consent

Aims and procedures of the study were explained and parents of all participants assigned informed consent before being enrolled in the study. Patients suffered from cancers were not included. After sample collection, Blastocystis infected patients were offered the antiprotozoal drug “metronidazole” with the standard dose of 40 mg/kg body weight.

References

  1. Ahmad Al Obaidi AH, Mohamed Al Samarai AG, Yahya Al Samarai AK, Al Janabi JM (2008) The predictive value of IgE as biomarker in asthma. J Asthma 45(8):654–663CrossRefGoogle Scholar
  2. Badparva E, Sadraee J, Kheirandish F, Frouzandeh M (2014) Genetic diversity of human blastocystis isolates in Khorramabad, central Iran. Iran J Parasitol 9(1):44Google Scholar
  3. Bakiri AH, Mingomataj EC (2010) Parasites induced skin allergy: a strategic manipulation of the host immunity. J Clin Med Res 2(6):247Google Scholar
  4. Clark CG (1997) Extensive genetic diversity in Blastocystis hominis. Mol Biochem Parasitol 87(1):79–83CrossRefGoogle Scholar
  5. Cooper PJ, Chico ME, Sandoval C, Nutman TB (2004) Atopic phenotype is an important determinant of immunoglobulin E-mediated inflammation and expression of T helper cell type 2 cytokines to Ascaris antigens in children exposed to ascariasis. J Infect Dis 190(7):1338–1346CrossRefGoogle Scholar
  6. Di Prisco MC, Hagel I, Lynch NR, Jimenez JC, Rojas R, Gil M, Mata E (1998) Association between giardiasis and allergy. Ann Allergy Asthma Immunol 81(3):261–265CrossRefGoogle Scholar
  7. Durmaz B, Cengiz Yakıncı MD, Mehmet Köroğlu MD (1996) Concentrations of total serum IgE in parasitized children and the effects of the antiparasitic therapy on IgE levels. J Turgut Ozal Med Cent 3(4):333Google Scholar
  8. Fitzsimmons CM, McBeath R, Joseph S, Jones FM, Walter K, Hoffmann KF, Kariuki HC, Mwatha JK, Kimani G, Kabatereine NB, Vennervald BJ (2007) Factors affecting human IgE and IgG responses to allergen-like Schistosoma mansoni antigens: molecular structure and patterns of in vivo exposure. Int Arch Allergy Immunol 142(1):40–50CrossRefGoogle Scholar
  9. Geiger SM, Massara CL, Bethony J, Soboslay PT, Carvalho OS, Corrêa-Oliveira R (2002) Cellular responses and cytokine profiles in Ascaris lumbricoides and Trichuris trichiura infected patients. Parasite Immunol 24(11–12):499–509CrossRefGoogle Scholar
  10. Gleich GJ, Zimmermann EM, Henderson LL, Yunginger JW (1982) Effect of immunotherapy on immunoglobulin E and immunoglobulin G antibodies to ragweed antigens: a six-year prospective study. J Allergy Clin Immunol 70(4):261–271CrossRefGoogle Scholar
  11. Gonzalez-Arenas NR, Villalobos G, Vargas-Sanchez GB, Avalos-Galarza CA, Marquez-Valdelamar LM, Ramirez-Miranda ME, Olivo-Diaz A, Romero-Valdovinos M, Martinez-Hernandez F, Maravilla P (2018) Is the genetic variability of Cathepsin B important in the pathogenesis of Blastocystis spp.? J Parasitol Res 117(12):3935–3943CrossRefGoogle Scholar
  12. Gupta R, Parsi K (2006) Chronic urticaria due to Blastocystis hominis. Australas J Dermatol 47(2):117–119CrossRefGoogle Scholar
  13. Hameed DM, Hassanin OM, Zuel-Fakkar NM (2011) Association of Blastocystis hominis genetic subtypes with urticaria. J Parasitol Res 108(3):553–560CrossRefGoogle Scholar
  14. Hanevik K, Dizdar V, Langeland N, Hausken T (2009) Development of functional gastrointestinal disorders after Giardia lamblia infection. BMC Gastroenterol 9(1):27CrossRefGoogle Scholar
  15. Hennino A, Bérard F, Guillot I, Saad N, Rozières A, Nicolas JF (2006) Pathophysiology of urticaria. Clin Rev Allergy Immunol 30(1):3–11CrossRefGoogle Scholar
  16. Hoffman WA, Pons JA, Janer JL (1934) The sedimentation-concentration method in Schistosomiasis mansoni. PRJ Public Health Trop Med 9:283–291Google Scholar
  17. Hussein EM, Hussein AM, Eida MM, Atwa MM (2008) Pathophysiological variability of different genotypes of human Blastocystis hominis Egyptian isolates in experimentally infected rats. J Parasitol Res 102(5):853–860CrossRefGoogle Scholar
  18. Irikov OA, Antokhin AI, Romanov YA (2009) Study of the dynamics of Blastocystis hominis reproduction in vitro. Bull Exp Biol Med 148(1):99CrossRefGoogle Scholar
  19. Javaherizadeh H, Khademvatan S, Soltani S, Torabizadeh M, Yousefi E (2014) Distribution of haematological indices among subjects with Blastocystis hominis infection compared to controls. PRZ Gastroenterol 9(1):38CrossRefGoogle Scholar
  20. Katsarou-Katsari A, Vassalos CM, Tzanetou K, Spanakos G, Papadopoulou C, Vakalis N (2008) Acute urticaria associated with amoeboid forms of Blastocystis spp. subtype 3. Acta Derm Venereol 88(1):80–81CrossRefGoogle Scholar
  21. Khademvatan S, Masjedizadeh R, Rahim F, Mahbodfar H, Salehi R, Yousefi-Razin E, Foroutan M (2017) Blastocystis and irritable bowel syndrome: frequency and subtypes from Iranian patients. Parasitol Int 66(2):142–145CrossRefGoogle Scholar
  22. Lee IL, Tan TC, Tan PC, Nanthiney DR, Biraj MK, Surendra KM, Suresh KG (2012) Predominance of Blastocystis sp. subtype 4 in rural communities, Nepal. Parasitol Res 110(4):1553–1562CrossRefGoogle Scholar
  23. Macdougall IC, Vernon K (2017) Complement activation-related pseudo-allergy: a fresh look at hypersensitivity reactions to intravenous iron. Am J Nephrol 45(1):60–62CrossRefGoogle Scholar
  24. Malheiros AF, Stensvold CR, Clark CG, Braga GB, Shaw JJ (2011) Molecular characterization of Blastocystis obtained from members of the indigenous Tapirapé ethnic group from the Brazilian Amazon region, Brazil. Am J Trop Med Hyg 85(6):1050–1053CrossRefGoogle Scholar
  25. Menounos PG, Spanakos G, Tegos N, Vassalos CM, Papadopoulou C, Vakalis NC (2008) Direct detection of Blastocystis sp. in human fecal samples and subtype assignment using single-strand conformational polymorphism and sequencing. Mol Cell Probe 22(1):24–29CrossRefGoogle Scholar
  26. Mohamed RT, El-Bali MA, Mohamed AA, Abdel-Fatah MA, El-Malky MA, Mowafy NM, Zaghlool DA, Bakri RA, Al-Harthi SA (2017) Subtyping of Blastocystis sp. isolated from symptomatic and asymptomatic individuals in Makkah, Saudi Arabia. Parasite Vector 10(1):174CrossRefGoogle Scholar
  27. Moosavi A, Haghighi A, Mojarad EN, Zayeri F, Alebouyeh M, Khazan H, Kazemi B, Zali MR (2012) Genetic variability of Blastocystis spp. isolated from symptomatic and asymptomatic individuals in Iran. Parasitol Res 111(6):2311–2315CrossRefGoogle Scholar
  28. Nagel R, Traub RJ, Kwan MM, Bielefeldt-Ohmann H (2015) Blastocystis specific serum immunoglobulin in patients with irritable bowel syndrome (IBS) versus healthy controls. Parasites Vectors 8(1):453CrossRefGoogle Scholar
  29. Northrop-Clewes CA, Rousham EK, Mascie-Taylor CN, Lunn PG (2001) Anthelmintic treatment of rural Bangladeshi children: effect on host physiology, growth, and biochemical status. Am J Clin Nutr 73(1):53–60CrossRefGoogle Scholar
  30. Old DC, Duguid JP (1970) Selective outgrowth of fimbriate bacteria in a static liquid medium. J Bacteriol 103(2):447–456Google Scholar
  31. Prieto-Lastra L, Pérez-Pimiento A, González-Sánchez LA, Iglesias-Cadarso A (2006) Chronic urticaria and angioedema in Giardia lamblia infection. Med Clin 126(9):358–359CrossRefGoogle Scholar
  32. Puthia MK, Lu J, Tan KS (2008) Blastocystis ratti contains cysteine proteases that mediate interleukin-8 response from human intestinal epithelial cells in an NF-κB-dependent manner. Eukaryot Cell 7(3):435–443CrossRefGoogle Scholar
  33. Rayan HZ, Ismail OA, El EG (2007) Prevalence and clinical features of Dientamoeba fragilis infections in patients suspected to have intestinal parasitic infection. J Egypt Soc Parasitol 37(2):599–608Google Scholar
  34. Robertson LJ, Hanevik K, Escobedo AA, Mørch K, Langeland N (2010) Giardiasis—why do the symptoms sometimes never stop? Trends Parasitol 26(2):75–82CrossRefGoogle Scholar
  35. Rossignol JF (2010) Cryptosporidium and Giardia: treatment options and prospects for new drugs. Exp Parasitol 124(1):45–53CrossRefGoogle Scholar
  36. Sardarian K, Hajilooi M, Maghsood A, Moghimbeigi A, Alikhani M (2012) A study of the genetic variability of Blastocystis hominis isolates in Hamadan, west of Iran. Jundishapur J Microbiol 5(4):555–559CrossRefGoogle Scholar
  37. Shahar E, Bergman R, Guttman Yassky E, Pollack S (2006) Treatment of severe chronic idiopathic urticaria with oral mycophenolate mofetil in patients not responding to antihistamines and/or corticosteroids. Int J Dermatol 45(10):1224–1227CrossRefGoogle Scholar
  38. Shen JQ, Tian CL, Lu ZC, Wan XL, Liu DY, Liu XQ, Wang J, Li XM (2013) Relationship between morphology and pathogenicity of Blastocystis hominis trophozoites. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi Chin J Parasitol Parasit Dis 31(2):138–139Google Scholar
  39. Souppart L, Moussa H, Cian A, Sanciu G, Poirier P, El Alaoui H, Delbac F, Boorom K, Delhaes L, Dei-Cas E, Viscogliosi E (2010) Subtype analysis of Blastocystis isolates from symptomatic patients in Egypt. J Parasitol Res 106(2):505–511CrossRefGoogle Scholar
  40. Stark D, Van Hal S, Marriott D, Ellis J, Harkness J (2007) Irritable bowel syndrome: a review on the role of intestinal protozoa and the importance of their detection and diagnosis. Int J Parasitol 37(1):11–20CrossRefGoogle Scholar
  41. Stemeseder T, Klinglmayr E, Moser S, Lang R, Himly M, Oostingh GJ, Zumbach J, Bathke AC, Hawranek T, Gadermaier G (2017) Influence of intrinsic and lifestyle factors on the development of IgE sensitization. Int Arch Allergy Immunol 173(2):99–104CrossRefGoogle Scholar
  42. Stensvold CR (2013) Comparison of sequencing (barcode region) and sequence-tagged-site PCR for Blastocystis subtyping. J Clin Microbiol 51(1):190–194CrossRefGoogle Scholar
  43. Stensvold C, Arendrup M, Nielsen H, Bada A, Thorsen S (2008) Symptomatic infection with Blastocystis spp. subtype 8 successfully treated with trimethoprim-sulfamethoxazole. Ann Trop Med Parasitol 102:271–274CrossRefGoogle Scholar
  44. Suresh K, Smith H (2004) Comparison of methods for detecting Blastocystis hominis. Eur J Clin Microbiol Infect Dis 23(6):509–511CrossRefGoogle Scholar
  45. Suresh K, Venilla GD, Tan TC, Rohela M (2009) In vivo encystation of Blastocystis hominis. J Parasitol Res 104(6):1373–1380CrossRefGoogle Scholar
  46. Tan KS (2008) New insights on classification, identification, and clinical relevance of Blastocystis spp. Clin Microbiol Rev 21(4):639–665CrossRefGoogle Scholar
  47. Udkow MP, Markell EK (1993) Blastocystis hominis: prevalence in asymptomatic versus symptomatic hosts. J Infect Dis 168(1):242–244CrossRefGoogle Scholar
  48. Van Bever HP, Chng SY, Goh DY (2004) Childhood severe acute respiratory syndrome, coronavirus infections and asthma. Pediatr Allergy Immunol 15(3):206–209CrossRefGoogle Scholar
  49. Vennila GD, Kumar GS, Anuar AK, Rajah S, Saminathan R, Sivanandan S, Ramakrishnan K (1999) Irregular shedding of Blastocystis hominis. J Parasitol Res 85(2):162–164CrossRefGoogle Scholar
  50. Vogelberg C, Stensvold CR, Monecke S, Ditzen A, Stopsack K, Heinrich-Gräfe U, Pöhlmann C (2010) Blastocystis spp. subtype 2 detection during recurrence of gastrointestinal and urticarial symptoms. Parasitol Int 59:469–471CrossRefGoogle Scholar
  51. Yan Y, Su S, Lai R, Liao H, Ye J, Li X et al (2006) Genetic variability of Blastocystis hominis isolates in China. Parasitol Res 99:597–601CrossRefGoogle Scholar
  52. Yoshikawa H, Wu Z, Pandey K, Pandey BD, Sherchand JB, Yanagi T, Kanbara H (2009) Molecular characterization of Blastocystis isolates from children and rhesus monkeys in Kathmandu, Nepal. Vet Parasitol 160(3–4):295–300CrossRefGoogle Scholar
  53. Zaglool DA, Khodari YA, Farooq MU (2012) Blastocystis hominis and allergic skin diseases; a single centre experience. Afr J Health Sci 2(1):66–69Google Scholar

Copyright information

© Indian Society for Parasitology 2019

Authors and Affiliations

  • Enas A. El Saftawy
    • 1
    • 2
    Email author
  • Noha M. Amin
    • 1
  • Dina H. Hamed
    • 3
  • Aly Elkazazz
    • 3
  • Sherihan Adel
    • 4
  1. 1.Medical Parasitology Department, College of MedicineCairo UniversityCairoEgypt
  2. 2.Medical Parasitology Department, College of MedicineArmed Forces College of MedicineCairoEgypt
  3. 3.Department of Pediatrics, Faculty of MedicineCairo UniversityCairoEgypt
  4. 4.Medical Biochemistry and Molecular Biology Department, College of MedicineAin Shams UniversityCairoEgypt

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