Possible Correlation between Giardia duodenalis Genotypes and Fecal Calprotectin in Children with Diarrhea
,
Abstract
Background: Giardiasis is one of the leading causes of diarrhea, particularly among children under the age of five in developing countries. Fecal calprotectin (FC) is an important biomarker for diagnosis and monitoring of inflammtory bowel disease, but other diagnoses should be considered in light of its elevation. We aimed to evaluate FC level in patients diagnosed with giardiasis and elucidate a possible correlation between Giardia genotypes and FC levels.
Methods: Overall, 120 fecal samples were collected from children aged 4-12 years and tested for giardiasis by light microscopy. Out of which, 50 samples were enrolled within two groups: group I “cases” and group II “controls” and then subjected to PCR amplification, sequencing of the beta-giardin (bg) gene of the parasite, and FC evaluation.
Results: Assemblage B was identified in 75%, and assemblage A in 25% of samples. FC levels were statistically elevated in “group I” in comparison to “group II”. Likewise, there was a statistically significant difference between FC levels in patients infected with assemblage A and assemblage B with a mean of 114 μg/gm and 202 μg/gm, respectively.
Conclusion: The study highlighted the possible association between Giardia genotype B and elevated FC levels, further detailed studies are necessary to clarify these finding.
1. Ryan U, Cacciò SM. Zoonotic potential of Giardia. Int J Parasitol. 2013; 43: 943–56.
2. Feng, Y, Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev. 2011; 24: 110–40.
3. Xiao L, Feng Y. Molecular epidemiologic tools for waterborne pathogens Cryptospor-idium spp. and Giardia duodenalis. Food Wa-terborne Parasitol. 2017; 8–9:14–32.
4. Franzén O, Jerlström-Hultqvist J, Castro E et al. Draft genome sequencing of Giardia intestinalis assemblage B isolate GS: is hu-man Giardiasis caused by two different species? PLoS Pathog. 2009;5(8):e1000560.
5. Puebla LJ, Núñez FA, Fernández YA et al. Correlation of Giardia duodenalis assemblag-es with clinical and epidemiological data in Cuban children. Infect Genet Evol. 2014;23:7-12.
6. Choy SH, Al-Mekhlafi HM, Mahdy MA et al. Prevalence and Associated Risk Factors of Giardia Infection among Indigenous Communities in Rural Malaysia. Sci Rep. 2014;4:6909.
7. Solaymani-Mohammadi S, Singer SM. Host immunity and pathogen strain con-tribute to intestinal disaccharidase impair-ment following a gut infection. J Immunol. 2011;187:3769–75.
8. Cotton JA, Beatty JK, Buret AG. Host-parasite interactions and pathophysiology in Giardia infections. Int J Parasitol. 2011;41:925–33.
9. Robertson LJ, Hanevik K, Escobedo AA et al. Giardiasis—Why do the symptoms sometimes never stop?. Trends Parasitol. 2010;26:75–82.
10. Bartelt LA, Sartor RB. Advances in under-standing Giardia: determinants and mech-anisms of chronic sequelae. F1000Prime Rep. 2015;7:62.
11. Hanevik K, Hausken T, Morken MH et al. Persisting symptoms and duodenal in-flammation related to Giardia duodenalis in-fection. J Infect. 2007;55(6):524-30.
12. Kolho KL, Alfthan H. Concentration of fecal calprotectin in 11,255 children aged 0-18 years. Scand J Gastroenterol. 2020;55(9):1024-27.
13. Salman YJ, Ali CHE, Abdul-Razaq AA. Fecal Calprotectin among patients infected with some protozoan infections.Int J Curr Microbiol App Sci. 2017;6(6): 3258-74.
14. Jeong SJ. The role of fecal calprotectin in pediatric disease. Korean J Pediatr. 2019;62(8):287-91.
15. Bustinduy AL, Sousa-Figueiredo JC, Adri-ko M et al. Fecal occult blood and fecal calprotectin as point-of-care markers of intestinal morbidity in Ugandan children with Schistosoma mansoni infection. PLoS Negl Trop Dis. 2013;7(11):e2542.
16. Lalle M, Pozio E, Capelli G et al. Genetic heterogeneity at the beta-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. Int J Parasitol. 2005; 35 (2): 207-13.
17. Caccio SM, De Giacomo M, Pozio E. Sequence analysis of the beta-giardin gene and development of a polymerase chain reaction-restriction fragment length polymorphism assay to genotype Giardia duodenalis cysts from human faecal samples. Int J Parasitol. 2002; 32 (8): 1023-30.
18. Mumolo MG, Bertani L, Ceccarelli L et al. From bench to bedside: Fecal calprotectin in inflammatory bowel diseases clinical set-ting. World J Gastroenterol. 2018;24(33):3681-94.
19. D'Angelo F, Felley C, Frossard J L. Cal-protectin in Daily Practice: Where Do We Stand in 2017?. Digestion. 2017; 95: 293-301.
20. Carroccio A, Iacono G, Cottone M et al. Diagnostic accuracy of fecal calprotectin assay in distinguishing organic causes of chronic diarrhea from irritable bowel syn-drome: a prospective study in adults and children. Clin Chem. 2003;49 (6 Pt 1):861-7.
21. Chen CC, Huang JL, Chang CJ et al. Fecal Calprotectin as a correlative marker in clin-ical severity of infectious diarrhea and use-fulness in evaluating bacterial or viral path-ogens in children. J Pediatr Gastroenterol Nutr. 2012; 55(5): 541-7.
22. Opintan JA, Newman MJ, Ayeh-Kumi PF et al. Pediatric diarrhea in southern Ghana: etiology and association with intestinal inflammation and malnutrition. Am J Trop Med Hyg. 2010;83(4):936-43.
23. Kohli A, Bushen OY, Pinkerton RC et al. Giardia duodenalis assemblage, clinical presentation and markers of intestinal inflammation in Brazilian children. Trans R Soc Trop Med Hyg. 2008;102(7):718-25.
24. Melissa Shapiro M, Shah N, Sehgal S. Se-verely Elevated Fecal Calprotectin in A Pe-diatric Patient with Persistent Giardiasis. Acad J Gastroenterol & Hepatol. 2021; 2(4).
25. Roxström-Lindquist K, Palm D, Reiner D et al. Giardia immunity--an update. Trends Parasitol. 2006; 22(1):26‐31.
26. Adeyemo FE, Singh G, Reddy P et al. Methods for the detection of Cryptosporidi-um and Giardia: from microscopy to nucle-ic acid-based tools in clinical and envi-ronmental regimes. Acta Trop. 2018; 184:15–28.
27. Wilke H, Robertson LJ. Preservation of Giardia cysts in stool samples for subse-quent PCR analysis. J Microbiol Methods. 2009; 78(3): 292–6.
28. Foronda P, Bargues MD, Abreu-Acosta N et al. Identification of genotypes Giardia in-testinalis of human isolates in Egypt. Parasi-tol Res. 2008;103:1177–81.
29. Taha S, Abd Al Aal Z, Saleh Z et al. Giar-dia intestinalis assemblages among Egyptian symptomatic children: Prevalence and sea-sonal distribution in Cairo, Egypt. J Egypt Soc Parasitol. 2018; 48:661–8.
30. Al-Mohammed HI. Genotypes of Giardia intestinalis clinical isolates of gastrointestinal symptomatic and asymptomatic Saudi children. Parasitol Res. 2011; 108:1375-81.
31. Sarkari B, Ashrafmansori A, Hatam GR et al. Genotyping of Giardia lamblia isolates from human in southern Iran. Trop Bio-med. 2012; 29:366-71.
32. Al-Yousefi NA, Mahdy MA, Xiao L et al. Molecular characterization of Giardia duode-nalis in Yemen. Exp Parasitol. 2013; 134 (2):141-7.
33. Aydin AF, Besirbellioglu BA, Avci IY et al. Classification of Giardia duodenalis parasites in Turkey into Groups A and B using re-striction fragment length polymorphism. Diagn Microbiol Infect Dis. 2004; 50:147–51.
34. Homan W, Mank T. Human giardiasis: genotype linked differences in clinical symptomatology. Int J Parasitol. 2001; 31:822–6.
35. George CM, Burrowes V, Perin J et al. Enteric Infections in Young Children are Associated with Environmental Enteropathy and Impaired Growth. Trop Med Int Health. 2018; 23(1):26‐33.
36. Jha AK, Chaudhary M, Dayal VM et al. Optimal cut‐off value of fecal calprotectin for the evaluation of ulcerative colitis: An unsolved issue?. JGH Open. 2018;2(5):207-13.
37. Banerjee A, Srinivas M, Eyre R et al. Faecal Calprotectin for differentiating between ir-ritable bowel syndrome and inflammatory bowel disease: a useful screen in daily gas-troenterology practice. Frontline Gastroen-terol. 2015; 6(1): 20–26.
38. Campbell DI, McPhail G, Lunn PG et al. Intestinal inflammation measured by fecal neopterin in Gambian children with enteropathy: association with growth failure, Giardia lamblia, and intestinal permeability. J Pediatr Gastroenterol Nutr. 2004; 39(2):153‐7.
39. Cotton JA, Motta JP, Schenck LP et al. Giardia duodenalis infection reduces granulocyte infiltration in an in vivo model of bacterial toxin-induced colitis and attenuates inflammation in human intestinal tissue. PLoS One. 2014;9(10):e109087.
2. Feng, Y, Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev. 2011; 24: 110–40.
3. Xiao L, Feng Y. Molecular epidemiologic tools for waterborne pathogens Cryptospor-idium spp. and Giardia duodenalis. Food Wa-terborne Parasitol. 2017; 8–9:14–32.
4. Franzén O, Jerlström-Hultqvist J, Castro E et al. Draft genome sequencing of Giardia intestinalis assemblage B isolate GS: is hu-man Giardiasis caused by two different species? PLoS Pathog. 2009;5(8):e1000560.
5. Puebla LJ, Núñez FA, Fernández YA et al. Correlation of Giardia duodenalis assemblag-es with clinical and epidemiological data in Cuban children. Infect Genet Evol. 2014;23:7-12.
6. Choy SH, Al-Mekhlafi HM, Mahdy MA et al. Prevalence and Associated Risk Factors of Giardia Infection among Indigenous Communities in Rural Malaysia. Sci Rep. 2014;4:6909.
7. Solaymani-Mohammadi S, Singer SM. Host immunity and pathogen strain con-tribute to intestinal disaccharidase impair-ment following a gut infection. J Immunol. 2011;187:3769–75.
8. Cotton JA, Beatty JK, Buret AG. Host-parasite interactions and pathophysiology in Giardia infections. Int J Parasitol. 2011;41:925–33.
9. Robertson LJ, Hanevik K, Escobedo AA et al. Giardiasis—Why do the symptoms sometimes never stop?. Trends Parasitol. 2010;26:75–82.
10. Bartelt LA, Sartor RB. Advances in under-standing Giardia: determinants and mech-anisms of chronic sequelae. F1000Prime Rep. 2015;7:62.
11. Hanevik K, Hausken T, Morken MH et al. Persisting symptoms and duodenal in-flammation related to Giardia duodenalis in-fection. J Infect. 2007;55(6):524-30.
12. Kolho KL, Alfthan H. Concentration of fecal calprotectin in 11,255 children aged 0-18 years. Scand J Gastroenterol. 2020;55(9):1024-27.
13. Salman YJ, Ali CHE, Abdul-Razaq AA. Fecal Calprotectin among patients infected with some protozoan infections.Int J Curr Microbiol App Sci. 2017;6(6): 3258-74.
14. Jeong SJ. The role of fecal calprotectin in pediatric disease. Korean J Pediatr. 2019;62(8):287-91.
15. Bustinduy AL, Sousa-Figueiredo JC, Adri-ko M et al. Fecal occult blood and fecal calprotectin as point-of-care markers of intestinal morbidity in Ugandan children with Schistosoma mansoni infection. PLoS Negl Trop Dis. 2013;7(11):e2542.
16. Lalle M, Pozio E, Capelli G et al. Genetic heterogeneity at the beta-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. Int J Parasitol. 2005; 35 (2): 207-13.
17. Caccio SM, De Giacomo M, Pozio E. Sequence analysis of the beta-giardin gene and development of a polymerase chain reaction-restriction fragment length polymorphism assay to genotype Giardia duodenalis cysts from human faecal samples. Int J Parasitol. 2002; 32 (8): 1023-30.
18. Mumolo MG, Bertani L, Ceccarelli L et al. From bench to bedside: Fecal calprotectin in inflammatory bowel diseases clinical set-ting. World J Gastroenterol. 2018;24(33):3681-94.
19. D'Angelo F, Felley C, Frossard J L. Cal-protectin in Daily Practice: Where Do We Stand in 2017?. Digestion. 2017; 95: 293-301.
20. Carroccio A, Iacono G, Cottone M et al. Diagnostic accuracy of fecal calprotectin assay in distinguishing organic causes of chronic diarrhea from irritable bowel syn-drome: a prospective study in adults and children. Clin Chem. 2003;49 (6 Pt 1):861-7.
21. Chen CC, Huang JL, Chang CJ et al. Fecal Calprotectin as a correlative marker in clin-ical severity of infectious diarrhea and use-fulness in evaluating bacterial or viral path-ogens in children. J Pediatr Gastroenterol Nutr. 2012; 55(5): 541-7.
22. Opintan JA, Newman MJ, Ayeh-Kumi PF et al. Pediatric diarrhea in southern Ghana: etiology and association with intestinal inflammation and malnutrition. Am J Trop Med Hyg. 2010;83(4):936-43.
23. Kohli A, Bushen OY, Pinkerton RC et al. Giardia duodenalis assemblage, clinical presentation and markers of intestinal inflammation in Brazilian children. Trans R Soc Trop Med Hyg. 2008;102(7):718-25.
24. Melissa Shapiro M, Shah N, Sehgal S. Se-verely Elevated Fecal Calprotectin in A Pe-diatric Patient with Persistent Giardiasis. Acad J Gastroenterol & Hepatol. 2021; 2(4).
25. Roxström-Lindquist K, Palm D, Reiner D et al. Giardia immunity--an update. Trends Parasitol. 2006; 22(1):26‐31.
26. Adeyemo FE, Singh G, Reddy P et al. Methods for the detection of Cryptosporidi-um and Giardia: from microscopy to nucle-ic acid-based tools in clinical and envi-ronmental regimes. Acta Trop. 2018; 184:15–28.
27. Wilke H, Robertson LJ. Preservation of Giardia cysts in stool samples for subse-quent PCR analysis. J Microbiol Methods. 2009; 78(3): 292–6.
28. Foronda P, Bargues MD, Abreu-Acosta N et al. Identification of genotypes Giardia in-testinalis of human isolates in Egypt. Parasi-tol Res. 2008;103:1177–81.
29. Taha S, Abd Al Aal Z, Saleh Z et al. Giar-dia intestinalis assemblages among Egyptian symptomatic children: Prevalence and sea-sonal distribution in Cairo, Egypt. J Egypt Soc Parasitol. 2018; 48:661–8.
30. Al-Mohammed HI. Genotypes of Giardia intestinalis clinical isolates of gastrointestinal symptomatic and asymptomatic Saudi children. Parasitol Res. 2011; 108:1375-81.
31. Sarkari B, Ashrafmansori A, Hatam GR et al. Genotyping of Giardia lamblia isolates from human in southern Iran. Trop Bio-med. 2012; 29:366-71.
32. Al-Yousefi NA, Mahdy MA, Xiao L et al. Molecular characterization of Giardia duode-nalis in Yemen. Exp Parasitol. 2013; 134 (2):141-7.
33. Aydin AF, Besirbellioglu BA, Avci IY et al. Classification of Giardia duodenalis parasites in Turkey into Groups A and B using re-striction fragment length polymorphism. Diagn Microbiol Infect Dis. 2004; 50:147–51.
34. Homan W, Mank T. Human giardiasis: genotype linked differences in clinical symptomatology. Int J Parasitol. 2001; 31:822–6.
35. George CM, Burrowes V, Perin J et al. Enteric Infections in Young Children are Associated with Environmental Enteropathy and Impaired Growth. Trop Med Int Health. 2018; 23(1):26‐33.
36. Jha AK, Chaudhary M, Dayal VM et al. Optimal cut‐off value of fecal calprotectin for the evaluation of ulcerative colitis: An unsolved issue?. JGH Open. 2018;2(5):207-13.
37. Banerjee A, Srinivas M, Eyre R et al. Faecal Calprotectin for differentiating between ir-ritable bowel syndrome and inflammatory bowel disease: a useful screen in daily gas-troenterology practice. Frontline Gastroen-terol. 2015; 6(1): 20–26.
38. Campbell DI, McPhail G, Lunn PG et al. Intestinal inflammation measured by fecal neopterin in Gambian children with enteropathy: association with growth failure, Giardia lamblia, and intestinal permeability. J Pediatr Gastroenterol Nutr. 2004; 39(2):153‐7.
39. Cotton JA, Motta JP, Schenck LP et al. Giardia duodenalis infection reduces granulocyte infiltration in an in vivo model of bacterial toxin-induced colitis and attenuates inflammation in human intestinal tissue. PLoS One. 2014;9(10):e109087.
| Files | ||
| Issue | Vol 17 No 4 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v17i4.11275 | |
| Keywords | ||
| Giardia duodenalis Genotypes Fecal calprotectin Diarrhea Egypt | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Abou-Seri H, Ibrahim A, Zahran F. Possible Correlation between Giardia duodenalis Genotypes and Fecal Calprotectin in Children with Diarrhea. Iran J Parasitol. 2022;17(4):488-496.
