The high sensitivity and specificity of rapid urease test in diagnosis of Helicobacter pylori infection in Moroccan children
-
Lahbib Hibaoui
,
Abdelhamid Massik
,
Zina Lebbar
,
Ghita Yahyaoui
,
Mustapha Mahmoud
,
Laila Bougnouch
,
Naoual Hamass
,
Laila Chbani
,
Bahia Bennani
,
Mohamed Amine Berrahou
,
Mounia Lakhdar Idriss
,
Moustapha Hida
Abstract
Background and Objectives: Infesting nearly 50% of the world's population, Helicobacter pylori are thought to cause peptic ulcers, as well as gastric adenocarcinoma. Several diagnostic methods are available to detect this bacterium; however, at least two must be used together for an accurate diagnosis. This study evaluated the use of rapid urease test for diagnosis of H. pylori infection in a pediatric population.
Materials and Methods: Five gastric biopsies were taken from children during a 2-year period for the purpose of histological, molecular, bacteriological culture, and rapid urease testing.
Results: Among 83 children, 38 were male, and 45 were female with an age ranging of 2 to 15 years. The infected group represented 31%. The rapid urease test had a sensitivity of 88.5%, a negative predictive value of 94%, a specificity of 84.2%, and a positive predictive value of 72%.
Conclusion: A rapid urease test may be appropriate for ruling out H. pylori infection after a negative result. The positive results however, may be confirmed by a second invasive test.
1. Kotilea K, Kalach N, Homan M, Bontems P. Helicobacter pylori infection in pediatric patients: update on diagnosis and eradication strategies. Paediatr Drugs 2018; 20: 337-351.
2. Roma E, Miele E. Helicobacter pylori infection in pediatrics. Helicobacter 2015; 20 Suppl 1: 47-53.
3. Hestvik E, Tylleskar T, Kaddu-Mulindwa DH, Ndeezi G, Grahnquist L, Olafsdottir E, et al. Helicobacter pylori in apparently healthy children aged 0-12 years in urban Kampala, Uganda: a community-based cross sectional survey. BMC Gastroenterol 2010; 10: 62.
4. Hasna B, Imane E, Ghizlane B, Reda JM, Abdeljabbar M, Hassan J, et al. Epidemiological study of Helicobacter pylori infection and its association with gastric carcinogenesis. Gulf J Oncolog 2021; 1: 7-13.
5. Bouihat N, Burucoa C, Benkirane A, Seddik H, Sentissi S, Al Bouzidi A, et al. Helicobacter pylori primary antibiotic resistance in 2015 in Morocco: A phenotypic and genotypic prospective and multicenter study. Microb Drug Resist 2017; 23: 727-732.
6. Sabbagh P, Javanian M, Koppolu V, Vasigala VR, Ebrahimpour S. Helicobacter pylori infection in children: an overview of diagnostic methods. Eur J Clin Microbiol Infect Dis 2019; 38: 1035-1045.
7. Burucoa C. Diagnostic tests for Helicobacter pylori infection in children. Arch Pediatr 2010; 17: 814-815.
8. Braden B. Diagnosis of Helicobacter pylori infection. BMJ 2012; 344: e828.
9. Sabbagh P, Mohammadnia-Afrouzi M, Javanian M, Babazadeh A, Koppolu V, Vasigala VR, et al. Diagnostic methods for Helicobacter pylori infection: ideals, options, and limitations. Eur J Clin Microbiol Infect Dis 2019; 38: 55-66.
10. Kraft C, Stack A, Josenhans C, Niehus E, Dietrich G, Correa P, et al. Genomic changes during chronic Helicobacter pylori infection. J Bacteriol 2006; 188: 249-254.
11. Kotilea K, Bontems P, Touati E. Epidemiology, diagnosis and risk factors of Helicobacter pylori infection. Adv Exp Med Biol 2019; 1149: 17-33.
12. Jones NL, Koletzko S, Goodman K, Bontems P, Cadranel S, Casswall T, et al. Joint ESPGHAN/NASPGHAN guidelines for the management of Helicobacter pylori in children and adolescents (Update 2016). J Pediatr Gastroenterol Nutr 2017; 64: 991-1003.
13. Patel SK, Pratap CB, Jain AK, Gulati AK, Nath G. Diagnosis of Helicobacter pylori: What should be the gold standard? World J Gastroenterol 2014; 20: 12847-12859.
14. Monteiro L, Oleastro M, Lehours P, Mégraud F. Diagnosis of Helicobacter pylori infection. Helicobacter 2009; 14 Suppl 1: 8-14.
15. Chey WD, Wong BCY, Gastroenterology PPC of the AC of. American college of gastroenterology guideline on the management of Helicobacter pylori infection. Am J Gastroenterol 2007; 102: 1808-1825.
16. Hirschl AM, Makristathis A. Methods to detect Helicobacter pylori: From culture to molecular biology. Helicobacter 2007; 12 Suppl 2: 6-11.
17. Akeel M, Elhafey A, Shehata A, Elmakki E, Aboshouk T, Ageely H, et al. Efficacy of immunohistochemical staining in detecting Helicobacter pylori in Saudi patients with minimal and atypical infection. Eur J Histochem 2021; 65: 3222.
18. Mégraud F, Lehours P. Helicobacter pylori detection and antimicrobial susceptibility testing. Clin Microbiol Rev 2007; 20: 280-322.
19. Ramis IB, De Moraes EP, Fernandes MS, Mendoza-Sassi R, Rodrigues O, Juliano CRV, et al. Evaluation of diagnostic methods for the detection of Helicobacter pylori in gastric biopsy specimens of dyspeptic patients. Braz J Microbiol 2012; 43: 903-908.
20. Diouf A, Martinez-Gomis J, Miquel M, Quesada M, Lario S, Sixou M. Comparaison de quatre paires d’amorces différentes dans la détection d’Helicobacter pylori dans les biopsies gastriques et les prélèvements oraux. Pathol Biol 2009; 57: 30-35.
21. Pandya HB, Agravat HH, Patel JS. Prevalence of Specific Helicobacter pylori CagA, VacA, IceA, UreC Genotypes and its Clinical Relevance in the Patients with Acid-Peptic Diseases. J Clin Diagn Res 2017; 11: DC23-DC26.
22. Kalaf EA, Al-Khafaji ZM, Yassen NY, Al-Abbudi FA, Sadwen SN. Study of the cytoxin-associated gene a (CagA gene) in Helicobacter pylori using gastric biopsies of Iraqi patients. Saudi J Gastroenterol 2013; 19: 69-74.
23. Chisholm SA, Owen RJ. Application of polymerase chain reaction-based assays for rapid identification and antibiotic resistance screening of Helicobacter pylori in gastric biopsies. Diagn Microbiol Infect Dis 2008; 61: 67-71.
24. Lim L-L, Ho K-Y, Ho B, Salto-Tellez M. Effect of biopsies on sensitivity and specificity of ultra-rapid urease test for detection of Helicobacter pylori infection: A prospective evaluation. World J Gastroenterol 2004; 10: 1907-1910.
25. Miftahussurur M, Yamaoka Y. Diagnostic methods of Helicobacter pylori infection for epidemiological studies: Critical importance of indirect test validation. Biomed Res Int 2016; 2016: 4819423.
26. Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, et al. Global prevalence of Helicobacter pylori infection: Systematic review and meta-analysis. Gastroenterology 2017; 153: 420-429.
27. Hasosah M. Accuracy of invasive and noninvasive methods of Helicobacter pylori infection diagnosis in Saudi children. Saudi J Gastroenterol 2019; 25: 126-131.
28. Thaker Y, Moon A, Afzali A. Helicobacter pylori: A review of epidemiology, treatment, and management. J Clin Gastroenterol Treat 2016; 2: 019.
29. Toscano EP, Madeira FF, Dutra-Rulli MP, Gonçalves LOM, Proença MA, Borghi VS, et al. Epidemiological and clinical-pathological aspects of Helicobacter pylori infection in Brazilian children and adults. Gastroenterol Res Pract 2018; 2018: 8454125.
30. Telmesani AMA. Helicobacter pylori: Prevalence and relationship with Abdominal pain in School Children in Makkah City, Western Saudi Arabia. Saudi J Gastroenterol 2009; 15: 100-103.
31. Maleknejad S, Mojtahedi A, Safaei-Asl A, Taghavi Z, Kazemnejad E. Primary antibiotic resistance to Helicobacter pylori strains isolated from children in northern Iran: A single center study. Iran J Pediatr 2015; 25(6): e2661.
32. Abbas M, Sharif FA, Osman SM, Osman AM, El Sanousi SM, Magzoub M, et al. Prevalence and associated symptoms of Helicobacter pylori infection among Schoolchildren in Kassala State, East of Sudan. Interdiscip Perspect Infect Dis 2018; 2018: 4325752.
33. Altamimi E, Alsharkhat N, Aljawarneh A, Abu Hamad MDR, Assi AA, Alawneh S, et al. Declining prevalence of Helicobacter pylori infection in Jordanian children, report from developing country. Heliyon 2020; 6(7): e04416.
34. El Khadir M, Alaoui Boukhris S, Benajah D-A, El Rhazi K, Ibrahimi SA, El Abkari M, et al. Detection of Helicobacter pylori urease antigen in saliva in patients with different gastric H. pylori status. J Chin Med Assoc 2016; 79: 363-367.
35. Benajah DA, Lahbabi M, Alaoui S, El Rhazi K, El Abkari M, Nejjari C, et al. Prevalence of Helicobacter pylori and its recurrence after successful eradication in a developing nation (Morocco). Clin Res Hepatol Gastroenterol 2013; 37: 519-526.
36. Alaoui Boukhris S, Benajah D-a, El Rhazi K, Ibrahimi SA, Nejjari C, Amarti A, et al. Prevalence and distribution of Helicobacter pylori cagA and vacA genotypes in the Moroccan population with gastric disease. Eur J Clin Microbiol Infect Dis 2012; 31: 1775-1781.
37. Fan C-C, Chen C-H, Chou C, Kao T-Y, Cheng AN, Lee AY-L, et al. A time-saving–modified Giemsa stain is a better diagnostic method of Helicobacter pylori infection compared with the rapid urease test. J Clin Lab Anal 2020; 34(4): e23110.
38. Calvet X, Sánchez-Delgado J, Montserrat A, Lario S, Ramírez-Lázaro MJ, Quesada M, et al. Accuracy of Diagnostic Tests for Helicobacter pylori: A Reappraisal. Clin Infect Dis 2009; 48: 1385-1391.
39. Lee T-H, Lin C-C, Chung C-S, Lin C-K, Liang C-C, Tsai K-C. Increasing biopsy number and sampling from gastric body improve the sensitivity of rapid urease test in patients with peptic ulcer bleeding. Dig Dis Sci 2015; 60: 454-457.
40. Seo J-H, Park JS, Yeom JS, Lim J-Y, Park C-H, Woo H-O, et al. Correlation between positive rate and number of biopsy samples on urease test in childhood Helicobacter pylori infection. J Korean Med Sci 2014; 29: 106-109.
41. Osaki T, Mabe K, Hanawa T, Kamiya S. Urease-positive bacteria in the stomach induce a false-positive reaction in a urea breath test for diagnosis of Helicobacter pylori infection. J Med Microbiol 2008; 57: 814-819.
42. Uotani T, Graham DY. Diagnosis of Helicobacter pylori using the rapid urease test. Ann Transl Med 2015; 3: 9.
43. Kalach N, Bontems P, Raymond J. Helicobacter pylori infection in children. Helicobacter 2017; 22 Suppl 1: 10.1111/hel.12414.
44. Li Y, Rimbara E, Thirumurthi S, Trespalacios A, Reddy R, Sabounchi S, et al. Detection of clarithromycin resistance in Helicobacter pylori following noncryogenic storage of rapid urease tests for 30 days. J Dig Dis 2012; 13: 54-59.
2. Roma E, Miele E. Helicobacter pylori infection in pediatrics. Helicobacter 2015; 20 Suppl 1: 47-53.
3. Hestvik E, Tylleskar T, Kaddu-Mulindwa DH, Ndeezi G, Grahnquist L, Olafsdottir E, et al. Helicobacter pylori in apparently healthy children aged 0-12 years in urban Kampala, Uganda: a community-based cross sectional survey. BMC Gastroenterol 2010; 10: 62.
4. Hasna B, Imane E, Ghizlane B, Reda JM, Abdeljabbar M, Hassan J, et al. Epidemiological study of Helicobacter pylori infection and its association with gastric carcinogenesis. Gulf J Oncolog 2021; 1: 7-13.
5. Bouihat N, Burucoa C, Benkirane A, Seddik H, Sentissi S, Al Bouzidi A, et al. Helicobacter pylori primary antibiotic resistance in 2015 in Morocco: A phenotypic and genotypic prospective and multicenter study. Microb Drug Resist 2017; 23: 727-732.
6. Sabbagh P, Javanian M, Koppolu V, Vasigala VR, Ebrahimpour S. Helicobacter pylori infection in children: an overview of diagnostic methods. Eur J Clin Microbiol Infect Dis 2019; 38: 1035-1045.
7. Burucoa C. Diagnostic tests for Helicobacter pylori infection in children. Arch Pediatr 2010; 17: 814-815.
8. Braden B. Diagnosis of Helicobacter pylori infection. BMJ 2012; 344: e828.
9. Sabbagh P, Mohammadnia-Afrouzi M, Javanian M, Babazadeh A, Koppolu V, Vasigala VR, et al. Diagnostic methods for Helicobacter pylori infection: ideals, options, and limitations. Eur J Clin Microbiol Infect Dis 2019; 38: 55-66.
10. Kraft C, Stack A, Josenhans C, Niehus E, Dietrich G, Correa P, et al. Genomic changes during chronic Helicobacter pylori infection. J Bacteriol 2006; 188: 249-254.
11. Kotilea K, Bontems P, Touati E. Epidemiology, diagnosis and risk factors of Helicobacter pylori infection. Adv Exp Med Biol 2019; 1149: 17-33.
12. Jones NL, Koletzko S, Goodman K, Bontems P, Cadranel S, Casswall T, et al. Joint ESPGHAN/NASPGHAN guidelines for the management of Helicobacter pylori in children and adolescents (Update 2016). J Pediatr Gastroenterol Nutr 2017; 64: 991-1003.
13. Patel SK, Pratap CB, Jain AK, Gulati AK, Nath G. Diagnosis of Helicobacter pylori: What should be the gold standard? World J Gastroenterol 2014; 20: 12847-12859.
14. Monteiro L, Oleastro M, Lehours P, Mégraud F. Diagnosis of Helicobacter pylori infection. Helicobacter 2009; 14 Suppl 1: 8-14.
15. Chey WD, Wong BCY, Gastroenterology PPC of the AC of. American college of gastroenterology guideline on the management of Helicobacter pylori infection. Am J Gastroenterol 2007; 102: 1808-1825.
16. Hirschl AM, Makristathis A. Methods to detect Helicobacter pylori: From culture to molecular biology. Helicobacter 2007; 12 Suppl 2: 6-11.
17. Akeel M, Elhafey A, Shehata A, Elmakki E, Aboshouk T, Ageely H, et al. Efficacy of immunohistochemical staining in detecting Helicobacter pylori in Saudi patients with minimal and atypical infection. Eur J Histochem 2021; 65: 3222.
18. Mégraud F, Lehours P. Helicobacter pylori detection and antimicrobial susceptibility testing. Clin Microbiol Rev 2007; 20: 280-322.
19. Ramis IB, De Moraes EP, Fernandes MS, Mendoza-Sassi R, Rodrigues O, Juliano CRV, et al. Evaluation of diagnostic methods for the detection of Helicobacter pylori in gastric biopsy specimens of dyspeptic patients. Braz J Microbiol 2012; 43: 903-908.
20. Diouf A, Martinez-Gomis J, Miquel M, Quesada M, Lario S, Sixou M. Comparaison de quatre paires d’amorces différentes dans la détection d’Helicobacter pylori dans les biopsies gastriques et les prélèvements oraux. Pathol Biol 2009; 57: 30-35.
21. Pandya HB, Agravat HH, Patel JS. Prevalence of Specific Helicobacter pylori CagA, VacA, IceA, UreC Genotypes and its Clinical Relevance in the Patients with Acid-Peptic Diseases. J Clin Diagn Res 2017; 11: DC23-DC26.
22. Kalaf EA, Al-Khafaji ZM, Yassen NY, Al-Abbudi FA, Sadwen SN. Study of the cytoxin-associated gene a (CagA gene) in Helicobacter pylori using gastric biopsies of Iraqi patients. Saudi J Gastroenterol 2013; 19: 69-74.
23. Chisholm SA, Owen RJ. Application of polymerase chain reaction-based assays for rapid identification and antibiotic resistance screening of Helicobacter pylori in gastric biopsies. Diagn Microbiol Infect Dis 2008; 61: 67-71.
24. Lim L-L, Ho K-Y, Ho B, Salto-Tellez M. Effect of biopsies on sensitivity and specificity of ultra-rapid urease test for detection of Helicobacter pylori infection: A prospective evaluation. World J Gastroenterol 2004; 10: 1907-1910.
25. Miftahussurur M, Yamaoka Y. Diagnostic methods of Helicobacter pylori infection for epidemiological studies: Critical importance of indirect test validation. Biomed Res Int 2016; 2016: 4819423.
26. Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, et al. Global prevalence of Helicobacter pylori infection: Systematic review and meta-analysis. Gastroenterology 2017; 153: 420-429.
27. Hasosah M. Accuracy of invasive and noninvasive methods of Helicobacter pylori infection diagnosis in Saudi children. Saudi J Gastroenterol 2019; 25: 126-131.
28. Thaker Y, Moon A, Afzali A. Helicobacter pylori: A review of epidemiology, treatment, and management. J Clin Gastroenterol Treat 2016; 2: 019.
29. Toscano EP, Madeira FF, Dutra-Rulli MP, Gonçalves LOM, Proença MA, Borghi VS, et al. Epidemiological and clinical-pathological aspects of Helicobacter pylori infection in Brazilian children and adults. Gastroenterol Res Pract 2018; 2018: 8454125.
30. Telmesani AMA. Helicobacter pylori: Prevalence and relationship with Abdominal pain in School Children in Makkah City, Western Saudi Arabia. Saudi J Gastroenterol 2009; 15: 100-103.
31. Maleknejad S, Mojtahedi A, Safaei-Asl A, Taghavi Z, Kazemnejad E. Primary antibiotic resistance to Helicobacter pylori strains isolated from children in northern Iran: A single center study. Iran J Pediatr 2015; 25(6): e2661.
32. Abbas M, Sharif FA, Osman SM, Osman AM, El Sanousi SM, Magzoub M, et al. Prevalence and associated symptoms of Helicobacter pylori infection among Schoolchildren in Kassala State, East of Sudan. Interdiscip Perspect Infect Dis 2018; 2018: 4325752.
33. Altamimi E, Alsharkhat N, Aljawarneh A, Abu Hamad MDR, Assi AA, Alawneh S, et al. Declining prevalence of Helicobacter pylori infection in Jordanian children, report from developing country. Heliyon 2020; 6(7): e04416.
34. El Khadir M, Alaoui Boukhris S, Benajah D-A, El Rhazi K, Ibrahimi SA, El Abkari M, et al. Detection of Helicobacter pylori urease antigen in saliva in patients with different gastric H. pylori status. J Chin Med Assoc 2016; 79: 363-367.
35. Benajah DA, Lahbabi M, Alaoui S, El Rhazi K, El Abkari M, Nejjari C, et al. Prevalence of Helicobacter pylori and its recurrence after successful eradication in a developing nation (Morocco). Clin Res Hepatol Gastroenterol 2013; 37: 519-526.
36. Alaoui Boukhris S, Benajah D-a, El Rhazi K, Ibrahimi SA, Nejjari C, Amarti A, et al. Prevalence and distribution of Helicobacter pylori cagA and vacA genotypes in the Moroccan population with gastric disease. Eur J Clin Microbiol Infect Dis 2012; 31: 1775-1781.
37. Fan C-C, Chen C-H, Chou C, Kao T-Y, Cheng AN, Lee AY-L, et al. A time-saving–modified Giemsa stain is a better diagnostic method of Helicobacter pylori infection compared with the rapid urease test. J Clin Lab Anal 2020; 34(4): e23110.
38. Calvet X, Sánchez-Delgado J, Montserrat A, Lario S, Ramírez-Lázaro MJ, Quesada M, et al. Accuracy of Diagnostic Tests for Helicobacter pylori: A Reappraisal. Clin Infect Dis 2009; 48: 1385-1391.
39. Lee T-H, Lin C-C, Chung C-S, Lin C-K, Liang C-C, Tsai K-C. Increasing biopsy number and sampling from gastric body improve the sensitivity of rapid urease test in patients with peptic ulcer bleeding. Dig Dis Sci 2015; 60: 454-457.
40. Seo J-H, Park JS, Yeom JS, Lim J-Y, Park C-H, Woo H-O, et al. Correlation between positive rate and number of biopsy samples on urease test in childhood Helicobacter pylori infection. J Korean Med Sci 2014; 29: 106-109.
41. Osaki T, Mabe K, Hanawa T, Kamiya S. Urease-positive bacteria in the stomach induce a false-positive reaction in a urea breath test for diagnosis of Helicobacter pylori infection. J Med Microbiol 2008; 57: 814-819.
42. Uotani T, Graham DY. Diagnosis of Helicobacter pylori using the rapid urease test. Ann Transl Med 2015; 3: 9.
43. Kalach N, Bontems P, Raymond J. Helicobacter pylori infection in children. Helicobacter 2017; 22 Suppl 1: 10.1111/hel.12414.
44. Li Y, Rimbara E, Thirumurthi S, Trespalacios A, Reddy R, Sabounchi S, et al. Detection of clarithromycin resistance in Helicobacter pylori following noncryogenic storage of rapid urease tests for 30 days. J Dig Dis 2012; 13: 54-59.
| Files | ||
| Issue | Vol 14 No 5 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i5.10960 | |
| Keywords | ||
| Helicobacter pylori; Children; Invasive tests; Rapid urease test; Polymerase chain reaction; Histology; Biopsy culture | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Hibaoui L, Massik A, Lebbar Z, Yahyaoui G, Mahmoud M, Bougnouch L, Hamass N, Chbani L, Bennani B, Amine Berrahou M, Lakhdar Idriss M, Hida M. The high sensitivity and specificity of rapid urease test in diagnosis of Helicobacter pylori infection in Moroccan children. Iran J Microbiol. 2022;14(5):669-676.
