Helicobacter pylori: Pathology and diagnostic strategies

American Journal of Clinical Pathology

Volumn 119, Issue 3, 2003, Pages 403-412

  Versalovic, James ^a  

^a TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

Duodenal ulcer; Gastric adenocarcinoma; Gastric cancer; Gastritis; Helicobacter pylori; Histology; MALT lymphoma; Peptic ulcer; Serology; Urease testing

Indexed keywords

AMOXICILLIN; ANTIBIOTIC AGENT; BACTERIAL ANTIGEN; BACTERIAL DNA; BISMUTH DERIVATIVE; CD4 ANTIGEN; CD8 ANTIGEN; CLARITHROMYCIN; COMPLEMENT; GAMMA INTERFERON; HISTAMINE H2 RECEPTOR ANTAGONIST; IMMUNOGLOBULIN A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 8; LEUKOTRIENE; MACROLIDE; METRONIDAZOLE; OMEPRAZOLE; PROTON PUMP INHIBITOR; RIBOSOME DNA; RIBOSOME RNA; TETRACYCLINE; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG; UREASE;

ANTIBIOTIC SENSITIVITY; ANTIBIOTIC THERAPY; ANTIGEN DETECTION; BACTERIUM CULTURE; BACTERIUM ISOLATE; CANCER RISK; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST; DISEASE ASSOCIATION; DRUG EFFICACY; DUODENOSCOPY; ERADICATION THERAPY; ESOPHAGOGASTRODUODENOSCOPY; ESOPHAGOSCOPY; FECES ANALYSIS; GASTROSCOPY; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HISTOPATHOLOGY; HUMAN; LABORATORY TEST; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR GENETICS; MUCOSA ASSOCIATED LYMPHOID TISSUE LYMPHOMA; NONHUMAN; PEPTIC ULCER; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVIEW; SENSITIVITY AND SPECIFICITY; SERODIAGNOSIS; STOMACH ADENOCARCINOMA; STOMACH CANCER; TECHNIQUE; UREA BREATH TEST; ADENOCARCINOMA; BREATH ANALYSIS; DIAGNOSTIC PROCEDURE; DIGESTIVE TRACT ENDOSCOPY; FECES; IMMUNOLOGY; ISOLATION AND PURIFICATION; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; STOMACH TUMOR;

ADENOCARCINOMA; ANTIGENS, BACTERIAL; BREATH TESTS; ENDOSCOPY, DIGESTIVE SYSTEM; FECES; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; LYMPHOMA, MUCOSA-ASSOCIATED LYMPHOID TISSUE; MICROBIAL SENSITIVITY TESTS; MOLECULAR DIAGNOSTIC TECHNIQUES; PEPTIC ULCER; STOMACH NEOPLASMS; UREASE;

EID: 0037362944     PISSN: 00029173     EISSN: None     Source Type: Journal    
DOI: 10.1309/5DTF5HT7NPLNA6J5     Document Type: Review

References (106)

1. Warren JR, Marshall BJ. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet. 1983;1:1273-1275.
2. NIH Consensus Development Panel on Helicobacter pylori in Peptic Ulcer Disease. NIH Consensus Conference: Helicobacter pylori in peptic ulcer disease. JAMA. 1994;272:65-69.
3. Neil GA. Do ulcers burn out or burn on? Managing duodenal ulcer diathesis in the Helicobacter pylori era. Am J Gastroenterol. 1997;92:387-393.
4. Tomb JF, White O, Kerlavage AR, et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature. 1997;388:539-547.
5. Alm RA, Ling LS, Moir DT, et al. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature. 1999;397:176-180.
6. Sonnenberg A, Everhart JE. The prevalence of self-reported peptic ulcer in the United States. Am J Public Health. 1996;86:200-205.
7. Dunn BE, Cohen H, Blaser MJ. Helicobacter pylori. Clin Microbiol Rev. 1997;10:720-741.
8. Cullen DJ, Collins BJ, Christiansen KJ, et al. When is Helicobacter pylori infection acquired? Gut. 1993;34:1681-1682.
9. Kosunen TU, Aromaa A, Knekt P, et al. Helicobacter antibodies in 1973 and 1994 in the adult population of Vammala, Finland. Epidemiol Infect. 1997;119:29-34.
10. Sipponen P, Kosunen TU, Samloff IM, et al. Rate of Helicobacter pylori acquisition among Finnish adults: a fifteen year follow-up. Scand J Gastroenterol. 1996;31:229-232.
11. Weir S, Cuccherini B, Whitney AM, et al. Recurrent bacteremia caused by a "Flexispira"-like organism in a patient with X-linked (Bruton's) agammaglobulinemia. J Clin Microbiol. 1999;37:2439-2445.
12. Eslick GD, Lim LL, Byles JE, et al. Association of Helicobacter pylori infection with gastric carcinoma: a meta-analysis. Am J Gastroenterol. 1999;94:2373-2379.
13. Graham DY, Rabeneck L. Patients, payers, and paradigm shifts: what to do about Helicobacter pylori [editorial]. Am J Gastroenterol. 1996;91:188-190.
14. Graham DY, De Boer WA, Tytgat GN. Choosing the best anti-Helicobacter pylori therapy: effect of antimicrobial resistance. Am J Gastroenterol. 1996;91:1072-1076.
15. Hunt RH. Peptic ulcer disease: defining the treatment strategies in the era of Helicobacter pylori. Am J Gastroenterol. 1997;92(4 suppl):36S-43S.
16. O'Connor F, Buckley M, O'Morain C. Helicobacter pylori: the cancer link. J R Soc Med. 1996;89:674-678.
17. Isaacson PG. Gastric lymphoma and Helicobacter pylori [editorial]. N Engl J Med. 1994;330:1310-1311.
18. Peek RM Jr, Blaser MJ. Pathophysiology of Helicobacter pylori-induced gastritis and peptic ulcer disease. Am J Med. 1997;102:200-207.
19. Marshall BJ. Helicobacter pylori. Am J Gastroenterol. 1994;89(8 suppl):S116-S128.
20. Glupczynski Y. The diagnosis of Helicobacter pylori infection: a microbiologist's perspective. Rev Med Microbiol. 1994;5:199-208.
21. Cutler AF. Testing for Helicobacter pylori in clinical practice. Am J Med. 1996;100:35S-39S.
22. Suerbaum S, Michetti P. Helicobacter pylori infection. N Engl J Med. 2002;347:1175-1186.
23. Sharma P, Topalovski M, Mayo MS, et al. Helicobacter pylori eradication dramatically improves inflammation in the gastric cardia. Am J Gastroenterol. 2000;95:3107-3111.
24. Rubin CE. Are there three types of Helicobacter pylori gastritis? Gastroenterology. 1997;112:2108-2110.
25. Faller G, Kirchner T. Helicobacter pylori and antigastric autoimmunity [in German]. Pathologe. 2001;22:25-30.
26. Uemura N, Okamoto S, Yamamoto S, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001;345:784-789.
27. Shapiro JL, Goldblum JR, Petras RE. A clinicopathologic study of 42 patients with granulomatous gastritis: is there really an "idiopathic" granulomatous gastritis? Am J Surg Pathol. 1996;20:462-470.
28. Ectors NL, Dixon MF, Geboes KJ, et al. Granulomatous gastritis: a morphological and diagnostic approach. Histopathology. 1993;23:55-61.
29. Wu TT, Hamilton SR. Lymphocytic gastritis: association with etiology and topology. Am J Surg Pathol. 1999;23:153-158.
30. Hayat M, Arora DS, Dixon MF, et al. Effects of Helicobacter pylori eradication on the natural history of lymphocytic gastritis. Gut. 1999;45:495-498.
31. Niemela S, Karttunen TJ, Kerola T. Treatment of Helicobacter pylori in patients with lymphocytic gastritis. Hepatogastroenterology. 2001;48:1176-1178.
32. Parsonnet J. Helicobacter pylori in the stomach: a paradox unmasked [editorial]. N Engl J Med. 1996;335:278-280.
33. Parsonnet J, Hansen S, Rodriguez L, et al. Helicobacter pylori infection and gastric lymphoma. N Engl J Med. 1994;330:1267-1271.
34. Bayerdorffer E, Oertel H, Lehn N, et al. Topographic association between active gastritis and Campylobacter pylori colonisation. J Clin Pathol. 1989;42:834-839.
35. Laine L, Chun D, Stein C, et al. The influence of size or number of biopsies on rapid urease test results: a prospective evaluation. Gastrointest Endosc. 1996;43:49-53.
36. Greenberg PD, Koch J, Cello JP. Clinical utility and cost effectiveness of Helicobacter pylori testing for patients with duodenal and gastric ulcers. Am J Gastroenterol. 1996;91:228-232.
37. Kuipers EJ. Helicobacter pylori and the risk and management of associated diseases: gastritis, ulcer disease, atrophic gastritis and gastric cancer. Aliment Pharmacol Ther. 1997;11(suppl 1):71-88.
38. Arista-Nasr J, Jimenez-Rosas F, Uribe-Uribe N, et al. Pathological disorders of the gastric mucosa surrounding carcinomas and primary lymphomas. Am J Gastroenterol. 2001;96:1746-1750.
39. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process: First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res. 1992;52:6735-6740.
40. Russmann H, Kempf VA, Koletzko S, et al. Comparison of fluorescent in situ hybridization and conventional culturing for detection of Helicobacter pylori in gastric biopsy specimens. J Clin Microbiol. 2001;39:304-308.
41. Keates S, Hitti YS, Upton M, et al. Helicobacter pylori infection activates NF-kappa B in gastric epithelial cells. Gastroenterology. 1997;113:1099-1109.
42. Munzenmaier A, Lange C, Glocker E, et al. A secreted/shed product of Helicobacter pylori activates transcription factor nuclear factor-kappa B. J Immunol. 1997;159:6140-6147.
43. Fischer W, Puls J, Buhrdorf R, et al. Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol Microbiol. 2001;42:1337-1348.
44. Crabtree JE, Farmery SM, Lindley IJ, et al. CagA/cytotoxic strains of Helicobacter pylori and interleukin-8 in gastric epithelial cell lines. J Clin Pathol. 1994;47:945-950.
45. Crabtree JE, Covacci A, Farmery SM, et al. Helicobacter pylori induced interleukin-8 expression in gastric epithelial cells is associated with CagA positive phenotype. J Clin Pathol. 1995;48:41-45.
46. Censini S, Lange C, Xiang Z, et al. Cag, a pathogenicity island of Helicobacter pylori, encodes type 1-specific and disease-associated virulence factors. Proc Natl Acad Sci U S A. 1996;93:14648-14653.
47. Akopyants NS, Clifton SW, Kersulyte D, et al. Analyses of the cag pathogenicity island of Helicobacter pylori. Mol Microbiol. 1998;28:37-53.
48. Day AS, Jones NL, Lynett JT, et al. cagE is a virulence factor associated with Helicobacter pylori-induced duodenal ulceration in children. J Infect Dis. 2000;181:1370-1375.
49. Karttunen RA, Karttunen TJ, Yousfi MM, et al. Expression of mRNA for interferon-gamma, interleukin-10, and interleukin-12 (p40) in normal gastric mucosa and in mucosa infected with Helicobacter pylori. Scand J Gastroenterol. 1997;32:22-27.
50. Tomita T, Jackson AM, Hida N, et al. Expression of interleukin-18, a Th1 cytokine, in human gastric mucosa is increased in Helicobacter pylori infection. J Infect Dis. 2001;183:620-627.
51. Guiraldes E, Duarte I, Pena A, et al. Proinflammatory cytokine expression in gastric tissue from children with Helicobacter pylori-associated gastritis. J Pediatr Gastroenterol Nutr. 2001;33:127-132.
52. Lehmann FS, Terracciano L, Carena I, et al. In situ correlation of cytokine secretion and apoptosis in Helicobacter pylori-associated gastritis. Am J Physiol Gastrointest Liver Physiol. 2002;283:G481-G488.
53. Houghton J, Fox JG, Wang TC. Gastric cancer: laboratory bench to clinic. J Gastroenterol Hepatol. 2002;17:495-502.
54. Rathbone BJ, Wyatt JI, Worsley BW, et al. Systemic and local antibody responses to gastric Campylobacter pyloridis in non-ulcer dyspepsia. Gut. 1986;27:642-647.
55. Perez-Perez GI, Dworkin BM, Chodos JE, et al. Campylobacter pylori antibodies in humans. Ann Intern Med. 1988;109:11-17.
56. Morris A, Nicholson G. Ingestion of Campylobacter pyloridis causes gastritis and raised fasting gastric pH. Am J Gastroenterol. 1987;82:192-199.
57. Sobala GM, Crabtree JE, Dixon MF, et al. Acute Helicobacter pylori infection: clinical features, local and systemic immune response, gastric mucosal histology, and gastric juice ascorbic acid concentrations. Gut. 1991;32:1415-1418.
58. Claeys D, Faller G, Appelmelk BJ, et al. The gastric H+,K+-ATPase is a major autoantigen in chronic Helicobacter pylori gastritis with body mucosa atrophy. Gastroenterology. 1998;115:340-347.
59. Kimmel B, Bosserhoff A, Frank R, et al. Identification of immunodominant antigens from Helicobacter pylori and evaluation of their reactivities with sera from patients with different gastroduodenal pathologies. Infect Immun. 2000;68:915-920.
60. Laheij RJ, Straatman H, Jansen JB, et al. Evaluation of commercially available Helicobacter pylori serology kits: a review. J Clin Microbiol. 1998;36:2803-2809.
61. Meijer BC, Thijs JC, Kleibeuker JH, et al. Evaluation of eight enzyme immunoassays for detection of immunoglobulin G against Helicobacter pylori. J Clin Microbiol. 1997;35:292-294.
62. Wilcox MH, Dent TH, Hunter JO, et al. Accuracy of serology for the diagnosis of Helicobacter pylori infection: a comparison of eight kits. J Clin Pathol. 1996;49:373-376.
63. Cutler AF, Havstad S, Ma CK, et al. Accuracy of invasive and noninvasive tests to diagnose Helicobacter pylori infection. Gastroenterology. 1995;109:136-141.
64. Vakil N, Rhew D, Soll A, et al. The cost-effectiveness of diagnostic testing strategies for Helicobacter pylori. Am J Gastroenterol. 2000;95:1691-1698.
65. Hilzenrat N, Lamoureux E, Weintrub I, et al. Helicobacter heilmannii-like spiral bacteria in gastric mucosal biopsies: prevalence and clinical significance. Arch Pathol Lab Med. 1995;119:1149-1153.
66. Fabris P, Bozzola L, Benedetti P, et al. H pylori infection in HIV-positive patients: a serohistological study. Dig Dis Sci. 1997;42:289-292.
67. European Helicobacter pylori Study Group. Current European concepts in the management of Helicobacter pylori infection: the Maastricht Consensus Report. Gut. 1997;41:8-13.
68. Faigel DO, Magaret N, Corless C, et al. Evaluation of rapid antibody tests for the diagnosis of Helicobacter pylori infection. Am J Gastroenterol. 2000;95:72-77.
69. Jaskowski TD, Martins TB, Hill HR, et al. Immunoglobulin A antibodies to Helicobacter pylori. J Clin Microbiol. 1997;35:2999-3000.
70. Hu LT, Mobley HL. Purification and N-terminal analysis of urease from Helicobacter pylori. Infect Immun. 1990;58:992-998.
71. Hazell SL, Mendz GL. How Helicobacter pylori works: an overview of the metabolism of Helicobacter pylori. Helicobacter. 1997;2:1-12.
72. Marshall BJ, Warren JR, Francis GJ, et al. Rapid urease test in the management of Campylobacter pyloridis-associated gastritis. Am J Gastroenterol. 1987;82:200-210.
73. Hazell SL, Borody TJ, Gal A, et al. Campylobacter pyloridis gastritis, I: detection of urease as a marker of bacterial colonization and gastritis. Am J Gastroenterol. 1987;82:292-296.
74. Bermejo F, Boixeda D, Gisbert JP, et al. Rapid urease test utility for Helicobacter pylori infection diagnosis in gastric ulcer disease. Hepatogastroenterology. 2002;49:572-575.
75. Monteiro L, de Mascarel A, Sarrasqueta AM, et al. Diagnosis of Helicobacter pylori infection: noninvasive methods compared to invasive methods and evaluation of two new tests. Am J Gastroenterol. 2001;96:353-358.
76. Monteiro L, Cabrita J, Megraud F. Evaluation of performances of three DNA enzyme immunoassays for detection of Helicobacter pylori PCR products from biopsy specimens. J Clin Microbiol. 1997;35:2931-2936.
77. Eshun JK, Black DD, Casteel HB, et al. Comparison of immunohistochemistry and silver stain for the diagnosis of pediatric Helicobacter pylori infection in urease-negative gastric biopsies. Pediatr Dev Pathol. 2001;4:82-88.
78. Pena JA, McNeil K, Fox JG, et al. Molecular evidence of Helicobacter cinaedi organisms in human gastric biopsy specimens. J Clin Microbiol. 2002;40:1511-1513.
79. Slomianski A, Schubert T, Cutler AF. [13C]urea breath test to confirm eradication of Helicobacter pylori. Am J Gastroenterol. 1995;90:224-226.
80. Klein PD, Malaty HM, Martin RF, et al. Noninvasive detection of Helicobacter pylori infection in clinical practice: the 13C urea breath test. Am J Gastroenterol. 1996;91:690-694.
81. Graham DY, Malaty HM, Cole RA, et al. Simplified 13C-urea breath test for detection of Helicobacter pylori infection. Am J Gastroenterol. 2001;96:1741-1745.
82. Graham DY, Klein PD, Evans DJ Jr, et al. Campylobacter pylori detected noninvasively by the 13C-urea breath test. Lancet. 1987;1:1174-1177.
83. Makristathis A, Pasching E, Schutze K, et al. Detection of Helicobacter pylori in stool specimens by PCR and antigen enzyme immunoassay. J Clin Microbiol. 1998;36:2772-2774.
84. Lu JJ, Perng CL, Shyu RY, et al. Comparison of five PCR methods for detection of Helicobacrer pylori DNA in gastric tissues. J Clin Microbiol. 1999;37:772-774.
85. van Doorn LJ, Henskens Y, Nouhan N, et al. The efficacy of laboratory diagnosis of Helicobacter pylori infections in gastric biopsy specimens is related to bacterial density and vacA, cagA, and iceA genotypes. J Clin Microbiol. 2000;38:13-17.
86. Maeda S, Yoshida H, Ogura K, et al. Helicobacter pylori specific nested PCR assay for the detection of 23S rRNA mutations associated with clarithromycin resistance. Gut. 1998;43:317-321.
87. Gramley WA, Asghar A, Frierson HF Jr, et al. Detection of Helicobacter pylori DNA in fecal samples from infected individuals. J Clin Microbiol. 1999;37:2236-2240.
88. Song Q, Haller B, Schmid RM, et al. Helicobacter pylori in dental plaque: a comparison of different PCR primer sets. Dig Dis Sci, 1999;44:479-484.
89. He Q, Wang JP, Osato M, et al. Real-time quantitative PCR for detection of Helicobacter pylori. J Clin Microbiol. 2002;40:3720-3728.
90. Harris A, Misiewicz JJ. Treating Helicobacter pylori: the best is yet to come? Gut. 1996;39:781-783.
91. Goddard AF, Logan RP. Antimicrobial resistance and Helicobacter pylori. J Antimicrob Chemother. 1996;37:639-643.
92. Vakil N, Hahn B, McSorley D. Clarithromycin-resistant Helicobacter pylori in patients with duodenal ulcer in the United States. Am J Gastroenterol. 1998;93:1432-1435.
93. Osato MS, Reddy R, Reddy SG, et al. Pattern of primary resistance of Helicobacter pylori to metronidazole or clarithromycin in the United States. Arch Intern Med. 2001;161:1217-1220.
94. Hardy DJ, Hanson CW, Hensey DM, et al. Susceptibility of Campylobacter pylori to macrolides and fluoroquinolones. J Antimicrob Chemother. 1988;22:631-636.
95. DeCross AJ, Marshall BJ, McCallum RW, et al. Metronidazole susceptibility testing for Helicobacter pylori: comparison of disk, broth, and agar dilution methods and their clinical relevance. J Clin Microbiol. 1993;31:1971-1974.
96. Hachem CY, Clarridge JE, Reddy R, et al. Antimicrobial susceptibility testing of Helicobacter pylori: comparison of E-test, broth microdilution, and disk diffusion for ampicillin, clarithromycin, and metronidazole. Diagn Microbiol Infect Dis. 1996;24:37-41.
97. National Committee for Clinical Laboratory Standards. Performance Standards for Antimicrobial Susceptibility Testing; Twelfth Informational Supplement. Wayne, PA: NCCLS; 2002:117. Approved Guideline M100-S12.
98. Versalovic J, Shortridge D, Kibler K, et al. Mutations in 23S rRNA are associated with clarithromycin resistance in Helicobacter pylori. Antimicrob Agents Chemother. 1996;40:477-480.
99. Debets-Ossenkopp YJ, Sparrius M, Kusters JG, et al. Mechanism of clarithromycin resistance in clinical isolates of Helicobacter pylori. FEMS Microbiol Lett. 1996;142:37-42.
100. Stone GG, Shortridge D, Versalovic J, et al. A PCR-oligonucleotide ligation assay to determine the prevalence of 23S rRNA gene mutations in clarithromycin-resistant Helicobacter pylori. Antimicrob Agents Chemother. 1997;41:712-714.
101. Versalovic J, Osato MS, Spakovsky K, et al. Point mutations in the 23S rRNA gene of Helicobacter pylori associated with different levels of clarithromycin resistance. J Antimicrob Chemother. 1997;40:283-286.
102. Pena JA, Fox JG, Ferraro MJ, et al. Molecular resistance testing of Helicobacter pylori in gastric biopsies. Arch Pathol Lab Med. 2001;125:493-497.
103. van Doorn LJ, Debets-Ossenkopp YJ, Marais A, et al. Rapid detection, by PCR and reverse hybridization, of mutations in the Helicobacter pylori 23S rRNA gene, associated with macrolide resistance. Antimicrob Agents Chemother. 1999;43:1779-1782.
104. van Doorn LJ, Glupczynski Y, Kusters JG, et al. Accurate prediction of macrolide resistance in Helicobacter pylori by a PCR line probe assay for detection of mutations in the 23S rRNA gene: multicenter validation study. Antimicrob Agents Chemother, 2001;45:1500-1504.
105. Chisholm SA, Owen RJ, Teare EL, et al. PCR-based diagnosis of Helicobacter pylori infection and real-time determination of clarithromycin resistance directly from human gastric biopsy samples. J Clin Microbiol. 2001;39:1217-1220.
106. Bazzoli F, Zagari M, Fossi S, et al. Urea breath tests for the detection of Helicobacter pylori infection. Helicobacter. 1997;2(suppl 1):S34-S37.