Distinguishing Features of Autoimmune Gastritis Depending on Previous Helicobacter pylori Infection or Positivity to Anti-Parietal Cell Antibodies: Results From the Autoimmune gastRitis Italian netwOrk Study grOup (ARIOSO)

Marco Vincenzo Lenti; Emanuela Miceli; Edith Lahner; Gabriele Natalello; Sara Massironi; Annalisa Schiepatti; Fabiana Zingone; Valentina Sciola; Roberta Elisa Rossi; Renato Cannizzaro; Elena Maria De Giorgi; Virginia Gregorio; Erica Fazzino; Antonella Gentile; Clarissa Petrucci; Emanuele Dilaghi; Giulia Pivetta; Alessandro Vanoli; Ombretta Luinetti; Marco Paulli; Andrea Anderloni; Maurizio Vecchi; Federico Biagi; Alessandro Repici; Edoardo Vincenzo Savarino; Shamim Joudaki; Mariangela Delliponti; Alessandra Pasini; Federica Facciotti; Fabio Farinati; Mario Milco D'Elios; Chiara Della Bella; Bruno Annibale; Catherine Klersy; Gino Roberto Corazza; Antonio Di Sabatino

doi:10.14309/ajg.0000000000002948

Distinguishing Features of Autoimmune Gastritis Depending on Previous Helicobacter pylori Infection or Positivity to Anti-Parietal Cell Antibodies: Results From the Autoimmune gastRitis Italian netwOrk Study grOup (ARIOSO)

Am J Gastroenterol. 2024 Jul 5. doi: 10.14309/ajg.0000000000002948. Online ahead of print.

Authors

Marco Vincenzo Lenti^{1

2}, Emanuela Miceli¹, Edith Lahner³, Gabriele Natalello^{1

2}, Sara Massironi⁴, Annalisa Schiepatti^{1

5}, Fabiana Zingone⁶, Valentina Sciola⁷, Roberta Elisa Rossi⁸, Renato Cannizzaro⁹, Elena Maria De Giorgi¹, Virginia Gregorio¹, Erica Fazzino¹, Antonella Gentile¹, Clarissa Petrucci¹, Emanuele Dilaghi³, Giulia Pivetta³, Alessandro Vanoli¹⁰, Ombretta Luinetti¹⁰, Marco Paulli¹⁰, Andrea Anderloni¹¹, Maurizio Vecchi⁷, Federico Biagi^{1

5}, Alessandro Repici^{8

12}, Edoardo Vincenzo Savarino⁶, Shamim Joudaki^{1

2}, Mariangela Delliponti², Alessandra Pasini², Federica Facciotti¹³, Fabio Farinati⁶, Mario Milco D'Elios¹⁴, Chiara Della Bella¹⁴, Bruno Annibale³, Catherine Klersy¹⁵, Gino Roberto Corazza^{1

2}, Antonio Di Sabatino^{1

2}

Affiliations

¹ Department of Internal Medicine and Medical Therapeutics, University of Pavia, Pavia, Italy.
² First Department of Internal Medicine, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.
³ Department of Medical-Surgical Sciences and Translational Medicine, Sant'Andrea Hospital, Sapienza University of Rome, Rome, Italy.
⁴ Division of Gastroenterology and Center for Autoimmune Liver Diseases, Department of Medicine and Surgery, Fondazione IRCCS San Gerardo dei Tintori; University of Milano-Bicocca, Monza, Italy.
⁵ Gastroenterology Unit of Pavia Institute, Istituti Clinici Scientifici Maugeri IRCCS, Pavia, Italy.
⁶ Department of Surgery, Oncology and Gastroenterology, University of Padua, Padua, Italy, Gastroenterology Unit, Azienda Ospedale-Università Padova, Padua, Italy.
⁷ Gastroenterology and Endoscopy Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico Milano, Milan, Italy.
⁸ Gastroenterology and Endoscopy Unit, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy.
⁹ Oncological Gastroenterology, Centro di Riferimento Oncologico di Aviano (CRO) IRCCS, Italy, Department of Medical, Surgical and Health Sciences, University of Trieste, Italy.
¹⁰ Unit of Anatomic Pathology, Department of Molecular Medicine, University of Pavia, and IRCCS San Matteo Hospital Foundation, Pavia, Italy.
¹¹ Gastroenterology and Digestive Endoscopy Unit, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.
¹² Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy.
¹³ IEO, European Institute of Oncology IRCCS, Department of Experimental Oncology, Milan, Italy; University of Milano-Bicocca, Department of Biotechnology and Biosciences, Milan, Italy.
¹⁴ Department of Molecular and Developmental Medicine, University of Siena, Siena, Italy.
¹⁵ Biostatistics & Clinical Trial Center, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.

PMID: 38976374
DOI: 10.14309/ajg.0000000000002948

Abstract

Introduction: To describe the clinical features and the risk of developing gastric tumors in patients with autoimmune gastritis (AIG).

Methods: This was a retrospective, longitudinal, multicenter study conducted at 8 Italian tertiary referral centers. We retrieved clinical data from all histologically proven patients with AIG. Differences between Helicobacter pylori -exposed vs H. pylori -naive and anti-parietal cell antibody (PCA)-positive vs PCA-negative patients were investigated. The rate of gastric adenocarcinoma and type 1 gastric neuroendocrine neoplasm (gNEN) was assessed. A multivariable model for factors associated with gNEN was fitted.

Results: A total of 1,598 patients with AIG (median age 58 years, interquartile range 46-68; F:M ratio 2.7:1) were included. H. pylori -naive patients were more likely to have a first-degree family history of AIG (14.7% vs 8.9%; P = 0.012), type 1 diabetes mellitus (4.9% vs 2.3%; P = 0.025), and pernicious anemia (30.9% vs 21.1%; P = 0.003). PCA-positive patients had significantly more associated autoimmune diseases (59.0% vs 42.9%; P < 0.001) and were more likely to have been diagnosed by a case-finding strategy (15.3% vs 2.6%; P < 0.001). Overall, 15 cases (0.9%) of gastric adenocarcinoma and 153 cases (9.6%) of gNEN occurred, with a global rate of 0.12 (95% confidence interval [CI] 0.07-0.20) and 1.22 (95% CI 1.03-1.42) per 100 person/year, respectively. Having a vitamin B12/iron deficiency manifestation at AIG diagnosis was associated with a 16.44 (95% CI 9.94-27.20 P < 0.001) hazard ratio of gNEN.

Discussion: The "pure" AIG pattern has typical features of an autoimmune disease and seems to be unrelated to H. pylori . In a tertiary referral setting, the risk of developing overt gastric adenocarcinoma is low, while patients with vitamin B12 deficiency complications at onset may benefit from a more intense endoscopic follow-up for early gNEN detection.