Skip to main content
Erschienen in: Indian Journal of Gastroenterology 2/2020

20.05.2020 | Original Article

Changes in the severity of gastric mucosal inflammation associated with Helicobacter pylori in humans coinfected with  intestinal helminths

verfasst von: Alisbeth Fuenmayor-Boscán, Ileana Hernández-Rincón, Gabriel Arismendi-Morillo, Edgardo Mengual, Zulbey Rivero, Gisela Romero, Maribel Lizarzábal, Melchor Álvarez-Mon

Erschienen in: Indian Journal of Gastroenterology | Ausgabe 2/2020

Einloggen, um Zugang zu erhalten

Abstract

Background

Though a few studies in animal models suggest that intestinal helminths (IH) favorably affect evolution of gastritis associated with Helicobacter pylori (H. pylori) the studies supporting this concept in humans are only a few and are based on serological data.

Methods

To evaluate the possible influence of IH on the human gastric mucosa, three groups of Venezuelan adults with gastropathy (endoscopically diagnosed) were studied: H. pylori−/IH− (n = 17), H. pylori+/IH− (n = 18), and H. pylori+/IH+ (n = 11). Histological analysis (hematoxylin-eosin) and immunohistochemical staining (peroxidase) for cytokines interleukin-1beta (IL-1β), tumor necrosis factor alpha (TNF-α), gamma interferon (IFN-γ), and interleukin 4 (IL-4) were undertaken in gastric antral biopsies.

Results

Expression of the four cytokines was detected in all individuals in varying degrees, but proinflammatory cytokines were expressed in a higher degree in the H. pylori+/IH− group, mainly IL-1β (Th1-dominant immune response), associated with a higher degree of both histological inflammation and gastric cancer risk index (GCRI), as compared to the H. pylori−/IH− group. In contrast, an increased expression of IL-4 and a reduced expression of proinflammatory cytokines (Th2-dominant response), plus the tendency to a lower degree of mononuclear infiltration, mucosal atrophy in gastric corpus, and GCRI, were evidenced in the coinfected group.

Conclusions

The findings of the present study is perhaps the first histological evidence of a possible modulatory effect of IH on the gastric mucosal inflammatory response due to H. pylori infection in humans.
Literatur
1.
Zurück zum Zitat Atherton JC, Blaser MJ. Coadaptation of Helicobacter pylori and humans: ancient history, modern implications. J Clin Invest. 2009;119:2475–87.CrossRef Atherton JC, Blaser MJ. Coadaptation of Helicobacter pylori and humans: ancient history, modern implications. J Clin Invest. 2009;119:2475–87.CrossRef
2.
Zurück zum Zitat Oluwasola AO. Genetic determinants and clinico-pathological outcomes of Helicobacter pylori infection. Ann Ib Postgrad Med. 2014;12:22–30.PubMedPubMedCentral Oluwasola AO. Genetic determinants and clinico-pathological outcomes of Helicobacter pylori infection. Ann Ib Postgrad Med. 2014;12:22–30.PubMedPubMedCentral
3.
Zurück zum Zitat Fox JG, Beck P, Dangler CA, et al. Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces Helicobacter-induced gastric atrophy. Nat Med. 2000;6:536–42.CrossRef Fox JG, Beck P, Dangler CA, et al. Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces Helicobacter-induced gastric atrophy. Nat Med. 2000;6:536–42.CrossRef
4.
Zurück zum Zitat Wroblewski LE, Peek RM, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Microbiol Rev. 2010;23:713–39.CrossRef Wroblewski LE, Peek RM, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Microbiol Rev. 2010;23:713–39.CrossRef
5.
Zurück zum Zitat Rogers AB. Gastric Helicobacter spp. in animal models: pathogenesis and modulation by extragastric coinfections. Methods Mol Biol. 2012;921:175–88.CrossRef Rogers AB. Gastric Helicobacter spp. in animal models: pathogenesis and modulation by extragastric coinfections. Methods Mol Biol. 2012;921:175–88.CrossRef
6.
Zurück zum Zitat Whary MT, Muthupalani S, Ge Z, et al. Helminth co-infection in Helicobacter pylori infected INS-GAS mice attenuates gastric premalignant lesions of epithelial dysplasia and glandular atrophy and preserves colonization resistance of the stomach to lower bowel microbiota. Microbes Infect. 2014;16:345–55.CrossRef Whary MT, Muthupalani S, Ge Z, et al. Helminth co-infection in Helicobacter pylori infected INS-GAS mice attenuates gastric premalignant lesions of epithelial dysplasia and glandular atrophy and preserves colonization resistance of the stomach to lower bowel microbiota. Microbes Infect. 2014;16:345–55.CrossRef
7.
Zurück zum Zitat Martin HR, Shakya KP, Muthupalani S, et al. Brugia filariasis differentially modulates persistent Helicobacter pylori gastritis in the gerbil model. Microbes Infect. 2010;12:748–58.CrossRef Martin HR, Shakya KP, Muthupalani S, et al. Brugia filariasis differentially modulates persistent Helicobacter pylori gastritis in the gerbil model. Microbes Infect. 2010;12:748–58.CrossRef
8.
Zurück zum Zitat Whary MT, Sundina N, Bravo LE, et al. Intestinal helminthiasis in Colombian children promotes a Th2 response to Helicobacter pylori: possible implications for gastric carcinogenesis. Cancer Epidemiol Biomark Prev. 2005;14:1464–9.CrossRef Whary MT, Sundina N, Bravo LE, et al. Intestinal helminthiasis in Colombian children promotes a Th2 response to Helicobacter pylori: possible implications for gastric carcinogenesis. Cancer Epidemiol Biomark Prev. 2005;14:1464–9.CrossRef
9.
Zurück zum Zitat Ek C, Whary MT, Ihrig M, Bravo LE, Correa P, Fox JG. Serologic evidence that Ascaris and Toxoplasma infections impact inflammatory responses to Helicobacter pylori in Colombians. Helicobacter. 2012;17:107–15. Ek C, Whary MT, Ihrig M, Bravo LE, Correa P, Fox JG. Serologic evidence that Ascaris and Toxoplasma infections impact inflammatory responses to Helicobacter pylori in Colombians. Helicobacter. 2012;17:107–15.
10.
Zurück zum Zitat Arismendi-Morillo G, Hernández I, Mengual E, Fuenmayor A, Romero G, Lizarzábal M. Comparison of three methods based on endoscopic gastric biopsies for diagnosis of Helicobacter pylori active infection in a clinical setting. Arq Gastroenterol. 2011;48:190–4. Arismendi-Morillo G, Hernández I, Mengual E, Fuenmayor A, Romero G, Lizarzábal M. Comparison of three methods based on endoscopic gastric biopsies for diagnosis of Helicobacter pylori active infection in a clinical setting. Arq Gastroenterol. 2011;48:190–4.
11.
Zurück zum Zitat Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The Updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol. 1996;20:1161–81.CrossRef Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The Updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol. 1996;20:1161–81.CrossRef
12.
Zurück zum Zitat Meining A, Bayerdörffer E, Müller P, et al. Gastric carcinoma risk index in patients infected with Helicobacter pylori. Virchows Arch. 1998;432:311–4.CrossRef Meining A, Bayerdörffer E, Müller P, et al. Gastric carcinoma risk index in patients infected with Helicobacter pylori. Virchows Arch. 1998;432:311–4.CrossRef
13.
Zurück zum Zitat Serrano C, Diaz MI, Valdivia A, et al. Relationship between Helicobacter pylori virulence factors and regulatory cytokines as predictors of clinical outcome. Microbes Infect. 2007;9:428–34.CrossRef Serrano C, Diaz MI, Valdivia A, et al. Relationship between Helicobacter pylori virulence factors and regulatory cytokines as predictors of clinical outcome. Microbes Infect. 2007;9:428–34.CrossRef
14.
Zurück zum Zitat Dhakhwa R, Acharya IL, Shrestha HG, Joshi DM, Lama S, Lakhey M. Histopathologic study of chronic antral gastritis. J Nepal Health Res Counc. 2012;10:57–60. Dhakhwa R, Acharya IL, Shrestha HG, Joshi DM, Lama S, Lakhey M. Histopathologic study of chronic antral gastritis. J Nepal Health Res Counc. 2012;10:57–60.
15.
Zurück zum Zitat Zhang C, Yamada N, Wu YL, Wen M, Matsuhisa T, Matsukura N. Comparison of Helicobacter pylori infection and gastric mucosal histological features of gastric ulcer patients with chronic gastritis patients. World J Gastroenterol. 2005;11:976–81. Zhang C, Yamada N, Wu YL,  Wen M, Matsuhisa T, Matsukura N. Comparison of Helicobacter pylori infection and gastric mucosal histological features of gastric ulcer patients with chronic gastritis patients. World J Gastroenterol. 2005;11:976–81.
16.
Zurück zum Zitat Lamarque D, Tran Van Nhieu J, Breban M. What are the gastric modifications induced by acute and chronic Helicobacter pylori infection? Gastroenterol Clin Biol. 2003;27:391–400.PubMed Lamarque D, Tran Van Nhieu J, Breban M. What are the gastric modifications induced by acute and chronic Helicobacter pylori infection? Gastroenterol Clin Biol. 2003;27:391–400.PubMed
17.
Zurück zum Zitat Vega-Ramos B, Rodríguez-Moguel L. Helicobacter pylori. Its relationships and morphological controversies. Rev Gastroenterol Mex. 2000;65 4 Suppl 2:34–40. Vega-Ramos B, Rodríguez-Moguel L. Helicobacter pylori. Its relationships and morphological controversies. Rev Gastroenterol Mex. 2000;65  4 Suppl 2:34–40.
18.
Zurück zum Zitat Lopes AI, Quiding-Jarbrink M, Palha A, et al. Cytokine expression in pediatric Helicobacter pylori infection. Clin Diagn Lab Immunol. 2005;12:994–1002.CrossRef Lopes AI, Quiding-Jarbrink M, Palha A, et al. Cytokine expression in pediatric Helicobacter pylori infection. Clin Diagn Lab Immunol. 2005;12:994–1002.CrossRef
19.
Zurück zum Zitat Strömberg E, Edebo A, Svennerholm AM, Lindholm C. Decreased epithelial cytokine responses in the duodenal mucosa of Helicobacter pylori-infected duodenal ulcer patients. Clin Diagn Lab Immunol. 2003;10:116–24.CrossRef Strömberg E, Edebo A, Svennerholm AM, Lindholm C. Decreased epithelial cytokine responses in the duodenal mucosa of Helicobacter pylori-infected duodenal ulcer patients. Clin Diagn Lab Immunol. 2003;10:116–24.CrossRef
20.
Zurück zum Zitat Lindholm C, Quiding-Järbrink M, Lönroth H, Hamlet A, Svennerholm AM. Local cytokine response in Helicobacter pylori-infected subjets. Infect Immun. 1998;66:5964–71. Lindholm C, Quiding-Järbrink M, Lönroth H, Hamlet A, Svennerholm AM. Local cytokine response in Helicobacter pylori-infected subjets. Infect Immun. 1998;66:5964–71.
21.
Zurück zum Zitat D’Elios MM, Manghetti M, De Carli M, et al. T helper 1 effector cells specific for Helicobacter pylori in the gastric antrum of patients with peptic ulcer disease. J Immunol. 1997;158:962–7. D’Elios MM, Manghetti M, De Carli M, et al. T helper 1 effector cells specific for Helicobacter pylori in the gastric antrum of patients with peptic ulcer disease. J Immunol. 1997;158:962–7.
22.
Zurück zum Zitat Bamford KB, Fan X, Crowe SE, et al. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology. 1998;114:482–92.CrossRef Bamford KB, Fan X, Crowe SE, et al. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology. 1998;114:482–92.CrossRef
23.
Zurück zum Zitat D’Elios MM, Amedei A, Benagiano M, Azzurri A, Del Prete G. Helicobacter pylori, T cells and cytokines: the ‘dangerous liaisons’. FEMS Immunol Med Microbiol. 2005;44:113–9. D’Elios MM, Amedei A, Benagiano M, Azzurri A, Del Prete G. Helicobacter pylori, T cells and cytokines: the ‘dangerous liaisons’. FEMS Immunol Med Microbiol. 2005;44:113–9.
24.
Zurück zum Zitat Amedei A, Cappon A, Codolo G, et al. The neutrophil-activating protein of Helicobacter pylori promotes Th1 immune responses. J Clin Invest. 2006;116:1092–101.CrossRef Amedei A, Cappon A, Codolo G, et al. The neutrophil-activating protein of Helicobacter pylori promotes Th1 immune responses. J Clin Invest. 2006;116:1092–101.CrossRef
25.
Zurück zum Zitat Pellicanò A, Imeneo M, Leone I, Larussa T, Luzza F. Enhanced activation of cyclooxygenase-2 downregulates Th1 signaling pathway in Helicobacter pylori-infected human gastric mucosa. Helicobacter. 2007;12:193–9. Pellicanò A, Imeneo M, Leone I,  Larussa T, Luzza F. Enhanced activation of cyclooxygenase-2 downregulates Th1 signaling pathway in Helicobacter pylori-infected human gastric mucosa. Helicobacter. 2007;12:193–9.
26.
Zurück zum Zitat Bimczok D, Clements RH, Waites KB, et al. Human primary gastric dendritic cells induce a Th1 response to H. pylori. Mucosal Immunol. 2010;3:260–9.CrossRef Bimczok D, Clements RH, Waites KB, et al. Human primary gastric dendritic cells induce a Th1 response to H. pylori. Mucosal Immunol. 2010;3:260–9.CrossRef
27.
Zurück zum Zitat Uehara A, Okumura T, Sekiya C, Okamura K, Takasugi Y, Namiki M. Interleukin-1 inhibits the secretion of gastric acid in rats: possible involvement of prostaglandin. Biochem Biophys Res Commun. 1989;162:1578–84. Uehara A, Okumura T, Sekiya C, Okamura K, Takasugi Y, Namiki M. Interleukin-1 inhibits the secretion of gastric acid in rats: possible involvement of prostaglandin. Biochem Biophys Res Commun. 1989;162:1578–84.
28.
Zurück zum Zitat Datta De D, Bhattacharjya S, Maitra M, et al. IL1β induced Smad 7 negatively regulates gastrin expression. PLoS One. 2011;6:e14775.CrossRef Datta De D, Bhattacharjya S, Maitra M, et al. IL1β induced Smad 7 negatively regulates gastrin expression. PLoS One. 2011;6:e14775.CrossRef
29.
Zurück zum Zitat Nutman TB. Looking beyond the induction of Th2 responses to explain immunomodulation by helminthes. Parasite Immunol. 2015;37:304–13.CrossRef Nutman TB. Looking beyond the induction of Th2 responses to explain immunomodulation by helminthes. Parasite Immunol. 2015;37:304–13.CrossRef
30.
Zurück zum Zitat Maizels RM, Smits HH, McSorley HJ. Modulation of host immunity by helminths: the expanding repertoire of parasite effector molecules. Immunity. 2018;49:801–18.CrossRef Maizels RM, Smits HH, McSorley HJ. Modulation of host immunity by helminths: the expanding repertoire of parasite effector molecules. Immunity. 2018;49:801–18.CrossRef
31.
Zurück zum Zitat Eichenberger RM, Ryan S, Jones L, et al. Hookworm secreted extracellular vesicles interact with host cells and prevent inducible colitis in mice. Front Immunol. 2018;9:850. Eichenberger RM, Ryan S, Jones L, et al. Hookworm secreted extracellular vesicles interact with host cells and prevent inducible colitis in mice. Front Immunol. 2018;9:850.
32.
Zurück zum Zitat Whary MT, Fox JG. Th1-mediated pathology in mouse models of human disease is ameliorated by concurrent Th2 responses to parasite antigens. Curr Top Med Chem. 2004;4:531–8.CrossRef Whary MT, Fox JG. Th1-mediated pathology in mouse models of human disease is ameliorated by concurrent Th2 responses to parasite antigens. Curr Top Med Chem. 2004;4:531–8.CrossRef
33.
Zurück zum Zitat Moreau E, Chauvin A. Immunity against helminths: interactions with the host and the intercurrent infections. J Biomed Biotechnol. 2010;428593. Moreau E, Chauvin A. Immunity against helminths: interactions with the host and the intercurrent infections. J Biomed Biotechnol. 2010;428593.
Metadaten
Titel
Changes in the severity of gastric mucosal inflammation associated with Helicobacter pylori in humans coinfected with  intestinal helminths
verfasst von
Alisbeth Fuenmayor-Boscán
Ileana Hernández-Rincón
Gabriel Arismendi-Morillo
Edgardo Mengual
Zulbey Rivero
Gisela Romero
Maribel Lizarzábal
Melchor Álvarez-Mon
Publikationsdatum
20.05.2020
Verlag
Springer India
Erschienen in
Indian Journal of Gastroenterology / Ausgabe 2/2020
Print ISSN: 0254-8860
Elektronische ISSN: 0975-0711
DOI
https://doi.org/10.1007/s12664-020-01023-0

Weitere Artikel der Ausgabe 2/2020

Indian Journal of Gastroenterology 2/2020 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Blutdrucksenkung könnte Uterusmyome verhindern

Frauen mit unbehandelter oder neu auftretender Hypertonie haben ein deutlich erhöhtes Risiko für Uterusmyome. Eine Therapie mit Antihypertensiva geht hingegen mit einer verringerten Inzidenz der gutartigen Tumoren einher.

„Jeder Fall von plötzlichem Tod muss obduziert werden!“

17.05.2024 Plötzlicher Herztod Nachrichten

Ein signifikanter Anteil der Fälle von plötzlichem Herztod ist genetisch bedingt. Um ihre Verwandten vor diesem Schicksal zu bewahren, sollten jüngere Personen, die plötzlich unerwartet versterben, ausnahmslos einer Autopsie unterzogen werden.

Hirnblutung unter DOAK und VKA ähnlich bedrohlich

17.05.2024 Direkte orale Antikoagulanzien Nachrichten

Kommt es zu einer nichttraumatischen Hirnblutung, spielt es keine große Rolle, ob die Betroffenen zuvor direkt wirksame orale Antikoagulanzien oder Marcumar bekommen haben: Die Prognose ist ähnlich schlecht.

Schlechtere Vorhofflimmern-Prognose bei kleinem linken Ventrikel

17.05.2024 Vorhofflimmern Nachrichten

Nicht nur ein vergrößerter, sondern auch ein kleiner linker Ventrikel ist bei Vorhofflimmern mit einer erhöhten Komplikationsrate assoziiert. Der Zusammenhang besteht nach Daten aus China unabhängig von anderen Risikofaktoren.

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.