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History of Helicobacter pylori , duodenal ulcer, gastric ulcer and gastric cancer
Open accessAbstract
Helicobacter pylori (H. pylori) infection underlies gastric ulcer disease, gastric cancer and duodenal ulcer disease. The disease expression reflects the pattern and extent of gastritis/gastric atrophy (i.e., duodenal ulcer with non-atrophic and gastric ulcer and gastric cancer with atrophic gastritis). Gastric and duodenal ulcers and gastric cancer have been known for thousands of years. Ulcers are generally non-fatal and until the 20th century were difficult to diagnose. However, the presence and pattern of gastritis in past civilizations can be deduced based on the diseases present. It has been suggested that gastric ulcer and duodenal ulcer both arose or became more frequent in Europe in the 19th century. Here, we show that gastric cancer and gastric ulcer were present throughout the 17th to 19th centuries consistent with atrophic gastritis being the predominant pattern, as it proved to be when it could be examined directly in the late 19th century. The environment before the 20th century favored acquisition of H. pylori infection and atrophic gastritis (e.g., poor sanitation and standards of living, seasonal diets poor in fresh fruits and vegetables, especially in winter, vitamin deficiencies, and frequent febrile infections in childhood). The latter part of the 19th century saw improvements in standards of living, sanitation, and diets with a corresponding decrease in rate of development of atrophic gastritis allowing duodenal ulcers to become more prominent. In the early 20th century physician's believed they could diagnose ulcers clinically and that the diagnosis required hospitalization for "surgical disease" or for "Sippy" diets. We show that while H. pylori remained common and virulent in Europe and the United States, environmental changes resulted in changes of the pattern of gastritis producing a change in the manifestations of H. pylori infections and subsequently to a rapid decline in transmission and a rapid decline in all H. pylori-related diseases.
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“H. pylori infection can lead to antrum-predominant gastritis, in which the oxyntic mucosa is not inflamed but a gastrin-driven increase in acid output occurs, along with the possible development of duodenal ulcer[67,68].”
From Proton pump inhibitors and dysbiosis: current knowledge and aspects to be clarified (2019) · cites this paper as [68]
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Cites
Traces of Human Migrations in Helicobacter pylori Populations
Falush, D., Wirth, T., Linz, B., Pritchard, J. K., Stephens, M., Kidd, M. S., Blaser, M. J., Graham, D. Y., Vacher, S., Perez-Perez, G. I., et al. (2003) · Science · doi:10.1126/science.1080857 · Cited by 1,019
Self-citationCampylobacter pylori and Peptic Ulcer Disease
Graham, D. Y. (1989) · Gastroenterology · doi:10.1016/s0016-5085(89)80057-5 · Cited by 726
Self-citationSalt, salted food intake, and risk of gastric cancer: Epidemiologic evidence
Tsugane, S. (2005) · Cancer Science · doi:10.1111/j.1349-7006.2005.00006.x · Cited by 353
Helicobacter pylori infection in the pathogenesis of duodenal ulcer and gastric cancer: A model
Graham, D. Y. (1997) · Gastroenterology · doi:10.1016/s0016-5085(97)70019-2 · Cited by 340
Self-citationDifferences in Genotypes ofHelicobacter pylorifrom Different Human Populations
Kersulyte, D., Mukhopadhyay, A. K., Velapatiño, B., Su, W. W., Pan, Z., Garcia, C. M., Hernandez, V., Valdez, Y., Mistry, R. S., Gilman, R. H., et al. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.11.3210-3218.2000 · Cited by 253
Helicobacter pylori in North and South America before Columbus
Yamaoka, Y., Orito, E., Mizokami, M., Gutiérrez, Ó., Saitou, N., Kodama, T., Osato, M. S., Kim, J. G., Ramirez, F. C., Mahachai, V., et al. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)02617-0 · Cited by 190
Self-citationFry, J. (1964) · BMJ · doi:10.1136/bmj.2.5412.809 · Cited by 139
Poor housing in childhood and high rates of stomach cancer in England and Wales
Barker, D., Coggon, D., Osmond, C., & Wickham, C. A. C. (1990) · British Journal of Cancer · doi:10.1038/bjc.1990.129 · Cited by 118
Review article: historic changes of Helicobacter pylori -associated diseases
Sonnenberg, A. (2013) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.12380 · Cited by 111
Vitamin C, Gastritis, and Gastric Disease: A Historical Review and Update
Aditi, A., & Graham, D. Y. (2012) · Digestive Diseases and Sciences · doi:10.1007/s10620-012-2203-7 · Cited by 101
Self-citationPathogenesis and therapy of gastric and duodenal ulcer disease
Shiotani, A., & Graham, D. Y. (2002) · Medical Clinics of North America · doi:10.1016/s0025-7125(02)00083-4 · Cited by 87
Self-citationAfrican, Asian or Indian enigma, the East Asian Helicobacter pylori : facts or medical myths
Graham, D. Y., Lü, H., & Yamaoka, Y. (2009) · Journal of Digestive Diseases · doi:10.1111/j.1751-2980.2009.00368.x · Cited by 82
Self-citationThe Transportation Revolution, 1815-1860
Barnes, J. A., & Taylor, G. R. (1952) · Journal of American History · doi:10.2307/1902859 · Cited by 81
Graham, D. Y., & Asaka, M. (2009) · Journal of Gastroenterology · doi:10.1007/s00535-009-0117-8 · Cited by 77
Self-citationHwang, H., Dwyer, J. T., & Russell, R. M. (2009) · Nutrition Reviews · doi:10.1111/j.1753-4887.1994.tb01394.x · Cited by 76
The Mortality from Cancer Throughout the World.
(1916) · JAMA · doi:10.1001/jama.1916.02580510130030 · Cited by 76
In vivo susceptibility of Campylobacter pylori.
Dy, G., Pd, K., Opekun, A. R., Ke, S., Polasani, R., Dj, E., Evans, D. G., Lc, A., Michaletz, P. A., & Yoshimura, H. H. (1989) · PubMed · Cited by 75
Evidence-based examination of the African enigma in relation toHelicobacter pyloriinfection
Agha, A., & Graham, D. Y. (2005) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365520510012280 · Cited by 74
Self-citationBreurec, S., Guillard, B., Hem, S., Brisse, S., Dieye, F. B., Huerre, M., Oung, C., Raymond, J., Tan, T. S., Thiberge, J.-M., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022058 · Cited by 73
Cassedy, J. H. (1977) · JAMA · doi:10.1001/jama.1977.03280010066031 · Cited by 71
Lee, Y. Y., Raj, S. M., & Graham, D. Y. (2013) · Helicobacter · doi:10.1111/hel.12058 · Cited by 69
Self-citationEcological study for refrigerator use, salt, vegetable, and fruit intakes, and gastric cancer
Park, B., Shin, A., Park, S. K., Ko, K., Hyun, S. W., Lee, E.-H., Gwack, J., Jung, E.-J., Cho, L. Y., Yang, J. J., et al. (2011) · Cancer Causes & Control · doi:10.1007/s10552-011-9823-7 · Cited by 68
Health, Height and Welfare: Britain 1700-1980
Floud, R., & Harris, B. J. (1996) · National Bureau of Economic Research · doi:10.3386/h0087 · Cited by 62
Attributable risks for stomach cancer in Northern Italy
Vecchia, C. L., D’Avanzo, B., Negri, E., Decarli, A., & Bénichou, J. (1995) · International Journal of Cancer · doi:10.1002/ijc.2910600603 · Cited by 62
The Peptic Gastric Ulcer — Histotopographic and Functional Investigations
Stadelmann, O., Elster, K., Stolte, M., Miederer, S. E., Deyhle, P., Demling, L., & Siegenthaler, W. E. (1971) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365527109181143 · Cited by 59
Helicobacter pylori: recombination, population structure and human migrations
Suerbaum, S., & Achtman, M. (2004) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2004.06.014 · Cited by 53
Early events in proton pump inhibitor‐associated exacerbation of corpus gastritis
Graham, D. Y., Opekun, A. R., Yamaoka, Y., Osato, M. S., & El-Zimaity, H. M. T. (2003) · Alimentary Pharmacology & Therapeutics · doi:10.1046/j.1365-2036.2003.01400.x · Cited by 51
Self-citationGastritis duodenitis, and circulating levels of gastrin in duodenal ulcer before and after vagotomy.
Meikle, D. D., Taylor, K. B., Truelove, S. C., & Whitehead, R. (1976) · Gut · doi:10.1136/gut.17.9.719 · Cited by 49
Conservation ofHelicobacter pyloriGenotypes in Different Ethnic Groups in Houston, Texas
Yamaoka, Y., Malaty, H. M., Osato, M. S., & Graham, D. Y. (2000) · The Journal of Infectious Diseases · doi:10.1086/315486 · Cited by 46
Self-citationGastritis and Its Consequences
K, &. R. (1936) · The American Journal of the Medical Sciences · doi:10.1097/00000441-193607000-00024 · Cited by 44
Sippy, B. W. (1983) · JAMA · doi:10.1001/jama.250.16.2192 · Cited by 38
Baron, J. H., & Sonnenberg, A. (2002) · Gut · doi:10.1136/gut.50.4.568 · Cited by 37
Jennings, D. A. (1940) · The Lancet · doi:10.1016/s0140-6736(00)61515-5 · Cited by 37
Glimpses of the Past from the Recently Unearthed Ancient Corpses in China
Cheng, T. O. (1984) · Annals of Internal Medicine · doi:10.7326/0003-4819-101-5-714 · Cited by 33
Prevention of Diarrhea Caused by Enterotoxigenic Escherichia coli: Lessons Learned with Volunteers
Graham, D. Y., & Evans, D. G. (1990) · Clinical Infectious Diseases · doi:10.1093/clinids/12.supplement_1.s68 · Cited by 29
Self-citationGASTRIC SECRETION IN FEVER AND INFECTIOUS DISEASES
Chang, H.-C. (1933) · Journal of Clinical Investigation · doi:10.1172/jci100486 · Cited by 28
A treatise of the materia medica and therapeutics
Eberle, J. (2011) · University of Michigan Library Repository · Cited by 27
High Prevalence of Duodenal Ulcer and Gastric Cancer in Dyspeptic Patients in Korea
Malaty, H. M., Kim, J. G., El-Zimaity, H. M. T., & Graham, D. Y. (1997) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365529708996529 · Cited by 27
Self-citationUbukata, H., Nagata, H., Tabuchi, T., Konishi, S., Kasuga, T., & Tabuchi, T. (2011) · Gastric Cancer · doi:10.1007/s10120-011-0005-9 · Cited by 27
Graham, D. Y. (1991) · Springer eBooks · doi:10.1007/978-3-642-75726-6_19 · Cited by 26
Self-citationThoughts about populations with unexpected low prevalences of Helicobacter pylori infection
Graham, D. Y., Yamaoka, Y., & Malaty, H. M. (2007) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/j.trstmh.2007.06.006 · Cited by 24
Self-citationDiet and gastric cancer: a case–control study in Shanghai urban districts
Su Juan, F. E. I., & Shu Dong, X. I. A. O. (2006) · Chinese Journal of Digestive Diseases · doi:10.1111/j.1443-9573.2006.00252.x · Cited by 23
Contemplating the Future without Helicobacter pylori and the Dire Consequences Hypothesis
Graham, D. Y., Yamaoka, Y., & Malaty, H. M. (2007) · Helicobacter · doi:10.1111/j.1523-5378.2007.00566.x · Cited by 23
Self-citationIntestinal metaplasia of gastric mucosa in autopsy materials in Hiroshima and Yamaguchi districts.
Kubo, T., & Imai, T. (1971) · PubMed · Cited by 19
Risk Factors Associated with Gastric Cancer in Patients with a Duodenal Ulcer
Cho, S., Choi, I. J., Kim, C. G., Kook, M., Lee, J. Y., Kim, B. C., Ryu, K. H., Nam, S. Y., & Kim, Y. (2010) · Helicobacter · doi:10.1111/j.1523-5378.2010.00805.x · Cited by 18
Ga, N. (1997) · PubMed · Cited by 18
Khan, A. K. A., Hasan, M. N., Pk, R., Aziz, S., Mahbubul Huq, K., Sm, A., & Sa, H. (1987) · PubMed · Cited by 15
Co‐Existing Gastric Cancer and Duodenal Ulcer Disease: Role of Helicobactor pylori Infection
Kim, H. Y., Kim, Y. B., Park, C. K., Yoo, J. Y., & Graham, D. Y. (1997) · Helicobacter · doi:10.1111/j.1523-5378.1997.tb00089.x · Cited by 13
Self-citationDuodenal Ulcer and Gastric Cancer
Sawyer, R. B. (1962) · Archives of Surgery · doi:10.1001/archsurg.1962.01310010113015 · Cited by 9
Hunger and History. The Influence of Hunger on Human History.
Fussell, G. E., & Prentice, E. P. (1949) · The Economic Journal · doi:10.2307/2226700 · Cited by 9
Clinical investigation on coexisting of duodenal ulcer and gastric cancer in China
Zhao, L. Y., Shen, Z.-X., Luo, H.-S., & Jp, Y. (2005) · International Journal of Clinical Practice · doi:10.1111/j.1368-5031.2005.00594.x · Cited by 6
Royal Free Hospital. ULCER OF THE STOMACH TREATED SUCCESSFULLY
Brinton, W. (1855) · BMJ · doi:10.1136/bmj.s3-3.155.1125 · Cited by 6
Weis, V. G., Sousa, J. F., LaFleur, B., Nam, K. T., Weis, J. A., Finke, P. E., Ameen, N. A., Fox, J. G., & Goldenring, J. R. (2012) · Gut · doi:10.1136/gutjnl-2012-302401 · Cited by 5
(1841) · Europe PMC (PubMed Central) · Cited by 4
Should We Worry About Gastric Cancer in Duodenal Ulcer Patients?
Goldin, E., Zimmerman, J., Okon, E., & Rachmilewitz, D. (1985) · Journal of Clinical Gastroenterology · doi:10.1097/00004836-198506000-00008 · Cited by 3
Gastric cancer following Helicobacter pylori eradication in duodenal ulcer patients
Zullo, A., Hassan, C., Eramo, A., & Morini, S. (2006) · Digestive and Liver Disease · doi:10.1016/j.dld.2006.01.030 · Cited by 3
THE DIAGNOSIS OF GASTRIC AND DUODENAL ULCER*
Quervain, F. D. (1914) · Annals of Surgery · doi:10.1097/00000658-191408000-00009 · Cited by 3
THE EARLY DIAGNOSIS OF CARCINOMA OF THE STOMACH, WITH THE BACTERIOLOGY OF THE STOMACH CONTENTS.
TURCK, F. B. (1895) · JAMA · doi:10.1001/jama.1895.02430100006001a · Cited by 2
Gastric secretion in fever and infectious diseases
(1933) · International Journal of Orthodontia and Dentistry for Children · doi:10.1016/s0097-0522(33)90268-3 · Cited by 2
DUODENAL ULCER AND ITS SURGICAL TREATMENT.
Milward, F. V. (1901) · The Lancet · doi:10.1016/s0140-6736(01)74366-8 · Cited by 1
Duodenal ulcer and gastric cancer; rare association or an indication for a change of policy?
Wilkinson, M., & Doig, L. A. (2005) · International Journal of Clinical Practice · doi:10.1111/j.1368-5031.2005.00654b.x · Cited by 1
The Differential Diagnosis of Duodenal Ulcer*
Jacobson, L., & Palmer, W. L. (1943) · Medical Clinics of North America · doi:10.1016/s0025-7125(16)36347-7 · Cited by 1
SPECIAL DIAGNOSIS IN ACUTE PERFORATIVE PERITONITIS.
Mackenzie, H. W. G. (1888) · The Lancet · doi:10.1016/s0140-6736(02)27886-1 · Cited by 1
Research works printed but not linked: 14
- Moynihan BGA. History. Peptic ulcer. Philadelphia: WB Saunders, 1910: 17-23
- Goldstein HI. Ulcer and cancer of the stomach in the mid- dle ages. J Internal Coll Surgeons 1943; 6: 482-489
- Wilber DL. The history of diseases of the stomach and duodenum with reference also to their etiology. In: Euster- man GB, Balfour DC, editors. The stomach and duodenum. Philadelphia: WB Saunders Company, 1935: 1-21
- Goldstein HI. The use of magnesium trisilicate colloidal kaolin and aluminum hydroxide in acid gastric therapy: Historical notes on ulcer of the stomach and duodenum. J Internal Coll Surgeons 1939; 2: 379-408
- Moynihan BGA. Duodenal ulcer. 2nd ed. Philadelphia: WB Saunders Company, 1912
- Moynihan BGA. Duodenal ulcer. 1st ed. Philadelphia: WB Saunders Company, 1910
- Gray HK, Balfour DC. Cancer of the stomach. Am J Cancer 1934; 22: 249-286
- Schlesinger H, Kaufmann. Uber einen milchsaure bilden- den bacillus und sein vorkommen im magensaft. Wien Klin Wochenschr 1895; 15: 225-229
- Boas II, Oppler B. Zur kenntniss des mageninhalts beim carcinoma ventriculi. Deutsch Med Wchnsch 1895; 21: 73-75
- Faber K. Chronic gastritis: its relation to achylia and ulcer. Lancet 1927; 2: 902-907
- Clark GK. Hunger and politics in 1842. J Mod History 1953; 25: 355-373
- Collinson H. Appendix 1: containing a detailed statement of all cases operated upon to the end of 1908, with an analysis and summary. In: Moynihan BGA, editor. Duodenal ulcer. 2nd ed. Philadelphia: W.B. Saunders Company, 1912: 317-465
- Moynihan BGA. Differential Diagnosis. Duodenal ulcer. 2nd ed. Philadelphia: W.B. Saunders Company, 1912: 139-57 76
- Latrobe CJ. Travels in North America. The American quar- terly review. Philadelphia: Lydia R. Bailey, 1835: 390-422
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Self-citation
Metadata
- Authors
- Graham, D. Y.
- Affiliations
- Michael E. DeBakey VA Medical Center (US)
- Corresponding author
- Graham, David Y
- ORCID
- Graham, David Y
- Venue
- World Journal of Gastroenterology
- Publisher
- Baishideng Publishing Group Inc.
- Published
- 2014
- Volume
- 20
- Issue
- 18
- Pages
- 5191
- ISSN
- 1007-9327 (ISSN-L)
- PMC
- PMC4017034
- OpenAlex
- W2058759666
- Cited by
- 357
- References
- 66
- Citations by year
- 2026: 14 · 2025: 40 · 2024: 34 · 2023: 38 · 2022: 37 · 2021: 41 · 2020: 34 · 2019: 36 · 2018: 36 · 2017: 18 · 2016: 14 · 2015: 13 · 2014: 2
- FWCI
- 2.96
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- World Journal of Gastroenterology (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Veterans Affairs (DK56338)
- Office of Research and Development
- National Institute of Diabetes and Digestive and Kidney Diseases (DK56338, DK062813, R01DK062813, P30DK056338)
- Topics
- Health Sciences › Medicine › Gastroenterology › Helicobacter pylori-related gastroenterology studies
- Social Sciences › Arts and Humanities › History and Philosophy of Science › History of Science and Medicine
- Social Sciences › Arts and Humanities › Archeology (arts and humanities) › Paleopathology and ancient diseases
- Keywords
- Helicobacter pylori, history of medicine, duodenal ulcer, gastric ulcer, gastric cancer, atrophic gastritis, environmental factors, sanitation, diet, vitamin deficiency, pediatric infection, ulcer diagnosis
- MeSH terms
- Animals, Duodenal Ulcer, Humans, Risk Factors, Stomach, Stomach Neoplasms, Stomach Ulcer, Time Factors, Prevalence, Helicobacter pylori, Helicobacter Infections, History, 17th Century, History, 18th Century, History, 19th Century, History, 20th Century, History, 21st Century, History, Ancient
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