Abstract
In the post-H. pylori eradication era, the clinical significance of gastric non-H. pylori helicobacters (NHPH; also referred to as H. heilmannii-like organisms and H. heilmannii sensu lato) is gradually increasing. This group of bacteria may inhabit the stomach of domestic and wild animals including cats, dogs, pigs, primates, rodents, cheetahs, and rabbits. NHPH are zoonotic microorganisms, meaning that they may transmit between animals and humans. They may be distinguished from H. pylori regarding their microbiology involving larger cells with more distinct spiral shape and bipolarity, localization in the stomach layer and regional distribution, urease activity and virulence factors, and relation to gastric diseases where gastric NHPH infection is often associated with milder gastritis than H. pylori but higher risk of gastric MALT lymphoma. At present, pure culture of NHPH species remains a challenge, but the full genome sequences of some of the species have been reported. Recent and ongoing prevalence studies indicate a higher clinical relevance of these bacteria than earlier impressions suggested. Current efforts in improving cultivation and detection methodology are contributing to an increased understanding of their microbiology, prevalence, and relevance to human diseases.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Stoffel MH, Friess AE, Burnens A, Schmassmann A, Neiger R. Distinction of gastric Helicobacter spp. in humans and domestic pets by scanning electron microscopy. Helicobacter. 2000;5:232–9.
Rappin J. Contre a l’etude de bacteri de la bouche a l’etat normal.1881;68. In: Breed RS, Murray EGD, Hitchens AP, editors. Bergey’s manual of determinative bacteriology. 6th ed. Baltimore: Williams and Wilkins Co; 1948. p. 217.
Bizzozero G. Ueber die schlauchformigen drusen desmagendarmkanals und die beziehungen ihres epithels zu demoberflachenepithel der schleimhaut. Archivfur MikrofkopischeAnatomie Entwickiungs mechanik. 1893;42:82.
Salomon H. Ueber das spirillum des saugetiermagens und seinverhalten zu den belegzellen. Centralblatt fur Bakteriologie, Parasitenkunde V Infektionskrankheiten. 1896;XIX:433–43.
Krienitz W. Ueber das Auftreten von Spirochaten verscheidener Form im Mageninhalt bei Carcinoma ventriculi. Dtsch Med Wocknenschr. 1906;32:872.
Kasai K, Kobayashi R. The stomach spirochete occurring in mammals. J Parasitol. 1919;6:1–11.
Weber AF, Schmittdiel EF. Electron microscopic and bacteriologic studies of spirilla isolated from the fundic stomachs of cats and dogs. Am J Vet Res. 1962;23:422–7.
Marshall BJ, Warren JR. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet. 1984;1(8390):1311–5.
Heilmann KL, Bochard F. Gastritis due to spiral shaped bacteria other than Helicobacter pylori: clinical, histological, and ultrastructural findings. Gut. 1991;32:137–40.
Dent JC, McNulty CA, Uff JC, Wilkinson SP, Gear MW. Spiral organisms in the gastric antrum. Lancet. 1987;11:96.
McNulty CA, Dent JC, Curry A, Uff JS, Ford GA, Gear MW, Wilkinson SP. New spiral bacterium in gastric mucosa. J Clin Pathol. 1989;42:585–91.
Dye KR, Marshall BJ, Fnerson HF, Onerrant RT, McCall RW. Gastritis in a human due to infection with an organism resembling the cat gastric spirillum. Gastroenterology. 1988;94:A108.
Itoh T, Yanagawa M, Singaki N, Masubuchi N, Takahashi S, Saito S. Isolation of Helicobacter heilmannii like organism from the stomachs of cynomolgus monkey and colonization of them in mice. Gastroenterology. 1994;106:A99.
Nakamura M, Murayama SY, Serizawa H, Sekiya Y, Eguchi M, Takahashi S, Nishikawa K, Takahashi T, Matsumoto T, Yamada H, Hibi T, Tsuchimoto K, Matsui H. “Candidatus Helicobacter heilmannii” from a cynomolgus monkey induces gastric mucosa-associated lymphoid tissue lymphomas in C57BL/6 mice. Infect Immun. 2007;75:1214–22.
Solnick JV, O’Rourke J, Lee A, Paster BJ, Dewhirst FE, Tompkins LS. An uncultured gastric spiral organism is a newly identified Helicobacter in humans. J Infect Dis. 1993;168:379–85.
Mendes EN, Queiroz DM, Rocha GA, Moura SB, Leite VH, Fonseca ME. Ultrastructure of a spiral micro-organism from pig gastric mucosa (“Gastrospirillum suis”). J Med Microbiol. 1990;33:61–6.
De Groote D, Ducatelle R, van Doorn LJ, Tilmant K, Quint WGV, Verschuurn A, Haesebrouck F. Detection of “Candidatus Helicobacter suis” in gastric samples of pig by PCR: comparison with other invasive diagnostic techniques. J Clin Microbiol. 2000;38:1131–5.
Haesebrouck F, Pasmans F, Flahou B, Smet A, Vandamme P, Ducatelle R. Non-Helicobacter pylori Helicobacter species in the human gastric mucosa: a proposal to introduce the terms H. heilmannii sensu lato and sensu stricto. Helicobacter. 2011;16:339–40.
Priestnall SL, Wiinberg B, Spohr A, Neuhaus B, Kuffer M, Wiedmann M, Simpson W. Evaluation of “Helicobacter heilmannii” subtypes in the gastric mucosas of cats and dogs. J Clin Microbiol. 2004;42:2144–51.
Fox JG. The non-H pylori helicobacters: their expanding role in gastrointestinal and systemic diseases. Gut. 2002;50:273–83.
Van den Bulck K, Baele M, Hermans K, Ducatelle R, Haesebrouck F, Decostere A. First report on the occurrence of “Helicobacter heilmannii” in the stomach of rabbits. Vet Res Commun. 2005;29:271–27.
Stolte M, Wellens E, Bethke B, Ritter M, Eidt H. Helicobacter heilmannii (formerly Gastrospirillum hominis) gastritis: an infection transmitted by animals? Scand J Gastroenterol. 1994;29:1061–4.
Lavelle JP, Landas S, Mitros FA, Conklin JL. Acute gastritis associated with spiral organisms from cats. Dig Dis Sci. 1994;39:744–50.
Chung T-H, Kim H-D, Lee Y-S, Hwang C-Y. Determination of the prevalence of Helicobacter heilmannii-like organisms type 2 (HHLO-2) infection in humans and dogs using non-invasive genus/species-specific PCR in Korea. J Vet Med Sci. 2014;76:73–9.
Liu J, He L, Haesebrouck F, Gong Y, Flahou B, Cao Q, Zhang J. Prevalence of coinfection with gastric Non-Helicobacter pylori Helicobacter (NHPH) species in Helicobacter pylori-infected patients suffering from gastric disease in Beijing, China. Helicobacter. 2015;20:284–90. doi:10.1111/hel.12201.
De Cooman L, Flahou B, Houf K, Smet A, Ducatelle R, Pasmans F, Haesebrougk F. Survival of Helicobacter suis bacteria in retail pig meat. Int J Food Microbiol. 2013;166(1):164–7. doi:10.1016/j.ijfoodmicro.2013.05.020.
Carnot P, Lelievre A. Morphologie du product d’excretion des cellules bordants. Comptes Rendus Soc Biol. 1909;66:311–3.
Regard C. Sur une curieuse lacalisation de spirilles parasites dans les canalisations glandulaires de la gastrique normale, chez le chien et le chat. Soc Biol. 1909;66:229–31.
Kubonova K, Trupl J, Jancula L, Polák E, Vráblik V. Presence of spiral bacteria (‘Gastrospirillum hominis’) in the gastric mucosa. Eur J Clin Microbial Infect Dis. 1991;10:459–60.
Yang HT, Goliger JA, Song M, Zhou D. High prevalence of Helicobacter heilmannii infection in China. Dig Dis Sci. 1998;43:1493.
Yali Z, Yamada N, Wen M, Matsuhisa T, Miki M. Gastrospirillum hominis and Helicobacter pylori infection in Thai individuals – comparison of histopathological changes of gastric mucosa. Pathol Int. 1998;48:507–11.
Kato S, Ozawa K, Sekine H, Ohyauchi M, Shimosegawa T, Minoura T, Iinuma K. Helicobacter heilmannii infection in a child after successful eradication of Helicobacter pylori: case report and review of literature. J Gastroenterol. 2005;40:94–7.
Stolte M, Kroher G, Meining A, Morgner A, Bayerdörffer E, Bethke B. A comparison of Helicobacter pylori and H. heilmannii gastritis. A matched control study involving 404 patients. Scand J Gastroenterol. 1997;32:28–33.
Morgner A, Lehn N, Andersen LPP, Thiede C, Bennedsen M, Trebesius K, Neubauer B, et al. Helicobacter heilmannii-associated primary gastric low-grade MALT lymphoma: complete remission after curing the infection. Gastroenterology. 2000;118:821–8.
Okiyama Y, Matsuzawa K, Hidaka E, Sano K, Akamatsu T, Ota H. Helicobacter heilmannii infection: clinical, endoscopic and histopathological features in Japanese patients. Pathol Int. 2005;55:398–404.
Foschini MP, Pieri F, Cerasoli S, Accardo P, Formica G, Biasiucci A, Donzelli C, et al. Helicobacter heilmannii: anatomo-clinical study of 14 new cases. Pathologica. 1999;91:18–24.
Sasaki M, Goji S, Tamura Y, Nakamura M, Matsui H, Murayama SY, Ebi M, Ogasawara N, Funai Y, Kasugai K. Helicobacter suis-infected nodular gastritis and a review of diagnostic sensitivity for Helicobacter heilmannii-like organisms. Case Rep Gastroenterol. 2015;9:179–87.
Vinette KM, Gibney KM, Proujansky R, Fawcett PT. Growth of Helicobacter pylori in a long spiral form does not alter expression of immunodominant proteins. BMC Microbiol. 2002;2:24.
Lee A, Dent J, Hazell S, McNulty C. Origin of spiral organisms in human gastric antrum. Lancet. 1988;1(8580):300–1.
Andersen LP, Norgaard A, Holck S, Blom J, Elsborg L. Isolation of a Helicobacter heilmannii-like organism from the human stomach. Eur J Clin Microbiol Infect Dis. 1996;15:95–6.
Jalava K, On SLW, Harrington CS, Andersen LP, Hanninen ML, Vandamme P. A cultured strain of “Helicobacter heilmannii”, a human gastric pathogen, identified as H. bizzozeronii: evidence for zoonotic potential of Helicobacter. Emerg Infect Dis. 2001;7:1036–8.
Trebesius K, Adler K, Vieth M, Stolte M, Haas R. Specific detection and prevalence of Helicobacter heilmannii-like organisms in the human gastric mucosa by fluorescent in situ hybridization and partial 16S ribosomal DNA sequencing. J Clin Microbiol. 2001;39:1510–6. doi:10.1128/JCM.39.4.1510-1516.2001.
Chisholm SA, Owen RJ. Development and application of a novel screening PCR assay for direct detection of ‘Helicobacter heilmannii’-like organisms in human gastric biopsies in Southeast England. Diagn Microbiol Infect Dis. 2003;46(1):1–7.
O’Rourke JL, Solnick JV, Neilan BA, Seidel K, Hayter R, Hansen LM, Lee A. Description of “Candidatus Helicobacter heilmannii” based on DNA sequence analysis of 16S rRNA and urease genes. Int J Syst Evol Microbiol. 2004;54:2203–11.
Baele M, Decostere A, Vandamme P, Ceelen L, Hellemans A, Chiers K, Ducatelle R, Haesebrouck F. Isolation and characterization of Helicobacter suis sp. nov. from pig stomachs. Int J Syst Evol Microbiol. 2008;58:1350–8.
Vermoote M, Vandekerckhove TTM, Flahou B, Pasmans F, Smet A, De Groote D, Van Criekinge W, et al. Genome sequence of Helicobacter suis supports its role in gastric pathology. Vet Res. 2011;42:51.
Arnold IC, Zigova Z, Holden M, Lawley TD, Rad R, Dougan G, Falkow S, et al. Comparative whole genome sequence analysis of the carcinogenic bacterial model pathogen Helicobacter felis. Genome Biol Evol. 2011;3:302–8.
Schott T, Rossi M, Hänninen M-L. Genome sequence of Helicobacter bizzozeronii strain CIII-1, an isolate from human gastric mucosa. J Bacteriol. 2011;193:4565–6.
Smet A, Van Nieuwerburgh F, Ledesma J, Flahou B, Deforce D, Ducatelle R, Haesebrouck F. Genome sequence of Helicobacter heilmannii sensu stricto ASB1 isolated from the gastric mucosa of a kitten with severe gastritis. Genome Announc. 2013;1:e00033–12.
Montecucco C, Rappuoli R. Living dangerously: how Helicobacter pylori survives in the human stomach. Nat Rev Mol Cell Biol. 2001;2:457–66.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer Japan
About this chapter
Cite this chapter
Nakamura, M. et al. (2016). Gastric Non-Helicobacter pylori Helicobacter: Its Significance in Human Gastric Diseases. In: Suzuki, H., Warren, R., Marshall, B. (eds) Helicobacter pylori. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55705-0_8
Download citation
DOI: https://doi.org/10.1007/978-4-431-55705-0_8
Published:
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-55704-3
Online ISBN: 978-4-431-55705-0
eBook Packages: MedicineMedicine (R0)