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World J Gastroenterol. Dec 21, 2014; 20(47): 17779-17787
Published online Dec 21, 2014. doi: 10.3748/wjg.v20.i47.17779
Helicobacter heilmannii sensu lato: An overview of the infection in humans
Mario Bento-Miranda, Ceu Figueiredo, Department of Pathology and Oncology, Faculty of Medicine of the University of Porto, 4200-465 Porto, Portugal
Ceu Figueiredo, Institute of Molecular Pathology and Immunology of the University of Porto, 4200-465 Porto, Portugal
Author contributions: Bento-Miranda M and Figueiredo C solely contributed to this paper.
Correspondence to: Ceu Figueiredo, PhD, Institute of Molecular Pathology and Immunology of the University of Porto, Rua Dr. Roberto Frias S/N, 4200-465 Porto, Portugal.
Telephone: +351-22-5570700 Fax: +351-22-5570799
Received: May 16, 2014
Revised: June 27, 2014
Accepted: July 29, 2014
Published online: December 21, 2014
Processing time: 218 Days and 19.6 Hours


Helicobacter heilmannii sensu lato (H. heilmannii s.l.) is a group of gastric non-Helicobacter pylori Helicobacter species that are morphologically indistinguishable from each other. H. heilmannii s.l. infect the stomach of several animals and may have zoonotic potential. Although the prevalence of these infections in humans is low, they are associated with gastric pathology, including mucosa-associated lymphoid tissue lymphoma, making them a significant health issue. Here, the taxonomy, epidemiology, microbiology, diagnosis, and treatment of these infections will be reviewed. The gastric pathology associated with H. heilmannii s.l. infections in humans will also be addressed. Finally, the features of the complete bacterial genomes available and studies on species-specific pathogenesis will be reviewed. The understanding of the mechanisms that underlie gastric disease development mediated by the different bacterial species that constitute H. heilmannii s.l. is essential for developing strategies for prevention and treatment of these infections.

Key Words: Helicobacter heilmannii sensu lato, Gastric non-Helicobacter pylori, Helicobacter species, Pathogenesis, Diagnosis, Treatment, Genomes

Core tip:Helicobacter heilmannii sensu lato is a group of non-Helicobacter pylori Helicobacter species that infect the stomach of animals and humans. In the human stomach, these infections are associated with several pathologies, but it is currently unknown whether certain species are more often associated with a certain disease outcome than others. The access to bacterial genomes together with the availability of increasing numbers of in vitro isolates will allow significant advances in the understanding of species-specific bacteria-host interactions in disease pathogenesis and will be essential for future development of strategies to prevent and treat these infections.


The first descriptions of spiral bacteria colonizing the stomach of animals date from the end of the 19th century[1], and reports of such microorganisms in the human stomach date from the beginning of the 20th century[2]. Also, by that time, the presence of urease activity in the stomach was reported[3], but no associations were made between this observation and the presence of microorganisms in the stomach. The occurrence of spirochetes in stomachs from autopsied individuals and in fresh gastric surgical specimens was reported later[3,4]. None of these findings received much attention, as the stomach was considered sterile and a hostile environment for bacteria. This view started to change only in 1982, when Marshall and Warren[5] successfully cultured Helicobacter pylori (H. pylori), a spiral-shaped, Gram-negative bacterium from a gastric biopsy specimen. Further studies have since shown that H. pylori is the most common chronic infection in humans, and established this species as the main etiologic factor in peptic ulcer disease, gastric carcinoma, and gastric mucosa-associated lymphoid tissue (MALT) lymphoma[6]. Since the discovery of H. pylori, many new Helicobacter species that infect human or animal hosts have been described, and the Helicobacter genus now includes more than 30 formally named species[7]. Here, we will review the gastric non-H. pylori Helicobacter species generally referred to as “Helicobacter heilmannii”, focusing on those that infect humans and on their impact in human disease.


A spiral-shaped bacterium colonizing the human gastric mucosa that was different from H. pylori was reported for the first time by Dent et al[8] in 1987. Two years later, the same authors described this bacterium and proposed a new genus and species-Gastrospirilum hominis[9]. Later 16S rRNA gene sequencing analysis led to its reclassification within the Helicobacter genus[10]. It was then provisionally renamed as Helicobacter heilmannii (H. heilmannii), in acknowledgement of Konrad Heilmann, the German pathologist who first studied the pathologic features of this infection in the human stomach[11]. Further 16S rRNA analysis of an increasing number of samples led to the sub-classification of H. heilmannii into type 1 and type 2[10,12]. It was shown that H. heilmannii type 1 represented a single species, H. suis, that colonizes the stomachs of pigs[13], whereas H. heilmannii type 2 represented a group of species that colonize the stomachs of cats and dogs and includes H. felis, H. bizzozeronii, H. salomonis, H. cynogastricus, H. baculiformis, and H. heilmannii sp. nov.[14]. The latter had been provisionally named ‘‘Candidatus H. heilmannii’’ in 2004, based on urease gene sequence analysis and because it could not be cultured in vitro at that time[14]. In fact, only very recently and after successful in vitro isolation, H. heilmannii was formally recognized as a valid species name[15].

To avoid further confusion in nomenclature, in 2011 the introduction of the terms Helicobacter heilmanni sensu lato (H. heilmanni s.l.) was proposed to refer to the non-H. pylori Helicobacter species detected in the stomachs of humans or animals if only histopathological, electron microscopy, or crude taxonomic data are available; and Helicobacter heilmannii sensu stricto (H. heilmanni s.s.) or the other species names if definite identification at the species level is achieved[16].


As many as 11 different H. heilmannii s.l. have been described colonizing the stomach of domesticated and wild animals[17], 5 of which have been found in the human stomach, namely H. suis, H. felis, H. bizzozeronii, H. salomonis, and H. heilmannii s.s. (Table 1).

Table 1 Natural hosts and characteristics of Helicobacter heilmannii s.l. species that infect humans.
SpeciesNatural hostLength/width (μm)Number and distribution of flagellaPeriplasmatic fibrilsIn vitro isolation from humansRef.
H. heilmannii s.l.
H. bizzozeroniiCat, dog, fox ,lynx5-10/0.310-20, bipolarNoYes[17,42,81,106]
H. felisCat, dog, rabbit, cheetah5-7.5/0.410-17, bipolarYesYes[17,45,68,80]
H. heilmannii s.s.Cat, dog, fox, lynx, non-human primates3.0-6.5/0.6-0.74-10, bipolarNoNo[15,17,82,106]
H. salomonisCat, dog, rabbit5-7/0.8-1.210-23, bipolarNoNo[17,43,106]
H. suisPig, non-human primates2.3-6.7/0.9-1.24-10, bipolarNoNo[17,44,83]
H. pylori2.5-5.0/0.5-1.04-8, unipolarNoYes[6]

In Western countries as well as in Japan, the prevalence of H. heilmannii s.l. in human gastric biopsies is generally lower than 1%, both in adults and in children[18-23]. Reports from China and Thailand indicate that the prevalence of the infection can reach 2% and 6%, respectively[24,25].

Because of the nomenclature problems and due to the difficulty of cultivating these bacteria to allow species differentiation, there are few studies addressing the prevalence of each species individually. In gastric biopsy samples with histological evidence of H. heilmannii s.l., polymerase chain reaction (PCR)-based techniques showed that H. suis is the most prevalent H. heilmannii s.l. species infecting the human stomach, with prevalence ranging from 14% to 37%[26,27]. H. salomonis was present in 21%, H. felis in 15%, H. heilmannii s.s. in 8%, and H. bizzozzeronni in 4% of cases[27]. Infection with two or more H. heilmannii s.l. species or H. pylori and H. heilmannii s.l. can be present in the same gastric biopsy[28,29].

While H. pylori is known to colonize mainly humans and few non-human primates, H. heilmanni s.l. species have other non-human and probably more important hosts, such as cats, dogs, and pigs[17]. In addition to being present in the stomach, H. heilmannii s.l. species have also been reported in the oral cavity of domestic dogs and cats and, recently, H. bizzozeronii and H. salomonis were detected in canine saliva[30-32]. Several reports have suggested the transmission of H. heilmanni s.l. from pets to their owners by direct contact[33-36]. A higher prevalence of H. heilmanni s.l. infection among people that live in rural areas and of those who often have contact with dogs, cats, cattle, or pigs has been described[37-39]. It has further been suggested that H. suis might be transmitted to humans by consumption of contaminated raw pork meat, where the bacterium can viably persist for up to 48 h[40]. Given this evidence, it has been hypothesized that H. heilmannii s.l. infection is a zoonosis.


All H. heilmannii s.l. species are Gram-negative, microaerophilic, and catalase- and urease-positive[17]. The first descriptions of H. heilmannii s.l. used the term “corkscrew-like” bacteria because of their morphology[41]. As a group, these bacteria are microscopically very similar, with spiral and coiled shape, with 4-6 helical turns and 2.3-10 μm in length (Table 1)[11,15,42-45]. H. heilmannii s.l. have varying number of flagella, which have bipolar distribution, and fix themselves to a blunt undulated part of the cell wall[11]. H. felis is the only H. heilmannii s.l. species that has periplasmatic fibrils[15,42-45]. H. suis has several contrasting features when compared with other H. heilmannii s.l. species, since it may be shorter in length and have fewer flagella[15,42-45].


The relationships between H. heimannii s.l. and disease in humans are mostly based on publications that have only identified the agent as gastric non-H. pylori Helicobacters.

The initial description by Dent et al[8] of H. heimannii s.l. in the gastric mucosa of 3 patients with gastritis was followed by several other publications, mostly case reports[46-49]. Since then, H. heilmannii s.l. infection has been reported in cases of peptic ulcer disease[19,24,39,50], gastric carcinoma[50-52], and gastric MALT lymphoma[21,50,53]. Infected patients may be asymptomatic or present dyspeptic symptoms, such as chronic epigastric pain, nausea, vomiting, heartburn, dysphagia, and post-prandial discomfort[11,19,50,54].

Heilmann and Borchard were the first to report the histopathological and ultrastructural features of a large series of 39 cases with H. heilmannii s.l. infection[11]. Bacteria were more frequently found colonizing the antrum although 20% of the cases presented microorganisms also in the fundus. H. heilmannii s.l. were found as single microorganisms or in small groups, located underneath the mucous layer, above the surface cells, and deep in the lumen of the foveolae. In ultrastructural analyses, the close contact of some bacteria with the membrane of surface mucous cells, in association with degenerative changes of the cell membrane and partial destruction of the microvilli was reported[11]. The presence of H. heilmannii s.l. inside mucous and parietal cells and inside parietal cell canaliculi in the corpus mucosa was also observed[11,50]. H. heilmannii s.l.-infected cases mostly presented mild active chronic gastritis in the antrum and mild inactive gastritis in the fundus.

Some years later, Stolte et al[50] undertook a study to compare the parameters of gastritis between 202 German patients infected with H. heilmannii s.l. and 202 matched control patients infected with H. pylori. In agreement with the previous findings[11], they observed that H. heilmannii s.l. colonization occurred predominantly in the antrum and mainly focally[50]. They also observed that the grading of the parameters of gastritis, such as the density of lymphocytic and neutrophilic infiltration, the replacement of foveolae by regenerative epithelium, and mucus depletion were significantly milder in H. heilmannii s.l. infection than in H. pylori infection. Additionally, the presence of lymphoid follicles and intestinal metaplasia were less common in H. heilmannii s.l. gastritis[50]. Similar findings were reported in studies comparing the histopathological changes in the gastric mucosa between H. heilmannii s.l. and H. pylori infections in patients from other geographic areas, including Thailand, Japan, and Korea[21,24,55].

Interestingly, Stolte et al[50] observed a relatively high prevalence of gastric MALT lymphoma in H. heilmannii s.l. gastritis (3.5%), which prompted them to investigate their material from a 10-year period[56]. They observed 8 MALT lymphomas among patients with H. heilmannii s.l. gastritis (1.5%) in comparison with 1745 MALT lymphomas among 263680 patients with H. pylori gastritis (0.7%), suggesting that patients infected with H. heilmannii s.l. develop MALT lymphoma more frequently than those with H. pylori[56].

Although in the previous studies there was not a clear identification of the bacteria at a species level, in experimentally infected animal models the administration of H. heilmannii s.s.-positive gastric biopsy homogenates to BALB/c and to C57BL/6 mice induced gastric MALT lymphoma[57-59]. Furthermore, infection with pure bacterial isolates of H. felis[60-62] and of H. suis[63] were shown to induce gastric MALT lymphoma-like lesions in the BALB/c and in the Mongolian gerbil models, respectively.

The contribution of H. heilmannii s.l. to the pathogenesis of the aforementioned diseases is highlighted in reports in which eradication treatment of the bacteria is followed by symptomatic relief[11,36] and complete regression of the infection-associated lesions[11,64], including low-grade gastric MALT lymphoma[21,53,55].


The diagnosis of H. heilmannii s.l. infection poses a complex challenge in comparison to the well-established tests for H. pylori. The diagnosis of H. pylori can be achieved by non-invasive tests, which are based on detection of antibodies, bacterial antigens, or urease activity in samples such as blood, breath or stools; and invasive tests, which involve an endoscopy with collection of gastric biopsy specimens for histology, culture, urease test, or molecular methods[6].

The diagnosis of H. heilmannii s.l. has been based mainly on histological detection, and for this, silver staining-based techniques, such as the Steiner and the Whartin-Starry stains are preferable to hematoxylin and eosin[41]. There are currently no specific antibodies available for immunohistochemical detection of H. heilmannii s.l.[65]. Importantly, and although there may be morphological differences in size, number of spirals, and tightness of coils among H. heilmannii s.l species, and between these and H. pylori, these criteria are not accurate for species identification, as different species may be morphologically very similar, and variation in morphology within a single species may also occur[9,11,17,41].

The use of rapid urease tests allowing the detection of urease activity directly in the gastric biopsy specimens may not be sensitive enough[66], as the colonization density of H. heilmannii s.l. is lower than that of H. pylori, and also will not be helpful for species identification.

The use of in vitro culture as a diagnostic test is also not feasible due to the very fastidious nature of these bacteria. So far, very few laboratories have succeeded in the isolation of H. heilmannii s.l. from the gastric mucosa of cats, dogs, or pigs[15,44,45,67] and only H. bizzozeronii and H. felis have been isolated from the human gastric mucosa[35,68-70].

Currently, the most accurate method available for conclusive species identification is the use of PCR, followed by sequencing of specific target genes. These include the urease A and B (ureA, ureB) genes, the heat shock protein 60 (hsp60) gene, and the gyrase subunit B (gyrB) gene[44,71-74]. Sequencing of the 16S rRNA gene and of the 23S rRNA gene allows distinction of H. suis from the rest of the H. heilmannii s.l. species[13,44].


H. heilmannii s.l. eradication treatment is indicated in patients that present with severe pathology and clinical symptomatology associated with the infection[17]. No randomized trials have been performed to evaluate the most suitable treatment for H. heilmannii s.l. infection. The treatment strategies used are identical to the triple therapy regimen for H. pylori eradication, which include a proton pump inhibitor and clarithromycin combined with amoxicillin or metronidazole for 2 wk[64,75,76]. An in vitro antimicrobial susceptibility study of H. bizzozeronii, H. felis, and H. salomonis isolates obtained from cats and dogs showed that they were sensitive to ampicillin, clarithromycin, and tetracycline, among other pharmacological agents[77]. However, acquired resistance to metronidazole was observed for some H. bizzozeronii and H. felis isolates[77]. More recently, it was confirmed that H. bizzozeronii had a rapid in vitro acquisition of resistance to metronidazole, which should be taken into account when treating this species[78]. In a mouse model of infection used for evaluating the antibiotic susceptibility of 2 different H. suis isolates to amoxicillin and omeprazole, a difference in susceptibility between the bacterial isolates was observed[79].


Only after successful in vitro isolation of these extremely fastidious microorganisms did pure bacterial isolates become available. The complete genomes of 4 of the 5 human-infecting H. heilmannii s.l. have now been published[80-83] (Table 2). The sequencing of these genomes showed that H. suis, H. felis, H. bizzozeronii, and H. heilmannii s.s. share many homologues to genes associated with colonization and virulence properties of H. pylori and of other bacteria[80-83]. These include the urease gene cluster, encoding a key enzyme to bacterial survival in the acidic gastric environment[6], the neutrophil-activating protein NapA, the γ-glutamyl transpeptidase, as well as complete or almost complete comB secretion system, required for DNA uptake by natural transformation[84]. Although these species contain homologues of genes encoding several outer membrane proteins of H. pylori, they do not harbor homologues to the BabA and SabA adhesins. They also lack homologues of the H. pylori cag pathogenicity island, including the gene encoding CagA, and of the vacuolating cytotoxin VacA. The H. suis genome is an exception, since it contains a vacA homologue[83]. The dissimilarities between the genomes of H. heilmannii s.l species and the H. pylori genome, including the lack of homologues to well-known H. pylori virulence factors associated with disease, may partially explain some of the differences between H. pylori and H. heilmannii s.l.-associated pathology[80-83].

Table 2 General features of the available Helicobacter heilmannii s.l. species genomes and homology to Helicobacter pylori virulence genes.
H. suisH. felisH. bizzozeroniiH. heilmannii s.s.
StrainHS1HS5CS1 (ATCC 49179)CIII-1ASB1
Host, CountryPig, BelgiumPig, BelgiumAdult cat, Australia47-yr-old female patient with severe gastric symptoms, FinlandKitten with severe gastritis, Belgium
Genome size (MB)16351670167317551805
G + C content39.9%39.9%44.5%46%47.4%
Function assigned10721066138712801183
PlasmidsNot foundNot foundOne (6.7 Kb; 5 CDSs)One (52.1 Kb; 77 CDSs)Not found
VacAYes (63% homology)Yes (22% homology)NoNoNo
Ref.Vermoote et al[83]Arnold et al[80]Schott et al[81]Smet et al[82]

Comparative genome analysis also provided a putative molecular basis for the zoonotic nature of H. heilmannii s.l species[85]. In comparison to H. pylori, H. bizzozeronii, H. felis, and H. suis have a higher metabolic versatility and a higher number of methyl-accepting chemotaxis proteins, possibly facilitating their adaptation and survival in the gastric environment of different host species[80,83,85].


The lack of pure isolates has also limited the information available on the pathogenesis and host responses of individual H. heilmannii s.l. species. The major exception is H. felis for which experimental models of infection have existed since the early 1990’s, and for which different mice strains have been well-established as models of chronic gastritis[86], gastric atrophy[87-89], gastric MALT lymphoma[60], and gastric carcinoma[90,91]. Infection with H. felis in these models are often also used to study the pathogenesis of infection and the host immune response to H. pylori[92-95].

More recently, H. suis, H. bizzozeronii, and H. heilmannii s.s. pure isolates have been used in experimental models of infection[63,96-99]. Experimental infections with H. suis in Mongolian gerbils, BALB/c mice, and C57BL/6 mice showed that while in gerbils H. suis mainly colonized the antrum, in both mice strains H. suis was able to colonize the entire stomach[63]. Colonization with H. suis induced parietal cell necrosis in the 3 animal strains, epithelial cell hyperproliferation, and inflammation. In vitro data confirmed that H. suis causes apoptosis and necrosis of gastric epithelial cells, and indicated that the γ-glutamyl transpeptidase (GGT) virulence factor is involved in epithelial cell death[100]. H. suis GGT was also shown to inhibit T lymphocyte proliferation, and bacterial outer membrane vesicles were identified as a putative delivery route of GGT to the lymphocytes residing in the deeper mucosal layers[101].

Further experimental infections of BALB/c and C57BL/6 mice using 9 H. suis strains, showed that all H. suis isolates induced a predominant T-helper (Th)17 response, but only mild upregulation of the Th2 cytokine interleukin (IL)-4, and no upregulation of Th1 markers, including interferon (IFN)-γ[98]. This contrasts with previously published data which showed that H. suis induced a predominantly Th1 local immune response, and IFN-γ had a major role in the gastric inflammatory process[99,102]. A possible explanation for these differences is that previous experimental infection studies have used homogenized gastric specimens from mice, pigs or non-human primates instead of pure bacterial isolates[99,102].

In the Mongolian gerbil model, infection with H. suis led to the development of MALT lymphoma-like lesions in some animals[63], and in experimentally infected pigs, H. suis induced severe gastritis and a significant reduction in weight gain[103].

Concerning H. bizzozeronii, experimental infections in BALB/c, C57BL/6, SJL, and CFW mice showed that bacteria were mainly located in the gastric pits, dispersed through the mucous layer of the surface epithelium, or in close association with the parietal cells[104]. In the Mongolian gerbil model, H. bizzozeronii induced mild to moderate lymphocytic and neutrophilic infiltration in the gastric antrum of some animals, which was sometimes accompanied by mild parietal cell loss[105]. In the same study, transmission electron microscopy of H. bizzozeronii-infected gerbils showed neither necrotic parietal cells nor bacteria adhering to the epithelium[105]. Overall, H. bizzozeronii appears to be associated with a lower pathogenicity than H. pylori or H. felis[85].

Infection with 9 different H. heilmannii s.s. isolates in the Mongolian gerbil model showed that strains had different abilities to colonize the gerbil stomach. Furthermore, only 78% of the strains were able to induce chronic active gastritis and lymphocytic aggregation, caused by upregulation of IL-1β[96]. H. heilmannii s.s. strains with higher colonization ability were associated with higher fundic gastrin expression and reduced antral expression of the of H+/K+ ATPase pump[96].

Overall, these studies demonstrate that not only are there differences in the bacterium-host interactions between diverse H. heilmannii s.l. species, but there are also differences in the pathogenic potential in strains within the same species. Further studies will be necessary to address this question, namely the virulence factors involved and their putative associations with disease.


It is now recognized that H. heilmannii s.l. does not represent a single species, but rather several distinct Helicobacter species. H. heilmannii s.l. infect the stomach of several animals and may have zoonotic potential. Although the prevalence of these infections in humans is low, they are associated with gastric pathology and confer a higher risk of gastric MALT lymphoma than that of H. pylori infection, making them a significant health issue. So far, there are no studies that permit a clear stratification of the characteristics of the diseases according to each individual species that constitutes the group of gastric non-H. pylori Helicobacter species known as H. heilmanni s.l. Therefore, methods that allow bacterial identification at a species level are necessary to better clarify the prevalence of the infection in humans. Access to the full bacterial genome sequences together with the availability of increasing number of in vitro isolates will allow significant advances in the understanding of bacteria-host interactions in disease pathogenesis and will be essential for developing strategies of prevention and treatment.


P- Reviewer: Daniel F, Guan YS S- Editor: Qi Y L- Editor: Cant MR E- Editor: Liu XM

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