The DOI matches its Crossref record; 16 of the 16 references it cites were found in a registry or an index; 4 of the 10 sources its claims cite were checked for support.
Occurrence of Helicobacter Infection in the Gastric Mucosa of Free-living Red Foxes (Vulpes vulpes)
Open accessAbstract
We studied gastric Helicobacter spp. in five red foxes (Vulpes vulpes). Samples of stomach from the cardia, corpus, pyloric antrum, and duodenum were subjected to histopathologic, immunohistochemical, and transmission electron microscopy (TEM) examination for the presence of Helicobacter and gastritis. All foxes had gastric Helicobacter-like organisms (GHLOs) on examination by light microscopy and TEM. Gastric Helicobacter-like organisms were present in all areas of the stomachs. Chronic mild or moderate gastric inflammation was associated with infection by GHLOs in one or more regions of the stomach, but there was no correlation between inflammation and infection. It is not clear whether the organisms were causing the minimal histologic lesions observed, but the gastric mucosa of free-living foxes appears to be commonly colonized with GHLOs. The frequent colonization of free-living foxes with distinct GHLOs possibly reflects their special characteristic in feeding and/or social behavior or the potential commensal nature of the bacteria in free-ranging foxes.
Overview
AI snapshot
Written from the paper’s full text.
TL;DR
All five free-living red foxes examined had gastric Helicobacter-like organisms (GHLOs), with three morphologic types resembling H. felis, “H. heilmannii,” and H. pylori. Infection was associated with mild chronic gastritis in most foxes, but there was no correlation between bacterial colonization and inflammation.
Key findings
- GHLOs were present in all five foxes by light microscopy and transmission electron microscopy; no GHLOs were visualized in the duodenum. In four foxes, spiral bacteria were present at all three gastric sites (cardia, corpus, pyloric antrum), and in a fifth fox bacteria were confined to the antrum.
- Three morphologically different bacteria were observed: H. felis-like organisms in three of five foxes, “H. heilmannii”-like organisms in three foxes, and H. pylori-like organisms in one fox. Two foxes had combined infection by two different morphologic types.
- One fox had no gastric inflammation; the others had mild gastritis in one or all parts of the stomach. Inflammatory cells consisted of lymphocytes and plasma cells, and lymphoid aggregates occurred in the lamina propria of the corpus or pyloric antrum in three foxes.
- There was no correlation between the presence or density of bacteria and gastric inflammation. Gastric epithelial changes were present only in the single fox harboring H. pylori-like organisms.
Methods
- Specimens were collected between December 2000 and December 2002 from five adult free-ranging red foxes (Vulpes vulpes; three male, two female) hunted by farmers in Turkey; average weight was 8 kg (range 7–9 kg).
- Samples from the cardia, corpus, pyloric antrum, and duodenum were examined histopathologically with hematoxylin and eosin and Warthin-Starry silver stain, immunohistochemically with a rabbit polyclonal antibody against Helicobacter pylori, and by transmission electron microscopy.
- Gastritis was classified and graded using a modification of the updated Sydney system; bacterial colonization was graded semiquantitatively, and morphologic characteristics were determined by measuring 50 bacteria from 10 fields at ×1,000 magnification.
Limitations
- The paper states that it is not clear whether the organisms were causing the minimal histologic lesions observed, and that whether less-common morphologies represent different forms of the same species or different organisms cannot be determined from the present study.
- The study examined only five foxes, a small sample evident from the text, limiting prevalence estimates and statistical inference.
- Identification relied on morphology, immunohistochemistry, and TEM rather than culture or molecular sequencing, so species-level classification remains presumptive.
Model-written summary. Check it against the paper before relying on it.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
4 of 10 cited sources checked · 2 supported · 0 flagged · accuracy not yet measured
- Interpretationcitation
The absence of a correlation between Helicobacter colonization density and severity or extent of mucosal changes is similar to results of other studies.
“The absence of a correlation between Helicobacter colonization density and severity or extent of mucosal changes is similar to results of other studies (Happonen et al., 1998;Yamasaki et al., 1998).”
Quote in the paperNot a substantial claim2 of 2 sources checked- cites Happonen et al., 1998 source
The Results and Clinical Implications (p. 1767) report no significant association between Helicobacter colonization density and the degree of gastric inflammation in the dogs studied. This supports the severity aspect of the claim, but our copy does not establish a lack of association with the extent of mucosal changes. (LLM, conf=0.84)
Experimental — accuracy not yet measured - cites Yamasaki et al., 1998 source
The Results (p. 2) report frequent grade-3 gastric spiral organism infection alongside mostly grade-1 gastric lesions, which is consistent with the cited comparison. But the paper grades the organisms’ location rather than colonization density and does not report a correlation analysis between density and the severity or extent of mucosal changes. (LLM, conf=0.77)
Experimental — accuracy not yet measured
- Findingown data
GHLOs were not visualized in the duodenum of any fox.
“no GHLOs were visualized in the duodenum.”
Quote in the paperNot a substantial claim - Findingown data
All five free-living red foxes examined had gastric Helicobacter-like organisms (GHLOs) on light microscopy and TEM.
“All foxes had gastric Helicobacter-like organisms (GHLOs) on examination by light microscopy and TEM.”
- Also stated in: § Abstract · plain
“Warthin-Starry and immunostaining revealed gastric bacteria in all foxes”
Quote in the paperSubstantial claim - Also stated in: § Abstract · plain
- Findingown data
The intensity of bacterial colonization was slightly greater in the pyloric antrum than in the other two gastric regions.
“In four foxes, spiral bacteria were present at all three sites in the stomach; the intensity of colonization was slightly more in the pyloric antrum than the other two gastric regions.In a fifth fox, bacteria were confined to the antrum.”
Quote in the paperNot a substantial claim - Findingown data
In two foxes, H. heilmannii-like organisms (HHLOs) were present together with H. felis-like organisms.
“In two foxes, ''H.heilmannii''like organisms (HHLOs) were present together with H. felis-like organisms.”
Quote in the paperNot a substantial claim
- Findingown data
Inflammatory cells consisted of lymphocytes and plasma cells.
“Inflammatory cells consisted of lymphocytes and plasma cells (Table 1).”
Quote in the paperNot a substantial claim - Findingown data
Gastric epithelial changes were present only in the single fox harboring HPLOs.
“Gastric epithelial changes were present only in the single fox harboring HPLOs.”
Quote in the paperNot a substantial claim - Findingown data
Chronic mild or moderate gastric inflammation was associated with infection by GHLOs in one or more regions of the stomach.
“Chronic mild or moderate gastric inflammation was associated with infection by GHLOs in one or more regions of the stomach”
Quote in the paperSubstantial claim - Findingown data
Sections from one fox had a relatively short form of spiral bacteria, corkscrew-like (4-6 turns), 4-5 μm in length, most closely resembling H. heilmannii with different morphology.
“Sections from one fox had a relatively short form of spiral bacteria.They were corkscrew-like (4-6 turns) and 4-5 m in length (Fig. 1).On the basis of these morphologic characteristics, they most closely resembled ''H.heilmannii,'' with different morphology.”
Quote in the paperNot a substantial claim- Rests on an assumption: Morphologic characteristics are sufficient to identify Helicobacter-like organisms as resembling H. felis, H. heilmannii, or H. pylori.
- Findingown data
Bacterial colonization densities ranged from mild to marked.
“Bacterial colonization densities ranged from mild to marked (Table 1).”
Quote in the paperNot a substantial claim - Findingown data
In three foxes, lymphoid aggregates occurred in the lamina propria of the corpus or pyloric antrum.
“In three foxes, lymphoid aggregates occurred in the lamina propria of the corpus or pyloric antrum.”
Quote in the paperNot a substantial claim - Findingown data
There was no correlation between the presence or density of bacteria and gastric inflammation.
“There was no correlation between the presence or density of bacteria and gastric inflammation.”
Quote in the paperSubstantial claim - Findingown data
Three morphologically different types of bacteria were observed in the gastric mucosa of infected foxes.
“Three morphologically different types of bacteria were observed.”
Quote in the paperNot a substantial claim - Interpretationreasoning
The chronic nature of the inflammation suggests that the foxes had harbored the infection for a long time.
“The chronic nature of the inflammation suggests that the foxes had harbored the infection for a long time.”
Quote in the paperNot a substantial claim - Interpretationown data
Helicobacter-like bacteria commonly colonize the gastric mucosa of free-living foxes.
“Helicobacter-like bacteria commonly colonize the gastric mucosa of free-living foxes”
- Also stated in: § Abstract · plain
“the stomach of free-living foxes is commonly colonized with Helicobacter-like organisms”
Quote in the paperSubstantial claim- Rests on an assumption: The five free-ranging foxes sampled in Turkey are representative of free-living red foxes generally.
- Also stated in: § Abstract · plain
- Probably not a substantial claim. 8
- It may state two separate claims as one. 10
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
PremisecitationSimilar mild chronic gastritis has been observed in natural or experimental Helicobacter infection in dogs and cats, and the scarcity of polymorphonuclear leucocytes is a feature of Helicobacter gastritis in most animal models, as well as in children.
“Similar mild chronic gastritis has been observed in natural or experimental Helicobacter infection in dogs (Lee et al., 1992) and cats (Norris et al., 1999), and the scarcity of polymorphonuclear leucocytes is a feature of Helicobacter gastritis in most animal models (Diker et al., 2002), as well as in children (Camorlinga-Ponce et al., 2003).”
Quote in the paperNot a substantial claim1 of 3 sources checkedProbably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationH. heilmannii may represent multiple species.
“''Helicobacter heilmannii'' may represent multiple species (Trebesius et al., 2001)”
Quote in the paperNot a substantial claim1 of 1 sources checked- cites Trebesius et al., 2001 source
It may state two separate claims as one.
Findingown dataIn four of five foxes, spiral bacteria were present at all three sites in the stomach (cardia, corpus, pyloric antrum); in the fifth fox, bacteria were confined to the antrum.
“In four foxes, spiral bacteria were present at all three sites in the stomach; the intensity of colonization was slightly more in the pyloric antrum than the other two gastric regions.In a fifth fox, bacteria were confined to the antrum.”
Quote in the paperSubstantial claimIt may state two separate claims as one.
Findingown dataA single animal had no gastric inflammation; the other foxes had mild gastritis in one or all parts of the stomach; gastritis scores within each animal were generally similar at all sites.
“A single animal had no gastric inflammation.The other foxes had mild gastritis in one or all parts of the stomach; the gastritis scores within each animal were generally similar at all sites.”
Quote in the paperNot a substantial claimIt may state two separate claims as one.
Findingown dataThe organisms in that specimen were a relatively short form of helical bacteria, with six to seven coils, average length 4-5 μm, distance 0.75-1 μm per turn, 0.8-1 μm diameter at center, tapering to 0.5-0.7 μm at ends, pitch 70-80° from longitudinal axis, at least one terminal tuft of five to eight flagella, and no periplasmic or axial fibrils observed.
“The organisms were a relatively short form of helical bacteria, with six to seven coils of average length of 4-5 m (Fig. 3a) and a distance of 0.75-1 m for every turn.They were 0.8-1 m in diameter at the center and tapered to a diameter of 0.5-0.7 m at the ends.The spirals were quite tight, with a pitch of 70-80Њ from the longitudinal axis (Fig. 3b).At least one terminal tuft of five to eight flag”
Quote in the paperSubstantial claimIt may state two separate claims as one.
Findingown dataThe presence of Helicobacter spp. in fox stomachs was associated with limited tissue reactions; the lesions consisted mainly of lymphoplasmacytic and some mucosal lymphocytic aggregates.
“The presence of Helicobacter spp. in fox stomachs was associated with limited tissue reactions; the lesions consisted mainly of lymphoplasmacytic and some mucosal lymphocytic aggregates.”
Quote in the paperSubstantial claimIt may state two separate claims as one.
Findingown dataImmunolabeling ranged from diffuse to focal, with most samples demonstrating positive organisms in the surface mucus covering the gastric epithelium; bacteria also occurred in gastric pits and glands.
“Immunolabeling ranged from diffuse to focal, with most samples demonstrating positive organisms in the surface mucus covering the gastric epithelium; bacteria also occurred in gastric pits and glands.”
Quote in the paperSubstantial claim- Rests on an assumption: The rabbit polyclonal antibody against H. pylori cross-reacts with the gastric Helicobacter organisms in foxes.
It may state two separate claims as one.
Findingown dataIn the semithin section of the specimen from a fox infected with Helicobacter resembling H. heilmannii, bacteria were on mucosal surfaces or within glandular lumina, often mixed with mucus strands, and also found intracellularly within gastric parietal cell canaliculi; there was no evidence of attachment to gastric epithelial cells.
“Bacteria were on the mucosal surfaces or within the glandular lumina and were often mixed with mucus strands.They were also found intracellularly within the gastric parietal cell canaliculi.There was no evidence of attachment to gastric epithelial cells.”
Quote in the paperNot a substantial claimIt may state two separate claims as one.
Findingown dataThe second bacterial type, found in three foxes, consisted of long and tightly coiled organisms (7-13 turns) with an average length of 8 μm, two to three turns at intervals of average 2 μm, did not taper at the ends, and was similar to H. heilmannii.
“The second bacterial type was found in three foxes.These bacteria were long and tightly coiled (7-13 turns) organisms with an average length of 8 m having two to three turns at intervals of average 2 m and did not taper at the ends.On the basis of these morphologic characteristics they were similar to ''H.heilmannii.''”
Quote in the paperNot a substantial claim- Rests on an assumption: Morphologic characteristics are sufficient to identify Helicobacter-like organisms as resembling H. felis, H. heilmannii, or H. pylori.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
Findingown dataA single fox had larger numbers of inflammatory cells in a single site (the antrum).
“A single fox had larger numbers of inflammatory cells in a single site (the antrum).”
Quote in the paperNot a substantial claimIt may state two separate claims as one.
Findingown dataA third morphologically distinct microorganism, about 3-4 μm long and 0.3-0.4 μm in diameter, was seen in the lumen of pyloric glands; its shape ranged among rodlike, slightly curved and spiral appearances; spiral forms usually displayed two to three loose spiral turns; bacteria occurred singly or in groups only in glandular lumina or on mucosal surfaces; most closely resembled H. pylori.
“The third morphologically distinct microorganisms about 3-4 m long and 0.3-0.4m in diameter were seen in the lumen of pyloric glands (Fig. 2).The shape ranged among rodlike, slightly curved and spiral appearances.Spiral forms usually displayed two to three loose spiral turns.The bacteria occurred singly or in groups only in the glandular lumina or on the mucosal surfaces.On the basis of these morp”
Quote in the paperSubstantial claim- Rests on an assumption: Morphologic characteristics are sufficient to identify Helicobacter-like organisms as resembling H. felis, H. heilmannii, or H. pylori.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
Study design and conductcitationThe classification and grading of gastritis was based on a modification of the updated Sydney system used to describe histologic lesions in humans with gastritis.
“The classification and grading of gastritis was based on a modification of the updated Sydney system used to describe histologic lesions in humans with gastritis (Dixon et al., 1996).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Dixon et al., 1996 source
- Rests on an assumption: The modified updated Sydney system for grading gastritis in humans is valid for grading gastritis in foxes.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
Interpretationown dataThe infrequent occurrence of less-common morphologies suggests they represent a different form of the same species rather than different organisms.
“Whether these less-common morphologies represent a different form of the same species or different organisms cannot be determined from the present study, although their infrequent occurrence suggests the former.”
Quote in the paperNot a substantial claimProbably not a substantial claim. It may be too vague to check against evidence. The paper may give no reason why it holds. It may state two separate claims as one.
InterpretationreasoningThe frequent colonization of free-living foxes with distinct GHLOs possibly reflects their special characteristic in feeding and/or social behavior or the potential commensal nature of the bacteria in free-ranging foxes.
“The frequent colonization of free-living foxes with distinct GHLOs possibly reflects their special characteristic in feeding and/or social behavior or the potential commensal nature of the bacteria in free-ranging foxes.”
Quote in the paperNot a substantial claimProbably not a substantial claim. The paper’s conclusions may not depend on it.
Study design and conductnone givenNormal rabbit serum was used as a negative control.
“Normal rabbit serum was used as a negative control.”
Quote in the paperNot a substantial claimProbably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationAn organism very similar to H. pylori has been isolated from captive cheetahs, lions, and tigers with gastritis.
“an organism very similar to H. pylori has been isolated from captive cheetahs (Eaton et al., 1993a, b), lions (Jakob et al., 1997;Seidel et al., 2001b), and tigers (Panthera tigris) (Jakob et al., 1997) with gastritis.”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites Eaton et al., 1993a, b
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites Jakob et al., 1997 source
- cites Seidel et al., 2001b
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
The paper relies on this without support.
The five free-ranging foxes sampled in Turkey are representative of free-living red foxes generally.
“Between December 2000 and December 2002, specimens were collected from five adult free-ranging foxes (Vulples vulpes; three male and two female) hunted by farmers in Turkey”
“the stomach of free-living foxes is commonly colonized with Helicobacter-like organisms”
The paper relies on this without support.
Morphologic characteristics are sufficient to identify Helicobacter-like organisms as resembling H. felis, H. heilmannii, or H. pylori.
“These morphologic features most closely resembled H. felis.”
“On the basis of these morphologic characteristics they were similar to ''H.heilmannii.''”
“On the basis of these morphologic characteristics, they most closely resembled H. pylori.”
The paper relies on this without support.
The modified updated Sydney system for grading gastritis in humans is valid for grading gastritis in foxes.
“The classification and grading of gastritis was based on a modification of the updated Sydney system used to describe histologic lesions in humans with gastritis (Dixon et al., 1996).”
The paper relies on this without support.
The rabbit polyclonal antibody against H. pylori cross-reacts with the gastric Helicobacter organisms in foxes.
“A primary rabbit polyclonal antibody against Helicobacter pylori (Dako Diagnostica GmbH, Hamburg, Germany) was used at a 1:300 dilution.”
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
TEM examination is attributed to all five foxes but was performed on one
MinorThe abstract says all foxes had organisms on examination by both light microscopy and TEM. The methods describe preparing gastric mucosa from only one case for TEM, so TEM could not have confirmed organisms in all five foxes.
“All foxes had gastric Helicobacter-like organisms (GHLOs) on examination by light microscopy and TEM.”
“Formalin-fixed gastric mucosa from one case were postfixed in 1% osmium tetroxide, dehydrated, infiltrated, and embedded in epoxy resin.”
Citations
Cites
The publisher hasn’t deposited this paper’s reference list.
Research works printed but not linked: 6
- DIKER, K. S., R. HAZIROGLU, M. AKAN, S. C ¸ELIK, AND N. KABAKC ¸I. 2002. The prevalence, coloni- zation sites and pathological effects of gastric hel- icobacters in dogs. Turkish Journal of Veterinary Animal Sciences 26: 345-351.
- M. B. BRIGGS, K. VENZKE, O. FORGE, AND R. D. MURNANE. 1998b. Gastric spiral bacteria and intramuscular sarcocysts in African lions from Namibia. Journal of Wildlife Diseases 34: 317-324.
- LUNA, L. G. 1968. Manual of histologic staining methods of the Armed Forces Institute of Pa- thology. 3rd Edition, McGraw-Hill Book Com- pany, New York, 238 pp.
- NEIGER, R. 2001. Helicobacter-gastritis in cats and dogs. In Proceedings of the 7th Federation of European Companion Animal Veterinary Asso- ciations and 47th Fachgruppe Kleintierkrankhei- ten der Deutschen Veterindrmedizinischen Ge- sellschaft congress. 25-28 October, Berlin, Ger- many, pp. 89-91.
- M. RUDOLPH, J. BAUER, A. KOLM, R. FRIES, G. DURSTEWITZ, AND W. JAKOB. 2001a. Occur- rence of Helicobacter sp. in a wide range of cap- tive carnivores. International Journal of Medical Microbiology 291 (Supplement 31): 3-4. , , , , , , AND . 2001b. Helicobacter sp. isolated from gastric mucosa of captive lions. Internation- al Journal of Medical Microbiology 291 (Supple- ment 31): 148.
- SHEN, Z., J. G. FOX, F. E. DEWHIRST, B.J. PASTER, C. J. FOLTZ, L. YAN, B. SHAMES, AND L. PERRY. 1997. Helicobacter rodentium sp. v., a urease- negative Helicobacter species isolated from lab- oratory mice. International Journal of Systematic Bacteriology 47: 627-634.
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Metadata
- Authors
- Erginsoy, S. D., Sozmen, M., Ozcan, K., & Tuzcu, M.
- Affiliations
- Kafkas University (TR)
- Department of Pathology, Faculty of Veterinary Medicine, University of Kafkas, Pasacayiri, Kars 36100, Turkey
- ORCID
- Tuzcu, Mehmet
- Venue
- Journal of Wildlife Diseases
- Publisher
- Wildlife Disease Association
- Published
- 2004-07
- Volume
- 40
- Issue
- 3
- Pages
- 548-554
- ISSN
- 0090-3558 (ISSN-L)
- OpenAlex
- W1975677773
- Semantic Scholar
- ce68e67f395633643411d7b7067d0b9045fbf2eb
- Cited by
- 6
- References
- 0
- Citations by year
- 2020: 1 · 2012: 1
- FWCI
- 0.00
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Wildlife Diseases (publishedVersion)
- PubMed (publishedVersion)
- BioOne Complete (BioOne) (submittedVersion)
- Topics
- Health Sciences › Medicine › Gastroenterology › Helicobacter pylori-related gastroenterology studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
- Keywords
- Helicobacter, red fox, gastric mucosa, gastritis, gastric colonization, commensal bacteria, stomach histopathology
- MeSH terms
- Animals, Animals, Wild, Female, Foxes, Gastric Mucosa, Gastritis, Immunohistochemistry, Male, Stomach, Helicobacter Infections, Helicobacter, Microscopy, Electron, Transmission
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