Although recent research has provided better insights into Helicobacter pylori, much remains unknown regarding non-H. pylori Helicobacter species in animals. Pet animals living close to humans may act as a potential reservoir for a diverse Helicobacter species. Hence, this study aimed to investigate Helicobacter spp.’s prevalence among pet animals suffering from gastroenteritis and their zoonotic relevance.
Materials and methods:
Eighty-seven fecal samples were collected from dogs (53) and cats (34) suffering from gastroenteritis. The DNA was extracted for the molecular detection of Helicobacter spp., H. canis, H. felis, and H. pylori through amplification of Helicobacter 16S rRNA as well as multiplex PCR targeting H. canis Hsp60, H. felis urease, and H. pylori urease C genes in all samples. Sequencing of some selected PCR amplicons and phylogenetic analysis were conducted.
Results:
The overall prevalence of Helicobacter spp. ws 34.5%, with the following rates: 37.7% and 29.4% among dogs and cats, respectively. H. canis had the highest occurrence rate (20.7%), whereas H. pylori was detected at 11.5%, followed by H. felis at 2.3%. Coinfection with more than one Helicobacter species has been documented. Furthermore, the phylogenetic analysis of three partial H. canis 16S rRNA sequences revealed a high genetic relatedness to strains derived from a diarrheic cat and human bacteremic patients with a history of pet exposure, indicating the public health implications of these sequences.
Conclusion:
The fecal carriage of diverse Helicobacter spp. among dogs and cats suffering from gastroenteritis, with a predominance of H. canis, highlights a potential risk of zoonotic transmission of such pathogens between pets and human contacts.
Get full access to this article
View all access options for this article.
References
1.
AbidiMZ, WilhelmMP, NeffJL, et al.Helicobacter canis bacteremia in a patient with fever of unknown origin. J Clin Microbiol, 2013; 51(3):1046–1048; doi: 10.1128/JCM.02548-12
2.
AhmadiR, ArfaeeF, JamshidiS, et al.Prevalence and diversity of enteric Helicobacter spp. in healthy and diarrheic cats. Iran J Microbiol, 2024; 16(4):569–575; doi: 10.1850/2/ijm.v16i4.16317
3.
AlonD, PaitanY, Ben-NissanY, et al.Persistent Helicobacter canis bacteremia in a patient with gastric lymphoma. Infection, 2010; 38(1):62–64; doi: 10.1007/s15010-009-9067-6
4.
AmorimI, SmetA, AlvesO, et al.Presence and significance of Helicobacter spp. in the gastric mucosa of Portuguese dogs. Gut Pathog, 2015; 7:12; doi: 10.1186/s13099-015-0057-1
5.
AshaoluJO, TsaiYJ, LiuCC, et al.Prevalence, diversity and public health implications of Helicobacter species in pet and stray dogs. One Health, 2022; 15:100430; doi: 10.1016/j.onehlt.2022.100430
6.
BhatAH. Bacterial zoonoses transmitted by household pets and as reservoirs of antimicrobial resistant bacteria. Microb Pathog, 2021; 155:104891; doi: 10.1016/j.micpath.2021.104891
7.
BridgefordEC, MariniRP, FengY, et al.Gastric Helicobacter species as a cause of feline gastric lymphoma: A viable hypothesis. Vet Immunol Immunopathol, 2008; 123(1–2):106–113; doi: 10.1016/j.vetimm.2008.01.016
8.
BurnensAP, StanleyJ, SchaadUB, et al.Novel Campylobacter-like organism resembling Helicobacter fennelliae isolated from a boy with gastroenteritis and from dogs. J Clin Microbiol, 1993; 31(7):1916–1917; doi: 10.1128/jcm.31.7.1916-1917.1993
9.
Canejo-TeixeiraR, OliveiraM, PissarraH, et al.A mixed population of Helicobacter pylori, Helicobacter bizzozeronii and “Helicobacter heilmannii” in the gastric mucosa of a domestic cat. Ir Vet J, 2014; 67(1):25; doi: 10.1186/2046-0481-67-25
10.
De CoomanL, HoufK, SmetA, et al.Presence of Helicobacter suis on pork carcasses. Int J Food Microbiol, 2014; 187:73–76; doi: 10.1016/j.ijfoodmicro.2014.06.016
11.
De GrooteD, Van DoornLJ, Van den BulckK, et al.Detection of non-pylori Helicobacter species in “Helicobacter heilmannii”-infected humans. Helicobacter, 2005; 10(5):398–406; doi: 10.1111/j.1523-5378.2005.00347.x
12.
EkmanE, FredrikssonM, Trowald-WighG. Helicobacter spp. in the saliva, stomach, duodenum and faeces of colony dogs. Vet J, 2013; 195(1):127–129; doi: 10.1016/j.tvjl.2012.05.001
13.
ElhaririM, HamzaD, ElhelwR, HamzaE. Occurrence of cagA+vacA s1a m1 i1 Helicobacter pylori in farm animals in Egypt and ability to survive in experimentally contaminated UHT milk. Sci Rep, 2018; 8(1):14260; doi: 10.1038/s41598-018-32671-0
14.
ElyasiB, RezaieA, Moori BakhtiariN, et al.Helicobacter genus in the intestine and liver of stray cats: The molecular, histopathological, and immunohistochemical study. Braz J Microbiol, 2020; 51(4):2123–2132; doi: 10.1007/s42770-020-00359-1
15.
FlahouB, RossiM, BakkerJ, et al.Evidence for a primate origin of zoonotic Helicobacter suis colonizing domesticated pigs. Isme J, 2018; 12(1):77–86; doi: 10.1038/ismej.2017.145
16.
FoleyJE, MarksSL, MunsonL, et al.Isolation of Helicobacter canis from a colony of bengal cats with endemic diarrhea. J Clin Microbiol, 1999; 37(10):3271–3275; doi: 10.1128/JCM.37.10.3271-3275.1999
17.
FoxJG, DroletR, HigginsR, et al.Helicobacter canis isolated from a dog liver with multifocal necrotizing hepatitis. J Clin Microbiol, 1996; 34(10):2479–2482; doi: 10.1128/jcm.34.10.2479-2482.1996
18.
FritzEL, SlavikT, DelportW, et al.Incidence of Helicobacter felis and the effect of coinfection with Helicobacter pylori on the gastric mucosa in the African population. J Clin Microbiol, 2006; 44(5):1692–1696; doi: 10.1128/JCM.44.5.1692-1696.2006
19.
GermaniY, DaugaC, DuvalP, et al.Strategy for the detection of Helicobacter species by amplification of 16S rRNA genes and identification of H. felis in a human gastric biopsy. Res Microbiol, 1997; 148(4):315–326; doi: 10.1016/S0923-2508(97)81587-2
20.
GerrardJ, AlfredsonD, SmithI. Recurrent bacteremia and multifocal lower limb cellulitis due to Helicobacter-like organisms in a patient with X-linked hypogammaglobulinemia. Clin Infect Dis, 2001; 33(10):E116–E8; doi: 10.1086/323405
21.
GhilHM, YooJH, JungWS, et al.Survey of Helicobacter infection in domestic and feral cats in Korea. J Vet Sci, 2009; 10(1):67–72; doi: 10.4142/jvs.2009.10.1.67
22.
GhysenK, SmetA, DenormeP, et al.An atypical presentation of an acute gastric Helicobacter felis infection. Acta Gastroenterol Belg, 2018; 81(3):436–438.
23.
HaesebrouckF, PasmansF, FlahouB, et al.Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clin Microbiol Rev, 2009; 22(2):202–223, Table of Contents; doi: 10.1128/CMR.00041-08
24.
Kubota-AizawaS, MatsubaraY, KanemotoH, et al.Transmission of Helicobacter pylori between a human and two dogs: A case report. Helicobacter, 2021; 26(3):e12798; doi: 10.1111/hel.12798
25.
KustersJG, van VlietAH, KuipersEJ. Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev, 2006; 19(3):449–490; doi: 10.1128/CMR.00054-05
26.
LardinoisB, BelkhirL, VerrokenA. Helicobacter canis: A review of microbiological and clinical features. Front Microbiol, 2021; 12:814944; doi: 10.3389/fmicb.2021.814944
27.
LecoindreP, ChevallierM, PeyrolS, et al.Gastric helicobacters in cats. J Feline Med Surg, 2000; 2(1):19–27; doi: 10.1053/jfms.2000.0063
28.
LeeA, FoxJG, OttoG, et al.A small animal model of human Helicobacter pylori active chronic gastritis. Gastroenterology, 1990; 99(5):1315–1323; doi: 10.1016/0016-5085(90)91156-z
29.
LeeA, HazellSL, O’RourkeJ, et al.Isolation of a spiral-shaped bacterium from the cat stomach. Infect Immun, 1988; 56(11):2843–2850; doi: 10.1128/iai.56.11.2843-2850.1988
30.
LeemannC, GambillaraE, Prod’homG, et al.First case of bacteremia and multifocal cellulitis due to Helicobacter canis in an immunocompetent patient. J Clin Microbiol, 2006; 44(12):4598–4600; doi: 10.1128/JCM.01453-06
31.
MalfertheinerP, MegraudF, O’MorainCA, et al.; European Helicobacter and Microbiota Study Group and Consensus panel. Management of Helicobacter pylori infection-the Maastricht V/Florence Consensus Report. Gut, 2017; 66(1):6–30; doi: 10.1136/gutjnl-2016-312288
32.
MarshallBJ, WarrenJR. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet, 1984; 1(8390):1311–1315; doi: 10.1016/s0140-6736(84)91816-6
33.
MihevcM, Koren KrajncM, Bombek IhanM, et al.Helicobacter canis bacteraemia in a rheumatoid arthritis patient treated with tofacitinib: Case report and literature review. Ann Clin Microbiol Antimicrob, 2021; 20(1):22; doi: 10.1186/s12941-021-00426-x
MoussaIM, EljakeeJ, BederM, et al.Zoonotic risk and public health hazards of companion animals in the transmission of Helicobacter species. J King Saudi Univ, 2021; 33(6):101494.
36.
MoyaertH, PasmansF, DucatelleR, et al.Evaluation of 16S rRNA gene-based PCR assays for genus-level identification of Helicobacter species. J Clin Microbiol, 2008; 46(5):1867–1869; doi: 10.1128/JCM.00139-08
37.
NeigerR, DieterichC, BurnensA, et al.Detection and prevalence of Helicobacter infection in pet cats. J Clin Microbiol, 1998; 36(3):634–637; doi: 10.1128/JCM.36.3.634-637.1998
38.
OchoaS, OjedaJ, MartínezOA, et al.Exploring the role of healthy dogs as hosts of enterohepatic Helicobacter species using cultivation-dependent and -independent approaches. Zoonoses Public Health, 2021; 68(4):344–352; doi: 10.1111/zph.12817
39.
PereiraMI, MedeirosJA. Role of Helicobacter pylori in gastric mucosa-associated lymphoid tissue lymphomas. World J Gastroenterol, 2014; 20(3):684–698; doi: 10.3748/wjg.v20.i3.684
40.
PragJ, BlomJ, KrogfeltKA. Helicobacter canis bacteraemia in a 7-month-old child. FEMS Immunol Med Microbiol, 2007; 50(2):264–267; doi: 10.1111/j.1574-695X.2007.00271.x
41.
RossiM, HänninenML, RevezJ, et al.Occurrence and species level diagnostics of Campylobacter spp., enteric Helicobacter spp. and Anaerobiospirillum spp. in healthy and diarrheic dogs and cats. Vet Microbiol, 2008; 129(3–4):304–314; doi: 10.1016/j.vetmic.2007.11.014
42.
SabbaghP, Mohammadnia-AfrouziM, JavanianM, et al.Diagnostic methods for Helicobacter pylori infection: Ideals, options, and limitations. Eur J Clin Microbiol Infect Dis, 2019; 38(1):55–66; doi: 10.1007/s10096-018-3414-4
43.
SabryMA, Abdel-MoeinKA, SeleemA. Evidence of zoonotic transmission of Helicobacter canis between sheep and human contacts. Vector Borne Zoonotic Dis, 2016; 16(10):650–653; doi: 10.1089/vbz.2016.1994
44.
SamirA, Abdel-MoeinKA, ZaherHM. Molecular detection of toxigenic Clostridioides difficile among diarrheic dogs and cats: A mounting public health concern. Vet Sci, 2021; 8(6):88; doi: 10.3390/vetsci8060088
45.
ScanzianiE, SimpsonKW, MonestiroliS, et al.Histological and immunohistochemical detection of different Helicobacter species in the gastric mucosa of cats. J Vet Diagn Invest, 2001; 13(1):3–12; doi: 10.1177/104063870101300102
46.
ShaabanSI, TalatD, KhatabSA, et al.An investigative study on the zoonotic potential of Helicobacter pylori. BMC Vet Res, 2023; 19(1):16; doi: 10.1186/s12917-023-03572-w
47.
ShakerAA, SamirA, ZaherHM, Abdel-MoeinKA. Occurrence of major human Extraintestinal pathogenic Escherichia coli sequence types among diarrheic pet animals: A potential public health threat. Vector Borne Zoonotic Dis, 2023; 23(11):568–575; doi: 10.1089/vbz.2022.0075
48.
ShakerAA, SamirA, ZaherHM, Abdel-MoeinKA. The burden of Acinetobacter baumannii among pet dogs and cats with respiratory illness outside the healthcare facilities: A possible public health concern. Vector Borne Zoonotic Dis, 2025; 25(2):118–124; doi: 10.1089/vbz.2024.0082
49.
ShakerAA, SamirA, ZaherHM, et al.Emergence of virulent extensively drug-resistant vancomycin-resistant Enterococci among diarrheic pet animals: A possible public health threat on the move. Vector Borne Zoonotic Dis, 2024; 24(9):600–606; doi: 10.1089/vbz.2023.0167
50.
ShakirSM, Powers-FletcherMV, SlechtaES, et al.Helicobacter canis bacteraemia and cellulitis in a patient with end-stage renal disease. JMM Case Rep, 2017; 4(11):e005126; doi: 10.1099/jmmcr.0.005126
51.
ShinozakiJK, SellonRK, CantorGH, et al. Fecal polymerase chain reaction with 16S ribosomal RNA primers can detect the presence of gastrointestinal Helicobacter in dogs. Veterinary Internal Medicne 2002;16(4):426–432; doi: 10.1111/j.1939-1676.2002.tb01260.x
52.
StanleyJ, LintonD, BurnensAP, et al.Helicobacter canis sp. nov., a new species from dogs: An integrated study of phenotype and genotype. J Gen Microbiol, 1993; 139(10):2495–2504; doi: 10.1099/00221287-139-10-2495
53.
SwennesAG, TurkML, TrowelEM, et al.Helicobacter canis colonization in sheep: A Zoonotic link. Helicobacter, 2014; 19(1):65–68; doi: 10.1111/hel.12097
54.
TaillieuE, ChiersK, AmorimI, et al.Gastric Helicobacter species associated with dogs, cats and pigs: Significance for public and animal health. Vet Res, 2022; 53(1):42; doi: 10.1186/s13567-022-01059-4
55.
TankovicJ, SmatiM, LamarqueD, et al.First detection of Helicobacter canis in chronic duodenal ulcerations from a patient with Crohn’s disease. Inflamm Bowel Dis, 2011; 17(8):1830–1831; doi: 10.1002/ibd.21610
56.
TeixeiraS, FilipeD, CerqueiraM, et al.Helicobacter spp. in the stomach of cats: Successful colonization and absence of relevant histopathological alterations reveals high adaptation to the host gastric niche. Vet Sci, 2022; 9(5):228; doi: 10.3390/vetsci9050228
57.
Van den BulckK, DecostereA, BaeleM, et al.Identification of non-Helicobacter pylori spiral organisms in gastric samples from humans, dogs, and cats. J Clin Microbiol, 2005; 43(5):2256–2260; doi: 10.1128/JCM.43.5.2256-2260.2005
58.
Van der VusseML, van SonWJ, OttA, et al.Helicobacter canis bacteremia in a renal transplant patient. Transpl Infect Dis, 2014; 16(1):125–129; doi: 10.1111/tid.12174
59.
WroblewskiLE, PeekRMJr, WilsonKT. Helicobacter pylori and gastric cancer: Factors that modulate disease risk. Clin Microbiol Rev, 2010; 23(4):713–739; doi: 10.1128/CMR.00011-10
60.
WüppenhorstN, von LoewenichF, HobmaierB, et al.Culture of a gastric non-Helicobacter pylori Helicobacter from the stomach of a 14-year-old girl. Helicobacter, 2013; 18(1):1–5; doi: 10.1111/j.1523-5378.2012.00990.x
