Abstract
Helicobacter spp. have been detected in different parts of gastrointestinal tract of dogs including the oral cavity, stomach, intestines and recently, hepatobilliary system. However, the transmission pathways of Helicobacter spp. have not been yet fully elucidated. Research in the last decade has proposed that oral–oral and fecal–oral transmissions, among others, may be a plausible route of this gastric infection. This study was carried out primarily to determine the existence of pylori and non-pylori Helicobacter spp. in the oral secretions and dental plaque of stray dogs of Iran as one of the possible routes of humans and animal infection and, secondly, to evaluate the accordance between oral and gastric colonization of Helicobacter spp. in these dogs. Forty-eight adult stray dogs were studied by PCR using 16S rRNA, Helicobacter felis, Helicobacter heilmannii, and Helicobacter pylori specific primers. Positive samples for 16S rRNA specific primers that did not meet the specified species of Helicobacter genus were randomly subjected to sequencing. Helicobacter spp. DNA was found in the oral and gastric specimens of 100 % of the stray dogs. There was not, however, any agreement between Helicobacter colonization at these two locations, at neither genus nor species level. Our study confirmed that the oral cavity of stray dogs routinely exposed to transient forms of bacteria and may temporarily harbor Helicobacter spp and Wolinella spp. Therefore, oral cavity as a source of Helicobacter spp. may act as a reservoir for transmission. However, it may not necessarily reflect the colonization status of the gastric mucosa.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Axon AT (1995) Review article: is Helicobacter pylori transmitted by the gastro-oral route? Aliment Pharmacol Ther 9:585–8
Brown LM (2000) Helicobacter pylori: epidemiology and routes of transmission. Epidemiol Rev 22:283–97
Craven M, Recordati C, Gualdi V, Pengo G, Luini M, Scanziani E, Simpson KW (2011) Evaluation of the Helicobacteraceae in the oral cavity of dogs. Am J Vet Res 72:1476–1481
Eaton KA, Radin MJ, Kramer L, Wack R, Sherding R, Krakowka S, Fox JG, Morgan DR (1993) Epizootic gastritis associated with gastric spiral bacilli in cheetahs (Acinonyx jubatus). Vet Pathol 30:55–63
Eaton KA, Dewhirst FE, Paster BJ, Tzellas N, Coleman BE, Paola J, Sherding R (1996) Prevalence and varieties of Helicobacter species in dogs from random sources and pet dogs: animal and public health implications. J Clin Microbiol 34:3165–70
Flejou JF, Diomande I, Molas G, Goldfain D, Rotenberg A, Florent M, Potet F (1990) Human chronic gastritis associated with non-Helicobacter pylori spiral organisms (Gastrospirillum hominis). Four cases and review of the literature. Gastroenterol Clin Biol 14:806–10
Germani Y, Dauga C, Duval P, Huerre M, Levy M, Pialoux G, Sansonetti P, Grimont PA (1997) 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 148:315–26
Happonen I, Linden J, Saari S, Karjalainen M, Hänninen ML, Jalava K, Westermarck E (1998) Detection and effects of helicobacters in healthy dogs and dogs with signs of gastritis. J Am Vet Med Assoc 213:1767–74
Harbour S, Sutton P (2008) Immunogenicity and pathogenicity of Helicobacter infections of veterinary animals. Vet Immunol Immunopathol 122:191–203
Heilmann KL, Borchard F (1991) Gastritis due to spiral shaped bacteria other than Helicobacter pylori: clinical, histological, and ultrastructural findings. Gut 32:137–140
Henry GA, Long PH, Burns JL, Charbonneau DL (1987) Gastric spirillosis in beagles. Am J Vet Res 48:831–836
Jalava K, On SL, Vandamme PA, Happonen I, Sukura A, Hänninen ML (1998) Isolation and identification of Helicobacter spp. from canine and feline gastric mucosa. Appl Environ Microbiol 64:3998–4006
Kauser F, Hussain MA, Ahmed I, Srinivas S, Devi SM, Majeed AA, Rao KR, Khan AA, Sechi LA, Ahmed N (2005) Comparative genomics of Helicobacter pylori isolates recovered from ulcer disease patients in England. BMC Microbiol 5:32
Lavelle JP, Landas S, Mitros FA, Conklin JL (1994) Acute gastritis associated with spiral organisms from cats. Dig Dis Sci 39:744–50
Lee A, Hazell SL, O’Rourke J, Kouprach S (1988) Isolation of a spiral-shaped bacterium from the cat stomach. Infect Immun 56:2843–50
McNulty CA, Dent JC, Curry A, Uff JS, Ford GA, Gear MW, Wilkinson SP (1989) New spiral bacterium in gastric mucosa. J Clin Pathol 42:585–91
Meining A, Kroher G, Stolte M (1998) Animal reservoirs in the transmission of Helicobacter heilmannii. Results of a questionnaire-based study. Scand J Gastroenterol 33:795–8
Morales-Espinosa R, Fernandez-Presas A, Gonzalez-Valencia G, Flores-Hernandez S, Delgado-Sapien G, Mendez-Sanchez JL, Sanchez-Quezada E, Muñoz-Pérez L, Leon-Aguilar R, Hernandez-Guerrero J, Cravioto A (2009) Helicobacter pylori in the oral cavity is associated with gastroesophageal disease. Oral Microbiol Immunol 24:464–8
Morgner A, Lehn N, Andersen LP, Thiede C, Bennedsen M, Trebesius K, Neubauer B, Neubauer A, Stolte M, Bayerdörffer E (2000) Helicobacter heilmannii-associated primary gastric low-grade MALT lymphoma: complete remission after curing the infection. Gastroenterology 118:821–8
Morris A, Ali MR, Thomsen L, Hollis B (1990) Tightly spiral shaped bacteria in the human stomach: another cause of active chronic gastritis? Gut 31:139–43
Neiger R, Dieterich C, Burnens A, Waldvogel A, Corthesy-Theulaz I, Halter F, Lauterburg B, Schmassmann A (1998) Detection and prevalence of Helicobacter infection in pet cats. J Clin Microbiol 36:634–7
Queiroz DM, Rocha GA, Mendes EN, Lage AP, Carvalho AC, Barbosa AJ (1990) A spiral microorganism in the stomach of pigs. Vet Microbiol 24:199–204
Rasmussen LT, Labio RW, Gatti LL, Silva LC, Queiroz VF, Smith A, Payão SL (2010) Helicobacter pylori detection in gastric biopsies, saliva and dental plaque of Brazilian dyspeptic patients. Mem Inst Oswaldo Cruz 105:326–30
Recordati C, Gualdi V, Tosi S, Facchini RV, Pengo G, Luini M, Simpson KW, Scanziani E (2007) Detection of Helicobacter spp. DNA in the oral cavity of dogs. Vet Microbiol 119:346–51
Regimbeau C, Karsenti D, Durand V, D'Alteroche L, Copie-Bergman C, Metman EH, Machet MC (1998) Low-grade gastric MALT lymphoma and Helicobacter heilmannii (Gastrospirillum hominis. Gastroenterol Clin Biol 22:720–3
Shojaee Tabrizi A, Jamshidi S, Oghalaei A, Zahraei Salehi T, Bayati Eshkaftaki A, Mohammadi M (2010) Identification of Helicobacter spp. in oral secretions vs. gastric mucosa of stray cats. Vet Microbiol 140:142–6
Solnick JV, Schauer DB (2001) Emergence of diverse Helicobacter species in the pathogenesis of gastric and enterohepatic diseases. Clin Microbiol Rev 14:59–97
Stolte M, Wellens E, Bethke B, Ritter M, Eidt H (1994) Helicobacter heilmannii (formerly Gastrospirillum hominis) gastritis: an infection transmitted by animals? Scand J Gastroenterol 29:1061–4
Strauss-Ayali D, Simpson KW, Schein AH, McDonough PL, Jacobson RH, Valentine BA, Peacock J (1999) Serological discrimination of dogs infected with gastric Helicobacter spp. and uninfected dogs. J Clin Microbiol 37:1280–7
Trebesius K, Adler K, Vieth M, Stolte M, Haas R (2001) 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 39:1510–6
Ulrich RM, Bohr PA, Zagoura A, Glasbrenner B, Thomas Wex T, Malfertheiner P (2002) A group-specific PCR assay for the detection of Helicobacteraceae in human gut. Helicobacter 7:378–383
Van den Bulck K, Decostere A, Baele M, Driessen A, Debongnie JC, Burette A, Stolte M, Ducatelle R, Haesebrouck F (2005) Identification of non-Helicobacter pylori spiral organisms in gastric samples from human, dogs, and cats. J Clin Microbiol 43:2256–60
Yali Z, Yamada N, Wen M, Matsuhisa T, Miki M (1998) Gastrospirillum hominis and Helicobacter pylori infection in Thai individuals: comparison of histopathological changes of gastric mucosa. Pathol Int 48:507–11
Yang H, Goliger JA, Song M, Zhou D (1998) High prevalence of Helicobacter heilmannii infection in China. Dig Dis Sci 43:1493
Acknowledgments
The first author would like to thank Dr. Alavi Tabatabaee for his help in the collection of samples. The authors wish to thank the Foodborne Diarrheal Diseases, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran, and the Faculty of Specialized Veterinary Sciences, Science and Research Branch, Islamic Azad University (IAU), Tehran, Iran, for their approval and financial support for conducting such an extensive investigation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Arfaee, F., Jamshidi, S., Azimirad, M. et al. PCR-based diagnosis of Helicobacter species in the gastric and oral samples of stray dogs. Comp Clin Pathol 23, 135–139 (2014). https://doi.org/10.1007/s00580-012-1584-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00580-012-1584-5