Skip to main content
PMC home page
Journal of Medical Microbiology logoLink to Journal of Medical Microbiology
. 2015 May;64(Pt 5):575–581. doi: 10.1099/jmm.0.000051

Co-infection of the Siberian hamster (Phodopus sungorus) with a novel Helicobacter sp. and Campylobacter sp.

Claude M Nagamine 1,†,✉, Zeli Shen 2,†, Richard H Luong 1, Gabriel P McKeon 1,‡, Norman F Ruby 3, James G Fox 2
PMCID: PMC4635475  PMID: 25752854

Abstract

We report the isolation of a novel helicobacter isolated from the caecum of the Siberian hamster (Phodopus sungorus). Sequence analysis showed 97 % sequence similarity to Helicobacter ganmani. In addition, we report the co-infection of these Siberian hamsters with a Campylobacter sp. and a second Helicobacter sp. with 99 % sequence similarity to Helicobacter sp. flexispira taxon 8 (Helicobacter bilis), a species isolated previously from patients with bacteraemia. Gross necropsy and histopathology did not reveal any overt pathological lesions of the liver and gastrointestinal tract that could be attributed to the Helicobacter or Campylobacter spp. infections. This is the first helicobacter to be identified in the Siberian hamster and the first report of co-infection of Helicobacter spp. and Campylobacter sp. in asymptomatic Siberian hamsters.

Introduction

The genus Helicobacter comprises Gram-negative, anaerobic or microaerophilic, fastidious, flagellated, spiral bacteria that inhabit the gastrointestinal and hepatobiliary tracts of many mammals and birds (Fox et al., 2006; Whary & Fox, 2004). Many Helicobacter spp. have been associated with diseases in humans (De Groote et al., 2000), pets and research animals (Whary & Fox, 2004). In humans, Helicobacter pylori infects 50 % of the world’s population, causing peptic ulcers in 10–15 % and gastric adenocarcinomas in 1–2 % of infected individuals (Fox & Wang, 2007). To date, five Helicobacter spp. have been isolated from laboratory hamsters, all from the Syrian hamster (Mesocricetus auratus). Helicobacter aurati was isolated from the caeca and inflamed stomachs of hamsters with gastritis (Patterson et al., 2000a) and Helicobacter cholecystus was isolated from the gallbladders of hamsters with cholangiofibrosis and centrilobular pancreatitis (Franklin et al., 1996). Helicobacter cinaedi (Gebhart et al., 1989) and Helicobacter mesocricetorum (Simmons et al., 2000) were isolated from the faecal pellets of normal hamsters. H. cinaedi has also been isolated from human patients, raising the possibility of zoonotic transmission to susceptible humans (Kiehlbauch et al., 1994). More recently, a novel Helicobacter sp., most closely related to Flexispira taxon 8 within the Helicobacter bilis/H. cinaedi group, was isolated from the livers and caeca of aged (18–24 months) hamsters with chronic hepatitis, hepatic dysplasia and fibrosis, and/or biliary hyperplasia (Fox et al., 2009). These reports show that helicobacters, under certain conditions, can cause lesions in hamsters, which may serve as a model for certain human conditions, such as chronic hepatitis, gastritis, cholangiofibrosis and centrilobular pancreatitis. There have been no reports of the isolation of helicobacters from other hamster species.

Similar to Helicobacter spp., Campylobacter spp. are Gram-negative, anaerobic or microaerophilic, fastidious, spiral-, curved- or rod-shaped, flagellated bacteria that inhabit the gastrointestinal tract of mammals and birds (Man, 2011). Campylobacteriosis is one of the leading causes of foodborne bacterial gastroenteritis in the USA (Scallan et al., 2011) and is a potential zoonotic pathogen from pets and laboratory animals (Beisele et al., 2011; Fox, 1982; Kaur et al., 2011; Rossi et al., 2008; Shen et al., 2001). Indeed, the Syrian hamster can serve as a reservoir for Campylobacter jejuni (Fox et al., 1981), and Campylobacter spp. DNA, along with H. aurati, has been identified in the stomachs of Syrian hamsters with gastritis (Patterson et al., 2000b), highlighting the zoonotic risk. We found no reports on whether Camyplobacter spp. exist in other hamster species.

The Siberian hamster (Phodopus sungorus), also called the Russian or Djungarian hamster, is a small (head–body length 7.0–9.0 cm, weight 19–45 g) hamster whose discontinuous distribution in the wild encompasses the steppes of south-west Siberia and north-eastern Kazakhstan and the steppes in the Minusinsk depression of the southern Krasnoyarsk Krai region of Russia (Ross, 1998). P. sungorus and its sibling species, Phodopus campbelli, have the most compressed reproductive cycles of the Eutheria, with females being able to wean a litter every 18 days (Newkirk et al., 1997). The Siberian hamster has a mean life span of 2.0–2.5 years (Ross, 1998) and is used in a variety of chronobiological studies (Butler & Zucker, 2009; Grone et al., 2011; Ruby et al., 2008; Schöttner et al., 2011; Tups et al., 2012) and in research on the evolution of parental behaviour (Ma et al., 2005; Stulberg & Wynne-Edwards, 1998; Wynne-Edwards & Lisk, 1989), parasite susceptibility (Ike et al., 2005; Uchida et al., 2003) and cancer (Kondo et al., 2008, 2009). As the popularity of the Siberian hamster increased as a household pet, there has been a corresponding increase in reports on Siberian hamster-associated respiratory allergic disease (Bertó et al., 2002) and bite-induced anaphylaxis in humans (Lim et al., 2004; Niitsuma et al., 2003; Torres et al., 2012).

Given previous reports of the isolation of Campylobacter and Helicobacter spp. in Syrian hamsters, we hypothesized that Helicobacter spp. and/or Campylobacter spp. are present in Siberian hamsters. Here, we report the isolation of a novel Helicobacter sp. from the caeca of aged Siberian hamsters. This is the first Helicobacter sp. identified in the Siberian hamster. In addition, we report the co-infection of Siberian hamsters with a novel Campylobacter sp.

Methods

Animals and husbandry.

Founders for the Siberian hamster breeding colony were obtained from Dr I. Zucker (University of California, Berkeley, CA, USA) and maintained in an Association for the Assessment and Accreditation for Laboratory Animal Care, International-accredited facility. The animals were housed in solid-bottomed, static cages (9×7×6 in) with hardwood bedding (Sani-Chips; P. J. Murphy), maintained on a long-day photoperiod (16 h light : 8 h dark) at an ambient temperature of 22 °C, and were provided a commercial rodent diet (LabDiet 5015; Purina) and tap water ad libitum. The colony was monitored for pathogens transmissible to mice by the exposure of 5-week-old Crl : CD1 (ICR) female mouse sentinels to dirty bedding from the colony. Health reports from the vendor (Charles River Laboratories) indicated that the Crl : CD1 (ICR) colony was negative for Helicobacter spp. After exposure to hamster dirty bedding, the mouse sentinels were found to be negative for mouse hepatitis virus, Sendai virus, mouse parvovirus, minute virus of mice, ectromelia virus, lymphocytic choriomeningitis virus, mouse rotavirus, Theiler’s murine encephalomyelitis virus, mouse adenoviruses 1 and 2, and ecto- and endoparasites. In the non-barrier facility where the Siberian hamsters were housed, screening for helicobacter and campylobacter is not performed routinely on the mouse sentinels. Follicular mites, presumably Demodex sp., were identified in the haired skin of asymptomatic hamsters from this colony (McKeon et al., 2011). The research was approved by the Stanford University Institutional Animal Care and Use Committee.

Gross necropsy and histopathology.

Eighteen aged (17–27 month) Siberian hamsters (12 female, six male) were euthanized humanely by carbon dioxide asphyxiation and processed for macro- and microscopic pathological analyses (McKeon et al., 2011). All of the hamsters were retired breeders and were clinically healthy at the time of euthanasia. All major soft and hard tissues and organs were fixed in 10 % neutral buffered formalin for 48–72 h, trimmed and then embedded in paraffin following routine procedures. Blocks were sectioned at 4–5 µm and representative sections of each tissue were processed for haematoxylin and eosin (H&E) staining. Select slides were silver stained using the Warthin–Starry method to identify argyrophilic bacteria. For the liver, all lobes except the caudate lobe were assessed using both H&E and Warthin–Starry staining. All slides were evaluated by one of the authors who is a board-certified veterinary pathologist (R. H. L).

Samples and bacterial isolation.

Of the 18 Siberian hamsters, caecal samples were obtained from five females and three males (17–20 months). Each caecum was divided into three samples: one was used for PCR analysis, a second sample was stored in sterile freeze medium (20 % glycerol in brain–heart infusion broth) at −80 °C and used for microbiological culture, and the third sample was fixed in 10 % neutral buffered formalin for histology. Faecal samples from a second group of 12 live hamsters were collected, placed into freeze medium and stored at −80 °C.

Caecal and faecal samples in freeze medium were homogenized and 100 µl aliquots of each slurry were placed on cefoperazone, vancomycin and amphotericin B (CVA) plates and passed through a 0.45 µm syringe filter onto blood agar plates (trypticase soy agar plate with 5 % sheep blood; Remel Laboratories). The CVA and blood agar plates were incubated at 37 °C under micro-aerobic conditions in a vented jar containing N2, H2 and CO2 (80 : 10 : 10) and were checked every 2–3 days for 3 weeks. Suspected bacterial growth was identified as Helicobacter or Campylobacter sp. on the basis of colony morphology, phase microscopy and Gram staining (Shen et al., 2001).

Helicobacter and Campylobacter spp. PCR amplification, sequencing and sequence analysis.

A portion of the caecal samples was sent to a commercial diagnostic laboratory for Helicobacter genus-specific and H. bilis- and H. hepaticus-specific PCR.

DNA samples were extracted from Helicobacter and Campylobacter spp. culture isolates using a High Pure PCR Template Preparation kit (Roche Molecular Biochemicals) and from Siberian hamster faecal samples using a QIAamp DNA Stool Mini kit (Qiagen). DNA samples were amplified by PCR using Helicobacter genus-specific and Campylobacter-specific primers as described previously (Fox et al., 2009; Shen et al., 2001, 2005). The Helicobacter genus-specific primers (C05 :  5′-ACTTCACCCCAGTCGCTG-3′, and C97 :  5′-GCTATGACGGGTATCC-3′) amplified a 1.2 kb amplicon from the 16S rRNA gene (Fox et al., 1998). The Campylobacter-specific primers (C98: 5′-GATTTTACCCCTACACCA-3′, and C99: 5′-GCGTGGAGGATGACACCT-3′) amplified a 300 bp PCR product from the 16S rRNA gene. The full-length 16S rRNA sequences of 1.6 kb from three helicobacter isolates and four campylobacter isolates were amplified using primers F24 and F25 (Dewhirst et al., 2005). The 1.6 kb 16S rRNA amplicons and 1.2 kb amplicons from helicobacter-specific PCR were purified, directly sequenced and compared with published helicobacter and campylobacter 16S rRNA genes in GenBank using a blast search. Lasergene software (DNASTAR) was used to reconstruct the 16S rRNA gene phylogenetic trees.

Results

Gross necropsy and histopathology

Gross and histological examination of the stomachs, small intestines, large intestines (including caeca), livers and gallbladders failed to reveal any significant lesions that could be similar to pathologies associated with Helicobacter spp. colonization and/or infection in any of the Siberian hamsters in this study. This included absence of significant gastritis, adenocarcinomas of the glandular stomach, portal hepatitis, hepatic nodular dysplasia, cholangiohepatitis, cholangiofibrosis, pancreatitis or typhlocolitis (Fig. 1). Warthin–Starry staining also failed to reveal any observable spiral bacteria in the stomachs, caeca, liver and gallbladder in these Siberian hamsters. In addition, no pathology related to Campylobacter spp. infection was observed.

Fig. 1. Photomicrographs of liver (a) and caecum (b) from a study Siberian hamster. The liver displayed a normal hepatic lobular histology, with observable portal triads (p.t.) and central veins (c.v.), and minimal to no evidence of inflammation, fibrosis or neoplasia. Similarly, the caecum also displayed normal histology, with the mucosa containing normal intestinal glands of regular height, with minimal inflammation, fibrosis or neoplasia. Additionally, the remainder of the gastrointestinal tract (including non-glandular stomach, glandular stomach, small intestines and colon) and gallbladder were also histologically normal (not shown). Warthin–Starry-stained sections also failed to reveal the presence of any spiral bacteria in these sections. Overall, these photomicrographs are representative of the gastrointestinal tracts and hepatobiliary system in all the Siberian hamsters examined in this study, except for the presence of a squamous papilloma in the non-glandular stomach in one hamster, and hemangiosarcoma in the liver of another hamster. H&E stain. Bars, 100 µm (a); 50 µm (b).

Fig. 1.

Open in a new tab

Incidental findings in the stomachs, small intestines, large intestines (including caeca), livers and gallbladders included a squamous papilloma in the non-glandular stomach (n = 1) and hepatic hemangiosarcoma (n = 1), as reported previously (McKeon et al., 2011).

PCR and sequence analysis

PCR analysis of the eight caecal samples at the commercial diagnostic laboratory showed that all were positive using a Helicobacter genus-specific PCR assay but were negative for H. bilis- or H. hepaticus-specific PCR assays.

Culture of the same eight caecal samples was performed on both CVA and blood agar plates. All eight samples produced positive growth on the CVA plates, but only two samples produced positive growth on the blood agar plates (Table 1). PCR amplification of the cultures from all CVA plates and one blood agar plate were positive for Helicobacter spp.; the culture from one blood agar plate was positive for Campylobacter spp. Direct sequencing of all nine Helicobacter-positive reactions identified a previously undescribed Helicobacter sp. that had 97 % sequence similarity to H. ganmani (Fig. 2a, samples 10-5747, 10-5750 and 10-5753). Sequence analysis of the single Campylobacter-specific reaction showed a 99 % sequence similarity to a previous Campylobacter isolate, MIT 97-5311, originally isolated from a Syrian hamster (Fig. 2b).

Table 1. Sex and age of Siberian hamsters that provided the caecal samples, microbiology culture conditions and sequence analysis.

These same samples were positive in a Helicobacter genus-specific PCR assay but negative for H. hepaticus- and H. bilis-specific PCR assays at an independent diagnostic laboratory. All blood agar cultures were passed through a 0.45 µm filter. F, female; M, male.

Sex/age (months) MIT ID Plate type Growth Sequence similarity
F/17 10-5748 CVA + 97 % Helicobacter ganmani
Blood agar −
F/17 10-5750 CVA + 97 % Helicobacter ganmani
Blood agar −
M/18 10-5749 CVA + 97 % Helicobacter ganmani
Blood agar −
M/18 10-5751 CVA + 97 % Helicobacter ganmani
Blood agar −
F/19 10-5747 CVA + 97 % Helicobacter ganmani
Blood agar −
F/20 10-5752 CVA + 97 % Helicobacter ganmani
Blood agar + 97 % Helicobacter ganmani
F/20 10-5753 CVA + 97 % Helicobacter ganmani
Blood agar −
M/20 10-5754 CVA plate + 97 % Helicobacter ganmani
Blood + 99 % Campylobacter MIT 97-5311
Open in a new tab

Fig. 2. Phylogenetic trees of 16s rRNA gene sequences showing the relationship of the helicobacter (Fig. 2a) and campylobacter (Fig. 2b) isolates in the present report (arrows) to previously sequenced isolates. GenBank accession numbers for the sequences used are shown. Bars, nucleotide substitutions per site.

Fig. 2.

Open in a new tab

PCR amplification of the 12 faecal samples using Helicobacter genus-specific primers showed five (41.7 %) to be helicobacter positive (Table 2). All helicobacter-positive faecal samples were also campylobacter positive (Table 2). An additional three faecal samples (25 %) were campylobacter positive only. Overall, eight faecal samples (66.7 %) were campylobacter positive. The 1.6 kb 16S rRNA sequence analysis of four campylobacter isolates showed 99 % sequence similarity to MIT 97-5311 (Fig. 2b, samples 10-7217 and 10-7222). Sequences of three 1.2 kb helicobacter-specific PCR products showed 99 % sequence similarity to Helicobacter sp. flexispira taxon 8 ( = H. bilis) (Table 2, Fig. 2a, sample 10-7218), a helicobacter isolated previously from bacteraemic human patients (Iten et al., 2001; Sorlin et al., 1999; Tee et al., 1998). Both strains had a 184 bp intervening sequence region. This strain also had over 99 % identity with an H. bilis isolate previously isolated from Syrian hamsters (Fox et al., 2009), although the intervening sequence was not present in Syrian hamster H. bilis strains. Table 3 shows a summary of the helicobacter and campylobacter samples.

Table 2. Helicobacter and Campylobacter PCR results of Siberian hamster faecal samples and sequence similarity of the amplicons.

MIT ID Helicobacter PCR Sequence similarity Campylobacter PCR Sequence similarity
10-7214 + + 99 % MIT97-5311
10-7215 + + 99 % MIT97-5311
10-7216 − −
10-7217 − + 99 % MIT97-5311
10-7218 + 99 % Helicobacter sp. flexispira and 99 % H.bilis +
10-7219 + 99 % Helicobacter sp. flexispira and 99 % H.bilis +
10-7220 − −
10-7221 − −
10-7222 − + 99 % MIT97-5311
10-7223 − −
10-7224 − +
10-7225 + 99 % Helicobacter sp. flexispira and 99 % H.bilis +
Open in a new tab

Table 3. Summary of Helicobacter and Campylobacter results for Siberian hamster caecal and faecal samples.

Species Test Caecum Faeces
Helicobacter Positive rate 8/8 5/12
16s rRNA sequences Novel Helicobacter H. sp. flexispira taxon 8 or H. bilis
Campylobacter Positive rate 1/8 8/12
16s rRNA sequences Campylobacter (MIT 97-5311) Campylobacter (MIT 97-5311)
Open in a new tab

Discussion

The Siberian hamster is a laboratory research animal and a common household pet. Knowledge of its microbiota allows laboratory animal medicine veterinarians to take the necessary precautions to avoid the transmission of potential pathogens to other laboratory animals and humans. Our data showed that the Siberian hamster colony sampled harboured at least two Helicobacter spp., a novel helicobacter with 97 % sequence similarity to H. ganmani (Fig. 2a, samples 10-5747, 10-5750 and 10-5753) and a helicobacter with 99 % sequence similarity to Helicobacter sp. flexispira taxon 8 ( = H. bilis) (Fig. 2a, sample 10-7218). In addition, this colony also harboured a novel campylobacter with 99 % sequence similarity to campylobacter isolate MIT 97-5311 (Fig. 2b, samples 10-7217 and 10-7222). It is unclear why the novel H. ganmani-like species was not amplified from faecal samples (Table 3). The fact that the caecal and faecal samples were obtained at different times may have contributed to this discrepancy. PCR of the caecal samples sent initially to the commercial diagnostic laboratory failed to identify H. bilis, whereas H. bilis was identified in the three faecal samples that were sequenced (Table 2). One explanation for this discrepancy is that, although mouse and Siberian hamster H. bilis share 99 % sequence similarity overall, mouse and Siberian hamster H. bilis sequences in the region where the PCR primer were designed are different. Consequently, mouse H. bilis primers may not amplify Siberian hamster H. bilis.

Molecular data suggest that bacterial 16S RNA gene sequence homologies of <97.5 % are unlikely to be from the same species (Stackebrandt & Goebel, 1994). Therefore, it is highly probable that the Helicobacter sp. isolated in the Siberian hamster represents a novel species. Additional studies are required to fully characterize this Helicobacter sp. (Dewhirst et al., 2000). Also of interest is the identification of hepatic hemangiosarcoma in an aged female Siberian hamster (McKeon et al., 2011). In B6C3F1 male mice with H. hepaticus-associated hepatitis, the incidence of both hepatocellular carcinoma and hemangiosarcoma was higher compared with control, uninfected mice (Hailey et al., 1998). However, given that we did not observe any evidence of helicobacter-induced lesions in the Siberian hamsters, whether there is a causative relationship between Helicobacter spp. infection and hemangiosarcoma in Siberian hamsters requires further studies.

The Campylobacter sp. identified had 99 % sequence similarity to a previous isolate, MIT 97-5311, that was isolated from the caecum of a Syrian hamster. Co-infection with Campylobacter spp. and Helicobacter marmotae was recently reported in wild-caught black-tailed prairie dogs (Cynomys ludovicianus) (Beisele et al., 2011). Unlike the prairie dogs, the present Siberian hamster colony has been maintained in the laboratory for several generations and the identification of Campylobacter sp. was unexpected. The authors are unaware of any reports on the prevalence of Campylobacter spp. infection among academic rodent colonies. This may be due to the low prevalence of Campylobacter spp. in research rodent colonies and/or the rarity of Campylobacter spp. diagnostic testing. Indeed, except for Syrian hamster colonies, most commercial and academic rodent colonies are not routinely screened for Campylobacter spp. (Livingston & Riley, 2003; Mähler et al., 2014; Pritchett-Corning et al., 2009; Yamamoto et al., 2001). Helicobacter sp. flexispira taxon 8 has been isolated from immunocompromised and immunocompetent patients with bacteraemia (Iten et al., 2001; Sorlin et al., 1999; Tee et al., 1998), raising the possibility that this Siberian hamster Helicobacter sp. may have zoonotic potential. Additional studies are needed to determine the pathogenic potential of the Siberian hamster Campylobacter and the Helicobacter spp. to other laboratory animals and/or humans.

Acknowledgements

This research was funded in part by Stanford University’s Department of Comparative Medicine and by NIH grants R01-OD011141 (J. G. F) and P30-ES002109 (J. G. F).

Abbreviations:

H&E

haematoxylin and eosin

References

  1. Beisele M., Shen Z., Parry N., Mobley M., Taylor N. S., Buckley E., Abedin M. Z., Dewhirst F. E., Fox J. G. ( 2011. ). Helicobacter marmotae and novel Helicobacter and Campylobacter species isolated from the livers and intestines of prairie dogs. J Med Microbiol 60, 1366–1374. 10.1099/jmm.0.032144-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bertó J. M., Peláez A., Fernández E., Lombardero M., Ferrer M. ( 2002. ). Siberian hamster: a new indoor source of allergic sensitization and respiratory disease. Allergy 57, 155–159. [PubMed] [Google Scholar]
  3. Butler M. P., Zucker I. ( 2009. ). Seasonal pelage changes are synchronized by simulated natural photoperiods in Siberian hamsters (Phodopus sungorus). J Exp Zool A Ecol Genet Physiol 311A, 475–482. 10.1002/jez.544 [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. De Groote D., Ducatelle R., Haesebrouck F. ( 2000. ). Helicobacters of possible zoonotic origin: a review. Acta Gastroenterol Belg 63, 380–387. [PubMed] [Google Scholar]
  5. Dewhirst F. E., Fox J. G., On S. L. ( 2000. ). Recommended minimal standards for describing new species of the genus Helicobacter . Int J Syst Evol Microbiol 50, 2231–2237. 10.1099/00207713-50-6-2231 [DOI] [PubMed] [Google Scholar]
  6. Dewhirst F. E., Shen Z., Scimeca M. S., Stokes L. N., Boumenna T., Chen T., Paster B. J., Fox J. G. ( 2005. ). Discordant 16S and 23S rRNA gene phylogenies for the genus Helicobacter: implications for phylogenetic inference and systematics. J Bacteriol 187, 6106–6118. 10.1128/JB.187.17.6106-6118.2005 [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fox J. G. ( 1982. ). Campylobacteriosis – a “new” disease in laboratory animals. Lab Anim Sci 32, 625–637. [PubMed] [Google Scholar]
  8. Fox J. G., Wang T. C. ( 2007. ). Inflammation, atrophy, and gastric cancer. J Clin Invest 117, 60–69. 10.1172/JCI30111 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fox J. G., Zanotti S., Jordan H. V. ( 1981. ). The hamster as a reservoir of Campylobacter fetus subspecies jejuni . J Infect Dis 143, 856. 10.1093/infdis/143.6.856 [DOI] [PubMed] [Google Scholar]
  10. Fox J. G., Li X., Yan L., Cahill R. J., Hurley R., Lewis R., Murphy J. C. ( 1996. ). Chronic proliferative hepatitis in A/JCr mice associated with persistent Helicobacter hepaticus infection: a model of helicobacter-induced carcinogenesis. Infect Immun 64, 1548–1558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fox J. G., Dewhirst F. E., Shen Z., Feng Y., Taylor N. S., Paster B. J., Ericson R. L., Lau C. N., Correa P., et al. ( 1998. ). Hepatic Helicobacter species identified in bile and gallbladder tissue from Chileans with chronic cholecystitis. Gastroenterology 114, 755–763. 10.1016/S0016-5085(98)70589-X [DOI] [PubMed] [Google Scholar]
  12. Fox J. G., Taylor N. S., Howe S., Tidd M., Xu S., Paster B. J., Dewhirst F. E. ( 2006. ). Helicobacter anseris sp. nov. and Helicobacter brantae sp. nov., isolated from feces of resident Canada geese in the greater Boston area. Appl Environ Microbiol 72, 4633–4637. 10.1128/AEM.02876-05 [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fox J. G., Shen Z., Muthupalani S., Rogers A. R., Kirchain S. M., Dewhirst F. E. ( 2009. ). Chronic hepatitis, hepatic dysplasia, fibrosis, and biliary hyperplasia in hamsters naturally infected with a novel Helicobacter classified in the H. bilis cluster. J Clin Microbiol 47, 3673–3681. 10.1128/JCM.00879-09 [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fox J. G., Ge Z., Whary M. T., Erdman S. E., Horwitz B. H. ( 2011. ). Helicobacter hepaticus infection in mice: models for understanding lower bowel inflammation and cancer. Mucosal Immunol 4, 22–30. 10.1038/mi.2010.61 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Franklin C. L., Beckwith C. S., Livingston R. S., Riley L. K., Gibson S. V., Besch-Williford C. L., Hook R. R., Jr ( 1996. ). Isolation of a novel Helicobacter species, Helicobacter cholecystus sp. nov., from the gallbladders of Syrian hamsters with cholangiofibrosis and centrilobular pancreatitis. J Clin Microbiol 34, 2952–2958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gebhart C. J., Fennell C. L., Murtaugh M. P., Stamm W. E. ( 1989. ). Campylobacter cinaedi is normal intestinal flora in hamsters. J Clin Microbiol 27, 1692–1694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Grone B. P., Chang D., Bourgin P., Cao V., Fernald R. D., Heller H. C., Ruby N. F. ( 2011. ). Acute light exposure suppresses circadian rhythms in clock gene expression. J Biol Rhythms 26, 78–81. 10.1177/0748730410388404 [DOI] [PubMed] [Google Scholar]
  18. Hailey J. R., Haseman J. K., Bucher J. R., Radovsky A. E., Malarkey D. E., Miller R. T., Nyska A., Maronpot R. R. ( 1998. ). Impact of Helicobacter hepaticus infection in B6C3F1 mice from twelve National Toxicology Program two-year carcinogenesis studies. Toxicol Pathol 26, 602–611. [DOI] [PubMed] [Google Scholar]
  19. Ike K., Komatsu T., Murakami T., Kato Y., Takahashi M., Uchida Y., Imai S. ( 2005. ). High susceptibility of Djungarian hamsters (Phodopus sungorus) to the infection with Babesia microti supported by hemodynamics. J Vet Med Sci 67, 515–520. 10.1292/jvms.67.515 [DOI] [PubMed] [Google Scholar]
  20. Iten A., Graf S., Egger M., Täuber M., Graf J. ( 2001. ). Helicobacter sp. flexispira bacteremia in an immunocompetent young adult. J Clin Microbiol 39, 1716–1720. 10.1128/JCM.39.5.1716-1720.2001 [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kaur T., Singh J., Huffman M. A., Petrzelková K. J., Taylor N. S., Xu S., Dewhirst F. E., Paster B. J., Debruyne L., et al. ( 2011. ). Campylobacter troglodytis sp. nov., isolated from feces of human-habituated wild chimpanzees (Pan troglodytes schweinfurthii) in Tanzania. Appl Environ Microbiol 77, 2366–2373. 10.1128/AEM.01840-09 [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kiehlbauch J. A., Tauxe R. V., Baker C. N., Wachsmuth I. K. ( 1994. ). Helicobacter cinaedi-associated bacteremia and cellulitis in immunocompromised patients. Ann Intern Med 121, 90–93. 10.7326/0003-4819-121-2-199407150-00002 [DOI] [PubMed] [Google Scholar]
  23. Kondo H., Onuma M., Shibuya H., Sato T. ( 2008. ). Spontaneous tumors in domestic hamsters. Vet Pathol 45, 674–680. 10.1354/vp.45-5-674 [DOI] [PubMed] [Google Scholar]
  24. Kondo H., Onuma M., Shibuya H., Sato T. ( 2009. ). Morphological and immunohistochemical studies of spontaneous mammary tumours in Siberian hamsters (Phodopus sungorus). J Comp Pathol 140, 127–131. 10.1016/j.jcpa.2008.09.012 [DOI] [PubMed] [Google Scholar]
  25. Lim D. L., Chan R. M., Wen H., Van Bever H. P., Chua K. Y. ( 2004. ). Anaphylaxis after hamster bites – identification of a novel allergen. Clin Exp Allergy 34, 1122–1123. 10.1111/j.1365-2222.2004.01992.x [DOI] [PubMed] [Google Scholar]
  26. Livingston R. S., Riley L. K. ( 2003. ). Diagnostic testing of mouse and rat colonies for infectious agents. Lab Anim (NY) 32, 44–51. 10.1038/laban0503-44 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ma E., Lau J., Grattan D. R., Lovejoy D. A., Wynne-Edwards K. E. ( 2005. ). Male and female prolactin receptor mRNA expression in the brain of a biparental and a uniparental hamster, Phodopus, before and after the birth of a litter. J Neuroendocrinol 17, 81–90. 10.1111/j.1365-2826.2005.01278.x [DOI] [PubMed] [Google Scholar]
  28. Mähler M., Berard M., Feinstein R., Gallagher A., Illgen-Wilcke B., Pritchett-Corning K., Raspa M., FELASA working group on revision of guidelines for health monitoring of rodents and rabbits ( 2014. ). FELASA recommendations for the health monitoring of mouse, rat, hamster, guinea pig and rabbit colonies in breeding and experimental units. Lab Anim 48, 178–192. 10.1177/0023677213516312 [DOI] [PubMed] [Google Scholar]
  29. Man S. M. ( 2011. ). The clinical importance of emerging Campylobacter species. Nat Rev Gastroenterol Hepatol 8, 669–685. 10.1038/nrgastro.2011.191 [DOI] [PubMed] [Google Scholar]
  30. McKeon G. P., Nagamine C. M., Ruby N. F., Luong R. H. ( 2011. ). Hematologic, serologic, and histologic profile of aged Siberian hamsters (Phodopus sungorus). J Am Assoc Lab Anim Sci 50, 308–316. [PMC free article] [PubMed] [Google Scholar]
  31. Newkirk K. D., Mcmillan H. J., Wynne-Edwards K. E. ( 1997. ). Length of delay to birth of a second litter in dwarf hamsters (Phodopus): evidence for post-implantation embryonic diapause. J Exp Zool 278, 106–114. [DOI] [PubMed] [Google Scholar]
  32. Niitsuma T., Tsuji A., Nukaga M., Izawa A., Okita M., Maruoka N., Morita S., Tsuyuguchi M. ( 2003. ). Two cases of anaphylaxis after dwarf hamster bites. Allergy 58, 1081. 10.1034/j.1398-9995.2003.00242.x [DOI] [PubMed] [Google Scholar]
  33. Patterson M. M., Schrenzel M. D., Feng Y., Xu S., Dewhirst F. E., Paster B. J., Thibodeau S. A., Versalovic J., Fox J. G. ( 2000. a). Helicobacter aurati sp. nov., a urease-positive Helicobacter species cultured from gastrointestinal tissues of Syrian hamsters. J Clin Microbiol 38, 3722–3728. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Patterson M. M., Schrenzel M. D., Feng Y., Fox J. G. ( 2000. b). Gastritis and intestinal metaplasia in Syrian hamsters infected with Helicobacter aurati and two other microaerobes. Vet Pathol 37, 589–596. 10.1354/vp.37-6-589 [DOI] [PubMed] [Google Scholar]
  35. Pritchett-Corning K. R., Cosentino J., Clifford C. B. ( 2009. ). Contemporary prevalence of infectious agents in laboratory mice and rats. Lab Anim 43, 165–173. 10.1258/la.2008.008009 [DOI] [PubMed] [Google Scholar]
  36. Ross, P. D. (1998). Phodopus sungorus America Society of Mammalogists. http://www.science.smith.edu/msi/msiaccounts.html.
  37. Rossi M., Hänninen M. L., Revez J., Hannula M., Zanoni R. G. ( 2008. ). Occurrence and species level diagnostics of Campylobacter spp., enteric Helicobacter spp. and Anaerobiospirillum spp. in healthy and diarrheic dogs and cats. Vet Microbiol 129, 304–314. 10.1016/j.vetmic.2007.11.014 [DOI] [PubMed] [Google Scholar]
  38. Ruby N. F., Hwang C. E., Wessells C., Fernandez F., Zhang P., Sapolsky R., Heller H. C. ( 2008. ). Hippocampal-dependent learning requires a functional circadian system. Proc Natl Acad Sci U S A 105, 15593–15598. 10.1073/pnas.0808259105 [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Scallan E., Hoekstra R. M., Angulo F. J., Tauxe R. V., Widdowson M. A., Roy S. L., Jones J. L., Griffin P. M. ( 2011. ). Foodborne illness acquired in the United States – major pathogens. Emerg Infect Dis 17, 7–15. 10.3201/eid1701.P11101 [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Schöttner K., Waterhouse J., Weinert D. ( 2011. ). The circadian body temperature rhythm of Djungarian Hamsters (Phodopus sungorus) revealing different circadian phenotypes. Physiol Behav 103, 352–358. 10.1016/j.physbeh.2011.02.019 [DOI] [PubMed] [Google Scholar]
  41. Shen Z., Feng Y., Dewhirst F. E., Fox J. G. ( 2001. ). Coinfection of enteric Helicobacter spp. and Campylobacter spp. in cats. J Clin Microbiol 39, 2166–2172. 10.1128/JCM.39.6.2166-2172.2001 [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Shen Z., Xu S., Dewhirst F. E., Paster B. J., Pena J. A., Modlin I. M., Kidd M., Fox J. G. ( 2005. ). A novel enterohepatic Helicobacter species ‘Helicobacter mastomyrinus’ isolated from the liver and intestine of rodents. Helicobacter 10, 59–70. 10.1111/j.1523-5378.2005.00292.x [DOI] [PubMed] [Google Scholar]
  43. Simmons J. H., Riley L. K., Besch-Williford C. L., Franklin C. L. ( 2000. ). Helicobacter mesocricetorum sp. nov., a novel Helicobacter isolated from the feces of Syrian hamsters. J Clin Microbiol 38, 1811–1817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Sorlin P., Vandamme P., Nortier J., Hoste B., Rossi C., Pavlof S., Struelens M. J. ( 1999. ). Recurrent “Flexispira rappini” bacteremia in an adult patient undergoing hemodialysis: case report. J Clin Microbiol 37, 1319–1323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Stackebrandt E., Goebel B. M. ( 1994. ). Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44, 846–849. 10.1099/00207713-44-4-846 [DOI] [Google Scholar]
  46. Stulberg S. E., Wynne-Edwards K. E. ( 1998. ). Maternal and pup contributions to different patterns of pup growth in Phodopus species. Physiol Behav 64, 715–722. 10.1016/S0031-9384(98)00133-4 [DOI] [PubMed] [Google Scholar]
  47. Tee W., Leder K., Karroum E., Dyall-Smith M. ( 1998. ). “Flexispira rappini” bacteremia in a child with pneumonia. J Clin Microbiol 36, 1679–1682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Torres J. A., Pastor-Vargas C., de las Heras M., Vivanco F., Cuesta J., Sastre J. ( 2012. ). An odorant-binding protein as a new allergen from Siberian hamster (Phodopus sungorus). Int Arch Allergy Immunol 157, 109–112. 10.1159/000324956 [DOI] [PubMed] [Google Scholar]
  49. Tups A., Stöhr S., Helwig M., Barrett P., Krol E., Schachtner J., Mercer J. G., Klingenspor M. ( 2012. ). Seasonal leptin resistance is associated with impaired signalling via JAK2–STAT3 but not ERK, possibly mediated by reduced hypothalamic GRB2 protein. J Comp Physiol B 182, 553–567. 10.1007/s00360-011-0637-4 [DOI] [PubMed] [Google Scholar]
  50. Uchida Y., Ike K., Kurotaki T., Takeshi M., Imai S. ( 2003. ). Susceptibility of Djungarian hamsters (Phodopus sungorus) to Neospora caninum infection. J Vet Med Sci 65, 401–403. 10.1292/jvms.65.401 [DOI] [PubMed] [Google Scholar]
  51. Whary M. T., Fox J. G. ( 2004. ). Natural and experimental Helicobacter infections. Comp Med 54, 128–158. [PubMed] [Google Scholar]
  52. Wynne-Edwards K. E., Lisk R. D. ( 1989. ). Differential effects of paternal presence on pup survival in two species of dwarf hamster (Phodopus sungorus and Phodopus campbelli). Physiol Behav 45, 465–469. 10.1016/0031-9384(89)90059-0 [DOI] [PubMed] [Google Scholar]
  53. Yamamoto H., Sato H., Yagami K., Arikawa J., Furuya M., Kurosawa T., Mannen K., Matsubayashi K., Nishimune Y., et al. ( 2001. ). Microbiological contamination in genetically modified animals and proposals for a microbiological test standard for national universities in Japan. Exp Anim 50, 397–407. 10.1538/expanim.50.397 [DOI] [PubMed] [Google Scholar]

Articles from Journal of Medical Microbiology are provided here courtesy of Microbiology Society

RESOURCES