Abstract
Bordetella hinzii isolated from the trachea and lungs of a laboratory mouse with a respiratory infection was identified based on its phenotypic and genetic traits. The mouse showed sneezing with a chattering sound but without nasal discharge, and histopathologic examination revealed rhinitis, tracheitis, and bronchopneumonia. The isolate was a gram-negative, oxidase- and catalase-positive, short rod-shaped organism that produced alkali from malonate. The results of biochemical identification, an alkali production test from malonate, and partial sequence analysis of the 16S rRNA gene (1523 bp) were consistent with those reported previously for B. hinzii. The isolate induced sneezing in ICR mice and sneezing and slight to severe dyspnea in NOD-SCID mice after experimental infection. Histopathologic examination revealed catarrhal rhinitis and bronchopneumonia in both strains of mice and interstitial pneumonia in NOD-SCID mice. In light of these findings, B. hinzii was deemed to be a novel causative agent of respiratory disease in mice. This report describes the first isolation of B. hinzii from a mouse and confirms the organism's pathogenicity in mice.
The genus Bordetella consists of 8 named species and 1 that is still awaiting formal description (Bordetella ansorpii sp. nov.).16 Some species in the genus are known pathogens of both humans and animals. B. pertussis and B. parapertussis are the causative agents of whooping cough in humans,19 and B. bronchiseptica is a respiratory pathogen in some animal species, including dogs,2,23 guinea pigs,24 pigs,14 rabbits,26 and laboratory rats.3 B. avium is a respiratory pathogen in poultry,4,12,13 whereas B. hinzii is a commensal organism of the respiratory tracts of poultry20,25 and an opportunistic pathogen in immunocompromised humans.7,9 Although some human clinical cases associated with B. hinzii infection have been associated with bacteremia,5,7,25 fatal septicemia,15 chronic cholangitis,1 and infectious pulmonary exacerbation in a patient with cystic fibrosis,8 no cases of overt clinical infection in nonhuman mammals have been reported previously. Although 1 strain of B. bronchiseptica from rabbits was reidentified as B. hinzii, thus leading to the first reported isolation of this species from a nonhuman mammal, a clinical description of B. hinzii infection in rabbits was not provided.20
We recently isolated B. hinzii from the trachea and lungs of a mouse with a respiratory infection. Here, we report this first case of B. hinzii infection in a mouse and present the results of experimental infection of ICR and NOD-SCID mice with the isolate to investigate its significance as a murine pathogen.
Materials and Methods
Index case.
A female C57 BL/6 mouse of unknown substrain and unknown age was delivered to the ICLAS Monitoring Center (Kawasaki, Japan) to investigate the cause of its sneezing with a chattering sound but without nasal discharge. The mouse was euthanized by exsanguination from the axillary artery and vein under isoflurane anesthesia and underwent routine serologic, bacteriologic, and parasitologic examinations as described previously11 and additional tests. Organisms under investigation included Bordetella bronchiseptica, Citrobacter rodentium, Corynebacterium kutscheri, Mycoplasma pulmonis, Pasteurella pneumotropica, Pseudomonas aeruginosa, Salmonella spp., and Staphylococcus aureus by culture; B. bronchiseptica, cilia-associated respiratory bacillus, Clostridium piliforme, Ectromelia virus, hantavirus, lymphocytic choriomeningitis virus, minute virus of mice, mouse adenovirus, mouse cytomegalovirus, mouse encephalomyelitis virus, mouse hepatitis virus, mouse parvovirus, Mycoplasma pulmonis, pneumonia virus of mice, rotavirus, reovirus type 3, and Sendai virus by serology; and intestinal protozoa, pinworms, and ectoparasites by microscopic observation. Pneumocystis carinii was examined by PCR assay of the left lobe of the lung as described previously.10 Respiratory bacteria were cultured by using tracheal swabs with 5% horse blood agar (Poa Media, Eiken Chemical, Tokyo, Japan) and were assessed by observation of the surface of agar plates after incubation for 48 h at 37 °C. In addition, the cut surface of the accessory lobe of the lung was streaked directly on 5% horse blood agar and incubated for 48 h at 37 °C.
Microbiologic investigations.
Biochemical tests of the isolate were performed (Api 20NE test kit, bioMérieux Japan, Tokyo, Japan) after Gram staining and oxidase and catalase tests. An alkali production test from malonate was performed by using malonate broth (Eiken Chemical) according to the manufacturer's instructions. Confirmation of growth of the isolate was confirmed using DHL agar (Poa Media, Eiken Chemical), which is commonly used for isolation of Bordetella bronchiseptica from contaminated samples from laboratory rodents and rabbits in Japan.17 In addition, a slide agglutination test with a rabbit antiserum to B. bronchiseptica strain BB1 (generated inhouse) was performed for the isolate. Briefly, 1 bacterial colony was mixed with 20 μl of rabbit antiserum on a slide glass and immediately was assessed by macroscopic observation.
Sequencing of the 16S rRNA gene and phylogenetic analysis.
Organisms grown on 5% horse blood agar were collected and washed with PBS by centrifugation (2300 × g for 5 min at 4 °C), and bacterial DNA was extracted (MagExtractor Genome DNA Kit, Toyobo, Osaka, Japan) according to the manufacturer's instructions. The 16S rRNA gene of the isolate was amplified by using universal primers A and H6 in 50-μl reaction mixtures containing 100 ng template DNA, 200 μM each dNTP (Takara Bio, Shiga, Japan), 10 μl 5× PCR buffer containing MgCl2 (Takara Bio), 0.3 μM each primer and 1.25 U PrimeSTAR HS DNA Polymerase (Takara Bio) on a GeneAmp PCR System 9700 thermal cycler (Applied Biosystems, Foster City, CA). The amplification program comprised 98 °C for 1 min, followed by 30 cycles of 98 °C for 10 s, 55 °C for 5 s, and 72 °C for 1.5 min, and a final extension step at 72 °C for 5 min. The amplified 16S rRNA gene of the isolate was cloned into a pUC118 cloning vector (Takara Bio) by using the Mighty Cloning Kit (Takara Bio). The nucleotide sequence of recombinant plasmid was determined by using the Taq DyeDeoxy Terminator Cycle Sequencing kit (Applied Biosystems) and an automated DNA sequencer (model 310, Applied Biosystems) with M13M4 and RV primers (Takara Bio) and sequence primers designed for this study: F1, 5′ GCA GGC GGT TCG GAA AGA AA 3′; F2, 5′ TCT AAT GAG ACT GCC GGT GA 3′; R1, 5′ GCA CCC TAC GTA TTA CCG CG 3′; and R2, 5′ ACA GCC ATG CAG CAC CTG TG-3′.
Sequences were assembled by using sequence analysis software (Genetyx version 7, Genetyx, Tokyo, Japan). This software also was used for multiple alignment and construction of a phylogenetic tree of the sequences. The sequence of the isolate was compared with the GenBank/EMBL/DDBJ data banks by using the NCBI FASTA program.22 The phylogenetic tree was constructed from a total of 1432 bp of the 16S rRNA gene sequence data of the isolate and deposited data of other Bordetella species in GenBank/EMBL/DDBJ data banks by using the neighbor-joining method.21 The branching pattern was tested with 1000 bootstrap replications.
Histopathologic examination for the index mouse.
Histopathologic examinations of the nasal cavity mucosa, trachea, right and accessory lobes of the lung, liver, spleen, and kidney were performed. These organs were fixed in 10% buffered formalin and stained with hematoxylin and eosin according to standard procedures. The nasal concha was decalcified with 5% formic acid prior to staining.
Experimental study.
The protocol for the animal experiments was approved by the institutional animal care and use committee according to the Regulations for Animal Experimentation of the Central Institute for Experimental Animals. Sixteen 4-wk-old SPF female Jcl:ICR (ICR) mice and sixteen 5-wk-old SPF female NOD/ShiJic-scidJcl (NOD-SCID) mice were obtained from a commercial supplier (CLEA Japan, Tokyo, Japan). Prior to the study, 2 mice of each strain were euthanized by exsanguination from the axillary artery and vein under isoflurane anesthesia and were examined for the following organisms, which were not included among those evaluated by the commercial supplier: mouse parvovirus, B. bronchiseptica, B. hinzii, S. aureus, and Pn. carinii for ICR mice and mouse parvovirus, B. bronchiseptica, and B. hinzii for NOD-SCID mice. The animals were housed in sterilized polycarbonate cages and kept in a microisolation rack system (FRP BIO2000, CLEA Japan) that consist of 16 individually ventilated boxes with glass fiber filters (FG50, American Air Filter, Louisville, KY) and an exhaust unit with a HEPA filter. The boxes accommodated each cage as an isolated environment. This microisolation rack system was used exclusively for this study throughout the experimental period. Sterilized commercial food pellets (CA1, CLEA Japan) and autoclaved tap water were provided ad libitum. Each cage was changed once weekly. The animals were maintained at room temperature of 23 to 25 °C and relative humidity of 50% to 60% under a 12:12-h light:dark cycle.
Ten mice of each strain were divided into 2 experimental groups inoculated with either a high or low dose of the bacterial suspension (5 × 107 CFU/ml or 5 × 103 CFU/ml, respectively). Four mice of each strain served as negative controls. The mice in the experimental groups were inoculated intranasally with 25 μl of each bacterial stock. The bacterial cells for the inocula were cultured on blood agar for 48 h at 37 °C, collected with sterilized swabs, and suspended in sterile PBS to the appropriate concentration. The inocula were confirmed as pure cultures by back-titration culture on horse blood agar. Control animals were inoculated with 25 μl sterile PBS only. All mice were euthanized as described earlier and examined on postinoculation day 28. The nasal concha, lungs and cecum of all mice underwent histopathologic examination after hematoxylin and eosin staining. Samples from nasal and tracheal swabs, the cut surface of the caudal lobe of the right lung, and 100 μl blood drawn from the heart were inoculated onto 5% horse blood agar for isolation of bacteria; cecal samples were grown on DHL agar. Recovered bacterial colonies were assessed by using Gram staining, oxidase and catalase tests, biochemical tests, and malonate broth and were confirmed as isolate 3224 by compliance with reported biochemical characteristics of B. hinzii.8,15 Mice that died during the incubation period did not undergo histopathologic or bacteriologic examinations because of extensive postmortem changes, such as autolysis.
Health status of animals in experimental study.
Vendor and inhouse monitoring reports indicated that the mice were free of bacterial, viral, and parasitic pathogens, as follows. On the basis of serologic test results, mice were free of cilia-associated respiratory bacillus, Cl. piliforme, Ectromelia virus, hantavirus, lymphocytic choriomeningitis virus, minute virus of mice, mouse adenovirus, mouse cytomegalovirus, mouse encephalomyelitis virus, mouse hepatitis virus, M. pulmonis, pneumonia virus of mice, rotavirus, reovirus type 3, and Sendai virus. Mice were free of B. bronchiseptica, B. hinzii, Ci. rodentium, Co. kutscheri, M. pulmonis, Pa. pneumotropica, Ps. aeruginosa, Salmonella spp., S. aureus and dermatophytes were not detected by culture methods. Parasite screening indicated that the animals were free of ectoparasites, intestinal protozoa, and pinworms. Pn. carinii, mouse parvovirus, Helicobacter hepaticus and H. bilis were not detected by PCR assay.
Slide agglutination test of serum from experimentally infected ICR mice.
To investigate crossreactivity between B. hinzii and B. bronchiseptica in serologic assays, serum samples from 10 experimentally infected ICR mice were obtained on postinoculation day 28 and were tested against B. bronchiseptica strain BB1 in slide agglutination tests. Briefly, 20 µl of each serum sample was mixed with 1 colony of B. bronchiseptica on a slide glass and immediately assessed by macroscopic observation.
Nucleotide sequence accession number.
The sequence data of the isolate have been deposited in the GenBank/EMBL/DDBJ data banks under accession no. AB371725.
Results
The mouse in the index case.
The index mouse arrived at our center after approximately 2 h transport by car. No emaciation or abnormal behavior was observed. Consolidation in the accessory lobe of the lung was found at necropsy. No gross lesions were apparent in other organs. Histopathologic examination revealed rhinitis, tracheitis, and bronchopneumonia. Rhinitis (Figure 1 A) and tracheitis were characterized by mild infiltration of inflammatory cells (mainly neutrophils) in the submucosa, slight epithelial necrosis, and mild mucus secretion. Bronchopneumonia was characterized by hyperplasia of peribronchial lymph nodes and infiltration of inflammatory cells, mainly neutrophils, in the peribronchial interstitium (Figure 2 A, B). Bronchopneumonia also was present in the other lobes of the lung but to a lesser degree than in the accessory lobe. All microbiologic monitoring items tested were negative for the mouse.
Figure 1.
Histopathology of nasal cavities of the mouse in the index case and experimentally infected mice. (A) The index case. (B) Experimentally infected ICR mouse in the high-dose group on postinoculation day 28. (C) Experimentally infected NOD-SCID mouse in the high-dose group on postinoculation day 28. These histopathologic changes were characterized by mild infiltration of inflammatory cells (mainly neutrophils) in the submucosa, slight epithelial necrosis, and mild mucus secretion. Hematoxylin and eosin stain; scale bar, 50 μm.
Figure 2.
Histopathology of lungs of the mouse in the index case and experimentally infected mice. (A, B) The index case. (C, D) Experimentally infected ICR mouse in the high-dose group on postinoculation day 28. (E, F) Experimentally infected NOD-SCID mouse in the high-dose group on postinoculation day 28. Bronchopneumonia in the mouse in the index case (A, B) and ICR mice (C and D) was limited to the peribronchiolar region and characterized by hyperplasia of peribronchial lymph nodes. In contrast, bronchopneumonia in NOD-SCID mice (E, F) was spread to deep branches of bronchioles, including terminal and respiratory bronchioles. Pulmonary changes in NOD-SCID mice were characterized by hypertrophy of alveolar septa due to infiltration of neutrophils (interstitial pneumonia) and infiltration of macrophages into the alveolar lumen. The mice shown in this figure are the same as those in Figure 1. Hematoxylin and eosin stain; scale bar, 50 μm (A, C, and E) or 10 μm (B, D, and F).
Microbiologic investigation.
Round, convex, glistening, small (2 to 3 mm), grayish bacterial colonies were isolated in pure culture on 5% horse blood agar inoculated with tracheal swabs and lung samples after 48 h of incubation at 37 °C. Gram staining of this isolate (assigned number 3224 at our institution) revealed gram-negative short rod-shaped bacteria. Isolate 3224 produced catalase and oxidase. Biochemical identification revealed a profile consistent with Bordetella avium (percent identification, 96.6%). The isolate yielded a positive alkali production test from malonate. Together these findings were suggestive of B. hinzii.8,15 Isolate 3224 grew on DHL agar and was not agglutinated by a rabbit antiserum to B. bronchiseptica in a slide agglutination test.
Sequencing of the 16S rRNA gene and phylogenetic analysis.
Partial sequencing (1523 bp) of the 16S rRNA gene of isolate 3224 by using universal primers A and H and FASTA searches of the GenBank/EMBL/DDBJ data banks revealed the closest similarity (99.9%) with the sequence of B. hinzii LMG 13051T (accession number, AF177667). The sequence of our isolate differed from B. hinzii LMG 13051T at only 2 of 1523 nucleotides. In phylogenetic analysis, isolate 3224 formed a monophyletic cluster with B. hinzii LMG 13501T (Figure 3) with a high bootstrap value (98%). This cluster occupied a position intermediate between the clusters of 4 Bordetella species and B. avium; these results were consistent with the previously reported phylogenetic position of B. hinzii.15
Figure 3.
Maximum likelihood consensus dendrogram based on 1432 consecutive positions of the 16S rRNA of the isolate and other Bordetella species. Numbers at branching nodes are percentage of 1000 bootstrap replications. The scale bar represents 0.01 substitutions per nucleotide position. The GenBank accession numbers of the sequences used to construct the phylogenetic tree are: B. ansorpii, AY594190; B. avium, AF177666; B. bronchiseptica, U04948; B. parapertussis, U04949; B. pertussis, AF142326; B. petrii, AJ249861; B. hinzii, AF177667; B. holmesii, U04820; B. trematum; AJ277798; and Pseudomonas aeruginosa (used as the outgroup), Z76651.
Experimentally infected mice.
By postinoculation day 3, all infected NOD-SCID mice showed sneezing with a chattering sound and slight dyspnea, as did all infected ICR mice by postinoculation day 10. The symptoms lasted throughout the experimental period (28 d after inoculation) in all mice. The sneezing in ICR mice gradually became less frequent over time. Whereas none of the ICR mice died, 4 of the NOD-SCID mice died or were euthanized for humane reasons due to severe dyspnea. One NOD-SCID mouse in the high-dose group died on postinoculation day 10, and 1 in the low-dose group died on postinoculation day 21. Two NOD-SCID mice in the high-dose group were euthanized on postinoculation days 11 and 15 (1 on each day). The NOD-SCID mice that died spontaneously had shown only slight dyspnea prior to their sudden death. Because their condition did not appear serious, euthanasia was not deemed necessary with regard to either severe disease or anticipation of spontaneous death.
On necropsy, mucus was present in the nasal cavities of all infected mice. No other gross lesions were noted in any of these animals, including the NOD-SCID mice that were euthanized on postinoculation days 11 and 15. Histopathologic examination revealed catarrhal rhinitis and bronchopneumonia in the lungs of all infected mice. Interstitial pneumonia was present in all infected NOD-SCID mice but not in the ICR mice. Rhinitis of mice of both strains was characterized by mild infiltration of inflammatory cells (mainly neutrophils) in the submucosa, slight epithelial necrosis, and mild mucus secretion (Figure 1 B, C). Bronchopneumonia in ICR mice was limited to the peribronchiolar region and was characterized by hyperplasia of peribronchial lymph nodes and infiltration of inflammatory cells, mainly neutrophils, in peribronchial interstitium (Figure 2 C, D). In contrast, bronchopneumonia in NOD-SCID mice was not limited to the peribronchiolar region but spread to deep branches of bronchioles such as terminal and respiratory bronchioles. Pulmonary changes in the NOD-SCID mice were characterized by hypertrophy of alveolar septa due to infiltration of neutrophils (interstitial pneumonia), and infiltration of macrophages into the alveolar lumen (Figure 2 E, F). NOD-SCID mice that were euthanized on postinoculation days 11 and 15 showed similar histopathologic changes to those of NOD-SCID mice on postinoculation day 28 (data not shown). Neither of the strains of mice had any histopathologic changes in the cecum. No clinical symptoms, gross lesions, and histopathologic changes were noted in any of the negative control animals.
Isolate 3224 was recovered from the nasal cavity, trachea, and lungs in pure culture and with some species of intestinal bacterial flora from the cecum in all infected animals on postinoculation day 28 (Table 1). The mice that were euthanized on postinoculation days 11 and 15 had the same bacterial isolation results as those from animals on postinoculation day 28 (data not shown). No bacteria were isolated from the blood samples of any of the mice. Among negative control mice, no bacteria were isolated from the nasal cavity, trachea, or lungs, but some species of intestinal bacterial flora were isolated from cecum.
Table 1.
Number of experimentally infected mice positive for Bordetella hinzii on postinoculation day 28
| Source of sample |
|||||
| Nasal cavity | Trachea | Lung | Blood | Cecum | |
| High dose | |||||
| ICR mice (n = 5) | 5 | 5 | 5 | 0 | 5 |
| NOD-SCID mice (n = 2)a | 2 | 2 | 2 | 0 | 2 |
| Low dose | |||||
| ICR mice (n = 5) | 5 | 5 | 4 | 0 | 5 |
| NOD-SCID mice (n = 4)b | 4 | 4 | 4 | 0 | 4 |
One mouse died on postinoculation day 10. One mouse each was euthanized on postinoculation days 11 and 15.
One mouse died on postinoculation day 21.
Slide agglutination test of serum from experimentally infected ICR mice.
All of the serum samples from the 10 experimentally infected ICR mice showed negative results for B. bronchiseptica in the slide agglutination test.
Discussion
According to the biochemistry profile, the isolate from the index case was tentatively identified as B. avium; this same profile previously was attributed also to B. hinzii.1,7,8,9,15 The production of alkali from malonate, a characteristic of our isolate, is a biochemical feature useful for distinguishing B. hinzii from B. avium.8,15 Although the characteristic cellular fatty acid composition of B. hinzii has been used for identification and discrimination from related species,5,9 the relative proportions of fatty acids can vary depending on whether bacterial cells are harvested after 24 or 48 h of incubation.15 Discrimination of B. hinzii from the phenotypically related species B. avium by cellular fatty acid analysis is not possible after 48 h of culture.15 In addition, cellular fatty acid composition can vary somewhat between B. hinzii strains.15 For these reasons, we did not use cellular fatty acid analysis for identification of our isolate in this study. Partial 16S rRNA sequencing recently was reported to be sufficient for identification of B. hinzii.15 The sequence of our isolate showed the closest similarity (99.9%) with B. hinzii LMG13501T (AF177667) in the GenBank/EMBL/DDBJ data banks. On the basis of these observations, isolate 3224 ultimately was identified as B. hinzii.
In the experimental infection study, all infected mice showed sneezing, and the symptoms were similar to those of the mouse in the index case. The frequency of sneezing in ICR mice decreased with time, and careful observation was necessary to confirm the symptoms in the latter half of the experimental period. Therefore, detection of chronic B. hinzii infection in immunocompetent mice solely by general observation may be difficult in advanced stages.
In routine microbiologic monitoring of laboratory mice, the trachea and cecum typically are used as culture samples to detect respiratory and intestinal bacterial pathogens, respectively.18 In the present study, the isolate was recovered from these sites in all experimentally infected mice. Therefore, these sites similarly may be useful as culture samples to detect B. hinzii in microbiologic monitoring of laboratory mice.
In this study, the C57BL/6 mouse in the index case showed negative results in the agglutination test for B. bronchiseptica, the Bordetella species most frequently associated with laboratory animals. All 10 experimentally infected ICR mice likewise showed negative results for B. bronchiseptica in the agglutination test on postinoculation day 28, and isolate 3224 was not agglutinated by a rabbit antiserum to B. bronchiseptica. Therefore, these 2 Bordetella species appear to differ antigenically, and this difference may be useful for a serologic test for B. hinzii.
B. hinzii is a commensal organism of the avian respiratory tract, and poultry have been suggested as important sources of human infection. However, some clinical cases lacked avian exposure,7,9 and the importance of poultry as a source of infection is not yet clear. With the exception of 1 case of B. hinzii infection in a rabbit,20 no previous reports have clearly indicated that mammals are potential hosts of this bacterium. However, the results of the present study suggest that mice may be a host of B. hinzii and therefore an important source of B. hinzii infection in humans.
In conclusion, B. hinzii was isolated from the trachea and lung of a mouse showing clinical symptoms and histopathologic changes in the respiratory tract, and the bacterium was identified by phenotypic and genetic analyses. Experimental infection with the isolate induced clinical symptoms in the respiratory tracts of ICR and NOD-SCID mice, and the organism was reisolated in pure culture from the nasal cavities and lungs of mice, which showed histopathologic changes. Therefore we suggest B. hinzii as a novel causative agent of respiratory disease in laboratory mice. This report is the first to describe the isolation of B. hinzii from a mouse and the confirmation of the organism's pathogenicity in this species.
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