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242
Laboratory Animals (1986) 20, 242-248.
Otitis media in guineapigs: pathology and bacteriology
R. BOOT·
&
H. C. WALVOORT
2
I
Department of Animal Supply and Laboratory for Parasitology and Mycology and
2
Laboratory for
Pathology, National Institute of Public Health and Environmental Hygiene, P.O. Box I, 3720 BA Bilthoven,
The Netherlands
Summary
In the course of post-mortem examination of conven-
tional random-bred and inbred (immunosuppressed)
strain
2/N
guinea pigs kept in separate quarters, otitis
media was diagnosed in 62 of 462 animals (13'4%)
and 18 of 66 animals (27,3%) respectively. Clinical
signs of otitis media were seen in only two random-
bred animals but in nearly 50% of affected inbred
animals. In random-bred guineapigs, purulent, often
bilateral, otitis media was associated mainly with the
isolation of Streptococcus zooepidemicus, Bordetella
bronchiseptica, Pasteurella and Actinobacillus spp.
and micrococci. In strain
2/N
guineapigs serous or
purulent often bilateral otitis media was associated
mainly with the isolation of B. bronchiseptica and
Pseudomonas aeruginosa serotypes 10 and 11. The
simultaneous occurrence of similar pathogenic bac·
teria in both ears of bilaterally affected animals and
in pneumonic lung tissue (in random-bred animals)
suggested ascending and descending infection
originating from the upper respiratory tract. It is
concluded that otitis media, associated with the iso-
lation of a variety of respiratory bacterial species,
must be considered a major disease problem in
guineapigs.
Keywords: Otitis media; Guineapigs; Bacterial in-
fections
Otitis media is an established disease entity in
conventional guineapigs. Responding to a question-
naire, five of 33 institutions considered otitis media
important in this animal species (Seamer
&
Chester-
man, 1967) but only limited information has
appeared in the literature on the pathology and
bacteriology of this lesion. Kohn (1974) examined
31 guineapigs with torticollis from three different
commercial breeders and Streptococcus zooepi-
demicus (Lancefield group C) was isolated most
frequently, followed by S. pneumoniae. Rigby
(1976) stated that S. pneumoniae infection in
guineapigs was probably most commonly seen as
otitis media but data were not presented. Using
X-ray examination Wagner et al. (1976) diagnosed
otitis media in 13% of guineapigs and S. pneumo-
Received 28 August 1985. Accepted 24 February 1986.
niae
(20%), S.
zooepidemicus
(15%),
Bordetella
bronchiseptica (12%) and Pseudomonas aeruginosa
(11
%)
were isolated from animals showing
radiopacity of the tympanic bulla.
We report the pathology and bacteriology of
mostly asymptomatic cases of otitis media observed
in random-bred and inbred (strain
2/N)
conven-
tional guineapigs.
Materials and methods
Sources and methods of isolation
All animals originated from the random-bred or the
inbred (strain
2/N)
colony in our Institute. The
colonies were kept in separate quarters under
conventional conditions. The animal technicians
supervising the inbred strain colony also worked
with conventional rabbits, rats and mice during part
of the study. The random-bred colony housed 2000
breeding females on average and showed a mortality
rate of about 5% per year. The inbred colony, the
production of which gradually replaced initially
imported animals, housed 50 breeding females on
average and showed a similar mortality rate. In both
colonies a variety of common bacterial pathogens
was present as has been described earlier for the
random-bred colony (Boot, Oosterom
&
Walvoort,
1983).
Most random-bred guinea pigs examined were
recently weaned animals or were from vaccine
control experiments (innocuity tests). Most inbred
animals had been subjected to immunosuppression
by cyclophosphamide treatment or sublethal whole
body irradiation. At post-mortem examination the
tympanic bullae were opened and samples from
grossly affected middle ears were taken using a
sterile bacteriological wire. Initially only one ear
was sampled in animals showing signs of bilateral
ear infection.
Samples were inoculated onto two plain sheep-
blood agars, a sheep-blood agar containing nalidixic
acid (40 flg/ml) and an Endo agar. One sheep-blood
agar was incubated anaerobically for 48 h at 37°C.
All other media were incubated aerobically for 48 h
at 37°C.
Growth on agar media was identified using
standard bacteriological procedures as described by
Otitis media in guinea pigs
Cowan (1974). P. aeruginosa isolates were typed as
described by Habs (1957).
Results
The guineapigs autopsied comprised 462 random-
bred and 66 strain
2/N
animals (Table 1). Otitis
media was diagnosed in 62 (13·4%) random-bred
and in 18 (27·3%) strain
21N
animals, with both ears
being affected in 40 (64·5%) and 14 (77·8%) animals
respectively. Clinical signs of otitis media, such as
torticollis, were noted in only two random-bred
guineapigs but in nearly 50% of affected animals in
the inbred strain, where these signs were the basis
for culling. In 33 random-bred and 11 strain
2/N
animals otitis media was considered the principal
disease but was considered an incidental finding in
the other cases, in which pneumonia and enteritis
were the major lesions. A characteristic pattern of
post-mortem findings was seen at necropsy of many
guinea pigs irrespective of whether otitis media was
considered a major or an incidental finding. This
pattern consisted of weight loss, dehydration, a
nearly empty gastrointestinal tract with a strikingly
small caecum and an enlarged adrenal cortex.
Macroscopically, otitis media presented as an
exudative lesion of the tympanic bulla, the nature of
the exudate varying from serous to purulent (Table
1). Chronic lesions were characterized by hyper-
ostosis of the tympanic bulla, which in some cases
nearly obliterated the lumen. In one random-bred
and three inbred guineapigs with bilateral otitis
there was a purulent lesion in one ear and a serous
lesion in the other.
243
Bacteriological findings in 76 middle ear samples
from the outbred guineapigs are given in Table 2.
From 10 of these samples (13·2%) no bacterial
growth was obtained. The remaining 66 samples
yielded 108 isolates which were assigned to 13
different bacterial species or genera. Eighty-eight of
the isolates (81·5%) were made up of the four most
common bacterial species or genera, i.e. S.
zooepidemicus (Lancefield group C) (45 or 41·7%),
B. bronchiseptica (20 or 18·5%), Pasteurella and
Actinobacillus spp. (14 or 13%) and Micrococcus
spp. (9 or 8·3%). S. zooepidemicus was found in all
12 chronic lesions. Other bacterial species or genera
isolated were each detected in less than 5·5% of all
samples examined by cultivation.
Pure cultures were obtained in 32 of the 66
samples (48·5%) yielding bacterial growth and
consisted of S. zooepidemicus (mostly from purulent
exudates), B. bronchiseptica, Proteus spp., Entero-
bacter cloacae and faecal streptococci.
Bacteriological findings in 23 middle ear samples
from the inbred guineapigs are presented in Table 3.
From one serous sample no bacterial growth was
obtained but the remaining 22 samples yielded 48
isolates, assigned to 11 bacterial species or genera.
Twenty-nine of these isolates (60·4%) were classi-
fied as B. bronchiseptica (18 or 37·5%) or P.
aeruginosa (11 or 22·9%). From the chronic lesions
B. bronchiseptica (three isolates) and S. aureus
(three isolates) were isolated. Other bacterial
species or genera were each cultivated from less
than 12-5% of all samples examined.
Pure cultures were obtained from 6 of the 22
Table 1. Pathomorphological features of otitis media in guineapigs
Lesion
Number of guineapigs
Random-bred Inbred
Otitis media
As major lesion,
As incidental
finding,
Total examined
unilateral
bilateral
unilateral
bilateral
62
8
25
14
15
462
18
2
9
2
5
66
12 (4)
2
16 (8)
2
Nature of lesion
Mucosal hyperaemia
Serous
Seromucous
Mucopurulent
Purulent
Not specified
Number of lesions
2
32 (4)"
5
3
52 (20)
8
Total
102
32
'Numerals in parentheses indicate the number of chronic lesions.
244
Boot
&
Walvoort
Table 2.
Bacteriological findings in otitis media in conventional random-bred guineapigs
Nature of lesion
Mucosal
Not
Bacteria hyperaemia Serous
Seromucous Mucopurulent Purulent
specified Total
Number of samples
2 28 3 2 36
5
76
No growth 1 7 2
10
S. zooepidemicus
10 (2)* 2
29 (16)
4 (3) 45 (21)
B. bronchiseptica
7 (4) 1
11 (3) 1
20 (7)
Pasteurella-Actinobacillus spp. 5
2 5
1 14
Micrococci 1
1
6
9
Diphtheroids 3
1
4
E. coli
4
4
Proteus spp.
1
1 (1)
3 (I)
E. cloacae
2 (1)
2 (I)
Faecal streptococci
2 (2)
2 (2)
Neisseria spp.
2
2
Aeromonas spp.
1
S.
aureus
1
P. aeruginosa
1
Total number of isolates 35 (9) 2 6
57 (20)
7 (3) 108 (32)
*Numerals in parentheses indicate the number of isolates (pure cultures).
Table 3. Bacteriological findings in otitis media in conventional strain
21N
guineapigs
Bacteria
Nature of lesion
Serous Purulent Not specified Total
Number of cases
No growth
B. bronchiseptica
P. aeruginosa
Pasteurella-Actinobacillus spp.
S.
aureus
Bacteroides spp.
E. coli
Klebsiella spp.
Diphtheroids
Proteus
spp.
Faecal streptococci
Peptostreptococcus spp.
Total number of isolates
10
1
7 (1)*
2 (2)
I (I)
1
2
1
2
1
18 (4)
12
10 (2)
8
2
2
1
2
28 (2)
2
23
1
18 (3)
11 (2)
3 (1)
3
3
3
2
2
1
I
1
48 (6)
*Numerals in parentheses indicate the number of isolates (pure cultures).
samples (27·3%) yielding bacterial growth and
consisted of B. bronchiseptica, P. aeruginosa and a
member of the Pasteurella-Actinobacillus group. P.
aeruginosa isolates were of serotype 10 (two iso-
lates) and serotype 11 (nine isolates).
The bacteriological findings in animals in which
both affected ears were sampled are presented in
Fig.!. Of the
12
random-bred guineapigs involved.
five animals showed similar bacteriological infection
of both ears. In all but four animals mixed infections
were detected. All animals positive for S. zooepi-
demicus yielded this micro-organism from both ears.
In th~ seven inbred guineapigs involved. four
animals showed similar bacteriological infection of
both ears. In all but two animals mixed infections
were found. Four of five animals positive for B.
Otitis media in guineapigs
S.
zoo~pid~micus
B.brfYlCflis~plica
Pasl~lla - Actinobacillus
spp,
micrococci
diphtheroids
E.
coli
Prot~us
spp,
E. cloaca~
faecal streptococci
N~iss~ria
sPP.
S.
auretJs
P aeruginosa
Bact~roid~s
sPP.
~plosl~plococcus
spp.
KI~bsi~lIa
spp.
245
random bred
inbred
2
3 4
5
6
7
8
9
10 11 12
2
3
4
5
6
7
••• ••
•
•
0 0
••
0
D •••
•
0
•
•
0
0
•
•
•
0
0
•
0
0
•
•
•
•
0
0
•
o
cultivated from one ear
• cultivated from both ears
Fig. 1. Bacteriological findings in bilateral otitis media in conventional guineapigs.
bronchiseptica contained this micro-organism in
both ears.
Bacteriological findings in animals simultaneously
suffering from otitis media and respiratory tract
infections are presented in Fig. 2. Of the 17
random-bred guinea pigs involved (nine with uni-
lateral and eight with bilateral ear infection) six
showed similar bacteriological infection at both
sampling sites. In nine of 12 animals with strepto-
coccal otitis media this micro-organism was also
recovered from pneumonic lung tissue. In four of
eight animals with B. bronchiseptica-associated
otitis media this species was also cultivated from the
respiratory tract. Escherichia coli was found at both
sites in one animal and Proteus spp. in another.
Only one inbred guineapig showed a similar infec-
tion of both the lung and the middle ear yielding
B.
bronchiseptica and P. aeruginosa from both sites.
Discussion
Our findings support the view that otitis media is a
common disease in guineapigs (Rigby, 1976; Wag-
ner, 1979). On the basis of pathological findings the
incidence of the condition in our random-bred
animals (13·4%) is equ!'.J to the incidence (13%)
reported by Wagner et al. (1976). The inbred strain
2/N
guineapigs showed a higher incidence of both
pathological lesions and clinical signs, possibly due
to the severe immunosuppression exerted on most
of these animals. Asymptomatic otitis media in
guineapigs was reported by Wagner (1979) to occur
frequently. However, Sea mer and Chesterman
(1967) and Rigby (1976) reported torticollis,
incoordination and circling to be commonly ob-
served, presumably dependent on extension of the
infection to the inner ear or brain. The incidence of
otitis media in our study will be an underestimation
since exact clinical data were not recorded. The
importance of otitis media as a disease condition for
guineapigs is suggested by its being considered the
major lesion in more than 50% of the random-bred
animals and in nearly 70% of the inbred animals in
which affected ears were found (Table 1).
Of serous samples from random-bred animals,
25% did not yield bacterial growth (Table 2). This
type of lesion might have reflected an early stage of
infection, possibly by a virus, before bacteria
established a secondary infection. Serous exudation
yielded bacterial growth more frequently in the
inbred animals (Table 3) than in random-bred
animals but only a limited number of samples were
examined. Serous exudates from random-bred ani-
mals had a wider range of bacterial species than
246 Boot
&
Walvoort
random bred inbred
5
6
7
8
9
10 11 12
13
14 15 16 17
1
•
••••
0 •• 0
•
0
••
0
•
0
0
0
0
0
•
•
0
00
o
Prot~us
SPP.
faecal streptococci
Neisseria
SPP.
234
r------------------------,---...,
S. zo~pid~micus
0 • •
B. bronchi~tic9
m
IE! •
Pasteurella-Actinobacillus
spp.
0
micrococci
0
E.co/i
S.
au~us
o
~
I:>iI
P. a~ruginosa
•
cultivated from
o
middle
ear
~ respiratory tract
• both sites
Fig. 2. Bacteriological findings in conventional guineapigs suffering from respiratory tract and middle ear infections.
purulent exudates. The role of the less common
bacterial species in otitis media is not clear. The
isolation of small numbers of micrococci, diphther-
oids and
Neisseria
spp. that are normally present on
the skin and on mucous membranes could result
from contamination during sampling. However, the
detection of large numbers of these species and of
Enterobacteriaceae and faecal streptococci, some-
times in pure culture, suggested a pathogenic role
for these organisms. Synergy of aerobic and faculta-
tively anaerobic weak pathogens in mixed infec-
tions, which were frequently detected in this study,
is well known (MacDonald, 1962; Roberts, 1967;
Thore, Burman
&
Holm, 1982). Fulghum et al.
(1982) described a comparable effect of mixtures of
aerobic and anaerobic weak pathogens and the
much more pathogenic species S. pneumoniae in
experimental otitis media in gerbils and chinchillas.
Thore, Burman and Holm (1982) did not find severe
acute otitis media after application of Bacteroides
asaccharolyticus or Peptostreptococcus micros but
concluded that there was serious pathogenic poten-
tial for Propionibacterium acnes in guineapigs.
Overall findings in random-bred guineapigs
showed the prevalence of purulent often bilateral
otitis media associated with the isolation of S.
zooepidemicus. B. bronchiseptica, Pasteurella and
Actinobacillus spp. and micrococci. These findings
differed clearly from the occurrence of serous or
purulent often bilateral ear infection in strain 2/N
animals from which B. bronchiseptica and P. aerugi-
nosa were the predominant isolates. Chronic lesions
were invariably associated with S. zooepidemicus in
the random-bred animals but with B. bronchiseptica
or
S. aureus
in strain
2/N
animals.
In contrast with Kohn (1974), Wagner et al.
(1976), Rigby (1976) and Wagner (1979), we did not
detect S. pneumoniae in our guineapigs. Although
S. pneumoniae is considered fastidious, the apparent
absence of this micro-organism was not likely to be
due to inadequate isolation techniques since we
were able to grow S. pneumoniae from other
sources. The detection of S. zooepidemicus (Lance-
field group C) as the predominant micro-organism
in the random-bred guinea pigs stresses the
importance of this micro-organism as a cause of
otitis media as reported earlier (Kohn, 1974; Rigby,
1976; Wagner et al., 1976; Wagner, 1979). S.
zooepidemicus was not isolated from any lesions in
inbred guineapigs but susceptibility of the 2/N strain
to Lancefield group C streptococcal infections has
been reported, mainly as a chronic cervical
lymphadenitis ('lumps') and (pleuro )pneumonia
(Fraunfelter et al., 1971). The latter workers did not
examine the middle ear. Absence of group C
streptococcal infection in the 2/N strain might be
partly due to the separate housing of both groups.
However, more than eight distinct antigenic types
have been identified in S. zooepidemicus (Moore
&
Bryans, 1969) which might show different abilities to
colonize different animal species and strains and
hence cause infection.
Otitis media in guineapigs
In spontaneous and experimental B. bronchi-
septica infections in guineapigs, the middle ear has
nearly always been omitted as a sampling site. The
frequent isolation of B. bronchiseptica from cases of
otitis media in our random-bred and inbred guinea-
pigs (18·5% and 37·5% respectively of all isolates)
exceeded the yield (12% of all isolates) reported by
Wagner et al. (1976). Kohn (1974) detected B.
bronchiseptica only once, in a mixed infection,
among 31 cases of otitis media. Whether differences
in attack rates in animals depend on the bacterio-
logical properties of B. bronchiseptica is not fully
understood (Bemis, Greisen
&
Appel, 1977a). B.
bronchiseptica isolates from different animal species
might show a different pathogenicity for guineapigs
as has been suggested from results from ex-
perimental infections in swine (Ross, Switzer
&
Duncan, 1967). The pathogenicity of various
guineapig strains for guineapigs was found to be
comparable, regardless of the original site of isola-
tion (Nakagawa et al., 1971).
The isolation of bacteria of the Pasteurella-
Actinobacillus group from guineapigs with otitis
media has been described previously for our
random-bred colony (Boot, Oosterom
&
Walvoort,
1983). Pasteurella and Actinobacillus spp. were also
isolated from strain
2/N
animals, although in-
frequently. Experimental infection, preferably in
gnotobiotic animals, will be necessary to assess the
pathogenicity of members of the Pasteurella-
Actinobacillus group more precisely.
The frequent isolation of P. aeruginosa from
affected ears in strain
2/N
guineapigs might partly
have resulted from the severe immunosuppression.
Indeed, P. aeruginosa is more frequently associated
with disease in immunocompromised hosts than
other bacterial species. Several ceHular and extra-
cellular products of P. aeruginosa have been impli-
cated in pathogenicity (Young, 1980) but no direct
correlation has been reported between P. aerugi-
nosa serotype and pathogenicity. Our P. aeruginosa
isolates were serotypes 10 and 11. Both serotypes
are frequently found in the faeces of mice and rats
from different colonies (Batema
et al.,
1983). From
our other colonies, serotypes 10 and 11 have been
isolated only from the faeces of healthy rabbits
whereas various other serotypes were found in our
rodents and rabbits (unpublished observations).
Our findings suggest that P. aeruginosa serotypes 10
and 11 might show more pathogenic potential in
strain 2/N guineapigs than other serotypes.
Several bacterial species isolated from otitis
media are considered to be normal inhabitants of
the upper respiratory tract. Group C streptococci
are commonly present on the tonsils or pharynx of
apparently healthy domestic animals (Stamm
&
Cobbs, 1980). Colonization is possibly mediated
247
through surface antigens as has been found for S.
pyogenes (Lancefield group A) in humans (Gibbons
&
van Houte, 1975). B. bronchiseptica preferen-
tially colonizes ciliated regions of the respiratory
tract (Bemis, Greisen
&
Appel, 1977b). Among the
members of the Pasteurella-Actinobacillus group,
which in general show a marked degree of specificity
for localization (Kilian
&
Frederiksen, 1981),
P.
multocida type A has been shown to colonize the
nasopharynx in rabbits through specific adhesins
interacting with receptors on the cell surface (Glor-
ioso et al., 1982). The occurrence of S. zooepidemi-
cus, B. bronchiseptica and Pasteurella and Actino-
bacillus spp. in both ears in cases of bilateral otitis
media (Fig. 1) suggests ascending infection from the
nasopharynx through the Eustachian tube. The
simultaneous occurrence of S. zooepidemicus and B.
bronchiseptica in pneumonic lung tissue and ear
exudates (Fig. 2) suggests concomitant descending
infection to the lower airways. Both ascending and
descending bacterial infection originating from the
upper respiratory tract might be triggered by viral
infections. Sendai virus infection occurs frequently
in guineapig colonies (Parker, Whiteman
&
Richter,
1978) and the interactions between Sendai virus and
bacterial pathogens in the lung are well recognized
(Jakab, 1981). Recently adenovirus infection in
guineapigs has been observed (Naumann
et al.,
1981; Brennecke, Dreier
&
Stokes, 1983). The role
of viral infections in guineapig otitis media has not
been examined. However, in experimental otitis
media in chinchillas, influenza A virus was shown to
enhance susceptibility to pneumococcal otitis media,
presumably through bactericidal and chemotactic
dysfunction of polymorphonuclear leucocytes and
damage to ciliated epithelium. The incidence of
pneumococcal otitis media increased as the time of
pneumococcus inoculation approached the time of
virus-induced leucocyte dysfunction (Abramson,
Giebink
&
Ouie, 1982). The effects of experimental
ear infection with influenza A virus alone proved to
be limited compared with the effects of infection
with S. pneumoniae alone (Giebink et al., 1980;
Giebink
&
Wright, 1983). The latter observations
suggest that the often used term secondary bacterial
infection reflects especially the time sequence of
processes in the development of otitis media.
We conclude that otitis media. associated with the
isolation of a variety of respiratory bacterial species,
must be considered a major disease problem in
gumeaplgs.
Acknowledgements
We would like to thank Mr A. E. Busschbach and
Mr C. Moolenbeek for competent technical assist-
ance and Mrs A. E. Karsten for typing the manu-
script.
248
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