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64
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scriptions of lesions associated with sal- included gross lesions were also Gram stained
monellosis in passerine species are rather (Culling et al., 1985). Histologic examination
was not conducted on birds received in 2000.
scarce; only a few reports describe histo-
pathologic findings (Hurvel, 1973; Routh Questionnaires
and Sleeman, 1995; Pennycott et al., 1998;
Epidemiologic information was obtained by
Daoust et al., 2000; Hudson et al., 2000). requesting the consignors of dead birds to fill
Healthy carriers of S. Typhimurium in in a questionnaire. However, only question-
passerine populations are considered to be naires from consignors who submitted birds
a major source of fatal infections (Greuel which laboratory examination subsequently
and Arnold, 1971; Hurvell et al., 1974; confirmed to be cases of salmonellosis were in-
cluded in the study. The questionnaires from
Pennycott et al., 1998; Daoust et al., consignors, whose dead birds were assigned
2000). Salmonella carriage in passerines other diagnosis than salmonellosis, were too
varying from 0–8.3% (in special cases 14– few to make a comparable statistical analysis of
43%); sparrows and starlings (Sturnus vul- the two groups, and thus excluded from the
garis) are the most common carriers (Wil- study. Data concerning time and duration of
the incidents, species and numbers of sick and
son and MacDonald, 1967; Goodchild and dead birds, the different species at the feeding
Tucker, 1968; Marx, 1969; Tizard et al., place, type of feed, feeding routines, as well as
1979; Brittingham et al., 1988; Čı́žek et al., earlier episodes with sick or dead birds, were
1994; Morishita et al., 1999). collected and analyzed using the computer pro-
In this study, we report pathologic find- gram Epi Info (version 6.04 b/c, Centers for
Disease Control and Prevention, Atlanta, Geor-
ings and epidemiologic data linked to fatal
5% CO2 atmosphere and in anaerobic condi- had intestinal infection only (carrier birds)
tions, respectively, while the BBLSA plate was and had died from trauma.
incubated aerobically. All plates were incubated
overnight at 37 C. Pathologic findings in bird carcasses
Cloacal swabs from live birds, and intestines
from carcasses, were cultured for Salmonella From a total of 145 birds subjected to
according to the Nordic Committee on Food thorough postmortem examination in 1999
Analysis (Anonymous, 1991). Briefly, cloacal and 2000, 94 had died from septicemic sal-
swabs were individually incubated in 9.9 ml
buffered peptone water (BPW) (Oxoid CM509, monellosis (Table 2). Affected birds were
Oxoid Limited, Hampshire, England) at 37 C equally distributed with regard to sex, and
for 24 hr. One hundred ml from each of five represented nine species. Most were ema-
samples were further pooled into 49.5 ml Rap- ciated or in poor body condition (84.0%)
paport-Vassiliadis Soya broth (RVS) (Oxoid with wasted pectoral muscles and no visi-
CM866) and incubated at 42 C for 24 hr. Fi-
nally, the pooled RVS-samples were inoculated ble fat. Affected birds (91.5%), except for
on modified brilliant green agar (Difco 218801) three Eurasian siskins, three common red-
and BBLSA and incubated at 37 C for 24 hr. polls (Carduelis flammea), one tree spar-
Meanwhile, the BPW-incubated swabs were row (Passer montanus) and one great tit
kept in a refrigerator for possible later investi- (Parus major), also had marked organ le-
gation. Intestines with contents were incubated
in BPW in a ratio of 1:10 (weight/volume), after sions (Table 2). The most constant finding
which 100 ml from each sample were trans- was yellow-white, multifocal to confluent
ferred to 10 ml RVS. Further the procedures necrosis in the wall of the esophagus and
were otherwise identical to those describe crop (77.7%) (Fig. 1). Scattered foci of ne-
TABLE 1. Salmonella Typhimurium 4, 12 : i : 1, 2-infection in birds found dead at 87 private feeding places
by species, Norway 1998–2000, common species observed at 70a feeding places, and isolation of S. Typhi-
murium 4, 12 : i : 1, 2 from carrier birds.
ic lesions were characterized by extensive had acute focal necrosis with little or no
necrosis with accumulation of inflamma- reactive change nor bacteria.
tory cells, and occasional multinucleated
Questionnaires
giant cells, in combination with small acute
foci of necrosis with no inflammatory re- Questionnaires were received from 71
sponse. Aggregates of Gram-negative bac- (82%) of 87 feeding places with confirmed
teria were seen in association with necro- cases of salmonellosis during 1998–2000,
sis, but also occurred elsewhere in hepatic representing 17 single cases and 54 out-
and splenic parenchyma. Pulmonary, re- breaks. Sick and dead birds were observed
nal, and myocardial findings included scat- from December to June, with a distinct
tered aggregates of Gram negative bacte- peak during February and March (Fig. 2).
ria, usually located within vessels, although The duration of the outbreaks varied from
in some sites, the aggregations were found less than 1 wk up to 4 mo (median51.35
in combination with small foci of necrosis. mo, mean51 mo).
Four of eight birds with septicemic sal- Overall, 205 birds were reported found
monellosis and no grossly visible lesions, dead; 121 of these birds were submitted
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5 (5)
—
—
—
—
—
—
—
43 (46)
Spleen
—
—
—
—
—
50 (53)
—
—
—
—
1
12 (13)
(9)
—
—
—
—
73 (78)
1 (3)
1 (1)
—
—
—
—
—
—
—
—
1
94
places.
Eurasian siskin (Carduelis spinus)
Bullfinch (Pyrrhula pyrrhula)
DISCUSSION
Extensive postmortem autolysis.
Our study supports earlier findings that distribution of this species (Cramp and
finches, like bullfinch, Eurasian siskin, Simmons, 1994). Although the great tit
common redpoll, and greenfinch, are par- and blue tit (Cyanistes caeruleus) were
ticularly susceptible to S. Typhimurium in- common species at most of the feeding
fection (Englert et al., 1967; Schaal and places in the present study, salmonellosis
Ernst, 1967; Borg, 1985; Routh and Slee- was confirmed only in four individuals. In
man, 1995; Daoust et al., 2000). Reports Norway and Sweden, only 5% of dead
of disease in common redpolls are restrict- great tits examined during more than 30
ed to the Scandinavian peninsula (Borg, yr died from salmonellosis (Borg, 1985;
1985) and North America (Daoust et al., Refsum et al., 2002). The explanation for
2000), probably reflecting the circumpolar the lower number of fatal infections in tits,
compared to finches, may lie in a greater
resistance to infection in tits, or behaviour
at the feeding place resulting in less ex-
posure to the bacterium. Gregarious spe-
cies like finches, siskins, and sparrows of-
ten seek feed on the ground, potentially
contaminated by droppings from infected
birds. These birds also probably run a
greater risk of being infected, since they
often stay for a prolonged time at the feed-
FIGURE 2. Observations of sick and dead birds at
feeding places by month, reported by consignors of
ing place (Englert et al., 1967; Cornelius,
dead birds confirmed to be cases of salmonellosis, 1969; Hurvell and Jevring, 1974; Daoust
Norway 1998–2000. et al., 2000). Tits usually pick food, often
JOURNAL OF WILDLIFE DISEASES
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from suspended feed or hanging feeders, disease may be acute, or even peracute in
and fly off the feeding place to consume it some birds.
elsewhere. In addition, the way the birds The overall prevalence of salmonella
eat seed might be important. Finches and carriage found in the present study (2.0%)
siskins can hold several seeds in their bills was probably an underestimation, due to
and husk them one at a time (Newton, sub-optimal sampling method, using cloa-
1972), while tits process feed by pecking cal swabs. The primary carrier species
it while held between the feet. Thus, in were identical to those species most often
contrast to finches, tits may be less ex- suffering from salmonellosis. No carriers
posed to potentially contaminated hulls. were found among 485 tits (Parus sp.) ex-
Whether there actually are species differ- amined. This result supports our recent
ences in resistance or not, needs further hypothesis, that tits are less exposed to the
clarification. bacterium. Other surveys of passerines
Common lesions in cases of fatal sal- have shown varying prevalences from
monellosis were necrosis in the crop/ 0–8.3 % (Wilson and MacDonald, 1967;
esophagus, liver, and spleen, as well as Goodchild and Tucker, 1968; Tizard et al.,
splenomegaly. These lesions were reported 1979; Čı́žek et al., 1994; Morishita et al.,
in other studies (Kösters and Scheer, 1967; 1999). However, with one exception (Ti-
Englert et al., 1967; Hurvell et al., 1974; zard et al., 1979), none of these studies
Pennycott et al., 1998; Daoust et al., provide explicit information as to whether
2000). We also found necrosis in the pro- or not the samples were collected from
tween birds at any time of the year, but rier birds are probably important in main-
summer feeding of birds is not common in taining a source of infection, causing spo-
Norway. radic cases or local epizootics of salmonel-
Contaminated feeding places seem to losis in passerines by contamination of
play an important role in the epizootiology feeding places. However, the influence of
of salmonellosis in passerines (Greuel and environmental factors in the epidemiology
Arnold, 1971; Locke et al., 1973; Borg, of extensive epizootics still remains poorly
1985; Pennycott et al., 1998). Crowds of understood.
birds visit feeding places during the winter
season, running a risk of being infected in- ACKNOWLEDGMENTS
directly from healthy carriers or sick birds. We thank the Norwegian Zoological Society
In our study, carrier birds and disease out- and the Norwegian Ornithological Society for
breaks occurred all over the country. Ap- publishing the requests for people to report
bird mortality. We thank the consignors for col-
proximately half the consignors reported lecting and submitting birds for laboratory ex-
previous observations of sick or dead birds amination and for completing the question-
consistent with fatal salmonellosis, thus in- naires. We are also grateful to the 21 voluntary
dicating a possible continuous local source local ornithologists who performed the carrier
of infection. In a follow-up investigation of investigations. We thank A. Stovner and K.
Nordby for technical assistance in connection
two feeding places, at which more than with postmortem and bacteriologic investiga-
one outbreak was reported in recent years, tions. Financial support was provided by
we isolated S. Typhimurium 4, 12: i : 1, 2 Sørlie9s Foundation.
CULLING, C. F. A., R. T. ALLISON, AND W. T. BARR. wild finches. Eine Tierärztliche Umschau 22: 66–
1985. Cellular pathology technique, 4th Edition, 71.
Butterworth & Co. Ltd., London, UK, pp. 155– LOCKE, L. N., R. B. SHILLINGER, AND T. JAREED.
180. 1973. Salmonellosis in passerine birds in Mary-
DAOUST, P. Y., D. G. BUSBY, L. FERNS, J. GOLTZ, S. land and West Virginia. Journal of Wildlife Dis-
MCBURNEY, C. POPPE, AND H. WHITNEY. 2000. eases 9: 144–145.
Salmonellosis in songbirds in the Canadian At- MARX, M. B. 1969. Two surveys of salmonella infec-
lantic provinces during winter-summer 1997–98. tion among certain species of wildlife in northern
Canadian Veterinary Journal 41: 54–59. Virginia (1963 and 1965–1966). American Jour-
ENGLERT, H. K., K. HAASS, J. SCHNEIDER, AND M. nal of Veterinary Research 30: 2003–2006.
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