595

Journal of Food Protection, Vol. 48, No. 7, Pages 595-599 (July 1985)
Copyright" International Association of Milk, Food, and Environmental Sanitarians

Prevalence and Distribution of Campylobacter jejuni

and Campylobacter coli in Retail Meats
N. J. STERN*, M. P. HERNANDEZ1, L. BLANKENSHIP2, K. E. DEIBEL3, S. DOORES4, M. P. DOYLE5,
H. NG6, M. D. PIERSON7, J. N. SOFOS8, W. H. SVEUM9 and D. C. WESTHOFF1

Meat Science Research Laboratory, ASI, Beltsville Agricultural Research Center, Agricultural Research Service, USDA, Beltsville, Maryland 20705

(Received for publication November 20, 1984)

ABSTRACT origin as vehicles of human disease. Raw or undercooked

Nine cooperating laboratories, distributed throughout the
United States, determined the interlaboratory reproducibility of
a sensitive, selective method for isolation of Campylobacter je-
juni and Campylobacter coli from foods, and determined the
prevalence and distribution of the organism in retail meats. A
double-blind inoculated/recovery experiment demonstrated the
ability to detect two cells of C. jejuni and C. coli per g of
meat at a rate of 96% among the cooperating laboratories.
However, a 7.5% false-positive rate for the presumptive detec-
tion of the organism was also reported. Samples of ground
beef, beef flank steak, lamb stew meat, broiler chicken, pork
sausage (without antimicrobials), and pork chops were selected
to assess the presence of Campylobacters. Each cooperator pur-
chased five of each of the above samples from the refrigerated
case of two retail outlets at quarterly intervals throughout the
year. A total of 2,160 retail samples were analyzed for the pres-
ence of C. jejuni and C. coli. Results indicated that about 30%
of the 360 chickens sampled yielded the organism. Analysis of
1,800 red meat products yielded Campylobacters at a rate of
about 5.1%. Pork samples yielded C. coli and other meats
yielded C. jejuni. Higher numbers of isolations from the red
meats were made during June and September (8.6%) as com-
pared with December and March (4.2%). These results provide
a baseline, for the prevalence of Campylobacters in these
selected foods, and also support epidemiologic data associating
mishandled foods of animal origin as a potential vehicle in
human gastroenteritis.
An estimated 600,000 cases per year of campylobacter-
induced enteritis occur in the United Kingdom (16),
where awareness of the organism is keen. The sources
for such large-scale infections are likely to be varied, but
numerous epidemiological reports link foods of animal
'University of Maryland, College Park.
2
Russell Research Center-USDA, Athens, GA.
*Ohio State University, Columbus.
''Pennsylvania State University, University Park.
1 MATERIALS AND METHODS
Food Research Institute-University of Wisconsin, Madison.
6
Western Regional Research Center-USDA, Albany, CA.
7 Interlaboratory
Virginia Polytechnic Institute and State University, Blacksburg.
^Colorado State University, Fort Collins.
^Armour Research Center, Scottsdale, AZ.
chickens recurringly are implicated in outbreaks (4,15,17)
as are unpasteurized milks (1,12). Other animal food
products such as hamburger (9) and pork (23) have been
implicated in epidemiologic studies, suggesting the trans-
mission of the organism from food to man.
The significance of widespread human infection trans-
mitted through foods of animal origin are implicit to the
food microbiologist charged with ensuring the public
health. Reports suggest appropriate means to cook,
freeze, or acidify products, thereby inactivating the
pathogen in food sources. To accurately assess the useful-
ness of any new processing technique in reducing the
numbers of Campylobacter jejuni and Campylobacter coli
on foods of animal origin, baseline data are needed to
correctly indicate the prevalence of the organism. These
data are presented in this report.
One similar survey was done under the auspices of the
British Public Health Laboratory Service (20). More than
6,000 meat samples were analyzed by 31 participating
laboratories employing a wide variety of non-standardized
procedures for recovery of C. jejuni and C. coli. The
study reported that 1.0% of the red meats at retail distri-
bution were contaminated with the organism and that
"the contamination rate of raw red meat by C. jejuni is,
in general, very l o w . " Several sensitive procedures for
detecting Campylobacters in foods have since become
available (3,6,22). In a comparison of selective enrich-
ment broths (14), the method described by Doyle and
Roman (6) was most sensitive and selective among three
methods. In the present study, this method (6) was em-
ployed in a standardized procedure among nine cooperat-
ing laboratories within the United States to determine: (a)
the inter-laboratory reproducibility of the method, (b) the
prevalence of C. jejuni and C. coli in selected retail
foods, and (c) the seasonal variations which might occur
on selected meat products.
reproducibility
Using a double-blind experimental protocol, in which both
the participants and the individual inoculating the encoded sam-

JOURNAL OF FOOD PROTECTION, VOL. 48, JULY 1985

596 STERN ET AL.
pies were ignorant of levels (or absence) of C. jejuni, nine par-
ticipating laboratories assessed inoculated cubes of beef stew
meat for the qualitative presence of C. jejuni and C. coli. Foot-
notes indicating author's affiliation on the title page do not
coincide with the laboratory numbers assigned in the tables.
Meat used for inoculation had been stored under frozen condi-
tions to reduce the potential for presence of indigenous Cam-
pylobacters (19). Cubes of beef, weighing about 25 g, were
placed into Ziploc bags (Dow Chemical Co., Indianapolis, IN),
to which the 1.0 ml of inoculum was added. Inocula consisted
of four strains of Campylobacters grown at 42°C overnight in
a biphasic Brucella broth/agar system (13), mixed on an equal
volume basis and diluted with 0.1% peptone. Strains used and
their sources were: (a) C. jejuni USN-312, J. Coolbaugh, Naval
Medical Research Institute (clinical isolate); (b) C. coli MDG-7,
Meat Science Research Laboratory (pig isolate); (c) C. jejuni
ATCC-29428, American Type Culture Collection (clinical iso-
late); and (d) C. jejuni JCH-665, Meat Science Research Labo-
ratory (chicken isolate). Inocula levels were determined by
enumerating colony-forming units on Campy-BAP medium (2).
The Campy-BAP plates were incubated for 48-72 h at 42°C
under a microaerobic atmosphere of 5% 0 2 , 10% CO2, and
85% N 2 . The various dilution levels of inocula were dispersed
onto the beef cubes, as were (Table 1) sterile portions of 0.1%
peptone controls. After encoding and inoculating, samples were
placed into insulated foamed plastic chests containing ice, in
an attempt to maximize viability of the test organism. The sea-
led chests were sent to the cooperating laboratories via an over-
night delivery service, and analysis for presence of C. jejuni
and C. coli began as soon after arrival as possible. Samples
were to be held under refrigeration until analysis.
Analyses of the coded samples were done by the following
procedure. When possible, 100 ml of Brucella broth (Oxoid
USA, Columbia, MD) or 0.1% peptone was used to wash the
sample by massaging and shaking for 2 min. The wash was
filtered through cheesecloth and then cells were sedimented by
centrifugation at about 16,000 x g at 4°C for about 10 min
to form a pellet containing the microflora associated with the
sample. Most often, a portion of the pellet was streaked directly
to a Campy-BAP plate and the remainder was suspended in the
enrichment broth described by Doyle and Roman (6). All media
used in this study were standardized and distributed through
Oxoid USA (Columbia, MD). Enrichment was carried out as
specified by using microaerobic conditions at 42°C under con-
stant agitation. The enrichment cultures were plated directly,
or after a 10"1 and 10"2 dilution, onto the surface of Campy-
BAP medium. Both the direct-streak plates and post-enrichment
plates were inspected for characteristic colonies resembling C.
jejuni and C. coli after 24, 48 and 72 h of incubation, with
microaerobic conditions reestablished after each examination.
Wet mounts of suspect colonies were observed by using either
phase-contrast or darkfield microscopy. Presumptive isolation
was indicated by presence of a comma, gull, spiral or s-shaped,
narrow (0.2 to 0.4 |xm) organism exhibiting a rapid, corkscrew-
like motion. Presumptive isolates were most often tested for
positive catalase and oxidase enzyme activities before reporting
the recovery of the organism. The interlaboratory reproducibil-
ity for recovery of inoculated Campylobacters from meats was
tested before and after the retail market survey.
Retail market survey
Approximately 1- to 2-lb (454 to 908 g) samples each of
ground beef, beef flank steak, lamb stew meat, broiler chicken,
pork sausage without antimicrobials, and pork chops were
JOURNAL OF FOOD PROTECTION. VOL. 48, JULY 1985
selected for this survey. Each cooperator purchased from the
refrigerated case of two retail outlets, five samples of each of
the above six products during the months of June, September,
December, 1983 and March, 1984. The product was kept cool
(ca. 4°C) until analysis. In total, 2,160 meat products were as-
sessed for the presence of C. jejuni and C. coli.
The whole-cuts of meats were rinsed by shaking/massaging
in 250 ml of Brucella broth or 0.1% peptone in plastic bags.
Twenty-five grams of the ground beef or pork sausage samples
were blended or stomached with 100 ml of the enrichment
broth, and isolation of C. jejuni and C. coli was carried out
as described above. When assessing ground beef samples for
presence of the organism, no blood was included in the enrich-
ment broth because such supplementation diminishes the recov-
ery sensitivity (Stern et al., accepted by J. Food Prot.). As in
the above interlaboratory reproducibility study, "presumptive"
isolations were based on morphology, rapid corkscrew-like mo-
tion, and oxidase and catalase reaction criteria. These isolates
were sent to the Meat Science Research Laboratory in transport
medium (21) for independent confirmation. Only those isolates
which survived transport and could be purified were subjected
to confirmation tests. Species confirmation and identification
were based on recommended criteria (11).
Statistical analysis
The analysis of variance test was used to (a) determine dif-
ferences in rates of C. jejuni and C. coli recovery among the
selected meats, (b) to demonstrate differences in cooperator's
isolation rates, and (c) to assess potential influence of the sea-
sonal variation. Data were normalized by using the arc sine
transformation for proportions. Duncan's multiple range test
was employed at the 5% level. Correlation coefficients were
calculated to determine the relation between the ' 'reported'' and
the "confirmed" observations.
RESULTS AND DISCUSSION
Interlaboratory reproducibility
Results indicating the recovery of C. jejuni and C. coli
from inoculated beef cubes, as reported by eight of the
cooperating laboratories participating in the double-blind
experiment, are given in Table 1. In the initial experi-
ment (May, 1983), laboratory five received samples
which were warm upon arrival. It is recognized (5) that
the viability of Campylobacters is rapidly diminished at
25°C. Consequently, data from this laboratory are not in-
cluded. Among the eight other cooperating laboratories
receiving appropriately cooled samples, the trends for re-
covering C. jejuni and C. coli substantiated the levels of
sensitivity suggested by the authors of the enrichment
method (6). These investigators (6) recovered levels of
one to four cells per g of inoculated hamburgers, in
100% of the instances. During the pre-survey inoculated-
sample trials, in the present study, the organism was pre-
sent at levels of about 0.7 cell per g of meat and recov-
ery was accomplished at a rate of about 67%. When the
inoculation level was increaased ten-fold (i.e. 7 cells
perg), recoveries were increased to about 82%. At this
point it was recognized that at least three factors could
account for lack of 100% consistent recoveries from the
inoculated samples: (a) the target organism may have
been inactivated during transport, (b) the competing
 CAMPYLOBACTER IN RETAIL MEATS 597

TABLE 1. Recovery of Campylobacter jejuni and Campylobacter coli from experimentally inoculated beef cubes" as reported by
eight cooperating laboratories participating in a double-blind experiment, on two separate occasions.
Number of correct reponses
May , 1983 May, 1984
No. of Campylobacter per sample No. of Campylobacter per samples
Laboratory 0.0 1.8 18 180 0.0 48 4800
1 5/5 0/5 4/5 4/5 10/10 5/5 5/5
2 3/5 5/5 2/5 2/5 9/10 4/5 5/5
3 5/5 1/5 5/5 5/5 10/10 5/5 5/5
4 5/5 2/5 4/5 4/5 10/10 5/5 5/5
5 extenuating circumstances -• data not included
6 4/5 1/5 2/5 5/5 6/10 5/5 5/5
7 5/5 0/5 4/5 5/5 9/10 5/5 5/5
8 5/5 3/5 4/5 5/5 10/10 5/5 5/5
9 4/5 3/5 2/5 3/5 10/10 5/5 5/5

TOTALS 36/40 15/40 27/40 33/40 74/80 39/40 40/40

(90%) (37.5%) (67.5%) (82.5%) (92.5%) (97.5%) (100%)
"Average beef cube samples weighed ca. 25 g and contained a total aerobic plate count ranging from 7.3 x 105 to 5.3 x 106.

microflora may have masked the presence of cam-

paylobacters, or (c) different levels of competence in re-
covery capabilities existed among the cooperators.
Both pre- and post-survey inoculated trials revealed
several false-positive recoveries. An inadequate and un-
satisfactory explanation is that indigenous Campylobacters
might have been present in the meat. However, among
five inoculated subsamples taken during each inoculated/
recovery experiment, no C. jejuni and C. coli could be
detected. The rate of false-positive recovery was greatest
for laboratory six, which also had the highest reported
levels of Campylobacter isolation and corresponded with
the lowest confirmed:reported correlation. Overall, the
rate of false-positive reporting would have been greatly
diminished if the cooperating laboratories had completely
characterized their isolates by the established taxonomic
criteria (11). However, such characterization was not
done and the isolates from the inoculated trials were not
sent back to the Meat Science Research Laboratory for
confirmation.
As the cooperative research proceeded, the ability to
recover the organism appeared to improve. At compara-
ble inoculation levels (2.0 and 0.7 cells per g) during the
post-survey inoculated sample trial, the rate of recovery
increased from 67% to about 98%, thus indicating the
general effectiveness in detecting this level of C. jejuni
and C. coli by the methods used. This level of sensitivity
seemed sufficient to detect the numbers reported to con-
taminate chickens, which range from 102 to 103 9 per
wing (7). The improved recovery capability in the second
inoculated/recovery experiment may also have been, in
part, due to use of more ice and insulation to help main-
tain the samples in a chilled condition during transport.
Retail market survey
Results as communicated by the participating laborato-
ries for the reported but unconfirmed recovery of C. je-
juni and C. coli from retail markets within the United
States are given in Table 2. The presence of C. jejuni
and C. coli, by meat product, ranged from a low of 3.6%
in ground beef to a high of 29.7% on broiler chickens.
The incidence of recovery from lamb stew meat (8.1%)
was highest (p<0.05) among the red meats sampled.
Chickens had significantly (p<0.05) higher prevalence of
C. jejuni compared with the other meats sampled. The
occurrence of the organism on red meats averaged 5.1%
of the samples, which is approximately five-fold greater
than the prevalence previously reported (20). Our study
employed standardized materials and methods for each
cooperator, whereas in the previous study no rigid criteria
were established for the methods used. The enrichment
method employed has been shown to be comparatively
effective for recovery of C. jejuni from foods (14). In
the present study, only C. coli was recovered from pork
products, whereas the other meats yielded only C. jejuni.
Laboratory six had the lowest correlation (r=.503) of
confirmed:reported isolations of the organism among all
of the cooperators. As laboratory six also had uniquely
high reported levels of Campylobacters from foods, the
data are also presented excluding this laboratory. Figure
1 presents the prevalence of C. jejuni and C. coli from
the meats samples. The pork and beef products yielded
lower isolation rates when the data are compared with
and without this one unique laboratory. Isolation rates re-
mained similar for both chicken and lamb stew products.
The prevalence of C. jejuni on chickens was inter-
mediate when compared with previous reports (8,10,18);
however, with the exception of the Turnbull and Rose
report (20), all other surveys assayed far fewer than the
360 samples assessed in the present report. With im-
proved methodology higher isolation rates can be antici-
pated, but the present report provides a controlled study
indicating the current prevalence of the organism in meats
from retail market refrigerated cases and should be used
for future comparisons.

JOURNAL OF FOOD PROTECTION, VOL. 48, JULY 1985

598 STERN ET AL.

— — o M
rn m (S ^ O 30-

C 3 M
( N O — OC-lTfrOff~1Tl" 25-
O -O ,"
:
£ £
<u ex •— O O — o - i ^ O ^ ™
20-
a . •£> c
O f N O ^ t O ^ O G 0
0
o
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o
(0

y y s?
10-
" m c o r i r - - m m f " > "

,1 5-

_ ^ - 0 — O O — <NO
n n r-i E
Chicken Pork Pork Ground Beef Lamb
— O •— O — O O <N ~ Chop Sausage Beef Flank Stew

Ov CO
— O O O — <N. O <^> ~
Figure 1. Prevalence of Campylobacter jejuni and Campylobac-
O O O O J O O O ^ C O ter coli isolated from 360 samples each of chicken, pork chop,
pork sausage, ground beef, beefflankand lamb stew (excludin
o o o o o o o o o data from laboratory 6).

— O O O — — O O <N
Variation was noted among the cooperating laboratories
O O O — — — OO^fr with regard to the reported prevalence of the organism.
Total prevalence of C. jejuni and C. coli reported by the
o— o o o ^ t o o o cooperators ranged from a low of 0.8% (laboratory three)
to a high of 22.5% (laboratory six), with a laboratory
O O O O — — O O O
average recovery rate of 9.2% from the meats tested.
O O O O O — O O O
With the exception of laboratory six, fairly high correla-
tions were obtained for reported and confirmed presence
^t
O O O O — o - i O O O
^t
of the organism from meats. Laboratory six also had a
relatively high number of false-positives in the inocu-
O O O O O ^ f r O f N O lated/recovery trial (Table 1). On the other hand, both
laboratories four and seven had good correlations of re-
o o o o — o — o o
ported and confirmed isolates (r=1.0 and 0.9, respec-
O O O O O f N O O -
tively), and had comparatively accurate results in the sec-
ond inoculated/recovery study (Table 1), but had signific-
o
O O O O O ^ f r O O f N V antly fewer recoveries in the survey. Explanations are
Q-
lacking to account for the laboratory-to-laboratory varia-
O O O — O n ^ O O O tions in the recovery rates. However, some of the re-
ported isolates could have been inactivated in transport
O O O O O f N O - O
and could account for some of the isolates falling into
the unconfirmed category. As an inadequate number of
O O O O O O O — O
cooperators were involved in this survey to properly as-
O O O O O r * - i O O r * - i
sess geographical distribution, no significance could be
II « obtained to determine the influence of location on the
O — O — O ^ O O O O
-a t3
prevalence of C. jejuni and C. coli in foods.
Current poultry husbandry practices do not provide for
r*lTtO^O(Nr*-i(NTtO
much seasonal variation in rearing. Similar ambient tem-
a G C ^ o O O ^ f r r ^ O ^ O O
peratures are held year round, similar feeds are adminis-
Q 5 tered, and relatively little contact with the outside envi-
\ o r s O ( N ( N r - ( N r - f n ronment is experienced by the birds. Consequently, it is
probable that less seasonal variation would occur with re-
^ m - ^ O O ^ t O i n O •c ° gard to Campylobacter prevalence on poultry products.
u u
o. P The data obtained were analyzed for isolation rates by
II c
«3 ' "
season for all products except for chicken (Table 2). Beef
s — ( N f ^ ^ t » n ^ o r - G o o N cattle, pigs and lambs are exposed to seasonal variation
and might be expected to show more influence. Trends
7? indicated lower prevalence of the organism isolated in

JOURNAL OF FOOD PROTECTION, VOL. 48, JULY 1985

 CAMPYLOBACTER IN RETAIL MEATS
December and March (4.5 and 3.9%) as compared with
June and September (8.6 and 8.6%), but no statistical
differences were noted due to the wide variation in recov-
ery rates among the reporting laboratories. Less dramatic
seasonal variation was observed when the data from labo-
ratory six were excluded; however, similar trends were
seen (Fig. 2). The prevalence of Campylobacters on the
red meats samples averaged 5.5% for June and Sep-
tember and fell to 3.8% for December and March.
6-
c
o
= 4-
— Tijd. Genees. 124:1631-1633.
o 10. Park, C. E., Z. K. Stankiewicz, J. Lovett, and J. Hunt. 1981.
v>
* 2 -
0J 1 1 1 1 1 1 1 1
June Sept. Dec. March
Figure 2. Prevalence of Campylobacter jejuni and Campylobac-
ter coli isolated from pork chop, pork sausage, ground beef,
beef flank and lamb stew (excluding data from laboratory 6)
as influenced by seasonal variation.
In conclusion, nine cooperating laboratories reported a
significant presence of C. jejuni and C. coli in selected
meats. Poultry yielded the organism from about 30% of
the 360 samples analyzed, whereas about 5% of the
1,800 red meat samples contained the potential human
pathogen. The method used was highly consistent (98%)
among the cooperators, enabling the recovery of 2 cells
of C. jejuni and C. coli per g of meat. The problem of
false-positive isolations persisted throughout this year
long study.
ACKNOWLEDGMENT
Presented at the 44th Annual Meeting of the Institute of Food Tech-
nologists, Anaheim, CaHfornia, June 10-13, 1984.
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