Emerging Infectious Diseases
[Volume 5 No.1 / January - February 1999]
Suggested Citation
Perspectives
Campylobacter jejuni—An Emerging Foodborne Pathogen
Sean F. Altekruse,* Norman J. Stern,† Patricia I. Fields,‡ and David L.
Swerdlow‡
*U.S. Food and Drug Administration, Blacksburg, Virginia, USA; †U.S.
Department of Agriculture, Athens, Georgia, USA; and ‡Centers for Disease
Control and Prevention, Atlanta, Georgia, USA
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Campylobacter jejuni is the most commonly reported bacterial
cause of foodborne infection in the United States. Adding to
the human and economic costs are chronic sequelae associated
with C. jejuni infection—Guillian-Barré syndrome and reactive
arthritis. In addition, an increasing proportion of human
infections caused by C. jejuni are resistant to antimicrobial
therapy. Mishandling of raw poultry and consumption of
undercooked poultry are the major risk factors for human
campylobacteriosis. Efforts to prevent human illness are needed
throughout each link in the food chain.
History
Awareness of the public health implications of Campylobacter infections has
evolved over more than a century (1). In 1886, Escherich observed organisms
resembling campylobacters in stool samples of children with diarrhea. In
1913, McFaydean and Stockman identified campylobacters (called related
Vibrio) in fetal tissues of aborted sheep (1). In 1957, King described the
isolation of related Vibrio from blood samples of children with diarrhea,
and in 1972, clinical microbiologists in Belgium first isolated
campylobacters from stool samples of patients with diarrhea (1). The
development of selective growth media in the 1970s permitted more
laboratories to test stool specimens for Campylobacter. Soon Campylobacter
spp. were established as common human pathogens. Campylobacter jejuni
infections are now the leading cause of bacterial gastroenteritis reported
in the United States (2). In 1996, 46% of laboratory-confirmed cases of
bacterial gastroenteritis reported in the Centers for Disease Control and
Prevention/U.S. Department of Agriculture/Food and Drug Administration
Collaborating Sites Foodborne Disease Active Surveillance Network were
caused by Campylobacter species. Campylobacteriosis was followed in
prevalence by salmonellosis (28%), shigellosis (17%), and Escherichia coli
O157 infection (5%) (Figure 1).
[Fig]
Figure 1. Cases of Campylobacter and other foodborne infections by
month of specimen collection; Centers for Disease Control and
Prevention/U.S. Department of Agriculture/Food and Drug
Administration Collaborating Sites Foodborne Disease Active
Surveillance Network, 1996.
Disease Prevalence
In the United States, an estimated 2.1 to 2.4 million cases of human
campylobacteriosis (illnesses ranging from loose stools to dysentery) occur
each year (2). Commonly reported symptoms of patients with laboratory-
confirmed infections (a small subset of all cases) include diarrhea,
fever, and abdominal cramping. In one study, approximately
half of the patients with laboratory-confirmed campylobacteriosis
reported a history of bloody diarrhea (3). Less frequently, C.
jejuni infections produce bacteremia, septic arthritis, and other
extraintestinal symptoms (4). The incidence of campylobacteriosis in
HIV-infected patients is higher than in the general population. For
example, in Los Angeles County between 1983 and 1987, the
reported incidence of campylobacteriosis in patients with AIDS was 519
cases per 100,000 population, 39 times higher than the rate in the general
population. (5). Common complications of campylobacteriosis in HIV-infected
patients are recurrent infection and infection with antimicrobial-resistant
strains 6). Deaths from C. jejuni infection are rare and occur primarily in
infants, the elderly, and patients with underlying illnesses (2).
Sequelae to Infection
Guillain-Barré syndrome (GBS), a demyelating disorder resulting in acute
neuromuscular paralysis, is a serious sequela of Campylobacter infection
(7). An estimated one case of GBS occurs for every 1,000 cases of
campylobacteriosis (7). Up to 40% of patients with the syndrome have
evidence of recent Campylobacter infection (7). Approximately 20% of
patients with GBS are left with some disability, and approximately 5% die
despite advances in respiratory care. Campylobacteriosis is also associated
with Reiter syndrome, a reactive arthropathy. In approximately 1% of
patients with campylobacteriosis, the sterile postinfection process occurs
7 to 10 days after onset of diarrhea (8). Multiple joints can be affected,
particularly the knee joint. Pain and incapacitation can last for months or
become chronic.
Both GBS and Reiter syndrome are thought to be autoimmune responses
stimulated by infection. Many patients with Reiter syndrome carry the HLA
B27 antigenic marker (8). The pathogenesis of GBS (9) and Reiter syndrome
is not completely understood.
Treatment of C. jejuni Infections
Supportive measures, particularly fluid and electrolyte replacement, are
the principal therapies for most patients with campylobacteriosis (10).
Severely dehydrated patients should receive rapid volume expansion with
intravenous fluids. For most other patients, oral rehydration is indicated.
Although Campylobacter infections are usually self limiting, antibiotic
therapy may be prudent for patients who have high fever, bloody diarrhea,
or more than eight stools in 24 hours; immunosuppressed patients, patients
with bloodstream infections, and those whose symptoms worsen or persist for
more than 1 week from the time of diagnosis. When indicated, antimicrobial
therapy soon after the onset of symptoms can reduce the median duration of
illness from approximately 10 days to 5 days. When treatment is delayed
(e.g., until C. jejuni infection is confirmed by a medical laboratory),
therapy may not be successful (10). Ease of administration, lack of serious
toxicity, and high degree of efficacy make erythromycin the drug of choice
for C. jejuni infection; however, other antimicrobial agents, particularly
the quinolones and newer macrolides including azithromycin, are also used.
Antimicrobial Resistance
The increasing rate of human infections caused by antimicrobial-resistant
strains of C. jejuni makes clinical management of cases of
campylobacteriosis more difficult (11,12). Antimicrobial resistance can
prolong illness and compromise treatment of patients with bacteremia. The
rate of antimicrobial-resistant enteric infections is highest in the
developing world, where the use of antimicrobial drugs in humans and
animals is relatively unrestricted. A 1994 study found that most clinical
isolates of C. jejuni from U.S. troops in Thailand were resistant to
ciprofloxacin. Additionally, nearly one third of isolates from U.S. troops
located in Hat Yai were resistant to azithromycin (11). In the
industrialized world, the emergence of fluoroquinolone-resistant strains of
C. jejuni illustrates the need for prudent antimicrobial use in food-animal
production (12). Experimental evidence demonstrates that
fluoroquinolone-susceptible C. jejuni readily become drug-resistant in
chickens when these drugs are administered (13). After flouroquinolone use
in poultry was approved in Europe, resistant C. jejuni strains emerged
rapidly in humans during the early 1990s (12). Similarly, within 2 years of
the 1995 approval of fluoroquinolone use for poultry in the United States,
the number of domestically acquired human cases of ciprofloxacin-resistant
campylobacteriosis doubled in Minnesota (14). In a 1997 study conducted in
Minnesota, 12 (20%) of 60 C. jejuni isolates obtained from chicken
purchased in grocery stores were ciprofloxacin-resistant (14).
Pathogenesis
The pathogenesis of C. jejuni infection involves both host- and
pathogen-specific factors. The health and age of the host (2) and C.
jejuni-specific humoral immunity from previous exposure (15) influence
clinical outcome after infection. In a volunteer study, C. jejuni infection
occurred after ingestion of as few as 800 organisms (16). Rates of
infection increased with the ingested dose. Rates of illness appeared to
increase when inocula were ingested in a suspension buffered to reduce
gastric acidity (16).
[Fig]
Figure 2. Scanning electron microscope image of Campylobacter
jejuni, illustrating its corkscrew appearance and bipolar flagella.
Source: Virginia-Maryland Regional College of Veterinary Medicine,
Blacksburg, Virginia.
Many pathogen-specific virulence determinants may contribute to the
pathogenesis of C. jejuni infection, but none has a proven role (17).
Suspected determinants of pathogenicity include chemotaxis,
motility, and flagella, which are required for attachment and
colonization of the gut epithelium (Figure 2) (17). Once colonization
occurs, other possible virulence determinants are iron acquisition,
host cell invasion, toxin production, inflammation and active secretion,
and epithelial disruption with leakage of serosal fluid (17).
Survival in the Environment
Survival of C. jejuni outside the gut is poor, and replication does not
occur readily (17). C. jejuni grows best at 37°C to 42°C (18), the
approximate body temperature of the chicken (41°C to 42°C). C. jejuni grows
best in a low oxygen or microaerophilic environment, such as an atmosphere
of 5% O(sub 2), 10% CO(sub 2), and 85% N(sub 2). The organism is sensitive
to freezing, drying, acidic conditions (pH < 5.0), and salinity.
Sample Collection and Transport
If possible, stool specimens should be chilled (not frozen) and submitted
to a laboratory within 24 hours of collection. Storing specimens in deep,
airtight containers minimizes exposure to oxygen and desiccation. If a
specimen cannot be processed within 24 hours or is likely to contain small
numbers of organisms, a rectal swab placed in a specimen transport medium
(e.g., Cary-Blair) should be used. Individual laboratories can provide
guidance on specimen handling procedures (18).
Numerous procedures are available for recovering C. jejuni from clinical
specimens (18). Direct plating is cost-effective for testing large numbers
of specimens; however, testing sensitivity may be reduced. Preenrichment
(raising the temperature from 36°C to 42°C over several hours), filtration,
or both are used in some laboratories to improve recovery of stressed C.
jejuni organisms from specimens (e.g., stored foods or swabs exposed to
oxygen) (19). Isolation can be facilitated by using selective media
containing antimicrobial agents, oxygen quenching agents, or a low oxygen
atmosphere, thus decreasing the number of colonies that must be screened
(18,19).
Subtyping of Isolates
No standard subtyping technique has been established for C. jejuni. Soon
after the organism was described, two serologic methods were developed, the
heat-stable or somatic O antigen (20) and the heat-labile antigen schemes
(21). These typing schemes are labor intensive, and their use is limited
almost exclusively to reference laboratories. Many different DNA-based
subtyping schemes have been developed, including pulsed-field gel
electrophoresis (PFGE) and randomly amplified polymorphic DNA (RAPD)
analysis (22). Various typing schemes have been developed on the basis of
the sequence of flaA, encoding flagellin (23); however, recent evidence
suggests that this locus may not be representative of the entire genome
(24).
Transmission to Humans
Most cases of human campylobacteriosis are sporadic. Outbreaks have
different epidemiologic characteristics from sporadic infections (2). Many
outbreaks occur during the spring and autumn (2). Consumption of raw milk
was implicated as the source of infection in 30 of the 80 outbreaks of
human campylobacteriosis reported to CDC between 1973 and 1992. Outbreaks
caused by drinking raw milk often involve farm visits (e.g., school field
trips) during the temperate seasons. In contrast, sporadic Campylobacter
isolates peak during the summer months (Figure 1). A series of case-control
studies identified some risk factors for sporadic campylobacteriosis,
particularly handling raw poultry (25,26) and eating undercooked poultry
(27-31) (Table). Other risk factors accounting for a smaller proportion of
sporadic illnesses include drinking untreated water (29); traveling abroad
(25); eating barbequed pork (28) or sausage (27); drinking raw milk (29,32)
or milk from bird-pecked bottles (33); and contact with dogs (27) and cats
(29,31), particularly juvenile pets or pets with diarrhea (25,34).
Person-to-person transmission is uncommon (25,32). Overlap is reported
between serotypes of C. jejuni found in humans, poultry, and cattle,
indicating that foods of animal origin may play a major role in
transmitting C. jejuni to humans (35).
In the United States, infants have the highest age-specific Campylobacter
isolation rate, approximately 14 per 100,000 person years. As children get
older, isolation rates decline to approximately 4 per 100,000 person years
for young adolescents. A notable feature of the epidemiology of human
campylobacteriosis is the high isolation rate among young adults,
approximately 8 per 100,000 person years. Among middle-aged and older
adults, the isolation rate is < 3 per 100,000 person years (2). The peak
isolation rate in neonates and infants is attributed in part to
susceptibility on first exposure and to the low threshold for seeking
medical care for infants (2). The high rate of infection during early
adulthood, which is pronounced among men, is thought to reflect poor
food-handling practices in a population that, until recently, relied on
others to prepare meals (2).
Reservoirs
The ecology of C. jejuni involves wildlife reservoirs, particularly wild
birds. Species that carry C. jejuni include migratory birds—cranes, ducks,
geese (36), and seagulls (37). The organism is also found in other wild and
domestic bird species, as well as in rodents (38). Insects can carry the
organism on their exoskeleton (39).
Table. Epidemiologic studies of laboratory-confirmed cases of sporadic
campylobacteriosis
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Foods
Number associated
with Animal
Cases Controls Date Population Location illness contacts Ref.
--------------------------------------------------------------------------
52 103 1989- Residents Norway Poultry, Dogs 27
1990 of three sausage
counties
218 526 1982- HMO Washington Undercooked Animals 30,
1983 patients State chicken with 34
diarrhea
29 42 1990 Residents England Bottled 33
of milk(sup a)
Manchester
45 45 1983- University Georgia Chicken Cats 31
1984 students
53 106 1982- Rural Iowa Raw milk 32
1983 children
40 80 1981 Residents Colorado Untreated Cats 29
of Denver, water,
Ft. Collins raw milk,
undercooked
chicken
54 54 1982 Residents Netherlands Chicken, 28
of pork,
Rotterdam barbequed
foods
10 15 1982 Residents Colorado Preparing 26
of chicken
Larimer
County
55 14 1980 Residents Sweden Preparing Kitten, 25
of chicken dog
Göteborg with
diarrhea
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(sup a)Bottle tops pecked by wild birds.
The intestines of poultry are easily colonized with C. jejuni. Day-old
chicks can be colonized with as few as 35 organisms (40). Most chickens in
commercial operations are colonized by 4 weeks (41,42). Vertical
transmission (i.e., from breeder flocks to progeny) has been suggested in
one study but is not widely accepted (43). Reservoirs in the poultry
environment include beetles (39), unchlorinated drinking water (44), and
farm workers (41,42,45). Feeds are an unlikely source of campylobacters
since they are dry and campylobacters are sensitive to drying.
C. jejuni is a commensal organism of the intestinal tract of cattle (46).
Young animals are more often colonized than older animals, and feedlot
cattle are more likely than grazing animals to carry campylobacters (47).
In one study, colonization of dairy herds was associated with drinking
unchlorinated water (48).
Campylobacters are found in natural water sources throughout the year. The
presence of campylobacters is not clearly correlated with indicator
organisms for fecal contamination (e.g., E. coli)(49). In temperate
regions, organism recovery rates are highest during the cold season
(49,50). Survival in cold water is important in the life cycle of
campylobacters. In one study, serotypes found in water were similar to
those found in humans (50). When stressed, campylobacters enter a "viable
but nonculturable state," characterized by uptake of amino acids and
maintenance of an intact outer membrane but inability to grow on selective
media; such organisms, however, can be transmitted to animals (51).
Additionally, unchlorinated drinking water can introduce campylobacters
into the farm environment (44,48).
Campylobacter in the Food Supply
C. jejuni is found in many foods of animal origin. Surveys of raw
agricultural products support epidemiologic evidence implicating poultry,
meat, and raw milk as sources of human infection. Most retail chicken is
contaminated with C. jejuni; one study reported an isolation rate of 98%
for retail chicken meat (52). C. jejuni counts often exceed 10(sup 3) per 100 g.
Skin and giblets have particularly high levels of contamination. In one
study, 12% of raw milk samples from dairy farms in eastern Tennessee were
contaminated with C. jejuni (53). Raw milk is presumed to be contaminated
by bovine feces; however, direct contamination of milk as a consequence of
mastitis also occurs (54). Campylobacters are also found in red meat. In
one study, C. jejuni was present in 5% of raw ground beef and in 40% of
veal specimens (55).
Control of Campylobacter Infection
On the Farm
Control of Campylobacter contamination on the farm may reduce contamination
of carcasses, poultry, and red meat products at the retail level (27).
Epidemiologic studies indicate that strict hygiene reduces intestinal
carriage in food-producing animals (41,42,45). In field studies, poultry
flocks that drank chlorinated water had lower intestinal colonization rates
than poultry that drank unchlorinated water (42,44). Experimentally,
treatment of chicks with commensal bacteria (56) and immunization of older
birds (57) reduced C. jejuni colonization. Because intestinal colonization
with campylobacters readily occurs in poultry flocks, even strict measures
may not eliminate intestinal carriage by food-producing animals (39,41).
At Processing
Slaughter and processing provide opportunities for reducing C. jejuni
counts on food-animal carcasses. Bacterial counts on carcasses can increase
during slaughter and processing steps. In one study, up to a 1,000-fold
increase in bacterial counts on carcasses was reported during
transportation to slaughter (58). In studies of chickens (59) and turkeys
(60) at slaughter, bacterial counts increased by approximately 10- to
100-fold during defeathering and reached the highest level after
evisceration. However, bacterial counts on carcasses decline during other
slaughter and processing steps. In one study, forced-air chilling of swine
carcasses caused a 100-fold reduction in carcass contamination (61). In
Texas turkey plants, scalding reduced carcass counts to near or below
detectable levels (60). Adding sodium chloride or trisodium phosphate to
the chiller water in the presence of an electrical current reduced C.
jejuni contamination of chiller water by 2 log(sub 10) units (62). In a
slaughter plant in England, use of chlorinated sprays and maintenance of
clean working surfaces resulted in a 10- to 100-fold decrease in carcass
contamination (63). In another study, lactic acid spraying of swine
carcasses reduced counts by at least 50% to often undetectable levels (64).
A radiation dose of 2.5 KGy reduced C. jejuni levels on retail poultry by
10 log(sub 10) units (65).
Conclusions
C. jejuni, first identified as a human diarrheal pathogen in 1973, is the
most frequently diagnosed bacterial cause of human gastroenteritis in the
United States. Sequelae including GBS and reactive arthritis are
increasingly recognized, adding to the human and economic cost of illness
from human campylobacteriosis. The emergence of fluoroquinolone-resistant
infections in Europe and the United States, temporally associated with the
approval of fluoroquinolone use in veterinary medicine, is also a public
health concern. The consumption of undercooked poultry and
cross-contamination of other foods with drippings from raw poultry are
leading risk factors for human campylobacteriosis. Reinforcing hygienic
practices at each link in the food chain—from producer to consumer—is
critical in preventing the disease.
Dr. Altekruse is a Public Health Service Epidemiology Fellow with the
Food and Drug Administration, Center for Veterinary Medicine. His current
research interest is antimicrobial-resistant foodborne pathogens.
Address for correspondence: Sean Altekruse, Virginia-Maryland
Regional College of Veterinary Medicine, Duckpond Road, Blacksburg, VA,
24060, USA; fax: 540-231-7367; e-mail: saltekru@vt.edu.
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Emerging Infectious Diseases
National Center for Infectious Diseases
Centers for Disease Control and Prevention
Atlanta, GA
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