An Emerging Foodborne
Sean F. Altekruse,* Norman J. Stern, Patricia I. Fields, and David
*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
|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
infectionGuillian-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.
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).
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.
In the United States, an estimated 2.1 to 2.4 million cases of human campylobacter-
iosis (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 campylobacter- iosis 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
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.
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).
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).
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% O2, 10% CO2, and 85% N2. 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).
The ecology of C. jejuni involves wildlife reservoirs, particularly wild
birds. Species that carry C. jejuni include migratory birdsranes,
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).
Epidemiologic studies of laboratory-confirmed cases of sporadic campylobacteriosis
|Residents of three counties
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|aBottle tops pecked by wild
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
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
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 103 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).
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 log10 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 log10 units (65).
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
chainfrom producer to consumeris 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: firstname.lastname@example.org.
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