Campylobacter antimicrobial drug resistance among humans, broiler chickens, and pigs, France.
ABSTRACT We describe isolates from human Campylobacter infection in the French population and the isolates' antimicrobial drug resistance patterns since 1986 and compare the trends with those of isolates from broiler chickens and pigs from 1999 through 2004. Among 5,685 human Campylobacter isolates, 76.2% were C. jejuni, 17.2% C. coli, and 5.0% C. fetus. Resistance to nalidixic acid increased from 8.2% in 1990 to 26.3% in 2004 (p < 10(-3)), and resistance to ampicillin was high over time. Nalidixic acid resistance was greater for C. coli (21.3%) than for C. jejuni (14.9%, p < 10(-3)). C. jejuni resistance to ciprofloxacin in broilers decreased from 31.7% in 2002 to 9.0% in 2004 (p = 0.02). The patterns of resistance to quinolones and fluoroquinolones were similar between 1999 and 2004 in human and broiler isolates for C. jejuni. These results suggest a potential benefit of a regulation policy limiting use of antimicrobial drugs in food animals.
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ABSTRACT: Infection with Campylobacter jejuni is one of the most common causes of gastroenteritis worldwide; it occurs more frequently than do infections caused by Salmonella species, Shigella species, or Escherichia coli O157:H7. In developed countries, the incidence of Campylobacter jejuni infections peaks during infancy and again during early adulthood. Most infections are acquired by the consumption and handling of poultry. A typical case is characterized by diarrhea, fever, and abdominal cramps. Obtaining cultures of the organism from stool samples remains the best way to diagnose this infection. An alarming recent trend is the rapid emergence of antimicrobial agent--resistant Campylobacter strains all over the world. Use of antibiotics in animals used for food has accelerated this trend. It is fortunate that complications of C. jejuni infections are rare, and most patients do not require antibiotics. Guillain-Barré syndrome is now recognized as a post-infectious complication of C. jejuni infection, but its incidence is <1 per 1000 infections. Careful food preparation and cooking practices may prevent some Campylobacter infections.Clinical Infectious Diseases 04/2001; 32(8):1201-6. · 9.37 Impact Factor
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ABSTRACT: To establish the incidence and aetiology of infectious intestinal disease in the community and presenting to general practitioners. Comparison with incidence and aetiology of cases reaching national laboratory based surveillance. Population based community cohort incidence study, general practice based incidence studies, and case linkage to national laboratory surveillance. 70 general practices throughout England. 459 975 patients served by the practices. Community surveillance of 9776 randomly selected patients. Incidence of infectious intestinal disease in community and reported to general practice. 781 cases were identified in the community cohort, giving an incidence of 19.4/100 person years (95% confidence interval 18.1 to 20.8). 8770 cases presented to general practice (3.3/100 person years (2.94 to 3.75)). One case was reported to national surveillance for every 1.4 laboratory identifications, 6.2 stools sent for laboratory investigation, 23 cases presenting to general practice, and 136 community cases. The ratio of cases in the community to cases reaching national surveillance was lower for bacterial pathogens (salmonella 3.2:1, campylobacter 7.6:1) than for viruses (rotavirus 35:1, small round structured viruses 1562:1). There were many cases for which no organism was identified. Infectious intestinal disease occurs in 1 in 5 people each year, of whom 1 in 6 presents to a general practitioner. The proportion of cases not recorded by national laboratory surveillance is large and varies widely by microorganism. Ways of supplementing the national laboratory surveillance system for infectious intestinal diseases should be considered.BMJ 05/1999; 318(7190):1046-50. · 14.09 Impact Factor
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ABSTRACT: Data from a general practice-based, case-control study on gastroenteritis and the pathogens related to this disease were used to study the association between specific pathogens and the infected patients' ages and symptoms. For comparison, the occurrence of these pathogens in control patients, stratified by age, also is presented. In children with gastroenteritis who were <5 years of age, rotavirus (in 21% of patients) and Norwalk-like virus (NLV; in 15%) were the most common pathogens. Among patients who were 5-14 years of age, Campylobacter species (in 16% of patients) and Giardia lamblia (in 10%) were the most common pathogens. In the older patients, Campylobacter species was also the most common pathogen (8% to 15% of patients). In addition, several symptoms in case patients were associated with specific pathogens. Blood in the stool was associated with infection with Campylobacter species. In patients with fever, Salmonella species, Campylobacter species, and rotavirus were detected relatively often. Vomiting was associated with NLV and rotavirus. This is the first study in The Netherlands and one of the first studies in the world that has investigated a broad range of pathogens recovered from an unselected population of patients who had consulted general practitioners because of gastroenteritis.Clinical Infectious Diseases 09/2001; 33(3):280-8. · 9.37 Impact Factor
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 2, February 2007 259
We describe isolates from human Campylobacter
infection in the French population and the isolates’ antimi-
crobial drug resistance patterns since 1986 and compare
the trends with those of isolates from broiler chickens and
pigs from 1999 through 2004. Among 5,685 human
Campylobacter isolates, 76.2% were C. jejuni, 17.2% C.
coli, and 5.0% C. fetus. Resistance to nalidixic acid
increased from 8.2% in 1990 to 26.3% in 2004 (p<10−3),
and resistance to ampicillin was high over time. Nalidixic
acid resistance was greater for C. coli (21.3%) than for C.
jejuni (14.9%, p<10−3). C. jejuni resistance to ciprofloxacin
in broilers decreased from 31.7% in 2002 to 9.0% in 2004
(p = 0.02). The patterns of resistance to quinolones and flu-
oroquinolones were similar between 1999 and 2004 in
human and broiler isolates for C. jejuni. These results sug-
gest a potential benefit of a regulation policy limiting use of
antimicrobial drugs in food animals.
rhea in humans worldwide (1–6). A recent study on illness
and death due to foodborne infections in France estimated
an isolation rate of 27–37/100,000 persons/year for
Campylobacter infection (7).
Campylobacter are part of normal enteric flora in ani-
mals (poultry, pigs, and cattle) and can be transmitted to
humans through contaminated foods (8). Several studies
identified chicken as the main source of infection (9,10).
Most Campylobacter enteric infections are self-limited
and do not require antimicrobial drug treatment. However,
ampylobacter infections are, along with Salmonella
infections, the most common cause of bacterial diar-
severe or long-lasting Campylobacter infections do occur
and may justify antimicrobial drug therapy. Macrolides as
first-line therapy and fluoroquinolones as alternative ther-
apy are recommended (2,11). Resistance of Campylo-
bacter to antimicrobial agents has increased substantially
during the past 2 decades and has become a matter of con-
cern in severe human Campylobacter infections (12–14).
Combined studies in humans and poultry have implicated
the use of fluoroquinolones in poultry in the emergence of
drug resistance (15–17). As a consequence, in 2004 the US
Food and Drug Administration withdrew the 1995/1996
approval for the new animal drug application to use
enrofloxacin for prophylaxis treatment or growth promo-
tion in poultry (18). Veterinary licensing of enrofloxacin in
poultry was approved by the European Union (EU) in
1991, and in 1999 the EU recommended limiting the use of
fluoroquinolones in poultry.
In this article, we describe characteristics of human
Campylobacter isolates in France and trends of antimicro-
bial resistance in such isolates from 1986 to 2004. Trends
of Campylobacter antimicrobial drug resistance in human
isolates were compared with those of isolates from broiler
chickens and pigs between 1999 and 2004.
Materials and Methods
National Surveillance System for Human
Surveillance for Campylobacter infections in France
is based on a network of laboratories that send their iso-
lates to the National Reference Center for Campylobacter
and Helicobacter (CNRCH). The network of participating
laboratories, limited to hospital laboratories from 1986 to
2001, was complemented by private (which usually cared
Campylobac ter Antimic robial Drug
Resistanc e among Humans, Broiler
Chickens, and Pigs, Franc e
Anne Gallay,* Valérie Prouzet-Mauléon,† Isabelle Kempf,‡ Philippe Lehours,† Leila Labadi,†
Christine Camou,† Martine Denis,‡, Henriette de Valk,* Jean-Claude Desenclos,*
and Francis Mégraud†
*Institut de Veille Sanitaire, Saint Maurice, France; †Centre
National de Référence des Campylobacter and Helicobacter,
Bordeaux, France; and ‡Agence Française de Sécurité Sanitaire
des Aliments, Ploufragan, France
for outpatients) and additional hospital laboratories in
2002 to be more representative of the whole French terri-
tory (19–21). The network is currently composed of 325
private laboratories (9% of the 3,444 registered private
laboratories in France), located in 90 of the 95 districts in
mainland France, and 92 hospital laboratories (25% of the
409 registered hospital laboratories). Participating labora-
tories perform a systematic screening for Campylobacter
in stools. Each isolate recovered is sent to CNRCH in a
transport medium (medium for storage of bacteria, Bio-
Rad, Marnes-la-Coquette, France) with information on the
type of specimen; date and district of isolation; patient’s
age, sex, and history of travel abroad; and eventual context
of an outbreak.
On reception at CNRCH, isolates are tested for viabil-
ity, confirmed as Campylobacter by standard phenotypic
identification, and identified at the species level with phe-
notypic methods and real-time PCR to differentiate
between C. jejuni, C. coli and C. fetus (2,22). The other
species are identified by comparing their 16S rDNA
sequences to those of DNAdatabases by using the BLAST
program (23). Identification at the species level is consid-
ered correct when at least 99% identity occurs with only 1
Antimicrobial Drug Resistance Monitoring of
Campylobacter in Humans
Campylobacter isolates from all species were evaluat-
ed for susceptibility to 7 antimicrobial drugs (nalidixic
acid, ciprofloxacin [since 2000], erythromycin, amoxi-
cillin, gentamicin, tetracycline, and doxycycline [since
2003]) by the agar diffusion method on Mueller-Hinton
agar enriched with 5% sheep blood by using antibiotic
disks, according to recommendations for Campylobacter
of the Antibiogram Committee of the French Society for
Microbiology (CA-SFM) (24). Since the hospital laborato-
ry network set up in 1986 was extended to private labora-
tories in 2002, antimicrobial susceptibility trends were
analyzed exclusively for hospital laboratory isolates
between 1986 and 2004. Multidrug resistance was defined
as resistance to >2 antimicrobial drugs.
Antimicrobial Drug Resistance Monitoring
in Broilers and Pigs
Surveillance of Campylobacter antimicrobial drug
resistance was implemented in France in 1999 for broilers
in conventional and free-range broiler farms and in 2000
for pigs as part of a surveillance program on resistance in
sentinel bacteria (Escherichia coli and Enterococcus spp.)
and zoonotic bacteria (Salmonella spp. and Campylobacter
spp.) in animal products for human consumption. Thus,
data collection began just after the ban of 4 antimicrobial
growth promoters (bacitracin zinc, spiramycin, virgini-
amycin, and tylosin phosphate) by the European
Community (EC) Council Regulation (No. 2821/98,
December 1998). Conventional broiler flocks are charac-
terized by an indoor rearing period of 6 weeks, and free-
range broiler flocks have an indoor rearing period of 6
weeks followed by 6 additional weeks with access to an
From 200 to 600 broiler cecal samples or pig fecal
samples were collected each year in 10 broiler and 10 pig
slaughterhouses representative of French production of
these animals for human consumption (25). Strain isola-
tion was performed in a central laboratory (Agence
Française de Sécurité Sanitaire des Aliments [AFSSA],
Ploufragan, France) for the first 2 years and then in district
veterinary laboratories, except for antimicrobial suscepti-
bility testing. After identifying isolates by using multiplex
PCR (26), the MIC of ampicillin, nalidixic acid,
enrofloxacin or ciprofloxacin, tetracycline, erythromycin,
and gentamicin were determined by agar dilution. As for
human isolates, susceptibility to antimicrobial drugs was
categorized according to the 2004 statement of the CA-
SFM (24). The study of antimicrobial resistance of
Campylobacter from animal sources was supported by the
French Ministry of Agriculture.
Differences between proportions and isolation rates
were tested by χ2and Fisher exact tests. Means were com-
pared with Student and Fisher tests. Patterns of antimicro-
bial resistance were analyzed by 4-year increments from
1986 to 2004.
Surveillance for Human Campylobacter Infections
From April 2002 to December 2004, CNRCH
received 5,685 presumptive Campylobacter isolates.
Among the 5,112 (89.9%) viable isolates, 3,896 (76.2%)
were C. jejuni, 878 (17.2%) C. coli, 257 (5.0%) C. fetus,
21 (0.4%) C. lari, 40 (0.8%) Arcobacter butzleri, and 13
(0.25%) other species of Campylobacter. Seven strains
(0.1%) were Helicobacter spp. A seasonal increase during
the warmer months was noted and was more pronounced
for C. jejuni.
The median age of patients was 29.4 years (range 5
days–100 years). Thirteen (0.2%) were newborns (5–30
days), 258 (4.5%) infants (1–11 months), 1,907 (33.5%)
children (1–10 years), 2,555 (44.9%) ages 11–65 years, and
767 (13.5%) >65 years (Figure 1). Isolation of
Campylobacter was more frequent among male than
female patients (male/female ratio = 1.2, p = 0.04), except
for young adults (16–30 years), with a male/female ratio =
0.9 (p<10−3). The ratio of C. jejuni to C. coli varied between
260Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 2, February 2007
4.5 and 7.2 in those <30 years of age and decreased there-
after. C. fetus was isolated among adults >30 years of age
and peaked in the elderly (p<10−3, Figure 2).
Among the 5,620 isolates with a known clinical
source, 5,253 (93.4%) were isolated from stools, 308
(5.5%) from blood, and 50 (0.9%) from other sites presum-
ably seeded as a result of bacteremic infections. Both C.
jejuni and C. coli were isolated essentially from stools,
whereas 158 (63.5%) of 249 C. fetus isolates were from
blood. Patients with blood isolates were older than those
with stool isolates (median age 69 years vs. 19.3 years,
Travel history was available for 1,370 (24.1%) case-
patients; 184 (3.2%) reported traveling outside France dur-
ing the 2 weeks before onset of illness. The country of
travel was specified for 169 (91.8%) case-patients (Africa,
98 persons; Asia, 26; Europe, 16; South America, 10; and
other countries, 19).
Antimicrobial Drug Resistance of Human
Resistance to nalidixic acid and tetracycline/doxycy-
cline increased from 1986–1989 to 2002–2004 (p<10−3,
Figure 3). Resistance to ampicillin, although frequent,
decreased from 49.2% (1,027/2,087) in 1986–1989 to
42.4% (501/1,198) in 2002–2004 (p<10−3). Resistance to
erythromycin remained low, and no isolate was resistant to
Nalidixic acid resistance increased from 8.2%
(26/315) in 1990 to 26.3% (115/438) in 2004 (p<10−3).
Resistance was greater for C. coli (21.3%) than C. jejuni
(14.9%, p<10−3, Figure 4). Nalidixic acid resistance
increased for C. jejuni >4-fold from 1995 to 1997 and for
C. coli >3-fold from 1994 to 1996. Then, resistance
decreased for both C. coli and C. jejuni in 1999 but
remained higher than before 1995 (Figure 4).
Ciprofloxacin resistance, tested since 2000, followed the
same pattern (Table).
Fifty-eight percent of Campylobacter isolates were
resistant to >1 drug, 34.7% to >2 drugs, and 20.0% to >3
drugs. The most common multidrug resistance (>2 drugs)
patterns included resistance to nalidixic acid or
ciprofloxacin, to doxycycline, and to ampicillin.
Among the case-patients ≤15 years of age, 28.0%
(618/2,207) had a Campylobacter strain resistant to
nalidixic acid compared with 37.6% (1,029/2,736) of the
case-patients >15 years of age (p<10−3). The proportion of
resistance to ciprofloxacin did not vary according to age
(27.3% of case-patients ≤15 years and 27.9% >15 years).
For ampicillin, 41.9% (925/2,207) of case-patients ≤15
years had a resistant strain compared with 37.3%
(1,024/2,736) of the case-patients >15 years (p = 0.001).
Of the case-patients who traveled abroad, for which
strain resistance was available, 40.3% (67/166) had a strain
resistant to ciprofloxacin, compared with 27.0%
(294/1,090) of case-patients who did not travel abroad
(p<10−3). For nalidixic acid, 42% (70/166) of case-patients
who traveled abroad compared with 34.7% (378/1,090) of
case-patients who did not had a resistant strain (p = 0.06).
Resistance to ampicillin was present for 28.3% (47/166)
who had traveled abroad compared with 31.1%
(339/1,090) for those who had not (p = 0.01).
Antimicrobial Resistance in Broilers and Pigs
Between 1999 and 2004, a total of 544 C. jejuni and
374 C. coli isolates were recovered from poultry, and 871
C. coli were recovered from pigs by the antibiotic resist-
ance surveillance system. Among the broiler isolates, the
proportion of C. jejuni from animals raised in standard and
export production facilities gradually decreased from
83.5% (279/334) in 1999 to 43% (28/65) in 2004 (p<10−3),
while the proportion of C. jejuni decreased from 32%
(18/57) to 10% (4/40) in the free-range production facili-
ties (p = 0.01).
Campylobacter isolates were inconstantly sensitive to
ampicillin, and a high proportion of isolates resistant to
tetracycline was recorded in poultry and pigs, but all
strains remained sensitive to gentamicin (Table). Isolates
from pigs were less frequently resistant to ampicillin but
more often resistant to tetracycline. For erythromycin,
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 2, February 2007261
Figure 2. Distribution of human Campylobacter strains by species
and patient age group, France, 2002–2004.
Figure 1. Distribution of Campylobacter isolates according to age
and sex of patient, France, 2002–2004.
Campylobacter Antimicrobial Drug Resistance, France
resistance was rare among C. jejuni strains (1.8%), but
much more frequent for C. coli (21.1% of broiler isolates
and 58.9% of pig isolates, p<10−3).
In broilers, C. coli strains were more often resistant to
ciprofloxacin (37.4%, 140/374) than were C. jejuni strains
(19.5%, 106/544), p<10−3) (Table, Figure 5). C. coli resist-
ance to ciprofloxacin increased in pigs from 12.3%
(39/316) in 2000 to 26.9% (18/67) in 2004 (p = 0.002). For
C. jejuni in broilers, after an increase in resistance from
16.8% (50/297) in 1999 to 31.7% (13/41) in 2002 (p =
0.02), resistance to ciprofloxacin decreased to 9.0% (3/32)
in 2004 (p = 0.02) (Table, Figure 5). Similar trends were
observed for quinolone resistance. The trend of resistance
to nalidixic acid and ciprofloxacin was similar for C. jeju-
ni isolated from humans and broilers between 1999 and
2004 (Table, Figure 5).
Our surveillance of Campylobacter isolates in France
indicates some differences with findings from other west-
ern countries, i.e., a greater proportion of C. coli (17.0%).
The epidemiologic characteristics of Campylobacter infec-
tions were, however, similar. Campylobacter is predomi-
nant in the summer (27), the isolation rate was much
greater in children <5 years of age, and C. jejuni was pre-
dominant. The rate of resistance to certain antimicrobial
drugs increased substantially from 1990 to 2004, and the
proportion of resistant isolates varied according to
Campylobacter sp. Resistance to quinolones was greater
for C. coli (21.3%) than for C. jejuni (14.9%). Quinolone
and fluoroquinolone resistance for C. coli was high in
broilers and pigs. Resistance to quinolone and fluoro-
quinolone for C. jejuni had the same pattern over time in
broilers and human isolates.
The proportion of C. coli was higher in France (17%)
than in the United States (<1%) or Belgium (11%) (2,28).
Methods for characterization of the species vary by coun-
try and by laboratory within a country (29,30). In France,
CNRCH routinely characterizes the species using a combi-
nation of phenotypic and molecular methods (specific
PCR) with verification of discrepant results (22). In some
other countries, Campylobacter are not routinely charac-
terized at the species level and could be incorrectly identi-
fied as C. jejuni or Campylobacter spp. This may account
for an underestimation of species other than C. jejuni in
some countries and therefore some distortion of the pro-
portion of antimicrobial drug resistance by species. In
France, the high proportion of C. coli isolates is probably
real, as an increasing proportion of C. coli is colonizing
broilers (31). This trend may be related to the use of differ-
ent isolation and identification methods, to a recent
increase in the ratio of C. coli to C. jejuni, or both. The ban
of antimicrobial growth promoters and of animal
protein–based feed may have influenced the digestive bac-
terial flora equilibrium of chickens. Udayamputhoor et al.
showed that the ceca of birds that receive plant
protein–based feed are less likely to be colonized with C.
jejuni than the ceca of birds that receive other types of feed
(32). Another hypothesis is that because 100% of pigs are
colonized by C. coli in France, the proximity of pig and
poultry farms in the main producing regions may result in
cross-contamination. However, this explanation is unlike-
ly because C. coli strains isolated from broilers and pigs
had different antimicrobial resistance patterns, and C. coli
poultry strains clustered separately from those of porcine
origin (33). Nonetheless, strains may undergo different
Resistance to ampicillin is of clinical interest because
this drug may be used for the treatment of severe
Campylobacter infections. The proportion of resistance to
ampicillin was higher among patients who did not travel
than among patients who did and in children <15 years. In
addition, resistance of Campylobacter isolates in humans
did not follow the same patterns over time as resistance in
broiler and porcine isolates. These results suggest that
resistance to ampicillin is more frequently domestically
acquired and may be related to the use of ampicillin in
human therapy because ampicillin is widely prescribed for
infections in children.
262Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 2, February 2007
Figure 3. Resistance of human Campylobacter spp. isolates to
antimicrobial agents, France, 1986-2004.
Figure 4. Quinolone resistance of human Campylobacter jejuni
and C. coli; France, 1986–2004.
Nalidixic acid resistance increased 5-fold from 1990
(5.3%) to 2004 (26.3%), consistent with trends observed in
other countries (16,17). The use of fluoroquinolones in
animal feed was approved in Europe in 1990. Studies have
shown the development of ciprofloxacin-resistant
Campylobacter in treated chickens and the spread of
ciprofloxacin-resistant Campylobacter from animal food
sources to humans (17,34,35). Australia, where fluoro-
quinolones have never been licensed for use in food-pro-
ducing animals, did not experience fluoroquinolone
resistance in human Campylobacter isolates (36).
The high proportions of resistance to nalidixic acid
and ciprofloxacin in broilers and pigs are consistent with
the findings of Desmonts et al. in France (31). In this study,
quinolone and fluoroquinolone resistance increased
between 1992–1996 and 2001–2002 among isolates from
standard chicken flocks, while resistance remained low for
free-range flock isolates. In France, antimicrobial growth
promoters have never been authorized in the production of
free-range chickens, contrary to standard methods of pro-
duction of chicken flocks, and antimicrobial therapy is
From 2002 to 2004, ciprofloxacin resistance dropped
substantially in C. jejuni isolated from broilers; nalidixic
acid resistance decreased as well, although not signifi-
cantly. The decrease in broilers may be related to the
restriction in the use of fluoroquinolones in animal feed
after the 1999 EU recommendation. Similarly, in
Denmark, resistance to macrolides of C. coli declined
after the prophylactic and growth-promoting use of
macrolides was banned (37). However, the decrease in
ciprofloxacin resistance occurred 2–3 years after the EU
recommendation, which suggests that EU recommenda-
tions were not followed immediately by application or,
alternatively, that the effect of the restriction in the use of
fluoroquinolones in animal feed is not immediate.
Unfortunately, no resistance data in broilers and pigs were
available before 1999, which is a limitation to interpret
recent trends in relation to the EU recommendations.
According to the French food security agency (AFSSA),
global sales of antimicrobial agents decreased consistent-
ly from 2001 through 2002, but information on species-
specific consumption was not available (38). Specific data
from veterinary prescriptions and livestock consumption
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 2, February 2007 263
Campylobacter Antimicrobial Drug Resistance, France
are necessary to quantify the amount of antimicrobial
agents consumed by animals.
C. jejuni nalidixic acid and ciprofloxacin resistance
decreased concomitantly in humans and broilers from
2002 to 2004. Because the decrease was less pronounced
in humans than in broilers, a longer period is needed to
detect an effect of the restriction in the use of antimicrobial
agents in animal feeds or resistance may be also related to
other exposure. Fluoroquinolones are the first drugs of
choice for the empiric treatment of human diarrhea or
prophylactic treatment associated with travel in France and
may be responsible for a part of resistance in humans (39).
However, >80% of patients infected with a ciprofloxacin-
resistant strain did not travel to a foreign country before
onset of illness, which indicates that a substantial propor-
tion of fluoroquinolone resistance was domestically
acquired (40). The resistance rate to ciprofloxacin was not
higher in adults compared with children, as could be
expected if treatment of cases was contributing to resist-
ance (39), because fluoroquinolone treatment is not used in
children ≤15 years of age.
In contrast to C. jejuni, we observed no decrease in
quinolone and fluoroquinolone resistance in C. coli in
pigs, broilers, or human isolates. The use of these antimi-
crobial agents in pigs may not have changed, and a part of
human C. coli infection may be related to other sources.
Alternatively, unknown mechanisms could be implicated
in C. coli resistance, such as a high number of point
Our study has several limitations. Laboratories partic-
ipate voluntarily in the surveillance network, which may
result in a selection of strains that is not representative of
the general population. However, all districts of mainland
France were included. In addition, this limitation, if it
exists, may not affect antimicrobial drug resistance
because participating laboratories routinely screen stools
for Campylobacter and send all their isolates to CNRCH.
Since the laboratory network was extended to private and
additional hospitals laboratories in 2002, this may have
had an effect on the trends in resistance. However, trends
of human antimicrobial susceptibility were analyzed
exclusively among strains from hospital laboratories from
1986 to 2004. In addition, characteristics of
Campylobacter isolates sent to CNRCH did not change for
age, sex, seasonality, and species after the network exten-
sion in 2002 (20,21). Comparison of human and animal
data was not based on a continuum between human iso-
lates and contaminated food consumption (isolates from
retail chicken). However, broiler chicken and pig data
were representative of French livestock and were consis-
tent with those of another recent survey done in France
The extension of the surveillance of human
Campylobacter allowed the epidemiologic characteristics
of Campylobacter infections that occurred in the general
French population to be better understood. Campylobacter
resistance to antimicrobial agents increased to a high level
among humans in France from 1990 through 2004.
Comparison of antimicrobial resistance patterns in
humans, broilers, and pigs from 1999 to 2004 showed sim-
ilar patterns of quinolone and fluoroquinolone resistance
for C. jejuni isolates from broilers and humans. These
results suggest that a limitation of the use of fluoro-
264 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 2, February 2007
Figure 5. Resistance of Campylobacter jejuni and C. coli to nalidix-
ic acid and ciprofloxacin in humans, broilers, and pigs, France,
1999–2004. Human strains were tested with ciprofloxacin since
2000. Strains isolated from poultry and pigs in 1999 and 2000
were tested with enrofloxacin, strains isolated between 2001 and
2004 were tested with ciprofloxacin.
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 2, February 2007265
quinolones in broilers may reduce fluoroquinolone resist-
ance of Campylobacter in humans. Other studies, howev-
er, are needed to further quantify the effect of restricted use
of antimicrobial drugs in animals on bacterial resistance in
human isolates. Ongoing national surveillance of
Campylobacter in humans, livestock, and animal feeds at
the retail level and antimicrobial susceptibility testing are
necessary to evaluate the effects of implementing
European policies. Further research is also needed to bet-
ter understand the relationship between antimicrobial use
in animals and humans and bacterial resistance in humans.
We thank the private community and public hospital labora-
tories that participated in the national surveillance of
Campylobacter infections in humans by sending their isolates to
This study was conducted in collaboration between the
Centre National de Référence des Campylobacter and
Helicobacter, AFSSA, and l’Institut de veille sanitaire in France
as part of their routine activity.
Dr Gallay is an epidemiologist in the unit of foodborne dis-
eases at the Institut de Veille Sanitaire, Saint Maurice, France.
She directs the program on Campylobacter infections and food-
borne viruses in France. Her research interests also include food-
borne and waterborne outbreaks.
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Address for correspondence: Anne Gallay, Institut de Veille Sanitaire,
Département des maladies infectieuses 12, rue du Val d’Osne 94 415
Saint Maurice, France; email: email@example.com
266Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 2, February 2007