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. 2003 Dec;47(12):3825–3830. doi: 10.1128/AAC.47.12.3825-3830.2003

Antimicrobial Resistance in Campylobacter jejuni and Campylobacter coli Strains Isolated in 1991 and 2001-2002 from Poultry and Humans in Berlin, Germany

Petra Luber 1,*, Jutta Wagner 2, Helmut Hahn 2, Edda Bartelt 1
PMCID: PMC296193  PMID: 14638490

Abstract

The susceptibilities of 430 Campylobacter jejuni strains and 79 C. coli strains to six antimicrobial agents were tested and analyzed. The two sets of strains originated from retail market chicken and turkey samples and from humans, respectively, in Berlin, Germany. Two groups of isolates, one dating from 1991 and the other dating from 2001-2002, were tested. Of the Campylobacter sp. isolates recovered from humans in 2001-2002, 45.1% were resistant to ciprofloxacin, 37.8% were resistant to tetracycline, 12.8% were resistant to ampicillin, and 50.0% were resistant to trimethoprim-sulfamethoxazole. All isolates were susceptible to gentamicin, while the overall rate of resistance to erythromycin was 6.1%. During the 10 years between the two sampling times, the rates of resistance to ciprofloxacin (P < 0.001), ampicillin (P = 0.035), and tetracycline (P = 0.01) increased significantly among strains isolated from humans. Furthermore, among human C. coli strains the rate of resistance to erythromycin rose from 7.1% in 1991 to 29.4% in 2001-2002. In comparison, Campylobacter sp. isolates from poultry already had high rates of resistance in 1991. Different rates of resistance to tetracycline among isolates from chickens and turkeys suggested the development of resistance during antimicrobial treatment in food animals. Thus, discrepancies in the antimicrobial resistance rates among Campylobacter isolates originating from poultry and humans support the hypothesis that at least some of the resistant Campylobacter strains causing infection in humans come from sources other than poultry products.

Infections with Campylobacter spp., particularly Campylobacter jejuni and C. coli, are among the most common causes of bacterial diarrhea in humans worldwide (22, 33). Whereas most cases of enteritis do not require treatment, as they are of short duration, clinically mild, and self-limiting, antimicrobial treatment is necessary for systemic Campylobacter infections, Campylobacter infections in immunosuppressed patients, and severe or long-lasting Campylobacter infections. Under these circumstances, erythromycin or fluoroquinolones are often recommended (2). Campylobacter infections usually occur as sporadic cases following the ingestion of improperly handled or cooked food.

Campylobacterioses are zoonotic diseases; and domestic animals such as poultry, pigs, and cattle may act as reservoirs for Campylobacter spp. As these may be transferred from animals to humans via food, the emergence of antimicrobial resistance in enteric Campylobacter spp. due to the use of antimicrobial agents in husbandry is a matter of concern (26, 34, 35, 37). Several case-control studies have identified the handling and consumption of poultry as a major risk factor for Campylobacter infections (8, 17, 32; J. Neimann, J. Engberg, K. Molbak, and H. C. Wegener, Proc. 4th Weltkongr. Lebensmittelinfektionen Intoxikationen, 1998). It is therefore important to know whether resistant Campylobacter strains can be isolated from foodstuffs of poultry origin, e.g., chicken and turkey meat, and whether these bacteria can be transferred to humans and cause infections in humans.

This study was conducted in order to compare the occurrence of antimicrobial resistance among C. jejuni and C. coli strains isolated from humans and from chicken and turkey food samples in one region of Germany. Some of the strains analyzed were isolated in 1991 and stored in a culture collection. A second set of strains was isolated in 2001-2002. Comparison of the resistance rates of both groups enabled us to study the development of antimicrobial resistance in this pathogen over a 10-year period.

MATERIALS AND METHODS

Sampling and bacterial isolates.

Poultry food samples were purchased at the retail level in Berlin, Germany. Besides different meat samples (breasts, drumsticks, wings), avian organs such as the liver, stomach, and heart were also sampled, as these represent the broad range of poultry products regularly consumed by German consumers. Isolation of Campylobacter spp. from foods was performed in general accordance with the ISO 10272 guideline (15). Thermophilic Campylobacter spp. were isolated from poultry meat samples by selective enrichment in Preston broth (5) for 24 h at 42°C in a microaerobic atmosphere (approximately 5% O2, 10% CO2, 85% N2). One loopful (10 μl) of broth was transferred to Preston agar (CM 67 plus selective supplements SR 117 and SR 48; Oxoid GmbH, Wesel, Germany). The agar plates were incubated at 42°C for 2 days in a microaerobic atmosphere and were examined for typical Campylobacter sp. colonies. Human isolates originated from patients with diarrhea in Berlin and were isolated by standard laboratory methods (18). One presumptive Campylobacter sp. isolate from each selective agar plate was identified to the species level by phase-contrast microscopy (characteristic morphology and motility), Gram staining, catalase and oxidase production, growth at 25 and 43°C, indoxyl acetate hydrolysis (27), hippurate hydrolysis, and susceptibility to nalidixic acid and cephalothin. All isolates were stored at −80°C in a freezer by using the Microbank system (PRO-LAB Diagnostics, Cheshire, United Kingdom). C. jejuni ATCC 33560 and C. coli ATCC 33559 were used as control strains.

The Campylobacter group from 1991 consisted of 252 isolates. A total of 139 Campylobacter spp. had been isolated from chicken meat samples, and 31 had originated from turkey meat samples. Furthermore, 82 isolates from human infections which had occurred in 1991 and 1992 in Berlin were investigated. From September 2001 to April 2002, poultry food samples were randomly obtained from selected retail shops in Berlin in order to generate a comparable group of Campylobacter sp. strains. Isolates of human origin were collected during the same time period in a clinical setting and from two medical laboratories. The second group sampled encompassed 257 isolates, of which 136 were from chickens, 39 were from turkeys, and 82 were from humans.

Antimicrobial susceptibility testing.

Susceptibility testing was performed by a broth microdilution method with Sensititre susceptibility plates (MCS Diagnostics BV, Swalmen, The Netherlands), as described recently (20). We tested the following antimicrobials at the indicated concentration ranges: erythromycin, tetracycline, and ciprofloxacin, 0.008 to 16 μg/ml; gentamicin and ampicillin, 0.015 to 32 μg/ml; and trimethoprim-sulfamethoxazole, 0.3 to 320 μg/ml.

Isolates were removed from the freezer and streaked onto Mueller-Hinton agar plates (CM 337; Oxoid) with 5% sheep blood and were incubated for 48 h at 42°C in a microaerobic atmosphere.

Several Campylobacter colonies were transferred to a tube with 5 ml of Mueller-Hinton broth (CM 405; Oxoid) to produce concentrations of approximately 5 to 6 log CFU/ml. This preculture was incubated for 24 h at 37°C in a MACS VA500 microaerophilic workstation incubator (Don Whitley Scientific Ltd., Shipley, United Kingdom) in a microaerophilic atmosphere consisting of 5% O2, 10% CO2, and 85% N2. For preparation of the test inoculum, 0.15 ml of the preculture was transferred to 10 ml of Mueller-Hinton broth, which resulted in a suspension of 6 to 7 log CFU/ml. Each well of the Sensititre susceptibility microtiter plates was filled with 100 μl of suspension, and the plates were sealed with an anaerobic-microaerobic film (JPD MO5660; Sensititre) and incubated in the MACS VA500 incubator at 37°C under microaerobic conditions. Test results were evaluated 24 h later. The Campylobacter control strains were included in each batch of broth microdilution tests. The MIC quality control limits for C. jejuni ATCC 33560 and C. coli ATCC 33559, which were used to control microdilution test performance, are given in Table 1. Additionally, Table 1 provides the recently issued NCCLS approved quality control ranges for C. jejuni ATCC 33560 for susceptibility testing of campylobacters by agar dilution (12, 25). Each lot of Mueller-Hinton broth was controlled according to NCCLS guideline M6-A (23) with Staphylococcus aureus ATCC 29213, Enterococcus faecalis ATCC 29212, Escherichia coli ATCC 25922, and Pseudomonas aeruginosa ATCC 27853.

TABLE 1.

MIC quality control limits used for control of microdilution test performance and MIC quality control ranges approved by NCCLS for susceptibility testing of Campylobacter spp. by agar dilution (reference method)

Agenta MIC quality control limits (μg/ml) for microdilution test performance
MIC quality control ranges (μg/ml)b approved by NCCLS (agar dilution) for C. jejuni ATCC 33560
C. coli ATCC 33559 C. jejuni ATCC 33560
ERY 2.0-8.0 1.0-4.0 1.0-8.0
GEN 0.25-1.0 1.0-4.0 0.5-4.0
AMP 4.0-16.0 1.0-4.0 NAc
CIP 0.5-2.0 0.25-1.0 0.125-1.0
TET 0.5-2.0 0.25-1.0 1.0-4.0
SXT 1/19-4/76 2/38-8/152 NA
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a

ERY, erythromycin; GEN, gentamicin; AMP, ampicillin; CIP, ciprofloxacin; TET, tetracycline; SXT, trimethoprim-sulfamethoxazole.

b

Tentative agar dilution quality control ranges approved by the NCCLS VAST subcommittee.

c

NA, no data available.

The following NCCLS MIC interpretive standards for members of the family Enterobacteriaceae (for erythromycin, the MIC interpretive standard of Staphylococcus spp. was used) (24) were used as breakpoints for Campylobacter resistance: for gentamicin and tetracycline, ≥16 μg/ml; for erythromycin, ≥8 μg/ml; for ampicillin, ≥32 μg/ml; for ciprofloxacin, ≥4 μg/ml; and for trimethoprim-sulfamethoxazole, ≥4/76 μg/ml.

Statistical analysis.

Statistical analysis was performed with SPSS (version 11.0) software. The results are presented in Table 2. The MIC ranges, the MICs at which 50% of the isolates are inhibited (MIC50s), the MIC90s, and the percentage of resistant isolates were calculated separately for each species and by origin.

TABLE 2.

Antimicrobial susceptibility testing results for 430 C. jejuni and 79 C. coli isolates and six antimicrobial agents

Agent, species, and yr Origin No. of isolates MIC (μg/ml)
% Resistant isolates
Range
MIC50 MIC90
Minimum Maximum
Erythromycin
    C. jejuni
        1991 Chicken 121 0.25 >16 1 2 2.5
Turkey 26 0.25 >16 1 4 3.8
Human 68 0.5 >16 1 2 1.5
        2001 Chicken 119 0.12 >16 1 2 0.8
Turkey 31 0.25 4 0.5 2 0
Human 65 0.25 2 1 2 0
    C. coli
        1991 Chicken 18 0.25 >16 1 8 5.6
Turkey 5 1 4 1 NDa 0
Human 14 0.25 >16 1 >16 7.1
        2001 Chicken 17 0.5 >16 2 16 5.9
Turkey 8 0.5 8 2 ND 12.5
Human 17 0.5 >16 2 >16 29.4
Gentamicin
    C. jejuni
        1991 Chicken 121 0.25 2 1 2 0
Turkey 26 0.5 2 1 2 0
Human 68 0.5 2 1 2 0
        2001 Chicken 119 0.25 2 1 1 0
Turkey 31 0.5 2 1 1 0
Human 65 0.5 4 1 2 0
    C. coli
        1991 Chicken 18 0.5 1 1 1 0
Turkey 5 0.12 2 1 ND 0
Human 14 1 4 1 4 0
        2001 Chicken 17 0.5 2 1 2 0
Turkey 8 0.5 1 1 ND 0
Human 17 0.25 2 1 2 0
Ampicillin
    C. jejuni
        1991 Chicken 121 0.25 >32 4 32 19.0
Turkey 26 0.25 >32 4 >32 19.2
Human 68 0.25 >32 4 32 8.8
        2001 Chicken 119 0.5 >32 4 >32 20.2
Turkey 31 0.5 >32 4 >32 38.7
Human 65 0.25 >32 4 >32 23.1
    C. coli
        1991 Chicken 18 0.5 16 4 16 0
Turkey 5 2 8 4 ND 0
Human 14 0.25 8 4 8 0
        2001 Chicken 17 1 >32 8 >32 23.5
Turkey 8 4 >32 8 ND 25.0
Human 17 1 8 4 8 0
Ciprofloxacin
    C. jejuni
        1991 Chicken 121 0.12 >16 0.5 >16 31.4
Turkey 26 0.12 >16 0.5 >16 30.8
Human 68 0.06 >16 0.25 1 5.9
        2001 Chicken 119 0.06 >16 0.5 >16 42.0
Turkey 31 0.12 >16 0.5 >16 29.0
Human 65 0.06 >16 1 >16 46.2/PICK>
    C. coli
        1991 Chicken 18 0.12 2 0.25 2 0
Turkey 5 0.25 2 1 ND 0
Human 14 0.06 0.5 0.25 0.5 0
        2001 Chicken 17 0.12 >16 16 >16 70.6
Turkey 8 0.06 >16 8 ND 50.0
Human 17 0.12 >16 0.5 >16 41.2
Tetracycline
    C. jejuni
        1991 Chicken 121 0.03 >16 0.25 >16 17.4
Turkey 26 0.06 >16 0.5 >16 34.6
Human 68 0.06 >16 0.12 >16 16.2
        2001 Chicken 119 0.06 >16 0.12 >16 19.3
Turkey 31 0.03 >16 0.5 >16 38.7
Human 65 0.03 >16 0.5 >16 38.5
    C. coli
        1991 Chicken 18 0.06 >16 0.12 >16 11.1
Turkey 5 16 >16 >16 ND 100.0
Human 14 0.06 >16 0.25 >16 35.7
        2001 Chicken 17 0.06 >16 >16 >16 58.8
Turkey 8 0.06 >16 >16 ND 62.5
Human 17 0.06 >16 0.5 >16 35.3
Trimethoprim-sulfamethoxazole
    C. jejuni
        1991 Chicken 121 3.5 >320 40 320 46.3
Turkey 26 10 320 80 320 57.7
Human 68 10 >320 80 320 61.8
        2001 Chicken 119 2.5 >320 80 >320 54.6
Turkey 31 5 320 40 320 32.3
Human 65 10 >320 40 320 47.7
    C. coli
        1991 Chicken 18 10 320 40 320 33.3
Turkey 5 40 160 80 ND 60.0
Human 14 10 >320 160 >320 71.4
        2001 Chicken 17 10 >320 40 >320 47.1
Turkey 8 10 160 20 ND 25.0
Human 17 5 >320 80 >320 58.8
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a

ND, not determined.

For each antimicrobial agent, the resistance rates for all Campylobacter spp. were calculated for each origin (chicken, turkey, or human). The chi-square test (P < 0.05 indicated significant; P < 0.01 indicated highly significant) was used to detect the significance of the developments over the 10-year period between the two sampling times. Data for C. coli were tested by Fisher's exact two-tailed test because of the low numbers.

In addition, the resistance rates for each sampling year were analyzed by the chi-square test to determine whether significant differences existed between the three origins.

RESULTS

The results of antimicrobial susceptibility testing, which were conducted separately for each agent, species, origin, and sampling period, are summarized in Table 2. The Campylobacter sp. isolates were sorted by origin, and the rates of resistance to each antimicrobial agent and by sampling time were calculated. The resistance rates over the 10-year period were investigated for significant differences (Table 3). Predominantly, the Campylobacter isolates of human origin showed significant increases in rates of resistance to ampicillin, ciprofloxacin, and tetracycline. When the rates of resistance of Campylobacter sp. isolates from different origins in 1991 were compared, isolates of human origin expressed significantly less resistance to ciprofloxacin (P < 0.001) than those of poultry origin, whereas no differences were found among the isolates of different origins recovered in 2001-2002. Campylobacter spp. of turkey origin were resistant to tetracycline significantly (P = 0.002) more often in 1991. Campylobacter spp. recovered from chicken products in 2001-2002 displayed significantly (P = 0.024) less resistance to tetracycline than those of turkey or human origin.

TABLE 3.

Rates of resistance of Campylobacter spp. to five antimicrobial agents by origin in 1991 and 2001-2002

Agenta Originb No. of isolates (1991/2001) % of resistant strains in:
Significance for increasing resistance over 10 yrb
1991 2001
ERY Chicken 139/136 2.9 1.5 NS
Turkey 31/39 3.2 2.6 NS
Human 82/82 2.4 6.1 NS
AMP Chicken 139/136 16.5 20.6 NS
Turkey 31/39 16.1 35.9 NS
Human 82/82 7.3 12.8 0.035c
CIP Chicken 139/136 27.3 45.6 0.002d
Turkey 31/39 25.8 33.3 NS
Human 82/82 4.9 45.1 <0.001d
TET Chicken 139/136 16.5 24.3 NS
Turkey 31/39 45.2 43.6 NS
Human 82/82 19.5 37.8 0.01c
SXT Chicken 139/136 44.6 53.7 NS
Turkey 31/39 58.1 30.8 0.02e
Human 82/82 63.4 50.0 NS
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a

ERY, erythromycin; AMP, ampicillin; CIP, ciprofloxacin; TET, tetracycline; SXT, trimethoprim-sulfamethoxazole.

b

Significance was determined by the chi-square test. NS, not significant.

c

Significant increase.

d

Highly significant increase.

e

Significant decrease.

C. jejuni was the predominant Campylobacter species recovered from infected humans and poultry. On average, 12.7% of the isolates from chickens, 18.3% of the isolates from turkeys, and 18.9% of the strains from humans belonged to the species C. coli. Species-specific resistance was found especially for erythromycin. None of the C. coli isolates recovered in 1991 were resistant to ampicillin or ciprofloxacin.

DISCUSSION

The lack of scientifically determined antibiotic breakpoint concentrations for Campylobacter spp. of human or veterinary origin is a general problem in the analysis of antimicrobial resistance in C. jejuni and C. coli. To separate susceptible from resistant Campylobacter strains, we chose to use NCCLS breakpoints for the family Enterobacteriaceae and Staphylococcus spp., as the vast majority of experimenters working with antimicrobial resistance in Campylobacter spp. do at present (1, 9, 10, 16, 19, 30). Other methods used internationally, e.g., the German Standard DIN 58940-4 (3), do have other breakpoint values for the Enterobacteriaceae. Breakpoints for resistance to ampicillin, gentamicin, and tetracycline are 1 log2 dilution lower, whereas the breakpoint for resistance to trimethoprim-sulfamethoxazole is about 1 dilution higher. However, for Campylobacter spp. all microbiological breakpoints in use are only assumptions, and clinical breakpoints do not exist. Thus, prediction of whether a pathogenic Campylobacter strain will respond to treatment with an appropriate antibiotic is not possible at present (31). Nevertheless, the arbitrarily set breakpoints enable us to study the emergence of antimicrobial resistance in members of this genus.

In correspondence with the data reported from studies from other countries over the past 5 years (10, 19, 28, 29, 36), antimicrobial sensitivity testing of German human Campylobacter spp. isolated in 2001-2002 revealed high rates of resistance to the beta-lactam ampicillin, quinolones, and tetracycline, while rates of resistance to erythromycin were low. Comparison with the resistance status of human Campylobacter spp. 10 years earlier demonstrated significant increases in the rates of resistance to ciprofloxacin (P < 0.01) as well as ampicillin and tetracycline (P < 0.05) (Table 3). The Campylobacter sp. isolates from poultry food samples obtained at the retail level in the same region and over the same time frames displayed different rates of susceptibility to the antimicrobials tested. In particular, the rate of resistance to ciprofloxacin of human Campylobacter spp. in 1991 was significantly (P < 0.001) lower than that of strains of poultry origin. However, as our collection of isolates was not exactly collected in a systematic manner in 1991 and as the numbers of isolates per population (human, chicken, turkey) were not large enough to be representative, the causes for the differences in rates of resistance between isolates from humans and poultry cannot be explained factually.

Increases in the rates of resistance to ciprofloxacin among human Campylobacter spp. after licensing of enrofloxacin for veterinary use have been reported in several countries (14, 28, 30), and the development of ciprofloxacin-resistant C. jejuni in broilers treated with ciprofloxacin has been experimentally proven in The Netherlands (16). We analyzed Campylobacter sp. isolates from the two poultry species separately, because raising of broilers and turkeys in an industrial production setting is characterized by several peculiarities; e.g., the average slaughter age of broiler flocks is 35 days, whereas turkey flocks are slaughtered after a minimum of 18 to 21 weeks (13). Thus, the probability that Campylobacter spp. from turkeys have been in contact with antimicrobials is much higher. Moreover, different antimicrobials are used to treat both avian species. For example, tetracycline is extensively used in turkey production (6) but not in broiler production. Indeed, we found different rates of resistance among the Campylobacter strains isolated from the two poultry products (Table 3). Most striking were the high rates of resistance to tetracycline among Campylobacter spp. from turkeys. In 1991, 45.2% of isolates from turkeys but only 16.5% of those from chickens were resistant to tetracycline (P = 0.002). In 2001-2002, the rate of resistance to tetracycline among Campylobacter spp. from chicken products had increased to 24.3%, but it was still significantly (P = 0.024) lower than that among isolates from turkey products (43.6%). In a recent publication from a Danish group studying antimicrobial resistance in zoonotic bacteria (4), Campylobacter isolates from turkeys also expressed much higher rates of resistance to tetracycline than those from chickens. In comparison, Ge et al. (11) found no differences in the rates of resistance to tetracycline among Campylobacter spp. from retail chicken or turkey, but described significantly higher rates of resistance to ciprofloxacin and erythromycin among isolates from retail turkey. Presumably, for at least some antimicrobial substances there is evidence of resistance induction in Campylobacter spp. from animals receiving treatment as part of animal husbandry practices.

There is evidence that C. jejuni and C. coli express different propensities to become resistant to macrolides (1, 11). In general, the rates of resistance to erythromycin among Campylobacter spp. seemed to be low in our study, but when we started to look at the data for the two species separately, a large percentage of erythromycin-resistant C. coli isolates from humans was identified (Table 2). Among the isolates recovered in 2001-2002, we found that 29.4% of the human C. coli isolates were resistant to erythromycin, whereas all C. jejuni isolates from humans were susceptible to the macrolide. As almost one-fifth (18.9%) of human Campylobacter spp. in our subset of strains belonged to the species C. coli, these findings should be regarded as relevant for antibiotic treatment of campylobacterioses in humans. The low numbers of erythromycin-resistant C. coli isolates found in poultry products give rise to the question of whether other important sources for human infections with this species exist. Compared with poultry, in which C. jejuni is the dominant species, the majority of strains originating from pigs belong to C. coli. Several investigators have found high rates of macrolide resistance among C. coli isolates from swine (1, 7, 21). Thus, pigs are likely to be a source for infections with erythromycin-resistant C. coli.

In summary, the rates of antimicrobial resistance among Campylobacter isolates increased strongly over the 10-year period from 1991 to 2001-2002. Resistance rates differed according to the species of the organism and the source of isolation. Therefore, in order to monitor trends in antimicrobial resistance among Campylobacter isolates, isolates should be differentiated at the species level. We found evidence for the development of resistance in Campylobacter spp. in poultry receiving antimicrobial agents as part of animal husbandry practices, but the extent to which the transmission of resistant Campylobacter spp. via poultry products takes place remains unclear. Our findings suggest that at least some of the resistant Campylobacter strains causing infections in humans come from sources other than poultry products.

Acknowledgments

This study was part of the FV 1339-134 research program, “Erarbeitung von Methoden zur Identifizierung und Isolierung von Campylobacter und deren Resistenzbestimmung,” supported by the German Federal Ministry of Consumer Protection, Food and Agriculture.

We thank Petra Vogt for excellent technical assistance. We also thank M. Chahin (Labor 28, Berlin, Germany) and I. Schulz (ILAT, Berlin, Germany) for kindly providing strains of human origin. Special thanks go to Elke Genschow for help with the statistical analysis.

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