JAC Advance Access originally published online on March 13, 2006
Journal of Antimicrobial Chemotherapy 2006 57(5):908-913; doi:10.1093/jac/dkl080
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Antimicrobial susceptibility of clinical isolates of non-jejuni/coli campylobacters and arcobacters from Belgium
1 National Reference Centre for Enteric Campylobacter, Saint-Pierre University Hospital, Brussels, Belgium; 2 Infectious Diseases Epidemiological Unit, Public Health School, Free University of Brussels, Brussels, Belgium; 3 Department of Microbiology, Saint-Pierre University Hospital, Brussels, Belgium; 4 Department of Veterinary Public Health, Faculty of Veterinary Medicine, Ghent University, Ghent, Belgium; 5 Department of Microbiology, Brugmann University Hospital, Brussels, Belgium; 6 Department of Human Ecology, Vrije Universiteit Brussel, Brussels, Belgium
* Correspondence address. Department of Microbiology, Saint-Pierre University Hospital, Rue Haute 322, B-1000 Brussels, Belgium. Tel: +32-2-535-4530; Fax: +32-2-535-4656; E-mail: olivier_vandenberg{at}stpierre-bru.be
Received 20 November 2005; returned 20 December 2005; revised 29 January 2006; accepted 20 February 2006
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Abstract |
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Objectives: To determine the susceptibility of non-jejuni/coli campylobacters and arcobacters isolated from diarrhoeal stool specimens in Belgium.
Methods: The MICs were determined using Etest for six antimicrobial agents including ampicillin, erythromycin, nalidixic acid, ciprofloxacin, gentamicin and tetracycline for the most frequently isolated non-jejuni/coli campylobacter and arcobacter strains in two University Hospital laboratories between 1995 and 2005.
Results: In total, 85 Campylobacter upsaliensis, 20 Campylobacter concisus, 11 Campylobacter fetus, 61 Arcobacter butzleri and 10 Arcobacter cryaerophilus isolates were tested. Most C. upsaliensis strains were susceptible to ampicillin (100%), gentamicin (100%), ciprofloxacin (94.1%) and tetracycline (100%), whereas 11.8 and 12.9% were resistant to nalidixic acid and erythromycin, respectively. For A. butzleri, 78.7% of isolates were susceptible to ampicillin and erythromycin. Most A. butzleri isolates were susceptible to ciprofloxacin (96.7%), nalidixic acid (82.0%), gentamicin (100%) and tetracycline (100%). All C. concisus strains were fully susceptible to ampicillin and tetracycline, but 5% of them were resistant to gentamicin, ciprofloxacin and erythromycin. Nearly all C. fetus and A. cryaerophilus strains were susceptible to erythromycin but the results should be interpreted with caution since only a small number of strains were tested.
Conclusions: Fluoroquinolones should be considered in the treatment of severe C. upsaliensis and A. butzleri infection. When clinically indicated, erythromycin remains the first choice for the treatment of intestinal campylobacteriosis caused by C. concisus and C. fetus.
Keywords: diarrhoea , resistance , Etest , Campylobacter upsaliensis , Campylobacter concisus
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Introduction |
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Campylobacter jejuni and Campylobacter coli are common causes of bacterial diarrhoea in humans worldwide.1,2 Apart from C. jejuni and C. coli, Campylobacter upsaliensis, Campylobacter fetus ssp. fetus, Campylobacter curvus and Campylobacter concisus have emerged as potential human enteric pathogens.3
However, the genus Campylobacter has undergone several taxonomic changes over the past decade, including the move of a number of species to either the new genus Arcobacter or the genus Helicobacter. Arcobacter butzleri and Arcobacter cryaerophilus have been associated with enteritis and occasionally bacteraemia in humans and animals.4,5 In the genus Helicobacter, Helicobacter fennelliae, Helicobacter pullorum and Helicobacter cinaedi have been increasingly isolated from diarrhoeal stools in both developing and industrialized countries.6
When the diagnosis of campylobacter infection is based exclusively upon classical bacteriological isolation on selective media, it is commonly observed that >95% of infections are caused by C. jejuni or C. coli, at least in industrialized countries.7 The contribution of other related species to diarrhoeal diseases is frequently underestimated due to the use of isolation and identification methods suitable only for C. jejuni and C. coli.
Several prevalence studies show that C. upsaliensis and C. concisus contribute significantly to the total campylobacter isolation rates in diarrhoeal patients in industrialized countries.8,9
By the application of our comprehensive isolation procedure for campylobacter species, which employs two selective media and a filtration method, we have previously reported a prevalence of non-jejuni/coli campylobacter of 0.53% in 67 599 stool specimens from 40 995 patients. This is a higher figure than that reported from other European countries.5
Non-jejuni/coli campylobacters also seem to be common in developing nations. In Thailand, they accounted for 18% of the campylobacter isolates obtained from children with diarrhoea, and in South Africa, Lastovica et al. found them in 12.0% of 19 535 stools also from children with diarrhoea.10,11
Diarrhoea caused by C. jejuni or C. coli is usually a self-limiting disease, though severity or duration of symptoms may necessitate antimicrobial therapy. In the latter case, the most commonly prescribed drugs are erythromycin or a fluoroquinolone such as ciprofloxacin.12 However, C. jejuni and C. coli readily acquire resistance to fluoroquinolones, which limits their use in the treatment of Campylobacter enteritis. Erythromycin resistance is acquired less readily; resistance rates of <5% are usual for C. jejuni but rates of up 80% have been reported in C. coli.12 Ampicillin, tetracycline, doxycycline and gentamicin are regarded as alternative drugs for treatment.13
Although many studies on the susceptibility patterns of C. jejuni or C. coli have been published, only scanty data are available on the antimicrobial resistance of other campylobacters and related organisms.
The aim of the present study was to determine, using the Etest method, the susceptibility to six antimicrobials of non-jejuni/coli campylobacter and arcobacter strains isolated from human diarrhoeal stool specimens in Belgium.
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Materials and methods |
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Strain collection and isolation
From January 1995 to June 2005, a total of 73 136 stool specimens from 42 287 patients submitted to the laboratory were routinely examined for arcobacters, campylobacters and helicobacters using two selective media and a filtration method. In brief, a faecal suspension (
1 g/mL in saline) was inoculated into Butzler's medium comprising Mueller–Hinton agar (Oxoid Ltd, Basingstoke, United Kingdom), 5% sheep blood and an antibiotic supplement: cefoperazone 30 mg/L, rifampicin 10 mg/L and amphotericin B 2 mg/L (Institute Virion, Rüschlikon, Switzerland).14 The plates were incubated for 48 h at 42°C in a microaerobic atmosphere (5% O2, 6% H2, 10% CO2 and 79% N2). The plates were examined daily for bacterial growth.
During the study period, the selective arcobacter culture method of de Boer was used.15 In brief, 0.5 g of stool was inoculated into an enrichment broth (Brucella broth, 5% laked horse blood and the antibiotic supplement consisting of piperacillin 75 mg/L, cefoperazone 25 mg/L, amphotericin B 10 mg/L, trimethoprim 20 mg/L and cycloheximide 100 mg/L) and incubated for 24 h at 25°C in the microaerobic atmosphere. After incubation, 40 µL of this enriched broth was inoculated onto arcobacter selective medium and the plates were then incubated for 3 days at 25°C in the microaerobic atmosphere and examined daily.
The membrane filtration method was performed as described by Lopez et al.16 Stool samples were diluted 1 : 5 in Brucella broth. Cellulose acetate filters, 50 mm in diameter and with a pore size of 0.45 µm, were placed on the surface of non-selective Mueller–Hinton agar plates containing 5% sheep blood. Eight drops of the faecal suspension were placed on top of the membrane and allowed to filter passively for 30 min at 37°C in air. The filters were then removed and the plates were incubated at 37°C in a microaerobic atmosphere for up to 10 days.
Identification of arcobacter, campylobacter and helicobacter species was performed using both morphological and biochemical characteristics, as recommended by Vandamme et al.17 Isolates were stored in skimmed milk at –70°C until further examination.
These cultures yielded non-jejuni/coli campylobacters and related organisms in 269 patients: C. upsaliensis, 39.0% (105 out of 269); A. butzleri, 30.1% (81 out of 269); Campylobacter concisus, 12.3% (33 out of 269); C. fetus, 5.2% (14 out of 269); and A. cryaerophilus, 4.5% (12 out of 269). Other species such as C. curvus, Campylobacter lari, H. pullorum, Campylobacter hyointestinalis and Campylobacter sputorum were found in small numbers (Figure 1).
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Antimicrobial susceptibility tests
The non-jejuni/coli campylobacter and arcobacter strains (one strain per patient) most frequently isolated during the study period were tested for antimicrobial susceptibility using the Etest method (AB Biodisk, Solna, Sweden). Because C. curvus, C. lari, H. pullorum, C. hyointestinalis and C. sputorum were found only sporadically, these species were not included in the present study.
Since Etest has been found to compare favourably with agar dilution methods, we chose this test for its ease of use in the routine testing of single isolates.18,19 The antibiotics tested were ampicillin, erythromycin, nalidixic acid, ciprofloxacin, gentamicin and tetracycline. Isolates were subcultured three times onto Columbia agar (Oxoid Ltd, Basingstoke, United Kingdom) containing 5% sheep blood for 24–72 h at 37°C in a microaerobic atmosphere before testing.
The inocula were adjusted to the turbidity of a 0.5 McFarland standard and plated on Mueller–Hinton agar supplemented with 5% sheep blood. Plates were incubated at 36°C for 48 h in a microaerobic atmosphere. The following control strains were used: Staphylococcus aureus ATCC 25923, S. aureus ATCC 29213, Escherichia coli ATCC 25922, C. jejuni ATCC 33560 and A. butzleri (LMG 10828). These strains were included in each run during the Etest.
The MIC was defined as the lowest concentration of an antimicrobial agent that completely inhibited visible growth, and was read at the point where the elliptical zone of inhibition intersected the MIC scale on the strip. Because standardized susceptibility data for campylobacter species are lacking, we described MIC50 and MIC90 as well as ranges and percentages of resistance of the six antibiotics tested.
The MIC50 and MIC90 represent the MICs that completely inhibited visible growth of 50% and 90% of the strains, respectively. Since the Clinical Laboratory Standards Institute (CLSI) recommendations do not include specific breakpoints for defining resistance in campylobacter species, the criteria used in our study for erythromycin and tetracycline were those of the CLSI for Staphylococcus species.20,21 For all other drugs, we used those for Enterobacteriaceae as described before by Englen et al.22 and by Luber et al.23 pending specific CLSI recommendations. The following resistance breakpoints were used in this study: ampicillin 
32 mg/L, ciprofloxacin 4 mg/L, tetracycline and gentamicin 16 mg/L, erythromycin 8 mg/L, nalidixic acid 32 mg/L (Table 1).
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The results of the antimicrobial susceptibility testing for 187 non-jejuni/coli campylobacter and arcobacter isolates (some isolates could not be recovered from storage) are shown in Table 1.
In the present study 12.9% (11 out of 85) of C. upsaliensis isolates were resistant to erythromycin, 5.9% (5 out of 85) to ciprofloxacin and 11.8% (10 out of 85) to nalidixic acid. The activity of nalidixic acid was lower than that of ciprofloxacin (MIC90 values of 4 and 0.13 mg/L, respectively). Strains resistant to ciprofloxacin were also resistant to nalidixic acid. All C. upsaliensis isolates tested were susceptible to ampicillin, tetracycline and gentamicin.
For A. butzleri, a high proportion of isolates were resistant to ampicillin (21.3%) and erythromycin (21.3%). Most A. butzleri isolates were susceptible to ciprofloxacin (96.7%), nalidixic acid (82.0%) and gentamicin (100%). Again, the activity of nalidixic acid was lower than that of ciprofloxacin (MIC90 values of 32 and 0.25 mg/L, respectively). Multidrug resistance to ampicillin, erythromycin and nalidixic acid was observed in 6.2% (5 out of 81) of A. butzleri strains. All A. butzleri isolates tested were susceptible to tetracycline.
Among the 20 isolates of C. concisus tested, 19 (95%) were susceptible to erythromycin and ciprofloxacin but 16 (80%) were resistant to nalidixic acid. The MIC90 values for nalidixic acid and ciprofloxacin were 32 and 0.25 mg/L respectively. All C. concisus isolates were susceptible to ampicillin (100%) and tetracycline (100%), but 5% of them were resistant to gentamicin.
For the 11 C. fetus and 10 A. cryaerophilus isolates, the results should be interpreted with caution since only a few were tested, but all of them were susceptible to ampicillin, gentamicin, erythromycin and tetracycline. We note that all C. fetus isolates were resistant to nalidixic acid but susceptible to ciprofloxacin, whereas all A. cryaerophilus isolates were susceptible to both antimicrobials.
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Discussion |
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Antimicrobial susceptibility patterns of C. jejuni and C. coli have been extensively studied in both developing and industrialized countries.12
To date, few studies have compared antimicrobial resistance in clinical isolates of non-jejuni/coli campylobacters and arcobacters. Susceptibility tests for campylobacter and arcobacter species are not standardized (there is no recommendation by the CLSI), so there is variability in the susceptibility reported. A number of different testing methods such as broth microdilution, disc diffusion and Etest have been used for campylobacters and arcobacters. In the present study, MICs for both non-jejuni/coli campylobacter and arcobacter species were determined using Etest.
In the present study, we found that 12.9% of the C. upsaliensis isolates, which is the most common species next to C. jejuni and C. coli among diarrhoeal patients, were resistant to erythromycin, the preferred antibiotic for campylobacter infection. Goossens et al.24 found a similar rate of 11.0% among 91 isolates of C. upsaliensis. On the other hand, like Patton et al.,25 we found that most C. upsaliensis isolates were susceptible to a wide range of antibiotics including fluoroquinolones, gentamicin and tetracycline. However in their study in the USA, Patton et al. reported that 15% (2 out of 13) of the C. upsaliensis were resistant to erythromycin, quite in line with our finding of 13%. Resistance to nalidixic acid was observed in 10 of the 85 isolates we tested, whereas 5.9% of them were resistant to ciprofloxacin. Within one dilution, the MIC50 and MIC90 observed for ciprofloxacin during our study were similar to those previously reported by Preston et al.26
At present, experience of antimicrobial treatment of C. upsaliensis infection is limited. There have been no controlled trials conducted of antibiotic treatment for C. upsaliensis-associated diarrhoea. Therefore, the place of antibiotic therapy in the treatment of infection caused by C. upsaliensis has yet to be defined.27
Among arcobacter isolates, both A. butzleri and A. cryaerophilus were found to be susceptible to ciprofloxacin and nalidixic acid. On the other hand, 21.3% of the A. butzleri isolates were resistant to ampicillin and erythromycin. These results are comparable to those of Atabay et al.,28 who found that all 39 A. butzleri broiler isolates were susceptible to aminoglycosides, nalidixic acid, enrofloxacin and tetracyclines, using a disc diffusion method. However in their study, one isolate was resistant to erythromycin and four showed intermediate resistance.
In another study on 30 environmental arcobacter isolates, Fera et al.29 showed that fluoroquinolones had a good activity against A. butzleri and A. cryaerophilus. These authors also reported high levels of resistance to macrolides. Recently, Houf et al.30 using the agar dilution test showed that human arcobacter strains display the same antibiotic resistance profiles as the strains isolated from poultry.
The low resistance rate to fluoroquinolones observed in the present study suggests that these drugs could be used for treating severe arcobacter enteritis. However, as for C. upsaliensis, experience of treatment of arcobacter infection with these antibiotics is limited, and due to the lack of controlled trials for antibiotic treatment, the place of such antibiotics in the treatment of infection by arcobacters has also yet to be defined.
All C. concisus and C. fetus isolates were fully susceptible to ampicillin, gentamicin and tetracycline, but 5% of C. concisus were resistant to ciprofloxacin and erythromycin.
Comparable results were obtained in Denmark by Aabenhus et al.,31 who reported resistance to ampicillin (2%), tetracycline (3%), ciprofloxacin (5%) and erythromycin (7%) in 109 C. concisus isolates tested using the Etest method. Recently Engberg et al.32 tested 43 C. concisus isolates and all of them were fully susceptible to all 11 antimicrobial agents tested, including ampicillin, gentamicin, tetracycline, erythromycin, ciprofloxacin and nalidixic acid. In several studies, C. concisus has been reported to be fully resistant to nalidixic acid.17 In the present study, 80% of C. concisus isolates were resistant to nalidixic acid, a similar figure to Van Etterijck et al.,33 who found 51% resistance also in Belgium. Concerning C. fetus, our results are comparable to those of Gaudreau et al.,34 who found that all the 45 strains tested were susceptible to ampicillin and erythromycin, although a few were resistant to gentamicin (2.2%), ciprofloxacin (6.7%) and tetracycline (24.4%). In 2003, Tremblay et al.35 reported that of 111 C. fetus isolates tested all were susceptible to ampicillin and gentamicin but 3% were resistant to ciprofloxacin and 34% resistant to tetracycline.
In conclusion, this study shows that fluoroquinolones should be considered in the treatment of severe C. upsaliensis and A. butzleri infection. However, the appearance of fluoroquinolone resistance in C. jejuni and C. coli suggests that acquired resistance might also compromise the treatment of illnesses caused by the former species.
When clinically indicated, erythromycin should still be recommended for the treatment of severe intestinal campylobacteriosis caused by C. concisus and C. fetus.
A controlled trial of antibiotic therapy for diarrhoea caused by non-jejuni/coli campylobacters and related organisms is needed to define resistance breakpoints and the place of antimicrobial drugs in such infections.
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There are no commercial or other associations that might pose a conflict of interest.
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Acknowledgements |
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We are grateful to Martin Skirrow, Roger Feldman and Sandra Ibekwem for their critical corrections. We would also like to thank the personnel of the Department of Microbiology for their daily technical assistance. The skilled technical assistance provided by Chantal Vandenborre is greatly appreciated. This work was supported in part by grants from the Foundation Vesale Research fellowship (foundation for medical research). This study was presented in part at the 11th International Congress on Infectious Diseases, Cancun, Mexico, 4–8 March 2004 (abstract P09.030) and at the 12th International Workshop on Campylobacter, Helicobacter and Related Organisms, Aarhus, Denmark, 6–10 September 2003 (abstract K-07).
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