- Email: [email protected]
First case of OXA-24-producing Acinetobacter baumannii in cattle from Reunion Island, France
ARTICLE IN PRESS International Journal of Antimicrobial Agents ■■ (2016) ■■–■■
Contents lists available at ScienceDirect
International Journal of Antimicrobial Agents j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / i j a n t i m i c a g
1
Q2 Letter to the Editor
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First case of OXA-24-producing Acinetobacter baumannii in cattle from Reunion Island, France Sir, Asymptomatic carriage of Acinetobacter baumannii has been identified in animals in Reunion Island, France [1,2]. The first study found 6.5% of pets sampled in veterinary clinics colonised with closely related A. baumannii assigned to sequence type 25 (ST25) [1], and another study identified a similar prevalence associated with high strain diversity [2]. These studies demonstrated the presence of A. baumannii outside the hospital setting on this island. Therefore, we wanted to explore other potential extrahuman reservoirs of A. baumannii in this area. The objective here was to report the results of a screening campaign performed on a sample of cattle to identify A. baumannii carriage on a farm on Reunion Island. On one day, the cattle heads inspected by a veterinarian on a single farm during routine examination were sampled by mouth swabbing. Swabs were inoculated in UTI agar medium (Oxoid Ltd., Basingstoke, UK), CHROMagar™ Acinetobacter agar medium (CHROMagar, Paris, France) and chromID™ BLSE agar medium (bioMérieux, Marcy-l’Étoile, France). The agar media were incubated for 48 h at 37 °C. Suspected A. baumannii colonies on culture were identified using a VITEK®2 system (bioMérieux) and by partial sequencing of the rpoB gene as reported previously [2]. Antimicrobial susceptibility was determined by the disk diffusion method according to the recommendations of the French Society for MiQ3 crobiology (http://www.sfm-microbiologie.org). Multilocus sequence typing (MLST) and determination of the presence of carbapenemaseencoding genes (blaOXA-23, blaOXA-24, blaOXA-58 and blaNDM-1) were performed as previously described [2]. From the 50 cattle heads of the farm, 6 were sampled. A. baumannii carriage was identified in five animals. Surprisingly, one isolate was resistant to carbapenems due to presence of the blaOXA-24 gene. All isolates remained susceptible to aminoglycosides, colistin, rifampicin and ciprofloxacin. The A. baumannii isolates were assigned to different STs: four to STs never identified previously (ST479, ST480, ST482 and ST587) and one to ST278. This is the first report of carbapenem-resistant A. baumannii isolated in cattle in France. This isolate belongs to a new ST (ST587). Carbapenem-resistant Acinetobacter spp. and A. baumannii have already been identified in cattle in France and Lebanon, respectively [3,4]. In those studies, the isolates recovered from animals produced OXA-23 or a combination of OXA-23 and OXA-58 enzymes. In the current study, the A. baumannii isolate produced OXA-24. Within the last years, OXA-24-like enzymes were more commonly detected among A. baumannii isolates from Southern Europe, but also from the USA and the UK. It is noteworthy that no carbapenemaseproducing A. baumannii had been isolated in our two preceding studies conducted in companion animals from Reunion Island.
One hypothesis for the presence of carbapenemase-producing A. baumannii in cattle could be the wide use of antibiotics in foodproducing animals that could be responsible for the selection of resistant bacteria, including carbapenemase-producing A. baumannii. For example, a recent study within the European Union and European Economic Area showed that a wide range of antimicrobial agents is used in these countries (i.e. tetracyclines, penicillins, macrolides, fluoroquinolones and others) [5]. A second interesting result is the diversity of the strains isolated in this study. Indeed, this is not consistent with the hypothesis of the spread of a unique strain from animal to animal, or with the presence of a unique strain in the environment of the farm that could have contaminated all of the animals. It is also noteworthy that the blaOXA-24 gene harboured by the carbapenem-resistant isolate did not disseminate to other A. baumannii isolates collected on the same cattle farm. These results are in accordance with our previous study conducted among pets from Reunion Island, with high strain diversity [2]. Overall, this study tends to confirm in livestock animals the result obtained in our preceding study conducted in pets, that A. baumannii is a micro-organism widely disseminated among animals living on Reunion Island. To our knowledge, this is also the first report of such A. baumannii strain diversity recorded from cattle living in the same environment. Further studies are needed to confirm these results. This study raises some questions: (i) what was the prevalence of A. baumannii carriage in the farm?; (ii) could this prevalence and strain diversity be recovered from all farms on Reunion Island?; and (iii) what could explain the strain diversity recorded in a few animals living in the same environment? Indeed, here the five A. baumannii isolates were assigned to different STs, among which four had never been described previously. This result suggests that a huge diversity of STs could be found in the cattle reservoir, maybe with isolates very different from those isolated in humans. One STs was already described, but has never been reported in the literature as isolated in humans or animals. Therefore, other investigations should be initiated to improve our understanding regarding the extrahospital transmission of these bacteria. Lastly, this first report of carbapenem-resistant A. baumannii in animals in France is a serious cause of concern.
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Acknowledgements
96 97 The authors thank the team of curators of the Institut Pasteur 98 (Paris, France) MLST system for importing novel alleles, profiles 99 and/or isolates at http://pubmlst.org/abaumannii/. 100 Funding: Financial support was provided by the Program ‘Appel Q4 101 à projet interne du CHU d’Angers, 2012’. 102 Competing interests: None declared. 103 Ethical approval: Information was given to the owner about the 104 study, and the consent of the owner was received. 105
http://dx.doi.org/10.1016/j.ijantimicag.2016.09.005 0924-8579/© 2016 Elsevier B.V. and International Society of Chemotherapy. All rights reserved.
Please cite this article in press as: Hélène PailhorièsMarie Kempf, Olivier Belmonte, Marie-Laure Joly-GuillouMatthieu Eveillard, First case of OXA-24-producing Acinetobacter baumannii in cattle from Reunion Island, France, International Journal of Antimicrobial Agents (2016), doi: 10.1016/j.ijantimicag.2016.09.005
ARTICLE IN PRESS Letter to the Editor / International Journal of Antimicrobial Agents ■■ (2016) ■■–■■
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References [1] Belmonte O, Pailhoriès H, Kempf M, Gaultier MP, Lemarié C, Ramont C, et al. High prevalence of closely-related Acinetobacter baumannii in pets according to a multicentre study in veterinary clinics, Reunion Island. Vet Microbiol 2014;170:446–50. [2] Pailhoriès H, Belmonte O, Kempf M, Lemarié C, Cuziat J, Quinqueneau C, et al. Diversity of Acinetobacter baumannii strains isolated in humans, companion animals, and the environment in Reunion Island: an exploratory study. Int J Infect Dis 2015;37:64–9. [3] Al Bayssari C, Dabboussi F, Hamze M, Rolain J-M. Emergence of carbapenemaseproducing Pseudomonas aeruginosa and Acinetobacter baumannii in livestock animals in Lebanon. J Antimicrob Chemother 2015;70:950–1. [4] Poirel L, Berçot B, Millemann Y, Bonnin RA, Pannaux G, Nordmann P. Carbapenemase-producing Acinetobacter spp. in cattle, France. Emerg Infect Dis 2012;18:523–5. [5] Catry B, Cavaleri M, Baptiste K, Grave K, Grein K, Holm A, et al. Use of colistincontaining products within the European Union and European Economic Area (EU/EEA): development of resistance in animals and possible impact on human and animal health. Int J Antimicrob Agents 2015;46:297–306.
Hélène Pailhoriès Marie Kempf * L’UNAM Université d’Angers, ATOMycA, Inserm Equipe Avenir, CRCNA, Inserm U892, 6299 CNRS, IRIS, CHU, Angers, France
Laboratoire de bactériologie, CHU Angers, Angers, France
132 133
Olivier Belmonte Laboratoire de bactériologie, CHU Félix Guyon, Saint-Denis, La Réunion, France
134 135 136
Marie-Laure Joly-Guillou Matthieu Eveillard L’UNAM Université d’Angers, ATOMycA, Inserm Equipe Avenir, CRCNA, Inserm U892, 6299 CNRS, IRIS, CHU, Angers, France Laboratoire de bactériologie, CHU Angers, Angers, France
137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152
* Corresponding author. Laboratory of Clinical Bacteriology, CHU Angers, 4 rue Larrey, 49000 Angers, France. Fax: +33 2 41 35 41 64. E-mail address: [email protected] (M. Kempf). 18 August 2016 15 September 2016
Please cite this article in press as: Hélène PailhorièsMarie Kempf, Olivier Belmonte, Marie-Laure Joly-GuillouMatthieu Eveillard, First case of OXA-24-producing Acinetobacter baumannii in cattle from Reunion Island, France, International Journal of Antimicrobial Agents (2016), doi: 10.1016/j.ijantimicag.2016.09.005
Contents lists available at ScienceDirect
International Journal of Antimicrobial Agents j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / i j a n t i m i c a g
1
Q2 Letter to the Editor
2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54
First case of OXA-24-producing Acinetobacter baumannii in cattle from Reunion Island, France Sir, Asymptomatic carriage of Acinetobacter baumannii has been identified in animals in Reunion Island, France [1,2]. The first study found 6.5% of pets sampled in veterinary clinics colonised with closely related A. baumannii assigned to sequence type 25 (ST25) [1], and another study identified a similar prevalence associated with high strain diversity [2]. These studies demonstrated the presence of A. baumannii outside the hospital setting on this island. Therefore, we wanted to explore other potential extrahuman reservoirs of A. baumannii in this area. The objective here was to report the results of a screening campaign performed on a sample of cattle to identify A. baumannii carriage on a farm on Reunion Island. On one day, the cattle heads inspected by a veterinarian on a single farm during routine examination were sampled by mouth swabbing. Swabs were inoculated in UTI agar medium (Oxoid Ltd., Basingstoke, UK), CHROMagar™ Acinetobacter agar medium (CHROMagar, Paris, France) and chromID™ BLSE agar medium (bioMérieux, Marcy-l’Étoile, France). The agar media were incubated for 48 h at 37 °C. Suspected A. baumannii colonies on culture were identified using a VITEK®2 system (bioMérieux) and by partial sequencing of the rpoB gene as reported previously [2]. Antimicrobial susceptibility was determined by the disk diffusion method according to the recommendations of the French Society for MiQ3 crobiology (http://www.sfm-microbiologie.org). Multilocus sequence typing (MLST) and determination of the presence of carbapenemaseencoding genes (blaOXA-23, blaOXA-24, blaOXA-58 and blaNDM-1) were performed as previously described [2]. From the 50 cattle heads of the farm, 6 were sampled. A. baumannii carriage was identified in five animals. Surprisingly, one isolate was resistant to carbapenems due to presence of the blaOXA-24 gene. All isolates remained susceptible to aminoglycosides, colistin, rifampicin and ciprofloxacin. The A. baumannii isolates were assigned to different STs: four to STs never identified previously (ST479, ST480, ST482 and ST587) and one to ST278. This is the first report of carbapenem-resistant A. baumannii isolated in cattle in France. This isolate belongs to a new ST (ST587). Carbapenem-resistant Acinetobacter spp. and A. baumannii have already been identified in cattle in France and Lebanon, respectively [3,4]. In those studies, the isolates recovered from animals produced OXA-23 or a combination of OXA-23 and OXA-58 enzymes. In the current study, the A. baumannii isolate produced OXA-24. Within the last years, OXA-24-like enzymes were more commonly detected among A. baumannii isolates from Southern Europe, but also from the USA and the UK. It is noteworthy that no carbapenemaseproducing A. baumannii had been isolated in our two preceding studies conducted in companion animals from Reunion Island.
One hypothesis for the presence of carbapenemase-producing A. baumannii in cattle could be the wide use of antibiotics in foodproducing animals that could be responsible for the selection of resistant bacteria, including carbapenemase-producing A. baumannii. For example, a recent study within the European Union and European Economic Area showed that a wide range of antimicrobial agents is used in these countries (i.e. tetracyclines, penicillins, macrolides, fluoroquinolones and others) [5]. A second interesting result is the diversity of the strains isolated in this study. Indeed, this is not consistent with the hypothesis of the spread of a unique strain from animal to animal, or with the presence of a unique strain in the environment of the farm that could have contaminated all of the animals. It is also noteworthy that the blaOXA-24 gene harboured by the carbapenem-resistant isolate did not disseminate to other A. baumannii isolates collected on the same cattle farm. These results are in accordance with our previous study conducted among pets from Reunion Island, with high strain diversity [2]. Overall, this study tends to confirm in livestock animals the result obtained in our preceding study conducted in pets, that A. baumannii is a micro-organism widely disseminated among animals living on Reunion Island. To our knowledge, this is also the first report of such A. baumannii strain diversity recorded from cattle living in the same environment. Further studies are needed to confirm these results. This study raises some questions: (i) what was the prevalence of A. baumannii carriage in the farm?; (ii) could this prevalence and strain diversity be recovered from all farms on Reunion Island?; and (iii) what could explain the strain diversity recorded in a few animals living in the same environment? Indeed, here the five A. baumannii isolates were assigned to different STs, among which four had never been described previously. This result suggests that a huge diversity of STs could be found in the cattle reservoir, maybe with isolates very different from those isolated in humans. One STs was already described, but has never been reported in the literature as isolated in humans or animals. Therefore, other investigations should be initiated to improve our understanding regarding the extrahospital transmission of these bacteria. Lastly, this first report of carbapenem-resistant A. baumannii in animals in France is a serious cause of concern.
55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95
Acknowledgements
96 97 The authors thank the team of curators of the Institut Pasteur 98 (Paris, France) MLST system for importing novel alleles, profiles 99 and/or isolates at http://pubmlst.org/abaumannii/. 100 Funding: Financial support was provided by the Program ‘Appel Q4 101 à projet interne du CHU d’Angers, 2012’. 102 Competing interests: None declared. 103 Ethical approval: Information was given to the owner about the 104 study, and the consent of the owner was received. 105
http://dx.doi.org/10.1016/j.ijantimicag.2016.09.005 0924-8579/© 2016 Elsevier B.V. and International Society of Chemotherapy. All rights reserved.
Please cite this article in press as: Hélène PailhorièsMarie Kempf, Olivier Belmonte, Marie-Laure Joly-GuillouMatthieu Eveillard, First case of OXA-24-producing Acinetobacter baumannii in cattle from Reunion Island, France, International Journal of Antimicrobial Agents (2016), doi: 10.1016/j.ijantimicag.2016.09.005
ARTICLE IN PRESS Letter to the Editor / International Journal of Antimicrobial Agents ■■ (2016) ■■–■■
2
106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 Q1 128 129 130 131
References [1] Belmonte O, Pailhoriès H, Kempf M, Gaultier MP, Lemarié C, Ramont C, et al. High prevalence of closely-related Acinetobacter baumannii in pets according to a multicentre study in veterinary clinics, Reunion Island. Vet Microbiol 2014;170:446–50. [2] Pailhoriès H, Belmonte O, Kempf M, Lemarié C, Cuziat J, Quinqueneau C, et al. Diversity of Acinetobacter baumannii strains isolated in humans, companion animals, and the environment in Reunion Island: an exploratory study. Int J Infect Dis 2015;37:64–9. [3] Al Bayssari C, Dabboussi F, Hamze M, Rolain J-M. Emergence of carbapenemaseproducing Pseudomonas aeruginosa and Acinetobacter baumannii in livestock animals in Lebanon. J Antimicrob Chemother 2015;70:950–1. [4] Poirel L, Berçot B, Millemann Y, Bonnin RA, Pannaux G, Nordmann P. Carbapenemase-producing Acinetobacter spp. in cattle, France. Emerg Infect Dis 2012;18:523–5. [5] Catry B, Cavaleri M, Baptiste K, Grave K, Grein K, Holm A, et al. Use of colistincontaining products within the European Union and European Economic Area (EU/EEA): development of resistance in animals and possible impact on human and animal health. Int J Antimicrob Agents 2015;46:297–306.
Hélène Pailhoriès Marie Kempf * L’UNAM Université d’Angers, ATOMycA, Inserm Equipe Avenir, CRCNA, Inserm U892, 6299 CNRS, IRIS, CHU, Angers, France
Laboratoire de bactériologie, CHU Angers, Angers, France
132 133
Olivier Belmonte Laboratoire de bactériologie, CHU Félix Guyon, Saint-Denis, La Réunion, France
134 135 136
Marie-Laure Joly-Guillou Matthieu Eveillard L’UNAM Université d’Angers, ATOMycA, Inserm Equipe Avenir, CRCNA, Inserm U892, 6299 CNRS, IRIS, CHU, Angers, France Laboratoire de bactériologie, CHU Angers, Angers, France
137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152
* Corresponding author. Laboratory of Clinical Bacteriology, CHU Angers, 4 rue Larrey, 49000 Angers, France. Fax: +33 2 41 35 41 64. E-mail address: [email protected] (M. Kempf). 18 August 2016 15 September 2016
Please cite this article in press as: Hélène PailhorièsMarie Kempf, Olivier Belmonte, Marie-Laure Joly-GuillouMatthieu Eveillard, First case of OXA-24-producing Acinetobacter baumannii in cattle from Reunion Island, France, International Journal of Antimicrobial Agents (2016), doi: 10.1016/j.ijantimicag.2016.09.005