High prevalence of closely-related Acinetobacter baumannii in pets according to a multicentre study in veterinary clinics, Reunion Island

doi:10.1016/j.vetmic.2014.01.042

Veterinary Microbiology

Volume 170, Issues 3–4, 4 June 2014, Pages 446-450

https://doi.org/10.1016/j.vetmic.2014.01.042 Get rights and content

Abstract

Our objective was to study the carriage of Acinetobacter baumannii (AB) in pets in Reunion Island (RI), a French territory in Indian Ocean. Overall, 138 pets were sampled (rectum, mouth, wounds if applicable) in 9 veterinary clinics (VC). The prevalence of AB carriage was 6.5% (95%CI; 2.4, 10.6) and 9 carriers were indentified from 4 VC. Hospitalization in a VC and antimicrobial treatment administered within the 15 preceding days were significantly associated with AB carriage (P < 0.01 and P < 0.05, respectively). Despite the VC in which animals have been sampled were located all around RI, most isolates (8/9) were closely-related (>90% similarity by pulsed-field gel electrophoresis). Additional studies are needed to improve the understanding about interactions between the different reservoirs of AB in RI.

Introduction

Acinetobacter baumannii (AB) has emerged over the last decade as a cause of healthcare-associated infections. Its clinical significance has been propelled by its remarkable ability to upregulate or acquire resistance determinant, making it one of the organisms threatening the current antibiotic era (Peleg et al., 2008, Higgins et al., 2010, Kempf and Rolain, 2012). The cross-transmission of this organism from patients to patients generating outbreaks, particularly in intensive care units and the possibilities of outbreak extension by patient transfers have been demonstrated (Naas et al., 2006, Giamarellou et al., 2008). In addition during the last decade, a lot of studies have reported the emergence of AB as an organism responsible for community-acquired infections, especially in tropical areas (Eveillard et al., 2013).

Reunion Island (RI) is a French territory located in the western Indian Ocean. Hospital-based retrospective data have demonstrated that AB is regularly isolated from clinical or screening samples obtained from patients within the 48 h following hospitalization in RI. Those data tend to indicate the existence of a human extra-hospital AB reservoir in RI. This carriage can be due to AB isolates acquired during a preceding hospitalization, but some other hypotheses can be proposed. One of them is an AB acquisition from an animal reservoir. In several studies conducted previously in veterinary clinics (VC), AB have been isolated in pets from clinical samples (Francey et al., 2000, Endimiani et al., 2011, Hamouda et al., 2011, Zordan et al., 2011). Our objective was to study the AB reservoir in pets in RI.

Section snippets

Materials and methods

A multicentre cross-sectional study was conducted in October 2012. All cats and dogs present on one day in 9 veterinary clinics (VC) (30% of all VC in RI) were sampled by swabbing rectum, mouth and wounds if applicable. All swabs were inoculated in 2 agar media: the UTI chromogenic agar medium (UTI, Oxoid, Basingstoke, UK) and the ESBL agar medium (AES, France), a selective medium for gram-negative bacilli resistant to third-generation cephalosporins. Bacterial identifications were performed

Results

Overall, 138 animals were sampled and 9 carriers (2 cats and 7 dogs) were identified from 4 VC. According to our methods of screening, cultivating and identifying, the prevalence of AB carriage was 6.5% (CI95%; 2.4, 10.6). Eight isolates had the same susceptibility pattern to antibiotics: they were susceptible to ticarcillin, carbapenems, aminoglycosides, rifampicin, and resistant to ciprofloxacine and cotrimoxazole. The other isolate was susceptible to all those antibiotics (Table 1).

The PFGE

Discussion

Today, increased attention is devoted to companion animal welfare, resulting in increased expenditure on veterinary care and prevention and therapy of infectious diseases. This situation is associated with a frequent use of antimicrobial agents in pet animals, may result in some laxity in antimicrobial prescription, and therefore can lead to inappropriate use of antimicrobial agents. It is well established that pet animals can be reservoirs of antimicrobial-resistant bacteria (Guardabassi et

Acknowledgements

We are very grateful to H. Lotteau, P. Legendre, G. Holzapfel, P. Melot, T. Lostfelt, L. Venturini, D. Plazanet, I. Lemercier, K. Teppe, and W. Severin for their participation to the study by sampling animals in their veterinary clinic.

A part of the results of this study was presented at the 9th International Symposium on the Biology of Acinetobacter, Cologne 2013, oral presentation O5-4.

References (23)

M. Eveillard et al.
Reservoirs of Acinetobacter baumannii outside the hospital and potential involvement in emerging human community-acquired infections
Int. J. Infect. Dis.
(2013)
H. Giamarellou et al.
Acinetobacter baumannii: a universal threat to public health?
Int. J. Antimicrob. Agents.
(2008)
A. Hamouda et al.
Epidemiology of Acinetobacter baumannii of animal origin
Int. J. Antimicrob. Agents
(2011)
M. Kempf et al.
Emergence of resistance to carbapenems in Acinetobacter baumannii in Europe: clinical impact and therapeutic options
Int. J. Antimicrob. Agents
(2012)
K.J. Towner
Acinetobacter: an old friend, but a new enemy
J. Hosp. Infect.
(2009)
R. Zarrilli et al.
Global evolution of multidrug-resistant Acinetobacter baumannii clonal lineages
Int. J. Antimicrob. Agents.
(2013)
A. Di Popolo et al.
Molecular epidemiological investigation of multidrug-resistant Acinetobacter baumannii strains in four Mediterranean countries with a multilocus sequence typing scheme
Clin. Microbiol. Infect.
(2010)
L. Diancourt et al.
The population structure of Acinetobacter baumannii: expanding multiresistant clones from an ancestral susceptible genetic pool
PLoS One
(2010)
A. Endimiani et al.
Acinetobacter baumannii isolates from pets and horses in Switzerland: molecular characterization and clinical data
J. Antimicrob. Chemother.
(2011)
T. Francey et al.
The role of Acinetobacter baumannii as a nosocomial pathogen for dogs and cats in an intensive care unit
J. Vet. Intern. Med.
(2000)

M. Giannouli et al.

Virulence-related traits of epidemic Acinetobacter baumannii strains belonging to the international clonal lineage I–II and to the emerging genotypes ST25 and ST78

BMC Infect. Dis.

(2013)

Cited by (35)

Acinetobacter baumannii
2023, Molecular Medical Microbiology, Third Edition
Acinetobacter baumannii is a gram-negative pathogen that is primarily associated with hospital acquired infections, predominantly aspiration pneumonia and catheter-associated bacteremia, but it can also cause soft tissue and urinary infections. In some geographical locations, it also causes community acquired pneumonia. The primary virulence factor of Acinetobacter is the ability of its capsule to evade clearance by the innate immune system, allowing high bacterial density to trigger LPS-TLR4-mediated sepsis. Nevertheless, because antibiotic therapy is so effective against susceptible strains, the primary driver of clinical outcome is antibiotic resistance. Unfortunately, rates of carbapenem-resistance are exceedingly high. Epidemiologic data suggest that more than 50% of isolates in intensive care units, and in some regions far greater, are carbapenem-resistant. Receipt of initially effective therapy remains the primary driver of outcome, reducing 30-day mortality threefold. However, due to its high frequency of extreme drug resistance phenotype, early initiation of effective therapy poses a significant clinical challenge.
Analysis of virulence proteins in pathogenic Acinetobacter baumannii to provide early warning of zoonotic risk
2023, Microbiological Research
Citation Excerpt :
On the one hand, A. baumannii causes a variety of animal infections and food contamination, with the basic characteristics of human-animal infections (Carvalheira et al., 2017; Marí-Almirall et al., 2019). On the other hand, some isolates separated from wildlife and domestic animals in recent years cause obvious animal pathogenicity compared with wild strains (Belmonte et al., 2014). At present, A. baumannii has been isolated from a variety of wild and domestic animals, including cattle, horses, pigs, rabbits, ferrets, snakes, rats, ducks, turkeys and chickens (Endimiani et al., 2011; Pereira et al., 2020).
Acinetobacter baumannii is a ubiquitous opportunistic pathogen usually with low virulence. In recent years, reports of increased pathogenicity of A. baumannii in livestock due to the migratory behaviour of wildlife have attracted public health attention. Our previous study reported that an A. baumannii strain isolated from dead chicks, CCGGD201101, showed enhanced pathogenicity, but the mechanism for increased virulence is not understood. Here, to screen potential virulence factors, the proteomes of the isolated strain CCGGD201101 and the standard strain ATCC19606 of A. baumannii were compared, and the possible virulence-enhancing mechanisms were further analysed. The 50 % lethal dose (LD₅₀) values of CCGGD201101 and standard strain ATCC19606 in ICR mice were determined to verify their bacterial toxicity. 2D fluorescence difference gel electrophoresis (2D-DIGE) combined with matrix-assisted laser desorption/ionization time of flight mass spectrometry (MALDI-TOF/TOF-MS) and quantitative real-time PCR (RTqPCR) were applied to screen and identify differentially expressed proteins or genes that may be related to virulence enhancement. Bioinformatics analyses based on proteinprotein interaction (PPI) networks were used to explore the function of potential virulence proteins. The pathogenicity of potential virulence factors was assessed by phylogenetic analyses and an animal infection model. The results showed that the LD₅₀ of CCGGD201101 for mice was 1.186 × 10⁶ CFU/mL, and the virulence was increased by 180.5-fold compared to ATCC19606. Forty-seven protein spots were significantly upregulated for the A. baumannii CCGGD201101 strain (fold change ≥1.5, p < 0.05). In total, 14 upregulated proteins were identified using proteomic analysis, and the mRNA expression levels of these proteins were nearly identical, with few exceptions. According to the PPI network and phylogenetic analyses, the I78 family peptidase inhibitor, 3-oxoacyl-ACP reductase FabG, and glycine zipper were screened as being closely related to the pathogenicity of bacteria. Furthermore, the I78 overexpression strains exhibited higher lethality in mouse infection models, which indicated that the I78 family peptidase inhibitor was a potential new virulence factor to enhance the pathogenicity of the A. baumannii CCGGD201101 strain. The present study helped us to better understand the mechanisms of virulence enhancement and provided a scientific basis for establishing an early warning system for enhanced virulence of A. baumannii from animals.
Physicochemical and structural characterization, epitope mapping and vaccine potential investigation of a new protein containing Tetratrico Peptide Repeats of Acinetobacter baumannii: An in-silico and in-vivo approach
2021, Molecular Immunology
Citation Excerpt :
Moreover, they are the most common cause of hospital-borne infections after Pseudomonas aeruginosa and are responsible for 2–10 % of nosocomial infections caused by gram-negative bacteria (Jeong et al., 2006; Yeom et al., 2013). A. baumannii is also known as an infectious species of animals (Belmonte et al., 2014; Molenaar and van Engelen, 2015; Zordan et al., 2011). But to date, no effective vaccine has been approved against this bacterium.
Acinetobacter baumannii is an opportunistic multidrug-resistant pathogen that causes a significant mortality rate. The proteins containing Tetratrico Peptide Repeats (TPRs) are involved in the pathogenicity and virulence of bacteria and have different roles such as transfer of bacterial virulence factors to host cells, binding to the host cells and inhibition of phagolysosomal maturation. So, in this study, physicochemical properties of a new protein containing TPRs in A. baumannii which was named PcTPRs1 by this study were characterized and its 3D structure was predicted by in-silico tools. The protein B and T cell epitopes were mapped and its vaccine potential was in-silico and in-vivo investigated. Domain analysis indicated that the protein contains the Flp pilus assembly protein TadD domain which has three TPRs. The helix is dominant in the protein structure, and this protein is an outer membrane antigen which, is extremely conserved among A. baumannii strains; thus, has good properties to be applied as a recombinant vaccine. The best-predicted and refined model was applied in ligand-binding sites and conformational epitopes prediction. Based on epitope mapping results, several epitopes were characterized which could stimulate both immune systems. BLAST results showed the introduced epitopes are completely conserved among A. baumannii strains. The in-vivo analysis indicates that a 101 amino acid fragment of the protein which contains the best selected epitope, can produce a good protectivity against A. baumannii as well as the whole TPR protein and thus could be investigated as an effective subunit and potential vaccines.
Acinetobacter in veterinary medicine, with an emphasis on Acinetobacter baumannii
2019, Journal of Global Antimicrobial Resistance
Acinetobacter spp. are aerobic, rod-shaped, Gram-negative bacteria belonging to the Moraxellaceae family of the class Gammaproteobacteria and are considered ubiquitous organisms. Among them, Acinetobacter baumannii is the most clinically significant species with an extraordinary ability to accumulate antimicrobial resistance and to survive in the hospital environment. Recent reports indicate that A. baumannii has also evolved into a veterinary nosocomial pathogen. Although Acinetobacter spp. can be identified to species level using matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry (MALDI-TOF/MS) coupled with an updated database, molecular techniques are still necessary for genotyping and determination of clonal lineages. It appears that the majority of infections due to A. baumannii in veterinary medicine are nosocomial. Such isolates have been associated with several types of infection such as canine pyoderma, feline necrotizing fasciitis, urinary tract infection, equine thrombophlebitis and lower respiratory tract infection, foal sepsis, pneumonia in mink, and cutaneous lesions in hybrid falcons. Given the potential multidrug resistance of A. baumannii, treatment of diseased animals is often supportive and should preferably be based on in vitro antimicrobial susceptibility testing results. It should be noted that animal isolates show high genetic diversity and are in general distinct in their sequence types and resistance patterns from those found in humans. However, it cannot be excluded that animals may occasionally play a role as a reservoir of A. baumannii. Thus, it is of importance to implement infection control measures in veterinary hospitals to avoid nosocomial outbreaks with multidrug-resistant A. baumannii.
The role of TonB-dependent copper receptor in virulence of Acinetobacter baumannii
2018, Infection, Genetics and Evolution
Acinetobacter baumannii is an opportunistic gram negative pathogen that can adhere to different surfaces and cause different nosocomial infections. To investigate the role of TonB-dependent copper receptor, an outer membrane protein, in virulence of A. baumannii, we deleted this receptor from A. baumannii chromosome. There was a significant decrease in biofilm formation by copper receptor deficient mutant strain. Similarly, the adherence to human epithelial cell and the hydrophobicity were declined. The survival rate of the mutant strain in human sera was reduced while no change was observed in motility of strains. In murine pneumonia model, the bacterial lethal dose 0 (LD₀), LD₅₀ and LD₁₀₀ were increased for mutant strain. Moreover, in vivo and in vitro experiments revealed changes in growth rate and dissemination of mutant strain; so that the bacterial load of the mutant was significantly reduced in the spleen and lung. The findings suggest a critical role for TonB-dependent copper receptor in virulence of A. baumannii.
OXA-23 and ISAba1–OXA-66 class D β-lactamases in Acinetobacter baumannii isolates from companion animals
2017, International Journal of Antimicrobial Agents
Citation Excerpt :
Different authors demonstrated that hospitalisation of pets in a veterinary clinic is significantly associated with carriage of A. baumannii [17,31,40]. Further risk factors, which are almost similar to those identified for human infections with the opportunistic pathogen A. baumannii, are underlying diseases, prior antimicrobial treatment and poor hygiene [17,31,40]. Actually, carbapenems are not licensed for treatment of small animals, and extra-label use, which would be allowed for emergency treatment and in case of poor efficacy of other licensed antimicrobial agents, is supposed to be rare.
Acinetobacter baumannii is recognised as a major pathogen of nosocomial infections that frequently show resistance to last-resort antimicrobials. To investigate whether A. baumannii from companion animals harbour carbapenem resistance mechanisms, 223 clinical isolates obtained from veterinary clinics between 2000 and 2013 in Germany were screened for carbapenem-non-susceptibility employing meropenem-containing Mueller–Hinton agar plates. Minimum inhibitory concentration (MIC) data were obtained using the VITEK^®2 system. Assignment to international clones (ICs) was done by multiplex PCR or repetitive sequence-based PCR employing the DiversiLab system. Clonality was studied using pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing (MLST). Genes encoding carbapenemases and aminoglycoside-modifying enzymes were detected by PCR. In three samples from dogs, carbapenem-resistant A. baumannii carrying the bla_OXA-23 gene on plasmids and located on transposon Tn2008 were identified. The isolates belonged to sequence type ST1^P (clonal complex CC1/IC1/pulsotype II) and ST10^P (CC10/IC8/pulsotype IV) according to the Pasteur MLST scheme, and to ST231^Ox (CC109) and ST585^Ox (CC447) following the Oxford scheme. Insertion sequence ISAba1 was identified upstream of bla_OXA-66 in 58 A. baumannii isolates. MLST referred them to ST2^P (CC2/IC2/pulsotypes I and III), ST208^Ox, ST350^Ox and ST556^Ox (all CC118), respectively. PFGE suggested nosocomial spread of these highly related strains, which frequently demonstrated a multidrug-resistant phenotype, in one veterinary clinic. These data show that A. baumannii from companion animals reveal resistance determinants and clonal lineages of strains globally emerging in humans. This suggests an interspecies transmission and warrants molecular surveillance of A. baumannii in veterinary clinics to mitigate its further spread.

View all citing articles on Scopus

View full text

Article preview

Veterinary Microbiology

Abstract

Introduction

Section snippets

Materials and methods

Results

Discussion

Acknowledgements

References (23)

Reservoirs of Acinetobacter baumannii outside the hospital and potential involvement in emerging human community-acquired infections

Int. J. Infect. Dis.

Acinetobacter baumannii: a universal threat to public health?

Int. J. Antimicrob. Agents.

Epidemiology of Acinetobacter baumannii of animal origin

Int. J. Antimicrob. Agents

Emergence of resistance to carbapenems in Acinetobacter baumannii in Europe: clinical impact and therapeutic options

Int. J. Antimicrob. Agents

Acinetobacter: an old friend, but a new enemy

J. Hosp. Infect.

Global evolution of multidrug-resistant Acinetobacter baumannii clonal lineages

Int. J. Antimicrob. Agents.

Molecular epidemiological investigation of multidrug-resistant Acinetobacter baumannii strains in four Mediterranean countries with a multilocus sequence typing scheme

Clin. Microbiol. Infect.

The population structure of Acinetobacter baumannii: expanding multiresistant clones from an ancestral susceptible genetic pool

PLoS One

Acinetobacter baumannii isolates from pets and horses in Switzerland: molecular characterization and clinical data

J. Antimicrob. Chemother.

The role of Acinetobacter baumannii as a nosocomial pathogen for dogs and cats in an intensive care unit

J. Vet. Intern. Med.

Virulence-related traits of epidemic Acinetobacter baumannii strains belonging to the international clonal lineage I–II and to the emerging genotypes ST25 and ST78

BMC Infect. Dis.

Cited by (35)

Acinetobacter baumannii

Analysis of virulence proteins in pathogenic Acinetobacter baumannii to provide early warning of zoonotic risk

Physicochemical and structural characterization, epitope mapping and vaccine potential investigation of a new protein containing Tetratrico Peptide Repeats of Acinetobacter baumannii: An in-silico and in-vivo approach

Acinetobacter in veterinary medicine, with an emphasis on Acinetobacter baumannii

The role of TonB-dependent copper receptor in virulence of Acinetobacter baumannii

OXA-23 and ISAba1–OXA-66 class D β-lactamases in Acinetobacter baumannii isolates from companion animals

Short communicationHigh prevalence of closely-related Acinetobacter baumannii in pets according to a multicentre study in veterinary clinics, Reunion Island

Abstract

Introduction

Section snippets

Materials and methods

Results

Discussion

Acknowledgements

Int. J. Infect. Dis.

Int. J. Antimicrob. Agents.

Int. J. Antimicrob. Agents

Int. J. Antimicrob. Agents

J. Hosp. Infect.

Int. J. Antimicrob. Agents.

Molecular epidemiological investigation of multidrug-resistant Acinetobacter baumannii strains in four Mediterranean countries with a multilocus sequence typing scheme

Clin. Microbiol. Infect.

The population structure of Acinetobacter baumannii: expanding multiresistant clones from an ancestral susceptible genetic pool

PLoS One

Acinetobacter baumannii isolates from pets and horses in Switzerland: molecular characterization and clinical data

J. Antimicrob. Chemother.

The role of Acinetobacter baumannii as a nosocomial pathogen for dogs and cats in an intensive care unit

J. Vet. Intern. Med.

Virulence-related traits of epidemic Acinetobacter baumannii strains belonging to the international clonal lineage I–II and to the emerging genotypes ST25 and ST78

BMC Infect. Dis.

Short communication
High prevalence of closely-related Acinetobacter baumannii in pets according to a multicentre study in veterinary clinics, Reunion Island