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Article

Prevalence and Risk Factors Associated with Multidrug Resistance and Extended-Spectrum β-lactamase Producing E. coli Isolated from Healthy and Diseased Cats

by
Mahmoud Fayez
1,2,
Ahmed Elmoslemany
3,
Ahmad A. Al Romaihi
4,
Abdulfattah Y. Azzawi
5,
Abdullah Almubarak
1 and
Ibrahim Elsohaby
6,7,8,*
1
Al-Ahsa Veterinary Diagnostic Lab, Ministry of Environment, Water and Agriculture, Al-Ahsa 31982, Saudi Arabia
2
Department of Bacteriology, Veterinary Serum and Vaccine Research Institute, Ministry of Agriculture, Cairo 131, Egypt
3
Hygiene and Preventive Medicine Department, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr El-Sheikh 33516, Egypt
4
National Center for the Prevention and Control of Plants and Animal Diseases, Riyadh 11195, Saudi Arabia
5
Ibrize Life Sciences, Dammam 32242, Saudi Arabia
6
Department of Animal Medicine, Faculty of Veterinary Medicine, Zagazig University, Zagazig City 44511, Egypt
7
Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Hong Kong SAR 999077, China
8
Centre for Applied One Health Research and Policy Advice (OHRP), City University of Hong Kong, Hong Kong SAR 999077, China
*
Author to whom correspondence should be addressed.
Antibiotics 2023, 12(2), 229; https://doi.org/10.3390/antibiotics12020229
Submission received: 16 December 2022 / Revised: 18 January 2023 / Accepted: 19 January 2023 / Published: 20 January 2023
(This article belongs to the Special Issue Antibiotics Used in Animals Disease Control)
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Abstract

:
Household cats have been identified as potential antimicrobial resistance (AMR) reservoirs, and the extended-spectrum β-lactamases (ESBL) producing E. coli circulating among cats has been more frequently reported globally, but the factors linked to its colonization remain poorly understood. Thus, the objectives of this study were to determine E. coli shedding and the occurrence of multidrug resistant (MDR)- and ESBL-producing E. coli, as well as to determine risk factors associated with colonization of MDR and ESBL-producing E. coli isolated from both healthy and diseased cats in the Eastern Province of Saudi Arabia. In a cross-sectional study, 2000 swabs were collected from five anatomical regions (anus, skin, ear canal, nares, and conjunctival sac) of 209 healthy and 191 diseased cats that were admitted to a veterinary clinic in the Eastern Province of Saudi Arabia. In addition, each cat owner filled out a questionnaire about their cat’s demographics, management, health status, and antimicrobial usage. E. coli was detected in 165 (41.3%) of all cats, including 59 (28.2%) healthy and 106 (55.5%) diseased cats. In total, 170 E. coli isolates were found in healthy (35.3%) and diseased (64.7%) cats. Susceptibility testing revealed that 123 (72.4%) of the E. coli isolates were resistant to at least one of the tested antimicrobials. Overall, 17.6% (30/170) of E. coli isolates were MDR, with 10 (5.9%) and 20 (11.8%) isolates found in healthy and diseased cats, respectively. However, only 12 (7.1%) E. coli isolates were resistant to cefotaxime and harbored the blaCTX-M gene (ESBL-producer), with seven (4.1%) in healthy and five (2.9%) in diseased cats. Risk factor analysis showed that the odds of MDR and ESBL-producing E. coli were (20 and 17) and (six and eight) times higher when the family and cats were previously treated with antimicrobials, respectively. The presence of a child in the cat’s family was also linked to an increased risk of MDR E. coli colonization (OR = 3.4). In conclusion, a high frequency of MDR and ESBL-producing E. coli was detected among healthy and diseased cats in Saudi Arabia, raising concerns about transmission to humans and supporting the need of a “One Health” approach to address the potential threats of cats as AMR reservoirs.

1. Introduction

Antimicrobials are important therapeutic agents for infectious bacterial diseases in companion animals. Antimicrobial substance efficacy loss can have serious consequences for animal health and welfare [1]. Antimicrobial resistance (AMR) in companion animals is a complicated topic that is becoming increasingly important due to patient factors and public health concerns [2]. A unique feature of AMR in companion animals is that their close contact with humans creates favorable conditions for interspecies transmission of multidrug resistant bacteria (MDR) [3]. An additional risk factor for the emergence and spread of AMR is the use of antimicrobials crucial to human health in companion animals [4].
Escherichia coli (E. coli) is a Gram-negative intestinal commensal that is frequently isolated from a broad range of infection sites in both animals and humans [5]. E. coli variants were classified based on their virulence properties into several pathotypes including Shiga toxin-producing E. coli (STEC), Enteroinvasive E. coli (EIEC), Enteropathogenic E. coli (EPEC), Enterotoxigenic E. coli (ETEC), Enterohaemorrhagic E. coli (EHEC), and Enteroaggregative E. coli [5]. The majority of the virulence genes, including the stx1, stx2, eaeA, and hlyA, are important for E. coli pathogenicity and are linked to diarrhea in both animals and humans [5]. Selection of appropriate antimicrobials is critical for effective treatment of these infections and subsequently to reduce the risk of the emergence of AMR in commensal and pathogenic E. coli [6]. However, antimicrobial misuse led to the development of MDR and extended-spectrum β-lactamase (ESBL) producing E. coli in healthy and diseased companion animals [7,8]. Dissemination of ESBL-producing E. coli among companion animals resulted in reduction in efficacy or failure of the antimicrobial therapy [9]. Furthermore, the presence of ESBL genes in commensal E. coli in healthy animals could transferred horizontally to pathogenic strains [10] and could also spread resistance to humans through fecal–oral contamination [11].
In Saudi Arabia, cats are among the most common household pets [12]. The close contact between cats and their owners provides favorable conditions for transmission of zoonotic pathogens, either directly (e.g., through petting, licking, or physical injuries) or indirectly (e.g., through contamination of food or the environment) [13]. ESBL genes have been found in commensal and clinical E. coli isolates recovered from cats and/or their owners worldwide [14], suggesting that ESBL-producing E. coli can spread in both directions from humans and animals [15,16].
Despite the fact that numerous studies have found ESBL-producing E. coli in companion animals all over the world [17,18,19], to the authors’ knowledge, no data on AMR profiles of E. coli isolates from cats in Saudi Arabia have been published yet. Furthermore, studies on the risk factors associated with ESBL-producing E. coli colonization in cats are limited. Therefore, the objectives of this study were to (1) investigate E. coli shedding from various anatomical locations in healthy and diseased cats; (2) determine the frequency of MDR and ESBL-producing E. coli isolated from healthy and diseased cats; (3) investigate the presence of some selected virulence genes to identify the pathotypes of ESBL-producing E. coli isolates; and (4) determine the potential risk factors linked to colonization of MDR and ESBL-producing E. coli in both healthy and diseased cats in the Eastern Province of Saudi Arabia.

2. Results

2.1. Cat Population

A total of 400 cats were sampled, with 52.3% (209/400) apparently healthy and admitted for vaccination and/or grooming. However, the remining 191 (47.7%) cats were admitted for clinical examination due to digestive distress (81/400), ear discharge (61/400), eye discharge (59/400), respiratory distress (39/400), and skin wound and/or abscess (64/400). The sampled cats were 56.7% females and 43.3% males. The study population included five different cat breeds: Persian (40.5%), Siamese (28%), Himalayan (14.8%), Birman (13.2%), Egyptian Mau (2.5%), and Arabian Mau (1%). The characteristics of the studied cat population are detailed in Table S2.

2.2. Prevalence of E. coli Isolates

Among all cats (n = 400), 165 (41.3%) were found to carry E. coli including 59 (28.2%) healthy and 106 (55.5%) diseased. A total of 170 E. coli isolates (including isolates recovered from two different anatomical locations in five cats) were found in healthy (35.3%) and diseased (64.7%) cats. There were no significant differences in the distribution of E. coli isolates between healthy and diseased cats, cat breeds, or sex (p > 0.33). The prevalence of E. coli isolates in healthy and diseased cats based on anatomical locations is presented in Table 1.

2.3. Antimicrobial Susceptibility Testing

Susceptibility testing revealed that 123 (72.4%) of the E. coli isolates showed resistance to at least one of the tested antimicrobials (Figure 1). The antimicrobial susceptibility test showed that 68.3% and 45.5% of resistant E. coli isolates were found in healthy and diseased cats, respectively. E. coli isolates resistant to AMP (53.5%) was the highest, followed by resistance to SXT (22.9%); however, none of the isolates were MEM resistant (Figure 2A). E. coli isolates found in healthy cats exhibited resistance patterns comparable to isolates recovered from diseased cats. Furthermore, the frequency of E. coli isolates resistant to AMP (odds ratio (OR): 2.6) was significantly higher in healthy cats than in diseased cats; however, no differences (p > 0.05) were found between diseased and healthy cats for the other antimicrobials. The frequency of resistant E. coli isolates recovered from various anatomical locations in healthy and diseased cats is depicted in Figure 2B. The MAR index of resistant E. coli isolates ranged from 0.09 to 0.64 with 24.4% of the isolates having an AMR index >0.2. AMR index of E. coli isolates from healthy (average = 0.21; range: 0.09–0.64) and diseased (average = 0.22; range: 0.09–0.55) cats was not significantly different (Figure 3).

2.4. MDR and ESBL-Producing E. coli

Overall, 17.6% (30/170) of E. coli isolates tested positive for MDR, with 10 (5.9%) and 20 (11.8%) isolates found in healthy and diseased cats, respectively (Table 2). MDR isolates were resistant to three to six different classes of antimicrobials. Furthermore, among the 170 E. coli isolates, only 12 (7.1%) were resistant to CTX and harbored the blaCTX-M gene (ESBL-producer) with seven (4.1%) in healthy and five (2.9%) in diseased cats (Table 2). Four different ESBL genes were found (blaCTX-M-1 and 15, blaTEM and blaSHV), and blaCTX-M-15 predominated (66.7%, 8/12), followed by blaTEM (50%, 6/12) (Table 3). Furthermore, one or more virulence genes were found in 41.7% (5/12) of the ESBL-producing E. coli isolates. The eaeA virulence gene was the most detected (5/12), followed by stx2 and hlyA (2/12). None of the ESBL-producing E. coli isolates possessed the virulence gene stx1 (Table 3).

2.5. Risk Factors for MDR and ESBL-Producing E. coli

Univariable analysis (p < 0.25) revealed a positive association between both MDR and ESBL-producing E. coli and a number of family characteristics such as antimicrobial use, previous antimicrobial use for the cat, having a child at home, and cat food type. However, only MDR E. coli was positively linked to the presence of acne, current use of antimicrobials for cats, and reason for visiting the veterinary clinic (Table 4). On the other hand, when females care for the cat, that reduces the risk of MDR and ESBL compared to males.
The results of multivariable analysis for factors associated with having MDR and ESBL-producing E. coli are shown in Table 5. The odds of MDR and ESBL were (20 and 17) and (six and eight) times higher when the family and cats were previously treated with antimicrobials, respectively. Furthermore, feeding a cat raw food or home-available food increases the odds of having MDR (nine and six times) and ESBL-producing E. coli (60 and 12 times) compared to feeding a cat dry food, respectively. The presence of a child in the cat’s family was also associated with an increased risk of MDR E. coli (OR = 3.4). Finally, cats in the care of females had lower odds of having MDR E. coli (OR = 0.2) than cats in the care of males.

3. Discussion

The number of animals kept as pets has increased significantly in recent decades; approximately 223 million pets are owned globally today [20]. Cats are one of the most common household pets, providing their owners with joy and companionship. However, the increased interaction between household cats and their owners creates favorable conditions for resistant pathogens transmission through direct and indirect contact [13,21]. Several studies have investigated the public health risks associated with the transfer of antimicrobial-resistant bacteria from cats [1,22]; however, studies investigated the risk factors associated with antimicrobial-resistant bacteria colonization are scarce. In the present study, 41.3% of cats were E. coli carriers, which is consistent with the E. coli isolation rates reported in Canada [23] and Hong Kong [24]. However, it was higher than the isolation rate (8.7%) reported in cats in South Korea [25]. This variation could be attributed to the number of cats in each study, sample type, sampling site, and cat health status. In this study, E. coli was recovered from 28.2% and 55.5% of apparently healthy and diseased cats, respectively. A similar isolation rate (52%) was observed in diseased cats in Italy [26], whereas a higher isolate rate (45.6%) was found among apparently healthy cats in China [19].
Antimicrobial resistance is an emerging and growing threat among many clinically relevant bacteria including E. coli. The high frequency of resistant E. coli (72.4%) found in the present study against antimicrobials commonly used in small animals and humans is an alarming finding. The results of this study are consistent with the high frequency of resistance to AMP and SXT reported for feline E. coli isolates in other studies [27,28]; however, the resistant rate to AMC (6.4%) was lower than that (15–100%) found in these studies. Moreover, all E. coli isolates were susceptible to MEM, suggesting the absence of carbapenems resistance among our isolates which is consistent with previous studies in cats from Australia [27] and China [19].
The MDR bacteria isolated from food-producing and companion animals have become an emerging problem [29,30]. In the present study, 17.6% of E. coli isolates were identified as MDR. Most studies reported a higher percentage of MDR E. coli in companion animals such as 66.8% in Poland [31], 56% in USA [18], 43.3% in Japan [32], and 23.8% in South Korea [28]. However, other studies have reported a lower percentage of MDR E. coli in cats such as 11.7% in Australia [27]. The variations in the percentages of MDR E. coli between studies could be explained by differences in the criteria used to classify isolates as MDR. The criteria developed by Magiorakos, et al. [33] were used to classify our isolates. Furthermore, the origin of the MDR isolates could explain the variation. Isolates recovered from healthy animals may not have been exposed to antimicrobials and thus demonstrate a low level of resistance. In this study, MDR isolates were found in both healthy and diseased cats; however, the percentage of MDR E. coli recovered from diseased (11.8%) was double that isolated from healthy cats (5.9%).
Many studies in the last decade have reported the spread of ESBL-producing E. coli from clinical isolates in cats [34,35]. Furthermore, it is now known that healthy animals can harbor antimicrobial resistant pathogens, including ESBL-producing E. coli [29,36]. In our study, the overall prevalence of ESBL-producing E. coli was 7.1%. A comparable prevalence has also been reported in UK (7%) [37] and Switzerland (7.5%) [38]. This prevalence, however, was higher than the 3.7% and 2% reported in companion animals in France [39] and Netherland [40]. Other studies have reported 0% of cats tested positive for ESBL-producing E. coli [29,41]. One of the possible explanations for this difference is the antimicrobial use strategy used by veterinarians in different countries. In this study, healthy cats (4.1%) had a higher rate of ESBL-producing E. coli than diseased cats (2.9%). Similarly, several studies have found ESBL-producing E. coli in healthy cats and dogs, but the prevalence is higher in diseased animals [42,43]. Although ESBL-producing E. coli was isolated from various anatomical regions, anus swabs were the most common source of ESBL-producing E. coli in our study, which is consistent with many other studies [42,44]. This is not surprising given that E. coli is frequently isolated from the digestive tract.
A diversity of blaESBL genes were reported in this study and are similar to those found in both humans [45] and food-producing animals [46] in Saudi Arabia. The predominant resistance gene found in the present study is blaCTX-M-15, which is consistent with previous studies in companion animals [37,44,47]. However, the blaCTX-M-1 was reported as the predominant in other studies [43,48], and the blaCTX-M-55 was detected in pets in mainland China [49].
In the present study, virulence associated genes (eaeA, stx2, and hlyA) were found in ESBL-producing E. coli isolated from healthy and diseased cats. E. coli is an opportunistic pathogen that lives in the intestinal microbiota of animals and humans. In this study, the molecular detection of the eaeA, stx2, and hlyA virulence genes suggested the dissemination of enteropathogenic and enterohemorrhagic E. coli in the investigated cats. Similar studies have reported the isolation of pathogenic E. coli from cats [50,51].
The identification of factors associated with MDR and ESBL-producing E. coli in pets would be valuable for controlling transmission between humans and animals. Previous studies showed that pet contact was related to ESBL carriage in humans [52,53]. Therefore, cats carrying ESBL-producing E. coli represent a potential risk to human health since they live closely together. This study found a higher risk of MDR and ESBL-producing E. coli in cats and family members who had previously received antibiotic treatment. This finding is in line with previous findings in humans [54] and companion animals [27,55]. A study on cats also revealed that prior antimicrobial treatment has a significant influence on the likelihood of E. coli isolate exhibiting MDR [56]. There was a positive association between MDR and having children at home. Children handle animals and touch their faces or mouths more frequently than adults, which increase the risk of disease transmission. The current study also showed feeding cats raw food was associated with higher risk of MDR and ESBL-producing E. coli infection compared to cats fed on dry food. A cohort study on 36 household cats showed strong association between feeding raw pet food and ESBL shedding [57]. The same study also isolated ESBL Enterobacteriaceae from 14 of 18 raw pet food products and zero of 35 non-raw pet food products [57].
There are some limitations to this study. One significant limitation of this study was the collection of data from a single veterinary clinic in Saudi Arabia. The study did, however, provide useful information about the trends in the burden of infections caused by ESBL producers in Saudi veterinary medicine.

4. Materials and Methods

4.1. Study Design and Sampling

Between January and December 2018, 2000 swabs were collected from 400 cats admitted to a veterinary clinic in Eastern Province of Saudi Arabia. Cats were voluntarily included in the study and were split into two groups according to the reason for visiting the clinic: healthy (n = 209) and diseased (n = 191). Healthy cats were admitted for vaccination and/or grooming. On the other hand, diseased cats were admitted for clinical examination and displayed one or more of the following clinical symptoms: diarrhea, respiratory signs, conjunctivitis, skin wound, otitis, and/or abscess. A professional veterinarian collected swabs from five different anatomical regions (anus, skin, ear canal, conjunctival sac, and nares) in each cat. Each swab was placed in a sterile tube with 2 mL of liquid brain–heart infusion broth (BHI: Difco) and sent to the laboratory at 4 °C to be analyzed later. Before sample collection, cat owners filled a questionnaire about demographics, cat management, health status, and antimicrobial use. A written consent form was also signed by cat owners who agreed to participate in the study.

4.2. E. coli Isolation and Identification

Swabs immersed in 2 mL BHI were preincubated in aerobic conditions overnight at 37 °C. A 10 µL of the suspension was then inoculated onto MacConkey agar (Oxoid, Basingstoke, Hampshire, UK) and incubated under aerobic conditions at 37 °C for 24–48 h. Suggestive E. coli colonies were collected, purified on 5% sheep blood agar, Gram stained, and identified to species level using Vitek 2 Compact (BioMerieux, Marcy l’Etoile, France) then stored at −70 °C in 40% glycerol saline.
For molecular conformation, the QIAamp DNA mini kit (Qiagen SA, Courtaboeuf, France) was used to extract the bacterial DNA from biochemically identified E. coli isolates according to the manufacturer’s instructions. PCR was performed on the extracted DNA using primers designed specifically for E. coli 16S rRNA amplification and sequencing Weisburg, et al. [58].

4.3. Antimicrobial Susceptibility Test

Antimicrobial susceptibility testing was conducted using the disc diffusion method, and the results were interpreted according to Clinical and Laboratory Standards Institute (CLSI) guidelines [59]. In the present study, antimicrobials tested were ampicillin (AMP: 10 μg), cefotaxime (CTX: 30 µg), amoxicillin-clavulanic acid (AMC: 20/10 μg), ciprofloxacin (CIP: 5 μg), tetracycline (TET: 30 µg), gentamicin (GEN: 10 μg), trimethoprim/sulfamethoxazole (SXT: 1.25/23.75 μg), streptomycin (STR: 10 μg), chloramphenicol (CHL: 30 μg), erythromycin (ERY: 15 μg), and meropenem (MEM: 10 μg). Isolates showing resistance to three or more antimicrobials classes (including β-lactams as one class) were classified as multidrug-resistant (MDR) [33]. The multiple antibiotic resistance (MAR) index was calculated by dividing the number of antibiotics to which an isolate is resistant to the total number of antibiotics tested for susceptibility [60].

4.4. ESBL-Producing E. coli Identification

Confirmed E. coli isolates were screened for phenotypic ESBL production by disk diffusion tests using cefotaxime (CTX: 30 μg) according to CLSI guidelines [61]. Phenotypically confirmed ESBL-producing E. coli were further characterized to identify the virulence (eaeA, hlyA, stx1, and stx2) and β-lactamase (blaCTX-M, blaTEM and blaSHV) genes using primers and reaction conditions (Table S1) previously described [62,63,64,65].

4.5. Statistical Analysis

The questioner’s data and laboratory analysis data were coded into dichotomous or categorical variables and then combined into a single data set. Data visualization was carried out using R software (version 4.2.0; R Foundation for Statistical Computing, Vienna, Austria). On the other hand, statistical modelling was performed using Stata Statistical Software v.17 (Stata Corp, College Station, TX, USA). Initially, Chi-square and Fisher’s Exact tests were used to identify the association between the presence of E. coli isolates and cat condition (healthy vs. diseased), breeds, and sex. However, univariable logistic regression was used to assess the associations between single variables and each of the outcome variables (1- MDR (1 = yes vs. 0 = no) and 2- ESBL (1 = yes vs. 0 = no). Spearman’s rank-order correlation statistics were used to examined for multicollinearity in variables with p < 0.25 and before being added as explanatory variables to multivariable logistic regression models. The final model was built manually using backward stepwise elimination at p < 0.05. The Hosmer–Lemeshow test was used to assess model fitness; however, receiver operating characteristic curve was used to assess the predictive ability of the model [66].

5. Conclusions

E. coli isolates recovered from healthy and diseased cats admitted to a veterinary clinic in Saudi Arabia showed high levels of resistance to the majority of tested antimicrobials. Our finding revealed the presence of MDR and ESBL-producing E. coli in both healthy and diseased cats, which pose a risk to public and animal health. Thus, to investigate the role of cats as vectors for antimicrobial resistance transmission to humans, an effective antimicrobial stewardship program as well as additional studies using a One Health approach may be required.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/antibiotics12020229/s1, Table S1: Primers, product size and annealing temperatures used in the present study to identify virulence and antimicrobial resistance genes.; Table S2: Description of variables collected from both healthy and diseased cats.

Author Contributions

Conceptualization, M.F., A.E. and I.E.; methodology, M.F., A.A.A.R., A.Y.A. and A.A.; software, M.F., A.E. and I.E.; validation, M.F., A.E. and I.E.; formal analysis, A.E. and I.E.; investigation, M.F., A.A.A.R., A.Y.A. and A.A.; resources, M.F., A.A.A.R., A.Y.A. and A.A.; data curation, M.F., A.E. and I.E.; writing—original draft preparation, M.F., A.E. and I.E.; writing—review and editing, M.F.; A.E.; A.A.A.R.; A.Y.A.; A.A. and I.E.; visualization, I.E.; project administration, M.F. All authors have read and agreed to the published version of the manuscript.

Funding

No specific funding was received.

Institutional Review Board Statement

The swab collection was conducted under the Saudi Ministry of Environment, Water, and Agriculture (MEWA) supervision and under the Ethical Approval of the Animal Health and Welfare Committee of MEWA. The study was performed in accordance with the regulations of the law of ethics of research on living creatures, set and monitored by the Saudi National Committee of Bioethics (NCBE).

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

Authors would like to thank the owners of the cats involved in the present study.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Pomba, C.; Rantala, M.; Greko, C.; Baptiste, K.E.; Catry, B.; Van Duijkeren, E.; Mateus, A.; Moreno, M.A.; Pyörälä, S.; Ružauskas, M. Public health risk of antimicrobial resistance transfer from companion animals. J. Antimicrob. Chemother. 2017, 72, 957–968. [Google Scholar] [CrossRef] [PubMed]
  2. Weese, J.S. Antimicrobial resistance in companion animals. Anim. Health Res. Rev. 2008, 9, 169–176. [Google Scholar] [CrossRef] [PubMed]
  3. Zhang, S.; Abbas, M.; Rehman, M.U.; Huang, Y.; Zhou, R.; Gong, S.; Yang, H.; Chen, S.; Wang, M.; Cheng, A. Dissemination of antibiotic resistance genes (ARGs) via integrons in Escherichia coli: A risk to human health. Environ. Pollut. 2020, 266, 115260. [Google Scholar] [CrossRef] [PubMed]
  4. Ewers, C.; Bethe, A.; Semmler, T.; Guenther, S.; Wieler, L. Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: A global perspective. Clin. Microbiol. Infect. 2012, 18, 646–655. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Kaper, J.B.; Nataro, J.P.; Mobley, H.L. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2004, 2, 123–140. [Google Scholar] [CrossRef]
  6. Weese, J.; Giguère, S.; Guardabassi, L.; Morley, P.; Papich, M.; Ricciuto, D.; Sykes, J.E. ACVIM consensus statement on therapeutic antimicrobial use in animals and antimicrobial resistance. J. Vet. Intern. Med. 2015, 29, 487–498. [Google Scholar] [CrossRef]
  7. Zhang, P.L.; Shen, X.; Chalmers, G.; Reid-Smith, R.J.; Slavic, D.; Dick, H.; Boerlin, P. Prevalence and mechanisms of extended-spectrum cephalosporin resistance in clinical and fecal Enterobacteriaceae isolates from dogs in Ontario, Canada. Vet. Microbiol. 2018, 213, 82–88. [Google Scholar] [CrossRef]
  8. Bortolami, A.; Zendri, F.; Maciuca, E.I.; Wattret, A.; Ellis, C.; Schmidt, V.; Pinchbeck, G.; Timofte, D. Diversity, virulence, and clinical significance of extended-spectrum β-lactamase-and pAmpC-producing Escherichia coli from companion animals. Front. Microbiol. 2019, 10, 1260. [Google Scholar] [CrossRef] [Green Version]
  9. Pitout, J.D.; Laupland, K.B. Extended-spectrum β-lactamase-producing Enterobacteriaceae: An emerging public-health concern. Lancet Infect. Dis. 2008, 8, 159–166. [Google Scholar] [CrossRef]
  10. Ramos, S.; Silva, V.; Dapkevicius, M.d.L.E.; Caniça, M.; Tejedor-Junco, M.T.; Igrejas, G.; Poeta, P. Escherichia coli as commensal and pathogenic bacteria among food-producing animals: Health implications of extended spectrum β-lactamase (ESBL) production. Animals 2020, 10, 2239. [Google Scholar] [CrossRef]
  11. Salinas, L.; Loayza, F.; Cárdenas, P.; Saraiva, C.; Johnson, T.J.; Amato, H.; Graham, J.P.; Trueba, G. Environmental spread of extended spectrum beta-lactamase (ESBL) producing Escherichia coli and ESBL genes among children and domestic animals in Ecuador. Environ. Health Perspect. 2021, 129, 027007. [Google Scholar] [CrossRef]
  12. Alrukban, M.O.; Alekrish, Y.A.; Alshehri, M.H.; Bajeaifer, Y.A.; Alhamad, M.H.; Sambas, F.A.; Alsouan, A.A. Awareness of pet owners in Riyadh regarding pet-related health risks and their associated preventative measures. Vector-Borne Zoonotic Dis. 2022, 22, 419–424. [Google Scholar] [CrossRef]
  13. Damborg, P.; Broens, E.M.; Chomel, B.B.; Guenther, S.; Pasmans, F.; Wagenaar, J.A.; Weese, J.S.; Wieler, L.H.; Windahl, U.; Vanrompay, D. Bacterial zoonoses transmitted by household pets: State-of-the-art and future perspectives for targeted research and policy actions. J. Comp. Pathol. 2016, 155, S27–S40. [Google Scholar] [CrossRef] [Green Version]
  14. Salgado-Caxito, M.; Benavides, J.A.; Adell, A.D.; Paes, A.C.; Moreno-Switt, A.I. Global prevalence and molecular characterization of extended-spectrum β-lactamase producing-Escherichia coli in dogs and cats–A scoping review and meta-analysis. One Health 2021, 12, 100236. [Google Scholar] [CrossRef]
  15. Johnson, J.R.; Miller, S.; Johnston, B.; Clabots, C.; DebRoy, C. Sharing of Escherichia coli sequence type ST131 and other multidrug-resistant and urovirulent E. coli strains among dogs and cats within a household. J. Clin. Microbiol. 2009, 47, 3721–3725. [Google Scholar] [CrossRef] [Green Version]
  16. Carvalho, A.; Barbosa, A.; Arais, L.; Ribeiro, P.; Carneiro, V.; Cerqueira, A. Resistance patterns, ESBL genes, and genetic relatedness of Escherichia coli from dogs and owners. Braz. J. Microbiol. 2016, 47, 150–158. [Google Scholar] [CrossRef] [Green Version]
  17. Sidjabat, H.E.; Townsend, K.M.; Lorentzen, M.; Gobius, K.S.; Fegan, N.; Chin, J.J.-C.; Bettelheim, K.A.; Hanson, N.D.; Bensink, J.C.; Trott, D.J. Emergence and spread of two distinct clonal groups of multidrug-resistant Escherichia coli in a veterinary teaching hospital in Australia. J. Med. Microbiol. 2006, 55, 1125–1134. [Google Scholar] [CrossRef]
  18. Shaheen, B.; Boothe, D.; Oyarzabal, O.; Smaha, T. Antimicrobial resistance profiles and clonal relatedness of canine and feline Escherichia coli pathogens expressing multidrug resistance in the United States. J. Vet. Intern. Med. 2010, 24, 323–330. [Google Scholar] [CrossRef]
  19. Cui, L.; Zhao, X.; Li, R.; Han, Y.; Hao, G.; Wang, G.; Sun, S. Companion Animals as Potential Reservoirs of Antibiotic Resistant Diarrheagenic Escherichia coli in Shandong, China. Antibiotics 2022, 11, 828. [Google Scholar] [CrossRef]
  20. Beetz, A.; Uvnäs-Moberg, K.; Julius, H.; Kotrschal, K. Psychosocial and psychophysiological effects of human-animal interactions: The possible role of oxytocin. Front. Psychol. 2012, 3, 234. [Google Scholar] [CrossRef]
  21. Guardabassi, L.; Schwarz, S.; Lloyd, D.H. Pet animals as reservoirs of antimicrobial-resistant bacteria. J. Antimicrob. Chemother. 2004, 54, 321–332. [Google Scholar] [CrossRef] [PubMed]
  22. Féria, C.; Machado, J.; Correia, J.D.; Gonçalves, J.; Gaastra, W. Virulence genes and P fimbriae PapA subunit diversity in canine and feline uropathogenic Escherichia coli. Vet. Microbiol. 2001, 82, 81–89. [Google Scholar] [CrossRef] [PubMed]
  23. Awosile, B.B.; McClure, J.T.; Saab, M.E.; Heider, L.C. Antimicrobial resistance in bacteria isolated from cats and dogs from the Atlantic Provinces, Canada from 1994–2013. Can. Vet. J. 2018, 59, 885. [Google Scholar] [PubMed]
  24. Chan, O.S.; Baranger-Ete, M.; Lam, W.W.; Wu, P.; Yeung, M.; Lee, E.; Bond, H.; Swan, O.; Tun, H.M. A retrospective study of antimicrobial resistant bacteria associated with feline and canine urinary tract infection in Hong Kong SAR, China—A case study on implication of first-line antibiotics use. Antibiotics 2022, 11, 1140. [Google Scholar] [CrossRef] [PubMed]
  25. Oh, Y.-I.; Seo, K.-W.; Kim, D.-H.; Cheon, D.-S. Prevalence, co-infection and seasonality of fecal enteropathogens from diarrheic cats in the Republic of Korea (2016–2019): A retrospective study. BMC Vet. Res. 2021, 17, 1–13. [Google Scholar] [CrossRef]
  26. Piccolo, F.L.; Belas, A.; Foti, M.; Fisichella, V.; Marques, C.; Pomba, C. Detection of multidrug resistance and extended-spectrum/plasmid-mediated AmpC beta-lactamase genes in Enterobacteriaceae isolates from diseased cats in Italy. J. Feline Med. Surg. 2020, 22, 613–622. [Google Scholar] [CrossRef]
  27. Saputra, S.; Jordan, D.; Mitchell, T.; San Wong, H.; Abraham, R.J.; Kidsley, A.; Turnidge, J.; Trott, D.J.; Abraham, S. Antimicrobial resistance in clinical Escherichia coli isolated from companion animals in Australia. Vet. Microbiol. 2017, 211, 43–50. [Google Scholar] [CrossRef] [Green Version]
  28. Jung, W.K.; Shin, S.; Park, Y.K.; Lim, S.-K.; Moon, D.-C.; Park, K.T.; Park, Y.H. Distribution and antimicrobial resistance profiles of bacterial species in stray cats, hospital-admitted cats, and veterinary staff in South Korea. BMC Vet. Res. 2020, 16, 1–14. [Google Scholar] [CrossRef] [Green Version]
  29. Costa, D.; Poeta, P.; Sáenz, Y.; Coelho, A.C.; Matos, M.; Vinué, L.; Rodrigues, J.; Torres, C. Prevalence of antimicrobial resistance and resistance genes in faecal Escherichia coli isolates recovered from healthy pets. Vet. Microbiol. 2008, 127, 97–105. [Google Scholar] [CrossRef]
  30. Van Duin, D.; Paterson, D.L. Multidrug-resistant bacteria in the community: Trends and lessons learned. Infect. Dis. Clin. 2016, 30, 377–390. [Google Scholar] [CrossRef]
  31. Rzewuska, M.; Czopowicz, M.; Kizerwetter-Świda, M.; Chrobak, D.; Błaszczak, B.; Binek, M. Multidrug resistance in Escherichia coli strains isolated from infections in dogs and cats in Poland (2007–2013). Sci. World J. 2015, 2015, 408205. [Google Scholar] [CrossRef] [Green Version]
  32. Harada, K.; Nakai, Y.; Kataoka, Y. Mechanisms of resistance to cephalosporin and emergence of O25b-ST131 clone harboring CTX-M-27 β-lactamase in extraintestinal pathogenic Escherichia coli from dogs and cats in Japan. Microbiol. Immunol. 2012, 56, 480–485. [Google Scholar] [CrossRef]
  33. Magiorakos, A.-P.; Srinivasan, A.; Carey, R.B.; Carmeli, Y.; Falagas, M.; Giske, C.; Harbarth, S.; Hindler, J.; Kahlmeter, G.; Olsson-Liljequist, B. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 2012, 18, 268–281. [Google Scholar] [CrossRef] [Green Version]
  34. Shaheen, B.W.; Nayak, R.; Foley, S.L.; Kweon, O.; Deck, J.; Park, M.; Rafii, F.; Boothe, D.M. Molecular characterization of resistance to extended-spectrum cephalosporins in clinical Escherichia coli isolates from companion animals in the United States. Antimicrob. Agents Chemother. 2011, 55, 5666–5675. [Google Scholar] [CrossRef] [Green Version]
  35. Huber, H.; Zweifel, C.; Wittenbrink, M.M.; Stephan, R. ESBL-producing uropathogenic Escherichia coli isolated from dogs and cats in Switzerland. Vet. Microbiol. 2013, 162, 992–996. [Google Scholar] [CrossRef]
  36. Jackson, C.; Davis, J.; Frye, J.; Barrett, J.; Hiott, L. Diversity of Plasmids and Antimicrobial Resistance Genes in Multidrug-Resistant Escherichia coli Isolated from Healthy Companion Animals. Zoonoses Public Health 2015, 62, 479–488. [Google Scholar] [CrossRef]
  37. Timofte, D.; Maciuca, I.E.; Williams, N.J.; Wattret, A.; Schmidt, V. Veterinary hospital dissemination of CTX-M-15 extended-spectrum beta-lactamase–producing Escherichia coli ST410 in the United Kingdom. Microb. Drug Resist. 2016, 22, 609–615. [Google Scholar] [CrossRef] [Green Version]
  38. Bogaerts, P.; Huang, T.-D.; Bouchahrouf, W.; Bauraing, C.; Berhin, C.; El Garch, F.; Glupczynski, Y.; Group, C.S. Characterization of ESBL-and AmpC-producing Enterobacteriaceae from diseased companion animals in Europe. Microb. Drug Resist. 2015, 21, 643–650. [Google Scholar] [CrossRef]
  39. Dahmen, S.; Haenni, M.; Châtre, P.; Madec, J.-Y. Characterization of bla CTX-M IncFII plasmids and clones of Escherichia coli from pets in France. J. Antimicrob. Chemother. 2013, 68, 2797–2801. [Google Scholar] [CrossRef] [Green Version]
  40. Dierikx, C.; van Duijkeren, E.; Schoormans, A.; van Essen-Zandbergen, A.; Veldman, K.; Kant, A.; Huijsdens, X.; van der Zwaluw, K.; Wagenaar, J.; Mevius, D. Occurrence and characteristics of extended-spectrum-β-lactamase-and AmpC-producing clinical isolates derived from companion animals and horses. J. Antimicrob. Chemother. 2012, 67, 1368–1374. [Google Scholar] [CrossRef]
  41. Murphy, C.; Reid-Smith, R.J.; Prescott, J.F.; Bonnett, B.N.; Poppe, C.; Boerlin, P.; Weese, J.S.; Janecko, N.; McEwen, S.A. Occurrence of antimicrobial resistant bacteria in healthy dogs and cats presented to private veterinary hospitals in southern Ontario: A preliminary study. Can. Vet. J. 2009, 50, 1047. [Google Scholar] [PubMed]
  42. Sun, Y.; Zeng, Z.; Chen, S.; Ma, J.; He, L.; Liu, Y.; Deng, Y.; Lei, T.; Zhao, J.; Liu, J.-H. High prevalence of blaCTX-M extended-spectrum β-lactamase genes in Escherichia coli isolates from pets and emergence of CTX-M-64 in China. Clin. Microbiol. Infect. 2010, 16, 1475–1481. [Google Scholar] [CrossRef] [PubMed]
  43. Hordijk, J.; Schoormans, A.; Kwakernaak, M.; Duim, B.; Broens, E.; Dierikx, C.; Mevius, D.; Wagenaar, J.A. High prevalence of fecal carriage of extended spectrum β-lactamase/AmpC-producing Enterobacteriaceae in cats and dogs. Front. Microbiol. 2013, 4, 242. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Yousfi, M.; Mairi, A.; Touati, A.; Hassissene, L.; Brasme, L.; Guillard, T.; De Champs, C. Extended spectrum β-lactamase and plasmid mediated quinolone resistance in Escherichia coli fecal isolates from healthy companion animals in Algeria. J. Infect. Chemother. 2016, 22, 431–435. [Google Scholar] [CrossRef]
  45. Yasir, M.; Ajlan, A.M.; Shakil, S.; Jiman-Fatani, A.A.; Almasaudi, S.B.; Farman, M.; Baazeem, Z.M.; Baabdullah, R.; Alawi, M.; Al-Abdullah, N. Molecular characterization, antimicrobial resistance and clinico-bioinformatics approaches to address the problem of extended-spectrum β-lactamase-producing Escherichia coli in western Saudi Arabia. Sci. Rep. 2018, 8, 1–11. [Google Scholar] [CrossRef] [Green Version]
  46. Fadlelmula, A.; Al-Hamam, N.A.; Al-Dughaym, A.M. A potential camel reservoir for extended-spectrum β-lactamase-producing Escherichia coli causing human infection in Saudi Arabia. Trop. Anim. Health Prod. 2016, 48, 427–433. [Google Scholar] [CrossRef]
  47. Zogg, A.L.; Simmen, S.; Zurfluh, K.; Stephan, R.; Schmitt, S.N.; Nüesch-Inderbinen, M. High prevalence of extended-spectrum β-lactamase producing Enterobacteriaceae among clinical isolates from cats and dogs admitted to a veterinary hospital in Switzerland. Front. Vet. Sci. 2018, 5, 62. [Google Scholar] [CrossRef] [Green Version]
  48. Costa, D.; Poeta, P.; Briñas, L.; Sáenz, Y.; Rodrigues, J.; Torres, C. Detection of CTX-M-1 and TEM-52 β-lactamases in Escherichia coli strains from healthy pets in Portugal. J. Antimicrob. Chemother. 2004, 54, 960–961. [Google Scholar] [CrossRef] [Green Version]
  49. Rao, L.; Lv, L.; Zeng, Z.; Chen, S.; He, D.; Chen, X.; Wu, C.; Wang, Y.; Yang, T.; Wu, P. Increasing prevalence of extended-spectrum cephalosporin-resistant Escherichia coli in food animals and the diversity of CTX-M genotypes during 2003–2012. Vet. Microbiol. 2014, 172, 534–541. [Google Scholar] [CrossRef]
  50. Puño-Sarmiento, J.; Medeiros, L.; Chiconi, C.; Martins, F.; Pelayo, J.; Rocha, S.; Blanco, J.; Blanco, M.; Zanutto, M.; Kobayashi, R. Detection of diarrheagenic Escherichia coli strains isolated from dogs and cats in Brazil. Vet. Microbiol. 2013, 166, 676–680. [Google Scholar] [CrossRef]
  51. Watson, V.E.; Jacob, M.E.; Flowers, J.R.; Strong, S.J.; DebRoy, C.; Gookin, J.L. Association of atypical enteropathogenic Escherichia coli with diarrhea and related mortality in kittens. J. Clin. Microbiol. 2017, 55, 2719–2735. [Google Scholar] [CrossRef] [Green Version]
  52. Meyer, E.; Gastmeier, P.; Kola, A.; Schwab, F. Pet animals and foreign travel are risk factors for colonisation with extended-spectrum β-lactamase-producing Escherichia coli. Infection 2012, 40, 685–687. [Google Scholar] [CrossRef]
  53. Van den Bunt, G.; Fluit, A.; Spaninks, M.; Timmerman, A.; Geurts, Y.; Kant, A.; Scharringa, J.; Mevius, D.; Wagenaar, J.; Bonten, M. Faecal carriage, risk factors, acquisition and persistence of ESBL-producing Enterobacteriaceae in dogs and cats and co-carriage with humans belonging to the same household. J. Antimicrob. Chemother. 2020, 75, 342–350. [Google Scholar] [CrossRef]
  54. Zhao, S.-Y.; Zhang, J.; Zhang, Y.-L.; Wang, Y.-C.; Xiao, S.-Z.; Gu, F.-F.; Guo, X.-K.; Ni, Y.-X.; Han, L.-Z. Epidemiology and risk factors for faecal extended-spectrum β-lactamase-producing Enterobacteriaceae (ESBL-E) carriage derived from residents of seven nursing homes in western Shanghai, China. Epidemiol. Infect. 2016, 144, 695–702. [Google Scholar] [CrossRef]
  55. Karkaba, A.; Hill, K.; Benschop, J.; Pleydell, E.; Grinberg, A. Carriage and population genetics of extended spectrum β-lactamase-producing Escherichia coli in cats and dogs in New Zealand. Vet. Microbiol. 2019, 233, 61–67. [Google Scholar] [CrossRef]
  56. Hernandez, J.; Bota, D.; Farbos, M.; Bernardin, F.; Ragetly, G.; Médaille, C. Risk factors for urinary tract infection with multiple drug-resistant Escherichia coli in cats. J. Feline Med. Surg. 2014, 16, 75–81. [Google Scholar] [CrossRef]
  57. Baede, V.O.; Broens, E.M.; Spaninks, M.P.; Timmerman, A.J.; Graveland, H.; Wagenaar, J.A.; Duim, B.; Hordijk, J. Raw pet food as a risk factor for shedding of extended-spectrum beta-lactamase-producing Enterobacteriaceae in household cats. PLoS One 2017, 12, e0187239. [Google Scholar] [CrossRef] [Green Version]
  58. Weisburg, W.G.; Barns, S.M.; Pelletier, D.A.; Lane, D.J. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 1991, 173, 697–703. [Google Scholar] [CrossRef] [Green Version]
  59. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing; Thirtieth CLSI Supplement M100-S30; CLSI: Wayne, PA, USA, 2020. [Google Scholar]
  60. Davis, R.; Brown, P.D. Multiple antibiotic resistance index, fitness and virulence potential in respiratory Pseudomonas aeruginosa from Jamaica. J. Med. Microbiol. 2016, 65, 261–271. [Google Scholar] [CrossRef]
  61. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals; CLSI: Wayne, PA, USA, 2018. [Google Scholar]
  62. Brian, M.; Frosolono, M.; Murray, B.; Miranda, A.; Lopez, E.; Gomez, H.; Cleary, T. Polymerase chain reaction for diagnosis of enterohemorrhagic Escherichia coli infection and hemolytic-uremic syndrome. J. Clin. Microbiol. 1992, 30, 1801–1806. [Google Scholar] [CrossRef]
  63. Pitout, J.; Thomson, K.; Hanson, N.; Ehrhardt, A.; Moland, E.; Sanders, C. β-Lactamases responsible for resistance to expanded-spectrum cephalosporins in Klebsiella pneumoniae, Escherichia coli, and Proteus mirabilis isolates recovered in South Africa. Antimicrob. Agents Chemother. 1998, 42, 1350–1354. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Gallien, P. Detection and Subtyping of ShigaToxin-Producing Escherichia coli (STEC). In PCR Detection of Microbial Pathogens; Springer: Berlin/Heidelberg, Germany, 2003; pp. 163–184. [Google Scholar]
  65. Pitout, J.D.; Hossain, A.; Hanson, N.D. Phenotypic and molecular detection of CTX-M-β-lactamases produced by Escherichia coli and Klebsiella spp. J. Clin. Microbiol. 2004, 42, 5715–5721. [Google Scholar] [CrossRef] [PubMed]
  66. Dohoo, I.R.; Martin, W.; Stryhn, H.E. Veterinary Epidemiologic Research; University of Prince Edward Island: Charlottetown, PE, Canada, 2003. [Google Scholar]
Antibiotics 12 00229 g001 550
Figure 1. Heat map based on the source and antimicrobial resistance patterns of the 170 E. coli isolates found in 400 cats.
Figure 1. Heat map based on the source and antimicrobial resistance patterns of the 170 E. coli isolates found in 400 cats.
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Antibiotics 12 00229 g002 550
Figure 2. Frequency of antimicrobial resistance of E. coli isolates. (A) recovered from healthy and diseased cats. (B) recovered from different anatomical locations in healthy and diseased cats.
Figure 2. Frequency of antimicrobial resistance of E. coli isolates. (A) recovered from healthy and diseased cats. (B) recovered from different anatomical locations in healthy and diseased cats.
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Figure 3. Multiple antibiotic resistance (MAR) index box plot of E. coli isolates recovered from different anatomical locations in healthy and diseased cats.
Figure 3. Multiple antibiotic resistance (MAR) index box plot of E. coli isolates recovered from different anatomical locations in healthy and diseased cats.
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Table
Table 1. Number of E. coli isolates found in 400 cats admitted to a veterinary clinic in Eastern Province of Saudi Arabia.
Table 1. Number of E. coli isolates found in 400 cats admitted to a veterinary clinic in Eastern Province of Saudi Arabia.
Anatomical LocationNumber (%) of E. coli IsolatesTotal
(n = 400)
Healthy Cats
(n = 209)		Diseased Cats
(n = 191)
Anus55 (26.3)87 (45.5)142 (35.5)
Skin3 (1.4)10 (5.2)13 (3.3)
Ear canal2 (1.0)8 (4.2)10 (2.5)
Conjunctival sac0 (0.0)5 (2.6)5 (1.3)
Nares0 (0.0)0 (0.0)0 (0.0)
Total60 (28.7)110 (57.6)170 (42.5)
Table
Table 2. Number of multidrug resistance (MDR) and extended-spectrum β-lactamase (ESBL) producing E. coli isolates found in healthy and diseased cats.
Table 2. Number of multidrug resistance (MDR) and extended-spectrum β-lactamase (ESBL) producing E. coli isolates found in healthy and diseased cats.
Anatomical LocationNNo. (%) of MDR E. coliTotal No. (%) ESBL E. coliTotal
HealthyDiseasedHealthyDiseased
Anus1429 (6.3)14 (9.9)23 (16.2)6 (4.2)5 (3.5)11 (7.7)
Skin131 (7.7)2 (15.4)3 (23.1)1 (7.7)0 (0.0)1 (7.7)
Ear canal100 (0.0)3 (30.0)3 (30.0)0 (0.0)0 (0.0)0 (0.0)
Conjunctival sac50 (0.0)1 (20.0)1 (20.0)0 (0.0)0 (0.0)0 (0.0)
Nares00 (0.0)0 (0.0)0 (0.0)0 (0.0)0 (0.0)0 (0.0)
Total17010 (5.9)20 (11.8)30 (17.6)7 (4.1)5 (2.9)12 (7.1)
Table
Table 3. Resistance, virulence genes and antimicrobial resistance patterns of 12 ESBL-producing E. coli isolates found in healthy and diseased cats.
Table 3. Resistance, virulence genes and antimicrobial resistance patterns of 12 ESBL-producing E. coli isolates found in healthy and diseased cats.
Cat No.GroupAnatomical LocationResistance Genes 1Virulence Genes 1Antimicrobial Resistance PatternsMAR 2
blaCTX-MblaTEMblaSHVeaeAstx1stx2hlyA
3HealthyAnusCTX-M-1––+–––AMP, CTX, SXT0.27
8HealthyAnusCTX-M-1+–––––AMP, AMC, CTX, CIP, SXT, CHL0.55
19HealthyAnusCTX-M-15+–––––AMP, AMC, CTX, CIP, SXT, CHL0.55
25DiseasedAnusCTX-M-15+–+–++AMP, AMC, CTX, TCY, SXT0.45
29HealthyAnusCTX-M-15+–––––AMP, CTX, TCY, GEN, STR0.45
29HealthySkinCTX-M-15+–––––AMP, CTX, TCY, GEN, STR0.45
41DiseasedAnusCTX-M-15––+–––AMP, CTX, GEN,0.27
44HealthyAnusCTX-M-15+–––––AMP, AMC, CTX, TCY, STR, SXT, CHL0.64
53DiseasedAnusCTX-M-1–+––––AMP, AMC, CTX, CIP, SXT, CHL0.55
82DiseasedAnusCTX-M-1––––––AMP, CTX, TCY0.27
216DiseasedAnusCTX-M-15––+–++AMP, CTX, SXT0.27
267HealthyAnusCTX-M-15––+–––AMP, CTX, SXT0.27
1 + = resistance or virulence genes positive; – = resistance or virulence negative; 2 MAR = multiple antibiotic resistance index.
Table
Table 4. Univariable results for risk factors associated with multidrug resistance (MDR) and extended-spectrum β-lactamase (ESBL) producing E. coli isolates found in 400 cats.
Table 4. Univariable results for risk factors associated with multidrug resistance (MDR) and extended-spectrum β-lactamase (ESBL) producing E. coli isolates found in 400 cats.
FactorsMDR E. coliESBL E. coli
OR 1p-ValueOR 1p-Value
Family use antimicrobials
  No1.00 (ref.) 1.00 (ref.)
  Yes13.10.0009.70.001
Family member with acne
  No1.00 (ref.) 1.00 (ref.)
  Yes3.30.0040.890.870
Hospitalization
  No1.00 (ref.) 1.00 (ref.)
  Yes3.10.0091.90.337
Previous antimicrobials use for cat
  No1.00 (ref.) 1.00 (ref.)
  Yes3.40.0064.10.040
Current antimicrobials use for cat
  No1.00 (ref.) 1.00 (ref.)
  Yes8.30.000--
Child at home
  No1.00 (ref.) 1.00 (ref.)
  Yes2.40.0522.90.122
Cat Living
  Indoor1.00 (ref.) 1.00 (ref.)
  Indoors–outdoors0.70.4612.30.295
Reason being at clinic
  Vaccination and/or grooming1.00 (ref.) 1.00 (ref.)
  Treatment2.030.0990.910.877
Cat care
  Adult male1.00 (ref.)0.0001.00 (ref.)0.016
  Adult female0.150.0000.210.025
  Child----
  All family0.150.013--
Food type
  Dry1.00 (ref.)0.0031.00 (ref.)0.006
  Wet0.990.9922.50.456
  Raw4.20.01316.80.001
  Home available5.20.00112.10.005
1 OR: odds ratio.
Table
Table 5. Multivariable results for risk factors associated with multidrug resistance (MDR) and extended-spectrum β-lactamase (ESBL) producing E. coli isolates found in 400 cats.
Table 5. Multivariable results for risk factors associated with multidrug resistance (MDR) and extended-spectrum β-lactamase (ESBL) producing E. coli isolates found in 400 cats.
FactorsMDR E. coliESBL E. coli
OR (95% CI) 1p-ValueOR (95% CI) 1p-Value
Family use antimicrobials
  No1.00 (ref.) 1.00 (ref.)
  Yes20.0 (6.29–63.69)0.00016.6 (3.29–84.08)0.001
Previous antimicrobials use for cat
  No1.00 (ref.) 1.00 (ref.)
  Yes5.5 (1.83–16.36)0.0027.8 (1.66–36.34)0.009
Child at home
  No1.00 (ref.)
  Yes3.4 (1.14–10.30)0.027--
Cat care
  Adult male1.00 (ref.)0.019--
  Adult female0.20 (0.06–0.69)0.011--
  Child----
  All family0.21 (0.03–1.29)0.092--
Food type
  Dry1.00 (ref.)0.0061.00 (ref.)0.001
  Wet0.93 (0.15–5.64)0.9392.7 (0.22–33.50)0.431
  Raw8.5 (1.74–41.70)0.00859.7 (7.16–497.54)0.000
  Home available6.3 (1.76–22.80)0.00512.4 (1.94–79.63)0.008
_cons0.004 (0.001–0.020)0.0000.001 (0.0001–0.005)0.000
1 OR: odds ratio; CI: confidence interval.
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Fayez, M.; Elmoslemany, A.; Al Romaihi, A.A.; Azzawi, A.Y.; Almubarak, A.; Elsohaby, I. Prevalence and Risk Factors Associated with Multidrug Resistance and Extended-Spectrum β-lactamase Producing E. coli Isolated from Healthy and Diseased Cats. Antibiotics 2023, 12, 229. https://doi.org/10.3390/antibiotics12020229

AMA Style

Fayez M, Elmoslemany A, Al Romaihi AA, Azzawi AY, Almubarak A, Elsohaby I. Prevalence and Risk Factors Associated with Multidrug Resistance and Extended-Spectrum β-lactamase Producing E. coli Isolated from Healthy and Diseased Cats. Antibiotics. 2023; 12(2):229. https://doi.org/10.3390/antibiotics12020229

Chicago/Turabian Style

Fayez, Mahmoud, Ahmed Elmoslemany, Ahmad A. Al Romaihi, Abdulfattah Y. Azzawi, Abdullah Almubarak, and Ibrahim Elsohaby. 2023. "Prevalence and Risk Factors Associated with Multidrug Resistance and Extended-Spectrum β-lactamase Producing E. coli Isolated from Healthy and Diseased Cats" Antibiotics 12, no. 2: 229. https://doi.org/10.3390/antibiotics12020229

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