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3 November 2026

13 Pages

Environmental ESKAPE Organisms and Other Environmental Equine-Specific Indicator Pathogens—Are They Relevant in Equine Nosocomial Wound Infections?

,
,
and
1
Equine Clinic: Surgery and Radiology, Freie Universität Berlin, Oertzenweg 19b, 14163 Berlin, Germany
2
Laboklin GmbH & CO.KG, Steubenstraße 4, 97688 Bad Kissingen, Germany
*
Author to whom correspondence should be addressed.
Antibiotics2026, 15(11), 1091;https://doi.org/10.3390/antibiotics15111091
This article belongs to the Special Issue Antibiotic Resistance and Antimicrobial Stewardship in Veterinary Medicine
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Abstract

Background: Multidrug-resistant organisms increasingly challenge infection prevention and control (IPC) in equine referral hospitals. Objectives: Assessment of selected environmental indicator pathogens in an equine teaching hospital and evaluation of their relevance for nosocomial wound infections. Study design: Observational study with repeated environmental sampling and retrospective evaluation of wound culture submissions. Methods: During three sampling periods (SPs), surface samples were collected across functional areas before and after routine cleaning/disinfection. Revision of the cleaning/disinfection protocols and environmental support staff feedback and training was performed between SP 1 and 2. Indicator pathogens were defined as an equine-adapted ESKAPEE-derived panel. Samples from surgical wounds were considered nosocomial if infection developed ≥3 days after hospitalisation. Results: Indicator pathogens were detected in all SPs, with the greatest frequency and diversity in SP 1. SP 1 yielded indicator pathogens in 25.7% of the 152 samples. After IPC optimisation, detection decreased in SP 2 to 11.2% of the 152 samples. In SP 3 with fewer samples (n = 42) sporadic recovery (7.1%) was observed. Contamination involved in particular high-touch surfaces and floors, and several pathogens persisted after cleaning/disinfection. Of 125 wounds, 38 met the criteria for nosocomial infection. Isolated from both, the environment and infected wounds were Streptococcus equi ssp. zooepidemicus, Staphylococcus aureus, Escherichia coli, and Enterobacter cloacae. Molecular typing was unavailable. Conclusions: Environmental equine-relevant indicator pathogens were detected across clinical areas. Some persisted after routine cleaning and/or were detected in nosocomial wound infections. Revision of cleaning/disinfection protocols with staff training was temporarily associated with reduced environmental contamination.

1. Introduction

Nosocomial infections and the emergence of multidrug-resistant organisms (MDROs) represent an increasing challenge in equine referral hospitals. In these referral hospitals, the treatment of critically ill horses, frequent invasive procedures, as well as intensive handling of the patients and possibly shared equipment contribute to the promotion and distribution of resistant bacteria. The frequently necessary antibiotic use in equine intensive care patients, both medical and surgical, promotes the emergence and persistence of MDROs as well. Therefore, for equine hospital biosecurity, structured infection prevention programmes as well as targeted environmental microbiological surveillance are essential [1,2,3,4,5,6,7,8,9,10,11,12,13].
Surveillance strategies in human medicine frequently focus on the so-called ESKAPE indicator pathogens (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, Enterobacter spp.)—pathogens that are commonly involved in nosocomial infections and that commonly show a high grade of antimicrobial resistance and therefore are able to “escape” antimicrobial therapy and infection control efforts [14]. Many of these organisms have also been increasingly identified in equine hospitals, both as causes of clinical disease and as colonisers of horses and the hospital environment [15,16]. Antimicrobial resistance surveillance data from equine clinical submissions in the United Kingdom have demonstrated the regular occurrence of resistant Enterobacterales and staphylococci, including organisms encompassed by the ESKAPE framework [13,17]. However, since beta-Lactamase-producing E. coli are commonly encountered in equine hospitals and are a well-recognised cause of equine hospital-acquired wound infections [6,9,18,19,20,21], the ESKAPE framework has been expanded to ESKAPEE [22].
In equine medicine, surgical site infections as well as infection of traumatic wounds are commonly caused by MDROs, often including pathogens of the ESKAPEE spectrum [18,19,21]. In addition, equine-adapted pathogens such as Streptococcus equi ssp. zooepidemicus are well-known causes of infections in equines. This organism may survive on environmental surfaces for variable periods depending on conditions, supporting the plausibility of indirect transmission routes and highlighting the importance of adequate biosecurity protocols in a clinical setting [23]. Therefore, these organisms typically causing hospital-acquired infections in horses should be included in an equine-clinic-specific indicator pathogen panel to optimise surveillance in these environments. Furthermore, equine patients may be colonised with indicator pathogens upon hospital admission or after antimicrobial therapy, which highlights the necessity of appropriate biosecurity protocols [18,21].
The combination of structured hygiene management and systematic evaluation of infection control protocols and resistance surveillance initiatives such as the Equine Veterinary Surveillance Network (EVSNET) provide the basis for a risk-based environmental surveillance specifically tailored to equine hospitals [3,17].
For this reason, this study aimed at the systematic assessment of the occurrence of selected environmental indicator pathogens as well as their occurrence in nosocomial wound infections in an equine hospital.

2. Material and Methods

2.1. Environmental Samples

During 3 sampling periods, impression smears of surfaces (DIN 10113-3) with agar plates provided by Laboklin GmbH & Co. KG (Bad Kissingen, Germany) were collected throughout the functional areas (surgery, treatment areas, stables) of the clinic. The samples were collected before and after cleaning and disinfection of the areas, regardless of macroscopic defilement. Samples collected before and after cleaning and disinfection were obtained from the same predefined sampling locations but not from the exact same spots. Adjacent surface areas were sampled to avoid potential interference caused by the removal of microorganisms during the initial contact-plate sampling.
Samples were collected in November 2021, February 2022 and June 2022. In June 2022, only sensitive surfaces were sampled, which led to a smaller sample size. Sensitive surfaces were defined as particularly relevant from a hygiene and infection prevention perspective due to their potential involvement in the transmission of microorganisms. In between November 2021 and February 2022, the cleaning and disinfection schedule was revised and optimised. Both the old and the new cleaning schedule are available in Supplementary File S1. Additionally, the environmental services staff responsible for cleaning and disinfection received substantial feedback and further training. Additional surfaces were included in the cleaning schedule, whereas others were not repeatedly sampled. Furthermore, the contact time of the disinfectants was increased.
Sampling period 2 was performed immediately after the revision of the cleaning schedule; sampling period 3, with a reduced sample size, was performed four months after the intervention.
Due to the highly variable detection of indicator pathogens during the sampling periods and in the different functional areas, statistical analysis was omitted, and a descriptive approach chosen.

2.2. Wound Infections

To identify potentially hospital-acquired infections with indicator pathogens, bacteriological samples of infected wounds were evaluated. Exclusively included in this study were samples of surgically created wounds in which the skin had been intact and surgically incised since traumatic injuries or older wounds may have been infected with indicator pathogens previously. As postoperative nosocomial wound infections usually manifest on the third day of hospitalisation at the earliest [24], only samples of wound infections occurring three days after surgery at the earliest were considered.
Samples of infected wounds were collected routinely and as clinically indicated. For this study, samples collected between October 2021 and June 2022 were considered. Therefore, considered wound samples were collected up to one month prior to the first sampling period until the end of the third sampling period. Since only clinically indicated samples were collected, an animal ethics approval application was not required. Upon admission, horse owners consented to the use of their horses’ anonymised data for scientific purposes.

2.3. Definition of Indicator Pathogens

In human medicine, nosocomial infections are often caused by the so-called ESKAPE pathogens, which comprise Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa and Enterobacter spp.
To adjust this selection of commonly multi-drug-resistant bacteria to an equine clinic, we added bacteria typically causing nosocomial (wound) infections in horses presented to our hospital. The equine-adapted ESKAPE-derived indicator pathogen panel was developed to investigate the occurrence of selected bacterial species of clinical and hygienic relevance in our equine hospital environment. The selection of microorganisms was based on their known or potential clinical relevance in horses, their role as opportunistic or wound-associated pathogens, and their relevance to environmental hygiene monitoring. Furthermore, the selection considered the clinical experience and pathogen spectrum encountered in our equine hospital and was designed as a targeted approach to monitoring selected bacterial species rather than as a comprehensive screening tool for all potential nosocomial pathogens. Accordingly, the detection of the selected microorganisms was performed at the species level, without specific characterisation of antimicrobial-resistance phenotypes. The panel focused on bacterial species considered relevant to equine wound infections and the hospital environment. Although Salmonella enterica is recognised as an important nosocomial pathogen in equine hospitals, it was not included as a specific target in the panel. Furthermore, methicillin-resistant Staphylococcus aureus (MRSA) was not investigated separately, as S. aureus detection was performed at the species level without antimicrobial susceptibility testing. The final selection of bacterial indicator pathogens included Streptococcus equi ssp. zooepidemicus, Staphylococcus aureus, Escherichia coli, Enterobacter cloacae, Enterococcus faecium, Enterococcus faecalis, Acinetobacter baumannii, Klebsiella pneumoniae and Pseudomonas aeruginosa.

2.4. Bacteriological Examinations

After sample collection, the samples were shipped cooled and overnight to Laboklin GmbH & Co. KG (Bad Kissingen, Germany). Upon arrival at the laboratory, the agar plates were incubated at +37 °C in an incubator. The incubation period was typically 48 h, and the plates were examined at both 24 and 48 h of incubation.
For identification of the bacteria, Matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry (MALDI-TOF-MS, Bruker, Bremen, Germany) was used.

3. Results

3.1. Detection of Indicator Pathogens in Surface Samples

Overall, indicator pathogens were detected in all sampling periods, with the highest number and diversity observed during sampling period 1. Acinetobacter spp. were the most frequently detected organisms in sampling period 1 (18/152), followed by Staphylococcus spp. (6/152), Enterococcus faecium (5/152), and Escherichia coli (5/152). Additionally, Pseudomonas spp. (4/152), Staphylococcus aureus (2/152), Enterococcus spp. (1/152), and Acinetobacter baumannii (1/152) were identified. In total, 39 (25.7%) samples tested positive for indicator pathogens (one sample 2 indicator pathogens, one sample 3 indicator pathogens). In sampling period 2, the overall detection frequency decreased, with Klebsiella pneumoniae emerging as the most frequently isolated pathogen (4/152), followed by Acinetobacter spp. (3/152) and Enterococcus faecium (3/152). Furthermore, Staphylococcus aureus (2/152), Escherichia coli (1/152), Pseudomonas spp. (1/152), Enterococcus faecalis (1/152), Enterobacter cloacae (1/152), and Streptococcus equi ssp. zooepidemicus (1/152) were detected. In total, 11.2% of the environmental samples tested positive for indicator pathogens in sampling period 2. In sampling period 3, fewer pathogens were identified overall in absolute numbers; however, 7.1% of the environmental samples tested positive for indicator pathogens. Pseudomonas spp. was the most frequently (2/42) isolated organism, followed by single detections of Staphylococcus aureus (1/42; Table 1).
Table 1. Overview of the detected indicator pathogens during the sampling periods (samples before and after cleaning and disinfection included).
Spatial distribution analysis showed that indicator pathogens were detected across multiple clinical areas, including isolation stables, intensive care stables, surgical theatres, induction and recovery areas, orthopaedic examination rooms, and medicine examination areas. Frequently contaminated sites included floors, stable door handles, mangers, walls, and medical equipment such as keyboards, ultrasound probes, endoscopes, and radiology equipment. Notably, several pathogens were detected both before and after cleaning and disinfection procedures. For example, Acinetobacter spp. were identified after disinfection on stable door handles, floors, and mangers in intensive care and isolation stables, as well as before disinfection on floors, equipment, and door handles in surgical and examination areas. Similarly, Enterococcus faecium, Escherichia coli, and Pseudomonas spp. were detected both before and after cleaning, indicating incomplete removal through routine hygiene measures. Staphylococcus aureus was detected after disinfection on examination tables and surgical door handles and before disinfection on thermometers and stable door handles. Klebsiella pneumoniae was exclusively detected before cleaning on surgical theatre floors, surgical equipment, and cleaning devices, suggesting potential reservoirs in the surgical environment. In sampling period 1, three surfaces tested positive for the same indicator pathogen before and after, 20 before and 13 after cleaning and disinfection. In sampling periods 2 and 3, no indicator pathogens were detected on the same surfaces before and after cleaning and disinfection. In sampling period 2, 12 surfaces tested positive before and five after cleaning and disinfection in sampling period three, the indicator pathogens on three surfaces were recovered after cleaning and disinfection. Overall, high-touch surfaces and floor areas represented the most frequent sites of contamination, and the persistence of indicator pathogens after cleaning highlights the potential for ongoing environmental reservoirs and the optimisation of cleaning and disinfection regimens within the clinical setting (Table 2).
Table 2. Location and relation to cleaning and disinfection of the detected indicator pathogens.

3.2. Detection of Indicator Pathogens in Wound Infections

In total, 125 samples of infected wounds were submitted. Of these, 38 were classified as nosocomial infections with indicator pathogens (mixed infections occurred). Of these 125 samples, 38 were classified as nosocomial, as they either originated from previously clean wounds or were taken during a timely close follow-up visit due to a wound infection associated with the performed surgery. Some of the submitted samples were taken as a precaution, while other wounds already showed signs of infection.
In the nosocomial wound infections, most frequently identified were Streptococcus equi ssp. zooepidemicus (n = 11), followed by Staphylococcus aureus (n = 8), and Escherichia coli (n = 8). Less frequently detected was Enterobacter cloacae (four samples). Neither Acinetobacter spp. nor Pseudomonas aeruginosa were detected in any of the collected wound samples. Streptococcus equi spp. zooepidemicus, Staphylococcus aureus, Escherichia coli, and Enterobacter cloacae were detected in both wound and surface samples, but a direct epidemiological link between individual cases was not possible, as no molecular typing was performed (Table 3).
Table 3. Overview of detected indicator pathogens in the 38 wounds with nosocomial infection (one mixed infection).

4. Discussion

This study evaluated environmental contamination with indicator pathogens in an equine teaching hospital across three sampling periods and assessed the impact of the revision of the cleaning and disinfection protocol and staff training after sampling period 1. The results demonstrate a progressive reduction in both the frequency and diversity of recovered pathogens over time, supporting the effectiveness of targeted infection prevention and control (IPC) interventions in the equine hospital environment. As antimicrobial susceptibility testing was not performed, no conclusions can be drawn regarding the antimicrobial resistance profiles of the detected isolates. The use of an equine-adapted ESKAPE-derived indicator pathogen panel was intended to assess the occurrence of selected bacterial species rather than to identify multidrug-resistant organisms.
During the first sampling period, multiple indicator organisms were detected across all tested functional areas of the clinic. Detected indicator pathogens included Acinetobacter spp., Enterococcus faecium, Escherichia coli, Pseudomonas spp. and Staphylococcus aureus.
High-touch surfaces such as door handles, keyboards, and medical equipment were identified as contaminated; furthermore, indicator pathogens were recovered both before and after cleaning and disinfection procedures.
These findings are consistent with previous reports describing widespread environmental contamination with diverse indicator pathogens in both equine and small animal hospitals, including intensive care units, surgical theatres, and isolation areas [25,26,27,28,29,30]. The detection of organisms following cleaning indicates that the original cleaning and disinfection procedures were insufficient to consistently eliminate environmental contamination.
After revision of the cleaning and disinfection schedule, a clear reduction in environmental contamination was observed during the second sampling period. However, the indicator pathogens were still identified after cleaning and disinfection but in fewer areas than after sampling period 1. This emphasises the previously reviewed possibility of survival or persistence of nosocomial pathogens on surfaces for months if inappropriate cleaning and disinfection procedures are employed [31].
In sampling period 2, fewer sampling sites yielded indicator pathogens, and some organisms identified previously were no longer detected. By the third sampling period, contamination with indicator pathogens had decreased further in absolute numbers, with only sporadic recovery of organisms such as Pseudomonas spp. and Staphylococcus aureus, but in looking at the relative numbers, an increase in their detection was observed. Notably, pathogens such as Acinetobacter baumannii and Klebsiella pneumoniae, detected earlier in the study, were not identified in the final sampling period. However, this observation must be interpreted carefully, since fewer environmental samples were collected in this sampling period. This reduction suggests that the revised cleaning and disinfection protocol as well as the staff training contributed to the observed reduction in detected indicator pathogens. Although direct causality cannot be definitively established, the temporal association strongly suggests that the revised cleaning and disinfection measures as well as the staff training contributed to the observed reduction as shown in sampling periods 2 and 3. The relative increase in indicator pathogens in sampling period 3 highlights the need for repeated staff training and ongoing optimisation of the cleaning and disinfection schedules in equine clinical environments.
It is worrying that some indicator pathogens were only detected after cleaning and disinfection. On the one hand, this may be due to a slightly different location being sampled than the one tested before cleaning and disinfection, but it may also indicate that the bacteria were present in the cleaning utensils, just like K. pneumoniae on the vacuum cleaner in this study, or there was bacterial resistance to the disinfection agent. Therefore, the selection of appropriate disinfectants, as mentioned as crucial in literature [32], was performed.
Studies in human medicine have shown that approximately 50% of the environment surrounding patients and intensive care surfaces were satisfactorily cleaned at baseline. After employment of a targeted control method (fluorescent targeting method) and providing substantial feedback to environmental services personnel, approximately 80% of the surfaces were cleaned adequately [33,34]—an effect that was also seen in this study though different indicators (fluorescence vs. presence of indicator pathogens) for adequate cleaning were used.
In the present study, high-touch surfaces and frequently handled equipment represented important contamination points, particularly during the first sampling period. This highlights the need to prioritise such sites within cleaning protocols—not only in equine but also in human clinics, these frequently handled, easily forgotten contact points are often insufficiently cleaned [33].
Effective environmental hygiene requires not only appropriate disinfectant selection but also correct dilution, adequate contact time, thorough mechanical cleaning and consistent adherence to the protocols [32]. Protocol revision and staff training likely improved one or more of these components in this study, which contributed to the reduction in detected indicator pathogens observed in later sampling periods.
Education and behavioural factors are also critical. Increased awareness among clinical and support staff may have improved compliance with hand hygiene, cleaning technique and biosecurity measures. For hand hygiene in human healthcare, for example, the World Health Organization recommends multimodal IPC strategies incorporating training, reminders and monitoring [35] since the combination of these strategies has proven to be more effective than protocol changes alone [36,37,38].
Despite encouraging results, some contamination persisted in surgical and examination areas during later sampling periods.
In addition to environmental contamination, several of the detected environmental indicator pathogens were also isolated from hospital-acquired wound infections, highlighting their clinical relevance and potential role in nosocomial transmission. The most frequently recovered organism from wound samples was Streptococcus equi ssp. zooepidemicus (n = 11), followed by Staphylococcus aureus and Escherichia coli (each n = 8), and Enterobacter cloacae (n = 4). The inclusion of horses with uncomplicated wound healing as a control group would have provided further insights into the occurrence of bacterial species in wounds without clinical signs of infection and helped to better understand the clinical relevance of the detected microorganisms. However, the findings of this study regarding bacteria involved in wound infection are consistent with the known epidemiology of equine wound infections, where streptococci, staphylococci and Gram-negative enteric organisms are common opportunistic pathogens [18,21,39,40]. The detection of Staphylococcus aureus, Escherichia coli and enterococci in both the hospital environment and clinical wound samples is of particular importance, as it suggests a potential link between environmental reservoirs and patient infections—however, horses may be colonised with these pathogens upon admission or during hospitalisation with and without antibiotic treatment [9,18,21,41].
Streptococcus equi ssp. zooepidemicus, the most frequently isolated wound pathogen in this study, is an opportunistic organism of the equine upper respiratory tract but is also an important opportunistic pathogen especially associated with respiratory disease [42,43,44].
Although it was only detected once in the environmental sampling, its high prevalence in wound infections suggests that endogenous flora and/or horse-to-horse transmission as well as adherence to a strict biosecurity protocol during bandage changes may also play a major role. Furthermore, it must be acknowledged that only a limited number of surfaces were sampled throughout the clinic, so that possible contamination with Streptococcus equi ssp. zooepidemicus might have been missed, which may have contributed to persistence and transmission within the hospital, particularly in high-risk areas.
Similarly, Staphylococcus aureus, isolated from both environmental samples and wounds, is a well-established cause of surgical-site infections in both humans, small animals, and horses [45,46,47,48]. Its ability to colonise skin, survive on dry surfaces and resist adverse environmental conditions enhances its transmission potential [49]. Environmental contamination with staphylococci therefore represents only one out of several significant risk factors for post-operative wound infections, particularly in surgical settings where invasive procedures compromise natural barriers [49].
The isolation of enteric organisms such as Escherichia coli and Enterobacter cloacae from wound infections further emphasises the importance of environmental hygiene, particularly in equine hospitals where faecal contamination is common since horses defaecate in their stables.
These organisms may be introduced into wounds directly from the patient’s own microbiota or indirectly via contaminated surfaces, equipment or personnel. Their presence in nosocomial wound infections highlights the need for strict adherence to cleaning, hand hygiene and aseptic techniques [5,15,50,51]. The use of culture-based methods and an incubation period of up to 48 h may have limited the detection of slow-growing or fastidious bacteria, which may have resulted in false-negative findings. Furthermore, the absence of molecular characterisation prevented a more detailed assessment of the genetic relatedness and potential transmission pathways of the bacterial isolates.
Importantly, some organisms detected in environmental samples during earlier sampling periods, such as Acinetobacter baumannii, were not isolated from wound infections in this study. This may reflect limited clinical transmission, effective infection prevention measures, or the opportunistic nature of these pathogens. Nevertheless, their presence in the hospital environment remains concerning due to their known ability to cause severe healthcare-associated infections [52,53,54].
Overall, the overlap between environmental and clinical isolates supports the hypothesis that the hospital environment may serve as a reservoir for opportunistic pathogens capable of causing wound infections. The reduction in environmental contamination observed after revision of the cleaning and disinfection protocol may therefore contribute not only to improved environmental hygiene but also to a reduced risk of nosocomial wound infections. These findings emphasise the importance of integrated infection prevention and control strategies addressing both environmental and patient-associated risk factors in equine hospitals.

5. Conclusions

This study shows that selected indicator pathogens, including equine-associated bacteria and members of the ESKAPEE group, can be found in the equine hospital environment and may play a role in nosocomial wound infections. Following improvements in cleaning and disinfection procedures and additional staff training, fewer bacterial detections were observed. However, some pathogens were still detected after cleaning and disinfection, highlighting the challenges of maintaining hygiene in a busy equine hospital. Although some bacterial species were found in both environmental and wound samples, a direct link between these findings could not be established. Overall, our results underline the importance of regular environmental monitoring, effective cleaning and disinfection practices, as well as continuous staff training. Further studies using molecular typing would help to better understand possible transmission routes between the hospital environment and equine patients.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/antibiotics15111091/s1, Supplementary File S1: Original and revised cleaning schedule.

Author Contributions

Conceptualisation, H.G., E.M., A.S. and S.D.S.; methodology, H.G.; validation, S.D.S. and A.S.; formal analysis, S.D.S. and A.S.; investigation, A.S.; data curation, S.D.S. and A.S.; writing—original draft, S.D.S.; writing—review and editing, S.D.S., A.S., E.M. and H.G.; supervision, H.G.; project administration, H.G. All authors have read and agreed to the published version of the manuscript.

Funding

The bacteriological examinations were sponsored by Laboklin GmbH, Bad Kissingen/Germany. The publication of this paper was supported by Open Access funds of Freie Universität Berlin.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to privacy restrictions.

Acknowledgments

The samples were collected and analysed as part of a dissertation project (A. Sauerwein).

Conflicts of Interest

Author E. Mueller is employed by the company Laboklin. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. Gehlen, H. Der Neue Hygienemanagement-Leitfaden 2020. Pferde Spieg. 2020, 23, 48–49. [Google Scholar] [CrossRef] [Scilit]
  2. Gehlen, H. Umgang Mit Antibiotikaresistenzen in Praxis Und Klinik. Leipz. Blaue Hefte 2020, 2, 174. [Google Scholar]
  3. Gehlen, H.; Klein, K.-S.; Stöckle, S.D.; Lübke-Becker, A.; Merle, R.; Köck, R.; Walther, B. Implementierung Und Evaluierung von Hygienemaßnahmen Zur Reduktion von Wundinfektionsraten in Einer Pferdeklinik. Pferdeheilkunde 2021, 37, 611–620. [Google Scholar] [CrossRef] [Scilit]
  4. Walther, B.; Janßen, T.; Gehlen, H.; Vincze, S.; Borchers, K.; Wieler, L.; Barton, A.; Lübke-Becker, A. Infektionsprävention und Hygienemanagement in Pferdekliniken. Berl. Munch. Tierarztl. Wochenschr. 2014, 127, 486–497. [Google Scholar] [CrossRef] [Scilit]
  5. Walther, B.; Lübke-Becker, A.; Stamm, I.; Gehlen, H.; Barton, A.K.; Janssen, T.; Wieler, L.H.; Guenther, S. Suspected Nosocomial Infections with Multi-Drug Resistant E. Coli, Including Extended-Spectrum Beta-Lactamase (ESBL)-Producing Strains, in an Equine Clinic. Berl. Munch. Tierarztl. Wochenschr. 2014, 127, 421–427. [Google Scholar] [CrossRef] [Scilit]
  6. Kauter, A.; Epping, L.; Ghazisaeedi, F.; Lübke-Becker, A.; Wolf, S.A.; Kannapin, D.; Stoeckle, S.D.; Semmler, T.; Günther, S.; Gehlen, H.; et al. Frequency, Local Dynamics, and Genomic Characteristics of ESBL-Producing Escherichia Coli Isolated from Specimens of Hospitalized Horses. Front. Microbiol. 2021, 12, 671676. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  7. Walther, B.; Klein, K.-S.; Barton, A.-K.; Semmler, T.; Huber, C.; Merle, R.; Tedin, K.; Mitrach, F.; Lübke-Becker, A.; Gehlen, H. Equine Methicillin-Resistant Sequence Type 398 Staphylococcus aureus (MRSA) Harbor Mobile Genetic Elements Promoting Host Adaptation. Front. Microbiol. 2018, 9, 2516. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  8. Scholtzek, A.D.; Hanke, D.; Walther, B.; Eichhorn, I.; Stöckle, S.D.; Klein, K.-S.; Gehlen, H.; Lübke-Becker, A.; Schwarz, S.; Feßler, A.T. Molecular Characterization of Equine Staphylococcus aureus Isolates Exhibiting Reduced Oxacillin Susceptibility. Toxins 2019, 11, 535. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  9. Walther, B.; Klein, K.-S.; Barton, A.-K.; Semmler, T.; Huber, C.; Wolf, S.A.; Tedin, K.; Merle, R.; Mitrach, F.; Guenther, S.; et al. Extended-Spectrum Beta-Lactamase (ESBL)-Producing Escherichia Coli and Acinetobacter Baumannii among Horses Entering a Veterinary Teaching Hospital: The Contemporary “Trojan Horse”. PLoS ONE 2018, 13, e0191873. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  10. Morley, P.S. Surveillance for Nosocomial Infections in Veterinary Hospitals. Vet. Clin. N. Am. Equine Pract. 2004, 20, 561–576. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  11. Benedict, K.M.; Morley, P.S.; Metre, D.C. Van Characteristics of Biosecurity and Infection Control Programs at Veterinary Teaching Hospitals. J. Am. Vet. Med. Assoc. 2008, 233, 767–773. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  12. Weese, J.S. A Review of Post-Operative Infections in Veterinary Orthopaedic Surgery. Vet. Comp. Orthop. Traumatol. 2008, 21, 99–105. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  13. Isgren, C.M.; Williams, N.J.; Fletcher, O.D.; Timofte, D.; Newton, R.J.; Maddox, T.W.; Clegg, P.D.; Pinchbeck, G.L. Antimicrobial Resistance in Clinical Bacterial Isolates from Horses in the UK. Equine Vet. J. 2022, 54, 390–414. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  14. Rice, L.B. Federal Funding for the Study of Antimicrobial Resistance in Nosocomial Pathogens: No ESKAPE. J. Infect. Dis. 2008, 197, 1079–1081. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  15. Maddox, T.W.; Clegg, P.D.; Williams, N.J.; Pinchbeck, G.L. Antimicrobial Resistance in Bacteria from Horses: Epidemiology of Antimicrobial Resistance. Equine Vet. J. 2015, 47, 756–765. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  16. Johns, I.C.; Adams, E.-L. Trends in Antimicrobial Resistance in Equine Bacterial Isolates: 1999–2012. Vet. Rec. 2015, 176, 334, Correction in Vet. Rec. 2016, 179, 330. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  17. Lawson, A.L.; Singleton, D.A.; Timofte, D.; William, N.J.; Pinchbeck, G.L. Equine Veterinary Surveillance Network (EVSNET): Occurrence and Resistance Patterns in ESKAPE Pathogens Isolated from Equine Clinical Submissions. Equine Vet. J. 2023, 55, 17–18. [Google Scholar] [CrossRef] [Scilit]
  18. Gehlen, H.; Klein, K.; Merle, R.; Lübke-Becker, A.; Stoeckle, S.D. Does Colonization with MRSA, ESBL—Producing Enterobacteriaceae, and/or Acinetobacter Baumannii—Increase the Risk for Postoperative Surgical Site Infection? Vet. Med. Sci. 2023, 9, 729–737. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  19. Stöckle, S.D.; Kannapin, D.A.; Kauter, A.M.L.; Lübke-Becker, A.; Walther, B.; Merle, R.; Gehlen, H. A Pilot Randomised Clinical Trial Comparing a Short-Term Perioperative Prophylaxis Regimen to a Long-Term Standard Protocol in Equine Colic Surgery. Antibiotics 2021, 10, 587. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  20. Kauter, A.; Brombach, J.; Lübke-Becker, A.; Kannapin, D.; Bang, C.; Franzenburg, S.; Stoeckle, S.D.; Mellmann, A.; Scherff, N.; Köck, R.; et al. Antibiotic Prophylaxis and Hospitalization of Horses Subjected to Median Laparotomy: Gut Microbiota Trajectories and Abundance Increase of Escherichia. Front. Microbiol. 2023, 14, 1228845. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  21. Stöckle, S.D.; Kannapin, D.A.; Merle, R.; Lübke-Becker, A.; Gehlen, H. Comparison of a Single-Shot Antibiotic Protocol Compared to a Conventional 5-Day Antibiotic Protocol in Equine Diagnostic Laparotomy Regarding Pre- and Postoperative Colonization with Multi-Drug-Resistant Indicator Pathogens. Antibiotics 2026, 15, 106. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  22. Sijtsema, M.; Stringer, T.; Hopman, N.E.M.; van der Graaf-van Bloois, L.; Duim, B.; van den Brom-Spierenburg, A.; Theelen, M.; Zomer, A.; Broens, E.M. Active Surveillance in an Equine Intensive Care Unit Identifies Clusters of ESKAPEE Pathogens in the Veterinary Hospital Environment. Vet. Microbiol. 2025, 303, 110439. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  23. Koirala, S.; Pantuzza, C.; Costa, M.d.O. Survival of Streptococcus equi subsp. zooepidemicus on Environmental Samples Is Affected by Material Type and Incubation Temperature. Vet. Res. Commun. 2023, 47, 2235–2240. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  24. Robert Koch-Institut. Robert-Koch-Institut Definitionen Nosokomialer Infektionen Für Die Surveillance Im Krankenhaus-Infektions- Surveillance-System (KISS-Definitionen) 2016; Robert Koch-Institut: Berlin, Germany, 2016. [Google Scholar] [CrossRef]
  25. Zendri, F.; Isgren, C.M.; Devaney, J.; Schmidt, V.; Rankin, R.; Timofte, D. Resistome-Based Surveillance Identifies ESKAPE Pathogens as the Predominant Gram-Negative Organisms Circulating in Veterinary Hospitals. Front. Microbiol. 2023, 14, 1252216. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  26. Bortolami, A.; Williams, N.J.; McGowan, C.M.; Kelly, P.G.; Archer, D.C.; Corrò, M.; Pinchbeck, G.; Saunders, C.J.; Timofte, D. Environmental Surveillance Identifies Multiple Introductions of MRSA CC398 in an Equine Veterinary Hospital in the UK, 2011–2016. Sci. Rep. 2017, 7, 5499. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  27. Murphy, C.P.; Reid-Smith, R.J.; Boerlin, P.; Weese, J.S.; Prescott, J.F.; Janecko, N.; Hassard, L.; McEwen, S.A. Escherichia Coli and Selected Veterinary and Zoonotic Pathogens Isolated from Environmental Sites in Companion Animal Veterinary Hospitals in Southern Ontario. Can. Vet. J. 2010, 51, 963–972. [Google Scholar] [PubMed]
  28. Lavigne, S.H.; Cole, S.D.; Daidone, C.; Rankin, S.C. Risk Factors for the Acquisition of a BlaNDM-5 Carbapenem-Resistant Escherichia Coli in a Veterinary Hospital. J. Am. Anim. Hosp. Assoc. 2021, 57, 101–105. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  29. Bernal-Rosas, Y.; Osorio-Muñoz, K.; Torres-García, O. Pseudomonas Aeruginosa: An Emerging Nosocomial Trouble in Veterinary. Rev. MVZ Cordoba 2015, 20, 4937–4946. [Google Scholar] [CrossRef] [Scilit]
  30. Burgess, B.A.; Morley, P.S. Risk Factors for Veterinary Hospital Environmental Contamination with Salmonella Enterica. Epidemiol. Infect. 2018, 146, 1282–1292. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  31. Kramer, A.; Schwebke, I.; Kampf, G. How Long Do Nosocomial Pathogens Persist on Inanimate Surfaces? A Systematic Review. BMC Infect. Dis. 2006, 6, 130. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  32. Rutala, W.A.; Weber, D.J. Disinfection, Sterilization, and Control of Hospital Waste. In Mandell, Douglas, and Bennett’s Principles and Practice of Infectious Diseases; Elsevier: Amsterdam, The Netherlands, 2014; pp. 3294–3309. [Google Scholar]
  33. Carling, P.C.; Parry, M.F.; Bruno-Murtha, L.A.; Dick, B. Improving Environmental Hygiene in 27 Intensive Care Units to Decrease Multidrug-Resistant Bacterial Transmission. Crit. Care Med. 2010, 38, 1054–1059. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  34. Carling, P.C.; Parry, M.M.; Rupp, M.E.; Po, J.L.; Dick, B.; Von Beheren, S. Improving Cleaning of the Environment Surrounding Patients in 36 Acute Care Hospitals. Infect. Control Hosp. Epidemiol. 2008, 29, 1035–1041. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  35. WHO Guidelines on Hand Hygiene in Health Care: First Global Patient Safety Challenge Clean Care Is Safer Care; World Health Organization: Geneva, Switzerland, 2009.
  36. Gholizad Gougjehyaran, H.; Motaarefi, H.; Sakhaei, S.; Ashrafi, M.; Zeinalpoor, S. The Effect of an Educational Program on Hand Hygiene Compliance among Nursing Students. BMC Nurs. 2025, 24, 411. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  37. Pittet, D.; Hugonnet, S.; Harbarth, S.; Mourouga, P.; Sauvan, V.; Touveneau, S.; Perneger, T.V. Effectiveness of a Hospital-Wide Programme to Improve Compliance with Hand Hygiene. Lancet 2000, 356, 1307–1312. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  38. Mu, X.; Xu, Y.; Yang, T.; Zhang, J.; Wang, C.; Liu, W.; Chen, J.; Tang, L.; Yang, H. Improving Hand Hygiene Compliance among Healthcare Workers: An Intervention Study in a Hospital in Guizhou Province, China. Braz. J. Infect. Dis. 2016, 20, 413–418. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  39. Patty, O.A. Streptococcus Equi subsp. zooepidemicus in New Zealand Horses. Master’s Thesis, The University of Waikato, Hamilton, New Zealand, 2012. [Google Scholar]
  40. Panchaud, Y.; Gerber, V.; Rossano, A.; Perreten, V. Bacterial Infections in Horses: A Retrospective Study at the University Equine Clinic of Bern. Schweiz. Arch. Tierheilkd. 2010, 152, 176–182. [Google Scholar] [CrossRef] [Scilit] [PubMed][Green Version]
  41. Johns, I.; Verheyen, K.; Good, L.; Rycroft, A. Antimicrobial Resistance in Faecal Escherichia Coli Isolates from Horses Treated with Antimicrobials: A Longitudinal Study in Hospitalised and Non-Hospitalised Horses. Vet. Microbiol. 2012, 159, 381–389. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  42. Anzai, T.; Walker, J.A.; Blair, M.B.; Chambers, T.M.; Timoney, J.E. Comparison of the Phenotypes of Streptococcus zooepidemicus Isolated from Tonsils of Healthy Horses and Specimens Obtained from Foals and Donkeys with Pneumonia. Am. J. Vet. Res. 2000, 61, 162–166. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  43. Newton, J.R.; Laxton, R.; Wood, J.L.N.; Chanter, N. Molecular Epidemiology of Streptococcus zooepidemicus Infection in Naturally Occurring Equine Respiratory Disease. Vet. J. 2008, 175, 338–345. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  44. Lindahl, S.B.; Aspán, A.; Båverud, V.; Paillot, R.; Pringle, J.; Rash, N.L.; Söderlund, R.; Waller, A.S. Outbreak of Upper Respiratory Disease in Horses Caused by Streptococcus Equi subsp. zooepidemicus ST-24. Vet. Microbiol. 2013, 166, 281–285. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  45. Cerullo, A.; Di Nicola, M.R.; Scilimati, N.; Bertoletti, A.; Pollicino, G.; Moroni, B.; Pepe, M.; Nannarone, S.; Gialletti, R.; Passamonti, F. Intra- and Post-Operative Bacteriological Surveys of Surgical Site in Horses: A Single-Centre Study. Microorganisms 2025, 13, 928. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  46. Humphreys, H. Staphylococcus aureus: The Enduring Pathogen in Surgery. Surgeon 2012, 10, 357–360. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  47. Owens, C.D.; Stoessel, K. Surgical Site Infections: Epidemiology, Microbiology and Prevention. J. Hosp. Infect. 2008, 70, 3–10. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  48. Vincze, S.; Stamm, I.; Kopp, P.A.; Hermes, J.; Adlhoch, C.; Semmler, T.; Wieler, L.H.; Lübke-Becker, A.; Walther, B. Alarming Proportions of Methicillin-Resistant Staphylococcus aureus (MRSA) in Wound Samples from Companion Animals, Germany 2010–2012. PLoS ONE 2014, 9, e85656, Correction in PLoS ONE 2014, 9, e96965. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  49. Morris, D.O.; Cole, S.D. The Epidemiology of Antimicrobial Resistance and Transmission of Cutaneous Bacterial Pathogens in Domestic Animals. J. Am. Vet. Med. Assoc. 2023, 261, S122–S129. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  50. Apostolakos, I.; Franz, E.; van Hoek, A.H.A.M.; Florijn, A.; Veenman, C.; Sloet-van Oldruitenborgh-Oosterbaan, M.M.; Dierikx, C.; van Duijkeren, E. Occurrence and Molecular Characteristics of ESBL/AmpC-Producing Escherichia Coli in Faecal Samples from Horses in an Equine Clinic. J. Antimicrob. Chemother. 2017, 72, 1915–1921. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  51. Singaravelu, A.; Leggett, B.; Leonard, F.C. Improving Infection Control in a Veterinary Hospital: A Detailed Study on Patterns of Faecal Contamination to Inform Changes in Practice. Ir. Vet. J. 2023, 76, 4. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  52. van der Kolk, J.H.; Endimiani, A.; Graubner, C.; Gerber, V.; Perreten, V. Acinetobacter in Veterinary Medicine, with an Emphasis on Acinetobacter Baumannii. J. Glob. Antimicrob. Resist. 2019, 16, 59–71. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  53. Turton, J.F.; Shah, J.; Ozongwu, C.; Pike, R. Incidence of Acinetobacter Species Other than A. Baumannii among Clinical Isolates of Acinetobacter: Evidence for Emerging Species. J. Clin. Microbiol. 2010, 48, 1445–1449. [Google Scholar] [CrossRef] [Scilit] [PubMed]
  54. Rühl-Teichner, J.; Jacobmeyer, L.; Leidner, U.; Semmler, T.; Ewers, C. Genomic Diversity, Antimicrobial Susceptibility, and Biofilm Formation of Clinical Acinetobacter Baumannii Isolates from Horses. Microorganisms 2023, 11, 556. [Google Scholar] [CrossRef] [Scilit] [PubMed]
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