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High Prevalence of Multidrug-Resistant Community-Acquired Methicillin-Resistant Staphylococcus aureus at the Largest Veterinary Teaching Hospital in Costa Rica

High Prevalence of Multidrug-Resistant Community-Acquired Methicillin-Resistant Staphylococcus... Methicillin-resistant Staphylococcus aureus (MRSA) is a pathogen associated with severe infections in companion animals present in the community, and it is diagnosed in animals admitted to veterinary hospitals. However, reports that describe the circulation of MRSA in animal populations and veterinary settings in Latin America are scarce. Therefore, the objective of this study was to determine the prevalence and investigate the molecular epidemiology of MRSA in the environment of the largest veterinary teaching hospital in Costa Rica. Preselected contact surfaces were sampled twice within a 6-week period. Antimicrobial resistance, SCCmec type, Panton-Valentine leukocidin screening, USA type, and clonality were assessed in all recovered isolates. Overall, MRSA was isolated from 26.5% (27/102) of the surfaces sampled, with doors, desks, and examination tables most frequently contaminated. Molecular analysis demonstrated a variety of surfaces from different sections of the hospital contaminated by three highly related clones/pulsotypes. All, but one of the isolates were characterized as multidrug-resistant SCCmec type IV-USA700, a strain sporadically described in other countries and often classified as community acquired. The detection and frequency of this unique strain in this veterinary setting suggest Costa Rica has a distinctive MRSA ecology when compared with other countries/regions. The high level of environmental contamination highlights the necessity to establish and enforce standard cleaning and disinfection protocols to minimize further spread of this pathogen and reduce the risk of nosocomial and/or occupational transmission of MRSA. Keywords: environment, MRSA, USA700, veterinary hospital Introduction In the case of Costa Rica, the Pan American Health Or- ganization reports that the prevalence of MRSA among orldwide, methicillin-resistant Staphylococcus hospital-associated S. aureus isolates has increased from 45% Waureus (MRSA) is a well-known pathogen associated to 70% between 2002 and 2007 (PAHO). These data are also with severe infections in hospitals and the community supported by two recent studies performed at the National (McDougal et al. 2003, Otter and French 2010, Chuang and Children’s Hospital of Costa Rica, where 44–61% of the S. Huang 2013, CDC 2016). In Latin America, reports of MRSA aureus isolates collected at the hospital’s bacteriology labo- colonization and infections are scarce. Nonetheless, this patho- ratory were classified as methicillin resistant (Jimenez- gen is considered one of the leading causes of nosocomial in- Truque et al. 2014, Yock-Corrales et al. 2014). fections in human hospitals, with prevalence ranging from 6% in In companion animal veterinary hospitals, MRSA outbreaks Cuba to as high as 80% in Chile and Peru (Loureiro et al. 2000, have been reported in patients and personnel in numerous PAHO 2005, Ribeiro et al. 2005, Guzman-Blanco et al. 2009). countries (Leonard et al. 2006, van Duijkeren et al. 2010, Programa de Investigacio´n en Enfermedades Tropicales (PIET), Escuela de Medicina Veterinaria, Universidad Nacional, Heredia, Costa Rica. Centro de Investigacio´n en Enfermedades Tropicales (CIET), Facultad de Microbiolog´ıa, Universidad de Costa Rica, San Jose´, Costa Rica. Department of Veterinary Preventive Medicine, College of Veterinary Medicine, The Ohio State University, Columbus, Ohio. Division of Epidemiology, The Ohio State University, Columbus, Ohio. ª Irene Rojas et al. 2017; Published by Mary Ann Liebert, Inc. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 645 646 ROJAS ET AL. Schwaber et al. 2013, Gro¨nlund Andersson et al. 2014, sampling was repeated. Surfaces were categorized as human, Steinman et al. 2015). However, reports describing the circu- animal, or mixed (human and animal) contact as previously lation of MRSA in animal populations and veterinary settings described (Hoet et al. 2011) (Table 1). Human contact sur- in Latin America are scarce. Only two peer-reviewed publi- faces were defined as those contacted by multiple people and cations appear to be available on this subject. One of them out of reach for animals (e.g., doors); animal contact surfaces describes the presence of MRSA in pigs in Peru (Arriola et al. were those primarily in direct contact with multiple animals 2011) and the second publication reports the prevalence of (e.g., examination tables); and mixed contact surfaces were MRSA among dogs and cats in Brazil, where only one cat was those in contact with both people and animals (e.g., ultra- positive (Quitoco et al. 2013). sound transducers). These surfaces were selected based on It is well known that MRSA can survive in the environ- the fact that they are highly touched or enter in direct human/ ment for long periods of time and remain infectious (Wa- animal contact multiple times a day. genvoort et al. 2000, Kramer et al. 2006). In fact, it has been At the time of this study, the HEMS-UNA had no stan- suggested that contaminated contact surfaces within veteri- dardized cleaning and disinfection protocols in place. Instead, nary settings could have been involved in the transmission of an informal routine was used, including one person in charge MRSA to patients (Van Balen et al. 2014). As a result, contact of the general cleaning (e.g., floor, doors, glasses, restrooms, surfaces have been considered a plausible reservoir for this and offices) and veterinary assistants and students in charge of pathogen and a potential source for nosocomial and occu- cleaning the work surfaces (e.g., examination tables, cages, pational infections within veterinary hospitals (Weese 2004, equipment, and surgery tables). General cleaning was per- Bergstrom et al. 2012b, Van Balen et al. 2013). As such, strict formed twice daily. Most commonly used cleaning products measures for the control and prevention of MRSA trans- included bleach and commercial disinfectant formulas. mission within veterinary settings are indicated. In recent years, the Veterinary Hospital of Minor Species Sampling techniques and processing and Wildlife of the Veterinary Medicine School at The Na- Two sampling techniques were used depending of the size of tional University of Costa Rica (HEMS-UNA, Spanish ac- the surface to be sampled (Hoet et al. 2011). Electrostatic cloths ronym for Hospital de Especies Menores y Silvestres de la (Swiffer ; Proctor and Gamble, Cincinnati, OH) were used to Universidad Nacional) experienced a number of small-scale sample large surfaces to be able to cover the entire area of the MRSA outbreaks involving veterinary students and per- surface (e.g., examination tables and cages). Cotton swabs sonnel. However, since the epidemiology of MRSA in premoistened in sterile trypticase soy broth (TSB, Becton; veterinary hospitals in Latin America is unknown, targeted Dickinson and Company, Sparks, MD) were used to sample implementation of specific interventions (including cleaning small surfaces (e.g., telephones and soap dispensers) (Table 1). and disinfection protocols) has been limited. For this reason, In some cases, multiple items of the same surface type (e.g., we performed a multiple-point cross-sectional study to de- two or more muzzles) or simply multiple surfaces (e.g.,ex- termine the presence and characteristics of MRSA strains on amination tables and doors) in the same area were sampled as a contact surfaces at the only academic referral veterinary pool with the same cloth or swab (Table 1). These samples are hospital in Costa Rica. referred to as pooled samples throughout this article. The aims of this study were as follows: (1) document the After sampling, electrostatic cloths were folded and placed extent of MRSA environmental contamination at HEMS- in a sterile bag to which TSB was added. In the case of cotton UNA, (2) identify the most commonly contaminated surfaces swabs, they were placed in sterile tubes with 2 mL of TSB. that could later be targeted for active cleaning and disinfec- All samples were incubated aerobically at 35C for 24 h as tion, (3) phenotypically and genotypically characterize all previously described (Weese et al. 2004, Hoet et al. 2011). MRSA isolates to establish epidemiological significance and For quality assurance, negative and positive controls were plausible origin of strains, and (4) to study its ecology in such included in every sampling. a setting. Isolation and identification Materials and Methods Staphylococcal isolation and characterization were per- Locations and surfaces sampled formed as previously described (Hoet et al. 2011). Plausible This cross-sectional study was conducted at the only ter- S. aureus isolates were confirmed with the VITEK identifier tiary referral and teaching veterinary hospital in Costa Rica Compact 2 (Biome`riux , Marcy l’Etoile, France) using the (HEMS-UNA) from May to June 2013. During this year, the GP card. Mannitol salt agar plates with 2 lg/mL oxacillin referral hospital received *3472 patients. Nearly 80% of (Sigma, Saint Louis, MO) were used to phenotypically test these cases required hospitalization with a 6-day average for methicillin resistance. hospitalization time. The hospital provides the following services: internal medicine, dermatology, neurology, ortho- mecA confirmation, Staphylococcal chromosome pedics, surgery, physical therapy, oncology, intensive care, cassette mec typing, Panton-Valentine leukocidin imaging (ultrasonography, radiology, and endoscopy), and screening, and pulse-field gel electrophoresis laboratory. The equipment and personnel in these services are used with both domestic and wildlife species (i.e., monkeys, Presence of the mecA gene and SCCmec types (I–VI) were parrots, macaws, raccoons, turtles, hamsters, rabbits, and big determined in all MRSA isolates (Borraz Orda´z 2006, Mil- wild felines, among others). heirico et al. 2007) using the following S. aureus strains as An initial sampling of 51 surfaces (Table 1), representing controls: ATCC 43300 (Type II), ANS46 (Type III), WIS *80% of the facility, was completed. Six weeks later, this (Type V), and HDE288 (Type VI). In addition, all isolates CA-MRSA AT A VETERINARY HOSPITAL IN COSTA RICA 647 Table 1. Environmental Contact Surfaces Sampled at the Veterinary Hospital of Minor Species and Wildlife of the Veterinary Medicine School at the National University of Costa Rica (HEMS-UNA) Location Human contact Animal contact Mixed contact a :b Examination room 1 Light switches n/a Examination table, door, and equipment a :b Examination room 3 Light switches n/a Examination table, door, and equipment :c Feline internal medicine Faucet Cages n/a :d :e Doors Examination tables :f :g Internal medicine A Chairs Examination tables n/a :d :h Doors Cages (small) : :i Office desk Cages (large) Medical record’s desk Keyboards Phone Light switch : :h Internal medicine B Door Cages (small) n/a :i Light switches Cages (large) Examination table : :e Ultrasound room Door Examination tables Ultrasound transducers :k Radiology room n/a n/a Examination table and doors :l Lead vests and cassettes Physical therapy room n/a n/a Physical therapy pool walls :m :e Presurgery room Cabinet drawers Examination tables n/a :d Doors Presurgery hall Soap dispensers n/a n/a Shelf handles :g Surgery rooms n/a Surgery tables n/a Warming pad Oxygen monitor : :h Orthopedic ward 1 Door Cages n/a : :h Orthopedic ward 2 Door Cages n/a : :i Infectious diseases ward Door Cages n/a Examination table : :o Miscellaneous Refrigerator Gurneys n/a Microwave Muzzles a q Light switches Bowls Washer and dryer controls Sample collected with swab. Sample collected with electrostatic cloth. Two light switches were sampled as a pool. One table, one door, and room equipment (stethoscope, rectal thermometer, and hand soap dispenser) were sampled as a pool. Eight cages were sampled as a pool. Two doors were sampled as a pool. Two tables were sampled as a pool. Four chairs were sampled as a pool. Four tables were sampled as a pool. Four cages were sampled as a pool. Three cages were sampled as a pool. Two keyboards were sampled as a pool. One table and two doors were sampled as a pool. Four vests and two cassettes were sampled as a pool. Two cabinets were sampled as a pool. Two dispensers were sampled as a pool. Two gurneys were sampled as a pool. Six muzzles were sampled as a pool. Ten bowls were sampled as a pool. n/a, not applied. were screened for the presence of Panton-Valentine leuko- (Van Balen et al. 2013, CDC/Pulse-Net) using the Salmonella cidin (PVL) genes (Lina et al. 1999) using NRS123 (form the serotype Branderup strain H9812 digested with XbaIasa Network on Antimicrobial Resistance in S. aureus) and molecular size marker. Strains with ‡ 98% similarity were ATCC 43300 as positive and negative controls, respectively. considered the same clone, and a similarity coefficient of Pulse-field gel electrophoresis (PFGE) of SmaI-digested ‡ 80% was selected to define clusters of highly related clones chromosomal DNA was performed as previously described (Van Balen et al. 2013). Designation of USA types was 648 ROJAS ET AL. performed comparing our isolates to a CDC (Centers for the three types of surfaces (human, animal, and mixed con- Disease Control and Prevention) database containing 100 tact), no statistical difference was observed ( p £ 0.16). S. aureus strains with the most typical band patterns for each Of the 27 MRSA-positive surfaces, only 4 (the faucet USA type, using >80% similarity as the cutoff point. This [isolate numbers I.6a, I.6b, and II.6a] and doors [I.7 and II.7b] database was provided by the Antimicrobial Resistance and of the feline internal medicine area, and the examination ta- Characterization Laboratory, Clinical and Environmental bles [I.11a and II.11] and large cages [I.16b and II.16b] of Microbiology Branch, Division of Healthcare Quality Pro- internal medicine A area) were contaminated on both sam- motion of the CDC (Atlanta, GA). pling dates. None of the MRSA strains found on these four surfaces (from the first and second sampling) were clonal, but they were highly related (Fig. 1). Antimicrobial susceptibility test (phenotyping) Since, in some cases, only two samples (one from each Kirby-Bauer disc diffusion (CLSI 2013) was used to detect sampling date) were collected per surface, proportion of antimicrobial susceptibility to the following: ampicillin (10 lg), contamination by surface will only be discussed in those with amoxicillin–clavulanic acid (20–10 lg), cephalothin (30 lg), a representative number of samples. In the case of human chloramphenicol (30 lg), doxycycline (30 lg), and enrofloxacin contact surfaces, 31.3% (5/16) of the access doors and 25.0% (5 lg). In addition, the VITEK 2 Compact using the AST-P577 (1/4) of the desks used by the personnel were MRSA positive. card was used to determine susceptibility to the following: On the other hand, among animal contact surfaces, 37.5% (6/ amikacin, cefoxitin, ciprofloxacin, clindamycin, erythromycin, 16) of the cages and 28.6% (4/14) of the examination-surgery gentamicin, levofloxacin, linezolid, minocycline, moxifloxacin, tables were found MRSA positive. nitrofurantoin, oxacillin, quinupristin–dalfopristin, rifampin, teicoplanin, trimethoprim–sulfamethoxazole, tetracycline, and Genotypic analysis vancomycin. MRSA ATCC 43300 and methicillin-susceptible S. aureus ATCC 25923 were used as control strains with rec- From the 27 MRSA-positive surfaces, a total of 28 isolates ognized susceptibility breakpoints described by the Clinical were phenotypically and genotypically characterized (2 isolates Laboratory Standards Institute (CLSI 2013). Multidrug resis- were obtained from the faucets in the feline internal medicine tance was defined as resistance to three or more classes of an- ward during the first sampling and determined to be 2 different timicrobials, including beta-lactams, as previously described MRSA clones). The presence of the mecA gene was confirmed in (Hoet et al. 2011). all 28 MRSA isolates, and all of them were characterized as SCCmec type IV. PVL screening revealed 6/28 (21.4%) positive isolates (Fig. 1). Based on their PFGE patterns, 27 isolates were Data analysis classified as USA700 (of which 6 were PVL positive) and 1 as The data were analyzed and described separately accord- USA800 (PVL negative) (Fig. 1); both clones are usually con- ing to type of contact surfaces (human, animal, or mixed). A sidered community-acquired MRSA (CA-MRSA). chi-squared test was conducted to compare the relationship Dendrogram analysis revealed that all but one isolate were between human, animal, and mixed contact surfaces. Statis- highly related and distributed in a single cluster, represented by tical significance was determined at the cutoff value of 0.05 three pulsotypes (Fig. 1). It was also noted that some MRSA ( p £ 0.05). strains (isolates sharing the same phenotypic profile, SCCmec type and pulsotype) were contaminating different areas of the Results hospital during the same sampling date. Examples of this con- tamination pattern include isolates I.10, I.20, I.27a, and I.32a Environmental MRSA detection (found in internal medicine A, internal medicine B, radiology A total of 102 environmental samples were collected at the room, and presurgery room, respectively, during the first sam- HEMS-UNA. Overall, 40.2% (41/102) and 26.5% (27/102) pling) and II.6a, II.14b, II.30a, and II.36 (found in the feline of the surfaces sampled were positive for S. aureus and internal medicine, internal medicine A, presurgery room, and the MRSA, respectively. On average, 49.0% (50/102) of the surgery room, respectively, during the second sampling) (Fig. 1). surfaces sampled were classified as human contact, 39.2% as (40/102) animal contact, and 11.8% as (12/102) mixed con- Antimicrobial susceptibility tact. Table 2 summarizes the distribution of MRSA con- tamination by type of contact surface and sampling period. Ten antimicrobial-resistant profiles were identified from When comparing the overall prevalence of MRSA between 28 MRSA isolates (Table 3). All 27 USA700 isolates showed Table 2. Prevalence of Methicillin-Resistant Staphylococcus aureus in Human, Animal, and Mixed Contact Surfaces at the Veterinary Hospital of Minor Species and Wildlife of the Veterinary Medicine School at the National University of Costa Rica (HEMS-UNA) Human contact MRSA/ Animal contact MRSA/ Mixed contact MRSA/ Total MRSA/ samples collected (%) samples collected (%) samples collected (%) samples collected (%) First sampling 7/25 (28.0) 7/20 (35.0) 2/6 (33.3) 16/51 (31.4) Second sampling 5/25 (20.0) 5/20 (25.0) 1/6 (16.7) 11/51 (21.6) Total 12/50 (24.0) 12/40 (30.0) 3/12 (25.0) 27/102 (26.5) MRSA, methicillin-resistant Staphylococcus aureus. 649 FIG. 1. Dendogram of methicillin-resistant Staphylococcus aureus isolates obtained from the environment at the Veterinary Hospital of Minor Species and Wildlife of the Veterinary Medicine School at the National University of Costa Rica (HEMS-UNA). Amk, amikacin; Gen, gentamicin; Amc, amoxicillin–clavulanic acid; Amp, ampicillin; Oxa, oxacillin; Cep, cephalothin; Cli, clindamycin; Ery, erythromycin; Chl, chloramphenicol; Eno, enrofloxacin; Cip, ciprofloxacin; Sxt, trimethoprim–sulfamethoxazole; Dox, doxycycline; Tet, tetracycline. 650 ROJAS ET AL. Table 3. Antimicrobial Resistance Profiles of Methicillin-Resistant Staphylococcus aureus Environmental Isolates from the Veterinary Hospital of Minor Species and Wildlife of the Veterinary Medicine School at the National University of Costa Rica (HEMS-UNA) Phenotypic profile No. of Abx classes No. of isolates % AmkAmpOxa 2 1 3.6 AmpAmcOxaCepCliEryEnoCip 4 1 3.6 AmkGenAmcAmpOxaCepCliEryCip 5 1 3.6 AmkGenAmcAmpOxaCepCliEryEnoCip 5 17 60.7 AmkGenAmcAmpOxaCepCliEryChlEnoCip 6 1 3.6 AmkGenAmcAmpOxaCepCliEryEnoCipDoxTet 6 1 3.6 AmkGenAmcAmpOxaCepCliEryEnoCipTet 6 3 10.7 AmkGenAmcAmpOxaCepCliEryCipSxt 6 1 3.6 AmkGenAmcAmpOxaCepCliEryChlEnoCipSxtTet 8 1 3.6 AmkGenAmpOxaCepCliEryChlEnoCipSxtTet 8 1 3.6 Abx, antibiotic; Amk, amikacin; Gen, gentamicin; Amc, amoxicillin–clavulanic acid; Amp, ampicillin; Oxa, oxacillin; Cep, cephalothin; Cli, clindamycin; Ery, erythromycin; Chl, chloramphenicol, Eno, enrofloxacin; Cip, ciprofloxacin; Sxt, trimethoprim–sulfamethoxazole; Dox, doxycycline; Tet, tetracycline. a high level of multidrug resistance with complex phenotypic Hoet et al. 2011, Van Balen et al. 2013) and, as mentioned, it profiles. In this group, 66.7% (18/27), 18.5% (5/27), and is in contrast to the predominant presence of HA-MRSA 7.4% (2/27) were resistant to 5, 6, and 8 antimicrobial classes, strains that are usually described in similar settings. respectively. In contrast, the USA800 was only resistant to The wide variety of contaminated contact surfaces across beta-lactams and aminoglycosides. None of the clindamycin- different areas of the HEMS-UNA with multidrug-resistant resistant isolates showed inducible resistance. All MRSA MRSA is concerning. Of the 51 surfaces selected to be isolates were susceptible to levofloxacin, linezolid, minocy- sampled, almost half (23/51) were found positive on either cline, nitrofurantoin, quinupristin–dalfopristin, rifampin, one or both sampling dates. The most prevalent surfaces in teicoplanin, and vancomycin. this study, doors, desks, cages, and examination tables, have also been described as commonly contaminated in other studies (Oie et al. 2002, Hoet et al. 2011, Bergstro¨m et al. Discussion 2012b, Van Balen et al. 2013), probably due to the fact that This study reports the high level of environmental con- they are touched by numerous people and/or animals several tamination (26.5%) with a multidrug-resistant CA-MRSA times per day. Once contaminated, a surface could become a in the largest veterinary teaching hospital in Costa Rica. potential source for on-going MRSA transmission. Of interest is the fact that, in other areas of the world (pri- The fact that 21.4% of the MRSA isolates found in the marily North America, Europe, and some countries in Asia), hospital environment harbored PVL genes is also concerning. similar settings have described HA-MRSA outnumbering PVL is a leukocidal toxin that has been suggested to increase community-associated strains in regard to environmental the virulence potential of CA-MRSA strains and is often contamination (Loeffler et al. 2005, Heller et al. 2009, Hoet associated with severe skin and soft tissue infections (Boyle- et al. 2011, Bergstro¨m et al. 2012a, Van Balen et al. 2013,). In Vavra and Daum 2007, Wu et al. 2010, Guillen et al. 2016, addition, the MRSA strain described in this study (USA700) Hewagama et al. 2016, Immergluck et al. 2017). Outbreaks of does not seem to be particularly prevalent in other countries MRSA-PVL-positive strains have been reported in both (Tenover et al. 2008, 2012, Otter and French 2010, Chuang healthcare and community settings, in some cases involving and Huang 2013, Hoet et al. 2013, Hidalgo et al. 2015). healthy individuals with no MRSA-associated risk factors However, it has been commonly suggested that the pre- (Tang et al. 2007, Maltezou et al. 2009, Higashiyama et al. dominant MRSA strain(s) present in a healthcare setting is 2011). These studies highlight how MRSA-PVL-positive strains could be easily spread (to other individuals and/or the usually a reflection of the most prevalent clones found in the environment) within a particular facility, especially when ap- general community served by that healthcare facility. It ap- pears that this holds true in Costa Rica, where recent studies propriate precautions (including—but not exclusive to—in- found USA700 was the most common strain type associated fection control, preventive measures, and personal hygiene) with MRSA soft tissue and invasive infections in children are not followed. (Jimenez-Truque et al. 2014, Yock-Corrales et al. 2014). At HEMS-UNA in particular, this environmental investi- Unfortunately, to date, few studies have investigated gation was performed after a number of small-scale undoc- MRSA (especially in animal populations) in Latin America umented MRSA outbreaks occurred among students and (Guzma´n-Blanco et al. 2009, Rodrı´guez-Noriega et al. 2010, staff. Even though it is not possible to determine the role that Arriola et al. 2011, Quitoco et al. 2013, Jimenez-Truque et al. the hospital environment could have played during the out- 2014, Yock-Corrales et al. 2014), which makes this study breaks, two conclusions could be drawn based on our results. unique, but limits the authors’ ability to analyze and interpret First, the high level of environmental contamination clearly the results. Nonetheless, the 26.5% CA-MRSA prevalence demonstrates that MRSA-PVL-positive and MRSA-PVL- found in the environment was almost twice as high as the negative strains are being introduced and spread throughout prevalence reported in other regions (Weese et al. 2004, the hospital, probably facilitated by inadequate cleaning and Loeffler et al. 2005, Heller et al. 2009, Murphy et al. 2010, disinfection. Second, the presence of MRSA-PVL-positive CA-MRSA AT A VETERINARY HOSPITAL IN COSTA RICA 651 isolates on a number of high-contact surfaces increases the relevant differences between veterinary hospitals (including exposure levels of personnel (occupational) and patients infrastructure and management), the possibility of extrapo- (nosocomial) to this highly pathogenic bacterium. lating our results to other settings is limited. Still, this is the From the occupational point of view, it has been found that first study reporting MRSA environmental contamination in a up to 42% of healthcare workers’ hands become ‘‘contami- veterinary teaching hospital in Central America, and could be nated’’ after being in contact with surfaces present in rooms used as a starting point for other countries in the same region. of patients infected with MRSA (Boyce et al. 1997, Bhalla et al. 2004). On their own, contaminated hands are not Conclusion equivalent to being colonized or infected with this pathogen, It is noteworthy and concerning to identify a multidrug- but it does increase the probability of either of these two resistant CA-MRSA strain (USA700), unfrequently reported scenarios to occur. In addition, contaminated hands could be in other countries, contaminating 26.5% surfaces at the involved in the transmission of MRSA to other coworkers largest veterinary teaching hospital in Costa Rica. In addi- and patients, as well as the contamination of other surfaces tion, 92.8% of the isolates recovered were resistant to ‡ 5 and/or areas of the hospital. antimicrobial classes and 21.4% were PVL positive, which From the nosocomial point of view, it is important to translate to a higher risk of life-threatening infections if recognize that animal patients often have direct and pro- nosocomial or occupational transmission of these highly longed contact with their surroundings (e.g., sniffing, licking, pathogenic bacteria were to occur within this setting. Since or lying on the floor), in this case, the hospital environment. USA700 has also been associated with soft tissue and inva- This reality increases the exposure to surfaces that, if con- sive infections (i.e., infectious endocarditis) in children in taminated, could potentially lead to the development of this country, further research is needed to understand if in- MRSA infections, especially in patients with open wounds or deed Costa Rica has a unique MRSA ecology in which this that are immunocompromised. Moreover, this is even more strain thrives. In conclusion, this report showed that the ep- concerning in those areas of the hospital where patients un- idemiology and ecology of MRSA in veterinary hospitals are dergo invasive procedures. Such is the case of the presurgery not universal, a fact that must be recognized by the veterinary and surgery rooms, where all of the animal contact surfaces community when managing this pathogen in their practices. sampled were found positive for MRSA. Due to the scope and design of this study, it is difficult to Acknowledgments determine the source(s) of the MRSA strains present in the HEMS-UNA environment. Nonetheless, PFGE results showed We wish to thank the personnel from the Bacteriology that all but one of the isolates were clonally related, suggesting a Laboratory (National University and University of Costa horizontal dissemination and/or independent introduction from a Rica) for their technical and logistical assistance, and Carlos common or few sources. During the environmental sampling ´ ´ ´ ´ Chacon-Dıaz, Yeimy Ramırez, and Jose PabloSolanofor their dates, there were no known clinical cases treated or hospitalized technical assistance and helpful discussions. The following re- with MRSA infections at the hospital. Therefore, an unidentified agent was provided by the Network on Antimicrobial Re- infected/colonized animal(s) and/or human(s) entering the hos- sistance in Staphylococcus aureus (NARSA) for distribution by pital is the most likely source responsible for introducing the BEIResources,NIAID,NIH: Staphylococcus aureus,Strain MRSA strain into the hospital. C1999000459 (NRS123) as a PVL-positive control. Once inside the hospital, inadequate cleaning/disinfection and lax biosecurity/prevention protocols were the most Author Disclosure Statement probable factors contributing to the dissemination of MRSA across the veterinary facility. This hypothesis is based on No competing financial interests exist. facts discussed in previous studies, where the implementation of appropriate and targeted cleaning and disinfection proto- References cols can effectively reduce MRSA environmental contami- Arriola C, Gu¨ere M, Larsen J, Skov R, et al. Presence of nation (Rampling et al. 2001, Boyce et al. 2009, Jinadatha methicillin-resistant Staphylococcus aureus in pigs in Peru. et al. 2015, Yuen et al. 2015, Semret et al. 2016). PLoS One 2011; 6:e28529. Considering the plausible occupational and nosocomial Bergstro¨m A, Gustafsson C, Leander M, Fredriksson M, et al. implications of a heavily contaminated environment in a Occurrence of methicillin-resistant Staphylococci in surgi- veterinary hospital, it is critical to improve current cleaning cally treated dogs and the environment in a Swedish animal and disinfection practices at the HEMS-UNA. Based on the hospital. J Small Anim Pract 2012a; 53:404–410. results obtained from this study, the administration has already Bergstro¨m K, Nyman G, Widgren S, Johnston C, et al. Infection started to develop a more standardized and adequate protocol prevention and control interventions in the first outbreak of customized to meet the HEMS-UNA needs in regard to pre- methicillin-resistant Staphylococcus aureus infections in an vention and control of MRSA and other important nosoco- equine hospital in Sweden. Acta Vet Scand 2012b; 54:14. mial pathogens. Future studies will be needed to evaluate the Bhalla A, Pults N, Gries D, Ray A, et al. Acquisition of noso- effectiveness and compliance of the hospital’s personnel to comial pathogens on hands after contact with environmental the newly established protocols. surfaces near hospitalized patients. Infect Control Hosp Epi- Last, samplings were performed for a short period of time, demiol 2004; 25:164–167. limiting our ability to evaluate the movement and mainte- ´ ´ Borraz Ordaz C. Epidemiologıa de la Resistencia a Meticilina nance of MRSA in the hospital environment. 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PLoS Yuen J, Chung T, Loke A. Methicillin-resistant Staphylococcus One 2007; 2:e:822. aureus (MRSA) contamination in bedside surfaces of a hos- Tenover F, McAllister S, Fosheim G, McDougal L, et al. pital wardand the potential effectiveness of enhanced disin- Characterization of Staphylococcus aureus isolates from na- fection with an antimicrobial polymer surfactant. Int J Environ sal cultures collected from individuals in the United States in Res Public Health 2015; 12:3026–3041. 2001 to 2004. J Clin Microbiol 2008; 46:2837–2841. Tenover F, Tickler I, Goering R, Kreiswirth B, et al. Char- Address correspondence to: acterization of nasal and blood culture isolates of methicillin- Armando E. Hoet resistant Staphylococcus aureus from patients in United Department of Veterinary Preventive Medicine States Hospitals. Antimicrob Agents Chemother 2012; 56: College of Veterinary Medicine 1324–1330. The Ohio State University Van Balen J, Kelley C, Nava-Hoet R, Bateman S, et al. Presence, 1920 Coffey Road distribution and molecular epidemiology of methicillin- Columbus, OH 43210 resistant Staphylococcus aureus in a small animal teaching hospital: A year-long active surveillance targeting dogs and E-mail: hoet.1@osu.edu http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Vector Borne and Zoonotic Diseases Pubmed Central

High Prevalence of Multidrug-Resistant Community-Acquired Methicillin-Resistant Staphylococcus aureus at the Largest Veterinary Teaching Hospital in Costa Rica

Vector Borne and Zoonotic Diseases , Volume 17 (9) – Sep 1, 2017

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Pubmed Central
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© Irene Rojas et al. 2017; Published by Mary Ann Liebert, Inc.
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1530-3667
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1557-7759
DOI
10.1089/vbz.2017.2145
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Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) is a pathogen associated with severe infections in companion animals present in the community, and it is diagnosed in animals admitted to veterinary hospitals. However, reports that describe the circulation of MRSA in animal populations and veterinary settings in Latin America are scarce. Therefore, the objective of this study was to determine the prevalence and investigate the molecular epidemiology of MRSA in the environment of the largest veterinary teaching hospital in Costa Rica. Preselected contact surfaces were sampled twice within a 6-week period. Antimicrobial resistance, SCCmec type, Panton-Valentine leukocidin screening, USA type, and clonality were assessed in all recovered isolates. Overall, MRSA was isolated from 26.5% (27/102) of the surfaces sampled, with doors, desks, and examination tables most frequently contaminated. Molecular analysis demonstrated a variety of surfaces from different sections of the hospital contaminated by three highly related clones/pulsotypes. All, but one of the isolates were characterized as multidrug-resistant SCCmec type IV-USA700, a strain sporadically described in other countries and often classified as community acquired. The detection and frequency of this unique strain in this veterinary setting suggest Costa Rica has a distinctive MRSA ecology when compared with other countries/regions. The high level of environmental contamination highlights the necessity to establish and enforce standard cleaning and disinfection protocols to minimize further spread of this pathogen and reduce the risk of nosocomial and/or occupational transmission of MRSA. Keywords: environment, MRSA, USA700, veterinary hospital Introduction In the case of Costa Rica, the Pan American Health Or- ganization reports that the prevalence of MRSA among orldwide, methicillin-resistant Staphylococcus hospital-associated S. aureus isolates has increased from 45% Waureus (MRSA) is a well-known pathogen associated to 70% between 2002 and 2007 (PAHO). These data are also with severe infections in hospitals and the community supported by two recent studies performed at the National (McDougal et al. 2003, Otter and French 2010, Chuang and Children’s Hospital of Costa Rica, where 44–61% of the S. Huang 2013, CDC 2016). In Latin America, reports of MRSA aureus isolates collected at the hospital’s bacteriology labo- colonization and infections are scarce. Nonetheless, this patho- ratory were classified as methicillin resistant (Jimenez- gen is considered one of the leading causes of nosocomial in- Truque et al. 2014, Yock-Corrales et al. 2014). fections in human hospitals, with prevalence ranging from 6% in In companion animal veterinary hospitals, MRSA outbreaks Cuba to as high as 80% in Chile and Peru (Loureiro et al. 2000, have been reported in patients and personnel in numerous PAHO 2005, Ribeiro et al. 2005, Guzman-Blanco et al. 2009). countries (Leonard et al. 2006, van Duijkeren et al. 2010, Programa de Investigacio´n en Enfermedades Tropicales (PIET), Escuela de Medicina Veterinaria, Universidad Nacional, Heredia, Costa Rica. Centro de Investigacio´n en Enfermedades Tropicales (CIET), Facultad de Microbiolog´ıa, Universidad de Costa Rica, San Jose´, Costa Rica. Department of Veterinary Preventive Medicine, College of Veterinary Medicine, The Ohio State University, Columbus, Ohio. Division of Epidemiology, The Ohio State University, Columbus, Ohio. ª Irene Rojas et al. 2017; Published by Mary Ann Liebert, Inc. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 645 646 ROJAS ET AL. Schwaber et al. 2013, Gro¨nlund Andersson et al. 2014, sampling was repeated. Surfaces were categorized as human, Steinman et al. 2015). However, reports describing the circu- animal, or mixed (human and animal) contact as previously lation of MRSA in animal populations and veterinary settings described (Hoet et al. 2011) (Table 1). Human contact sur- in Latin America are scarce. Only two peer-reviewed publi- faces were defined as those contacted by multiple people and cations appear to be available on this subject. One of them out of reach for animals (e.g., doors); animal contact surfaces describes the presence of MRSA in pigs in Peru (Arriola et al. were those primarily in direct contact with multiple animals 2011) and the second publication reports the prevalence of (e.g., examination tables); and mixed contact surfaces were MRSA among dogs and cats in Brazil, where only one cat was those in contact with both people and animals (e.g., ultra- positive (Quitoco et al. 2013). sound transducers). These surfaces were selected based on It is well known that MRSA can survive in the environ- the fact that they are highly touched or enter in direct human/ ment for long periods of time and remain infectious (Wa- animal contact multiple times a day. genvoort et al. 2000, Kramer et al. 2006). In fact, it has been At the time of this study, the HEMS-UNA had no stan- suggested that contaminated contact surfaces within veteri- dardized cleaning and disinfection protocols in place. Instead, nary settings could have been involved in the transmission of an informal routine was used, including one person in charge MRSA to patients (Van Balen et al. 2014). As a result, contact of the general cleaning (e.g., floor, doors, glasses, restrooms, surfaces have been considered a plausible reservoir for this and offices) and veterinary assistants and students in charge of pathogen and a potential source for nosocomial and occu- cleaning the work surfaces (e.g., examination tables, cages, pational infections within veterinary hospitals (Weese 2004, equipment, and surgery tables). General cleaning was per- Bergstrom et al. 2012b, Van Balen et al. 2013). As such, strict formed twice daily. Most commonly used cleaning products measures for the control and prevention of MRSA trans- included bleach and commercial disinfectant formulas. mission within veterinary settings are indicated. In recent years, the Veterinary Hospital of Minor Species Sampling techniques and processing and Wildlife of the Veterinary Medicine School at The Na- Two sampling techniques were used depending of the size of tional University of Costa Rica (HEMS-UNA, Spanish ac- the surface to be sampled (Hoet et al. 2011). Electrostatic cloths ronym for Hospital de Especies Menores y Silvestres de la (Swiffer ; Proctor and Gamble, Cincinnati, OH) were used to Universidad Nacional) experienced a number of small-scale sample large surfaces to be able to cover the entire area of the MRSA outbreaks involving veterinary students and per- surface (e.g., examination tables and cages). Cotton swabs sonnel. However, since the epidemiology of MRSA in premoistened in sterile trypticase soy broth (TSB, Becton; veterinary hospitals in Latin America is unknown, targeted Dickinson and Company, Sparks, MD) were used to sample implementation of specific interventions (including cleaning small surfaces (e.g., telephones and soap dispensers) (Table 1). and disinfection protocols) has been limited. For this reason, In some cases, multiple items of the same surface type (e.g., we performed a multiple-point cross-sectional study to de- two or more muzzles) or simply multiple surfaces (e.g.,ex- termine the presence and characteristics of MRSA strains on amination tables and doors) in the same area were sampled as a contact surfaces at the only academic referral veterinary pool with the same cloth or swab (Table 1). These samples are hospital in Costa Rica. referred to as pooled samples throughout this article. The aims of this study were as follows: (1) document the After sampling, electrostatic cloths were folded and placed extent of MRSA environmental contamination at HEMS- in a sterile bag to which TSB was added. In the case of cotton UNA, (2) identify the most commonly contaminated surfaces swabs, they were placed in sterile tubes with 2 mL of TSB. that could later be targeted for active cleaning and disinfec- All samples were incubated aerobically at 35C for 24 h as tion, (3) phenotypically and genotypically characterize all previously described (Weese et al. 2004, Hoet et al. 2011). MRSA isolates to establish epidemiological significance and For quality assurance, negative and positive controls were plausible origin of strains, and (4) to study its ecology in such included in every sampling. a setting. Isolation and identification Materials and Methods Staphylococcal isolation and characterization were per- Locations and surfaces sampled formed as previously described (Hoet et al. 2011). Plausible This cross-sectional study was conducted at the only ter- S. aureus isolates were confirmed with the VITEK identifier tiary referral and teaching veterinary hospital in Costa Rica Compact 2 (Biome`riux , Marcy l’Etoile, France) using the (HEMS-UNA) from May to June 2013. During this year, the GP card. Mannitol salt agar plates with 2 lg/mL oxacillin referral hospital received *3472 patients. Nearly 80% of (Sigma, Saint Louis, MO) were used to phenotypically test these cases required hospitalization with a 6-day average for methicillin resistance. hospitalization time. The hospital provides the following services: internal medicine, dermatology, neurology, ortho- mecA confirmation, Staphylococcal chromosome pedics, surgery, physical therapy, oncology, intensive care, cassette mec typing, Panton-Valentine leukocidin imaging (ultrasonography, radiology, and endoscopy), and screening, and pulse-field gel electrophoresis laboratory. The equipment and personnel in these services are used with both domestic and wildlife species (i.e., monkeys, Presence of the mecA gene and SCCmec types (I–VI) were parrots, macaws, raccoons, turtles, hamsters, rabbits, and big determined in all MRSA isolates (Borraz Orda´z 2006, Mil- wild felines, among others). heirico et al. 2007) using the following S. aureus strains as An initial sampling of 51 surfaces (Table 1), representing controls: ATCC 43300 (Type II), ANS46 (Type III), WIS *80% of the facility, was completed. Six weeks later, this (Type V), and HDE288 (Type VI). In addition, all isolates CA-MRSA AT A VETERINARY HOSPITAL IN COSTA RICA 647 Table 1. Environmental Contact Surfaces Sampled at the Veterinary Hospital of Minor Species and Wildlife of the Veterinary Medicine School at the National University of Costa Rica (HEMS-UNA) Location Human contact Animal contact Mixed contact a :b Examination room 1 Light switches n/a Examination table, door, and equipment a :b Examination room 3 Light switches n/a Examination table, door, and equipment :c Feline internal medicine Faucet Cages n/a :d :e Doors Examination tables :f :g Internal medicine A Chairs Examination tables n/a :d :h Doors Cages (small) : :i Office desk Cages (large) Medical record’s desk Keyboards Phone Light switch : :h Internal medicine B Door Cages (small) n/a :i Light switches Cages (large) Examination table : :e Ultrasound room Door Examination tables Ultrasound transducers :k Radiology room n/a n/a Examination table and doors :l Lead vests and cassettes Physical therapy room n/a n/a Physical therapy pool walls :m :e Presurgery room Cabinet drawers Examination tables n/a :d Doors Presurgery hall Soap dispensers n/a n/a Shelf handles :g Surgery rooms n/a Surgery tables n/a Warming pad Oxygen monitor : :h Orthopedic ward 1 Door Cages n/a : :h Orthopedic ward 2 Door Cages n/a : :i Infectious diseases ward Door Cages n/a Examination table : :o Miscellaneous Refrigerator Gurneys n/a Microwave Muzzles a q Light switches Bowls Washer and dryer controls Sample collected with swab. Sample collected with electrostatic cloth. Two light switches were sampled as a pool. One table, one door, and room equipment (stethoscope, rectal thermometer, and hand soap dispenser) were sampled as a pool. Eight cages were sampled as a pool. Two doors were sampled as a pool. Two tables were sampled as a pool. Four chairs were sampled as a pool. Four tables were sampled as a pool. Four cages were sampled as a pool. Three cages were sampled as a pool. Two keyboards were sampled as a pool. One table and two doors were sampled as a pool. Four vests and two cassettes were sampled as a pool. Two cabinets were sampled as a pool. Two dispensers were sampled as a pool. Two gurneys were sampled as a pool. Six muzzles were sampled as a pool. Ten bowls were sampled as a pool. n/a, not applied. were screened for the presence of Panton-Valentine leuko- (Van Balen et al. 2013, CDC/Pulse-Net) using the Salmonella cidin (PVL) genes (Lina et al. 1999) using NRS123 (form the serotype Branderup strain H9812 digested with XbaIasa Network on Antimicrobial Resistance in S. aureus) and molecular size marker. Strains with ‡ 98% similarity were ATCC 43300 as positive and negative controls, respectively. considered the same clone, and a similarity coefficient of Pulse-field gel electrophoresis (PFGE) of SmaI-digested ‡ 80% was selected to define clusters of highly related clones chromosomal DNA was performed as previously described (Van Balen et al. 2013). Designation of USA types was 648 ROJAS ET AL. performed comparing our isolates to a CDC (Centers for the three types of surfaces (human, animal, and mixed con- Disease Control and Prevention) database containing 100 tact), no statistical difference was observed ( p £ 0.16). S. aureus strains with the most typical band patterns for each Of the 27 MRSA-positive surfaces, only 4 (the faucet USA type, using >80% similarity as the cutoff point. This [isolate numbers I.6a, I.6b, and II.6a] and doors [I.7 and II.7b] database was provided by the Antimicrobial Resistance and of the feline internal medicine area, and the examination ta- Characterization Laboratory, Clinical and Environmental bles [I.11a and II.11] and large cages [I.16b and II.16b] of Microbiology Branch, Division of Healthcare Quality Pro- internal medicine A area) were contaminated on both sam- motion of the CDC (Atlanta, GA). pling dates. None of the MRSA strains found on these four surfaces (from the first and second sampling) were clonal, but they were highly related (Fig. 1). Antimicrobial susceptibility test (phenotyping) Since, in some cases, only two samples (one from each Kirby-Bauer disc diffusion (CLSI 2013) was used to detect sampling date) were collected per surface, proportion of antimicrobial susceptibility to the following: ampicillin (10 lg), contamination by surface will only be discussed in those with amoxicillin–clavulanic acid (20–10 lg), cephalothin (30 lg), a representative number of samples. In the case of human chloramphenicol (30 lg), doxycycline (30 lg), and enrofloxacin contact surfaces, 31.3% (5/16) of the access doors and 25.0% (5 lg). In addition, the VITEK 2 Compact using the AST-P577 (1/4) of the desks used by the personnel were MRSA positive. card was used to determine susceptibility to the following: On the other hand, among animal contact surfaces, 37.5% (6/ amikacin, cefoxitin, ciprofloxacin, clindamycin, erythromycin, 16) of the cages and 28.6% (4/14) of the examination-surgery gentamicin, levofloxacin, linezolid, minocycline, moxifloxacin, tables were found MRSA positive. nitrofurantoin, oxacillin, quinupristin–dalfopristin, rifampin, teicoplanin, trimethoprim–sulfamethoxazole, tetracycline, and Genotypic analysis vancomycin. MRSA ATCC 43300 and methicillin-susceptible S. aureus ATCC 25923 were used as control strains with rec- From the 27 MRSA-positive surfaces, a total of 28 isolates ognized susceptibility breakpoints described by the Clinical were phenotypically and genotypically characterized (2 isolates Laboratory Standards Institute (CLSI 2013). Multidrug resis- were obtained from the faucets in the feline internal medicine tance was defined as resistance to three or more classes of an- ward during the first sampling and determined to be 2 different timicrobials, including beta-lactams, as previously described MRSA clones). The presence of the mecA gene was confirmed in (Hoet et al. 2011). all 28 MRSA isolates, and all of them were characterized as SCCmec type IV. PVL screening revealed 6/28 (21.4%) positive isolates (Fig. 1). Based on their PFGE patterns, 27 isolates were Data analysis classified as USA700 (of which 6 were PVL positive) and 1 as The data were analyzed and described separately accord- USA800 (PVL negative) (Fig. 1); both clones are usually con- ing to type of contact surfaces (human, animal, or mixed). A sidered community-acquired MRSA (CA-MRSA). chi-squared test was conducted to compare the relationship Dendrogram analysis revealed that all but one isolate were between human, animal, and mixed contact surfaces. Statis- highly related and distributed in a single cluster, represented by tical significance was determined at the cutoff value of 0.05 three pulsotypes (Fig. 1). It was also noted that some MRSA ( p £ 0.05). strains (isolates sharing the same phenotypic profile, SCCmec type and pulsotype) were contaminating different areas of the Results hospital during the same sampling date. Examples of this con- tamination pattern include isolates I.10, I.20, I.27a, and I.32a Environmental MRSA detection (found in internal medicine A, internal medicine B, radiology A total of 102 environmental samples were collected at the room, and presurgery room, respectively, during the first sam- HEMS-UNA. Overall, 40.2% (41/102) and 26.5% (27/102) pling) and II.6a, II.14b, II.30a, and II.36 (found in the feline of the surfaces sampled were positive for S. aureus and internal medicine, internal medicine A, presurgery room, and the MRSA, respectively. On average, 49.0% (50/102) of the surgery room, respectively, during the second sampling) (Fig. 1). surfaces sampled were classified as human contact, 39.2% as (40/102) animal contact, and 11.8% as (12/102) mixed con- Antimicrobial susceptibility tact. Table 2 summarizes the distribution of MRSA con- tamination by type of contact surface and sampling period. Ten antimicrobial-resistant profiles were identified from When comparing the overall prevalence of MRSA between 28 MRSA isolates (Table 3). All 27 USA700 isolates showed Table 2. Prevalence of Methicillin-Resistant Staphylococcus aureus in Human, Animal, and Mixed Contact Surfaces at the Veterinary Hospital of Minor Species and Wildlife of the Veterinary Medicine School at the National University of Costa Rica (HEMS-UNA) Human contact MRSA/ Animal contact MRSA/ Mixed contact MRSA/ Total MRSA/ samples collected (%) samples collected (%) samples collected (%) samples collected (%) First sampling 7/25 (28.0) 7/20 (35.0) 2/6 (33.3) 16/51 (31.4) Second sampling 5/25 (20.0) 5/20 (25.0) 1/6 (16.7) 11/51 (21.6) Total 12/50 (24.0) 12/40 (30.0) 3/12 (25.0) 27/102 (26.5) MRSA, methicillin-resistant Staphylococcus aureus. 649 FIG. 1. Dendogram of methicillin-resistant Staphylococcus aureus isolates obtained from the environment at the Veterinary Hospital of Minor Species and Wildlife of the Veterinary Medicine School at the National University of Costa Rica (HEMS-UNA). Amk, amikacin; Gen, gentamicin; Amc, amoxicillin–clavulanic acid; Amp, ampicillin; Oxa, oxacillin; Cep, cephalothin; Cli, clindamycin; Ery, erythromycin; Chl, chloramphenicol; Eno, enrofloxacin; Cip, ciprofloxacin; Sxt, trimethoprim–sulfamethoxazole; Dox, doxycycline; Tet, tetracycline. 650 ROJAS ET AL. Table 3. Antimicrobial Resistance Profiles of Methicillin-Resistant Staphylococcus aureus Environmental Isolates from the Veterinary Hospital of Minor Species and Wildlife of the Veterinary Medicine School at the National University of Costa Rica (HEMS-UNA) Phenotypic profile No. of Abx classes No. of isolates % AmkAmpOxa 2 1 3.6 AmpAmcOxaCepCliEryEnoCip 4 1 3.6 AmkGenAmcAmpOxaCepCliEryCip 5 1 3.6 AmkGenAmcAmpOxaCepCliEryEnoCip 5 17 60.7 AmkGenAmcAmpOxaCepCliEryChlEnoCip 6 1 3.6 AmkGenAmcAmpOxaCepCliEryEnoCipDoxTet 6 1 3.6 AmkGenAmcAmpOxaCepCliEryEnoCipTet 6 3 10.7 AmkGenAmcAmpOxaCepCliEryCipSxt 6 1 3.6 AmkGenAmcAmpOxaCepCliEryChlEnoCipSxtTet 8 1 3.6 AmkGenAmpOxaCepCliEryChlEnoCipSxtTet 8 1 3.6 Abx, antibiotic; Amk, amikacin; Gen, gentamicin; Amc, amoxicillin–clavulanic acid; Amp, ampicillin; Oxa, oxacillin; Cep, cephalothin; Cli, clindamycin; Ery, erythromycin; Chl, chloramphenicol, Eno, enrofloxacin; Cip, ciprofloxacin; Sxt, trimethoprim–sulfamethoxazole; Dox, doxycycline; Tet, tetracycline. a high level of multidrug resistance with complex phenotypic Hoet et al. 2011, Van Balen et al. 2013) and, as mentioned, it profiles. In this group, 66.7% (18/27), 18.5% (5/27), and is in contrast to the predominant presence of HA-MRSA 7.4% (2/27) were resistant to 5, 6, and 8 antimicrobial classes, strains that are usually described in similar settings. respectively. In contrast, the USA800 was only resistant to The wide variety of contaminated contact surfaces across beta-lactams and aminoglycosides. None of the clindamycin- different areas of the HEMS-UNA with multidrug-resistant resistant isolates showed inducible resistance. All MRSA MRSA is concerning. Of the 51 surfaces selected to be isolates were susceptible to levofloxacin, linezolid, minocy- sampled, almost half (23/51) were found positive on either cline, nitrofurantoin, quinupristin–dalfopristin, rifampin, one or both sampling dates. The most prevalent surfaces in teicoplanin, and vancomycin. this study, doors, desks, cages, and examination tables, have also been described as commonly contaminated in other studies (Oie et al. 2002, Hoet et al. 2011, Bergstro¨m et al. Discussion 2012b, Van Balen et al. 2013), probably due to the fact that This study reports the high level of environmental con- they are touched by numerous people and/or animals several tamination (26.5%) with a multidrug-resistant CA-MRSA times per day. Once contaminated, a surface could become a in the largest veterinary teaching hospital in Costa Rica. potential source for on-going MRSA transmission. Of interest is the fact that, in other areas of the world (pri- The fact that 21.4% of the MRSA isolates found in the marily North America, Europe, and some countries in Asia), hospital environment harbored PVL genes is also concerning. similar settings have described HA-MRSA outnumbering PVL is a leukocidal toxin that has been suggested to increase community-associated strains in regard to environmental the virulence potential of CA-MRSA strains and is often contamination (Loeffler et al. 2005, Heller et al. 2009, Hoet associated with severe skin and soft tissue infections (Boyle- et al. 2011, Bergstro¨m et al. 2012a, Van Balen et al. 2013,). In Vavra and Daum 2007, Wu et al. 2010, Guillen et al. 2016, addition, the MRSA strain described in this study (USA700) Hewagama et al. 2016, Immergluck et al. 2017). Outbreaks of does not seem to be particularly prevalent in other countries MRSA-PVL-positive strains have been reported in both (Tenover et al. 2008, 2012, Otter and French 2010, Chuang healthcare and community settings, in some cases involving and Huang 2013, Hoet et al. 2013, Hidalgo et al. 2015). healthy individuals with no MRSA-associated risk factors However, it has been commonly suggested that the pre- (Tang et al. 2007, Maltezou et al. 2009, Higashiyama et al. dominant MRSA strain(s) present in a healthcare setting is 2011). These studies highlight how MRSA-PVL-positive strains could be easily spread (to other individuals and/or the usually a reflection of the most prevalent clones found in the environment) within a particular facility, especially when ap- general community served by that healthcare facility. It ap- pears that this holds true in Costa Rica, where recent studies propriate precautions (including—but not exclusive to—in- found USA700 was the most common strain type associated fection control, preventive measures, and personal hygiene) with MRSA soft tissue and invasive infections in children are not followed. (Jimenez-Truque et al. 2014, Yock-Corrales et al. 2014). At HEMS-UNA in particular, this environmental investi- Unfortunately, to date, few studies have investigated gation was performed after a number of small-scale undoc- MRSA (especially in animal populations) in Latin America umented MRSA outbreaks occurred among students and (Guzma´n-Blanco et al. 2009, Rodrı´guez-Noriega et al. 2010, staff. Even though it is not possible to determine the role that Arriola et al. 2011, Quitoco et al. 2013, Jimenez-Truque et al. the hospital environment could have played during the out- 2014, Yock-Corrales et al. 2014), which makes this study breaks, two conclusions could be drawn based on our results. unique, but limits the authors’ ability to analyze and interpret First, the high level of environmental contamination clearly the results. Nonetheless, the 26.5% CA-MRSA prevalence demonstrates that MRSA-PVL-positive and MRSA-PVL- found in the environment was almost twice as high as the negative strains are being introduced and spread throughout prevalence reported in other regions (Weese et al. 2004, the hospital, probably facilitated by inadequate cleaning and Loeffler et al. 2005, Heller et al. 2009, Murphy et al. 2010, disinfection. Second, the presence of MRSA-PVL-positive CA-MRSA AT A VETERINARY HOSPITAL IN COSTA RICA 651 isolates on a number of high-contact surfaces increases the relevant differences between veterinary hospitals (including exposure levels of personnel (occupational) and patients infrastructure and management), the possibility of extrapo- (nosocomial) to this highly pathogenic bacterium. lating our results to other settings is limited. Still, this is the From the occupational point of view, it has been found that first study reporting MRSA environmental contamination in a up to 42% of healthcare workers’ hands become ‘‘contami- veterinary teaching hospital in Central America, and could be nated’’ after being in contact with surfaces present in rooms used as a starting point for other countries in the same region. of patients infected with MRSA (Boyce et al. 1997, Bhalla et al. 2004). On their own, contaminated hands are not Conclusion equivalent to being colonized or infected with this pathogen, It is noteworthy and concerning to identify a multidrug- but it does increase the probability of either of these two resistant CA-MRSA strain (USA700), unfrequently reported scenarios to occur. In addition, contaminated hands could be in other countries, contaminating 26.5% surfaces at the involved in the transmission of MRSA to other coworkers largest veterinary teaching hospital in Costa Rica. In addi- and patients, as well as the contamination of other surfaces tion, 92.8% of the isolates recovered were resistant to ‡ 5 and/or areas of the hospital. antimicrobial classes and 21.4% were PVL positive, which From the nosocomial point of view, it is important to translate to a higher risk of life-threatening infections if recognize that animal patients often have direct and pro- nosocomial or occupational transmission of these highly longed contact with their surroundings (e.g., sniffing, licking, pathogenic bacteria were to occur within this setting. Since or lying on the floor), in this case, the hospital environment. USA700 has also been associated with soft tissue and inva- This reality increases the exposure to surfaces that, if con- sive infections (i.e., infectious endocarditis) in children in taminated, could potentially lead to the development of this country, further research is needed to understand if in- MRSA infections, especially in patients with open wounds or deed Costa Rica has a unique MRSA ecology in which this that are immunocompromised. Moreover, this is even more strain thrives. In conclusion, this report showed that the ep- concerning in those areas of the hospital where patients un- idemiology and ecology of MRSA in veterinary hospitals are dergo invasive procedures. Such is the case of the presurgery not universal, a fact that must be recognized by the veterinary and surgery rooms, where all of the animal contact surfaces community when managing this pathogen in their practices. sampled were found positive for MRSA. Due to the scope and design of this study, it is difficult to Acknowledgments determine the source(s) of the MRSA strains present in the HEMS-UNA environment. Nonetheless, PFGE results showed We wish to thank the personnel from the Bacteriology that all but one of the isolates were clonally related, suggesting a Laboratory (National University and University of Costa horizontal dissemination and/or independent introduction from a Rica) for their technical and logistical assistance, and Carlos common or few sources. During the environmental sampling ´ ´ ´ ´ Chacon-Dıaz, Yeimy Ramırez, and Jose PabloSolanofor their dates, there were no known clinical cases treated or hospitalized technical assistance and helpful discussions. The following re- with MRSA infections at the hospital. Therefore, an unidentified agent was provided by the Network on Antimicrobial Re- infected/colonized animal(s) and/or human(s) entering the hos- sistance in Staphylococcus aureus (NARSA) for distribution by pital is the most likely source responsible for introducing the BEIResources,NIAID,NIH: Staphylococcus aureus,Strain MRSA strain into the hospital. C1999000459 (NRS123) as a PVL-positive control. Once inside the hospital, inadequate cleaning/disinfection and lax biosecurity/prevention protocols were the most Author Disclosure Statement probable factors contributing to the dissemination of MRSA across the veterinary facility. This hypothesis is based on No competing financial interests exist. facts discussed in previous studies, where the implementation of appropriate and targeted cleaning and disinfection proto- References cols can effectively reduce MRSA environmental contami- Arriola C, Gu¨ere M, Larsen J, Skov R, et al. 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Presence, 1920 Coffey Road distribution and molecular epidemiology of methicillin- Columbus, OH 43210 resistant Staphylococcus aureus in a small animal teaching hospital: A year-long active surveillance targeting dogs and E-mail: hoet.1@osu.edu

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Vector Borne and Zoonotic DiseasesPubmed Central

Published: Sep 1, 2017

References