Open-access Resistance profile and biofilm production of microorganisms isolated in operating rooms

Perfil de resistencia y producción de biopelículas de microorganismos aislados en quirófanos

  • SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Objectives:  to evaluate the resistance profile and biofilm formation in isolates from operating rooms in two hospitals in the southwestern region of Goiás.

Methods:  an experimental laboratory study was conducted, with samples collected between March and August 2023.

Results:  of the 50 samples collected, 104 bacteria were isolated, 81.7% (85/104) gram-positive and 18.3% (19/104) gram-negative. Of these, 55.3% (47/85) of the Staphylococcus genus were classified as multidrug-resistant and methicillin-resistant, and 15.7% (3/19) of the Gram-negative bacteria were classified as multidrug-resistant. 66.34% (69/104) were biofilm producers, with 79.7% (55/69) being Gram-positive and 20.3% (14/69) Gram-negative.

Conclusions:  this finding is of great concern, as these microorganisms in hospital environments pose a high risk for surgical site infections that are difficult to treat due to multidrug-resistant strains.

Descriptors:
Surgicenters; Cross Infection; Microbial Drug Resistance; Staphylococcus aureus; Biofilms.

RESUMO

Objetivos:  avaliar o perfil de resistência e formação de biofilme em isolados de centros cirúrgicos de 2 hospitais da região sudoeste de Goiás.

Métodos:  estudo de caráter experimental laboratorial, onde foram realizadas coletas durante os meses de março a agosto de 2023.

Resultados:  das 50 amostras coletadas, foram isoladas 104 bactérias, 81,7% (85/104) gram-positivas e 18,3% (19/104) gram-negativas. Destas, 55,3% (47/85) do gênero Staphylococcus foram classificadas como multidroga resistente e resistente a meticilina e 15,7% (3/19) das gram-negativas como multidroga resistente. 66,34% (69/104) foram produtoras de biofilme, sendo 79,7% (55/69) gram-positivas e 20,3% (14/69) gram-negativas.

Conclusões:  tal achado traz grande preocupação visto que estes microrganismos em ambientes hospitalares apresentam risco elevado para infecções de sítio cirúrgico de difícil tratamento devido às cepas multirresistentes.

Descritores:
Centros Cirúrgicos; Infecção Hospitalar; Resistência Microbiana a Medicamentos; Staphylococcus aureus; Biofilmes.

RESUMEN

Objetivos:  evaluar el perfil de resistencia y formación de biopelículas en aislados de quirófanos de dos hospitales de la región suroeste de Goiás.

Métodos:  estudio experimental de laboratorio, en el que se realizaron recolecciones durante los meses de marzo a agosto de 2023.

Resultados:  de las 50 muestras recogidas, se aislaron 104 bacterias, 81,7 % (85/104) grampositivas y 18,3 % (19/104) gram-negativas. De estas, el 55,3 % (47/85) del género Staphylococcus se clasificaron como multirresistentes y resistentes a la meticilina, y el 15,7 % (3/19) de las gram-negativas como multirresistentes. El 66,34 % (69/104) eran productoras de biofilm, siendo el 79,7 % (55/69) gram-positivas y el 20,3 % (14/69) gram-negativas.

Conclusiones:  este hallazgo es muy preocupante, ya que estos microorganismos en entornos hospitalarios presentan un alto riesgo de infecciones del sitio quirúrgico difíciles de tratar debido a las cepas multirresistentes.

Descriptores:
Centros Quirúrgicos; Infección Hospitalaria; Farmacorresistencia Microbiana; Staphylococcus aureus; Biopelículas.

INTRODUCTION

The hospital environment is a large reservoir of virulent microorganisms that can cause Healthcare-Associated Infections (HAIs) in patients, especially in cases of prolonged hospitalizations, invasive and surgical procedures, and also due to exogenous factors related to the environment, materials, and equipment. In Brazil, concern about healthcare-associated infections (HAIs) has been growing since the 1990s, and they currently represent the fourth leading cause of mortality in Intensive Care Units (ICUs)(1,2).

Data from the National Biosafety Agency (ANBIO) indicate that 80% of hospitals do not adequately control HAIs. Furthermore, data from the National Regulatory Agency for Private Health Insurance and Plans (ANS) indicates that more than 45,000 Brazilians die annually as a result of these diseases, and the World Health Organization (WHO) estimates this number to be even higher, reaching 100,000 cases per year(3-5).

The interaction of different microorganisms in the same environment, especially in hospitals, favors the development of some mechanism of resistance to antimicrobials(6,7), which occurs due to various mutations, hindering the treatment of bacterial infections and potentially leading to unfavorable clinical outcomes, and even patient death(6,8,9).

Another aggravating factor of hospital microorganisms is their ability to produce biofilms, which consist of a layer of extracellular polymeric substance (EPS), composed of polysaccharides, extracellular DNA, proteins, lipids, surfactants, flagella, and pili, thus providing protection to the microorganisms present there, as they are highly resistant to antimicrobial agents and environmental disinfectants(10,11).

Inside biofilms, these microorganisms have the ability to interact/communicate with each other, a process called Quorum sensing (QS). This factor facilitates the transfer of multidrug-resistant plasmids, favoring the development of persistent infectious diseases. According to the National Institutes of Health in the United States, approximately 80% of all infections worldwide are associated with the presence of biofilms(10,11).

Some hospital environments are more susceptible to the presence and growth of microorganisms, and among these is the operating room, as it is a place where many patients and professionals pass through, where several types of invasive procedures are performed, in addition to artificial climate control and the use of materials and equipment(12,13). These infections can be classified as exogenous when they originate from a source external to the patient, or endogenous when they originate from the patient themselves. Exogenous transmission is primarily through direct contact, but it can also occur indirectly through contaminated equipment, instruments, and surfaces, or even through improperly processed implant materials(14-17).

Due to all these related factors, HAIs, particularly surgical site infections (SSIs), are a significant concern for patient safety and can occur in both major surgeries and minor procedures(18).

OBJECTIVES

To identify, evaluate the antimicrobial resistance profile, and verify the biofilm formation of microorganisms isolated from surfaces in operating rooms.

METHODS

Study type or design

Ethical review and approval were waived for this study, as it is an experimental laboratory study of surface sample collection, based on Revised Standards for Quality Improvement Reporting Excellence (SQUIRE 2.0)®(19).

Local

The study was conducted in the operating room of two healthcare facilities located in the Southwest of Goiás. One of medium complexity and another of high complexity, three and four operating rooms, providing services in various areas such as internal medicine, pediatrics, obstetrics, general surgery, orthopedics, urology, ophthalmology, otolaryngology, among others.

The laboratory analyses were developed in the Bacteriology and Mycology Laboratory of the Biomedicine course at the Federal University of Jataí - GO (LBM-UFJ).

Period and collection of samples

The collections were carried out between the months of March to August 2023. To identify and evaluate the antimicrobial resistance profile and verify biofilm formation, samples were collected using sterile Swabs moistened with a 0.9% saline solution, the samples were rubbed over the entire surface of the selected objects, which were: computer keyboards and mouses, suction machine cords, electrosurgical unit cords, electrosurgical unit foot pedal, cardiac monitor lead connectors, and blood pressure monitor cuffs, obtaining a total of 50 samples.

After collection, swabs were placed in previously identified test tubes containing Brain Heart Infusion (BHI) (HIMEDIA®) broth, packaged in a thermal box, and transported to LBM-UFJ, where they remained incubated for 24 h in a Biochemical Oxygen Demand (BOD) incubator at a temperature of 35°C-37°C.

Microbiological analyses

Bacterial growth was determined based on the BHI (HIMEDIA®) broth cloudiness. Samples showing growth were streaked onto Blood Agar - AS (KASVI®) and incubated for 24 hours in a BOD incubator at a temperature of 35°C-37°C. After the incubation period, it was observed whether there was growth, as well as the number of distinct colonies on each plate. The morphologically different colonies were re-inoculated (secondary isolation) to achieve the purity of each colony, allowing the performance of further identification tests. The previously isolated samples (observing hemolysis patterns and Gram staining) were subjected to traditional biochemical tests for identification(20).

Analysis of resistance and biofilm production

The Kirby-Bauer disk diffusion method was used to perform the antimicrobial susceptibility test(21), depositing antimicrobial discs in a Petri dish (140x15mm) containing Mueller Hinton agar (HIMEDIA®) previously inoculated with an isolated bacterial strain of approximately 1.5 x 108 CFU/ml (0.5 of the scale of McFarland), incubated at 35-37ºC for 24h. The results were interpreted by comparing the diameter of the inhibition halo with the classifications of the cut-off points established by the Brazilian Committee on Antimicrobial Susceptibility Testing (BrCAST) and in this way they were classified as sensitive, intermediate, or resistant(21).

The resistance profile of the Staphylococcus group to oxacillin (with the resistant ones being classified as MRSA - methicillin-resistant Staphylococcus aureus, MRSE - methicillin-resistant Staphylococcus epidermidis, and MRSS- methicillin-resistant Staphylococcus saprophyticus), of the Enterococcus sp. group to vancomycin (with the resistant ones being classified as VRE - vancomycin-resistant Enterococcus) and Enterobacteriaceae resistant to imipenem (with the resistant ones classified as: possible KPC)(21).

For the classification of the multiresistance profile, the criteria proposed by Magiorakos et al.(22) were adopted, where isolates that did not show resistance or showed up to two classes were classified as Not MDR (Not multidrug resistant); isolates that showed resistance to at least one representative in three or more classes of antimicrobials were classified as MDR (multidrug resistance); and the isolates showing resistance to all agents from all classes were classified as PDR (pan drug resistance)(22).

For conducting tests of biofilm production, the isolates were thawed and an aliquot was transferred to a test tube containing BHI broth. After 24 hours of incubation, the biofilm was mounted in 96-well plates containing 198 μL of Tryptic Soy Broth enriched medium - TSB (HIMEDIA®) and 2 μL of BHI + Strain, this being incubated at 35°C-37°C in a BOD incubator for 48h. Subsequently, the steps described by Stepanovic et al.(23) were followed, which included the plate reading phase: plate washing, fixation and staining, and finally, measurement of results using a microtiter plate reader (KASVI®). The interpretation was expressed through the cutoff point (Cut off - ODc) described in Chart 1.

Chart 1
Interpretation of biofilm production

RESULTS

The results obtained from the microbiological analysis of samples collected in two hospitals provide a comprehensive view of the presence of microorganisms in these facilities. Of the 50 samples analyzed, all showed growth of at least one type of microorganism, totaling 104 isolated bacteria. Characterization of the bacteria based on Gram staining revealed a predominance of Gram-positive bacteria, representing 81.7% (85/104) of the total, compared to Gram-negative bacteria, which constituted 18.3% (19/104).

Figure 1 provides a representation of the bacterial species identified (Staphylococcus sp. (4), Staphylococcus epidermidis (20), Staphylococcus aureus (38), Staphylococcus saprophyticus (7), coagulase-negative Staphylococcus (11), Streptococcus viridans (1), Enterococcus sp. (4), Proteus mirabilis (3), Escherichia coli (7), Shigella sp. (3) and Acinetobacter sp. (5).

Figure 1
Frequency of bacteria isolated on surfaces and objects in surgical suites of two hospitals in southwestern Goiás

Regarding resistance mechanisms, in the present study it was observed that 57.7% (60/104) of the isolates showed resistance to antimicrobials and were classified as MDR according to Magioarakos et al.(12) criteria. Moving on to the evaluation of biofilm formation capacity, it was observed that 66.3% (69/104) of the isolates have this characteristic, with 89.8% (62/69) being weak producers, 5.8% (4/69) moderate producers, and 4.4% (3/69) strong producers, as shown in Chart 2.

Chart 2
Sample origin, resistance profile, and biofilm production capacity

DISCUSSION

Among HAIs, SSI stands out as a major concern in the hospital setting, and they can be caused by a wide range of bacteria, both gram-negative and/or gram-positive ones(17). In the operating room, when preventive measures are not implemented or are neglected, the risk of infection increases considerably, potentially causing temporary or permanent damage, and even death to patients(24).

This study showed that microorganisms were isolated from all surfaces where samples were collected, and among these were species that cause HAIs, with a significant resistance profile to antimicrobials, in addition to the capacity for biofilm production. These findings corroborate a study conducted in a hospital in Belo Horizonte, with the same objective, pointing to significant data related to the incidence of microorganisms on surfaces and objects in an operating room, namely: Coagulase-negative Acinetobacter baumannii, Enterobacter sp., and Staphylococcus, bacteria that are potential causes of HAIs, particularly SSIs, given the presence of isolates with high antimicrobial resistance profiles(25).

Another study(13) evaluated the bacterial profile found on the surfaces and equipment of an operating room, and microorganisms were isolated from all of them, with a prevalence of gram-positive cocci, with S. aureus being the most frequent occurrence, corroborating the findings of this study, where all surfaces and objects tested showed bacterial growth, with a predominance of the genre Staphylococcus, and the prevalence of S. aureus being highlighted. This pathogen is part of the human skin microbiota, but it can cause various infections in hospital settings, such as respiratory, systemic, and surgical site infections.

Similar research(26) also pointed to a higher prevalence of the species S. aureus, which is closely linked to the development of HAIs, primarily by methicillin-resistant strains (MRSA). In the present study, 77.8% (81/104) of the isolates are of the genus Staphylococcus. Of these, 58.02% (47/81) showed resistance to oxacillin, classified as MDR/MRSA, and 66.66% (54/81) are biofilm-producing strains. It should be noted that this species has the ability to produce biofilms, which hinders the immune response and pharmacological therapy(17).

Enterococcus sp. consists of a genus of Gram-positive bacteria naturally found in the gastrointestinal tract; however, studies indicate the presence of species within this genus associated with hospital-acquired infections, which is particularly relevant when these bacteria develop vancomycin resistance (VRE) mechanisms, as they can cause opportunistic infections that spread easily in the hospital environment. Study conducted at a university hospital(12) points to high prevalence rates for Enterococcus sp. in various sectors of the hospital, being the second most frequently found in the samples of surgical incisions secretion. This study, in turn, isolated 3.84% (0.5/104) of the samples, and all of these proved sensitive to vancomycin; however, 75% (03/04) of the isolates were classified as MDR, thus pointing to an imminent risk of developing SSI, given that these microorganisms are producers of surface polysaccharides (enterococcal polysaccharide antigen) essential for biofilm development, which is directly linked to antimicrobial resistance as well as pathogenesis(27).

In the present study, 18.3% (19/104) of the bacteria isolated were gram-negative (E. coli, Proteus mirabilis, Acinetobacter sp. and Shigella sp.) species, where 21.05% (04/19) exhibited multidrug resistance (MDR) to the tested antimicrobials. Furthermore, this study also corroborates the findings of a previous research project(28) that shows that superbacteria are one of the biggest challenges faced in the hospital environment, especially in SSIs.

Moreover, the biofilm production capacity was evaluated, as this is a characteristic associated with bacterial virulence and resistance. The presence of biofilm can contribute to the persistence of HAIs and hinder appropriate treatment(29). The analysis revealed variations in biofilm production, with 66.34% (69/104) of the isolates classified as biofilm producers, 79.7% (55/69) as gram-positive bacteria and 20.3% (14/69) as gram-negative bacteria. The same was shown in a study(30) conducted at a hospital in Pokhara, Nepal, which assessed the contamination of frequently touched objects, and found a higher prevalence of S. aureus in the 181 samples analyzed, with 36.3% being methicillin-resistant and 31.8% being biofilm producers.

Study limitations

As the bacterial strains were being identified, the performance of several subcultures of the same sample was required so that the colony could be isolated to proceed with the identification flowchart. Therefore, a single sample required around 5 to 6 days for identification, due to the fact that a single plate exhibited polymicrobial growth.

Contributions to the fields of nursing, health, or public policy

HAIs can be prevented and controlled through the implementation of infection prevention and control measures at all levels of healthcare. Preventing HAIs is the responsibility of healthcare facilities and all staff members. Everyone must work together to reduce the risk of infection for both patients and healthcare workers themselves(31). The association between antimicrobial resistance and biofilm production highlights the need for the implementation of integrated infection control strategies, emphasizing the fundamental role of healthcare professionals, the early identification of bacteria, and the implementation of appropriate preventive measures essential to mitigating the risks of hospital-acquired infections associated with these microorganisms(32,33).

CONCLUSIONS

The results presented provide valuable insights for hospital health management, highlighting the importance of continuous surveillance, infection control practices, and the development of personalized therapeutic strategies to address microbiological diversity and antimicrobial resistance in hospital settings. Given these findings, it is necessary for staff working in the Operating Room (OR) to adopt improved cleaning and disinfection measures for surfaces and objects aiming to reduce the risk of cross-infections.

FUNDING

The Research Support Foundation of the State of Goiás (FAPEG).

AVAILABILITY OF DATA AND MATERIAL

The research data are available within the article.

REFERENCES

  • 1 Agência Nacional de Vigilância Sanitária (Anvisa). Curso básico de controle de infecção hospitalar: Caderno B: principais síndromes infecciosas e hospitalares. Brasília: ANVISA; 2000.
  • 2 Agência Nacional de Vigilância Sanitária (Anvisa). Critérios diagnósticos de infecção relacionada à assistência à saúde. Brasília (DF): Anvisa; 2013.
  • 3 Associação Nacional de Biossegurança (Anbio). Biossegurança hospitalar. Brasília: Anbio; 2012.
  • 4 Agência Nacional de Saúde Suplementar (ANS). ANS alerta sobre o controle das infecções hospitalares [Internet]. Brasília: ANS; 2022[cited 2023 Apr 19]. Available from: https://www.gov.br/ans/pt-br/assuntos/noticias/qualidade-da-saude/ans-alerta-sobre-o-controle-das-infeccoes-hospitalares
    » https://www.gov.br/ans/pt-br/assuntos/noticias/qualidade-da-saude/ans-alerta-sobre-o-controle-das-infeccoes-hospitalares
  • 5 Organização Mundial da Saúde (OMS). OMS lança primeiro relatório global sobre prevenção e controle de infecções [Internet]. Genebra: OMS; 2022[cited 2023 Apr 19]. Available from: https://www.who.int/news/item/06-05-2022-who-launches-first-ever-global-report-on-infection-prevention-and-control
    » https://www.who.int/news/item/06-05-2022-who-launches-first-ever-global-report-on-infection-prevention-and-control
  • 6 Santos NQ. A resistência bacteriana no contexto da infecção hospitalar. Texto Contexto Enferm. 2004;13(23):64-70. https://doi.org/10.1590/S0104-07072004000500007
    » https://doi.org/10.1590/S0104-07072004000500007
  • 7 Abeeg PTGM, Silva LL. Controle de infecção hospitalar em unidade de terapia intensiva: estudo retrospectivo. Semina: Ciênc Biol Saúde. 2011;32(1):47-58. https://doi.org/10.5433/1679-0367.2011v32n1p47
    » https://doi.org/10.5433/1679-0367.2011v32n1p47
  • 8 Domingos II. Bactérias multirresistentes em uma abordagem da temática por meio do ensino por investigação[Dissertação] [Internet]. Ouro Preto: UFOP; 2023 [cited 2024 Feb 10]. Available from: https://monografias.ufop.br/handle/35400000/5352
    » https://monografias.ufop.br/handle/35400000/5352
  • 9 Jiménez Pearson MA, Galas M, Corso A, Hormazábal JC, Duarte Valderrama C, Salgado Marcano N, et al. Latin American consensus to define, categorize, and report multidrug-resistant, extensively drug-resistant, or pandrug-resistant. Rev Panam Salud Publica. 2019;43:e65. https://doi.org/10.26633/rpsp.2019.65
    » https://doi.org/10.26633/rpsp.2019.65
  • 10 Donlan RM. Papel dos biofilmes na resistência antimicrobiana. Asaio J. 2000;46:S47-52. https://doi.org/10.1097/00002480-200011000-00037
    » https://doi.org/10.1097/00002480-200011000-00037
  • 11 Abrantes JA, Nogueira JMR. Biofilme e células persisters: da persistência à resistência microbiana. Rev Bras Anál Clin. 2022;54(3):1-3. https://doi.org/10.21877/2448-3877.202200074
    » https://doi.org/10.21877/2448-3877.202200074
  • 12 Lima FLO, Almeida PC, Oliveira GAL. Enterococcus spp. resistente à vancomicina e sua disseminação em infecções no ambiente hospitalar. Pesqui Soc Desenvolv. 2020;8:e738986404. https://doi.org/10.33448/rsd-v9i8.6404
    » https://doi.org/10.33448/rsd-v9i8.6404
  • 13 Santos AB, Silva KS, Santana MMR, Marques MW, Naue CR. Perfil bacteriano das superfícies e equipamentos do Bloco Cirúrgico de um Hospital Universitário. VITTALLE. 2020;32(1):101-7. https://doi.org/10.14295/vittalle.v32i1.11048
    » https://doi.org/10.14295/vittalle.v32i1.11048
  • 14 Bolick D. Segurança e controle de infecção. Rio de Janeiro: Reichmann & Afonso; 2000.
  • 15 Lacerda RA. Controle de infecção em centro cirúrgico: fatos, mitos e controvérsias [Internet]. São Paulo: Atheneu; 2003 [cited 2024 Feb 10]. p.315-24. Available from: https://repositorio.usp.br/item/001390284
    » https://repositorio.usp.br/item/001390284
  • 16 Dresch F, Birkheuer CF, Rampel C, Maciel MJ. Contaminação de superfícies localizadas em unidades de terapia intensiva e salas de cirurgia: uma revisão sistemática da literatura. Rev Epidemiol Control Infec. 2018;8(1):85-91. https://doi.org/10.17058/reci.v1i1.9897
    » https://doi.org/10.17058/reci.v1i1.9897
  • 17 Abrantes JA, Nogueira JMR. Biofilme e células persisters: da persistência à resistência microbiana. Rev Bras Anál Clin. 2022;54(3):1-3. http://dx.doi.org/10.21877/2448-3877.202200074
    » http://dx.doi.org/10.21877/2448-3877.202200074
  • 18 Berríos-Torres SI, Umscheid CA, Bratzler DW, Leas B, Stone EC, Kelz RR, et al. Centers for Disease Control and Prevention Guideline for the Prevention of Surgical Site Infection, 2017. JAMA Surg. 2017;152(8):784-91. https://doi.org/10.1001/jamasurg.2017.0904
    » https://doi.org/10.1001/jamasurg.2017.0904
  • 19 Ogrinc G, Davies L, Goodman D, Batalden P, Davidoff F, Stevens D. SQUIRE 2.0 (Standards for Quality Improvement Reporting Excellence): revised publication guidelines from a detailed consensus process. J Nurs Care Qual. 2016;31(1):1-8. https://doi.org/10.1097/NCQ.0000000000000153
    » https://doi.org/10.1097/NCQ.0000000000000153
  • 20 Winn WC, Allen SD, Janda WM, Koneman EW, Procop GW, Scheckenberger PC, et al. Koneman, diagnóstico microbiológico: texto e atlas colorido. 6ª ed. Rio de Janeiro: Guanabara Koogan; 2008.
  • 21 Brazilian Committee on Antimicrobial Susceptibility Testing (BrCAST). Documentos BrCAST [Internet]. 2021 [cited 2023 Sep 20]. Available from: http://www.brcast.org.br
    » http://www.brcast.org.br
  • 22 Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268-81. https://doi.org/10.1111/j.1469-0691.2011.03570.x
    » https://doi.org/10.1111/j.1469-0691.2011.03570.x
  • 23 Stepanovic S, Vukovic D, Hola V. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by Staphylococci. APMIS. 2007;115:891-9. https://doi.org/10.1111/j.1600-0463.2007.apm_630.x
    » https://doi.org/10.1111/j.1600-0463.2007.apm_630.x
  • 24 Abreu IM, Rocha RC, Avelino FVSD, Guimarães DBO, Nogueira LT, Madeira MZA. Cultura de segurança do paciente em centro cirúrgico: visão da enfermagem. Rev Gaúcha Enferm. 2019;40(esp):e20180198. https://doi.org/10.1590/1983-1447.2019.20180198
    » https://doi.org/10.1590/1983-1447.2019.20180198
  • 25 Oliveira AC, Kovner CT, Silva RS. Infecção hospitalar em unidade de tratamento intensivo de um hospital universitário brasileiro. Rev Latino-Am Enfermagem [Internet]. 2010[cited 2023 Sep 20];18(2):97-104 Available from: https://www.scielo.br/j/rlae/a/8qbHRdwYM9n8M9gNjqQnPSM/?format=pdf⟨=pt
    » https://www.scielo.br/j/rlae/a/8qbHRdwYM9n8M9gNjqQnPSM/?format=pdf⟨=pt
  • 26 Wisniewski GV, Fiorin TM, Almeida Alves I. Identificação e avaliação do perfil de resistência de bactérias isoladas da unidade de terapia intensiva de um hospital da região noroeste do Rio Grande do Sul. RICSB. 2020;4(1):11-23. https://doi.org/10.31512/ricsb.v4i1.183
    » https://doi.org/10.31512/ricsb.v4i1.183
  • 27 Guerardel Y, Sadovskaya I, Maes E, Furlan S, Chapot-Chartier MP, Mesnage S, et al. Complete structure of the enterococcal polysaccharide antigen (EPA) of vancomycin-resistant Enterococcus faecalis V583 reveals that EPA decorations are teichoic acids covalently linked to a rhamnopolysaccharide backbone. mBio [Internet]. 2020[cited 2023 Sep 20];11(2):e00277-20. https://doi.org/10.1128/mBio.00277-20
    » https://doi.org/10.1128/mBio.00277-20
  • 28 Borges RM, Nunes CP. Infecções por Acinetobacter baumannii em unidades de terapia intensiva. Rev Med Fam Saúde Ment. 2019;1(2):45-56. Available from: https://revista.unifeso.edu.br/index.php/medicinafamiliasaudemental/article/view/1626
    » https://revista.unifeso.edu.br/index.php/medicinafamiliasaudemental/article/view/1626
  • 29 Lopes MC, Évora BS, Cidral TA, Botelho LB, Melo MC. Bacteremia por Acinetobacter radioresistens: primeiro relato de caso no Brasil. J Bras Patol Med Lab. 2019;55(6):669-74. https://doi.org/10.5935/1676-2444.20190059
    » https://doi.org/10.5935/1676-2444.20190059
  • 30 Bhatta DR, Hamal D, Shrestha R, Subramanya SH, Baral N, Singh RK, et al. Bacterial contamination of frequently touched objects in a tertiary care hospital of Pokhara, Nepal: how safe are our hands? Antimicrob Resist Infect Control. 2018;7:97. https://doi.org/10.1186/s13756-018-0385-2
    » https://doi.org/10.1186/s13756-018-0385-2
  • 31 Erdem I, Yildirim I, Safak B, Karaali R, Erdal B, Ardic E, et al. A 5-year surveillance of healthcare-associated infections in a university hospital: a retrospective analysis. SAGE Open Med. 2022. https://doi.org/10.1177/20503121221091789
    » https://doi.org/10.1177/20503121221091789
  • 32 Borges FV, Silva LVB, Barcelos KK, Soerger M, Moreira TC, Oliveira TMA, et al. Superbacterial infection in the organic center and in the Intensive Care Unit: an integrative review. RSD. 2023;12(1):e421213945. https://doi.org/10.33448/rsd-v12i1.39453
    » https://doi.org/10.33448/rsd-v12i1.39453
  • 33 Assefa M, Amare A. Biofilm-associated multi-drug resistance in hospital-acquired infections: a review. Infect Drug Resist. 2022;15:5061-8. https://doi.org/10.2147/IDR.S379502
    » https://doi.org/10.2147/IDR.S379502

Correspondence

Corresponding author: Vanessa Bridi, E-mail: vanessabridi@hotmail.com

EDITOR IN CHIEF:

Dulce Barbosa

ASSOCIATE EDITOR:

Richarlisson Morais

Publication Dates

  • Publication in this collection
    28 Sept 2026
  • Date of issue
    2026

History

  • Received
    22 May 2025
  • Accepted
    26 Nov 2025
location_on
Associação Brasileira de Enfermagem SGA Norte Quadra 603 Conj. "B" - Av. L2 Norte 70830-102 Brasília, DF, Brasil, Tel.: (55 61) 3226-0653, Fax: (55 61) 3225-4473 - Brasília - DF - Brazil
E-mail: reben@abennacional.org.br
rss_feed Acompanhe os números deste periódico no seu leitor de RSS
Ir para o topo Reportar erro