Nosocomial infections lengthen the length of hospitalisation by 4 days on average, and about one third of all hospital-acquired infections are considered preventable. However, the classification of an infection as nosocomial does not mean that there is a causal relationship between a medical intervention and the occurrence of the infection ¹. In Germany the mortality attributable to nosocomial multi-drug resistant organisms (MDRO) is between 6,000 and 15,000 patients, around 30,000 to 35,000 patients develop infections. The problems of nosocomial infections and increasing antimicrobial resistance are highly relevant and should not be underestimated ². One of the organisms present in the community is Staphylococcus aureus, an opportunistic pathogen that can colonise skin and mucous membranes, such as the nostrils, and remain quiescent and asymptomatic without decreasing its infective capacity, thus giving rise to the asymptomatic carrier state, in which it transmits from host to host and spreads in the environment causing infections in different areas of the body ^{3, 4}.

Staphylococcus aureusis capable of producing resistance to most antibiotics used in empirical treatment ⁵. It presents several resistance mechanisms, including the mecA gene, which disables methicillin and beta-lactam antibiotics such as quinolones, lincosamides and carbapenems such as imipenem and meropenem, increasing morbidity, mortality and treatment costs ^{6, 7}. Methicillin-resistant Staphylococcus aureus(MRSA) is a major cause of hospital-acquired infections that are increasingly difficult to combat due to emerging resistance to all current classes of antibiotics 8. MRSA colonisation of the nares, whether present in the community or acquired during hospitalisation, increases the risk of MRSA infection. Identification of MRSA colonisation on admission may point to a high-risk population that could benefit from interventions to decrease the risk of subsequent MRSA infection ⁹. Replacement of hospital strains by community-associated strains has been observed; most risk factors of patients infected with community and hospital strains were similar, suggesting that, so far, community strains behave like their traditional hospital-associated counterparts ¹⁰.

The increase in the incidence of MRSA infection has been associated with the recognition of new MRSA clones known as community-associated MRSA (CA-MRSA). CA-MRSA strains differ from hospital MRSA strains; they infect a different group of patients, cause different clinical syndromes, differ in antimicrobial susceptibility patterns, spread rapidly among healthy people in the community, and often also cause infections in healthcare settings ¹¹. Staphylococcus aureus resistance is a problem if not adequately treated and prevented from spreading, the objective of the study was to evaluate the antimicrobial susceptibility of Staphylococcus aureus from nasopharyngeal isolates of Biology, Nursing and Human Medicine students of the Universidad Nacional Pedro Ruiz Gallo who have nosocomial contact.

Materials and methods

The present research work is an exploratory cross-sectional study, carried out in the Microbiology and Parasitology laboratories of the Faculty of Biological Sciences of the Universidad Nacional Pedro Ruiz Gallo. The sample size was determined on the basis of a pilot sample of 15 students, five students from each faculty evaluated, of which 30 % tested positive for Staphylococcus aureus. The total number of students who participated was 150, distributed among 50 students from the Faculty of Biological Sciences in the last cycles, 50 nursing students who already attend medical centres and 50 fourth year medical students from the Universidad Nacional Pedro Ruiz Gallo. Nasal swab samples of students from three professional schools of the National University ?Pedro Ruiz Gallo?, during the period October 2015-March 2016 of the National University Pedro Ruiz Gallo. Only those students who agreed to participate in the study after signing the informed consent form were included, who subsequently underwent nasal swabbing to obtain the sample. The study was accepted by the ethics committee of the Universidad Nacional Pedro Ruiz Gallo.

Bacterial isolation

Samples were obtained by nasal swabbing by inserting a swab into the nostril of the carrier, rotating three times clockwise and three times counterclockwise. They were immediately seeded on Salted Mannitol Agar plates by exhaustion and streaking for primary isolation; incubated at 35-37 °C for 24 hours, under aerobic conditions.

At the end of incubation, the characteristics of the suspected Staphylococcus aureuscolonies were determined, and microbiological identification was carried out according to the Bacteriological Procedures Manual on Intrahospital Infections-INS ¹².

For phenotypic identification, conventional biochemical assays were performed and antimicrobial susceptibility was assessed using the Kirby-Bauer method (agar diffusion method).

Determination of antibiotic susceptibility by antibiogram

It consisted of using a plate with Müller Hinton agar, where a bacterial suspension adjusted to the 0.5 standard of the Mc Farland scale was inoculated. The antibiotics used to evaluate Staphylococcus aureus were: Oxacillin, Vancomycin, Penicillin, Imipenem, Ampicillin/Sulbactam and Cefoxitin. Isolates with intermediate rank were considered as resistant, taking into account the sensitivity or resistance parameters of the Performance Standards for Antimicrobial Susceptibility Testing ¹³.

Determination of cross-reactivity of Oxacillin-resistant Staphylococcus aureusstrains with other antibiotics.

After assessing the antibiotic resistance of Staphylococcus aureus, a second antibiogram was performed on those strains that were resistant to Oxacillin, to determine cross-reactivity with other antibiotics. The antibiotics used were; Ceftazidime, Azithromycin, Cefotaxime, Gentamicin, Amikacin, Ciprofloxacin, Ceftriaxone and Cefuroxime; Oxacillin (was placed in the centre of the agar plate).

Factors associated with Staphylococcus aureuscarriers

The following epidemiological factors were assessed by means of a survey: overcrowding (if the person shared a bedroom with more than 3 other people), passive or active smoking (if the person smoked or lived with at least one smoker), constant exposure to dust (if the person?s locality or home is very exposed to dust), people with chronic respiratory diseases at home (asthma, allergic rhinitis, etc.) and precariousness of housing. Clinical factors such as: recurrent pharyngeal infections, history of acute respiratory infections (colds and flu), history of allergies and self-medication.

Statistical analysis of data

With the results obtained, a database was created using Microsoft Excel 2013. Frequency distribution tables were drawn up to organise the data into joint classes, with the aim of representing the data obtained in percentages, and on the basis of these, to carry out the descriptive analysis and draw graphs to facilitate understanding of the results. The statistical software InfoStat was used.

Results

A total of 150 nasal swab samples were analysed, 43 (28.6 %) positive cultures for Staphylococcus aureus were isolated; 107 (71.4 %) negative cultures for Staphylococcus aureuswere negative.

Regarding the frequency of Staphylococcus aureus, it was determined that, of the 43 strains obtained, the professional school of Biological Sciences had the highest number of isolates 18 (12 %), followed by the professional school of Human Medicine 14 (9.3 %), with Nursing being the professional school with the fewest isolates 11 (7.3 %).

Susceptibility profile of Staphylococcus aureusisolates

From the isolation of the 43 strains of Staphylococcus aureus, the antibiogram was performed in order to evaluate the susceptibility of the microorganism under study, determining that 90.6% of the strains were resistant to Oxacillin, 81.3% to Sulfamethoxazole - Trimethoprim, 95.3% to Penicillin, 34.8% to Cefoxitin, and all strains were 100% sensitive to Imipenem and Vancomycin. Isolates with an intermediate range in the antibiogram readings were considered resistant ( Table 1)

Table 1
Resistance profile of Staphylococcus aureusfrom nasal isolates from students of the Universidad Nacional Pedro Ruiz Gallo.

Cross-reaction of Staphylococcus aureusstrains resistant to Oxacillin with other antibiotics.

A second antibiogram was performed on the strains that were resistant to Oxacillin, to determine cross-reactivity with other antibiotics, especially cephalosporins. Thirty-nine strains were tested, of which 2.6% were resistant to Ceftazidime, 12.8% to Azithromycin, 15.4% to Cefotaxime, and 20.9% to Gentamicin; in contrast, they were 100% sensitive to Amikacin, Ciprofloxacin, Ceftriaxone and Cefuroxime ( Table 2).

Table 2.
Cross-reaction of Staphylococcus aureusstrains resistant to Oxacillin.

Clinical factors associated with nasal isolates from students at the Universidad Nacional Pedro Ruiz Gallo

All participants in the present study were surveyed in order to detect possible clinical factors associated with bacterial colonisation in the study, which included: Recurrent pharyngeal infections (FI), History of acute respiratory infections (AIR), History of allergies (AA); Self-medication habits (HA).

The data provided by the survey after evaluation of the positive isolates of Staphylococcus aureus, showed that 9.3% of the participants had recurrent pharyngeal infections, 41.3% had a history of acute respiratory infections, including colds and flu, 42% suffered from allergies, and 46% had the habit of self-medicating; relating the history with prevalent results, to students with positive isolates and resistant to the antibiotics evaluated. Self-medication was the common clinical factor in all positive Staphylococcus aureusisolates.

Epidemiological factors associated with nasal isolates from students at the Universidad Nacional Pedro Ruiz Gallo.

The survey of students from the professional schools evaluated included epidemiological factors that may be associated with the bacterial colonisation under study, considering overcrowding (H), passive smoking (FP), active smoking (FA), constant exposure to dust (EP) and living with people with chronic respiratory diseases (ERC) as predisposing factors.

The results obtained from the survey provided the following information; of the total Staphylococcus aureuspositive isolates, 2% of participants indicated that they lived in overcrowded conditions, 16% indicated that they were passive smokers, 6.6% active smokers, 44% that they had constant exposure to dust, and 21.3% that they lived with family members with chronic respiratory diseases. The prevalent epidemiological factors were constant exposure to dust and living with patients with chronic respiratory diseases.

Discussion

More local data on CA-MRSA infections are needed so that dermatologists and community physicians can assess the risk of such infections among their patients and avoid inappropriate administration of beta-lactams. No single change in prescribing practices will completely alleviate the selective pressure for the spread of community-acquired MRSA and will not exacerbate resistance in pyogenic streptococci, commonly found along with S. aureus in skin and soft tissue infections. The importance of hygiene to prevent the spread of community-acquired MRSA in the community should be emphasised ^{14, 15}.

Of the samples analysed in our study, 28.6% were found to be positive for the pathogen under study, coinciding with López et al., 2013 who, when evaluating medical students attached to a hospital in Spain, found that 39.3% were colonised by S. aureus;16 likewise Gaona et al, 2009 found that 45.3% of a group of pre-clinical students were carriers of S. aureus17; this disagrees with Villafañe et al., 2013 ¹⁸, who found that 14.88% of students in the Bacteriology programme were carriers of S. aureus. The associated risk factors were the predisposing factors for the personnel evaluated to present the characteristic of being carriers; coinciding in that the positive S. aureus isolates were from those students who were more exposed to the hospital environment, as well as those who received antimicrobial therapy in the last three months, also relating the deficiency in hand washing, due to the fact that many students were unaware of the hygiene protocol, and others had not received specific training. The result that differs from the other studies due to the low frequency of nasal carriage is related to the fact that the students evaluated were from minor cycles, without much contact with hospital patients, in addition to complying with biosecurity measures and correct hand washing during the performance of their work.

Although it is true that most research on the frequency and profile of microbial susceptibility is carried out on healthcare personnel and patients hospitalised in critical areas, when the results obtained in the present study were compared, it was determined that they coincide with Sanabria et al, 2008 ¹⁹, Otth et al., 2007 ²⁰, Arteaga-Delgado et al., 2016 ²¹, who investigated Staphylococcus aureuscarriers in hospital staff, with a percentage of isolates similar to that obtained in the present study; however, studies such as those of González et al, 2005 ²², Platzer et al., 2008 ²³ and Paganini et al., 2009 ²⁴, showed that the isolates obtained for the evaluation of carriers at the intrahospital level is greater than 60%; although research such as that of Aguilar et al. 2009 ²⁵, in a hospital in our region, determined a low frequency of Staphylococcus aureusisolates in the healthcare personnel they evaluated.

With regard to the frequency of Staphylococcus aureusisolates in each professional school, Biological Sciences presented the highest number of isolates (12%), followed by the professional school of Human Medicine (9.3%), with Nursing being the professional school with the fewest isolates (7.3%), due to the type of exposure of the students sampled to the hospital environment as they progress through the university cycles, whether in the clinical laboratory area or in the care area; coinciding with Gaona et al, 2009 ¹⁷ and Villafañe et al. , 2013 ¹⁸, who pointed out that in relation to the advancement in the study cycles, the carrier status is increasing between 2.2% and 3.1% respectively. In the hospital setting, the difference between one area and another will be determined by the direct contact between healthcare staff and patients, with the areas with the highest frequency of carriers of pathogenic bacteria being neonatology, surgery and gynaecology, as detailed by Aguilar et al. 2009 ²⁵ in their research.

Regarding the antibiotic susceptibility profile, the Staphylococcus aureusstrains evaluated were 90.6% resistant to oxacillin, 81.3% resistant to Sulfamethoxazole-Trimethoprim and 34.8% to cefoxitin; differing from Gaona et al, 2009, whose strains under study were all sensitive to oxacillin in a first test, in a second evaluation 1.3% of the strains showed resistance to oxacillin, they did not evaluate resistance to SXT or cefoxitin; López, et al., 2013 ¹⁶ did not evaluate resistance to oxacillin and cefoxitin, but did evaluate resistance to SXT, finding all their isolates sensitive. In reference to hospital isolates, Mamani et al., 2003, found that 32% of S. aureus strains were resistant to oxacillin; González et al., 2005, found oxacillin resistance in 9.3% of their isolates.

In Staphylococcus aureus, methicillin resistance can be detected by the diffusion technique, with oxacillin and/or cefoxitin discs. Resistance to oxacillin is induced by the mecA gene and implies resistance to all beta-lactams, which is why antibiogram evaluation must be careful; in case of heteroresistance, strains are often shown to be sensitive to many beta-lactams, an interpretation that can lead to therapeutic failure, strains with homogeneous resistance to oxacillin show high level of cross-resistance to all beta-lactams including penicillins, cephalosporins, carbapenems and monobactams. Cefoxitin-resistant S. aureus strains also indicate the presence of Susceptibilidad antibiótica de Staphylococcus aureusde aislados nasales en estudiantes del norte de Perú, thus resistance to all beta-lactams, cefoxitin sensitivity rules out methicillin heteroresistance ²⁶.

The penicillin evaluation showed resistance in 95.3% of the isolated strains, coinciding with Zelaya et al., 2001 ²⁷ who isolated Staphylococcus aureusin 61.67% of samples from nasal cavities and 46.67% from health personnel at a hospital in Ica, reporting that all isolates were resistant to penicillin; Sanabria et al, 2003 ²⁸ in Paraguay and Otth et al., 2007 ²⁰ in Chile, in a similar work reported Penicillin resistance in 98% and 86%, respectively, in S. aureus isolates from hospitalised patients. The mechanism of penicillin resistance is currently very frequent in S. aureus, with the prevalence of resistant strains being around 90%, figures that are variable according to the different institutions and hospitalisation units.

100% of the strains tested showed sensitivity to Vancomycin and Imipenem, coinciding with Gaona et al., 2009 and Villafañe et al., 2013, who obtained absolute sensitivity results with vancomycin, not evaluating resistance with Imipenem in both cases. In clinical isolates, Mamani et al., in a hospital in Lima, and Sanabria et al., in a hospital in Paraguay, both in 2003 obtained 100% vancomycin-sensitive strains; in Ica, Zelaya et al., 2001 determined that 94.60% of Staphylococcus aureusstrains isolated from nasal cavities were sensitive to imipenem; Aguilar et al. in 2009 in Lambayeque did not find multi-resistance in their research.

When analysing the susceptibility patterns obtained, it could be seen that only 2 strains (4.7%) were resistant to a single antibiotic, 6 strains (13.9%) to two antibiotics, 23 strains (53.4%) to three antibiotics, 11 strains (25.5%) to four antibiotics; finding only 1 strain (2.3%) sensitive to all antibiotics evaluated; showing cases of multiresistance; not agreeing with López, et al, 2012, Gaona et al., 2009 and Villafañe et al., 2013, who in their research with university students did not find multiresistance in the strains they evaluated; in the hospital environment they agree with Mendoza et al, 2000 ²⁹, who found that 50 % of the isolates obtained were methicillin-resistant Staphylococcus aureus(MRSA), all of which were multiresistant, disagreeing with Sanabria et al, 2003 in their investigation of nasal carriers from three health centres determined that 21% of the isolated strains were methicillin-resistant, with only one strain resistant to all the antibiotics evaluated, except vancomycin, while Otth et al., 2007 in their study in hospitalised patients, outpatients and carriers, found six patterns of resistance in S. aureus strains; no strains resistant to vancomycin were found.

In the evaluations carried out, no specific resistance profile pattern was found among the Staphylococcus aureusstrains that were analysed, showing that the resistance patterns observed indicate the frequency and consumption of antibiotics used by university students. To perform the analysis of the cross-reaction with other antibiotics to the strains that were resistant to Oxacillin, 39 strains were evaluated, of which 2.6% showed resistance to Ceftazidime, 12.8% to Azithromycin, 15.4% to Cefotaxime, and 20.9% to Gentamicin; on the other hand, they were 100% sensitive to Amikacin, Ciprofloxacin, Ceftriaxone and Cefuroxime; in agreement with Sanabria et al, 2003, who evaluated strains of methicillin-resistant Staphylococcus aureusand all showed cross-resistance to at least 4 antibiotics. Although research on bacterial susceptibility and resistance profile for S. aureus exists, no further work was found on the analysis of antibiotic cross-reactivity for our microorganism under study.

Regarding the detection of possible clinical factors associated with bacterial colonisation of Staphylococcus aureus, the data provided by the survey after evaluation of the positive isolates determined that 9.3% of the participants had recurrent pharyngeal infections and 41.3% had a history of acute respiratory infections, including colds and flu, either due to some type of respiratory virus that favours bacterial colonisation, 42% suffered from allergies, and 46% were in the habit of self-medicating; The background was related to prevalent results, to students with positive and resistant isolates to the antibiotics evaluated. Self-medication was the common clinical factor in all positive Staphylococcus aureusisolates. Villafañe et al., 2013 considers that hospitalisation and living with people who work in hospitals are risk factors that allow the acquisition of nosocomial strains that can subsequently be transmitted to communities; López, et al., 2013 found that a considerable percentage of students who lived with family members who worked in a health centre (31.4%), and suffered from asthma (9.3%).

Regarding the detection of possible clinical factors associated with Staphylococcus aureusbacterial colonisation, the data provided by the survey after the evaluation of positive isolates determined that 9.3% of the participants had recurrent pharyngeal infections and 41.3% had a history of acute respiratory infections, including colds and flu, either due to some type of respiratory virus that favours bacterial colonisation, 42% suffered from allergies, and 46% were in the habit of self-medicating; The background was related to prevalent results, to students with positive isolates that were resistant to the antibiotics evaluated. Self-medication was the common clinical factor in all positive Staphylococcus aureusisolates. Villafañe et al., 2013 considers that hospitalisation and living with people who work in hospitals are risk factors that allow the acquisition of nosocomial strains that can subsequently be transmitted to communities; López, et al., 2012 found that a considerable percentage of students who lived with family members who worked in a health centre (31.4%), and suffered from asthma (9.3%). A total of 150 nasal swab samples were analysed, resulting in 43 positive isolates for Staphylococcus aureus, representing 28.6% of the total study population. Of the Staphylococcus aureusisolates, 90.6% were resistant to Oxacillin, 19% to Sulfamethoxazole - Trimethopin, 95.3% to penicillin, 18.6% to Vancomycin and 38% to Cefoxitin, with all isolates being sensitive to Imipenem.

When analysing the cross-reactivity of the 39 strains of Staphylococcus aureusresistant to Oxacillin with other antibiotics, especially with cephalosporins, it was determined that 2.6% showed resistance to Ceftazidime, 12.8% to Azithromycin, 15.4% to Cefotaxime and 20.9% to Gentamicin; all the strains tested were sensitive to Amikacin, Ciprofloxacin, Ceftriaxone and Cefuroxime. Of all the students at the Universidad Nacional Pedro Ruiz Gallo who participated in the present investigation, it was determined that the Professional School of Biological Sciences had the highest frequency of Staphylococcus aureusisolates.

References

1. Kerwat K, Graf J, Wulf H. Krankenhaushygiene Nosokomiale Infektionen. Vol. 45, Anasthesiologie Intensivmedizin Notfallmedizin Schmerztherapie. 2010. p. 30?1.

2. Gastmeier P, Geffers C, Herrmann M, Lemmen S, Salzberger B, Seifert H, et al. Nosokomiale Infektionen und Infektionen mit multiresistenten Erregern - Häufigkeit und Sterblichkeit. Dtsch Medizinische Wochenschrift. 2016 Mar 16;141(6):421?427.

3. Conde A. Staphylococcus aureus infections. N Engl J Med. 1998;339(27):2026.

4. Golubchik T, Batty EM, Miller RR, Farr H, Young BC, Larner-Svensson H, et al. Within-Host Evolution of Staphylococcus aureus during Asymptomatic Carriage. PLoS One. 2013 May 1;8(5).

5. Hodille E, Badiou C, Bouveyron C, Bes M, Tristan A, Vandenesch F, et al. Clindamycin suppresses virulence expression in inducible clindamycin-resistant Staphylococcus aureus strains 11 Medical and Health Sciences 1108 Medical Microbiology. Ann Clin Microbiol Antimicrob. 2018 Oct 20;17(1).

6. Becker K, Denis O, Roisin S, Mellmann A, Idelevich EA, Knaack D, et al. Detection of mecA-and mecC-positive methicillin-resistant staphylococcus aureus (MRSA) isolates by the new Xpert MRSA Gen 3 PCR assay. J Clin Microbiol. 2016 Jan 1;54(1):180?4.

7. Prère MF, Baron O, Cohen Bacrie S, Fayet O. Genotype MRSA, a new genetic test for the rapid identification of staphylococci and detection of mecA gene. Pathol Biol. 2006 Oct;54(8-9 SPEC.ISS.):502?505.

8. Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H, Spratt BG. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci U S A. 2002 May 28;99(11):7687?7692.

9. Davis KA, Stewart JJ, Crouch HK, Florez CE, Hospenthal DR. Methicillin-Resistant Staphylococcus aureus (MRSA) Nares Colonization at Hospital Admission and Its Effect on Subsequent MRSA Infection. Clin Infect Dis [Internet]. 2004 Sep 15 [cited 2020 Feb 5];39(6):776?82. Available from: https://academic.oup.com/cid/article-lookup/doi/10.1086/422997

10. Popovich KJ, Weinstein RA, Hota B. Are Community-Associated Methicillin-Resistant Staphylococcus aureus (MRSA) Strains Replacing Traditional Nosocomial MRSA Strains? Clin Infect Dis [Internet]. 2008 Mar 15 [cited 2020 Feb 5];46(6):787?94. Available from: https://academic.oup.com/cid/article-lookup/doi/10.1086/528716

11. David MZ, Daum RS. Community-associated methicillin-resistant Staphylococcus aureus: Epidemiology and clinical consequences of an emerging epidemic. Vol. 23, Clinical Microbiology Reviews. American Society for Microbiology; 2010. p. 616?687.

12. Sacsaquispe R, Ventura G. Manual de procedimientos bacteriolgógicos en infecciones intrahospitalarias [Internet]. 2002 [cited 2020 Feb 5]. 109 p. Available from: https://www.gob.pe/institucion/minsa/informes-publicaciones/284839-manual-de-procedimientos-bacteriologicos-en-infecciones-intrahospitalarias

13. Wikler M, Cockerill F, Craig W, Dudley M, Eliopoulos G, Hecht D. Performance Standards for Antimicrobial Susceptibility Testing; Seventeenth Informational Supplement. CLSI docum. Vol. 27, Clinical and Laboratory Standars Institute - NCCLS. Wayne, PA: Clinical and Laboratory Standards Institute; 2007. 1?182 p.

14. Eady EA, Cove JH. Staphylococcal resistance revisited: Community-acquired methicillin resistant Staphylococcus aureus - An emerging problem for the management of skin and soft tissue infections. Vol. 16, Current Opinion in Infectious Diseases. Lippincott Williams and Wilkins; 2003. p. 103?24.

15. Noriega Ricalde LM, González P, Hormazábal JC, Pinto C, Canals M, Munita JM, et al. Staphylococcus aureus comunitario resistente a cloxacilina: Comunicación de los primeros cinco casos descritos en Chile. Rev Med Chil. 2008 Jul;136(7):886?91.

16. López-Aguilera S, Del Mar Goñi-Yeste M, Barrado L, González-Rodríguez-Salinas CM, Otero JR, Chaves F. Colonización nasal por Staphylococcus aureus en estudiantes de medicina: Importancia en la transmisión hospitalaria. Enferm Infecc Microbiol Clin. 2013; 31(8):500?5.

17. Cifuentes MAG, Chaparro DIR, Serrato MCP, Peña ACP, Pinilla MI, Gutiérrez GR. Variación del estado de portador de Staphylococcus aureus en una población de estudiantes de medicina. Rev Ciencias la Salud [Internet]. 2009 [cited 2020 Feb 5];7(1):37?46. Available from: https://revistas.urosario.edu.co/index.php/revsalud/article/view/374

18. Villafañe Ferrer L, Pinilla Pérez M, Carpintero Polanco Y, Cueto Cantillo V, Solís Sotomayor Y. Portación nasal de staphylococcus aureus en estudiantes de bacteriología. Salud Uninorte. 2013;29(2):151?9.

19. Gabriela Sanabria B. Evolution of resistance in Staphylococcus aureus. Vol. 3, Rev. Inst. Med. Trop.

20. Otth Rademacher L, Wilson Sch. M, Bustamante H. N, Fernández J. H, Otth L. C. Susceptibilidad antimicrobiana y patrones de resistencia de Staphylococcus aureus aislados de pacientes y portadores en la ciudad de Valdivia, Chile. Rev Chil Infectol. 2008 Jun;25(3):175?178.

21. Arteaga-Delgado LC, Espinosa-López Y, Chávez-Vivas M. Prevalencia de Staphylococcus aureus que coloniza el personal de salud de un hospital de la ciudad de Cali. Ciencias la Salud. 2016;14(1):9?19.

22. González Mesa L, Morffi Figueroa J, Nadal Becerra L, Vallín Plous C, Contreras R RG. Frecuencia de aislamiento de Staphylococcus spp meticilina resistentes y Enterococcus spp vancomicina resistentes en hospitales de Cuba. Revista Cubana de Farmacia [Internet]. 2005 [cited 2020 Feb 5];39. Available from: http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S0034-75152005000300003

23. Platzer M L, Aranís J C, Beltrán M C, Fonseca A X, García C P. Colonización nasal bacteriana en población sana de la ciudad de Santiago de Chile: ¿Existe portación de Staphylococcus aureus meticilino resistente comunitario? Rev Otorrinolaringol y cirugía cabeza y cuello. 2010;70(2):109?116.

24. Paganini MH, Della L. P, Muller O. B, Ezcurra G, Uranga M, Aguirre C, et al. Infecciones por Staphylococcus aureus resistente a meticilina adquiridas en la comunidad en niños antes sanos y en niños relacionados al hospital en la Argentina. Rev Chil Infectol. 2009 Oct;26(5):406?412.

25. Aguilar-Gamboa FR, Valiente JN, Mantilla MM. Portadores Nasofaríngeos de Staphylococcus aureus y Streptococcus pneumoniae en personal de Salud del Hospital Provincial Docente Belén de Lambayeque [Internet]. Vol. 1, Revista Experiencia en Medicina del Hospital Regional Lambayeque. 2015 [cited 2020 Feb 5]. Available from: http://rem.hrlamb.gob.pe/index.php/REM/article/view/17

26. Nodarse Hernández CR. Detección de Staphylococcus aureus resistente a meticilina mediante disco de cefoxitina. Rev Cuba Med Mil [Internet]. 2009 [cited 2020 Feb 5];38(3?4):30?39. Available from: http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S0138-65572009000300004

27. Zelaya-Trebejo L, Zelaya-Vargas J, Miranda-Soberón U, Guillermo-Albites J, Hernández-Zúñiga D. Portadores intrahospitalarios de Staphylococcus aureus y sensibilidad a los antimicrobianos. Rev Peru Enfermedades Infecc y Trop [Internet]. 2006 [cited 2020 Feb 5];1(1). Available from: http://sisbib.unmsm.edu.pe/BVRevistas/SPEIT/2001_n1/Articulo_Original/pag_16.htm

28. Sanabria G. Evolución de la resistencia en el Staphylococcus aureus. Rev Inst Med Trop [Internet]. 2008 [cited 2020 Feb 5];3(2):27?39. Available from: http://revistas.ins.gov.py/index.php/revistaimt/article/view/142

29. Mendoza N. C, Barrientos M. C, Panizza F. VEU, Concha BEU, Romero PP, Barahona CFTMM, et al. Prevención de la infección intrahospitalaria por Staphylococcus aureus resistente a meticilina mediante el manejo de portadores. Rev Chil Infectol. 2000;17(2):129?134.

Author notes

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