Sage Journals: Discover world-class research

Abstract

Staphylococcal infection is associated with significant morbidity and mortality in critically ill patients. Using data from 16,681 patients who had a nasal Staphylococcus aureus polymerase chain reaction (PCR) assay on admission to the intensive care unit (ICU) of Royal Perth Hospital between March 2006 and September 2016, this retrospective cohort study assessed whether nasal S. aureus colonisation on admission to an ICU was predictive of concurrent or subsequent S. aureus infections. Culture-proven S. aureus infections were identified using the hospital microbiology database. Of the 16,681 patients included, 565 (3.4%) had a positive methicillin-resistant S. aureus (MRSA) assay, 146 (0.9%) had a positive methicillin-sensitive S. aureus (MSSA) assay and eight (0.05%) had both positive MRSA and MSSA assays. Of those 565 patients with a positive MRSA PCR assay, 79 (13.8%) had concurrent or subsequent MRSA infections. Of those 146 patients with a positive MSSA PCR assay, only 5 (3.4%) had MSSA infection. The sensitivity and specificity for the MRSA PCR assay in predicting concurrent or subsequent MRSA infection were 72.7% (95% confidence intervals (CI) 63.4%–80.8%) and 97.0% (95% CI 96.8%–97.3%), respectively. The sensitivity and specificity for the MSSA PCR assay in predicting concurrent or subsequent MSSA infection were 3.3% (95% CI 1.1%–7.6%) and 99.1% (95% CI 98.9%–99.2%), respectively. Both nasal MRSA and MSSA PCR assays had a high specificity and negative predictive value in predicting MRSA and MSSA infections, respectively, suggesting that in centres without endemic S. aureus infections, a negative nasal MRSA or MSSA PCR assay may be useful to reduce unnecessary empirical antibiotic therapy against S. aureus.

Keywords

Bacteraemia colonisation infection polymerase chain reaction prediction screening

Introduction

Staphylococcus aureus infections are common¹ and are associated with substantial morbidity and mortality.^2–4 In 2015–2016, 1440 cases of hospital-acquired bacteraemia due to either methicillin-resistant S. aureus (MRSA; 19%) or methicillin-sensitive S. aureus (MSSA; 81%), with an overall incidence of 0.73 per 10,000 days of patient care, were reported in Australian public hospitals.⁵ S. aureus bacteraemia is associated with >10% hospital mortality,^2,3 and MRSA bacteraemia is often empirically treated with antibiotics to which the pathogen is not susceptible in vitro while cultures and susceptibilities are pending, resulting in prolonged bacteraemia and increased incidence of metastatic seeding of infection compared to MSSA bacteraemia.³ On the other hand, unnecessary anti-MRSA therapy also has significant risks at both patient and community levels, including nephrotoxicity from vancomycin, anaphylaxis to teicoplanin⁶ and development of vancomycin-resistant Enterococci.⁷ As such, it is imperative to develop rapid and reliable ways to identify patients who are at high risk of MRSA infection—in particular MRSA bacteraemia—so that prompt appropriate empirical antibiotics can be initiated while minimising overuse of broad-spectrum antibiotics.⁸

S. aureus can be found in different body sites such as the skin, rectum, vagina, gastrointestinal tract and axilla. Once the bacteria are in contact with the nasal mucosa, they will interact with epithelial cell ligands, such as loricrin and cytokeratin 10 (K10), and colonise the anterior nares.⁹ It has been estimated that up to 30% of the human population are asymptomatically and permanently colonised with S. aureus in their anterior nares.⁹ In critically ill patients, recent studies have suggested that nasal colonisation with S. aureus is associated with a higher subsequent risk of S. aureus infections, including bacteraemia.^10–12 In addition, nasal decolonisation of S. aureus is associated with a reduced risk of S. aureus pneumonia in critically ill patients and surgical site infection prior to surgery.^13,14 Nonetheless, whether nasal S. aureus colonisation—confirmed by a polymerase chain reaction (PCR) assay—on admission to an intensive care unit (ICU) is predictive of all forms of subsequent MRSA and MSSA infections is uncertain.

We hypothesised that nasal MRSA and MSSA colonisation in the critically ill on admission to an ICU can be predictive of MRSA and MSSA infections, respectively. In this retrospective cohort study, we aimed to determine the associations between a positive nasal MRSA/MSSA PCR assay on admission to ICU and concurrent or subsequent S. aureus infections during the same hospitalisation.

Methods

Patients and setting

Nasal swabs were taken for all patients admitted to the ICU of Royal Perth Hospital within the first hour of admission to identify MRSA colonisation for infection control purposes. Nasal swabs were taken only on admission to the ICU, including readmissions, but not during ICU stay. Contact precaution measures including use of an isolation room would be implemented for patients who were identified as MRSA colonised. Eradication therapy, such as topical mupirocin, was not used. In this study, 16,681 consecutive patients who were admitted to the ICU between 30 March 2006 and 30 September 2016 were included. Patients admitted to the co-located high dependency unit were not screened for MRSA and were excluded from this study unless they were subsequently admitted to the ICU. For patients who had more than one ICU admission during the same hospitalisation, only the nasal MSSA and MRSA PCR results in the index ICU admission were used in this study.

The nasal colonisation for MRSA and MSSA was determined by a PCR assay using either the IDI-MRSA (from March 2006 to June 2013) or the automated BD Max (from July 2013 to the end of study period) system, with the results available within three hours in the study centre.^15,16 The first-generation BD Max MRSA assay was not able to identify correctly the mecA empty cassette or the MRSA strains with methicillin resistance gene mecC and some MRSA mec right-extremity junction type strains.¹⁷ In this study, patients with a positive MRSA or MSSA PCR assay, and any concurrent or subsequent culture-confirmed MRSA or MSSA infections during the same hospital stay, were identified using the hospital microbiology database. An infection due to S. aureus was defined as either growth of S. aureus from a sterile site (e.g. blood or joint fluid) or identification of S. aureus from a non-sterile site (e.g. wound or sputum) while there was clinical and/or radiological evidence of infection and no other cause/pathogen could be identified. The microbiology data of the study patients were then merged with the ICU administrative database for this clinical audit (CSQU approval number 13773).

Outcomes

The primary outcome of this study was the ability of a positive nasal MRSA or MSSA PCR assay in predicting concurrent or subsequent culture-proven MRSA or MSSA infection during the same hospital stay. Sensitivity, specificity, positive and negative predictive values, positive and negative likelihood ratios and area under the receiver operating characteristic curve were used to describe the ability of a nasal MRSA and MSSA PCR assay to predict concurrent or subsequent MRSA and MSSA infections, respectively.

Statistical analyses

Because we did not have prior local data on the incidence of a positive nasal MRSA or MSSA PCR assay, the number of patients included was maximised by including all patients who were admitted to the ICU after MRSA/MSSA PCR was initiated for routine use as an infection control measure until initiation of this audit.

Descriptive categorical and continuous data are presented as the number (%) and median (interquartile range (IQR)), respectively. In addition to sensitivity and specificity, the ability of a positive nasal MRSA PCR assay to predict concurrent or subsequent MRSA infection was further assessed by logistic regression with and without adjusting for important covariates in a subgroup of patients with either MRSA/MSSA infection or a positive nasal MRSA/MSSA PCR assay. The covariates used for adjustment were markers of severity of acute and chronic illnesses which might confound the relationship between colonisation and infection. The time from confirming MSSA/MRSA colonisation to infection was not analysed because many of our study patients had concurrent MSSA/MRSA infections instead of development of such infections subsequently. All statistical analyses were conducted using IBM SPSS Statistics for Windows v24.0 (IBM Corp., Armonk, NY, USA) and MedCalc for Windows v12.5 (MedCalc Software Ltd, Ostend, Belgium), and a two-tailed alpha error of <5% was taken as significant. De-identified study data are available on request from the corresponding author.

Results

Of the 16,681 patients eligible and included in the study, 565 (3.4%) had a positive MRSA PCR assay, 146 (0.9%) had a positive MSSA PCR assay, and eight (0.05%) had both positive MRSA and MSSA PCR assays. The rates of MRSA infection (109/16,681; 0.65%) and colonisation (573/16,681; 3.4%) in patients admitted to our ICU were relatively low. Of the 719 patients who had a positive MRSA or MSSA PCR assay, 94 (13%) had coexisting or subsequent MRSA or MSSA infections compared to only 1.0% incidence of MRSA or MSSA infections among those who did not have a positive MRSA or MSSA PCR assay (n = 15,962 patients; Figure 1). Of the 109 and 151 culture-proven MRSA and MSSA infections, 62% and 92% were isolated from sterile sites, including blood culture, joint fluid, pleural fluid or tissue (e.g. heart valve, bone and vascular grafts; Table 1), respectively.

Figure 1.

Flow chart showing the patients with and without a positive polymerase chain reaction (PCR) for methicillin-sensitive Staphylococcus aureus (MSSA) or methicillin-resistant Staphylococcus aureus (MRSA) and subsequent risk of MSSA or MRSA culture-proven infection. The proportion of patients and incidence rate of MRSA infections (estimated using median length of hospital stay of 15 days) among those without a positive nasal MRSA PCR assay were 0.18% and 0.44 per 1000 patient years, respectively. Two patients with negative MRSA and MSSA PCR assays had both MRSA and MSSA infections.

Table 1.

Characteristics of patients who had either a positive PCR assay for MSSA/MRSA or MSSA/MRSA culture-proven infection (N = 883).

Variable	Median (IQR) or n (%)
Age (years)	49 (33–66)
Male	564 (63.9)
APACHE II score	17 (10–23)
Length of intensive care unit stay (hours)	73 (34–166)
Length of hospital stay (days)	15 (5.7–30.1)
Intensive care unit mortality	135 (15.3)
Hospital mortality	179 (20.3)
MRSA culture-proven infection:	109 (12.3%)^a
Blood culture	31 (29)
Wound	54 (50)
Joint fluid	3 (3)
Pleural fluid	6 (6)
Tissue (e.g. heart valve, bone, graft)	28 (26)
MSSA culture-proven infection:	151 (17.1)^a
Blood culture	59 (39)
Wound	11 (7)
Joint fluid	18 (12)
Pleural fluid	14 (9)
Tissue (e.g. heart valve, bone, graft)	48 (32)
Chronic cardiovascular disease	58 (6.6)
Chronic respiratory disease	50 (5.7)
Cirrhosis	36 (4.1)
End-stage renal failure requiring dialysis	54 (6.1)^c
Current immunosuppressive therapy^b	19 (2.2)
Current immunosuppressive disease^b	21 (2.3)

^aNumber of patients; some patients had more than one positive culture specimen.

^bAccording to the APACHE model, current immunosuppressive diseases include active leukaemia, acquired immune deficiency syndrome, lymphoma, severe autoimmune disease and documented diffuse metastatic cancer; immunosuppressive therapy includes patients treated with chemotherapy, radiation or long-term low-dose steroids (during 30 days prior to hospitalisation) or recent high-dose steroid (≥1.5 mg/kg for ≥5 days).

^c35 patients had a positive nasal MRSA PCR assay without MRSA infection, six patients had MRSA infections without a positive nasal MRSA PCR assay and eight patients both nasal MRSA PCR positive assay and MRSA infection.

PCR: polymerase chain reaction; MSSA: methicillin-sensitive Staphylococcus aureus; MRSA: methicillin-resistant Staphylococcus aureus; IQR: interquartile range; APACHE: Acute Physiology and Chronic Health Evaluation.

Of the 883 patients who had either a positive nasal MRSA/MSSA PCR assay or MRSA/MSSA infection, infection/sepsis was the commonest clinical admission diagnosis (n = 160), followed by trauma (n = 75), postoperative management after major surgery (n = 63), acute cardiovascular diseases (n = 51), acute neurological diseases (n = 50) and acute respiratory diseases (n = 44). The characteristics of these 883 patients are described in Table 1.

Of those 565 patients with a positive MRSA PCR assay, 79 (13.8%) had concurrent MRSA infections on ICU admission (n = 72) or developed MRSA infections subsequently (n = 7; median = 2 days, IQR 1–11); 78/79 patients had a positive MRSA PCR assay alone, but one patient had both positive MRSA and MSSA PCR assays. Of those 146 patients with a positive MSSA PCR assay, five (3.4%) had concurrent MSSA infection (n = 1) or developed subsequent MSSA infection (n = 4; median = 3 days, IQR 1–6), and two (1.4%) developed MRSA infection (Figure 1). The proportion of patients and incidence rate of MRSA infections (estimated using median length of hospital stay of 15 days) among those without a positive nasal MRSA PCR assay were 0.18% and 0.44 per 1000 patient years, respectively.

Both nasal MRSA and MSSA PCR assays had a high specificity and negative predictive value but low sensitivity and positive predictive value in predicting concurrent or subsequent MRSA and MSSA infections, respectively. The sensitivity and specificity for a positive MRSA PCR assay for MRSA infection were 72.7% (95% confidence interval (CI) 63.4%–80.8%) and 97.0% (95% CI 96.8%–97.3%), respectively. The sensitivity and specificity for a positive MSSA PCR assay for MSSA infection were 3.3% (95% CI 1.1%–7.6%) and 99.1% (95% CI 98.9%–99.2%), respectively (Table 2).

Table 2.

Predictive parameters of MSSA and MRSA PCR assays for concurrent or subsequent MSSA and MRSA culture-proven infection, respectively.

	Mean (95% CI)
MRSA PCR
Sensitivity	72.7% (63.4–80.8)
Specificity	97.0% (96.8–97.3)
Positive likelihood ratio	24.5 (21.2–28.2)
Negative likelihood ratio	0.28 (0.21–0.38)
Positive predictive value	14.0% (12.3–15.8)
Negative predictive value	99.8% (99.7–99.9)
Area under the receiver operating characteristic curve	0.849 (0.843–0.854)
MSSA PCR
Sensitivity	3.3% (1.1–7.6)
Specificity	99.1% (98.9–99.2)
Positive likelihood ratio	3.5 (1.5–8.4)
Negative likelihood ratio	0.98 (0.95–1.01)
Positive predictive value	3.1% (1.3–7.1)
Negative predictive value	99.1% (99.0–99.2)
Area under the receiver operating characteristic curve	0.512 (0.504–0.519)

CI: confidence interval; MSSA: methicillin-sensitive Staphylococcus aureus; MRSA: methicillin-resistant Staphylococcus aureus; PCR: polymerase chain reaction.

In the univariable logistic regression analysis, there was a suggestion that a positive nasal MRSA PCR was associated with an increased risk of having MRSA infection, but this was not statistically significant (odds ratio (OR) = 1.55, 95% CI 0.99–2.43, P =0.056). This result remained unchanged (OR = 1.64, 95% CI 0.96–2.79, P = 0.068) after adjusting for age, Acute Physiology and Chronic Health Evaluation II score and coexisting diseases (Table 3). End-stage renal failure requiring dialysis was the only major comorbidity associated with an increased risk of MRSA infection (OR = 2.08, 95% CI 1.01–4.26, P = 0.047).

Table 3.

Logistic regression showing the relationship between a positive nasal MRSA PCR assay and risk of having concurrent or subsequent MRSA infection after adjusting for other covariates (N = 883).

Predictors	Odds ratio (95% CI)	P-value
Age (per year increment)	1.00 (0.99–1.02)	0.687
APACHE II score (per score increment)	1.03 (1.00–1.05)	0.054
Positive nasal MRSA PCR assay	1.64 (0.96–2.79)	0.068
Chronic respiratory disease	1.96 (0.92–4.16)	0.080
Chronic cardiovascular disease	1.37 (0.59–3.18)	0.472
Current immunosuppressive therapy^a	2.08 (0.44–9.72)	0.354
Current immunosuppressive disease^a	1.00 (0.28–3.61)	0.995
End-stage renal failure requiring dialysis	2.08 (1.01–4.26)	0.047
Cirrhosis	1.20 (0.47–3.07)	0.711

^aAccording to the APACHE model, current immunosuppressive diseases include active leukaemia, acquired immune deficiency syndrome, lymphoma, severe autoimmune disease and documented diffuse metastatic cancer; immunosuppressive therapy includes patients treated with chemotherapy, radiation or long-term low-dose steroids (during 30 days prior to hospitalisation) or recent high-dose steroid (≥1.5 mg/kg for ≥5 days).

OR: odds ratio; MSSA: methicillin-sensitive Staphylococcus aureus; MRSA: methicillin-resistant Staphylococcus aureus; PCR: polymerase chain reaction; APACHE: Acute Physiology and Chronic Health Evaluation.

Discussion

A delay in initiating appropriate antimicrobial therapy for infection, in particular for those with bacteraemia, is associated with an increased risk of organ failure, metastatic infection and mortality.^3,18–21 In this study, our results showed that both nasal MRSA and MSSA PCR assays have a high specificity and negative predictive value but a low sensitivity, especially the MSSA PCR assay, to predict concurrent or subsequent clinical staphylococcal infections. These results are consistent with a recent systematic review on the utility of nasal MRSA PCR assays in predicting MRSA infections (pooled specificity was >90%, but positive predictive value was only 50%),²² suggesting that only a negative MRSA PCR assay may have clinical utility when the probability of having subsequent MRSA infection would be low and empirical vancomycin therapy for any suspected nosocomial sepsis may not be indicated, especially in clinical areas where MRSA is not endemic, as in our study centre. Conversely, a positive MRSA PCR assay is not particularly helpful with a low sensitivity and low positive predictive value. Initiating empirical vancomycin based on a positive MRSA PCR assay result would thus lead to overuse of vancomycin, resulting in increased healthcare costs, risks of nephrotoxicity and development of organisms resistant to vancomycin.^7,23

Unlike the association between MRSA infection and nasal MRSA PCR assay, the association between a positive nasal MSSA swab and systemic MSSA infection has so far received little attention.²⁴ In this study, we showed that the prevalence of a positive nasal MSSA PCR assay in our patients was much lower than expected compared to the general population.⁹ This result may be related to the fact that many study patients might have received broad-spectrum antibiotics prior to their ICU admissions, or the nasal MSSA PCR assay was just not as sensitive. In a study of 79 episodes of S. aureus (MRSA 12% and MSSA 87%) bacteraemia,²⁴ the incidence of a positive nasal swab culture for MSSA or MRSA was <50%, suggesting that the sensitivity of a nasal swab culture for MSSA is low. If this study’s results as well as ours are confirmed by other studies, use of a MSSA PCR assay to identify patients who are at increased risk of MSSA infection including MSSA bacteraemia will not be cost effective. Nonetheless, due to its high negative predictive value, a negative MSSA PCR assay may still be useful to exclude concurrent MSSA infection, similar to the utility of a negative MRSA PCR assay.

This study showed that patients with end-stage renal failure requiring dialysis admitted to our ICU were at increased risk of having MRSA infections independent of their nasal MRSA colonisation status. This result is consistent with other reports showing end-stage renal failure is a risk factor of MRSA colonisation, infection and infection-related mortality.^25–30 Within the nested cohort of our patients who were either colonised or infected with MSSA/MRSA, the MRSA infection rate among those with end-stage renal failure was high (14/54; 26%) compared to those without end-stage renal failure (73/668; 12.3%). If our results are confirmed by other Australian ICUs, perhaps empirical vancomycin therapy should be considered in critically ill patients who have end-stage renal failure when serious systemic infection or bacteraemia is suspected, especially if they are known to be colonised with MRSA, or in centres where MRSA infection is endemic.

Finally, we need to acknowledge the limitations of this study. First, staphylococcal infections are not endemic in our centre, and this would increase the negative predictive values of both nasal MSSA and MRSA PCR assays in predicting staphylococcal infection. As such, our results may not be generalisable to centres that have endemic staphylococcal infections. Second, we only analysed patients with culture-proven staphylococcal infection. It is possible that some staphylococcal infections might have occurred among those who had been colonised with MRSA or MSSA, but the microbiological cultures were not taken or they were treated empirically with antibiotics, reducing the yield of subsequent microbiological cultures. In addition, we also did not have data on MRSA contact prior to index ICU admission. Prospective research including contact history will be useful to assess whether this can strengthen the ability of nasal MRSA PCR assay in predicting MRSA infections. Third, the sensitivity of using nasal swabs to detect bacterial colonisation may be subject to variations in the techniques in obtaining the nasal swabs, as well as how many nasal swabs are taken. A recent study suggested that significantly more (P = 0.016) patients with two negative nasal swabs returned with a recurrent MRSA infection or colonisation than those who had three consecutive negative nasal swabs (27.8% versus 17.0%, respectively).³¹ Finally, the sensitivity of a PCR assay is known to be dependent on the strains of staphylococcal bacteria, which can vary substantially between different populations.³² This important limitation has recently been overcome with the development of two new generations of more sensitive MRSA PCR assays.¹⁷

Conclusions

Both nasal MRSA and MSSA PCR screening assays obtained on admission to the ICU had a high specificity in predicting concurrent or subsequent S. aureus infections, respectively. However, the sensitivity of both MRSA and MSSA PCR assays were low, especially for the MSSA PCR assay. These results suggest that only a negative MSSA and MRSA PCR assay may have some degree of clinical utility when the probability of having staphylococcal infection would be low and empirical anti-staphylococcal antibiotic therapy would not be indicated for patients with nosocomial sepsis, especially in ICUs where S. aureus infections are not an endemic problem.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship and/or publication of this article.

ORCID iD

Kwok M Ho

References

Monaco

Pimentel de Araujo

Cruciani

, et al. Worldwide epidemiology and antibiotic resistance of Staphylococcus aureus. Curr Top Microbiol Immunol 2017; 409: 21–56.

Lam

Gregson

Robinson

, et al. Epidemiology and outcome determinants of Staphylococcus aureus bacteremia revisited: a population-based study. Infection 2019; 47: 961–971.

Robinson

JO.

Risk factors and outcomes of methicillin-resistant Staphylococcus aureus bacteraemia in critically ill patients: a case control study. Anaesth Intensive Care 2009; 37: 457–463.

Yaw

Robinson

KM.

A comparison of long-term outcomes after meticillin-resistant and meticillin-sensitive Staphylococcus aureus bacteraemia: an observational cohort study. Lancet Infect Dis 2014; 14: 967–975.

Australian Institute of Health and Welfare. Staphylococcus aureus bacteraemia in Australian public hospitals 2015–16: Australian hospital statistics. Health services series no. 74. Cat. no. HSE 184, https://www.aihw.gov.au/reports/hospitals/ahs-2015-16-sab/contents/table-of-contents (2017, accessed 20 August 2019).

Cook

Harper

Anaesthesia, surgery and life-threatening allergic reactions. Report and findings of the Royal College of Anaesthetists’ 6th National Audit Project: perioperative anaphylaxis, https://www.nationalauditprojects.org.uk/NAP6home?newsid=959 (2018, accessed 19 January 2020).

Karandikar

Milliren

Zaboulian

, et al. Limiting vancomycin exposure in pediatric oncology patients with febrile neutropenia may be associated with decreased vancomycin-resistant enterococcus incidence. J Pediatric Infect Dis Soc. Epub ahead of print 11 October 2019. DOI: 10.1093/jpids/piz064.

Kluytmans

Control of meticillin-resistant Staphylococcus aureus (MRSA) and the value of rapid tests. J Hosp Infect 2007; 65: 100–104.

Sakr

Brégeon

Mège

, et al. Staphylococcus aureus nasal colonization: an update on mechanisms, epidemiology, risk factors, and subsequent infections. Front Microbiol 2018; 9: 2419.

10.

Gagnaire

Botelho-Nevers

Martin-Simoes

, et al. Interplay of nasal and rectal carriage of Staphylococcus aureus in intensive care unit patients. Eur J Clin Microbiol Infect Dis 2019; 38: 1811–1819.

11.

Honda

Krauss

Coopersmith

, et al. Staphylococcus aureus nasal colonization and subsequent infection in intensive care unit patients: does methicillin resistance matter? Infect Control Hosp Epidemiol 2010; 31: 584–591.

12.

Smith

Erdman

Ferreira

, et al. Clinical utility of methicillin-resistant Staphylococcus aureus nasal polymerase chain reaction assay in critically ill patients with nosocomial pneumonia. J Crit Care 2017; 38: 168–171.

13.

Septimus

EJ.

Nasal decolonization: what antimicrobials are most effective prior to surgery?

Am J Infect Control 2019; 47: A53–57.

14.

Nardi

Di Silvestre

De Monte

, et al. Reduction in gram-positive pneumonia and antibiotic consumption following the use of a SDD protocol including nasal and oral mupirocin. Eur J Emerg Med 2001; 8: 203–214.

15.

Desjardins

Guibord

Lalonde

, et al. Evaluation of the IDI-MRSA assay for detection of methicillin-resistant Staphylococcus aureus from nasal and rectal specimens pooled in a selective broth. J Clin Microbiol 2006; 44: 1219–1223.

16.

Dalpke

Hofko

Hamilton

, et al. Evaluation of the BD Max StaphSR assay for rapid identification of Staphylococcus aureus and methicillin-resistant S. aureus in positive blood culture broths. J Clin Microbiol 2015; 53: 3630–3632.

17.

Silbert

Kubasek

Galambo

, et al. Evaluation of BD Max StaphSR and BD Max MRSAXT assays using ESwab-collected specimens. J Clin Microbiol 2015; 53: 2525–2529.

18.

Marchaim

Kaye

Fowler

, et al. Case-control study to identify factors associated with mortality among patients with methicillin-resistant Staphylococcus aureus bacteraemia. Clin Microbiol Infect 2010; 16: 747–752.

19.

Hounsom

Grayson

Melzer

Mortality and associated risk factors in consecutive patients admitted to a UK NHS trust with community acquired bacteraemia. Postgrad Med J 2011; 87: 757–762.

20.

Weiss

Fitzgerald

Balamuth

, et al. Delayed antimicrobial therapy increases mortality and organ dysfunction duration in pediatric sepsis. Crit Care Med 2014; 42: 2409–2417.

21.

Lodise

McKinnon

Swiderski

, et al. Outcomes analysis of delayed antibiotic treatment for hospital-acquired Staphylococcus aureus bacteremia. Clin Infect Dis 2003; 36: 1418–1423.

22.

Butler-Laporte

De L’Étoile-Morel

Cheng

, et al. MRSA colonization status as a predictor of clinical infection: a systematic review and meta-analysis. J Infect 2018; 77: 489–495.

23.

Gardete

Tomasz

Mechanisms of vancomycin resistance in Staphylococcus aureus. J Clin Invest 2014; 124: 2836–2840.

24.

Marshall

McBryde

The role of Staphylococcus aureus carriage in the pathogenesis of bloodstream infection. BMC Res Notes 2014; 7: 428.

25.

Grünewald

Lindner

Weiß

, et al. Staphylococcus colonization, mortality and morbidity in hemodialysis patients: 10 years of observation. Int J Hyg Environ Health 2013; 216: 751–754.

26.

Chen

Shieh

Sung

JM.

Increasing staphylococcus species resistance in peritoneal dialysis-related peritonitis over a 10-year period in a single Taiwanese center. Perit Dial Int 2018; 38: 266–270.

27.

Wang

HC.

Risk factors to predict drug-resistant pathogens in hemodialysis-associated pneumonia. BMC Infect Dis 2016; 16: 377.

28.

Ştefan

Stancu

Căpuşă

, et al. Catheter-related infections in chronic hemodialysis: a clinical and economic perspective. Int Urol Nephrol 2013; 45: 817–823.

29.

Schmid

Romanos

Schiffl

, et al. Persistent nasal methicillin-resistant Staphylococcus aureus carriage in hemodialysis outpatients: a predictor of worse outcome. BMC Nephrol 2013; 14: 93.

30.

Hsueh

, et al. Maintenance haemodialysis and delayed administration of appropriate antibiotics increase 30-day mortality among patients with non-hospital-acquired meticillin-resistant Staphylococcus aureus bacteraemia. Int J Antimicrob Agents 2010; 35: 511–512.

31.

Richards

Tremblay

Assessment of current methicillin-resistant Staphylococcus aureus screening protocols and outcomes at an academic medical center. Am J Infect Control 2019; 47: 906–910.

32.

Kim

Cha

, et al. Multiplex real-time PCR assay for detection of methicillin-resistant Staphylococcus aureus (MRSA) strains suitable in regions of high MRSA endemicity. J Clin Microbiol 2013; 51: 1008–1013.

Positive nasal Staphylococcus aureus polymerase chain reaction assay is not sensitive in predicting concurrent or subsequent Staphylococcus aureus infection in critically ill patients

Abstract

Keywords

Introduction

Methods

Patients and setting

Outcomes

Statistical analyses

Results

Discussion

Conclusions

Footnotes

Declaration of conflicting interests

Funding

ORCID iD

References