Rapid and actionable nasal-swab screening supports antimicrobial stewardship in patients with pneumonia: a prospective study

Abstract

Background

Methicillin-resistant Staphylococcus aureus (MRSA) nasal screening by polymerase chain reaction (PCR) is a rapid diagnostic tool with a high negative predictive value for pneumonia caused by MRSA. MRSA remains an important emerging pathogen in China and at present, there is little published data on the effect of rapid MRSA test results on antibiotic utilization for pneumonia.

Methods

A total of 300 inpatients who met the criteria of pneumonia in a tertiary general hospital were randomly assigned to a notification group (NG, n = 150) or a control group (CG, n = 150). Nasal swabs were collected and tested with the Xpert SA Nasal Complete Test (Cepheid, Sunnyvale, CA) to determine MRSA colonization status. Attending clinicians were immediately informed of test results for patients in NG while results were not released to an attending physician in CG. Subsequently, relevant medical records were collected and analyzed.

Results

Patients in the NG received a shorter duration of antimicrobial therapy compared to the CG (5.66 vs. 7.87 days, P < 0.001). Fewer renal injuries (1.33% vs. 8%; P = 0.015), and lower costs of antimicrobial agents ($621.78 vs. $881.70; P = 0.013) were observed in NG patients compared to those in the CG. Further, this intervention did not increase the in-hospital mortality (12.67% vs. 16.67%, P = 0.327).

Conclusions

Rapid and actionable MRSA PCR screening using nasal swabs helped reduce unnecessary anti-MRSA treatment. Early management of antimicrobials not only reduced the duration of anti-MRSA drug exposure but also antimicrobial-related adverse events.

Supplementary Information

The online version contains supplementary material available at 10.1186/s13756-025-01615-5.

Introduction

Methicillin-resistant Staphylococcus aureus (MRSA) is a common pathogen that can cause a variety of infections ranging from skin infections, to pneumonia and bacteremia [1, 2]. Worldwide, an estimated 15% of ICU infections are caused by Staphylococcus aureus, and nearly one-third of those (31%) are due to MRSA [3, 4]. Patients infected with MRSA had a significantly longer length of hospital stay, higher cost of care, and higher mortality than those with MSSA infections [5–7]. In the post-pandemic era, the detection rate of methicillin-resistant Staphylococcus aureus (MRSA) in respiratory specimens ranges from 3–10% [8, 9]. MRSA ranks among the prominent pathogens causing pneumonia in cases of hospital-acquired pneumonia (HAP) [10]. Meanwhile, while the MRSA infection rate in community-acquired pneumonia (CAP) remains relatively low at approximately 1%, it persists as a significant etiological agent. Consequently, nearly one-third of adults hospitalized with CAP receive anti-MRSA antibiotic therapy [11, 12]. Which is why the critical need for rapid and precise clinical diagnostic tools should be called out.

MRSA are frequent colonizers of human skin, which includes nares, groin, axilla, and throat [13–17]. The nares are the most common site of colonization and the site usually used to assess colonization. The ability to rule out MRSA as a cause of pneumonia using nasal swab specimens for polymerase chain reaction (PCR) testing has attracted considerable attention in recent years. The Infectious Diseases Society of America (IDSA) and the American Thoracic Society (ATS) published a guideline that proposed the empirical treatment for patients at high risk of MRSA infection [18, 19]. The 2018 Chinese guidelines for the diagnosis and treatment of adults with hospital-associated and ventilator-associated pneumonia [20], also recommend the use of glycopeptides (vancomycin, norvancomycin, teicoplanin) or linezolid for empiric anti-MRSA therapy in patients at risk of MRSA infection. It is well known that empiric treatment is not the most beneficial for patients. Inappropriate antimicrobial use, especially treatment with unnecessarily broad agents, increases the risk of antimicrobial resistance, adverse medical events, and increases healthcare costs [21–24]. The IDSA-ATS guideline advocates stopping anti-MRSA therapy as soon as negative MRSA test results are available. However, traditional bacterial culture and susceptibility testing methods may take 2–3 days to deliver results. The alternative approach suggested in the guideline is to use PCR-based testing on nasal swab specimens, which enables quick and accurate results in as little as one hour. Although routine testing for bacterial pneumonia still uses culture methods of sputum or bronchoscopy specimens, there are many challenges to pneumonia diagnostics and in most cases we do not identify a causative pathogen. The use of MRSA PCR using nasal swab samples enables short turnaround time and non-invasive specimen collection. When the pathogen will remain unknown, it is especially useful it is to rule out MRSA. Previous studies showed that MRSA nasal screening assays demonstrate exceptional negative predictive efficacy exceeding 95% (NPV > 95%) in ruling out MRSA-associated pulmonary infections [25–28]. The negative predictive value for MRSA is very high allowing discontinuation of anti-MRSA therapy [29].

Data from China using this PCR-based approach to guide anti-MRSA therapy are not available. Thus, we conducted a study to determine whether nasal swab MRSA PCR screening can be used as a tool to support antimicrobial stewardship and whether patients can benefit from optimized antimicrobial stewardship.

Materials and methods

From August 2021 to November 2022, we conducted a prospective study of the potential impact of rapid PCR testing for MRSA on antimicrobial therapy for pneumonia in a comprehensive teaching hospital. The patients in the study population were mainly adults diagnosed with pneumonia (including community-acquired pneumonia and hospital-associated pneumonia), and the initiation of empirical anti-MRSA treatment (i.e., vancomycin, linezolid or teicoplanin) was not more than 24 h post admission. We excluded patients with nasal congestion, severe epistaxis/burns/ulcers/fractures or open wounds in the nasal cavity, patients undergoing intranasal mupirocin decolonization, agranulocytosis, and patients undergoing bone marrow transplantation.

Prospective study protocol

This study has been approved by the Medical Ethics Committee of Xiangya Hospital of Central South University (no.202012194). Prior to the collection of samples, each patient signed an informed consent form (signed by the family member if the patient was unconscious). Information was collected from the hospital’s electronic medical system, where all authors can ensure the confidentiality of patient data. The study was conducted strictly according to the declaration of Helsinki.

All enrolled patients were alternately included in the notification group (NG) or the control group (CG) according to the time sequence of the beginning of empirical anti- MRSA treatment. We collected nasal swabs from each study patient for the Cepheid Xpert SA Nasal Complete Test (Sunnyvale, CA, USA) according to the manufacturer’s instructions. The detection method was real-time Polymerase Chain Reaction (hereinafter referred to as PCR) for qualitative detection of proprietary sequences for the staphylococcal protein A (spa) gene, the gene for methicillin resistance (mecA), and the staphylococcal cassette chromosome mec (SCCmec) inserted into the SA chromosomal attB site. Sputum and/or bronchoalveolar lavage fluid (BALF) specimens were routinely collected for MRSA culture using standard of care methods when feasible. Samples were tested within 24 h of the receipt of anti MRSA antibiotics. The results of nasal swab samples in the NG were reported to the attending physicians via paper-based reports within 36 h, while results for the CG remained neither actively notified nor accessible through any platform. Notably, results from both groups were excluded from electronic medical record systems to eliminate incidental discovery possibilities. This design ensured that healthcare providers in CG had no access to MRSA nasal screening results throughout the study period, whereas NG clinicians received exclusive paper notifications. The diagnosis and treatment pathways for the CG and NG are following the recommendations of the ATS/IDSA guidelines for diagnosis and treatment of adult pneumonia [18, 19].

Clinical data collection

Data collected included culture results of respiratory samples, PCR results of nasal swabs and respiratory samples, duration of anti-MRSA treatment (primary endpoint), defined as the time from initiation to discontinuation of MRSA-targeted antibiotics (vancomycin, linezolid, or teicoplanin), and length of hospitalization. Hospitalization expenses and antibacterial drug expenses were also calculated. Other outcome measures included any adverse events related to the use of antimicrobials. The study end point was either the patient’s death, improvement and discharge, or the date of withdrawal from the study. Although detailed preadmission histories (e.g., prior antibiotic exposure, MRSA colonization history) were not systematically collected due to the emergency setting of pneumonia admissions, all enrolled patients met the guidelines’ criteria for empirical anti-MRSA therapy initiation [18, 19]. This decision was made by attending physicians based on comprehensive risk assessment, including but not limited to: severe pneumonia (e.g., requiring ICU admission, mechanical ventilation), failure of initial antibiotic therapy, or local epidemiological factors (e.g., high MRSA prevalence in the region).

Statistical analysis

Normally, distributed continuous variables were expressed as mean ± standard deviation (SD) and compared using Student’s t-test and non-normally distributed continuous variables were expressed as median (inter-quartile range [IQR]) and were compared using the Wilcoxon Sum Rank test. Categorical variables were expressed as count and percentage, which were compared using a chi-squared or Fisher’s exact test. Logistic regression (backward LR) methods (univariate, multivariate) were used to determine the Grouping and other clinical characteristics on time for anti-MRSA treatment. Odds ratios (ORs) and their corresponding 95% confidence interval (CI) were calculated. Subgroup analyses of ICU patients were conducted post-hoc to explore the intervention’s robustness in critically ill populations. The statistical analyses mentioned above were performed using the SPSS statistics 25.0. Significance level P = 0.05 was considered statistically significant among the relevant analyses.

Results

Baseline characteristics of patients

We enrolled 307 adult patients who were treated with vancomycin, linezolid, or teicoplanin for presumed pneumonia. Seven patients were excluded from final analysis (Fig. 1).

Fig. 1.

Flow chart of patients entering this cohort

The clinical characteristics and comparison of 300 patients in the NG and the CG are shown in Table 1.

Table 1.

Baseline clinical characteristics of the study cohorts. (n = 150 per group; total N = 300)

		Notification group(n = 150)	Control group(n = 150)	P value
Male (%)		104 (69.33)	110 (73.33)	0.370
Type of pneumonia (%)	CAP	116 (77.33)	105 (70.00)	0.149
	HAP	34 (22.67)	45 (30.00)	0.190
Age (± S)		62.21 ± 16.57	59.61 ± 15.31	0.154
Diabetes (%)		22 (14.67)	33 (22.00)	0.101
Hypertension (%)		63 (42.00)	67 (44.67)	0.641
Heart failure (%)		31 (20.66)	22 (14.67)	0.173
Tumor (%)		14 (9.33)	18 (12.00)	0.454
Cerebrovascular diseases (%)		61 (40.67)	49 (32.67)	0.151
Obstructive/Restrictive lung disease (%)		55 (36.67)	48 (32.00)	0.395
Liver function damage (%)		10 (3.33)	8 (5.33)	0.627
Renal function damage (%)		15 (10.00)	18 (12.00)	0.580
Tuberculosis (%)		3 (2.00)	1 (0.67)	0.311
Connective tissue disease (%)		8 (5.33)	10 (6.67)	0.808
Deep vein catheterization (%)		84 (56.00)	79 (52.67)	0.562
Arterial catheterization (%)		92 (61.33)	87 (58.00)	0.556
Nasogastric tube (%)		89 (59.33)	99 (66.0)	0.233
Hemofiltration (%)		13 (8.67)	13 (8.67)	1.000
Intubation of the trachea (%)		61 (40.67)	70 (46.67)	0.295
Tracheostomy (%)		30 (20.00)	25 (16.67)	0.456
Surgery or trauma in one month (%)		30 (30.00)	32 (21.33)	0.776
Immunomodulators (%)		33 (22.00)	39 (26.00)	0.417
Chemotherapy (%)		3 (2.00)	0 (0.00)	0.247
Combined with beta-lactam antibiotics		28 (18.67)	25 (16.67)	0.650
WBC (x109/L)[M (P25, P75)]		12.80 (9.05, 16.70)	12.35 (8.00, 15.05)	0.616
NE % [M (P25, P75)]		81.64 (75.60, 90.75)	81.76 (76.42, 90.15)	0.415
ALT (U/L)[M (P25, P75)]		40.32 (6.23, 15.45)	72.75 (17.40, 61.20)	0.456
SCR (umol/L)[M (P25, P75)]		165.14 (53.85, 210.45)	115.54 (55.85, 124.83)	0.714
CRP [M (P25, P75)]		106.47 (43.08, 161.35)	107.49 (41.25, 160.00)	0.790
PCT (ng/mL) [M (P25, P75)]		3.88 (0.21, 2.53)	3.04 (0.15, 2.20)	0.737

CAP, Community acquired pneumonia; HAP, Hospital acquired pneumonia; WBC, White blood cell; NE %, Percentage of neutrophils; ALT, Alanine aminotransferase; SCR, Serum creatinine; CRP, C-reactive protein; PCT, Procalcitonin; IQR, Interquartile range

The clinical characteristics and comparison of 300 patients in the NG and CG are shown in Table 1. Both groups demonstrated comparable baseline profiles, with no statistically significant differences in comorbidities or pre-treatment parameters.The pneumonia subtypes distribution showed 116 (77.3%) community-acquired pneumonia (CAP) cases in NG versus 105 (70.0%) in CG (P = 0.149), while hospital-acquired pneumonia (HAP) occurred in 34 (22.7%) and 45 (30.0%) patients respectively (P = 0.190). Of particular clinical relevance, respiratory culture analysis revealed MRSA detection in 16 patients (5.33% overall prevalence), with detailed pathogen distribution patterns illustrated in Fig. 2.

Fig. 2.

Detection rate of pathogenic bacteria in respiratory tract samples of patients treated with anti-MRSA in the whole hospital

Analysis of the differences between the NG and CG

Patient clinical characteristics were similar in the two groups. The selection of anti-MRSA drugs in the two groups is shown in Supplementary Fig. 1, linezolid was utilized in 215 cases (71.67%), vancomycin in 81 cases (27.00%), and teicoplanin in 4 cases (1.33%), demonstrating significant preferential selection of oxazolidinone-class antimicrobial agents in the therapeutic regimen.

There is a significant difference in the duration of anti-MRSA treatment between the two groups (Fig. 3). The average duration of vancomycin, linezolid and teicoplanin use in the NG was 5.66 ± 3.75 days, which was significantly shorter than 7.87 ± 4.84 days in the CG (P < 0.001). There are differences between NG and CG in renal injury (0% vs. 4.67%; P = 0.015) and liver injury (1.33% vs. 8%; P = 0.006) with more adverse events in the CG. The in-hospital mortality in the NG did not increase compare with CG (12.67% vs. 16.67%, P = 0.327). The total cost of hospitalization (including all medical expenditures: PCR testing, diagnostics, medications, bed fees, and ancillary services) was $14652.57 ($7772.53, $28442.47) in the CG and $10772.14 ($5970.76, $21934.47) in the NG, but this was not statistically significant. However, the antibiotic cost in NG was less than CG ($621.78 ($323.15, $1309.40) vs. $881.70 ($416.93, $2324.73), P = 0.013). Other outcome measures are shown in Table 2.

Fig. 3.

Time of empirical anti MRSA treatment in NG and CG. A. is a broken line graph showing the number of patients who discontinued anti-MRSA treatment over time. B. is a violin diagram showing the distribution of the time to stop anti-MRSA treatment in the two groups. NG, notification group. CG, control group. ****, P < 0.001

Table 2.

Clinical outcomes between notification and control groups

	Notification group (n = 150)	Control group (n = 150)	P value
MRSA nasal colonization (%)	13 (8.66)	14 (9.33)	0.84
Duration of anti-MRSA (days) (±S)	5.66 ± 3.75	7.87 ± 4.84	<0.001
Hospitalization costs ($)[M (P25, P75)]	10772.14 (5970.76, 21934.47)	14652.57 (7772.53,28,442.47)	0.061
Antibiotic costs ($)[M (P25, P75)]	621.78 (323.15, 1309.40)	881.70 (416.93, 2324.73)	0.013
Hospital length of stay (days) (±S)	18.13 ± 12.42	22.63 ± 19.07	0.179
ICU length of stay (days) (±S)	8.88 ± 10.29	10.50 ± 11.15	0.270
In-hospital mortality (%)	19(12.67)	25(16.67)	0.327
Thrombocytopenia (%)	1 (0.67)	5 (3.33)	0.214
New bacteria (%)	22 (14.67)	34 (22.67)	0.075
Enter ICU (%)	2 (1.33)	4 (2.67)	0.684
Antibiotic associated diarrhea (%)	3 (2.00)	8 (5.33)	0.281
Renal function damage (%)	0 (0.00)	7 (4.67)	0.015
Liver function damage (%)	2 (1.33)	12 (8.00)	0.006

Multivariate analysis of stopping anti-MRSA treatment, which was adjusted for potential confounders including suggested by the results of univariate analysis, showed that the NG was an independent influencing factor for patients to stop anti-MRSA treatment within 4 days (OR = 4.50, 95% CI 2.572,7.872, p < 0.001) (Table 3). Excluding the 27 patients with positive MRSA nasal screening, 84/273 (30.77%) had empirical anti-MRSA treatment discontinued within 4 days. The group of patients who continued antibiotics had longer hospital stays, hospital costs, and duration of antibiotic use compared with those patients who downgraded or discontinued antibiotics within 4 days (Table 4).

Table 3.

Grouping and other clinical characteristics on time for anti-MRSA treatment in recipients, univariable and multivariable analyses

Variables	Level	Time for anti-MRSA treatment		P value (Fisher’s exact test)	Univariable analyses			Multivariable analyses
		<4days	≥ 4days		P value	OR	95%CI	P value	OR	95%CI
Sex	Male	77 (39.29%)	119 (60.71%)	1	0.961	1.014	0.591,1.740
	Female	30 (38.96%)	47 (61.04%)
Age	<65	48 (30.00%)	112 (70%)	0.801	0.786	1.071	0.615,1.764
	≥ 65	40 (28.57%)	100 (71.43%)
Group	NG	66 (44.00%)	84 (56.00%)	<0.001	<0.001	4.571	2.623,7.967	<0.001	4.5	2.572,7.872
	CG	22 (14.67%)	128 (85.33%)
ICU	Yes	51 (29.48%)	122 (70.52%)	1	0.948	1.017	0.615,1.682
	No	37 (29.13%)	90 (70.87%)
Diabetes	Yes	15 (27.27%)	40 (72.73%)	0.746	0.71	0.884	0.460,1.698
	No	73 (29.80%)	172 (70.20%)
Hypertension	Yes	36 (27.69%)	94 (72.31%)	0.611	0.585	0.869	0.525,1.439
	No	52 (30.59%)	118 (69.41%)
Heart failure	Yes	16 (30.19%)	37 (69.81%)	0.869	0.88	1.051	0.550,2.008
	No	72 (29.15%)	175 (70.85%)
Tumor	Yes	7 (21.88%)	25 (78.12%)	0.413	0.33	0.646	0.269,1.555
	No	81 (30.22%)	187 (69.78%)
Cerebrovascular diseases	Yes	34 (30.91%)	76 (69.09%)	0.694	0.648	1.127	0.675,1.881
	No	54 (28.42%)	136 (71.58%)
Obstructive/ Restrictive lung disease	Yes	29 (28.16%)	74 (71.84%)	0.79	0.746	0.917	0.541,1.552
	No	59 (29.95%)	138 (30.05%)
Liver function impairment	Yes	6 (33.33%)	12 (76.67%)	0.79	0.701	1.22	0.443,3.359
	No	82 (29.08%)	200 (70.92%)
Renal impairment	Yes	9 (27.27%)	24 (72.73%)	0.842	0.783	0.892	0.397,2.006
	No	79 (29.59%)	188 (70.41%)
Tuberculosis	Yes	1 (25.00%)	3 (75.00%)	1	0.848	0.801	0.082,7.805
	No	87 (29.39%)	209 (70.61%)
Connective tissue disease	Yes	6 (33.33%)	12 (76.67%)	0.79	0.701	1.22	0.443,3.359
	No	82 (29.08%)	200 (70.92%)
Tracheal cannula	Yes	35 (29.92%)	82 (70.08%)	0.897	0.86	1.047	0.630,1.741
	No	53 (28.96%)	130 (71.04%)
Arterial catheterization	Yes	51 (28.49%)	128 (71.51%)	0.7	0.697	0.905	0.546,1.499
	No	37 (30.58%)	84 (69.42%)
Deep vein catheterization	Yes	46 (28.22%)	117 (71.78%)	0.703	0.644	0.889	0.540,1.464
	No	42 (30.66%)	95 (69.34%)
Nasogastric tube	Yes	46 (24.47%)	142 (75.53%)	0.019	0.017	0.54	0.325,0.896	0.035	0.562	0.329,0.960
	No	42 (37.50%)	70 (62.50%)
Surgery or trauma in one month	Yes	15 (24.19%)	47 (75.81%)	0.351	0.32	0.721	0.379,1.372
	No	73 (30.67%)	165 (69.33%)
Immunomodulators	Yes	18 (25.00%)	54 (75.00%)	0.377	0.355	0.752	0.412,1.375
	No	70 (30.70%)	158 (69.30%)
Chemotherapy	Yes	0 (0.00%)	3 (100.00%)	0.558	0.254	0.177	0.009,3.467
	No	88 (44.67%)	109 (56.33%)

Table 4.

Patients with negative nasal-swab PCR test results analyzed according to duration of anti-MRSA

	<4 days(n = 84)	≥ 4 days (n = 189)	P Value
Hospital length of stay (±S)	17.61 ± 16.15	21.39 ± 15.95	0.006
ICU length of stay (±S)	8.31 ± 11.50	9.81 ± 9.69	0.070
Hospitalization costs [M (P25, P75)]	9783.16 (4579.92, 20707.49)	14645.09 (7314.64, 25287.11)	0.016
Antibiotic costs [M (P25, P75)]	491.23 (262.23, 1226.22)	867.11 (439.54, 2073.50)	0.002
In-hospital mortality (%)	9(6.00)	32 (21.33)	0.184
New bacteria (%)	11(7.33)	40 (26.67)	0.114
Renal function damage (%)	0(0.00)	5(3.33)	0.328
Liver function damage (%)	1(0.67)	12(8.00)	0.124
Thrombocytopenia (%)	1 (0.67)	4 (2.67)	1.000
Antibiotic associated diarrhea (%)	0(0.00)	11(7.33)	0.050
Enter ICU (%)	0(0.00)	6(4.00)	0.182

Discussion

In recent years, through effective measures for healthcare-associated infection prevention and control, the incidence of MRSA infection has decreased [2]. The current anti-MRSA treatment for pneumonia is still mainly empirical, which has led to an increasing number of patients being exposed to unnecessary antimicrobial agents in clinical practice.

The findings of our study demonstrated that the nasal swab-based PCR assay for methicillin-resistant Staphylococcus aureus (MRSA) exhibited a NPV of 99.64% (Supplementary Table 2), aligning with the predictive performance reported in prior clinical validation studies [25–27, 30]. Thus, PCR is an excellent method for ruling out MRSA pneumonia.

A previous prospective analysis of 45 patients by Paonessa et al. [31] suggested that physicians of patients with MRSA-negative BALF stop anti-MRSA treatment immediately. Duration was significantly shorter with vancomycin or linezolid and there were no significant adverse events compared to the control group. The above studies show that the rapid de-escalation of antibiotics guided by quick and accurate PCR results is effective and safe. However, The intervention’s greatest stewardship impact may reside in overcoming ‘clinical inertia’ - where negative PCR results provided objective justification for de-escalation in cases where clinicians otherwise maintained unnecessarily broad coverage. Future implementation studies should measure behavioral drivers of inappropriate empiric prescribing. Previous study have stopped empirical anti MRSA drugs immediately when MRSA screening was negative [32], which did not really reflect the degree of PCR detection of nasal swabs and the difference in prognosis. This prompted us to initiate this current study.

We collected a large number of samples from patients in a prospective trial. Initially, it was unclear whether patients would benefit from a reduction in this empiric use. However, we found that physicians in the NG were more willing to change antibiotics than the CG (44.52% vs. 14.67%, P<0.05). Although we only provided nasal swab results to treating physicians, some of them still chose to discontinue empiric treatment when the nasal swabs were negative (Fig. 3). Most doctors in the NG stopped anti-MRSA treatment within 4 days, while the time of stopping anti-MRSA treatment in the CG was significantly longer. The peak time for doctors in NG to stop anti- MRSA treatment was 3–4 days. This may be because doctors did not act immediately on the results of nasal swab screening. The patients in CG received empirical anti-MRSA treatment according to the published guidelines, since their doctors did not receive any information on MRSA screening results. Thus, drug withdrawal peak for the CG occurred on the sixth clinical day. Notably, the paper-based notification system used in this study may have contributed to this delay. While paper reports ensured controlled information dissemination per protocol, real-world implementation could be optimized through electronic medical record (EMR) alerts or pharmacist/infectious disease (ID) specialist interventions. Automated EMR alerts would provide instantaneous results to clinicians, potentially accelerating therapeutic de-escalation.Future studies should evaluate these multimodal approaches to maximize the impact of rapid diagnostics on antimicrobial stewardship. However, a small number of patients in the CG had therapy stopped on the third day. This may reflect the doctor’s response to the culture results (as opposed to the nasal screening results). In this regard, our study likely reflects what occurs in routine clinical practice. The results show that many clinicians are still conservative in the selection and discontinuation of antibiotics. At present, there are few published data on the effect of rapid MRSA test results on antibiotic choice by doctors in China.

We further investigated the reasons why doctors adjusted anti-MRSA treatment within the 4-day time frame. The results showed that being in the NG was an independent predictor affecting this change. This means that the major factor that influenced doctors to change antibiotic strategies was the negative MRSA nasal swab results. However, we also found that having an indwelling gastric tube was an independent risk factor for patients to receive more than 4 days of anti-MRSA treatment. Previous research found that the presence of a nasogastric tube was an independent risk factor for acquiring MRSA during the ICU stay when data for MRSA carriers and patients without carriage of MRSA were compared [33, 34]. This may be the reason why doctors chose to continue anti-MRSA treatment in this group of patients. In contrast to previous studies, this research showed that empiric treatment duration was longer. We believe that this can be attributed, in part, to the low detection rate of respiratory samples, along with the influence of changes in the patient’s condition on physicians’ prescribing practices. Nevertheless, the significant differences observed between the two groups underscore the effectiveness of the implemented strategy. To enhance the optimization of antimicrobial drug management at an earlier stage, the current conservative prescribing practices may be improved by enhancing physicians’ understanding of nasal screening methods and through targeted training.

We specifically analyzed the ICU subgroup (Supplementary Table 1). Among these critically ill patients, those who discontinued anti-MRSA therapy within 4 days demonstrated significantly lower acquisition of new pathogens compared to the delayed discontinuation group (13 cases [15.85%] vs. 27 cases [30%], P = 0.028). Furthermore, in the MRSA nasal swab-negative cohort requiring antibiotic de-escalation, early discontinuation within 4 days (n = 82) was associated with complete absence of antibiotic-associated diarrhea (0/82, 0.00%), contrasting with 11 cases (7.33%) in the delayed discontinuation group (n = 150) (P = 0.050). These novel findings regarding pathogen acquisition patterns and diarrheal complications in specific ICU populations have not been previously documented. Importantly, mortality rates remained comparable between the early and delayed discontinuation groups (8.54% vs. 9.33%, P = 0.842), confirming the safety profile of rigorous antibiotic stewardship protocols.

Mortality, length of hospitalization, and economic costs are all important issues in any intervention study [5, 35]. In our study, the cost of using antibiotics in the NG was significantly lower than that in the CG. In ICU inpatients, the average cost of antibiotics and hospitalization expenses in the NG were significantly lower than those in the CG (Supplementary Table 1). Statistical analysis of the patients in the hospital found that the cost of antibacterial drugs in the NG was significantly less than that in the CG, but there was no significant statistical difference in the total hospitalization cost. Infection rates with antimicrobial-resistant bacteria in intensive care unit (ICU) patients are higher than that in patients on ordinary wards, and the risk of infection transmission it is also higher in ICU settings [36].

This study still has limitations. The use of linezolid as the primary empiric medication choice is worth mentioning, as this isn’t standard practice in other eographical areas and can affect the expected costs and side-effect profile. The current research was carried out is a single medical center, which is a comprehensive tertiary teaching hospital. The prevalence of MRSA, and thus the efficacy of the MRSA screening in different types of hospitals, may vary. Although the sample size of this study was larger than that of other prospective studies, it may be subject to more confounding factors. We attempted to control for these factors in our data analysis.

In conclusion, the nasal swab-based PCR screening method could help reduce unnecessary anti-MRSA treatment more quickly. Early management of antimicrobials to reduce the experience of anti-MRSA drug treatment reduce the side effects of antibacterial drugs, and also help reduce the economic burden of antibiotic treatment.

Supplementary Information

Below is the link to the electronic supplementary material.

Author contributions

Siyao Chen: Conceptualization, data curation, formal analysis, investigation, methodology, writing-original draft. Xinghui Gao, Fred Tenover: Resources, manuscript writing editing. Ming Zheng, Letao Chen: Statistical analysis. Yuanyuan Xiao, Caixia Tan, Juan Zhou, Ting Liu, Sisi Zhang, Yiran Hu, Yang Liu: investigation. Chunhui Li, Anhua Wu, Yi-Wei Tang: Conceptualization, project administration, supervision, manuscript review and editing.

Data availability

No datasets were generated or analysed during the current study.

Declarations

Competing interests

The authors declare no competing interests.