Provider Perceptions of Antibiotic Initiation Strategies for Hospital-Acquired Pneumonia

Abstract

Background:

The practice of rapidly initiating antibiotic therapy for patients with suspected infection has recently been criticized yet remains commonplace. Provider comfort level has been an understudied aspect of this practice.

Hypothesis:

We hypothesized that there would be no significant differences in provider comfort level between the two treatment groups.

Methods:

We prospectively surveyed critical care intensivists who provided care for patients enrolled in the Trial of Antibiotic Restraint in Presumed Pneumonia (TARPP), which was a multicenter cluster-randomized crossover trial that evaluated an immediate antibiotic initiation protocol compared with a protocol of specimen-initiated antibiotic initiation in ventilated patients with suspected new-onset pneumonia. At the end of each enrollment arm, physicians at each center were surveyed regarding their overall comfort level with the recently completed treatment arm, and perception of adherence. Both a paired and unpaired analysis was performed.

Results:

We collected 51 survey responses from 31 unique participants. Providers perceived a higher rate of adherence to the immediate initiation arm than the specimen-initiated arm (Always Adherent: 37.5% vs. 11.1%; p = 0.045). Providers were less comfortable waiting for objective evidence of infection in the specimen-initiated arm than with starting antibiotic agents immediately (Very Comfortable: 83.3% vs. 40.7%; p = 0.004). For the smaller paired analysis, there was no longer a difference in comfort level.

Conclusions:

There may be differences in provider comfort levels and perceptions of adherence when considering two different antibiotic initiation strategies for suspected pneumonia in ventilated patients. These findings should be considered when planning future studies.

Intensive care unit (ICU)-acquired pneumonia is a widely prevalent problem that is associated with increased risk of in-hospital mortality.¹ The diagnosis of pneumonia can be difficult to identify in the ICU population given the broad differential to consider in trauma and surgical patients with leukocytosis or increasing oxygen requirements.^2,3 The overuse of antibiotic agents can result in costly bacterial resistance, adverse drug effects, and opportunistic infections, which has triggered support for increased antibiotic stewardship,^4,5 Therein lies the balance to promptly treat suspected pneumonia while limiting unnecessary antimicrobial use.

Given this diagnostic and treatment dilemma, multiple societies have offered clinical and culture-based guidelines for antibiotic initiation.^6,7 The Surviving Sepsis Campaign (SSC) has softened its stance regarding rapid initiation of antibiotic agents in its most recent guidelines for patients with possible sepsis without shock, allowing a time-limited course for investigation.^8,9 Although efforts have been made to better define which patients would and would not benefit from early initiation of antibiotic agents, provider perceptions of antibiotic use are understudied and underreported in the literature. Multiple studies have expressed concern with antibiotic overuse without concomitant evidence for decreased mortality, but none have asked providers specifically their comfort in withholding antibiotics.^10–13 Our study aims to address this gap by describing both provider adherence and comfort level with two protocols for antibiotic initiation in an ICU setting.

Methods

The Trial of Antibiotic Restraint in Presumed Pneumonia (TARPP) was a prospective cluster-randomized crossover study of antibiotic initiation strategies in intubated patients with suspected pneumonia.¹⁴ Each participating site underwent independent full Institutional Review Board (IRB) review and obtained approval at their respective institutions before the study began; ethics committee review was not required. Each site participated in two antibiotic initiation protocols: immediate and specimen-initiated. In the immediate protocol, patients suspected of having hospital-acquired pneumonia had their antibiotic agents started immediately after collection of a culture specimen regardless of their clinical status. In the specimen-initiated protocol, patients who were not on vasopressors had antibiotic agents withheld until there was objective evidence of an infection (usually in the form of a gram stain). Patients on vasopressors were started on antibiotics immediately regardless of protocol. Full results of the study are published elsewhere.¹⁴

Two rounds of surveys were distributed electronically to participating intensivists at each institution. The list of intensivists was provided by each of the primary site investigators. The first round of surveys was distributed after completion of the first arm of the study and during the washout period. All surveys distributed during this first period were collected prior to the start of the second arm of the study. The second round of surveys was sent after completion of the study but prior to completion of data analysis. Each provider received the same survey, but the survey questions were conditionally tailored to the protocol that each group had just finished based on provider selection of the site where they worked. For example, during the first round of the survey, participants that selected that they worked at sites A and B were asked about the immediate protocol while sites C and D were surveyed about the specimen-initiated protocol. This order was switched during the second round.

Respondents were asked to rank the level of perceived protocol adherence to the study as well as their overall comfort level on a five-point Likert scale. Respondents surveyed after completion of the specimen-initiated protocol were also asked to select from a list of clinical findings that may lead them to start antibiotic agents without waiting for culture results. A copy of the survey is included in the Supplementary Appendix. Please note that the surveys use the terms “aggressive” to refer to the immediate arm and “conservative” to refer to the specimen-initiated arm. These terms were updated for the final article.

Statistical analysis of survey responses was performed. Descriptive statistics were used. Given the small sample size, and because not every respondent answered both surveys, variables were analyzed as using both a paired and unpaired analysis. The paired analysis was conducted on the smaller subset of physicians that answered both surveys. Both χ² and Fisher exact test were used to compare categorical variables. Comparisons of continuous variables were done using Student t-test for the unpaired analysis. The Stuart Maxwell test and paired t-test were used for the paired analysis. All statistical analysis was conducted using SAS 9.4 (SAS Institute, Cary, NC) and R (version 4.3.1; R Foundation for Statistical Computing, Vienna, Austria).

Results

A total of 68 surveys were sent to 36 unique providers over the two survey periods. Thirty-one unique providers (86.1%) responded to at least one of the surveys whereas 20 providers answered both surveys (55.6%). The overall response rate was 75% for both survey periods. Overall respondent characteristics are listed in Table 1. Most respondents were male and had been in practice for 10 years or less. Most respondents reported that they split their time evenly between several clinical areas including critical care. There were no differences in respondent characteristics based on protocol (paired or unpaired analysis).

Table 1.

Respondent Provider Characteristics

	Unique responders		Immediate		Specimen initiated
	31		24		27		p ^a
Institution							0.98
A	8	25.8%	6	25.0%	7	25.9%
B	5	16.1%	3	12.5%	5	18.5%
C	5	16.1%	4	16.7%	4	14.8%
D	13	41.9%	11	45.8%	11	40.7%
Gender: female	6	19.4%	3	12.5%	5	18.5%	0.71
Practice years							0.88
0–5	12	38.7%	8	33.3%	10	37.0%
6–10	8	25.8%	8	33.3%	6	22.2%
11–15	6	19.4%	3	12.5%	6	22.2%
16–20	3	9.7%	3	12.5%	3	11.1%
>20	2	6.5%	2	8.3%	2	7.4%
Primary clinical focus^b							0.95
General surgery	7	22.6%	6	25.0%	5	18.5%
Trauma	2	6.5%	2	8.3%	2	7.4%
Critical care	0	0.0%	0	0.0%	0	0.0%
Emergency general surgery	1	3.2%	0	0.0%	1	3.7%
Other	0	0.0%	0	0.0%	0	0.0%
Split evenly over several areas	22	71.0%	16	66.7%	19	70.4%
Board specialty
General surgery	30	96.8%	24	100.0%	26	96.3%	1.0
Critical care	30	96.8%	23	95.8%	26	96.3%	1.0

No statistical differences when only paired samples analyzed.

Represents comparisons between immediate and specimen initiated groups only.

Percentages in unique responders column equal >100% because one respondent changed answer between first and second survey.

Provider perceptions of study adherence and comfort levels are listed in Table 2. Respondents perceived a higher rate of adherence for the immediate protocol than the specimen-initiated protocol. For smaller subset of paired survey responses, the mean perception of adherence was not statistically different when analyzed categorically but mean perception of adherence remained lower in the specimen-initiated arm (4.4 ± 0.50 vs. 4.1 ± 0.39; p = 0.04). Similarly, respondents were more comfortable with the immediate protocol than the specimen-initiated protocol when all survey responses were included. In the smaller paired sample, there was no difference in comfort level between the two groups. For respondents who had just completed the specimen-initiated protocol, worsening Pao₂/Fio₂ ratio, increasing white blood cell count, and findings on bronchoscopy were the most commonly selected causes of starting antibiotic agents without waiting for culture results (Table 3). Respondent comments regarding their comfort participating in either the immediate or specimen-initiated protocols are listed in Table 4.

Table 2.

Respondent Perception of Adherence and Comfort Level

	Immediate		Specimen Initiated
	24		27		p
Perception of adherence					0.045^a
1—Never	0	0.0%	0	0.0%
2—Almost Never	0	0.0%	0	0.0%
3—About half the time	0	0.0%	1	3.7%
4—Almost always	15	62.5%	23	85.2%
5—Always	9	37.5%	3	11.1%
Mean perception of adherence	4.38	±0.49	4.07	±0.38	0.02

Comfort level					0.02^a
1—Very uncomfortable	0	0.0%	1	3.7%
2—Somewhat uncomfortable	1	4.2%	5	18.5%
3—Neutral	2	8.3%	3	11.1%
4—Somewhat comfortable	1	4.2%	7	25.9%
5—Very comfortable	20	83.3%	11	40.7%
Mean Comfort Level	4.67	±0.82	3.81	±1.27	0.006^a

Not statistically significant when smaller subset of paired surveys are analyzed.

Table 3.

Provider Indications for Initiation of Antibiotics in Normotensive Patients

	Specimen initiated
	27
Worsening Pao₂/Fio² ratio	17	63.0%
Increasing WBC	8	29.6%
Findings on bronchoscopy	11	40.7%
Lactic acidosis (without hypotension)	5	18.5%
Overall burden of comorbidities	3	11.1%
New or worsening AKI	3	11.1%
Patient age	2	7.4%
None of the above	3	11.1%

WBC = white blood cell count; AKI = acute kidney injury.

Table 4.

Respondent Comments by Protocol

Immediate protocol comments	Specimen initiated protocol comments
“Equipoise”	“I was fairly certain waiting would be safe from experience”
“Fairly clear cut for instances encountered”	“I trust ____________.”
“I'm not sure that patient population needs antibiotics”	“Minimal risk when excluding septic shock”
“It is the standard practice”	“More comfortable with early antibiotics”
“Pretty standard practice”	“I've had so much experience with patients who might be infected but are not”
“Traditional practice here”	“I feel that some of those folks didn't need antibiotics and it was good to wait and see”
“I felt comfortable knowing patient was on treatment in case they decompensated overnight”	“Felt I had a good understanding of my patient and would intervene if needed to provide best care of my patient”
“It's always easier to start ABX and stop them then to wish I had started them…”	“My comfort was directly related to the patient's hemodynamic stability”
“Our whole team was well informed, and we made a conscious effort to adhere to the protocol”	“My only discomfort was around patients who seemed to clinically deteriorate while we were awaiting results”
“Reasonable considering the information and the suspicion for pneumonia”	“Unless patient was rapidly declining, I felt that I had time to get data”
“This is our general practice- to start pts if we have a high level of concern. Remember as surgeons, we are occasionally wrong but never in doubt”	“That's my typical practice pattern, take clinical clues and add evidence to confirm then treat. the exceptions would be in septic patients with high probability despite no objective evidence”
	“The study had appropriate physiologic triggers to be able to start antibiotics immediately in the few patients who needed that. Otherwise, I felt very comfortable waiting for objective evidence”
	“Unless I feel that patients are dying in front of me with an overwhelming infection, I feel fine waiting until I know that I have to treat. Usually there is a ramp-up of sorts, which is hopefully the time that the cultures are pending”

ABX = antibiotic agents.

One hundred percent of respondents stated that they would participate in a similar study in the future. Comments regarding the respondents who felt it was important to participate in similar studies are listed in Table 5.

Table 5.

Respondent Comments Participating in Similar Studies

“Anything to advance our care”	“It is helping to answer an important question”
“Further evidence-based approach/protocol”	“Made sense and saw seemed safe”
“Good research and answering a good question”	“We need answers”
“Great topic to study”	“Well-designed study Easy to participate”
“I suspect it will yield valuable information”	“Relentless pursuit of improvement”
“I think it's important”	“Reasonable study to change our practice model”
“Interested in the answer”	“Because I trust and value Dr._________ opinions”
“Low risk, important outcomes”	“Evidence based patient care”
“This is important work”	“Enjoy research and feel clinically based research is helpful to developing guidance in care”
“Important question with implications for sepsis care as well as antibiotic stewardship”	“Enjoy being in multi-institutional study and contributing”
“It was easy and not cumbersome and was not perceived to negatively impact patient care”	“Pushing the limits of knowledge and destroying anachronistic thought”
“I like finding the right answers to clinic questions. Also, very well-run study”	“Felt this was well designed and will answer important questions to provide EVIDENCE for our 'gray hair' behavior”
“Very beneficial and excellent effort to minimize unnecessary initiation of antibiotics - increases stewardship for safe care practices”	“I think there is equipoise in this area. In additionally, the study design allows for us to go off protocol if I felt that was necessary for patient care”
“Very important to establish high level evidence in correct antibiotic application to avoid use solely based on “anticipation” of infection when not warranted. Opportunity to be part of increasing awareness and antimicrobial stewardship”	“While my comfort with doing this is one thing, I would feel even more comfortable if I knew I was doing the right thing. This is a very common issue in the STICU - we need more data to help guide us”
“There are still unsolved questions with regard to antibiotic management in patients with sepsis, there's best clinical practice that is also affected by threat of not initiating sepsis management empirically but there are several grey areas in between”

Discussion

In this prospective survey study of physicians participating in a randomized trial of antibiotic initiation strategies, we observed that provider perceptions of adherence and comfort level may differ and may not necessarily correlate with physician behavior during the trial.

In TARPP, adherence rates between the two protocols were not statistically different (74.2% in immediate vs. 82.8% in specimen-initiated; p = 0.15). Most of the non-compliance in the study (72.5%) was due to failure to stop antibiotic agents once cultures were negative, not due to off-protocol initiation.¹⁴ In our full survey cohort, however, perceived adherence rates were statistically different between the two protocols with providers believing that adherence was higher in the immediate protocol. Mean perception of adherence remained statistically lower in the specimen-initiated arm when only paired surveys are considered. The difference in actual versus perceived adherence suggests a persistent bias toward immediate initiation protocols.

The Severe Sepsis and Septic Shock Management Bundle (SEP-1) from The Center for Medicare and Medicaid Services (CMS) may promote this bias through tying hospital reimbursement to compliance with rapid initiation of antibiotics. When providers in our survey were asked for comments regarding the immediate protocol, it was reported multiple times that it was in concordance with standard practice at that institution. A large systematic review of qualitative studies of physician antibiotic prescribing practices identified multiple health system-related extrinsic factors that influence prescribing practices including time-pressures, healthcare organizational structures, and guidelines.¹⁵ Nicks et al.¹⁰ found that more than half of the respondents in their survey study reported prescribing antibiotic agents to patients they did not believe had pneumonia in an effort to comply with the CMS guidelines. Many physicians report feeling anxiety about missing an infection, which drives antibiotic overuse even in cases in which infection is uncertain.¹⁶

In the full unpaired survey cohort, we also observed a difference in the reported comfort level of providers between the two protocols. Providers were more comfortable with the immediate protocol compared with waiting for objective evidence in the specimen-initiated protocol. Providers commented that their comfort level was directly tied to patient stability. These observed differences were not found in the smaller paired analysis. A recent survey by Taylor et al.¹⁷ observed that physicians had higher thresholds of for initiating antibiotic agents when the patient's severity of illness is low. It is important to note that TARPP was designed to initiate antibiotic agents immediately for any patient requiring vasopressor support regardless of study protocol. When excluding the patients in septic shock, providers reported feeling comfortable waiting to initiate antibiotic agents.

These reported perceptions seem to align with the changes made in the SSC 2021 guidelines, which allow for up to three hours of additional workup prior to initiation of antibiotic agents for those patients not in septic shock.⁸ Complacency and fear of worsening clinical status may also play a large part in explaining the observed differences in provider comfort level in our study.¹⁵ Bisarya et al.¹⁸ observed an association between the timing of antibiotic agents and progression to septic shock, although the timing of antibiotic agents was not associated with mortality in their study.

When asked what would prompt the provider to deviate from the specimen-initiated protocol and start antibiotics before objective evidence of infection, the highest-ranked indications were worsening Pao₂/Fio₂ ratio, findings on bronchoscopy, and increasing white blood cell count. Clinical findings, changes in ventilator settings, and provider predictions have been found to correlate poorly with pneumonia.^3,19–21 Klein Klouwenberg et al.²² demonstrated that 43% of patients with an admission diagnosis of sepsis were found to have been unlikely to have an infection upon retrospection with 13% having an infection likelihood of none and 30% with a likelihood of only possible. In their study, patients with pneumonia had the lowest likelihood of having a definite infection compared with the remainder of the cohort (16% vs. 33%; p < 0.001).²² Our survey findings demonstrate that the findings that clinicians focus upon may not correlate with a high likelihood of infection.

Our survey concluded with asking respondents why they believed participation in a study such as TARPP is important to the field of critical care. Overall, our respondents noted this is an area lacking evidence-based data to support a protocol for antibiotic restraint. Respondents commented on the importance of antibiotic stewardship to avoid overuse of antibiotics, which is not without risk. Lindsay et al.⁴ performed a systematic review and meta-analysis of antimicrobial stewardship programs in critical care patients that suggested the implementation of these programs did not increase patient mortality. Respondent comments were few enough that we have chosen to display them without classification or editing apart from removing a few names. The reader is free to make their own interpretation of the comments.

Our study is strengthened by obtaining prospective surveys of physicians participating in a clinical trial of antibiotic initiation. As the sites were cluster-randomized, the physician responses are similarly cluster-randomized. Limitations of this study include a small sample size in survey respondents and that we could not obtain responses from all physicians after participating in both arms. In particular, the paired analysis is of an even smaller subset of survey responses and so is underpowered to detect smaller potential differences. Because not every physician answered both surveys our decision to perform both unpaired and paired analysis with resulting differences in statistical results leads to some challenges in interpretation. Also, our survey questions were limited, and we did not collect more nuanced data from the participants. We also did not ask the surveyed physicians about the evidence that they used to inform their judgements. Last, we are unable to pair individual physician responses with individual patients within the study cohort and are unable to draw conclusions between individual physician perspectives and compliance or outcomes. Our findings are therefore inherently limited and are not generalizable to a broader cohort.

Conclusions

There may be substantial differences in provider comfort levels and perceptions of adherence when considering two different antibiotic initiation strategies for suspected pneumonia in ventilated patients. Our study found a potential discrepancy in actual versus perceived adherence, with providers exhibiting no difference in actual adherence to immediate versus specimen-initiated protocols for the treatment of suspected pneumonia. This survey highlights provider interest in further research in this area.

Footnotes

Authors' Contributions

Conceptualization: Guidry. Methodology: Guidry, Beyene, Sawyer, Hughes. Formal analysis: Guidry. Investigation: O'Dell, Beyene, Watson, Sawyer, Chollet-Hinton, Atchison, Derickson, Cooper, Pennington, VandenBerg, Halimeh, Guidry. Writing: Swilling, Guidry. Editing and review: All authors. Visualization: Swilling. Funding acquisition: Guidry.

Funding Information

Dr. Guidry received a grant from the Surgical Infection Society Foundation for this study.

Author Disclosure Statement

The authors have no relevant financial interests to disclose.

Supplementary Material

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Supplementary Material

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