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The Effects of Postoperative Residual Neuromuscular Blockade on Hospital Costs and Intensive Care Unit Admission

A Population-Based Cohort Study

Grabitz, Stephanie D., MD*; Rajaratnam, Nishan, MD*; Chhagani, Khushi, BS*; Thevathasan, Tharusan, Cand Med*; Teja, Bijan J., MD, MBA; Deng, Hao, MD, MPH*; Eikermann, Matthias, MD, PhD†,‡; Kelly, Barry J., MD, MSc

doi: 10.1213/ANE.0000000000004028
Anesthetic Clinical Pharmacology: Original Clinical Research Report
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SDC

BACKGROUND: Postoperative residual neuromuscular blockade continues to be a frequent occurrence with a reported incidence rate of up to 64%. However, the effect of postoperative residual neuromuscular blockade on health care utilization remains unclear. We conducted a retrospective cohort study to investigate the effects of postoperative residual neuromuscular blockade on hospital costs (primary outcome), intensive care unit admission rate, and hospital length of stay (secondary outcomes).

METHODS: We performed a prespecified secondary analysis of data obtained in 2233 adult patients undergoing surgery under general anesthesia. Postoperative residual neuromuscular blockade was defined as a train-of-four ratio <0.9 in the postanesthesia care unit (PACU). Our confounder model adjusted for a variety of patient, surgical, and anesthesia-related factors. We fitted truncated negative binomial regression models for hospital cost and hospital length of stay analyses and a logistic regression model for our intensive care unit admission analysis.

RESULTS: Overall, 457 (20.5%) patients in our cohort had residual neuromuscular blockade on admission to the PACU. Postoperative residual neuromuscular blockade was not independently associated with increased hospital costs (adjusted incidence rate ratio, 1.04, CI, 0.98–1.11; P = .22). There were significantly higher odds of intensive care unit admission in those with postoperative residual neuromuscular blockade compared to those without (adjusted odds ratio, 3.03, CI, 1.33–6.87; P < .01). Further, we found a trend toward increased hospital length of stay in patients with postoperative residual neuromuscular blockade (adjusted incidence rate ratio, 1.09; P = .06). Sensitivity analysis using the same model in the day of surgery admissions and ambulatory surgery confirmed our findings.

CONCLUSIONS: Postoperative residual neuromuscular blockade at PACU admission was not significantly associated with increased hospital costs, but was associated with higher rates of intensive care unit admission. These findings support the view that clinicians should continue to work to reduce the rate of postoperative residual neuromuscular blockade.

From the *Department of Anesthesia, Critical Care, and Pain Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts

Department of Anesthesia, Critical Care, and Pain Medicine, Harvard Medical School, Beth Israel Deaconess Medical Center, Boston, Massachusetts

Klinik für Anästhesiologie und Intensivmedizin, Universität Duisburg-Essen, Essen, Germany.

Published ahead of print 12 December 2018.

Accepted for publication December 12, 2018.

Funding: Dr Eikermann reports receipt of grants from Merck; personal fees (honoraria) from Merck; funding from Jeffrey and Judith Buzen; holds equity in Calabash Bioscience and an investigator-initiated grant (IISP# 39442) was provided by Schering-Plough Research Institute, Kenilworth, NJ, a Division of Schering Corporation, to the Massachusetts General Hospital.

The authors declare no conflicts of interest.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s website.

S. D. Grabitz and N. Rajaratnam contributed equally and share first authorship.

Clinical trial number and registry URL: clinicaltrials.gov (NCT01718860).

Reprints will not be available from the authors.

Address correspondence to Barry J. Kelly, MD, MSc, Department of Anesthesia, Critical Care and Pain Medicine, Harvard Medical School, Beth Israel Deaconess Medical Center, 330 Brookline Ave, Boston, MA 02215. Address e-mail to bjkelly@bidmc.harvard.edu.

See Editorial, p 1065

KEY POINTS

  • Question: Is there an association between postoperative residual neuromuscular blockade in postanesthesia care unit and hospital costs?
  • Findings: Postoperative residual neuromuscular blockade in postanesthesia care unit was not associated with increased hospital costs but there was a significant increase in the odds of intensive care unit admission.
  • Meaning: Postoperative residual neuromuscular blockade is prevalent and its association with an increased odds of intensive care unit admission should alert clinicians to screen for its presence.

Recent data suggest that nondepolarizing neuromuscular blocking agents are associated with increased rates of postoperative respiratory complications.1 In addition, nondepolarizing neuromuscular blocking agent dose dependability increases the odds of hospital readmission and the hospital length of stay.2 However, it is unclear whether the observed association between nondepolarizing neuromuscular blocking agent and adverse patient outcomes in these studies was related to impaired neuromuscular transmission, given that objective evidence of postoperative residual neuromuscular blockade by train-of-four ratio was not evaluated. Postoperative residual neuromuscular blockade continues to be a frequent occurrence with reported incidences ranging from 4% to 64%.3–8

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Rationale

The effect of residual neuromuscular blockade on health care utilization and cost remains unclear. We hypothesized that postoperative residual neuromuscular blockade at admission to the postanesthesia care unit (PACU) is associated with increased hospital costs. We also hypothesized that postoperative residual neuromuscular blockade would be associated with increased odds of intensive care unit admission and hospital length of stay.

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Study Objectives

The aim of this retrospective observational study was to evaluate the effects of postoperative residual neuromuscular blockade on our primary outcome, hospital costs. Secondary analyses were conducted to evaluate the effects of postoperative residual neuromuscular blockade on potential cost-influencing factors such as unplanned postoperative intensive care unit admission and hospital length of stay. Postoperative residual neuromuscular blockade was defined as the presence of a train-of-four ratio measured by acceleromyography of the adductor pollicis muscle of <0.9.9

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METHODS

Setting and Data

This study is a secondary analysis of a previously published study using data collected between 2008 and 2013 at Massachusetts General Hospital, a tertiary care facility in Boston, MA.10 The study was approved by the institutional review board and the need for written informed consent was waived by the institutional review board. The study was registered at clinicaltrials.gov (NCT01718860, principal investigator: Matthias Eikermann; date of registration October 29, 2012) and adheres to the applicable STrengthening the Reporting of OBservational studies in Epidemiology guidelines. Train-of-four measurements in the PACU, age, sex, body mass index, postoperative intensive care unit admission, hospital length of stay, as well as principal surgical procedures were recorded. We performed chart review of all postoperative intensive care unit admissions to retrieve information on the principal medical indication for intensive care unit admission and to ensure that only unplanned, rather than scheduled intensive care unit admissions, independent of patient’s preoperative clinical status, were recorded. Hospital costs and hospital admission type (inpatient or ambulatory) were retrieved from the Enterprise Performance Systems Inc (Chesterfield, MO) database, a performance improvement and financial planning system, which are outcomes that have been previously validated by our research group.11,12

Enterprise Performance Systems Inc separately tracks direct and indirect expenses. Direct costs include expenses that are directly related to patient care, whereas indirect costs are not linked to patient care (eg, financial service department costs). Direct costs can further be subdivided into direct fixed and direct variable costs. Direct variable costs vary with the patient’s specific care (performed procedures, required monitoring, medications, etc), whereas direct fixed costs are linked to patient care but are nonvariable (equipment, buildings, etc). The total costs represent the sum of direct and indirect expenses incurred by the institution.

Data on patient characteristics such as the Charlson comorbidity index were obtained from the Research Patient Data Registry (Partners Healthcare, Boston, MA), a centralized registry that retrieves clinical information for research purposes. We retrieved information about perioperative surgical and anesthesia-related parameters, as well as medication administration and physiologic data from patient monitors from the Anesthesia Information Management System. We performed a chart review of body mass index, American Society of Anesthesiologists (ASA) physical status score, and duration of surgery in 300 patients to confirm data validity. Diagnoses were coded based on the International Statistical Classification of Diseases and Related Health Problems, ninth revision.13

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Population

The study cohort consisted of a consecutive cohort of patients undergoing surgery under general anesthesia and given nondepolarizing neuromuscular blocking agents (ie, atracurium, cisatracurium, vecuronium, or rocuronium) between 2008 and 2013 at Massachusetts General Hospital. Patients were excluded if not extubated directly after the procedure, if <18 years of age, or if they were transferred directly to the intensive care unit after surgery. Further, patients were excluded if they had procedures or conditions that did not allow for T4/T1 to be measured by ulnar nerve stimulation (ie, dual upper extremity bandages or external fixations). Adductor pollicis muscle acceloromyography was recorded on 96% of all screened patients in the original study during the study period, minimizing selection bias.

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Exposure

The primary independent variable was postoperative residual neuromuscular blockade. We defined postoperative residual neuromuscular blockade as the presence of a train-of-four ratio of <0.9,9 measured by acceleromyography of the adductor pollicis muscle using a quantitative train-of-four monitor (TOF-watch SX; Schering-Plough, Kenilworth, NJ). Postoperative residual neuromuscular blockade was a dichotomous variable, the presence of which defined exposure and the absence of which defined nonexposure. Train-of-four monitoring was performed on each patient within 10 minutes of PACU admission. The mean values of 2 consecutive train-of-four ratios were used to generate this variable and postoperative residual neuromuscular blockade was predefined as a train-of-four ratio <0.9. Additional methodological details on postoperative data collection and train-of-four measurements can be found in Supplemental Digital Content, Document, http://links.lww.com/AA/C698.

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Outcomes

The primary outcome was hospital costs. This continuous variable was defined as the sum of total direct patient-service costs and total indirect costs allocated to departments in a step-down structure. In addition, we have performed a sensitivity analyses using the previously described breakdowns of total costs as the dependent variable. Direct variables costs vary with individual patient care (eg, procedures, monitoring, medications). Additional parameters of health care utilization such as postoperative intensive care unit admission within 7 days after surgery and hospital length of stay were defined as secondary outcomes. Due to the sensitivity of internal financial figures, and to provide more generalizable cost estimates in the analysis, we did not report specific dollar amounts, but rather the incident rate ratio, as a relative estimate.

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Covariates

To control for the numerous patient, surgical, and anesthesia-related variances, a robust confounder control model was created for the adjusted analysis of the primary outcome, hospital costs. The covariates included in this model were age, gender, ASA physical status, emergency status, Charlson comorbidity index, work relative value units, admission type, night surgery, duration of surgery, intraoperative fluids, intraoperative long-acting opioid (morphine) dose equivalents, hypotensive minutes with mean arterial pressure <55 mm Hg, protective ventilation, intraoperative vasopressor dose, age-adjusted minimum alveolar concentration, median inspired oxygen fraction, preoperative beta-blocker use within 28 days, preexisting respiratory failure (within 7 preoperative days), use of neuraxial anesthesia, use of regional anesthesia, admission from a nursing home or skilled nursing facility, and home oxygen dependence. Pre- and postoperative opioid prescription were included as covariates in sensitivity analyses in the secondary analysis evaluating the association of postoperative residual neuromuscular blockade and intensive care unit admission. Furthermore, we included the time of surgery completion into this regression model in an additional sensitivity analysis.

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Power Analysis

An a priori power analysis was not conducted due to the retrospective nature of this study. Based on our included observed data, we estimated that we had 80% power to detect an effect size of 0.1, from a 2 independent samples t test. This effect size equates to a difference in hospital costs of approximately 19.3% of mean costs, assuming the observed between group mean difference of $3270, a SD of $32,700 for our primary outcome and a mean cost of $16,920 in the group that did not have postoperative residual neuromuscular blockade in PACU.

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Statistical Analysis

The analysis for the primary outcome, hospital costs, was performed using adjusted truncated negative binomial regression, to present costs as a ratio and keep institute-specific costs sensitive. The cost data in our dataset was recorded as only positive integers (no zeros, no decimal places), which might also be viewed as the accumulated counts of each 1 dollar. Descriptives of the outcome indicated overdispersion. For this reason, we elected to use truncated negative binomial regression. Further information regarding model selection including a calibration curve is presented in Supplemental Digital Content, Document, Section 6, http://links.lww.com/AA/C698. To enhance the robustness of our model, we performed sensitivity analyses using components of total costs as the dependent variable. In addition, we performed further sensitivity analysis in the subgroup, day of surgery admissions and ambulatory surgery to exclude indirect costs of prior hospital admission up to that point.

We used logistic regression analyses to test the association between postoperative residual neuromuscular blockade in PACU and intensive care unit admission adjusting for the previously listed covariates. Results are presented as odds ratios or incidence rate ratios with 95% CIs.

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Missing Data

The primary analysis was performed using the complete case method. In a sensitivity analysis, values for missing covariates were imputed using multiple imputation by chained equations. More specifically, variables with missing data were imputed using all covariates and the outcome of the primary model utilizing 10 burn-in rounds followed by a total of 10 final imputations using the Stata command “mi impute.” The model estimates were combined using variance estimates that combine imprecision both within and across imputations.

Data analysis was performed using STATA 13 (StataCorp LP, College Station, TX). A 2-tailed P value <.05 was considered statistically significant.

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RESULTS

Table 1

Table 1

Figure

Figure

Among the 3000 patients in the database who underwent general anesthesia and who had train-of-four ratio assessment in the PACU, 2233 met inclusion criteria for our primary analysis (Figure). There were 457 (20.5%) patients diagnosed with postoperative residual neuromuscular blockade in the PACU. Proportion of males and mean Charlson comorbidity index were higher in patients experiencing postoperative residual neuromuscular blockade (Table 1). The majority of the study patients were admitted on the day of surgery (n = 1930).

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Hospital Costs (Primary Analysis)

Table 2

Table 2

On initial unadjusted truncated negative binomial regression analysis, postoperative residual neuromuscular blockade was associated with an increase in total hospital costs (incidence rate ratio, 1.14, 95% CI, 1.06–1.22; P < .001). Following adjustment for our a priori defined confounders, there was no longer a significant difference in hospital costs between patients experiencing postoperative residual neuromuscular blockade and those without residual paralysis (adjusted incidence rate ratio, 1.04, CI, 0.98–1.11; P = .22). The findings from the primary regression analysis remained robust using the imputed database (adjusted incidence rate ratio, 1.05, CI, 0.99–1.12; Table 2). Further assessment of effect modification as suggested by the editor and reviewers is provided in Supplemental Digital Content, Document, Section 4, http://links.lww.com/AA/C698.

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Intensive Care Unit Admission and Hospital Length of Stay (Secondary Analysis)

A total of 42 patients of n = 2233 were postoperatively admitted to the intensive care unit, giving an incidence rate of 1.8%. The incidence rates in the postoperative residual neuromuscular blockade and no postoperative residual neuromuscular blockade group were 3.3% (n = 15) and 1.5% (n = 27), respectively. There were no fatalities in this cohort. The adjusted odds of intensive care unit admission in the postoperative residual neuromuscular blockade group compared to the unexposeed group was 3.03, (CI, 1.33–6.87; P = .008). The adjusted incidence rate ratio of hospital length of stay was 1.09 (CI, 1.00–1.19; P = .058) in the postoperative residual neuromuscular blockade group (Table 2).

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Exploratory Analyses

Although postoperative residual neuromuscular blockade was defined as a train-of-four ratio <0.9 in this study and in other similar studies,3,9 we further explored the connection between postoperative residual neuromuscular blockade and our primary outcome, total hospital costs, in patients with postoperative train-of-four ratio <0.8 and train-of-four ratio <0.7, which indicate a deeper level of residual neuromuscular blockade.9 The adjusted analyses showed no significant differences between the exposure and control groups: train-of-four <0.8 (adjusted incidence rate ratio, 1.05, CI, 0.94–1.17; P = .35) and train-of-four <0.7 (adjusted incidence rate ratio, 1.08, CI, 0.86–1.36; P = .49). Thus, in our cohort, a correlation between postoperative residual neuromuscular blockade and costs of the index hospitalization was not observed even at increased levels of postoperative residual neuromuscular blockade.

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Sensitivity Analyses

We repeated our costs analysis using the components of total costs as the dependent variables. As highlighted in Table 2, the unadjusted incidence rate ratio for variable direct costs was 1.15 (CI, 1.07–1.12) and the adjusted incident rate ratio was 1.03 (CI, 0.96–1.11). We performed sensitivity analysis using the subgroup day of surgery admissions and ambulatory surgery to exclude indirect costs of prior hospital admission up to the event “postoperative residual neuromuscular blockade in PACU.” In the day of surgery admission subgroup, the adjusted incident rate ratio for increased costs was 1.04 (CI, 0.99–1.09).

When additionally adjusting the secondary regression model for preoperative opioid use, we found a significant association between postoperative residual neuromuscular blockade and higher odds of postoperative intensive care unit admission. Including the opioid prescription on the day of discharge as a covariate in this regression analysis again confirmed robustness of the association between postoperative residual neuromuscular blockade and postoperative intensive care unit admission.

A variable indicating if the surgical case was completed in the morning (7 AM–11:59 AM), in the afternoon (noon – 4:59 PM), or at night (5 PM–6:59 AM) was included as covariate in an additional sensitivity analysis, which confirmed the independent association of postoperative residual neuromuscular blockade and postoperative admission to the intensive care unit (Table 2).

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DISCUSSION

In this retrospective study of 2233 patients who underwent general anesthesia, 457 (20.5%) demonstrated postoperative residual neuromuscular blockade on admission to the PACU. Our analyses revealed that postoperative residual neuromuscular blockade was not associated with a significant increase in estimated total or direct variable health care costs. However, we found that postoperative residual neuromuscular blockade in the PACU was associated with a 3-fold increase in the odds of being admitted to the intensive care unit.

Consistent with a previously published incidence rate of 22% of postoperative residual neuromuscular blockade at our institution,4 we observed an incidence rate of 20.5% of postoperative residual neuromuscular blockade in this cohort. Based on the original protocol, patients within the original study were consecutively screened for recruitment if they received general anesthesia with nondepolarizing neuromuscular blocking agent. The short, predefined time frame of the train-of-four assessment (10 minutes after PACU admission) and the high rate of consecutively enrolled patients (96%) minimized selection bias.

Rates of postoperative residual neuromuscular blockade in other studies vary from 4% to 64%.3–8 However, these studies did not report reintubations or admissions to the intensive care unit. We previously reported an associated increase in the mean PACU length of stay of 80 minutes with postoperative residual neuromuscular blockade (P = .03).4 In 2012, Thilen et al5 studied postoperative residual neuromuscular blockade in 150 patients and reported postoperative residual neuromuscular blockade incidence rate of 52% in their group via adductor pollicis muscle monitoring. Although some patients (n = 13) in that cohort were electively ventilated in the PACU to facilitate regional anesthesia, there were no reported respiratory complications or intensive care unit admissions. The Residual Curarization and its Incidence at Tracheal Extubation study reported one of the highest incidences of postoperative residual neuromuscular blockade across all studies (63.5%), when the phenomenon was screened for in 302 postabdominal surgery patients across 8 Canadian hospitals, with only 1 patient requiring reintubation. This study did not report intensive care unit admission data or costs.3 Despite these high incidence rates, routine monitoring to evaluate the reversal of postoperative residual neuromuscular blockade is not considered part of minimum monitoring standards in most clinical settings. A large international survey in 2010 revealed that 19.3% of European and 9.4% of US clinicians do not use neuromuscular monitors in postoperative evaluations and that pharmacological reversal was routinely administered by only 18% of European and 34.2% of US clinicians surveyed.7

Our secondary analysis demonstrated a 3-fold increase in the odds of intensive care unit admission from the PACU in those determined to have postoperative residual neuromuscular blockade. This finding has not been previously reported. Previous studies have shown an association between postoperative residual neuromuscular blockade and both increased respiratory complications and delayed discharge from the PACU,1,4 but few have reported unanticipated intensive care unit admission rates. For instance, in 2015, McLean et al1 demonstrated a dose-dependent association between intermediate-acting neuromuscular blocking agents and postoperative respiratory complications. Over 48,000 cases were included for analysis of the association between dosing of nondepolarizing neuromuscular blocking agent and a composite outcome of respiratory complications within 3 postoperative days. In this study, the reintubation rate was 0.3% and they did not report intensive care unit admission or hospital costs.

Much debate exists within the literature as to whether intensive care unit admission universally translates into better outcomes, despite presumed increased hospital costs.14,15 Our group has postulated that an acuity threshold may exist below which the risks of intensive care unit admission outweigh the benefits.16 In this study, we found a trend toward increased hospital length of stay in patients with postoperative residual neuromuscular blockade, which in part may be explained by admission of patients with lower acuity except for residual neuromuscular blockade. In contrast to a previous study,17 we found differential effects of residual neuromuscular blockade on intensive care unit admission rate. This may be in part explained by low intensive care unit bed occupancy in our study center. Lower occupancy facilitates early intensive care unit admission, as opposed to keeping patients who need extended postoperative care longer in the PACU. The PACU is a very cost-intensive location in the hospital with a nurse-to-patient ratio equivalent to the intensive care unit. Effects of residual neuromuscular blockade on costs of care may be different in a clinical scenario where procedures would need to be canceled as a result of lack of availability of intensive care unit beds. Therefore, based on the results of our analyses, it would be advisable for clinicians to screen for residual neuromuscular blockade in the perioperative setting before transfer to the PACU, and to take appropriate measures ensuring complete recovery of normal neuromuscular physiology to offset the risk of unnecessary intensive care unit admission or increased PACU length of stay. As our study was conducted in a well-resourced academic center with critical care bed elasticity, further studies to validate our findings using large heterogeneous datasets may provide more insight into the problem of postoperative residual neuromuscular blockade in the PACU and its burden on a variety of intensive care unit structures. Our group recently studied the effect of incentivized protocols for checking adequate reversal of nondepolarizing neuromuscular blocking agent in the perioperative setting and found lower odds of postoperative pulmonary complications, lower costs, and shorter duration of hospital stay after implementation of the quality improvement initiative.18

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Strengths

A major strength of this study is that we measured train-of-four ratio at PACU admission prospectively in a large sample size using industry standard TOFwatch technology (TOF-Watch, Organon, Finland). Our hypothesis was further tested with exploratory analyses using lower train-of-four thresholds for our exposure variable of postoperative residual neuromuscular blockade and still failed to show significantly increased hospital costs. Several sensitivity analyses confirmed the robustness of our findings. We believe our study has face validity, as characterized by (1) the good coverage of surgical patients from Massachusetts General Hospital without preselection of patients causing selection bias; (2) a confounder model that addresses the wide range of comorbidities and procedures; and (3) the absence of cost differences and the minimal beta error observed in our analysis.19,20 The model results are a good representation of the actual cost. For example, the model predicted increase cost of 27% for patients with a high ASA physical status classification (≥III) compared to patients with a lower ASA physical status (I or II). Similarly, the model predicted a cost increase of 87% moving from lowest to highest costly surgical service. Finally, the incidence rate of postoperative residual neuromuscular blockade in the entire cohort was 20.5%, which we believe to be accurate based on the fact that 96% of consecutively recruited patients in the original study had valid train-of-four values at PACU admission.

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Limitations

Our single center, large tertiary referral hospital may not allow generalizability to smaller, less well-resourced health care settings. In addition, despite a robust confounder model, we present observational data where unknown factors may confound the results. Our institution is not able to separate costs before and after PACU admission, so our analysis is limited by data points collected before the exposure, postoperative residual neuromuscular blockade in PACU, which may affect the direct association of postoperative residual neuromuscular blockade on hospital costs.

Perioperative cost data are often dominated by a few outlier patients, which make it hard to identify associations between preventable complications, such as postoperative residual neuromuscular blockade, and costs. One such outlier in our cohort was dependent on home oxygen therapy. Given the highly skewed distribution of costs in our cohort, we conducted a sensitivity analysis excluding this 1 true outlier patient. The main findings did not change when excluding this patient from the analysis; we again found no association of postoperative residual neuromuscular blockade and costs in the adjusted analysis (adjusted incidence rate ratio, 1.03, CI, 0.97–1.10), whereas postoperative residual neuromuscular blockade was significantly associated with postoperative intensive care unit admission. Finally, information about some outcomes (hospital length of stay and costs) was retrieved from administrative data where misclassification is possible.

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CONCLUSIONS

We found that postoperative residual neuromuscular blockade in the PACU was not associated with increased health care costs, but with a significant increase in the odds of intensive care unit admission. Residual neuromuscular blockade is prevalent and underdiagnosed, and adequate prevention may decrease rates of unplanned intensive care unit admission associated with residual neuromuscular blockade.

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DISCLOSURES

Name: Stephanie D. Grabitz, MD.

Contribution: This author helped with literature review, data extraction, coding, study design, data analysis, writing and revision of the manuscript.

Name: Nishan Rajaratnam, MD.

Contribution: This author helped with literature review, data extraction, coding, data analysis, study design, statistical analysis plan, and writing the manuscript.

Name: Khushi Chhagani, BS.

Contribution: This author helped with data extraction, coding, data analysis, study design, statistical analysis plan, and writing the manuscript.

Name: Tharusan Thevathasan, Cand Med.

Contribution: This author helped with literature review, data extraction, coding, study design, and data analysis.

Name: Bijan J. Teja, MD, MBA.

Contribution: This author helped with study design, statistical analysis plan, data analysis, and writing the manuscript.

Name: Hao Deng, MD, MPH.

Contribution: This author helped with study design and statistical analysis planning.

Name: Matthias Eikermann, MD, PhD.

Contribution: This author conceived the study hypothesis, helped with study design, and approved the final manuscript.

Name: Barry J. Kelly, MD, MSc.

Contribution: This author helped with literature review, study design, statistical analysis plan, data analysis, writing, submission and revision of the manuscript.

This manuscript was handled by: Ken B. Johnson, MD.

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