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Factors Associated With Swallowing Assessment After Oral Endotracheal Intubation and Mechanical Ventilation For Acute Lung Injury
Factors Associated With Swallowing Assessment After Oral Endotracheal Intubation and Mechanical Ventilation For Acute Lung Injury
Measurements and Main Results: Before hospital discharge, Keywords: deglutition; deglutition disorders; intubation; referral
79 (44%) patients completed a swallowing assessment, among and consultation; acute lung injury
(Received in original form June 21, 2014; accepted in final form September 25, 2014 )
Supported by the following grants from the National Institutes of Health: P050HL73994, 5KL2RR025006, and 1K23DC011056.
Author Contributions: All authors reviewed, offered critical revision, and gave approval for final submission. M.B.B.: participated in study design,
completed analyses, provided interpretation of data, completed manuscript writing; M.G.-F.: participated in study design, completed analyses,
provided interpreation of data; P.A.M.-T.: participated in study design, completed data acquisition, provided interpretation of data; C.S.: participated in
study design, completed data acquisition, provided interpretation of data; J.B.P.: provided interpretation of data; D.M.N.: participated in study design,
completed data acquisition, provided interpretation of data.
Correspondence and requests for reprints should be addressed to Dale M. Needham, M.D., Ph.D., Division of Pulmonary and Critical Care Medicine, Johns
Hopkins University School of Medicine, 1830 East Monument Street, 5th Floor, Baltimore, MD 21205. E-mail: dale.needham@jhmi.edu
Ann Am Thorac Soc Vol 11, No 10, pp 1545–1552, Dec 2014
Copyright © 2014 by the American Thoracic Society
DOI: 10.1513/AnnalsATS.201406-274OC
Internet address: www.atsjournals.org
Invasive airways are necessary for endotracheal intubation and (2) patient and a noninstrumental procedure that includes
respiratory support in most patients with organizational factors associated with these assessment of the patient’s signs and
acute lung injury (ALI). However, one swallowing assessments. symptoms of dysphagia with attempted
potential iatrogenic effect of an oral swallowing of oral secretions and/or sips of
endotracheal intubation in mechanically water. The VFSS is a validated instrumental
ventilated patients is impairments in the Methods assessment in which fluoroscopy is used
anatomy and physiology of the pharynx to determine (1) the presence and severity
and larynx that may be associated with Study Population of physiologic swallowing impairments, (2)
subsequent swallowing disorders (1–7). This assessment was conducted as a the effect of compensatory strategies, (3)
Aspiration, a consequence of disordered secondary analysis of a prospective cohort the manner (e.g., oral versus nonoral)
swallowing (i.e., dysphagia), occurs in study in which researchers evaluated of receiving safe nutrition, and (4) the
14–56% of patients who have been ICU care (provided as part of routine consistencies of foods and liquids a patient
mechanically ventilated for at least 48 hours clinical practice) and associations with can safely consume on an oral diet (if
(5–8). Moreover, dysphagia is associated short- and long-term patient outcomes (23). applicable) (25, 26). Although the fiberoptic
with poor patient outcomes, such as feeding Patients were eligible for enrollment in the endoscopic evaluation of swallowing
tube placement, increased hospital length cohort study if they were adults 18 years of (FEES) is routinely conducted in some
of stay, nursing home placement, and age or older, mechanically ventilated, and settings, the hospital sites included in this
increased risk of death (9). diagnosed with ALI as per the American- study do not routinely perform FEES; thus,
Recognition of dysphagia and referrals European Consensus Conference criteria FEES was not included in our primary
to speech-language pathologists (SLPs) (24). Patients were recruited from 13 ICUs outcome. Hospital Site 3 was the only site
for swallowing assessment have increased at 3 university-affiliated teaching hospitals with an ICU-based, nurse-administered
dramatically over the past 20 years in and 1 Veterans Administration hospital in swallowing assessment algorithm that could
neurology and otolaryngology patient Baltimore, Maryland. Patients with ALI prompt physicians for SLP referrals (14).
populations (10–12). During this same with primary neurological disease or This algorithm was based on the patient’s
period of time, nurses have become more trauma and neurological specialty ICUs at level of alertness, speech-language skills,
aware of the risks of dysphagia and participating hospitals were excluded from oral motor skills, maintenance of oral
aspiration and have been trained to the study. The following were the key patient secretions, and clinical signs of aspiration
complete dysphagia screenings, particularly exclusion criteria: (1) more than 5 days (e.g., coughing, choking) with the
in neurological intensive care units (ICUs) of mechanical ventilation before ALI, (2) introduction of various volumes of water.
(13–17). A national survey found that preexisting cognitive impairment or There were no important differences in SLP
41% of hospitals reported using clinical a communication/language barrier, (3) availability between hospital sites, with all sites
screening protocols after extubation, most transfer into a study site ICU with preexisting requiring SLP assessments to be completed
often administered by nursing staff, and ALI of more than 24 hours’ duration, (4) within 24 hours after physician referral.
that in 3% of hospitals SLPs care for all limitations in ICU care at the time of study
recently extubated patients (18). Moreover, eligibility (e.g., no use of vasopressors), and Patient and Organizational Variables
the survey authors reported that guidelines (5) preexisting illness with a life expectancy Relevant patient and organizational
for SLP referral after extubation were shorter than 6 months. variables potentially associated with
present in 29% of hospitals, with the To increase the homogeneity of the a swallowing assessment were selected on
majority (60%) of SLPs using a clinical patient population with respect to dysphagia the basis of a review of the prior literature
bedside swallowing evaluation and 40% risk factors, we also excluded study patients and investigators’ knowledge in this
completing a videofluoroscopic swallow study who (1) had undergone a tracheostomy field. The following were the patient
(VFSS). In addition to these self-reported, before or during their ICU stay and/or (2) demographic and clinical factors evaluated
survey-based results, prospective evaluation had ever had a nasal endotracheal tube in this study: age, sex, race, comorbidity
of clinical practice, as part of routine care, inserted during their ICU stay. Moreover, status (Charlson Index [27] and Functional
is needed to more fully understand the patients who died prior to hospital Comorbidity Index [28]), the presence
epidemiology of swallowing assessment for discharge were excluded, because this of neurologic and upper gastrointestinal
ALI and other nonneurological populations analysis focused on the epidemiology of comorbidities, ICU admitting diagnostic
of critically ill patients (19, 20). swallowing assessment up to the time of category, primary risk factors for ALI,
Patients with ALI frequently have high hospital discharge among ALI survivors. severity of illness (based on Acute
severity of illness and an extended duration Physiology and Chronic Health Evaluation
of mechanical ventilation, with concomitant Primary Outcome Variable II score [29] and Sequential Organ Failure
impaired pulmonary function and muscle The primary outcome measure was Assessment (SOFA) score [30] at ICU
weakness after extubation (21, 22). Patients prevalence of a swallowing assessment in the admission), intubation duration, any
with ALI may be at especially high risk for hospital after extubation as documented in reintubation required, and ICU length of
dysphagia and aspiration after extubation. the medical record. For purposes of this stay. Organizational factors consisted of
Consequently, we further analyzed evaluation, an assessment included either type of ICU (i.e., surgical or medical) and
a multisite prospective cohort of patients (1) a swallow screening completed by hospital study site. The duration of oral
with ALI to evaluate (1) the prevalence a nurse or SLP or (2) a VFSS completed endotracheal intubation was measured in
of swallowing assessments after oral by an SLP. The swallow screening is days since incident intubation. Patients
Patient demographics
Age group, yr, median (IQR) 49 (40, 59) 50 (44, 61) 46 (37, 57) 0.065
Female, n (%) 83 (47%) 42 (53%) 41 (41%) 0.13
Race, n (%)† 0.93
Black 71 (40%) 31 (39%) 40 (40%)
White 106 (60%) 48 (61%) 58 (59%)
Other 1 (1%) 0 (0%) 1 (1%)
Baseline health status
Comorbidity scores, median (IQR)
Charlson Comorbidity Index at ICU admission 1 (0, 4) 1 (0, 4) 1 (0, 3) 0.23
Functional Comorbidity Index at ICU 1 (0, 3) 1 (0, 3) 2 (0, 3) 0.27
admission
Neurologic disease, n (%) 32 (49%) 14 (50%) 18 (49%) 1.00
Upper gastrointestinal disease, n (%) 40 (62%) 16 (57%) 24 (65%) 0.61
ICU characteristics
ICU admission diagnosis, n (%)† 0.40
Respiratory (including pneumonia) 103 (58%) 43 (54%) 60 (61%)
Nonpulmonary sepsis and infectious disease 25 (14%) 13 (16%) 12 (12%)
Upper gastrointestinal disease 21 (12%) 13 (16%) 8 (8%)
Cardiovascular disease 8 (4%) 2 (3%) 6 (6%)
Trauma 7 (4%) 3 (4%) 4 (4%)
Other 14 (8%) 5 (6%) 9 (10%)
Primary risk factors for ALI
Aspiration, n (%) 23 (13%) 8 (10%) 15 (15%) 0.37
Pneumonia, n (%) 88 (49%) 39 (49%) 49 (49%) 1.00
APACHE II score at ICU admission, median (IQR) 23 (19, 28) 23 (19, 28) 23 (17, 29) 0.90
SOFA score at ALI onset, median (IQR) 8 (5, 10) 8 (5, 10) 8 (6, 10) 0.22
Ever reintubated, n (%) 29 (16%) 11 (14%) 18 (18%) 0.54
Intubation duration, d, median (IQR) 8 (5, 11) 9 (7, 13) 7 (4, 10) ,0.001
Organizational characteristics
Medical (vs. surgical) ICU, n (%) 142 (80%) 58 (73%) 84 (85%) 0.064
Hospital study site, n (%)† 0.014
1 52 (29%) 21 (27%) 31 (31%)
2 65 (37%) 22 (28%) 43 (43%)
3‡ 61 (34%) 36 (46%) 25 (25%)
Definition of abbreviations: ALI = acute lung injury; APACHE II = Acute Physiology and Chronic Health Evaluation II; ICU = intensive care unit; IQR =
interquartile range; SOFA = Sequential Organ Failure Assessment.
*Wilcoxon rank-sum test, Fisher’s exact test, or x2 test.
†
Percentages may not add to 100% due to rounding.
‡
Hospital uses a referral algorithm.
hospital sites had undergone a swallowing swallowing assessments by SLPs have been conducted, it is uncertain when SLP
assessment prior to hospital discharge. The been suggested by the American Speech- assessments should be performed (19, 20).
variables independently associated with Language-Hearing Association (46). To our Despite our evaluation of potentially
swallowing assessments were female sex, knowledge, however, there are no published relevant demographic, clinical, and ICU/
longer intubation duration, and hospital studies in which researchers empirically hospital organizational factors, it appears
study site. The hospital site with an evaluated screening tests or models for SLP that completion of swallowing assessments
algorithm for swallowing assessment after referral after extubation of critically ill patients. in nonneurological populations of critically
extubation had more than a twofold In a systematic review of dysphagia ill patients is highly variable and that the
increased odds of swallowing assessment following endotracheal intubation (19), the prevalence varies substantially between
compared with the other two hospital sites. authors reported that four studies (4, 5, 7, 8) hospitals.
There are a number of screenings for evaluated medical and surgical ICU patients, This wide variability in the frequency of
swallowing dysfunction (14, 16, 33–40), with the prevalence of dysphagia ranging performing swallowing assessments as part
with several designed for specific patient from 44% to 62%. Of the 178 patients in of routine medical care (27%, 28%, and
populations, such as stroke, Parkinson’s our cohort, 44% completed swallowing 46% of patients in the present study at
disease, and head and neck cancer. A assessments while in the hospital, with 75% Hospital Sites 1, 2, and 3, respectively) may
number of self-assessments of swallowing of these initial assessments occurring in be disproportionately low compared with
difficulties are used to augment these the ICU. However, because remarkably few the estimated 44–62% prevalence of
screening tests (41–45). Additionally, high-quality studies of swallowing and postextubation dysphagia in critically ill
several screening models for referrals for dysphagia in critically ill patients have patients (4, 5, 7, 8). Moreover, the use of
Table 2. Patient characteristics by hospital unit type for initial swallowing assessment clinical utility of either of these algorithms
has not been empirically evaluated in
Characteristics ICU (n = 59) Ward P value* this patient population, and we are not
(n = 20) aware of any rigorous, evidence-based
guidelines for when screening and/or
Patient demographics instrumental swallowing assessment
Age group, yr, median (IQR) 51 (45, 60) 49 (42, 63) 0.96 should take place after orotracheal
Female, n (%) 28 (47%) 14 (70%) 0.12 extubation. Validation of clinical
White, n (%) 34 (58%) 14 (70%) 0.43 screening methods is needed in this
Baseline health status
Comorbidity scores, median (IQR) patient population to ensure benefits,
Charlson Comorbidity Index at ICU 1 (0, 4) 2 (1, 6) 0.22 without unintentional harms, to patients
admission and to avoid nonbeneficial increases in
Functional Comorbidity Index at ICU 1 (0, 3) 2 (1, 3) 0.65 clinicians’ workloads.
admission
Neurologic disease, n (%) 9 (47%) 5 (56%) 1.00 The duration of oral endotracheal
Upper gastrointestinal disease, n (%) 11 (58%) 5 (56%) 1.00 intubation with mechanical ventilation was
ICU characteristics independently associated with swallowing
ICU admission diagnosis, n (%) 0.85 assessment in the present study. This
Respiratory (including pneumonia) 32 (54%) 11 (55%) may reflect clinicians’ beliefs that the
Nonpulmonary sepsis and infectious 9 (15%) 4 (20%)
disease likelihood or the potential danger of
Upper gastrointestinal disease 10 (17%) 3 (15%) dysphagia increases with duration of
Cardiovascular disease 1 (2%) 1 (5%) intubation. However, we did not address
Trauma 3 (5%) 0 (0%) the association of swallowing physiology
Other 4 (7%) 1 (5%)
Primary risk factors for ALI with the duration of intubation in the
Aspiration, n (%) 5 (8%) 3 (15%) 0.41 present study, so the validity of these
Pneumonia, n (%) 30 (51%) 9 (45%) 0.80 beliefs remains unclear (19).
APACHE II score at ICU admission, median (IQR) 22 (17, 29) 24 (18, 30) 0.79 A final factor that was significantly
SOFA score at ALI onset, median (IQR) 8 (6, 11) 8 (5, 10) 0.24 associated with completion of a swallowing
Ever reintubated, n (%) 10 (17%) 1 (5%) 0.27
Intubation duration, d, median (IQR) 8 (7, 11) 10 (8, 16) 0.07 assessment was sex. We found that
Organizational characteristics females with ALI had a twofold increase
Medical (vs. surgical) ICU, n (%) 41 (69%) 17 (85%) 0.25 in the odds of completing a swallowing
Hospital study site, n (%)† 0.10 assessment. This finding may be consistent
1 14 (24%) 7 (35%)
2 14 (24%) 8 (40%) with the intubation literature which
3‡ 31 (53%) 5 (25%) suggests that females are at greater risk for
laryngeal injury and related swallowing
Definition of abbreviations: ALI = acute lung injury; APACHE II = Acute Physiology and Chronic Health difficulties, possibly due to the placement
Evaluation II; ICU = intensive care unit; IQR = interquartile range; SOFA = Sequential Organ
of oversized endotracheal tubes
Failure Assessment.
*Wilcoxon rank-sum test, Fisher’s exact test, or x2 test. (1, 47–49). Additional prospective,
†
Percentages may not add to 100% due to rounding. physiologically based studies with well-
‡
Hospital uses a referral algorithm. controlled, nonneurological populations
of critically ill patients are needed
swallowing assessments at Sites 1 and 2 was of swallowing assessments between to more fully address potential sex
disproportionately lower than at Site 3, hospitals. The hospital-wide, ICU-based, differences in swallowing assessments
suggesting that Sites 1 and 2 may be nurse-administered swallowing assessment and dysphagia.
missing patients who need to be screened used algorithm at Hospital Site 3 may By offering this prospective, multisite
(especially because the rate of failed explain the significantly higher rate of research in which we determined the
assessments was not lower at the site that swallowing assessments completed in the frequency of swallowing assessments
had a higher frequency of assessments). ICU. The use of an algorithm such as that completed by both nursing staff and SLPs as
Our data underscore previous findings (18) used at Hospital Site 3 (14), or as suggested part of routine clinical practice, we add to
and provide some empirical evidence by others (20), as well as screening tools data gathered in a previously published
regarding variability in clinical practice, and in general, could give rise to greater national survey of SLPs’ self-reported
they highlight the need for more rigorous opportunities for early identification (and practices (18). Therefore, in the present
clinical research designed to assess the subsequent intervention, if necessary) study, we provide additional insight into
frequency of postextubation dysphagia, of patients with dysphagia with resultant variability between institutions with regard
including diagnostic evaluation focused on aspiration. The clinical utility of the to swallowing assessments administered
swallowing physiology and application in algorithm use at Hospital Site 3 is based on after extubation. This variability may
treatment strategies to help guide clinical a small consensus validation panel in which arise, in part, because of limitations of the
practice and hospital policies. a convenience sample of 25 patients with existing literature on the prevalence and
In the present study, we did not address stroke was used, most of which was not risks of postextubation dysphagia, the
the reasons for differences in the frequency compared against a reference standard. The validation of swallowing assessments in this
Table 4. Factors associated with swallowing assessment completion during hospital admission in subjects with acute lung injury
Patient demographics
Age 1.02 (1.00, 1.04) 0.083 1.02 (0.99, 1.04) 0.069
Female 1.61 (0.88, 2.91) 0.119 2.01 (1.03, 3.97) 0.041
White 1.07 (0.58, 1.96) 0.832
Baseline health status
Comorbidity scores, median (IQR)
Charlson Comorbidity Index at ICU admission 1.06 (0.94, 1.20) 0.318
Functional Comorbidity Index at ICU 0.88 (0.72, 1.07) 0.204
admission
Neurologic disease 1.06 (0.40, 2.82) 0.914
Upper GI disease 0.72 (0.26, 1.98) 0.527
ICU characteristics
Upper gastrointestinal disease as ICU admission 2.24 (0.88, 5.71) 0.091 2.54 (0.84, 7.70) 0.100
diagnosis
Primary risk factors for ALI
Aspiration 0.63 (0.25, 1.57) 0.324
Pneumonia 0.99 (0.55, 1.80) 0.986
APACHE II score at ICU admission 1.00 (0.97, 1.04) 0.844
SOFA score at ALI onset 1.07 (0.98, 1.17) 0.129 1.03 (0.93, 1.14) 0.610
Ever reintubated 0.73 (0.32, 1.65) 0.446
Intubation duration 1.10 (1.03, 1.18) 0.003 1.13 (1.05, 1.22) 0.001
Organizational characteristics
Medical (vs. surgical) ICU 0.49 (0.23, 1.04) 0.062 0.66 (0.28, 1.56) 0.347
Hospital study site
1 Reference Reference
2 0.76 (0.35, 1.61) 0.467 0.68 (0.29, 1.62) 0.387
3† 2.13 (1.00, 4.51) 0.050 2.41 (1.00, 5.79) 0.049
Definition of abbreviations: ALI = acute lung injury; APACHE II = Acute Physiology and Chronic Health Evaluation II; ICU = intensive care unit; IQR =
interquartile range; SOFA = Sequential Organ Failure Assessment.
*P values were calculated using simple and multiple logistic regression analysis for bivariable and multivariable results, respectively. Covariates were
included in the multivariable logistic model based on a bivariable association at P,0.10.
†
Hospital uses a referral algorithm.
with the occurrence of in-hospital extubation and when swallowing Author disclosures are available with the text
swallowing assessments. There is assessments are indicated. Further clinical of this article at www.atsjournals.org.
variability in clinical practice among research is needed to create a solid
hospitals, possibly reflecting limitations in evidence base to guide the use of Acknowledgment: The authors thank Victor
existing knowledge as to which patients swallowing assessments after extubation Dinglas for his assistance with data management
are at the greatest risk for dysphagia after in critically ill patients. n for this study.
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