Introduction
The rate of swallowing disorders, termed dysphagia , vary by clinical diagnoses, occurring in up to 93% of patients with severe traumatic brain injuries (TBIs), 30% of all TBIs, and 23% of spinal cord injuries.1-3 Dysphagia can lead to malnutrition, aspiration , dehydration, aspiration pneumonia , mortality, and an increase in hospital length of stay (HLOS)4-6 Risk factors for dysphagia include geriatric age (≥65 years old), central nervous system disorders, neurological disorders, presence of osteophytes in the cervical spine, severe narrowing of the corticobulbar tract, gastroesophageal reflux disease, hyperthyroidism, hypothyroidism, benzodiazepine use, mechanical ventilation dependence, tracheostomy placement, and nasogastric tube insertion.3,4,7
Mekata et al. demonstrated that c-collars restrict the cervical spine during swallowing, restrict the extension of several cervical vertebra, and prolong the epiglottic inversion times, pharyngoesophageal segment opening time, and hyoid anterosuperior elevation time.8 C-collars change the swallowing function including the point of initiation of swallow response, presence of pharyngeal residue, laryngeal penetration, and hyoid bone movement.9 This restriction caused by c-collars placement may increase the risk for dysphagia .
Currently, the American College of Surgeon guideline for the management of TBIs, the Eastern Association for trauma practice management, and the Yale Swallow Protocol do not recommend dysphagia screening specifically for patients with a c-collar placed, patients with a TBI, or those with a cervical spine injury.6,10-12 The Yale Swallow Protocol, which is the diagnostic tool for dysphagia used at our center, is indicated for all patients considered to be at risk for aspiration .13 However, aspiration is not established as a complication from c-collar application; therefore, it remains unclear if patients with c-collars applied should be screened per the Yale Swallow Protocol. Additionally, the Yale Swallow Protocol excludes patients from examination for a variety of reasons including if the head-of-bed is restricted to less than 30°, which may prevent some patients with a c-collar placed from screening.13 The purpose of this study was to determine if patients who had a c-collar placed are at an increased risk for dysphagia or aspiration among a population of TBI and cervical spine injury patients when compared with those without a c-collar placed. This information is important to establish if there should be widespread screening for dysphagia across TBI and cervical spine injury patients with a c-collar placed to prevent subsequent outcomes.
Methods
This retrospective cohort study at a U.S. Level 1 trauma center included geriatric patients (aged ≥65 years old) admitted from January 2016 to December 2018 with a cervical spine injury or a TBI, because these patients are often stabilized with c-collars. TBI was defined as a diagnosis of subdural hematoma (SDH), subarachnoid hemorrhage (SAH), epidural hematoma (EDH), diffuse axonal injury (DAI), intracerebral hemorrhage (ICH), intraventricular hemorrhage (IVH), parenchymal hemorrhage, cerebral edema, or loss of consciousness (LOC). Patients who had a c-collar placed were compared to patients who did not. This study was approved by our Institutional Review Board with a waiver of consent on March 28, 2020.
Data for this study were collected from the trauma registry or the patients' electronic medical record. Included variables and how they were summarized were as follows: c-collar placed (yes/no), age (continuous), sex [% (n) male], race [% (n) White, Black or African American, Asian, or Other or unknown], injury severity score (ISS, continuous), Glasgow Coma Scale (GCS, continuous), comorbidities [% (n), comorbidities were also summarized as a count (continuous)], injury diagnoses [% (n), SAH, SDH, ICH, IVH, cervical spine injury, cerebral edema, DAI, LOC, parenchymal hemorrhage, and acute hemorrhage], complications [% (n), intubated, unplanned return to the intensive care unit (ICU), bed rest, cardiac arrest with cardiopulmonary resuscitation, deep vein thrombosis (DVT), MI, stroke or cerebrovascular accident (CVA), aspiration , non–ventilator-associated pneumonia , probable aspiration pneumonia (combination of aspiration and pneumonia diagnoses), respiratory failure , and swallow therapy for dysphagia (yes/no)], ICU length of stay (ICU LOS, continuous, days), HLOS (continuous, days), in-hospital death (% died, n), and discharge disposition [% (n), categorized as: home or home with health services, skilled nursing facility, rehabilitation, long-term care, hospice, or left against medical advice]. Comorbidities collected in the registry included hypertension, mental health condition, dementia, functional dependence, bleeding disorder, chronic obstructive pulmonary disease (COPD), diabetes, alcohol use disorder, drug use disorder, smoker, renal failure, steroid use, congestive heart failure, CVA, cirrhosis, cancer, obesity, pulmonary artery disease, and myocardial infarction (MI), but only those prevalent among more than 10% of the population were summarized in the article. Mental health conditions included schizophrenia, bipolar disorder, major depressive disorder, social anxiety disorder, posttraumatic stress disorder, and antisocial personality disorder. The primary outcome was dysphagia . Screening for dysphagia was ordered at the discretion of the on-call trauma physician and diagnosed by a speech therapist using the Yale Swallow Protocol. If dysphagia was confirmed, swallow therapy was conducted. All other outcomes collected were secondary outcomes.
Continuous variables were summarized as mean or median values and were compared using Student's t -test and Kruskal–Wallis test. Categorical or dichotomous variables were summarized as proportions (counts) and were compared using Fisher's exact test or chi-square test. Logistic stepwise regression was used to assess for confounding; entry and exit criteria were set at alpha <0.05. A stratified analysis was conducted by receipt of swallow therapy. An alpha <0.05 defined significance.
Results
There were 684 patients, 78.5% (537) did not have a c-collar placed and 21.5% (147) did. Overall, the patients were 49.8% male, with a median age of 77 years and a mean ISS of 13.4. The patients were similar in age (p = .82), gender (p = .43), race (p = .09), ISS (p = .73), and GCS (p = .15; Table 1 ). Although the median number of comorbidities was similar between groups, p = .86, patients with a c-collar placed were less likely to have a mental health condition (8% vs. 16%, p = .01) and more likely to have COPD (18% vs. 11%, p = .02). Other comorbidities were comparable between groups. Patients who had a c-collar placed were also less likely to have an SDH (31% vs. 59%, p < .0001), SAH (25% vs. 37%, p = .004), or LOC (29% vs. 58%, p < .0001) and were more likely to have a cervical spine injury (69% vs. 13%, p < .0001) than patients without a c-collar placed. There was a significantly higher proportion of patients with a c-collar placed who had a combination of a TBI and a cervical spine injury than among patients who did not have a c-collar placed (26% vs. 7%, p < .0001). Other diagnoses were similar between groups.
Table 1. -
Demographic and Clinical Characteristics
No c-collar, n = 537
C-collar, n = 147
p -value
Age, median (IQR), years
77.0 (71.0, 84.0)
78.0 (70.0, 83.0)
.82
Sex, % female (n)
50.6% (272)
53.1% (78)
.43
Race, % (n)
.09
 White
84.5% (454)
90.5% (133)
 Black or African American
3.0% (16)
1.4% (2)
 Asian
3.0% (16)
0% (0)
 Other or unknown
9.5% (51)
8.2% (12)
ISS, median (IQR)
12.0 (6.0, 18.0)
11.0 (9.0, 17.0)
.73
GCS, median (IQR)
15.0 (15.0, 15.0)
15.0 (14.0, 15.0)
.15
Comorbidities, % (n)
 Hypertension
59.6% (320)
65.3% (96)
.21
 Mental health condition
16.2% (87)
7.5% (11)
.01
 Dementia
19.9% (107)
15.6% (23)
.24
 Functional dependance
18.4% (99)
17.0% (25)
.69
 Advanced directive
20.1% (108)
15.0% (22)
.16
 COPD
11.0% (59)
18.4% (27)
.02
 Diabetes
20.5% (110)
23.1% (34)
.49
 Alcohol use
7.8% (42)
12.9% (19)
.054
 Coagulopathy
22.0% (118)
21.1% (31)
.82
 Comorbidity count
2 (1, 4)
3 (1, 4)
.86
Diagnosis, % (n)
 SDH
58.5% (314)
30.6% (45)
<.0001
 SAH
37.1% (199)
24.5% (36)
.004
 EDH
1.7% (9)
4.1% (6)
.11
 ICH/IVH
15.8 (85)
10.9% (16)
.13
 Cerebral edema
1.9% (10)
0.7% (1)
.47
 Parenchymal hemorrhage
2.2% (12)
3.4% (5)
.38
 LOC
59.6% (320)
28.6% (42)
<.0001
 Cervical spine injury
12.7% (68)
69.4% (102)
<.0001
 TBI and cervical spine injury, % (n)
6.5% (35)
25.9% (38)
<.0001
 TBI only
86.8% (466)
29.9% (44)
 Cervical spine only
6.7% (36)
44.2% (65)
Bold indicates statistical significance at p < .05.
COPD = chronic obstructive pulmonary disease; EDH = epidural hemorrhage; GCS = Glasgow Coma Scale; ICH/IVH = intracranial hemorrhage or intraventricular hemorrhage; ISS = injury severity score; LOC = loss of consciousness; SAH = subarachnoid hemorrhage; SDH = subdural hemorrhage; TBI = traumatic brain injury.
Dysphagia was significantly more common among patients with a c-collar placed than among those without a c-collar placed (54% vs. 39%, p = .002; Table 2 ). There was a significantly higher proportion of patients with a c-collar placed who had respiratory failure (p = .0002), were intubated (p = .01), were put on bed rest (p = .0001), and had an MI (p = .04) when compared with patients who did not have a c-collar placed. Although the proportion of patients with aspiration was higher among those with a c-collar placed (8% vs. 4%), the difference was not significant (p = .11). Other complications were similar between groups, including pneumonia (p = .85) and probable aspiration pneumonia (p = .70). The median HLOS was significantly longer for patients with a c-collar placed (5 vs. 3 days, p < .0001); however, the median ICU LOS was statistically similar between groups (1 vs. 0 days, p = .08). Patients with a c-collar placed were discharged home or home with health services significantly less often (p < .0001) and to rehabilitation significantly more often (p < .0001). Other discharge dispositions and the rate of in-hospital deaths (p = .06) were comparable between groups.
Table 2. -
Outcomes and Complications
No c-collar, n = 537
C-collar, n = 147
p -value
Complications, % (n)
 Swallow therapy for dysphagia
39.3% (211)
53.7% (79)
.002
 Pneumonia
3.7% (20)
3.4% (5)
.85
 Aspiration
4.3% (23)
7.5% (11)
.11
 Probable aspiration pneumonia
1.7% (9)
0.7% (1)
.70
 Respiratory failure
6.9% (37)
17.0% (25)
.0002
 Intubation
4.7% (25)
10.2% (15)
.01
 Unplanned return to ICU
3.2% (17)
1.4% (2)
.39
 Bed rest
0% (0)
2.7% (4)
.0001
 Cardiac arrest with CPR
1.3% (7)
0.7% (1)
.53
 DVT
0.7% (4)
0% (0)
.58
 MI
0% (0)
1.4% (2)
.04
 Stroke or CVA
0.7% (4)
0.7% (1)
>.99
 ICU LOS, median (IQR)
0.0 (0.0, 3.0)
1.0 (0.0, 4.0)
.08
 HLOS, median (IQR)
3.0 (1.0, 6.0)
5.0 (3.0, 8.0)
<.0001
Discharge disposition, % (n)
 Home or home with health services
49.3% (265)
26.5% (39)
<.0001
 Skilled nursing facility
31.1% (167)
36.7% (54)
.2
 Rehabilitation
9.1% (49)
22.5% (33)
<.0001
 Long-term care
1.5% (8)
3.4% (5)
.16
 Hospice
4.1% (22)
2.7% (4)
.44
 Left AMA
0.4% (2)
0% (0)
>.99
 In-hospital mortality, % (n)
4.8% (26)
8.8% (13)
.06
Bold indicates statistical significance at P < 0.05.
AMA = against medical advice; CPR = cardiopulmonary resuscitation; CVA = cerebrovascular accident; DVT = deep vein thrombosis; HLOS = hospital length of stay; ICU: intensive care unit; LOS = length of stay; MI = myocardial infarction, VAP = ventilator-associated pneumonia .
Across all patients, regardless of c-collar status, pneumonia (6.6% vs. 1.5%, p = .001), respiratory failure (13.1% vs. 6.1%, p = .002), and aspiration (9.3% vs. 1.8%, p < .0001) were significantly more common among patients who had dysphagia than among patients who did not have dysphagia (data not visualized).
Patients with c-collars placed were 1.8 times more likely to have dysphagia than patients without c-collars placed, even after adjustment for age, ISS, and GCS (Table 3 ). After adjustment for ISS, GCS, dysphagia , cerebral edema, and having both a TBI and a cervical spine injury, patients with c-collars placed were 2.1 times more likely to experience respiratory failure than patients who did not have c-collars placed. Having a c-collar placed did not significantly increase the odds for aspiration or pneumonia , before or after adjustment.
Table 3. -
Logistic Regression Models Examining the Effect of C-collar Placement on Outcomes
Outcome-adjusted covariates
Unadjusted OR (CI)
Adjusted OR (CI)
Swallow therapy for dysphagia
1.8 (1.2, 2.6)
1.8 (1.2, 2.6)
Age
1.7 (1.2, 2.4)
ISS
1.7 (1.3, 2.4)
GCS
1.9 (1.3, 2.7)
Aspiration
1.8 (0.9, 3.8)
1.5 (0.7, 3.2)
ISS
2.3 (1.1, 5.2)
Swallow therapy
4.9 (2.1, 11.5)
Pneumonia
0.9 (0.3, 2.5)
0.5 (0.2, 1.4)
GCS
3.1 (1.3, 7.0)
Swallow therapy
3.9 (1.5, 10.2)
TBI and cervical spine injury
4.9 (1.9, 12.8)
Respiratory failure
2.8 (1.6, 4.8)
2.1 (1.1, 4.0)
ISS
2.9 (1.5, 5.9)
GCS
4.7 (2.5, 8.6)
Swallow therapy
2.0 (1.1, 3.8)
Cerebral edema
10.0 (2.5, 39.7)
TBI and cervical spine injury
5.2 (2.6, 10.5)
Bold denotes statistical significance. Continuous variables were dichotomized for the model based on the overall central tendency: age comparisons were >80 versus ≤80 years old, ISS comparisons were >10 versus ≤10, and GCS comparisons were <15 versus 15.
CI = confidence interval; GCS = Glasgow Coma Scale; ISS = injury severity score; OR = odds ratio; TBI = traumatic brain injury.
Outcomes Stratified by Receipt of Swallow Therapy
When examining only patients who did not receive swallow therapy, not only were patients with a c-collar significantly more likely to have respiratory failure (p < .0001), but they were also significantly more likely to have aspiration (p = .02), Figure 1 . Pneumonia was trending toward being significantly more common among those with a c-collar placed who did not receive swallow therapy but did not reach statistical significance (p = .07). Alternatively, among only patients who did receive swallow therapy, there were no differences in the proportion of patients with aspiration (p = .87), pneumonia (p = .09), or respiratory failure (p = .30) by c-collar placement.
Figure 1.: Outcomes stratified by receiving swallow therapy.
Figure 1 displays the proportion of patients with the following outcomes: pneumonia , respiratory failure , and aspiration , stratified by the receipt of swallow therapy. The left side of the figure (first 6 bars) represents patients who were not treated with swallow therapy and the right side of the figure (second 6 bars) represents patients who did receive swallow therapy. The dark grey bars represent patients who had a c-collar placed, whereas the light grey bars represent patients who did not have a c-collar placed. Patterned bars indicate that the outcome was significantly different by c-collar placement.
Limitations
This was a single-center retrospective study with rare outcomes. The results could be confounded by additional characteristics that were not evaluated such as c-collar type, duration of c-collar application, or other comorbidities. Future studies should determine if protocolized swallow examinations before food introduction for all TBI and cervical spine injury patients with c-collars decrease the risk for complications.
Discussion
Across all patients admitted with TBIs or cervical spine injuries, it was observed that c-collars significantly increased the odds of dysphagia and for respiratory failure . However, in this study there was evidence that the effect of c-collar placement was modified by receipt of swallow therapy. Among patients who did not receive swallow therapy, those with a c-collar placed were at an increased risk of not only respiratory failure but also for aspiration . Whereas, among those who did receive swallow therapy, there was no difference in any outcome at all by c-collar placement. This suggests that swallow therapy had a protective effect on the development of complications while masking the effect of c-collars on development of aspiration . Additionally, patients with dysphagia were significantly more likely to have pneumonia , aspiration , and respiratory failure than patients without dysphagia ; thus, using a dysphagia screening protocol could potentially reduce the risk for these complications.
This is the first study, to our knowledge, to indicate that c-collars increased the risk for dysphagia . Previous studies have demonstrated that c-collars restrict movement during swallowing, which could explain this observation.8,9,14 In fact, Stambolis et al. demonstrated that c-collars caused mechanical changes in swallowing patterns for healthy adults, providing evidence that the effect of c-collars on swallowing is differentiated from the effect of the clinical diagnoses associated with c-collar application on dysphagia .9 One study reported that decreased oral health hygiene among patients with brain injuries increased the risk for dysphagia , which could also be a factor in this study.15 Unusual anatomical variations may play a role in developing dysphagia after c-collar application.14 In a case study of a patient with a prominent laryngeal who developed dysphagia , the c-collar did not fit properly, but once removed, the patient was able to swallow normally again.14 Although anatomical variations were not collected, the likelihood of dysphagia was significantly 80% higher for patients with a c-collar placed than patients without a c-collar placed.
In addition to observing dysphagia was more common among patients with a c-collar placed, receipt of swallow therapy hid the effect of c-collar placement on the development of aspiration . This discovery indicates that TBI and cervical spine patients with a c-collar placed should be screened for dysphagia with the Yale Swallow Protocol because the Yale Swallow Protocol recommends those considered at risk for aspiration be screened for dysphagia .13 Although the data showed that aspiration was more common among patients with a c-collar placed who did not receive swallow therapy, a previous study found that c-collar application did not significantly increase the risk for aspiration .9 This could be because they only tested for aspiration in healthy adults on a single examination day, whereas the injury diagnoses, age, and length of time with a c-collar applied may also contribute to the risk for aspiration .9,16 In fact, the European Society for Swallowing Disorders reported that silent aspiration is more common among healthy older adults due to prolonged oropharyngeal phasing, a delay in triggering the pharyngeal swallow response, and increased pharynx residue, which could be exacerbated by c-collars.17 Bhattacharya et al.18 also found that c-collars did not increase the risk for aspiration ; however, their study had a small sample size (n = 22), without statistical testing, and the Yale Swallow Protocol was used before introducing foods, which could dramatically affect their results. In this study, receiving swallow therapy protected patients against developing aspiration .
Nakanishi et al.16 did not examine aspiration as an outcome but found that the duration of c-collar application significantly increased the risk of pneumonia in geriatric patients with cervical vertebrae injuries. Pneumonia was rare (3.6%) in this population, and even more rare was the combination of pneumonia and aspiration (1.4%). Although there was no difference in pneumonia by c-collar placement, in the stratified analysis (Figure 1 ) it can be seen how when the effect of swallow therapy is removed, the rate of pneumonia is higher among patients with a c-collar placed. However, it was observed that patients who had dysphagia (regardless of c-collar status) were significantly more likely to develop pneumonia . Hansen et al. identified GCS and the Rancho Los Amigos Scale as risk factors for pneumonia among severe TBI patients but did not examine c-collar placement as a predictor.2 They suggest that a reduction of consciousness leads to relaxation of muscles in the larynx and thereby reduces airway closure, but it has been observed that c-collars reduced the diameter of the oropharyngeal airway and increased the presence of pharyngeal residue, factors that could contribute to pneumonia .2,9
Another novel finding in this population was the effect of c-collar placement on respiratory failure . One study reported that respiratory failure was the most common cause of death among geriatric patients with cervical spine fractures who were most often treated with rigid collars or halo braces.19 But the authors did not stratify the results by c-collar application; therefore, it is unclear specifically how c-collar placement affected the risk of respiratory failure .19 Ala et al.20 reported that c-collar application in trauma patients significantly decreased lung capacity and spirometry parameters and suggested early removal of c-collars for patients with underlying lung diseases. Dysphagia screening followed by swallow therapy if needed may reduce the risk for respiratory failure as seen in this study.
Receipt of swallow therapy (Figure 1 ) among patients with c-collars had a protective effect against development of pneumonia , respiratory failure , and aspiration . Thus, early identification and management of dysphagia may reduce the risk for these complications. Bhattacharya et al. conducted a study on the use of c-collars among trauma patients and similarly concluded that foods and liquids should not be reintroduced until after patients with c-collars pass a swallow screening or dysphagia testing and are medically and neurologically stable.18 In 2016, Lee et al. reported that dysphagia characteristics in TBI patients are similar to those in stroke patients and concluded that the therapeutic approaches for dysphagia in stroke patients may be applied to TBI patients, but this approach has yet to be widely adapted.5,10 Due to the findings of this study, a dysphagia screening protocol with subsequent swallow therapy, if indicated, was implemented for patients with c-collars before reintroduction of foods and liquids. Future studies evaluating the efficacy of dysphagia screening protocols in a population of TBIs and cervical spine injury patients with c-collars are needed to confirm these findings.
Conclusions
In this study of patients with TBIs or cervical spine injuries, c-collar placement increased the odds for respiratory failure and dysphagia . There was evidence that the effect of c-collar placement was modified by receipt of swallow therapy. When removing the effect of swallow therapy, c-collar placement also increased the risk for aspiration . Regardless of c-collar status, patients who had dysphagia were at an increased risk for pneumonia , aspiration , and respiratory failure .
Implications
This novel finding indicates that TBI or cervical spine injury patients with c-collars placed should be screened for dysphagia per the Yale Swallow Protocol. Swallow therapy had a protective effect on development of pneumonia , aspiration , and respiratory failure among patients with c-collars placed. Because those with dysphagia were at an increased risk of subsequent complications, dysphagia screening and swallow therapy may improve diagnosis rates and lead to a reduction in complications.
Authors' Biographies
Stephanie Jarvis, MPH , is an epidemiologist based in Denver, CO with the Injury Outcomes Network (ION) research team based. Her current role is to lead research projects through protocol development, analysis, abstract, and manuscript drafting.
Alexandre Sater, BS , is a recent graduate of Biology based in Parker, CO. His current research role is data collection, study design, and critical review of abstracts and manuscripts prepared.
Jeffrey Gordon, MD , is a resident at Swedish Medical Center based in Englewood, CO. His current research role is data collection, study design, and critical review of abstracts and manuscripts prepared. He also has presented this study at the American Association for the Surgery of Trauma and the Surgical Infection Society conferences.
Allan Nguyen, MD , is a resident at Swedish Medical Center based in Englewood, CO. His current research role is data collection, study design, and critical review of abstracts and manuscripts prepared. He assisted with starting up this quality improvement project.
Kaysie Banton, MD , is the Trauma Medical Director at Swedish Medical Center in Englewood, CO. Her current role in research is to oversee research conduct within Swedish Medical Center, to assist residents with research, and to assist with study design and critical review of abstracts and manuscripts prepared. She also directs changes to care based on quality improvement project or study results.
David Bar-Or, MD , is the Director of ION Research in Englewood, CO. He oversees all studies conducted by ION research and is involved with every aspect of the ION Research team studies from study hypothesis generation, protocol development, to drafting and reviewing articles. Dr. Bar-Or is also an adjunct professor at Kansas City University and Rocky Vista University.
Acknowledgments
The authors would like to thank their Clinical Research Coordinator Breanna Nickels, their Project Manager Diane Redmond, their IRB coordinator Tina Thompson, and their senior epidemiologist Kristin Salottolo for their assistance with this project.
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