Archives of Physical Medicine and Rehabilitation
Volume 89, Issue 11 , Pages 2114-2120, November 2008

The Association of Functional Oral Intake and Pneumonia in Patients With Severe Traumatic Brain Injury

  • Trine S. Hansen, MPH

      Affiliations

    • Department of Neurorehabilitation, Brain Injury Unit, Copenhagen University Hospital Hvidovre, Hvidovre, Denmark
    • Department of Occupational Therapy, Copenhagen University Hospital Hvidovre, Hvidovre, Denmark
    • Corresponding Author InformationReprint requests to Trine S. Hansen, MPH, Dept of Neurorehabilitation 354, Hvidovre Hospital, Kettegaard Allé 30, DK-2650 Hvidovre, Denmark
    • ,
  • Klaus Larsen, PhD

      Affiliations

    • Clinical Research Unit, Copenhagen University Hospital Hvidovre, Hvidovre, Denmark
    • ,
  • Aase W. Engberg, DMSc

      Affiliations

    • Department of Neurorehabilitation, Brain Injury Unit, Copenhagen University Hospital Hvidovre, Hvidovre, Denmark

Article Outline

Abstract 

Hansen TS, Larsen K, Engberg AW. The association of functional oral intake and pneumonia in patients with severe traumatic brain injury.

Objectives

To investigate the incidence and onset time of pneumonia for patients with severe traumatic brain injury (TBI) in the early phase of rehabilitation and to identify parameters associated with the risk of pneumonia.

Design

Observational retrospective cohort study.

Setting

Subacute rehabilitation department in a university hospital in Denmark.

Participants

Patients (N=173) aged 16 to 65 years with severe TBI who were admitted during a 5-year period. Patients are transferred to the brain injury unit as soon as they ventilate spontaneously.

Interventions

Not applicable.

Main Outcome Measure

Pneumonia.

Results

Twenty-seven percent of the patients admitted to the brain injury unit were in treatment for pneumonia; pneumonia developed in 12% of the patients during rehabilitation; the condition occurred within 19 days of admission in all but 1 patient. Of these patients, 81% received nothing by mouth. Three factors identified patients at highest risk of pneumonia: Glasgow Coma Scale score less than 9 (1 day after cessation of sedation); Rancho Los Amigos Scale score less than 3 (on admission); and no oral intake on admission. Having a tracheotomy tube and/or feeding tube was also associated with a higher occurrence of pneumonia.

Conclusions

Among patients with severe TBI, 27% had pneumonia at transfer from the intensive care unit. Pneumonia developed in only 12% of the participants during rehabilitation. Patients with a low level of consciousness and patients with a tracheotomy tube or feeding tube had a higher likelihood of pneumonia.

Key Words: Brain injuries, Deglutition disorders, Pneumonia, Rehabilitation

List of Abbreviations: CRP, C-reactive protein, FOIS, Functional Oral Intake Scale, GCS, Glasgow Coma Scale, ICU, intensive care unit, IQR, interquartile range, LES, lower esophageal sphincter, LOS, length of stay, PEG, percutaneous endoscopic gastrostomy, PTA, posttraumatic amnesia, RLAS, Rancho Los Amigos Scale, TBI, traumatic brain injury

 

PATIENTS WITH TBI are at risk of developing problems with swallowing, eating, and drinking.1, 2 In recent years, the number of intensive specialized rehabilitation units for patients with TBI has increased, and positive effects of intensive interdisciplinary rehabilitation have been reported.3, 4, 5 Problems with eating and drinking—with an incidence as high as 93%6 in patients with severe TBI—have been found and can be potentially life-threatening by leading to malnutrition, dehydration, aspiration pneumonia,7 and prolonged length of hospital stay.8 Several risk factors for aspiration pneumonia have been reported, such as endotracheal intubation, mechanical ventilation, poor oral hygiene,9 oral feeding (if the patients aspirate food or liquid),8, 10, 11 and food supplementation (PEG or nasogastric tube).12

Patients with TBI admitted to an ICU are at high risk of contracting pneumonia.8 In this early stage of recovery, pneumonia is found to occur within an average of 3 days of hospitalization13 and is associated with severity of trauma.8, 14 When patients transfer to subacute rehabilitation, they often begin to be more active, and adequate nutrition is important,15 either orally or by a supplemental tube feeding. At this stage of rehabilitation, some patients are supported with a tracheotomy tube and/or feeding tube; many have a low level of consciousness.3 In this early phase of rehabilitation, several patient care issues become important, such as monitoring for clinical signs of aspiration, maintaining good oral hygiene, minimizing risk of reflux, managing secretions, providing tube feeding (when relevant), carefully managing tracheotomy tube (when relevant), and carefully managing initiation of oral feeding.16

Previous research of TBI and pneumonia often has been done during acute stages in the ICU or in neurosurgery clinics.8, 17, 18, 19, 20 At our brain injury unit, patients with severe TBI are admitted to subacute intensive rehabilitation as soon as they ventilate spontaneously. Eighty percent of the patients are transferred directly from the neurosurgical wards.3

To learn more about how to prevent pneumonia in this high-risk patient group, we investigated the incidence and onset time of pneumonia and identified parameters associated with the risk of pneumonia in this early phase of rehabilitation.

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Methods 

This is a retrospective observational study using data collected from hospital records and chart reviews.

Participants 

In October 2000, the subacute rehabilitation of all severely injured patients with TBI in Denmark was centralized to 2 units, each with geographically defined uptake areas.

The present study includes patients from the uptake area of Copenhagen, which includes the eastern half of Denmark, Greenland, and the Faroe Islands, encompassing a total of 2.4 million inhabitants. All hospitals in the uptake area, and, in particular, the 2 neurosurgical clinics in the area, agreed to refer patients who fulfilled the following set criteria. Highest priority was given to patients who, after initial treatment in a neurosurgical or other clinic, had a GCS21 score in the range 3 through 12 one day after cessation of sedation and patients with a GCS of 13–14 one day after cessation of sedation if they have severe focal neurologic deficits and/or are severely agitated. All such survivors were transferred as soon as they ventilated spontaneously. The brain injury severity was confirmed by prospective assessment of the duration of the PTA period. All 177 patients, age 16 to 65 years, admitted during a 5-year period from October 2000 to December 2005 were evaluated for eligibility. We excluded patients on the basis of previously known swallowing problems due to neurologic diseases or other diagnoses. Four patients met this criterion and 173 patients were included in the study. Patients older than 65 years were excluded because swallowing function can be diminished in older age groups of otherwise healthy people.22

According to the rehabilitation program of the brain injury unit,3 all patients were enrolled in an extensive around-the-clock rehabilitation program by interdisciplinary teams starting on the day of admission. Functional rehabilitation was based on the principles developed by Affolter and Stricker,23 Davies,24 and Coombes.25, 26 The program emphasizes sensory stimulation, facilitation of normative movements, and daily activities, even for patients in a vegetative state. Patients were discharged when they were: able to go home, able to continue the rehabilitation in a local and less intensive setting, or referred to a nursing home if no progress was made for a 3-month period.3

Swallowing Therapy and Oral Hygiene 

Examination of the mouth and a clinical evaluation of swallowing were done for all patients on the day of admission, in line with the treatment guidelines for facial oral tract therapy.25, 26 Facial oral tract therapy was developed by speech and language therapist Kay Coombes and provides a structured way to assess and treat disturbances in facial expression, movement of the jaw for eating and articulation, breathing, swallowing, and voice.25, 26 Treatment methods include slow, organized touch of the patient's hands, facilitating hand-to-hand and hand-to-face contact, along with specific oral stimulation, therapeutic oral hygiene routines, and facilitation of swallowing. Facial oral tract therapy does not require that the patients are capable of following verbal instructions. Therefore, patients with a low level of consciousness also receive facial oral tract therapy. All patients who experienced problems with oral intake, oral hygiene, breathing, and communication were enrolled in a treatment program according to facial oral tract therapy.

Patients who experienced problems with oral hygiene were treated both by the occupational therapist and caregivers. They facilitate participation in brushing teeth and cleaning the mouth. Patients who were not eating by mouth also received oral stimulation to maintain sensory input and prevent deprivation. To prevent pneumonia in patients fed exclusively by feeding tube, the patients were mobilized several times a day. In bed the patients were positioned in a 30° side-lying position (if tolerated). Supine position was avoided if possible. If the patient lay supine, the head of the bed was elevated and caregivers and therapists carefully monitored oral hygiene and accumulated secretions in the oral cavity. At our brain injury unit, a patient with a feeding tube is given bolus feedings if tolerated. Continuous feedings are given to patients with a low level of consciousness and/or patients who do not tolerate bolus feeding. All feeding begins with aspiration of the ventricle, and if more than 100mL material rests in the ventricle, clinicians caring for the patient stop the tube feeding and wait at least 1 hour before feeding is resumed. A feeding pump connected to the feeding tube monitors the feeding.

Dependent Variables 

Pneumonia, an inflammation in the lung parenchyma, is defined as follows in our hospital: (1) appearance of new infiltrative changes on chest radiograph that can be explained by pneumonia and/or (2) increase in temperature to more than 38.5°C with an increase in CRP to more than 50mg/L and leukocyte count more than 9 cells/L, accompanied by respiratory symptoms such as dyspnea, coughing, and/or purulent expectoration.27 If these criteria were absent or not documented, the diagnosis was not acknowledged and used in this study. If the same patient was diagnosed with pneumonia several times, all episodes were noted. For patients who showed signs of pneumonia as previously defined, the laboratory clinicians at the hospital routinely examined bacteria in tracheal secretions.

Independent Variables 

GCS,21 which consists of values from 3 to 15, was measured 1 day after cessation of sedation. Patients with scores less than 9 are considered to be in coma, and patients with scores of 15 are able to follow commands, are fully oriented, and have spontaneous eye opening. Time in acute care (time from injury until admission to subacute rehabilitation brain injury unit), FIM instrument28 scores (range 18 [lowest]–126 [highest]) of level of independence, and RLAS29 scores (range 1 [no response]–8 [purposeful and appropriate response]) were all measured at admission. FOIS was assessed retrospectively based on a chart review.6 The scale consists of 7 levels. Levels 1 through 3 relate to varying degrees of nonoral feeding, and levels 4 through 7 relate to varying degrees of oral feeding without nonoral supplementation.30 LOS corresponds to time from admission to discharge from subacute rehabilitation brain injury unit. Duration of PTA31 was prospectively assessed by neuropsychologists by means of the Galveston Orientation and Amnesia Test.

Statistical Analyses 

All data were analyzed using SPSSa package for Windows.

We described patient demographic variables by median, IQR, minimum, and maximum values for continuous variables and by number and percentage for categorical variables.

We used a Kaplan-Meier plot to estimate the time from admission to occurrence of pneumonia and the risk of contracting pneumonia and log-rank test to calculate the risk difference between patients grouped by severity of brain injury. If a patient did not contract pneumonia he/she was censored at the time of discharge in the analysis. We estimated the size of difference by a univariate Cox proportional hazards model, and analyzed covariates that changed over time using a time-dependent covariate Cox proportional hazards model.

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Results 

Demographic Data 

Patients had a median age of 35 years (IQR, 24–51y). Median GCS score measured 1 day after cessation of sedation was 11 (IQR, 9–13). For 81% of the patients, PTA duration exceeded 4 weeks. At admission to the brain injury unit, median FIM score was 18.5 (IQR, 18–38.5). Median time in acute care was 15 days (10–24) and LOS at brain injury unit 86 days (53.5–163.5d), respectively. Ninety-three percent had some degree of problems with oral intake at admission to brain injury unit (FOIS score <7). Sixty-eight percent of patients were admitted with a feeding tube, and 21% with a tracheotomy tube. Forty-five percent of patients had a prolonged problem with eating and drinking and received a PEG tube during their rehabilitation at the brain injury unit.

Pneumonia 

Incidences of pneumonia are presented in table 1.

Table 1. Incidence of Pneumonia
Incidencen%
No pneumonia10963
Pneumonia at admission4627
Pneumonia at BIU2112
No. of episodes of pneumonia
1127
253
342

Abbreviation: BIU, brain injury unit.

At the time that the patients were admitted to our brain injury unit, 46 (27%) were in treatment for pneumonia, and pneumonia developed in 21 (12%) at the unit. Results of the microbiologic investigations are shown in table 2 for 20 patients (data unavailable in 1 case). More than 1 species was found in secretions from 3 patients.

Table 2. Etiologic Agents From Tracheal Secretion in 20 Patients With Pneumonia
CocciCases%
Staphylococcus aureus420
Coagulase-negative staphylococci315
Gram-negative diplococci15
Gram-negative bacilli
Klebsiella species420
Pseudomonas aeruginosa315
Citrobacter species15
Enterobacter cloacae15
Haemophilus influenzae15
No growth630

Of the 21 patients, 2 (10%) had pneumonia at admission, pneumonia developed once in 12 (57%), 5 (24%) had 2 episodes of pneumonia, and 4 (19%) had 3 episodes of pneumonia. Onset time of the first episode of pneumonia ranged from 1 day to 19 days after admission for all patients, except one in whom pneumonia developed after 71 days and who died after 86 days. Because this time interval differs greatly relative to the others, this patient was excluded as an outlier. In the following results, we focus only on the time until the first episode of pneumonia.

We found that 17 (81%) of the 21 patients who had pneumonia in the brain injury unit were totally dependent on tube feeding and received nothing by mouth (FOIS score of 1), 3 patients developed pneumonia when they were given minimal attempts of food and/or liquid by mouth but were still dependent on tube feeding (FOIS score range, 2–3), and pneumonia developed in 1 patient when he had a total oral diet but still needed special preparation or compensation (FOIS score of 5).

In figure 1, the Kaplan-Meier plot shows the risk of pneumonia as a function of time within the first 3 weeks after admission. The 5-day, 10-day, and 15-day rates were estimated at 6%, 8%, and 11%, respectively. After 19 days, pneumonia did not develop for the first time in any more patients. At this time the risk of pneumonia was 12%.

Kaplan-Meier plots estimating the risk that pneumonia will develop in patients in the brain injury unit, grouped by severity of brain injury, are shown in figure 2. We found that patients admitted with a low GCS score (<9) had a higher risk (25%) of pneumonia developing compared with a risk of 13% among patients with a moderate risk (GCS score range, 9–12), and a risk of 2% among those with a high GCS score (>12). Pneumonia did not develop in most patients with an RLAS score of 3 or more (ie, able to obey commands), whereas pneumonia developed shortly after admission (within the range of 1–9 days) in 23% of the patients with a lower RLAS score. Patients with an FOIS score of 1 had a 12% risk of pneumonia, patients with FOIS score of 2 or 3 had a 7% risk, and patients with an FOIS score of 4 or more had only a 1% risk of pneumonia.

  • View full-size image.
  • Fig 2. 

    Kaplan-Meier plots showing the estimated risks of pneumonia by parameters of severity of head injury, functional oral intake at admission, and time in acute care.

Log-rank test showed that differences in risk of pneumonia among groups was statistically significant (P<.01) for GCS score, RLAS score, and FOIS score. Pneumonia developed in 18% of the patients admitted with low functional ability (FIM score <19), whereas patients with a high FIM score (>55) had only a 7% risk. Patients in acute care more than 24 days had a 12% risk whereas patients in acute care fewer than 7 days had only a 4% risk of pneumonia. However, there is no statistical evidence showing that the risks between the groups in FIM score and time in acute care differ (P>.05). Results from the Cox proportional hazards model are presented in table 3.

Table 3. Association Between Risk of Pneumonia and Severity of Brain Injury, Functional Oral Intake at Admission, and Time in Acute Care
ScalesWald χ2P⁎Hazard Ratio95% CI
GCS10.81<.01
<9(ref) 1.00
9–12 .030.320.11–0.92
>12 <.010.050.05–0.29
RLAS13.76<.01
≤2(ref) 1.00
3 .010.130.03–0.61
4 .020.160.03–0.77
≥5 <.010.070.01–0.55
Time in acute care (d)3.44.33
>24(ref) 1.00
16–24 .531.710.55–5.34
10–15 .701.280.37–4.45
<10 .290.410.08–2.12
FIM3.24.36
<19(ref) 1.00
19–36 .210.440.12–1.16
37–54 .940.000.00–0.00
>55 .140.320.07–1.44
FOIS9.30<.01
1(ref) 1.00
2–3 .160.350.08–1.53
≥4 .010.060.01–0.42

NOTE. All analysis adjusted for age and sex; time in acute care GCS score measured 1 day after cessation of sedation; multiple Cox regression hazard model.

Abbreviation: CI, confidence interval.

⁎Significant at P<.05.

We found a strong association between GCS score (Wald χ2=10.81, P<.01), RLAS score (Wald χ2=13.76, P<.01), and FOIS score (Wald χ2=9.3, P<.01). Again, there was no statistically significant association between time in acute care and FIM.

Table 4 shows results from the time-dependent covariate model. We found a higher incidence of pneumonia in patients with tube feeding (Wald χ2=8.99, P=.01) and for patients with a tracheotomy tube (Wald χ2=6.94, P=.01).

Table 4. Relationship Between Feeding Tube and Tracheostomy Tube on Incidence of Pneumonia
TubeWald χ2P⁎Hazard Ratio95% CI
Feeding8.99.01
No feeding tube (ref) 1.00
Nasogastric .0118.852.46–144.48
PEG tube .087.450.77–72.50
Tracheotomy6.94.01
No tracheostomy (ref) 1.00
Tracheostomy .013.551.38–9.10

NOTE. Cox proportional hazard regression model with time-dependent covariates.

Abbreviation: CI, confidence interval.

⁎Significant at P<.05.

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Discussion 

We retrospectively summed episodes of pneumonia in a 5-year period in a subacute rehabilitation department for patients with severe TBI. Brain injury has already been documented to be associated with a risk of pneumonia.32 In this study, we evaluated the incidence and risk factors of pneumonia in the early phase of rehabilitation for patients with severe TBI. We found that 12% of the patients developed pneumonia one time during hospitalization in a subacute specialized rehabilitation unit, and that pneumonia developed in all except one patient within 19 days after admission. GCS and RLAS scores were associated with risk of pneumonia. This is in agreement with findings from other studies.8, 14, 33, 34, 35 Explanatory factors could be that reduction of consciousness leads to relaxation of muscles in the larynx and thereby reduces airway closure,34 supported by Huxley et al,34 who reported that 45% of healthy adults aspirated during sleep and 70% of patients with depressed consciousness aspirated. Moreover, Saxe et al36 found that low GCS scores are associated with lower tone in the LES.

Studies of patients with TBI in ICUs have described the incidence of pneumonia as high as 41% to 60%.8, 13, 14 Several special risk factors are related to pneumonia for patients in an ICU compared with patients in rehabilitation units. These factors include risk of aspiration in association with the trauma or accident,13 coma, and mechanical ventilation.37, 38, 39 However, the patients at the brain injury unit could also be at high risk due to the short time in acute care (mean, 15d). Even so, the incidence rate of pneumonia decreased to 12% in our brain injury unit compared with 27% at admission.

We found that 81% of the patients in whom pneumonia developed were fed exclusively by feeding tube. This result will not lead to advice against using feeding tubes because the only realistic alternative was intravenous nourishment. However, our results confirm that even if experienced staff takes precautions, a feeding tube does not eliminate the risk of aspiration. Our result leads to the conclusion that patients with a feeding tube either aspirate saliva, oral or laryngeal secretion, or regurgitate gastric content,40 supported by results from other studies investigating neurologic patient groups.41, 42 Dent et al43 found that gastroesophageal reflux is most frequent in the postprandial state and therefore more frequent in patients given continuous feeding instead of intermittent bolus feeding. Which method is preferable has been discussed in the literature35, 44, 45 but no consensus has been reached. Rhoney et al35 found that continuous enteral feeding was better tolerated in patients with acute brain injuries; however, for risk of pneumonia they only found evidence (P=.22) among nonventilated patients. On the contrary, Tejada Artigas et al45 found that continuous enteral feeding was a risk factor for nosocomial pneumonia in patients with trauma admitted to an ICU, supported by Jacobs et al44 in an earlier study with patients from an ICU. In our department, we give continuous feedings or very slow bolus feedings to patients with very low consciousness. One could hypothesize that a risk factor for pneumonia in our patients could be that mobilization of a patient with low tone in the LES with food in the stomach increases the risk of vomiting or reflux and thereby risk of aspiration. Cole et al41 found in a single case study that an infusion rate more than 50mL/h increased the risk of reflux and suggested that increased feeding volume further could lead to gastric retention and distension, resulting in relaxation of the LES and leading to reflux.41, 46 This was supported by the findings of Ahtaridis et al.46

Some patients with severe TBI produce more saliva and secretions, which, in combination with reduced swallowing rate, could lead to risk of pneumonia. Especially in patients with poor oral hygiene, aspiration of saliva, for which feeding tubes do not offer any protection, can lead to pneumonia.9, 47, 48, 49 Oral hygiene is a problem often not recognized in critically ill patients, including patients with TBI, and can become severe due to cognitive problems, hypersensitivity in the oral cavity, impaired saliva production, nonoral feeding, decreased mobility, drugs, and intubations.50, 51, 52

We also found that a tracheotomy tube in our patient group was associated with a higher risk of pneumonia, which supports results from other studies.53, 54, 55, 56, 57 A tracheotomy tube may be necessary for protection of the airway and protection of accumulated secretions, but it may also cause colonization of pathogens in the oropharynx,58 absence of expiratory airflow through the larynx,59 impaired laryngeal movement, loss of protective mechanisms such as vocal cord closure, and loss of laryngeal reflex,60, 61 all factors associated with aspiration. In addition, patients with severe TBI have weakened immune systems and therefore are at increased risk of inflammations.62 It is not in the nature of this study to evaluate the optimal time for removal of tracheotomy tube, but we can recommend close monitoring of patients with a tracheotomy tube to prevent pneumonia.

Our findings clearly indicate that low GCS scores and presence of a tracheotomy tube or feeding tube are associated with higher rate of pneumonia in patients with severe TBI. We do not, however, present evidence that these factors have a causal relationship with pneumonia. Presence of a tracheotomy tube or feeding tube could potentially contribute to causing pneumonia, but another viable explanation is severe dysphagia, which may be why these patients need to have a tracheotomy tube or feeding tube. The aspiration pneumonia could have been caused by the dysphagia, with the tracheotomy tube and feeding tube as epiphenomena having no role in pathogenesis of the pneumonia. This possibility can be addressed in future prospective studies.

Because oral hygiene could be a potential cause of pneumonia,9 we are now implementing a rating scale that makes it possible in future studies to address oral hygiene. Furthermore, we have started implementation of fiberoptic endoscopic evaluation of swallowing.

Study Limitations 

This study method is associated with some limitations. We could not document the diagnosed pneumonia as aspiration pneumonia. However, each episode of pneumonia was specified as aspiration pneumonia in the medical files, and the spectrum of bacteria is similar to findings from earlier published studies of aspiration pneumonia.63, 64

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Conclusions 

Among patients with severe TBI, 27% had pneumonia at the time of transfer from the ICU. Pneumonia developed in only 12% during subacute rehabilitation at our brain injury unit. Higher incidence of pneumonia was found in patients with low level of consciousness, tracheotomy, and exclusive tube-feeding. To prevent pneumonia, therapists and other health care professionals caring for patients with problems with oral intake should be aware of these parameters during rehabilitation.

Supplier

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Acknowledgments 

We thank the professionals in the interdisciplinary teams at the brain injury unit: occupational therapists, physiotherapists, neuropsychologists, nurses, speech therapists, and medical doctors for their contributions with data collection. We also thank the chief physician at brain injury unit for helping with the definition of pneumonia.

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  • a Version 13.0; SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.

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PII: S0003-9993(08)00531-5

doi:10.1016/j.apmr.2008.04.013

Archives of Physical Medicine and Rehabilitation
Volume 89, Issue 11 , Pages 2114-2120, November 2008

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