Introduction

Hospital-acquired pneumonia is the second most common nosocomial infection in critically ill patients and is associated with increased mortality, morbidity and cost of care. Incidence of hospital acquired pneumonia in critically ill patients generally ranges from 9 to 20% [1]. Critically ill patients frequently require prolonged intubation and ventilator support. Swallowing dysfunction and pulmonary aspiration often occur in patients who receive prolonged mechanical ventilation [2,3,4,5].

Aspiration pneumonia can occur for various reasons, several studies have shown a significant association between dysphagia and aspiration pneumonia [6,7,8]. Several mechanisms for this problem include disuse atrophy of muscles during intubation, suppression of cough reflexes, inconsistent triggering of swallowing reflex, diminished proprioception, and residual effect of sedatives [6, 9].

Evidence suggests that intubation for more than 48 h can cause transient injury to the larynx with a subsequent reduction in protective mechanisms and increased oropharyngeal secretions once patient is extubated. The presence of orotracheal tube has been shown to alter the mechanoceptors and chemoreceptors of pharyngeal mucosa, causing dysfunction of swallowing reflex. The prevalence of swallowing dysfunction post-extubation has been reported to occur in 20 and 83% of those patients intubated longer than 48 h [2].

FEES is a procedure where fiberoptic endoscope is passed through nose to visualize the larynx, pharynx and the patient is asked to swallow a food bolus. It can achieve a complete assessment of the pharyngeal stage of swallowing. It includes five components: assessment of structural changes in the larynx and pharynx, assessment of movement and sensation, assessment of secretions management, direct visualization of swallowing function for food and liquid, and response to therapeutic interventions.

Several studies have evaluated orotracheal intubation as an isolated factor for the development of dysphagia, some authors [2,3,4,5] include neurological patients in their studies, disregarding the consequences that may be related to the patient’s own neurological problem.

Objective of our study was to evaluate critically ill patients who were intubated for causes other than neurological and try to define the exact impact of intubation on swallowing using FEES as diagnostic and therapeutic tool.

Materials and Methods

All adult ICU patients who were intubated for ≥ 48 h were included in the study. Head injury patients, patients with abnormal neurological status, completely disoriented patients were excluded from the study.

Patients were assessed for swallowing either in ENT department or bed side, in Intensive Care Unit (ICU) using FEES.

Patients were examined in supine position with the head of bed elevated to approximately 70° with the bend of the bed at the patient’s lower back and in patients who are able to sit on a chair during the procedure; it was performed in sitting position. A fibreoptic laryngoscope was passed trans-nasally to the oropharynx, where the larynx and surrounding structures visualized.

Patients were led through various tasks to evaluate the anatomical changes in the larynx, sensory and motor status of the pharyngeal and laryngeal swallow mechanism. Stained liquid and semi-liquid/semisolid boluses were then given to determine the integrity of pharyngeal deglutition. The interior of the larynx and airway was examined for evidence of food penetration i,e when food particle is within the laryngeal vestibule Fig. 1 and aspiration, when food particle enters below the true vocal folds before and after each swallow was noted. Patient who aspirated with cough reflex was labeled aspirator and without cough reflex as silent aspirator. Patients who had aspiration or silent aspiration were given swallowing therapy by speech and swallowing Pathologist. Those patients who had aspiration were reassessed after 5–7 days of swallow therapy to note any improvement in their swallowing. Patients who did not show any aspiration were started on oral feeds after the test.

Fig. 1
figure 1

FEES showing residue of semisolid (porridge) Bolus I,e penetration

Results

In the study period of 1 year we performed FEES in 41 ICU patients who were intubated for minimum of 48 h; we excluded patients who were intubated for neurological causes and head injury. Our study population included patients in the age range of 18–74 years.

Our patient population was heterogeneous with diseases ranging from infectious disease, hanging, diabetic ketoacidosis, trauma etc. Important feature of our study was lack of confounding factors as we excluded patients with head injury, chronic neurological disorders and patients who were totally disoriented. Duration of intubation was in the range of 2–9 days, Most of the patients were intubated for 6 days.

19 (46.3%) patients had abnormal laryngeal findings and normal laryngeal findings were seen in 22 (53.7%). Types of laryngeal injury observed are mentioned in Table 1. Of 41 patients studied 12 had congested vocal cords, 4 had congested arytenoids, 3 had arytenoids ulcers, 3 had left vocal cord palsy, 1 had bilateral restricted vocal cord movements, left arytenoids prolapsed, epiglottic edema.

Table 1 Type of laryngeal injury

Of 41 patients 6(14.6%) had aspiration both for liquids and semisolids and only one had aspiration for liquid but not for semisolid feed. All patients who aspirated had some laryngeal injury.

In 6 patients who had aspiration initially as diagnosed with FEES, swallowing function recovered fully as found during repeat FEES which was done after swallow therapy on 5th–7th day.

There was no correlation between age of patient (≤ 40 years) and laryngeal abnormality (p = 0.278) or occurrence of aspiration (p = 1.0). There was no significant association between gender of patient and laryngeal abnormality (p = 0.79) or occurrence of aspiration (p = 0.662).

There was no significant association between duration of intubation and occurrence of aspiration (p = 1.00).

Laryngeal Abnormality was just significant for duration of intubation more than/equal to 5 days and occurrence of aspiration (p = 0.053). Only patients with abnormal laryngeal finding showed aspiration on FEES. Among patients with Normal Laryngeal finding none experienced aspiration. Among patients with Abnormal laryngeal findings, 6 (31.6%) experienced aspiration and 13 (68.4%) had no aspiration. The correlation was statistically significant (p = 0.006).

Discussion

Swallowing is a complex process that needs coordination of over 25 pairs of muscles in oral cavity, pharynx, larynx and esophagus [10]. Neural control of swallowing, which has both voluntary and involuntary components is mediated by interactions between cortical centres in both hemispheres, the “swallowing center” within the brainstem, cranial nerves (V, VII, IX sensory, IX motor, X and XII), and pharyngeal receptors (touch, pressure, chemical stimulus, and water [11].

Videofluroscopy was traditionally considered as a gold standard for diagnosis of oropharyngeal dysphagia as it provides comprehensive information of swallowing and also to assess therapeutic efficacy. However limitations of the procedure including accessibility, need of radiation and radiologist with fluoroscopy machine. This is particularly of concern to evaluate dysphagia in critically ill patients who are bedridden.

FEES has evolved over time as an alternative to videofluoroscopy especially when evaluation has to be done bedside. It is a safe and effective diagnostic tool in swallowing evaluation and helps in swallowing therapy as a visual display to help patients learn various swallowing maneuvers [2, 12, 13]. It can be used in a wide variety of settings including office evaluation, inpatients and ICU settings [13].

The reports of dysphagia associated with a neurological injury are common [2, 14,15,16]. Several diseases of neurological origin can affect the neuronal structures controlling the complex mechanisms of oropharyngeal swallowing. According to León and Clavé [14], more than 30% of patients who suffered a stroke, 52–82% of patients with Parkinson disease, 100% of patients with amyotrophic lateral sclerosis, 44% of patients with multiple sclerosis, 84% of patients with Alzheimer’s disease and more than 60% of institutionalized elderly patients present oropharyngeal dysphagia.

A study by Aviv et al. on laryngopharyngeal sensitivity in stroke patients showed that there was a significant impairment of laryngopharyngeal sensitivity which may attribute to dysphagia and aspiration [17]. Incidence of dysphagia in stroke patient varies from 25% [18] to 67% [19]. Gerf Hafner et al., included tracheostomy patients (46%) in their study; found aspiration in 69.3% of their study population. Majority of patients who had aspiration had indwelling tracheostomy tube (50.8%) in contrast to those who were intubated with endotracheal tube (48%). Incidence of silent aspiration was also high in tracheostomy patients (36.8%) as against (17%).

Disregarding these findings and evaluating orotracheal intubation as an isolated factor for the development of dysphagia, some authors [4, 17, 20] include neurological patients in their studies, correlating the presence of dysphagia resulting from the use of endotracheal tubes and ignoring the consequences that may be related to the patient’s own neurological status.

Aiming to clarify this point of view, our purpose was to study the swallowing abnormality in extubated patients without any kind of brain damage and who were not tracheostomized.

According to a study by Bordan et al. [21] there was increase of 14% chances of aspiration with everyday increase in duration of intubation. According to another study by Brown et al. [22], there was a significant increase in risk of post extubation dysphagia by 73% for duration of more than 72 h of intubation when compared to those intubated for less than 72 h (23%) [22]. Our study did not show any significant association between duration of intubation and occurrence of aspiration.

According to a study by Postma et al. [23], prevalence of abnormal laryngopharyngeal findings was 79% following extubation, findings included arytenoids edema (33%), granuloma (31%), vocal cord palsy (24%), mucosal lesions (17%), vocal fold bowing (14%), diffuse edema (11%), airway stenosis (3%) and ulcer (6%).

A study by Perie et al. showed that aspiration occurs in patients with unilateral recurrent laryngeal nerve palsy [24], this explains our study where 3 patients who had unilateral vocal cord palsy also aspirated. Study by Leder et al. also showed that majority of patients with traumatic intubation suffered from aspiration [3]. This explains our study where all patients who aspirated had some form of laryngeal injury.

Our experience suggests that FEES can be employed as a useful diagnostic tool in ICU patients to assess aspiration because of its feasibility and portability. Given the high likelihood of serious medical complications of dysphagia, particularly pneumonia, we recommend that swallowing assessments should be conducted on patients undergoing prolonged intubation durations. Increasing awareness among intensivist and medical personnel handling endotracheal tubes about laryngeal injury secondary to intubation by ensuring Smooth intubation and handling of endotracheal tubes.

Conclusions

41 patients were evaluated by FEES; 6 (14%) had aspiration and 19 (46%) had post intubation trauma. There was a statistically significant association between laryngeal injury and occurrence of aspiration. All patients who had aspiration responded to swallowing therapy and on repeat FEES had no aspiration after 5–7 days. There was no significant association between duration of intubation and occurrence of aspiration. There was no significant association between age and occurrence of aspiration.