Oropharyngeal Dysphagia in Acute Cervical Spinal Cord Injury: A Literature Review

Temporary or permanent nerve damage related to the injury itself can directly contribute to dysphagia pathogenesis. Lower cranial nerves that play a key role in swallowing, glossopharyngeal (IX), vagus (X), and hypoglossal nerves (XII), are vulnerable to damage from cSCI due to compression of the brainstem [37]. Cervical spinal nerves also contribute to safe and efficient swallowing. The ansa cervicalis is a combination of fibers that include the hypoglossal and cervical spinal nerves (C1–C3)[38]. It provides motor innervation to the geniohyoid muscle as well as the strap muscles (omohyoid, sternohyoid, sternothyroid, thyrohyoid), which contribute to hyolaryngeal excursion and airway protection during swallowing [38]. In addition to neural impairments, anatomical alterations in the upper airway post injury can impair swallowing function. Patients with cervical kyphosis (i.e., abnormal curvature of the cervical spine) have been shown to have increased hypopharyngeal transit times and impaired airway protection [39]. The impact of atypical anatomy on swallowing function in patients with cSCI, who often have additional spinal fusion hardware and soft tissue thickening/edema, is not well documented but this is likely a contributor to dysphagia in this population [35].

The potential impact of operative approaches and techniques have been well described in a number of review papers over the last 10 years, including detailed recommendations to reduce the risk of postoperative dysphagia [16, 18]. The dC2–C7 angle is thought to play an important role in the development of dysphagia in both anterior and posterior cervical spine surgery [23]. Intra-operative measurement of the dC2–C7 angle is practical and essential in avoiding inadvertent postoperative swallowing difficulties. Complications related to cSCI surgery, such as compression in the cervical spine related to hardware placement, altered pharyngeal and spinal structure, and sensory impairments related to temporary or permanent neuropathy and/or edema are known risk factors for dysphagia (Figs. 1a and b). The prominence of the plate can impact on bolus flow and thicker plates have been associated with greater risk of dysphagia [40]. Halo braces and neck collars have been shown to affect swallowing biomechanics in terms of timing and displacement in healthy adults [41, 42] and therefore may add to swallowing difficulties a patient may be experiencing.

Paralysis or impairment of the major respiratory muscles with injuries above C5 interrupts normal breathing patterns, which are essential for safe and efficient swallowing [43, 44]. Precise respiratory–swallowing coordination is vital for airway protection [43]. Expiration before and after swallowing is the most common breathing pattern in healthy adults [44, 45]. It serves to expel any misdirected materials from the airway after swallowing, offering an additional airway protective mechanism. Deviation from this respiratory–swallowing pattern is associated with increased risk of airway invasion [43]. Initiation or completion of swallowing with an inspiration serves to bring air and potentially misdirected food or fluid particles into the lungs [43, 46]. There are no studies that specifically evaluate respiratory–swallowing coordination in patients with cSCI. However, patients with cSCI have reduced lung volumes and shortness of breath [47]. This atypical breathing pattern is likely to contribute to respiratory–swallowing discoordination and increased risk of airway invasion.

The phrenic nerve (C3-C5) provides exclusive motor control to the diaphragm, the primary muscle for inspiration. There is strong evidence for the role of the diaphragm in safe swallowing [48]. Active contraction of the diaphragm creates an active breath hold or ‘swallow breath’ during swallowing [48, 49]. This preserves respiratory volume for post-swallow expiration that is important for airway protection and airway clearance [48]. Activation of the diaphragm creates negative trans-diaphragmatic pressure [50, 51]. During swallowing, this contributes to a favorable pressure gradient (i.e., a suction effect) for bolus flow across the upper esophageal sphincter [51]. Recent studies in animal models of cSCI demonstrate that the absence of diaphragmatic activation during swallowing disrupts negative pressure generation in the esophagus and results in disordered laryngeal muscle activity, contributing to penetration and aspiration [52]. These preliminary findings suggest that damage to the phrenic nerve and diaphragm innervation following cSCI may also directly contribute to swallowing dysfunction.

Respiratory muscle dysfunction associated with cSCI can also impair airway clearance mechanisms that are vital for safe ingestion of food and fluid. The cough response protects the airway from foreign bodies or irritants, including mis-directed food, fluid, and saliva. The intercostal and abdominal muscles are important for coughing and effective airway clearance. Following cSCI, cough is impaired to various degrees depending on the level and completeness of the injury with more dysfunction observed at higher levels of injury [25]. In patients with complete cSCI at C5 and above, all measures of respiratory function (including forced vital capacity, forced expiratory volume, and peak expiratory flow rate) were found reduced by at least 50% of predicted normal values [53]. This indicates that the cough response to aspiration of food, fluid, and saliva is likely impaired in these patients. Additionally, reduced respiratory and cough function are associated with increased risk of penetration, aspiration, and aspiration pneumonia across a range of patient populations [54‐58]. This is due to the shared anatomical and neural substrates of coughing and swallowing. Furthermore, laryngeal muscle impairments due to direct injury, or management of the spinal injury, can result in vocal fold dysfunction and poor glottal adduction resulting in reduced cough efficiency and effectiveness [59].

While the focus of this review is on oro-pharyngeal dysphagia in cSCI, the relationship between oropharyngeal and esophageal impairments is well documented in the literature [60‐62]. Research suggests that esophageal symptoms are often under-reported in patients with SCI [63], therefore, dysphagia clinicians should take an active role in screening and referring patients to gastroenterology, given the potential for adverse consequences on swallowing safety and efficiency. In addition, given the functional interrelationship between the pharynx and esophagus, pharyngeal impairments may be impacted by esophageal abnormalities [61]. Patients with cSCI are at high risk of esophageal impairments [60, 64]. Autonomic dysfunction following cSCI can cause dysmotility of the gastrointestinal system leading to paralytic ileus [65]. Second, damage to upper esophageal mucosa can occur from penetrating traumatic injuries, such as knife stabbings and gunshot wounds and as a complication of cervical spinal surgery, due to displaced screws or metal work [66, 67]. These esophageal changes can promote esophageal dysmotility, gastroesophageal reflux disease (GERD), and upper esophageal dysfunction [60, 68].

For traumatic cSCI patients, the early focus is on maintaining good respiratory function and minimizing neurological damage following injury to the spine. For injuries C5 and above, there is a high risk of respiratory failure due to paralysis of respiratory muscles that will necessitate the need for mechanical ventilation [47, 69]. Although non-invasive ventilation (NIV) and negative pressure options are available [68], usual practice is to insert an alternative airway, in the form of a tracheostomy to assist with both ventilation and toileting/secretion management. Both tracheal intubation and tracheostomy can cause a range of acute and chronic laryngeal complications that contribute to dysphagia [70, 71]. Potential complications include laryngeal edema, vocal cord palsy, sensory impairments, stenosis, and granuloma and readers are directed to Wallace and colleagues for a thorough review of this evidence [70].

Numerous studies have demonstrated that the presence of a tracheostomy is a significant independent risk factor for dysphagia after cSCI [14, 31, 72‐74]. One study reported a threefold risk (RR: 3.67) of dysphagia with a tracheostomy following cSCI [73]. The cause of dysphagia following tracheostomy is complex and multifactorial. The presence of a tracheostomy substantially alters pharyngeal and laryngeal biomechanics. It impairs hyolaryngeal excursion that is necessary for airway protection during swallowing and opening of the upper esophageal sphincter for bolus transport to the stomach [10, 11, 14]. Changes in subglottic air pressure (with an open versus close tracheostomy tube), are known to affect pharyngeal swallowing physiology, including bolus transit times and airway invasion [75]. The absence of subglottic air pressure during swallowing may disturb the favorable pressure gradient for movement of the bolus into the esophagus [51]. The presence of a tracheostomy and need for ventilation creates an alteration to respiratory–swallowing coordination with increased risk of aspiration [76]. Further desensitization of the upper airway due to tracheostomy may affect airway protection and cough sensitivity in acute patients. Disruption to vital capacity leads to respiratory muscle fatigue and a failure to wean from ventilator support [77].

Early detection of dysphagia is therefore of high clinical value to prevent aspiration pneumonia. However, despite the known risks of dysphagia following cSCI, no routine method of screening exists [11]. One of the key challenges in this patient population is that patients with cSCI with tracheostomy may not demonstrate overt signs of laryngeal penetration or aspiration (e.g., coughing after food/liquid intake) due to reduced or absent laryngeal sensation and/or weak cough—a phenomenon known as silent aspiration. This makes it challenging for healthcare staff to screen for dysphagia prior to referral to SLP for instrumental swallowing assessment. Clinical or bedside swallow screening requires administration of food or fluid trials to evoke adverse motor response such as coughing to determine a patient’s swallowing dysfunction.

Validated dysphagia screening tools have been evaluated with patients with cSCI. Posillico, Golob [84] used the Yale Swallow Protocol [85] with all patients admitted with a suspected spinal cord injury. The authors reported a 16.7% incidence of dysphagia. This bedside screening tool had high sensitivity (84.2%) and specificity (95.8%) for detecting dysphagia. However, 48.4% of the 221 patients were excluded from the screening process because they were critically ill and instrumental assessments were only conducted on those who failed their Yale. Thus, the sensitivity and specificity of the tool for detecting dysphagia in a true clinical cohort of cSCI patients is unclear. Other dysphagia screening tools with high sensitivity and specificity have been developed for stroke and neurogenic populations. These include the water swallowing test, the Mann assessment of swallowing ability (MASA) [86], and the Gugging swallowing screen (GUSS) [87]. However, their sensitivity and specificity for identifying dysphagia and aspiration in patients with cSCI are currently unknown and may, again, be limited given the unique pathogenesis and risk factors of dysphagia in cSCI. In response to this, The Dysphagia following Acute Cervical Spinal Cord Injury (DAISY) swallow screening tool [88] was developed through international expert consensus. It focuses on identifying risk factors for dysphagia and presence of clinical symptoms suggestive of aspiration in cSCI, i.e., injury risk, clinical risk, and urgency (Table 3). This tool enables healthcare staff to identify risk factors for dysphagia prior to commencing oral trials and preventing adverse outcomes. If risks are evident a referral to SLP or another dysphagia clinician is recommended for diagnostic instrumental assessment. If clinical symptoms of dysphagia are already evident then the team are instructed to review and change current clinical management and identify possible causes. This may highlight processes such as mouth care or managing thirst that may be exacerbating dysphagia. Further validation of this screening tool is planned alongside a SCI-specific FEES protocol.

Cough reflex testing is a screening tool that is used in other patient populations with neurogenic dysphagia (e.g., acute stroke, Parkinson’s Disease) to identify risk of silent aspiration. It involves inhalation of a tussive (i.e., cough evoking) agent, most often citric acid or capsaicin, at concentrations that are known to elicit a cough response in healthy individuals. In the clinical setting, cough reflex testing is used in the acute stages to support clinical decision-making regarding patients’ risk of silent aspiration [89]. To date, no studies have evaluated the validity of cough reflex testing in patients with acute cSCI and dysphagia for this purpose. Lin and colleagues [90] evaluated citric acid cough thresholds (i.e., the concentrations of citric acid that were required to elicit a cough response) in healthy individuals and individuals with chronic thoracic and cSCI (1–20 years post injury). They found that cough thresholds were reduced in those with chronic SCI, compared to the control group, meaning that individuals with chronic SCI had enhanced upper airway sensation i.e., hypersensitivity [91]. In contrast, Dicpinigaitis and colleagues [25] found no difference in capsaicin cough threshold in individuals with chronic cSCI (5–41-year post injury) and healthy controls. While capsaicin is known to target different cough mechanisms to citric acid [92], the findings suggest that upper airway sensation may be intact, or in fact enhanced, in chronic SCI. However, it is highly likely that blunted laryngeal sensation contributes to aspiration and silent aspiration in the acute phase post cSCI, especially in patients who are intubated [93]. Studies are needed to determine the validity of cough reflex testing for identifying silent aspiration in acute cSCI.

Swallow screening establishes those likely to have dysphagia and clinical swallowing evaluations at bedside may enable clinicians to hypothesize about possible swallowing difficulties and gauge a patient’s risk of aspiration and aspiration pneumonia. However, instrumental assessments, namely, Videofluoroscopic Swallow Study (VFSS), Flexible Endoscopic Evaluation of Swallowing (FEES), and High-resolution Impedance Manometry (HRIM) allow clinicians to evaluate swallowing biomechanics to inform rehabilitation and management. VFSS has been reported more frequently in research studies with cSCI patients. However, it is important to note that with VFSS and HRIM, there is a requirement for the patient to be able to tolerate transport to radiology or gastroenterology clinics and maintain an upright seating position. Thus, findings from VFSS and HRIM studies may be bias towards people with less severe or acute cSCI.

FEES is a more accessible tool in the acute and critical care settings as it can be performed at a patient’s bedside. FEES provides detailed imaging of the pharyngeal and laryngeal structures; however, it does not provide a view of oral stage activity. FEES enables evaluation of secretions and airway patency, facilitating clinical decision making for a patient’s ability to tolerate oral trials. Clinical settings can vary in their access to these instrumental assessments and the availability of SLP services, affecting dysphagia diagnosis and development of swallow rehabilitation programs [94].

Working as a multidisciplinary team can maximize outcomes for patients with a multifaceted approach [95, 96]. Patients with cSCI need a personalized care approach to tracheostomy and ventilator weaning that takes into consideration respiratory muscle paralysis and fatigue that reduces the usual pace of weaning [97, 98]. SLPs have a role to play in evaluating laryngeal function alongside the weaning process [70]. There is limited published research in SLP rehabilitation for patients with cSCI. This is perhaps in part due to the heterogeneous population and the challenges of doing research in patients with acute illness. As a result, SLPs need to utilize advanced clinical reasoning and evidence from other patient populations in managing dysphagia in patients with cSCI. Despite the paucity of evidence, it is reasonable to consider that optimizing certain factors may increase the likelihood of improved dysphagia outcomes. These include positioning, management of patients’ psychological wellbeing, and management of dry mouth and taste and smell changes. In addition, given the level of dependency, those supporting patients with oral care and at mealtimes should have the required training to do so. The need for SLP intervention is recognized [1, 21] and some of the areas of treatment currently in practice are summarized in Table 4, alongside emerging therapies.

Dick et al. [82] recently published a case series documenting the effects of an individualized swallowing intervention for four patients cSCI (2 traumatic, 6 weeks-10yrs since injury). Intervention was tailored to participants underlying physiologic impairment (i.e., reduced pharyngeal constriction, impaired hyoid displacement, etc.) identified on instrumental assessment, and involved exercises such as the effortful swallow, Mendelsohn maneuver and chin tuck against resistance. Improvements in timing and swallowing biomechanics were observed post intervention. Functional swallowing improvements were also noted, with three out of four patients able to have their feeding tubes removed post intervention. This study highlights the benefit of tailored interventions to improve swallowing outcomes in patients with cSCI.

A recent systematic review by Berlowitz and colleagues [110] evaluated the effects of respiratory muscle training in patients with cSCI. Respiratory muscle training comprised specific training of inspiratory and/or expiratory muscles using a device or singing in one study. Results indicated that respiratory muscle training was safe in patients with cSCI and no adverse effects were noted. Increases in vital capacity, maximum inspiratory pressures, and maximum expiratory pressure were reported post intervention. While the precise effects on swallowing outcomes remain unclear, the findings suggest that respiratory muscle training could enhance cough, swallowing, and airway clearance mechanisms for patients with cSCI based on previously published literature documenting the relationship between improvements in aerodynamic measures and swallowing safety in other neurogenic populations [55, 56, 113, 114]. This is further supported by research demonstrating positive effects of expiratory muscle strength training (EMST) on swallowing safety and airway protective mechanisms in patients with neurogenic dysphagia [115‐119]. Furthermore, enhancing respiratory muscle strength is known to decrease risk of aspiration pneumonia [58, 120, 121]. Studies to evaluate the effects of respiratory muscle training on swallowing outcomes in patients with cSCI are urgently needed.

Abdominal functional electrical stimulation (FES) involves the application of surface electrodes that emit electrical pulses (20–50 Hz) to the abdominal muscles to achieve muscle contraction. Recent studies demonstrated that abdominal FES could improve forced vital capacity, vital capacity, peak expiratory flow, and unassisted cough production in patients with tetraplegia [111, 122, 123]. To date, no study has evaluated swallowing specific outcomes following abdominal FES in patients with cSCI. However, the findings suggest that abdominal FES could enhance airway clearance mechanisms and swallowing outcomes [55, 56, 113, 124]. Including swallowing outcomes in future clinical trials on FES is required.

There is growing interest in the use of therapeutic AIH to enhance limb and respiratory function in patients with cSCI [125]. AIH involves exposing individuals to bouts of low oxygen interspersed with normal oxygen levels to enhance plasticity in spinal synaptic pathways. It can be combined with other treatments such as drug treatments, cortical or spinal stimulation, and task-specific training to optimize functional outcomes [125]. Studies have shown that AIH enhances limb and respiratory function in animal models [126, 127] and patients with cSCI [128‐130]. The greatest functional effects are observed when AIH precedes task-specific motor training, in that, AIH serves as a ‘plasticity primer’ [112]. The precise underlying mechanisms of this therapeutic effect are still under investigation. However, results suggest that AIH combined with swallowing-specific training may enhance swallowing function for patients with cSCI. AIH interventions are highly novel and remain in Phase I/II clinical trials and are not yet ready for widespread clinical implementation.

There are many unique challenges to rehabilitation in this population that we do not encounter in neurorehabilitation of other patients populations. Bracing, collars, and neck fixation alters and restricts neck position during mealtimes often with a tendency for a slightly superiorly tilted head posture rather than a perhaps more protective chin tucked position [41, 131]. Bracing, collars, and neck fixation also make some compensatory swallowing strategies such as head tilt, turn, and chin tuck maneuvers difficult or prohibitive and may make some rehabilitation exercises unmanageable such as the Shaker head lift [82]. Psychological impacts of injury including fear, anxiety, and low mood may all make return to oral intake as well as exercise adherence a challenge [132, 133]. Some services are heavily focused on independence of mobility and self-care for rehabilitation discharge with little focus on swallowing and voice recovery [134]. Living with a spinal injury comes with many other complications that can impact on rehabilitation including hypotension, risk of pressure areas, and trunk and head control. Pain and fatigue during movement may also reduce rehabilitation capabilities. Appetite, taste, and smell disturbances impact motivation to return to oral intake.

While initial treatment of a patient with a SCI will take place in their acute center, ongoing rehabilitation will take place in either a specialist SCI center or non-specialist rehabilitation center. Specialist centers are established in a number of high-income countries, however, in these countries, there may be a limited number of specialist beds available. A recent report in the UK identified reduced bed capacity in specialist units resulting in cSCI patients remaining in non-specialist units for prolonged periods of time [135]. For those patients requiring ventilator support, bed capacity is even more restricted with many units taking small numbers due to the high care demands and staffing requirements.

It has been suggested that early admission to a specialist spinal injury center can improve patient outcomes and that dysphagia management practices differ between specialist and non-specialist settings. A survey conducted by McRae et al. [136] aimed to explore clinical practices within specialist and non-specialist critical care units in the management of cSCI patients with respiratory and swallowing impairments. This study identified an increased use of instrumental swallow studies in specialist centers and increased use of cuff deflation during weaning to help restore verbal communication and support swallowing. These differences would suggest that a patient’s dysphagia rehabilitation is optimized in a specialist center with access to a specialist dysphagia team including a Speech–Language Pathologist (SLP). There is an indication that those receiving rehabilitation in a specialist center achieve greater functional gains than those who do not [137]. This is supported by McRae’s findings [136] that non-specialist centers had lower expectations for patients returning to safe eating and drinking and an increased reliance on diet and fluid modifications to manage dysphagia. As part of the patient pathway, they will often transition from non-specialist to specialist centers. This difference in dysphagia management can leave patients feeling confused and disengaged with the rehabilitation process. The need for a consistent multidisciplinary team (MDT) approach to dysphagia management is therefore required. Many SCI centers have outreach teams, and providing they include a SLP, this may go some way to bridging this skills and knowledge gap and ensuring a consistent approach to dysphagia management.

Length of stay in inpatient rehabilitation units can vary considerably and the factors that contribute to this are myriad. Those with a higher, more severe spinal cord injury have a longer length of stay than those with incomplete paraplegia. Associated complications including pressure sores, poor nutritional status, and respiratory compromise can also increase length of stay. The average length of stay for a cSCI in the UK is 3 months, in contrast the median length of rehabilitation stay in the US is 32 days [138]. To varying degrees depending on the country and setting, a patient’s discharge date will be determined by their medical stability, functional gains, motivation for therapy, funding, and access to a suitable discharge destination. In U.K. health systems, a goal-focused approach is utilized, whereby inpatient stays will be extended if appropriate patient goals are identified. Once a patient is discharged, there are logistical and service provision barriers to accessing an instrumental swallow assessment and intensive dysphagia therapy. Given these pressures, specialist, targeted input from appropriately trained clinicians is vital to optimize patient outcomes during inpatient stays.

Best practice guidelines should be used to ensure patients access specialist care at the right time and ensure a proactive approach to identifying dysphagia based on clinical risk factors is employed. Access to a SLP with specialist skills in cSCI can help improve dysphagia management. Further research into optimal models of care for cSCI patients is needed to inform service development worldwide, this should include longitudinal data examining long-term outcomes following admission to specialist and non-specialist centers.