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Respiratory Management Following Spinal Cord Injury

2 Contact Hours
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This peer reviewed course is applicable for the following professions:
Advanced Practice Registered Nurse (APRN), Certified Nurse Practitioner, Clinical Nurse Specialist (CNS), Licensed Practical Nurse (LPN), Licensed Vocational Nurses (LVN), Nursing Student, Occupational Therapist (OT), Occupational Therapist Assistant (OTA), Registered Nurse (RN), Registered Nurse Practitioner, Respiratory Care Practitioner, Respiratory Therapist (RT)
This course will be updated or discontinued on or before Sunday, April 19, 2026

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CEUFast, Inc. is accredited as a provider of nursing continuing professional development by the American Nurses Credentialing Center's Commission on Accreditation. ANCC Provider number #P0274.


CEUFast, Inc. is an AOTA Provider of professional development, Course approval ID#04923. This distant learning-independent format is offered at 0.2 CEUs Intermediate, Categories: OT Service Delivery and Foundational Knowledge. AOTA does not endorse specific course content, products, or clinical procedures. AOTA provider number 9757.

Outcomes

≥ 92% of participants will know how and why respiratory complications occur after a spinal cord injury and how these complications are mitigated.

Objectives

After completing this continuing education course, the participant will be able to meet the following objectives:

  1. Identify the location of and the muscles used in inspiration and expiration.
  2. Describe the mechanics of respiration.
  3. Explain the American Spinal Injury Association Impairment Scale (AIS) used to classify the degree of impairment in SCI.
  4. Describe the respiratory complications specific to mechanically ventilated SCI patients.
  5. Determine the proper assessment of pulmonary function following SCI.
  6. Explain the interventions that can be used in the management of compromised pulmonary function following SCI to optimize the patient’s quality of life.
  7. Determine the preferred method for weaning a SCI patient from mechanical ventilation.
  8. Identify the advantages of a tracheostomy.
CEUFast Inc. and the course planners for this educational activity do not have any relevant financial relationship(s) to disclose with ineligible companies whose primary business is producing, marketing, selling, re-selling, or distributing healthcare products used by or on patients.

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Respiratory Management Following Spinal Cord Injury
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To earn a certificate of completion you have one of two options:
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    (NOTE: Some approval agencies and organizations require you to take a test and "No Test" is NOT an option.)
Author:    Dana Bartlett (RN, BSN, MA, MA, CSPI)

Introduction

Respiratory complications, acute and long-term, are the main cause of morbidity and mortality in patients who have had a spinal cord injury (SCI) (Bach et al., 2020a; Berlowitz et al., 2016; Garshick, 2021; Olivero et al., 2020; Reyes et al., 2020; Schilero et al., 2018a)

These complications include (but are not limited to) (Berlowitz et al. 2016; Garshick, 2021; Olivero et al., 2020; Reyes et al., 2020; Schilero et al., 2018a):

  • Atelectasis
  • Pneumonia
  • Pulmonary edema
  • Thromboembolism
  • Respiratory failure

The degree of respiratory dysfunction is related to the extent and level of the neurological injury, and patients who have suffered a high cervical and thoracic injury are at the highest risk (Berlowitz et al., 2016; Garshick, 2020; Schilero et al., 2018a).

Respiratory dysfunction that leads to respiratory complications in SCI is complex and involves many factors; examples include (Garshick, 2021; Reyes et al., 2020):

  • Abnormal/weak cough
  • Airflow limitation
  • Ventilatory muscle impairment/paralysis
  • Bronchial hyperresponsiveness
  • Excess bronchial mucous production
  • Abnormal/decreased lung capacities and volumes
  • Autonomic dysfunction

Pulmonary complications are a common and well-known problem in SCI, but there is relatively little information about their management. Despite years of experience and research, there are still many unknowns in the treatment of SCI (Fehlings et al., 2017), and treatment recommendations are, at times, based on clinical experience and expert opinion. Management of care with appropriate interventions, prevention of pulmonary complications associated with SCI, and support for a return to the maximal level of functioning will be discussed.

Inspiration

The following muscles are those involved in the action of inspiration or inhalation of air (see Figure 1) (Randleman et al., 2021):

  • Diaphragm:
    • Major muscle which mediates inspiration
    • Innervated by the phrenic nerve (C3 to C6 nerve roots)
  • Accessory muscles of inspiration are the:
    • External intercostals
    • Innervated by thoracic nerve roots, T2-T11
  • Clavicular portions of the pectoralis major, C5 to T1
  • Scalene:
    • Innervated by cervical nerve roots C3 to C8
  • Sternocleidomastoids and trapezius:
    • Innervated via cervical nerve roots C2 to C4 and accessory nerve XI (Sternocleidomastoid) and C1 to C4 and accessory nerve XI (Trapezius)
    • Patients with high SCI can sometimes utilize oral, pharyngeal, and laryngeal muscles for short-term ventilation by projecting boluses of air past the glottis (glossopharyngeal breathing), although these muscles are not traditionally thought of as muscles of respiration

Expiration

The following muscles are those involved in the action of expiration or exhalation of air (See Figure 1) (Randleman et al., 2021):

  • Abdominal wall muscles:
    • Rectus abdominous
    • Obliques
    • Transversus abdominus
    • All these abdominal muscles are innervated by the lower thoracic and lumbar nerve roots, T6 to L3
  • Internal intercostals:
    • Innervated by the thoracic nerve roots T1 to T11

Figure 1
Muscles of Respiration

Muscles of Respiration

The process of inspiration involves the contraction of the diaphragm and the external intercostal muscles that allow the chest cavity to expand (Costanzo, 2018). At high levels of ventilatory activity, the accessory muscles are recruited to aid in this process (Costanzo, 2018). Expiration is a passive process, and normally it does not require the active use of the abdominal and the internal intercostal muscles. However, the abdominal and internal intercostal muscles are recruited when forced exhalation is needed, like during a cough or when exercising (Garshick, 2021). If a patient cannot generate a forced exhalation, i.e., a patient who has an SCI, an effective cough cannot be produced, and pulmonary secretions cannot be removed (Garshick, 2021).  Also, the abdominal muscles and the internal intercostal muscles contribute to the normal functioning of the diaphragm, and when these muscles are not functioning, the efficiency of the diaphragm is negatively affected (Garshick, 2021).

Review of Mechanics of Respiration

Figure 2
Movement of the Rib Cage During Respiration

Movement of the Rib Cage During Respiration

Movement of the Rib Cage During Inspiration (Figure 2):

  • The diaphragm contracts and flattens
  • The external intercostal muscles contract while the internal intercostal muscles relax
  • The ribs move upwards and outwards while the sternum moves up and forward
  • The volume of the thoracic cavity increases
  • Air pressure in the lungs causes them to expand to fill up the enlarged space in the thorax
  • Expansion of the lungs causes the air pressure inside them to decrease
  • Atmospheric pressure is now higher than the pressure within the lungs, so air moves into the lungs

Movement of the Rib Cage During Expiration (Figure 2):

  • The diaphragm relaxes and arches upwards
  • The internal intercostal muscles contract while the external intercostal muscles relax
  • The ribs move downwards and inwards while the sternum moves down to its original position
  • The volume of the thoracic cavity decreases
  • The lungs become compressed, and the air pressure inside them increases as the volume decreases
  • The air pressure within the lungs becomes higher than the atmospheric pressure, so the air is forced out of the lungs to the exterior

You can use this mnemonic tool to help you remember what happens to the intercostal muscles during respiration:

  • Inhalation = RICE:
    • R: Relax your
    • I: Intercostal muscles and
    • C: Contract your
    • E: External intercostal muscles
  • Exhalation = ERIC:
    • E: External intercostal muscles
    • R: Relax and your
    • I: Intercostal muscles
    • C: Contract

The degree of respiratory failure associated with traumatic injuries to the spinal cord primarily depends on the level of the spinal lesion, and cervical and high-level thoracic injuries impair the function of the diaphragm, the intercostal muscles, the abdominal muscles, and the accessory muscles that are the primary movers of inspiration and expiration (Wang et al., 2020).

In addition, a complete SCI, defined as the absence of motor or sensory function below the injury (classified as American Spinal Injury Association (ASIA) score A), results in greater functional impairment than incomplete injuries (ASIA scores B–D). Other factors that are associated with pulmonary complications in SCI patients are age, preexisting medical illnesses, smoking, and associated major traumatic injuries (Garshick, 2021).

Pulmonary Function Tests (PFTs)

Spirometry (meaning the measuring of breath) is the most common of the pulmonary function tests (PFTs). Spirometry measures lung function, specifically the amount (volume) and/or speed (flow) of air that can be inhaled and exhaled. Spirometry generates charts that show the volume and flow of air with one inhalation and one exhalation.

Lung Volumes and Lung Capacities

There are four lung volumes and four lung capacities. A lung capacity consists of two or more lung volumes (Costanzo, 2018):

The four lung volumes are:

  1. Tidal volume (VT): The volume of air moved into or out of the lungs during quiet breathing.
  2. Inspiratory reserve volume (IRV): The maximal volume that can be inhaled from the end-inspiratory level.
  3. Expiratory reserve volume (ERV): The maximal volume of air that can be exhaled from the end-expiratory position.
  4. Residual volume (RV): The volume of air remaining in the lungs after maximal exhalation.

The four lung capacities are:

  1. Vital capacity (VC): The volume of air breathed out after the deepest inhalation.
  2. Forced vital capacity (FVC): the determination of the vital capacity from a maximally forced expiratory effort.
  3. Total lung capacity (TLC): The volume in the lungs at maximal inflation (the sum of VC and RV).
  4. Inspiratory capacity (IC): The sum of IRV and VT.
    1. Functional residual capacity (FRC): The volume in the lungs at the end-expiratory position.

Forced expiratory volume in one second (FEV1): The volume of air exhaled at the end of the first second of forced expiration.

Individuals with SCI exhibit reduced lung volumes and flow rates because of respiratory muscle weakness. Changes in the spirometric measurements in SCI are dependent on injury level and posture (Schilero et al., 2018a).

The higher the level of injury, the greater the decrease in PFT parameters (Schilero et al., 2018). Patients who have an SCI are often in the supine/recumbent position, and FVC, FEV1, and VC are increased in this position (Schilero et al., 2018b). When a patient is erect, the abdominal contents fall forward, and the diaphragm flattens. This impairs the ability of the major muscle of inspiration in patients with quadriplegia/tetraplegia.

Injury to the cervical or thoracic spinal cord affects the spinal nerves that innervate respiratory muscles. The diaphragm, the major muscle of inspiration, receives its innervation from the third, fourth, and fifth cervical spinal segments (Figure 3).

  • If a patient has paralysis of diaphragmatic, intercostal, and abdominal muscles from an injury above the C3 level and the patient is not mechanically ventilated, survival is not possible (Vázquez et al., 2013).
  • With an incomplete C2 to C4 injury or an injury at C5 or below, the patients will have neural control of the diaphragm and may have spontaneous respiration (Vázquez et al., 2013), but their respiratory function is substantially compromised.

Figure 3
Vertebra

Vertebra Front and Side

The respiratory pattern of patients who have diaphragmatic paralysis is often a paradoxical movement of the abdomen: the abdominal wall retracts during inspiration and protrudes during the expiration phase (Vázquez et al., 2013; Hachmann et al., 2017):

  • This occurs more often in cervical SCIs, and it is caused by a lack of spinal motor activation of the external intercostals and weak abdominal wall contractions.
  • Alterations in the chest wall, lung, and abdominal compliance in quadriplegia/tetraplegia are associated with an increase in the work of breathing and may contribute to respiratory muscle fatigue.
  • Respiratory paralysis can also decrease the patient’s ability to cough, and an impaired/absent ability to cough is common after an SCI.

After the initial stage of spinal shock has passed, patients with quadriplegia/tetraplegia may develop abnormal spinal reflexes and respiratory muscle spasticity (Garshick, 2021). This decreases the elasticity of the abdominal compartment (Vázquez et al., 2013). Spastic contractions of the abdominal muscles increase the load of the inspiratory muscles, and this increases the pressure that must be overcome for inspiration to be initiated (Vazquez et al., 2013).

Assessment of Level and Completeness of SCI

Pulmonary physiologic changes due to SCI are related to the extent of neurological impairment. The American Spinal Injury Association Impairment Scale (AIS) is used to classify the degree of impairment that is based on strength in key muscles and a sensory examination (Table 1) (Hansebout & Kachur, 2018; Sánchez et al., 2020):

Table 1
American Spinal Injury Association (ASIA) Impairment Scale (AIS)
A
  • Complete cord injury.
    • No motor or sensory function is preserved in the sacral segments S4-5.
B
  • Incomplete cord injury.
    • Sensory but not motor function is preserved below the neurologic level and includes the sacral segments (light touch or pinprick at S4-5 or deep anal pressure), AND no motor function is preserved more than three levels below the motor level on either side of the body.
C
  • Incomplete cord injury.
    • Motor function is preserved at the most caudal sacral segments for voluntary anal contraction (VAC) OR the patient meets the criteria for sensory incomplete status (sensory function preserved at the most caudal sacral segments S4-S5 by LT, PP, or DAP) and has some sparing of motor function more than three levels below the ipsilateral motor level on either side of the body.
    • This includes key or non-key muscle functions to determine motor incomplete status) For AIS C-, less than half of the key muscles below the single NLI have a muscle grade of ≥ 3.
    • LT = Light touch, PP = Pinprick, Dap + Deep anal pressure, NIL =Neurologic level of injury
D
  • Incomplete cord injury.
    • Motor function as defined above with at ≥ half of key muscle functions below the NLI having a muscle function ≥ 3. 
E
  • Normal motor and sensory function.
    • Sensation and motor function are graded as normal in all segments and the patient had prior deficits.

*Muscle function is graded using the International Standards for Neurologic Classification of Spinal Cord Injury.

*For an individual to receive a grade of C or D (i.e., motor incomplete status), he/she must have either:

  1. Voluntary anal sphincter contraction or
  2. Sacral sensory sparing with sparing of motor function more than three levels below the motor level for that side of the body.

*Patients without an initial spinal cord injury do not receive an AIS grade.

The patient’s strength in key muscle groups is assessed and graded. A muscle grade of 5/5 is normal, and a grade of 3/5 means the muscle can be moved against gravity (Naqvi & Sherman, 2021):

  • The motor level is defined as the most caudal key muscle that is graded 3/5 or 4/5, with the segment cephalad to that level graded 5/5.
  • The sensory level is defined as the most caudal dermatome to have normal sensation for both pinprick and light touch.
  • For areas that lack key muscles to test, such as between T2 and L1, sensory findings are used to estimate motor levels.

Complete motor SCI includes: (See Table 1 above)

  • AIS A (no sensory or motor function preserved below the neurologic level)
  • AIS B (sensory but no motor function preserved below the neurologic level)

Incomplete motor SCI includes: (See Table 1 above)

  • AIS C, where motor function in less than half of the key muscles below the neurologic level have a muscle grade of less than 3
  • AIS D more than half the key muscles below the neurologic level have a muscle grade of 3 or more

With quadriplegia/tetraplegia, there is an injury to at least one of the eight cervical segments of the spinal cord. With paraplegia, there is an injury in the thoracic, lumbar, or sacral regions.

Pulmonary Physiologic Changes

Respiratory dysfunction that causes pulmonary complications in SCI patients is complex and involves many factors, these include (Berlowitz et al, 2016; Garshick, 2021; Reyes et al., 2020):

  • Abnormal/weak cough
  • Airflow limitation
  • Ventilatory muscle impairment/paralysis
  • Bronchial hyperresponsiveness
  • Excess bronchial mucous production
  • Abnormal/decreased lung capacities and volumes
  • Autonomic dysfunction
  • Abnormal chest wall compliance

Timing of Changes in Ventilatory Function

Immediately after an SCI, flaccid paralysis can occur, affecting all the muscles that are caudal to the level of injury (Berlowitz et al., 2016; Hansebout & Kchur, 2018). This physiologic state is known as spinal shock or spinal paralysis (Berlowitz et al., 2016; Garshick, 2021; Hansebout & Kachur, 2018). Spinal shock may continue for days or many months, and during the recovery period, the patient’s pulmonary function is impaired, primarily due to impairment of the muscles of respiration (Berlowitz et al., 2016; Garshick, 2021; Hansebut & Kachur, 2018). Pulmonary function is also impaired because of a decrease in chest compliance, decreased airflow, hyper-responsiveness of the bronchial passages, and an abnormally blunted response to hypercapnia (Garshick, 2021).

After resolution of spinal paralysis, spastic paralysis occurs, muscle tone is increased, and pulmonary function should improve (Grashick, 2021; Vázquez et al., 2013). This improvement typically happens several days or several weeks after the injury (Garshick, 2021). Improvement in respiratory muscle performance after SCI largely occurs in the first year following injury.

Impairment of Ventilatory Muscle Function

The extent of ventilatory muscle impairment depends upon the degree and location of the injury, as well as the duration of time since the injury. The higher the level and more complete the injury, the more likely it is that there will be respiratory muscle dysfunction (Table 2).

Spinal Cord LevelMuscle InvolvementEffect on RespirationClinical Consequence
C1-3Complete paralysis of all respiratory musclesVital capacity is only 5-10% of normal. Absent coughApnea and immediate death
C3-6Varied Impairment of diaphragmatic contractionVital capacity 20% of normal. Weak and ineffective coughVentilation necessary in the acute stages. The majority will be weaned from mechanical ventilation
C6-8Diaphragm and accessory cervical inspiratory muscles intact. Intercostals and abdominal muscles intact Expiration is entirely passive. Secretion retention. No respiratory failure unless co-existing lung/chest injury/illness
T2-4 Vital capacity 30-50% normal. Weak cough 
Table 2
Respiratory Complications with SCI

Ventilatory muscles innervated below the level of a complete SCI are completely nonfunctional (AIS A or B), while the degree of ventilatory muscle compromise is variable in patients with incomplete injuries (AIS C or D) (See Table 1 above):

  • Complete injury above C3 causes:
    • Near-total ventilatory muscle paralysis because the phrenic nerve, which innervates the diaphragm, arises from the third to fifth cervical roots.
    • Denervation of the intercostal, abdominal muscles, sternocleidomastoid, and trapezius muscles.
    • Due to complete paralysis of the respiratory muscles, patients with SCI above the C3 root have acute ventilatory failure and do not survive unless manual ventilation is rapidly instituted at the accident scene. In addition to ventilatory dysfunction, these patients are unable to cough without assistance.
  • Injury involving C3 through C5 cause:
    • Variable impairment of diaphragmatic strength.
    • Variable impairment of the accessory muscles of ventilation (e.g., scalenes, sternocleidomastoid, trapezius).
    • Respiratory failure requiring mechanical ventilation is common during the first few days to weeks after the injury, either due to respiratory muscle weakness and fatigue or precipitated by atelectasis or pneumonia.
    • As the initial muscle flaccidity transitions to spasticity and accessory muscles are recruited and strengthened, spontaneous ventilation is often adequate for weaning from mechanical ventilation.
    • In addition to ventilatory dysfunction, these patients have an impaired cough due to loss of expiratory muscle strength.
  • Injury at C6 through C8:
    • Patients with complete cervical SCI but with intact diaphragm function can inhale via the diaphragm and accessory muscles in the neck.
    • Exhalation occurs primarily through the passive recoil of the chest wall and lungs because the primary muscles of exhalation (internal intercostals and muscles of the abdominal wall) are paralyzed, and the clavicular portions of the pectoralis major muscles provide only a small contribution (De Troyer et al., 1986; Estenne et al., 1989).
    • Thus, cough is impaired, and even if these patients do not have initial respiratory failure, they are at an increased risk of respiratory muscle fatigue in the setting of respiratory system loading (e.g., pneumonia or excess secretions).
  • Patients with injuries of the thoracic spinal cord have:
    • Intact diaphragm function.
    • Less impairment of overall ventilator muscle function despite some loss of intercostal muscle strength and impaired stabilization of the rib cage due to abdominal wall paralysis.
    • The main respiratory impairment for these patients is an inefficient cough mechanism.

Excess Bronchial Mucus Production

Excess bronchial mucous production is caused by autonomic dysfunction that causes a predominantly parasympathetic stimulation of the lungs (Andrade et al, 2021; Bach et al, 2020a).

Changes in Lung and Chest Wall Compliance

Lung and chest wall compliance is reduced in patients who have had an SCI (Garshick, 2021). This change is complicated and not completely understood, but it may be related to reduced lung volume and changes in surfactants (Garshick, 2021). Also, the joints, ligaments, and tendons of the rib cage will stiffen over time, limiting chest wall compliance (Bach et al, 2020b).

Airflow Limitation and Bronchial Hyperresponsiveness

Patients who have a cervical or high thoracic spinal SCI and tetraplegia have increased airway resistance, expiratory airflow limitation, and bronchial hyperresponsiveness/bronchospasms (Andrade et al., 2021; Garschick, 2021; Hill et al., 2022).  

The cause/causes of these abnormalities are likely due to (Andrade et al., 2021; Garshick, 2021; Hill et al., 2022):

  1. A reduced functional capacity (a result of alveolar collapse and small airway closure)
  2. A change/loss of sympathetic innervation to the airways 

The expiratory airflow limitation can be reversed with an inhaled anticholinergic, e.g., ipratropium, or an inhaled beta-2 agonist, e.g., albuterol (Garshick, 2021; Schilero et al., 2018a).

Changes in Ventilatory Control

Individuals with quadriplegia/tetraplegia do not have a normal increase in the ventilatory drive when blood carbon dioxide levels are increased, and if supplementary oxygen is given to these patients, they can develop hypercapnia (Garshick, 2021; Bach et al., 2020a). The mechanisms for this are not completely understood, and this issue has not been extensively researched; it may be caused by a decrease in blood pressure when the patient is in a sitting position (Garshick, 2021).

Assessment of Pulmonary Function

Performing PFTs and calculations of the predicted PFT values need to be adjusted/modified when doing PFTs in patients who have had an SCI (Garshick, 2021).

Garshick (2021) notes: “Many SCI patients, particularly those with complete tetraplegia, cannot meet the acceptability and reproducibility standards for spirometry set by the American Thoracic Society (ATS).”  (Note: Specific recommendations for measuring PFTs in SCI patients was not addressed in the most current (2019) ATS PFT measurement recommendations). 

  • Measurement of Height (Garshick, 2021; Diggisie et al., 2018; Pothirat et al., 2015):
    • Height is used to calculate predicted pulmonary function values, but in non-SCI patients, height is measured while the patients are standing; this is obviously not possible for a patient who has had an SCI.
    • For patients who have had an SCI, height should be measured when the patient is supine.
    • Height can be estimated by using body measurements like arm span, but this technique may not be accurate, and measuring height while the patient is supine is preferred.
    • It is not recommended to rely on the patient’s recall of her/his height.
  • Posture:
    • The vital capacity in SCI patients will often increase when they move from a sitting position to a supine; the normal response is a decrease.
  • Mouthpiece (Garshick, 2021):
    • Flange-style and tube-style mouthpieces can be used to measure PFTs, and for SCI patients, a flange-style may underestimate expiratory muscle strength; a tube-style mouthpiece should be used.
  • Confounding factors (Garshick, 2021):
    • Research has found that factors like age and smoking history can affect PFT results in SCI patients.
  • PFT results (Garshick, 2021; Raab et al., 2019; van Silfhout et al., 2016):
    • It is not uncommon for PFT results, e.g., FCV, to be abnormal in SCI patients.
    • Respiratory function is decreased immediately after the SCI, and then there is typically an improvement over the first few months-year after the injury.
    • What the long-term course of pulmonary function will be after an SCI – a decline, stability, or an improvement – is less clear.
    • Some authors have found that even several decades after an SCI, pulmonary function has not declined, while other authors have come to the opposite conclusion.
    • Understanding this issue and making conclusions is difficult because patients differ in their ability to train their respiratory muscles, changes in pulmonary function can vary depending on factors age, body mass, and cigarette smoking, and relatively little research has been done on this topic.

Management of Compromised Pulmonary Function Following SCIs

Elective Intubation and Mechanical Ventilation

Approximately 90% of patients who have had a traumatic SCI will need intubation, and up to 40% of patients who had a complete cervical lesion will become ventilator-dependent (Schreiber et al., 2021).

The two most important markers that predict the need for intubation are the level of the injury and the ASIA classification (Yonemitsu et al., 2021; Hasenbout & Kachur, 2018; Bach, 2020a; Garshick, 2020):

  • Complete lesions above C5 require intubation in virtually 100% of cases. In these patients, elective intubation is recommended.
  • Hypoxia in an SCI patient can adversely affect the patient’s neurological status, and many patients who have cervical spinal cord injury have a delayed onset of respiratory complications and need late elective intubation.
  • Intubation is necessary for managing secretions.
  • Also, SCI is often accompanied by many complications like trauma, coma, ARDS, and multi-organ system insufficiency, and in these situations, non-invasive ventilation will not be effective.
  • There are no specific criteria for ventilator settings that are specific to SCI patients. Garshick (2020) recommends using general guidelines and adjusting the ventilator settings as needed.

Ventilator-Induced Diaphragmatic Dysfunction

The thickness and excursion of the diaphragm reflect the ability of this muscle to move and contract, and the diaphragm is one of the primary muscles of inspiration. Also, patients who have a high cervical or thoracic injury depend primarily on the diaphragm for ventilation (Vázquez et al., 2013)

Critically ill patients and patients who have had an SCI often develop diaphragmatic atrophy and limited diaphragmatic excursion (Guzel et al., 2022; Reardon et al., 2021; Soták et al., 2021; Zhu et al., 2021). Diaphragmatic dysfunction can negatively affect pulmonary function, and it is a major factor in the failure to wean patients from mechanical ventilation (Zhu et al., 2019; Soták et al., 2021; Qian et al., 2018).

Ventilator-induced diaphragmatic dysfunction (VIDD) is also associated with increased ICU stay, increased mortality, and prolonged mechanical ventilation (Reardon et al., 2021).

Ventilator-induced diaphragmatic dysfunction can occur very quickly after mechanical ventilation has begun. Levine et al. (2008) found that after 18-69 hours of mechanical ventilation, there was significant atrophy in the myofibers of the diaphragms of brain-dead patients.  

Ventilator-induced diaphragmatic dysfunction (VIDD) is caused by mechanical ventilation (muscle inactivity because of mechanical ventilation) and factors like infections, malnutrition, sepsis, and the use of glucocorticoids and neuromuscular blockers (Reardon et al., 2021; Soták et al., 2021). Ultrasonography is the most effective technique for assessing the structure and function of the diaphragm in SCI patients and critically ill patients (Qian et al., 2018; Soták et al., 2021; Zambon et al., 2017; Zhu et al., 2021).  

Currently, there are no well-proven and universally used methods for preventing VIDD. Phrenic nerve stimulation has been successful in animal experiments, and there is some promising research on its use in humans (Reardon et al., 2021; Sotak et al., 2021)

Weaning: When and How

The start of weaning and the strategy to employ is determined by the following three factors:

  1. Degree of respiratory function at the time weaning is started.
  2. Level of the injury.
  3. Respiratory pathophysiology of the SCI.

There is relatively little research on weaning SCI patients from mechanical ventilation, and the studies on this topic that are available are often small, observational, and have study design problems (Garshick, 2020; Schreiber et al., 2021)

The criteria for suitability for weaning from Garshick (2020) and Bach (2020a), respectively, are outlined below in the bulleted lists. Regarding the criteria, Garshick (2020) wrote: “The accuracy of weaning predictors (e.g., rapid shallow breathing index) in predicting weaning success has not been specifically addressed in this patient population, and we typically follow standard clinical criteria for weaning . . .” Schreiber et al. (2021) wrote: “The probability of weaning success remains difficult to predict; no previous systematic review or meta-analysis has been conducted on the topic, and no societal guidelines or recommendations on weaning are available for this population.” 

  • Any problem of respiratory failure has been resolved.
  • pH > 7.25
  • PaO2/FiO2 ≥150* or SpO2 ≥90 percent on FiO2 ≤ 40 percent and positive end-expiratory pressure (PEEP) ≤ 5 cmH2O (* A threshold of PaO2/FiO2 ≥120 can be used for patients with chronic hypoxemia. Some patients require higher levels of PEEP to avoid atelectasis during mechanical ventilation.
  • The patient is hemodynamically stable.
  • The patient can initiate a breath.
  • The patient is fully awake and cooperative and is not receiving sedation or is minimally sedated.
  • Afebrile.
  • Normal white blood cell count.
  • The patient’s oxyhemoglobin saturation is ≥ 95% without supplemental oxygen for 12 hours.
  • The PaCO2 is ≤ 40 mm Hg at a peak inspiratory pressure < 30 cm H2O (except if morbidly obese) and with full ventilatory support as needed.
  • An oxyhemoglobin desaturation of < 95% can be reversed by mechanical insufflation-exsufflation and by suctioning when the airway cuff is inflated.
  • If the patient is intubated, there is a positive leak test with the cuff deflated.
  • If the patient has a tracheostomy, unassisted cough peak flows unassisted or assisted, or mechanical insufflation-exsufflation flows exceed 160 L/m with the tube removed, ostomy covered, and the patient is getting non-invasive ventilatory support (NVS) as needed.

Weaning is done by using exercise-rest periods (Bach, 2020a; Füssenich et al., 2018; Garshick, 2020). The patient is disconnected from the ventilator, and continuous oxygen or compressed humidified air is delivered. He/she breathes spontaneously for a while, and then the patient is put back on full ventilatory support (Bach, 2020a). If the patient has a motor-complete cervical SCI, the patient should be weaned while recumbent; this will put the diaphragm higher and allow for a more effective contraction (Garshick, 2020)

The periods of spontaneous breathing are increased as tolerated, and the patient should be monitored for signs that spontaneous breathing is difficult, e.g., agitation, increased heart rate and/or respiratory rate, or a decrease in vital capacity (Garshick, 2020).  

Manually assisted coughing, mechanical insufflation-exhalation, endotracheal suctioning, and other types of chest physiotherapy are important for preventing atelectasis during the weaning period (Garshick, 2020). Garshick (2020) recommends using chest physiotherapy techniques before each weaning period.   

It is known that patients with cervical SCI have increased resistance in the airways due to a loss of sympathetic control.

  • For quadriplegic/tetraplegic patients, there are studies with medications that attempt to counteract this effect, thus facilitating weaning. These medications include (Zakresek et al., 2017):
    • Bronchodilators (salmeterol) appear to improve respiratory function, inducing an anabolic effect on the respiratory musculature.
    • Methylxanthines (theophylline) may be effective in facilitating respirator weaning in patients who have an A or B-level SCI.

The effectiveness of these medications as an adjunct to weaning has not yet been proven, and clinical experience is very limited.

Non-Invasive Ventilation: Acute and Chronic Respiratory Failure and Weaning

Non-invasive ventilation (NIV) is defined as the delivery of positive pressure ventilation without the use of an invasive device (an endotracheal tube or a tracheostomy) and by way of a noninvasive device like a face mask, a nasal mask, or nasal prongs (Hyzy & McSparron, 2021b).

Non-invasive ventilation can be delivered by a standard or portable ventilator, and the interface device can be (Hyzy & McSparron, 2021b):

  1. An oronasal mask
  2. A nasal mask
  3. Nasal prongs
  4. A full-face mask
  5. A helmet

The two commonly used modes of delivery are bilevel NIV, commonly called bilevel positive airway pressure (BPAP – not BiPAP), and continuous positive airway pressure, CPCP (Hyzy & McSparron, 2021b).

Non-invasive ventilation is a well-established technique, and it can be used (Daoud et al., 2020; Hill & Kramer, 2022; Hyzy & McSparron, 2021a):

  1. To treat patients who are not intubated or do not have a tracheostomy and who have acute or chronic respiratory dysfunction caused by a neuromuscular or chest wall disease, including SCI patients. This technique is commonly used to treat chronic respiratory dysfunction in SCI patients. It can be used to treat acute respiratory dysfunction in SCI patients, but there is little experience with this.
    1. There are no universally used criteria for patient selection for NIV in this clinical situation.
    2. Hill & Kramer (2022) recommend using objective data like an FVC that is < 50% of the predicted value, a maximum expiratory pressure <40 cm H2O, an appropriate diagnosis, and subjective clinical findings. It is recommended to start NIV in these patients as soon as possible.
    3. In acute respiratory failure, there are no universally used protocols for NIV weaning. Weaning can begin when the patient’s respiratory and gas exchange status are normalizing, e.g., the respiratory rate is ≥ 12 and ≤ 22 breaths per minute, the patient is hemodynamically stable, and the peripheral oxygen saturation is ≥ 90% while on ≤ 60% FiO2 and as the patient can tolerate the procedure. There are no universally used protocols for NIV weaning I chronic respiratory failure.
  2. To wean SCI patients who are endotracheally intubated and to wean SCI patients who have a tracheostomy and are ventilator-dependent and as an aid to tracheal decannulation (Ceriana et al., 2019; Guia et al., 2021; Ker et al., 2021; Schrieber et al., 2021; Toki et al., 2021).
    1. The use of NIV for weaning SCI patients is not new. Bach & Alba (1990) described a case series of 23 quadriplegics, ventilator-dependent patients with tracheostomies who were treated with NIV. Seventeen of the patients had their tracheostomies closed. The authors concluded that chronic SCI patients with a tracheostomy could be managed by NIV, and reports of other similar cases have been published in the medical literature (Kim et al., 2017; Rybczynski et al., 2019).  

Non-invasive ventilation as a technique for weaning and (hopefully) decannulating SCI patients has many benefits. It can help avoid many of the complications of acute and long-term tracheostomy tube placement, and it has been used successfully (Guia et al., 2021; Ker et al., 2021; Toki et al., 2021). Most SCI patients who have ventilatory insufficiency should be considered for NIV weaning, and it is recommended to begin NIV weaning as soon as possible (Toki et al., 2021; Guia et al., 2021)

To be considered as a candidate for NIV weaning, patients should (Ker et al., 2021; Toki et al., 2021):

  • Be fully awake, cooperative, and not using sedation.
  • Not have a swallowing disorder.
  • Be able to cough.
  • Have no organ failure or infection.
  • Have an oxygen saturation > 95% without supplemental oxygen.
  • Have an arterial carbon dioxide partial pressure ≤ 40 mm Hg.
  • Have a peak inspiratory pressure (PIP) < 35 cm H2O.

This weaning technique has been successfully used, but it has not been well studied. It is noted that there are no established guidelines/protocols for the indications for and timing of NIV weaning (Hill & Kramer, 2022; Guia et al., 2021; Ker et al., 2021; Toki et al., 2021)

Respiratory Electrostimulation: Phrenic and Diaphragmatic Pacemakers

Phrenic or diaphragmatic pacemakers are a form of respiratory support that may be used for the partial or complete withdrawal of mechanical ventilation in patients with SCI, thereby improving their quality of life (Wijkstra et al., 2022).

Electrostimulation of the phrenic nerve consists of triggering diaphragmatic contractions through direct electrical stimulation of the phrenic nerve in the neck and chest.

Candidates for electrostimulation include patients with (Marion, 2022; Wijkstra et al., 2022):

  • Functional phrenic nerves and diaphragm
  • No severe airway disease or pulmonary parenchyma
  • Spinal injuries above C4

It is, therefore, necessary before implantation to perform phrenic nerve conduction studies (Vashisht & Chowdry, 2021). The pacing electrodes can be placed in the chest, the diaphragm, or the neck. After implantation, a period of diaphragmatic conditioning is needed to improve the muscle tone of the diaphragm, which may have atrophied due to lack of use (Marion, 2022).

Patients will often be on electrophrenic respiration for part of or the whole day, and then during the night, the patient will receive ventilator support (Vázquez et al., 2013).

Advantages of electrophrenic respiration include (DiMarco, 2013):

  • Fewer episodes of infection when compared to conventional ventilation.
  • Greater survival with a better quality of life due to improved sociability, convenience, and mobility.

Regarding quadriplegic/tetraplegic patients who have an inadequate function of the phrenic nerves and in whom the implantation of phrenic/diaphragmatic pacemakers is not possible, there are experimental studies in animals that have suggested that high-frequency spinal cord stimulation (HF-SCS) may someday be an alternative approach for SCI patients (DiMarco & Kowalski, 2019).

Approximately 50% of tetraplegic patients who are ventilator-dependent will be able to achieve full-time ventilatory support with diaphragmatic pacing (DiMarco & Kowalski, 2019). It is important to note that diaphragmatic pacemakers only supplement the inspiratory function and do not replace the expiratory functions such as coughing or the removal of secretions. It is here where rehabilitation and external mechanical assistance have considerable importance.

Tracheostomy

Tracheostomy is a common procedure in patients with traumatic SCI, especially in cervical SCI or thoracic level with associated injuries.

Effective therapy in patients with cervical SCI consists of (Foran et al., 2022; Hansebout & Kuchar, 2018):

  • Early intubation
  • Tracheostomy (Long-term management)

For patients with incomplete injuries, evidence of respiratory failure should prompt immediate airway intervention with endotracheal intubation. Patients who have been endotracheally intubated are at risk for respiratory and other complications, and in many cases, an elective tracheostomy is performed to prevent these issues when prolonged mechanical ventilation is likely (Foran et al., 2022; Mubashir et al., 2021; Handesbout & Kuchar, 2018) (Foran et al., 2022).

Tracheostomy can make weaning easier by decreasing airway resistance, it can make suctioning easier and more effective, it reduces the complications of long-term endotracheal intubation, and it is more comfortable than endotracheal intubation (Foran et al., 2022).

Risk factors that indicate the need for post-injury tracheostomy include (Hansebout & Kuchar, 2018; Long et al., 2022; Yu et al., 2022):

  • Active pneumonia
  • Old age
  • Male gender
  • Comorbid lung diseases
  • High-level injury severity score
  • Preexisting comorbid illness
  • Low Glasgow Coma Scale score
  • Smoking history

Specific to a cervical SCI cohort, the extent of the injury was the most important factor in determining the need for a tracheostomy (Branco et al., 2011).

In a retrospective study, patients with high-thoracic SCI have more respiratory complications (including the need for tracheostomy and intubation), even after adjustment for age, sex, and Glasgow Coma Scale (GCS), compared with patients with low-thoracic SCI or thoracolumbar fractures (Cotton et al., 2005). In this study, respiratory complications significantly increased the mortality risk in less severely injured patients.

Winslow et al. (2022) noted that respiratory complications are as important as the level of injury is contributing to the prediction of length of stay.

The literature has suggested that early tracheostomy (within the first 7 days) has many advantages, including (but not limited to) (Foran et al., 2022; Mubashir et al., 2021):

  • Shorter duration of mechanical ventilation (MV)
  • Shorter ICU stay
  • Reduced risk of in-hospital mortality
  • Decreased duration of sedation
  • Decreased incidence of ventilator-associated pneumonia (VAP) 

However, Mubashir et al. (2021) notes that evaluating the available evidence is difficult and “. . .  it is challenging to make conclusive interpretations. Future prospective trials with a larger patient population are needed to fully assess short- and long-term outcomes of tracheostomy timing following acute SCI.” 

Several recent systematic reviews also found that early tracheostomy does not reduce mortality and finds no effect on the duration of MV or intensive care stay in a general critical care population (Foran et al., 2022).

Both surgical and percutaneous tracheostomies (PTs) can be safely performed in the ICU (Kaczmarek et al., 2017). A PT is done by making a small incision and then a blunt dilation of the trachea to insert the tracheostomy tube.

Advantages of PT include (Kaczmarek et al., 2017; Ramakrishnan et al., 2019)

  • PT is quicker to perform.
  • It can be done at the bedside, obviating the need to transfer critically ill, ventilated patients to the operating room.
  • A smaller incision with less bleeding.
  • Injury to the adjacent neck structures is minimized.
  • Lower rate of infection.

Patients who have had an SCI and will undergo spinal fusion surgery and a tracheostomy require special attention. The presence of a tracheostomy stoma could cause cross-contamination from the tracheostomy incision site to the spinal surgery incision site, and this has made the timing of the two procedures with each one an issue of concern (Galeiras et al., 2018). Performing the tracheostomy after the spinal surgery has typically been the approach, but the optimal time for separating the two procedures is not known. Although the research is limited, several studies found no infections or a very low rate of infection when a tracheostomy is done without waiting or with waiting several weeks after spinal surgery (Galeiras et al., 2018).

Tracheostomy reduces the work of breathing and reduces airway resistance, intrinsic positive end-expiratory pressure (PEEP), and peak inspiratory pressures (PIP) (Chen et al., 2019; Hyzy & McSparron, 2021a). Tracheostomy can also make ventilatory weaning easier (Hyzy & McSparron, 2021a).

Conservative Management of Respiratory Dysfunction

Although pulmonary complications are a common and well-known problem in SCI, there is relatively little information about their management. Despite years of experience and research, there are still many unknowns in the treatment of SCI, and treatment recommendations are, at times, based on clinical experience and expert opinion (Fehlings et al., 2017).

Many patients who have an SCI cannot generate sufficient lower intrathoracic and expiratory pressure to produce an effective cough and clear secretions (Berlowitz et al., 2016; Nygren-Bonnier et al., 2018). This puts them at risk for atelectasis, impaired gas exchange, and infections (Nygren-Bonnier et al., 2018). One of the most important goals of treating respiratory dysfunction in SCI patients is managing secretions to prevent these complications (Reyes et al., 2020; Vázquez et al., 2013)

Many techniques can be used to manage and clear secretions, including (but not limited to (Bach et al., 2020; Blakeman et al., 2022; Luo, 2021; Spinou, 2020; Reyes et al., 2020; Vázquez et al., 2013)

  • Postural drainage
  • Assisted coughing
  • Glossopharyngeal breathing
  • Respiratory muscle training
  • Percussion and vibration
  • Airway suctioning

Deciding what treatments should be used should be done on a case-by-case basis, and the need will be, obviously, greater for some patients. Bach et al. (2020) indicated that if an SCI patient does not have a tracheostomy and is medically stable, “. . . there is neither theoretic reason why, nor evidence that, routine chest oscillation, percussion, and vibration benefit them unless they have an acute pulmonary disease or are overwhelmed with peripheral secretions.”

Interventions for mobilizing secretions are essential for preventing mucus plugs, atelectasis, pneumonia, and respiratory failure and should be started early after the injury.

Postural Drainage

Postural drainage uses positioning to help move pulmonary secretions to the upper airway so that they can be removed by coughing or other methods (Luo, 2021; Vázquez et al., 2013).

The positioning of the patient with the affected lung area in the upper position allows for gravity to help in the drainage.

Different postural drainage positions can be used: 

  • Bach et al. (2020a) list nine
  • Luo (2021) lists five
  • Vázquez et al. (2013) list five

The position should be held for approximately 20 minutes, and postural drainage can be combined with percussion and vibration (Bach et al., 2020a). The goal is to drain the peripheral airway divisions (Bach et al., 2020a). To drain the six central airway divisions, an effective cough must be produced (Bach et al., 2020a).

Percussion and Vibration

Percussion and vibration consist of external manipulations of the chest to mobilize secretions.

The technique of pulmonary percussion is done by tapping on the chest with a cupped hand. A percussion vest and hand-held percussion devices can be used as well, and percussion can be combined with postural drainage (Reyes et al., 2020; Vázquez et al., 2013). Vibration is essentially the same technique, except that a vibrating force is applied. The 11th and 12th ribs, often called the floating ribs, should not be contacted during percussion and vibration (Vázquez et al., 2013).

Contraindications to percussion and vibration include (Vázquez et al, 2013):

  • Acute hemoptysis
  • Chest burns and wounds
  • Fractured ribs
  • Increased intracranial pressure
  • Instability of the cardiovascular system
  • Pulmonary embolism
  • Significant pleural effusion
  • Tension pneumothorax
  • Unstable spine

Assisted Coughing Techniques

An intact, normal cough is necessary to clear airway secretions. Patients who have had an SCI, for several reasons, often have a weak and ineffective cough, putting them at risk for pulmonary complications like atelectasis and pneumonia (Reyes et al., 2020; Vázquez et al., 2013). Assisted coughing techniques that target the inspiratory or expiratory phase to either assist a cough or stimulate a cough are commonly used as preventive therapy (Reyes et al., 2020; Spinou, 2020; Vázquez et al., 2013). Assisted coughing techniques that can be used are discussed below.

Assisted coughing techniques have been used for many years, and the research indicates that all the commonly used techniques can improve airway clearance, and adverse effects are uncommon (Morrow et al., 2021; Spinou, 2020). However, there is little evidence that can be used to compare techniques, and what evidence there is suggests that in terms of improving peak cough flow, the assisted cough techniques are similar (Morrow et al., 2021; Spinou, 2020).

Manually Assisted Coughing

This maneuver consists of abdominal thrusts directed posteriorly and towards the patient’s head (Bach, 2020). The patient inhales, coughs, and the abdominal thrust is done (Reyes et al., 2020). The effectiveness of manually assisted coughing can be improved with the prior administration of nebulized saline to thin the secretions. Contraindications to manually assisted coughing include (Spinou, 2020):

  • Internal abdominal complications
  • The recent placement of a vena cava filter
  • Rib fractures
  • Unstable spine in traction

Mechanically Assisted Coughing

This procedure, also called Mechanical Insufflation-Exsufflation, is begun by applying positive pressure to the airway (insufflation) using a mechanical device and via a face mask, mouthpiece, tracheostomy to immediately afterward transform this positive pressure into negative pressure (exsufflation) (Bach, 2020; Reyes et al., 2020; Vázquez et al., 2013)

The lungs are fully inflated and then fully emptied within 4 to 6 seconds, and a sudden change of pressure occurs within 0.02. seconds is enough to effectively clear respiratory secretions (Bach, 2020).

There is some evidence that cough peak flow (the maximum amount of airflow generated during a cough) is improved when a manually assisted cough and mechanical insufflation-exsufflation are used together (Spinou, 2020). There is evidence that suggests that mechanical insufflation-exsufflation is better than manually assisted coughing for improving cough peak flow (Spinou, 2020). An anticholinergic or a beta2 agonist bronchodilator may increase the effectiveness of mechanical insufflation-exhalation if administered prior to simulated cough (Bach et al., 2020a)

Advantages in the use of an insufflation-exsufflation device during intensive and post-intensive care may be (Vázquez et al., 2013)

  • Reduction in the number of bronchoscopies
  • Reduction in the number of respiratory complications
  • Reduction in weaning time

Contraindications to the use of insufflation-exsufflation devices include (Reyes et al., 2020; Vázquez et al., 2013):

  • History of barotrauma, e.g., pneumothorax, pneumomediastinum, presence of an IVC filter
  • Presence of pulmonary bullae 

Glossopharyngeal Breathing

Glossopharyngeal breathing has been used for decades as a way of improving cough effectiveness and pulmonary function (Nygren-Bonnier et al., 2018; Spinou, 2020; Reyes et al., 2020). The patient is instructed to do a total lung capacity maneuver and then to use his/her mouth and throat muscles to inhale as many gulps of air as possible, followed by a passive exhalation (Berlowitz et al., 2016; Nygren-Bonnier et al., 2018; Reyes et al., 2020).

Glossopharyngeal breathing can be difficult and uncomfortable to do, but it can improve peak cough flow, total lung capacity, and vital capacity (Nygren-Bonnier et al., 2018; Reyes et al., 2020). This technique can cause dizziness, syncope, and abnormal changes in blood pressure and heart rate (Nygren-Bonnier et al., 2018). Therefore, it is vital that patients must be instructed on how to do glossopharyngeal breathing correctly.

Airway Suctioning

Airway suctioning is an important part of secretions management in patients who have an artificial airway (Blakeman et al., 2022). Blakeman et al. (2022) reviewed the available literature and made these recommendations for the practice of artificial airway suctioning:

  • The indications for suctioning are:
    • Breath sounds
    • Visual secretions in the artificial airway
    • A sawtooth pattern on the ventilator waveform
  • As-needed suctioning only, not scheduled suctioning, is recommended.
  • Close and open suctioning can be used. Use a sterile technique when doing open suctioning.
  • Preoxygenate patients before suctioning.
  • Avoid instilling normal saline before suctioning.
  • Suction pressure should be < -200 mmHg in adults, and < -120 mmHg in pediatric and neonates.
  • Limit suctioning time to 15 seconds or less.
  • Deep suctioning should only be used when shallow suctioning is ineffective.
  • There is very little information on using bronchoscopy for secretion removal. Routine use of bronchoscopy to remove secretions is not recommended. There is no question that bronchoscopy with alveolar lavage is an effective method for removing secretions, but it is not exempt from complications such as tracheobronchial irritation, edema, and aspiration. The technique should be reserved for patients who do not respond to more conservative measures or for taking microbiological samples.

Complications of suctioning include increased arterial pressure, increased heart rate, cardiac arrhythmias, and oxygen desaturation. Preoxygenation, sedation, and suctioning as needed may help avoid these complications (Blakeman et al., 2022).

Respiratory Muscle Training (RMT)

Respiratory muscle training (RMT) has been successfully and safely used for patients who have had an SCI (Berlowitz & Tamplin, 2013; Boswell-Ruys et al., 2020; McDonald & Stiller, 2019; Reyes et al., 2020; Wang et al., 2021)

A wide variety of devices and techniques have been used for RMT, including (but not limited to) (Boswell-Ruys et al., 2020):

  • Breathing against abdominal weights
  • Glossopharyngeal breathing
  • Incentive flow spirometry
  • Positive expiratory pressure devices
  • Resistance devices

No evidence supports one type of RMT in favor of another. Although the current research indicates that RMT is a useful therapy for patients who have had an SCI, evidence of its support has come from small studies (Berlowitz & Tamplin, 2013; Boswell-Ruys et al., 2020; Bach et al., 2020a). RMT can also increase muscle strength. However, these gains can quickly be lost, so RMT needs to be ongoing, and the increase in muscle strength may not necessarily help prevent respiratory complications (Bach et al., 2020a).

Case Study

Scenario/Patient Description

Per EMS (1900): At approximately 18:00, 18-year-old Thomas Hutton dove face-first into the 3-foot end of a cement swimming pool after drinking beer all afternoon with his friends. He hit his forehead on the bottom of the pool. His friends pulled him out of the pool while calling 911. He has not regained consciousness since.

Upon arrival in the emergency department, EMS reports:

  • GCS: 3
  • BP: 150-170/70-80
  • HR: 140-160, sinus tachycardia
  • RR: 40-50, rapid, shallow
  • SaO2: 87-90%

The patient is on a backboard with a semi-rigid cervical collar in place.

A 20-gauge peripheral IV was placed in the left antecubital with 1000 ml Normal Saline infusing at 100 ml/hr. Patient on 100% rebreather mask with oral airway inserted.

Intervention

  • Continue backboard and semi-rigid collar.
  • Continue monitoring GCS.
  • Place EKG leads to cardiac monitoring.
  • Place pulse oximetry.
  • Place BP cuff.
  • Insert another 20 gauge IV into the right antecubital vein while drawing stat Hgb/Hct, blood ETOH level serum electrolytes, coagulation studies, and cell blood counts.
  • Bedside fingerstick for a blood glucose level.
  • Draw ABG for stat results.
  • Insert urinary catheter and send stat urine drug screen to the lab.
  • Inspect, palpate, percuss, and auscultate the following systems where feasible: neurologic, integumentary, pulmonic, cardiovascular, abdominal, urinary
  • Imaging studies:
    • Chest x-ray: AP and lateral
    • Cervical spine x-rays: AP, lateral and odontoid
    • Head and neck CT
  • Continue to try to locate family to ascertain information about drug allergies, current medication and immunization status, and past medical and surgical history.

Discussion of Outcomes

GCS continues at 3.
Chest x-rays show pulmonary infiltrates.
Cervical spine x-rays indicate an extension teardrop fracture at C2, with neck CT confirming the diagnosis.
Head CT shows a fracture of the frontal bone with a hematoma at the base of the occiput.
All laboratory tests WNL except:

  • Blood alcohol level 0.42
  • ABG’s show acute respiratory acidosis: pH 7.26, PaO2 75, PaCO2 56, HCO3 24, BE -4

Continuing GCS of 3 with imaging studies indicative of a severe head injury and an extension teardrop fracture at C2: A neurologist and neurosurgeon should be consulted.

Chest x-ray indicating pulmonary infiltrates and respiratory acidosis coupled with continuing hypertension, rapid, shallow respirations, and lower than expected SaO2 per oximetry: Emergent intubation indicated.

Conclusion

Pulmonary physiologic changes due to SCI are related to the extent of neurological impairment. The American Spinal Injury Association Impairment Scale (AIS) is used to classify the degree of impairment that is based on strength in key muscles and a sensory examination.

Immediately after SCI, flaccid paralysis affects all muscles caudal to the level of injury (i.e., spinal shock). Subsequent improvements in pulmonary function are due primarily to functional descent of the neurologic injury level as spinal cord inflammation resolves, enhanced recruitment of accessory ventilatory muscles, retraining of deconditioned muscles, and the evolution from flaccid to spastic paralysis.

The extent of ventilatory muscle impairment depends upon the degree and location of the injury, as well as the duration of time since the injury. The higher the level and more complete the injury, the more likely it is that there will be respiratory muscle dysfunction. Complete injury above C3 produces near-total ventilatory muscle paralysis because the phrenic nerve, which innervates the diaphragm, arises from the third to fifth cervical roots.

Immediately after an SCI, flaccid paralysis can occur, affecting all the muscles that are caudal to the level of injury. This physiologic state is known as spinal shock or spinal paralysis. This state may continue for days or months, and during this time, pulmonary function is impaired. This is primarily due to impairment of the muscles of respiration but also due to a decrease in chest compliance, decreased airflow, hyper-responsiveness of the bronchial passages, and an abnormally blunted response to hypercapnia.

After the resolution of spinal paralysis, spastic paralysis occurs. During spastic paralysis, muscle tone is increased, and pulmonary function should improve. This happens several days or several weeks after the injury. Improvement in respiratory muscle performance after SCI largely occurs in the first year following injury.

Assessment of pulmonary function in SCI patients is done with PFTs.  Performing PFTs and calculations of the predicted PFT values need to be adjusted/modified when doing PFTs in patients who have had an SCI. Many SCI patients will have abnormal PFTs, but there is an improvement over the first few months-year after the injury. 

After an SCI, the long-term course of pulmonary function can be a decline, stability, or improvement.  

Approximately 90% of patients who have had a traumatic SCI will need intubation, and up to 40% of patients who had a complete cervical lesion will become ventilator-dependent. It is best to proceed with intubation under controlled circumstances rather than waiting until the condition becomes an emergency, as hypoxia in an SCI patient can adversely affect the patient’s neurological and many patients who have cervical spinal cord injury have a delayed onset of respiratory complications. Intubation is necessary for managing secretions, and SCI is often accompanied by many complications like trauma, coma, ARDS, and multi-organ system insufficiency. In these situations, non-invasive ventilation will not be effective. There are no specific criteria for ventilator settings that are specific to SCI patients.

If it is likely that the patient may be ventilator-dependent for a long time, a tracheostomy is recommended. Tracheostomy can make weaning easier by decreasing airway resistance, it can make suctioning easier and more effective, it reduces the complications of long-term endotracheal intubation, and it is more comfortable than endotracheal intubation. Tracheostomy can be done at the bedside (PT) or in the OR.

In regard to criteria for weaning eligibility, Garshick (2020) wrote: “The accuracy of weaning predictors (e.g., rapid shallow breathing index) in predicting weaning success has not been specifically addressed in this patient population, and we typically follow standard clinical criteria for weaning . . .” Schreiber et al. (2021) indicates that the probability of weaning success continues to be difficult to predict as there are no previous systematic review or meta-analysis has been conducted on the topic. Schreiber et al. (2021) also state that there are no societal guidelines or recommendations on weaning that are available and specific to this population of patients. Therefore, the typical weaning protocol is utilized. This protocol is alternating periods of exercise (the patient is disconnected from the ventilator) and rest (the patient is reconnected to the ventilator).

Conservative methods of preventing respiratory complications in SCI patients include:

  • Postural drainage
  • Assisted coughing
  • Glossopharyngeal breathing
  • Percussion and vibration
  • Airway suctioning
  • RMT 

Phrenic or diaphragmatic pacemakers are a form of respiratory support that may be used for the partial or complete withdrawal of mechanical ventilation in patients with SCI. Electrostimulation of the phrenic nerve consists of triggering diaphragmatic contractions through direct electrical stimulation of the phrenic nerve in the neck and chest.

Non-invasive ventilation (NIV) is defined as the delivery of positive pressure ventilation without the use of an invasive device and by way of a noninvasive device like a face mask, a nasal mask, or nasal prongs. Non-invasive ventilation can be delivered by a standard or portable ventilator. The two commonly used modes of delivery are bilevel NIV, commonly called bilevel positive airway pressure (BPAP – not BiPAP), and continuous positive airway pressure, CPCP. Non-invasive ventilation is a well-established technique that can be used to treat patients who are not intubated or do not have a tracheostomy. It can also be used for those who have acute or chronic respiratory dysfunction caused by a neuromuscular or chest wall disease, including SCI. In addition, it can also be used to wean SCI patients who are endotracheally intubated, those who have a tracheostomy and are ventilator-dependent, as well as for those requiring tracheal decannulation.

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Implicit Bias Statement

CEUFast, Inc. is committed to furthering diversity, equity, and inclusion (DEI). While reflecting on this course content, CEUFast, Inc. would like you to consider your individual perspective and question your own biases. Remember, implicit bias is a form of bias that impacts our practice as healthcare professionals. Implicit bias occurs when we have automatic prejudices, judgments, and/or a general attitude towards a person or a group of people based on associated stereotypes we have formed over time. These automatic thoughts occur without our conscious knowledge and without our intentional desire to discriminate. The concern with implicit bias is that this can impact our actions and decisions with our workplace leadership, colleagues, and even our patients. While it is our universal goal to treat everyone equally, our implicit biases can influence our interactions, assessments, communication, prioritization, and decision-making concerning patients, which can ultimately adversely impact health outcomes. It is important to keep this in mind in order to intentionally work to self-identify our own risk areas where our implicit biases might influence our behaviors. Together, we can cease perpetuating stereotypes and remind each other to remain mindful to help avoid reacting according to biases that are contrary to our conscious beliefs and values.

References

  • Andrade, M.J., Quintas, F.L., Silva, A.M. & Cruz, P. (2021). Is autonomic dysreflexia a cause of respiratory dysfunction after spinal cord injury? Spinal Cord Series and Cases;7(1):4. Visit Source.
  • Bach, J.R. (2020). Continuous noninvasive ventilatory support for patients with respiratory muscle dysfunction. UpToDate. August 20, 2020. Accessed February 25, 2022, Visit Source.
  • Bach, J.R., Burke, L. & Chiou, M. (2020a). Conventional Respiratory Management of Spinal Cord Injury. Physical Medicine and Rehabilitation Clinics of North America, 31(3), 379-395. Visit Source.
  • Bach, J.R. & Alba, A.S. (1990). Noninvasive options for ventilatory support of the traumatic high level quadriplegic patient. Chest, 98(3), 613-619. Visit Source.
  • Berlowitz, D.J., Wadsworth B. & Ross, J. (2016). Respiratory problems and management in people with spinal cord injury. Breathe (Sheff), 12(4), 328–340. Visit Source.
  • Berlowitz, D.J. & Tamplin, J. (2013). Respiratory muscle training for cervical spinal cord injury. Cochrane Database of Systematic Reviews, Jul 23;(7):CD008507. Visit Source.
  • Blakeman, T.C., Scott, J.B., Yoder, M.A., Capellari, E. & Strickland, S.L. (2022). AARC Clinical Practice Guidelines: Artificial Airway Suctioning. Respiratory Care, 67(2), 258-271. Visit Source.
  • Boswell-Ruys, C.L., Lewis, C.RH., Wijeysuriya, N.S., McBain, R.A., Lee, B.B., McKenzie, D.K., Gandevia, S.C. & Butler, J.E. (2020). Impact of respiratory muscle training on respiratory muscle strength, respiratory function and quality of life in individuals with tetraplegia: A randomised clinical trial. Thorax, 75(3), 279-288. Visit Source.
  • Branco, B.C., Plurad, D., Green, D.J., Inaba, K., Lam, L., Cestero, R., Bukur, M. & Demetriades, D. (2011). Incidence and clinical predictors for tracheostomy after cervical spinal cord injury: a National Trauma Databank review. Journal of Trauma, 70(1):111-5. Visit Source.
  • Ceriana, P., Nava, S., Vitacca, M., Carlucci, A., Paneroni, M., Schreiber, A, Pisani L. & Ambrosino, N. (2019). Noninvasive ventilation during weaning from prolonged mechanical ventilation. Pulmonology, 25(6), 328-333. Visit Source.
  • Chen, G-Q., Sun, X-M., Wang, Y-M., Zhou, Y-M., Chen, J-R., Cheng, K-M., Yang, Y-L. & Zhou, J-X. (2019). Additional expiratory resistance elevates airway pressure and lung volume during high-flow tracheal oxygen via tracheostomy. Science Reports, 10;9(1):14542. Visit Source.
  • Costanzo, L.S. (2018). Chapter 5: Respiratory Physiology. In L.S. Costanzo. Physiology (6th Ed), (pp 191-197). Elsevier. Visit Source.
  • Cotton, B.A., Pryor, J.P., Chinwalla, I., Wiebe, D.J., Reilly, P.M., & Schwab, C.W. (2005). Respiratory complications and mortality risk associated with thoracic spine injury. Journal of Trauma, 59(6), 1400-1407; discussion 1407-1409. Visit Source.
  • Daoud, A., Haider, S. & Sankari, A. (2020). Noninvasive ventilation and spinal cord injury. Sleep Medicine Clinics, 15(4), 461-470. Visit Source.
  • De Troyer, A., Estenne, M. & Heilporn, A. (1986). Mechanism of active expiration in tetraplegic patients. New England Journal of Medicine, 314(12),740-744. Visit Source.
  • Diggisie, A., Argaw, A. & Belachew, T. (2018). Developing an equation for estimating body height from linear body measurements of Ethiopian adults. Journal of Physiological Anthropology, 26;37(1):26. Visit Source.
  • DiMarco, A.F. & Kowalski, K.E. (2019). High-frequency spinal cord stimulation in a subacute animal model of spinal cord injury. Journal of Applied Physiology (1985), 27(1), 98-102. Visit Source.
  • DiMarco, A.F. (2013). Chapter 62: Diaphragmatic Pacing. In M.J. Tobin (Ed). Principles and Practice of Mechanical Ventilation (Online edition). McGraw-Hill Education. Accessed February 25, 2022. Visit Source.
  • Estenne M., Knoop, C., Heilporn, A. De Troyer, A. (1989). The effect of pectoralis muscle training in tetraplegic subjects. American Review of Respiratory Diseases, 139(5,1218-1222. Visit Source.
  • Fehlings, M.G., Kwon, B.K. & Tetreault, L.A. (2017). Guidelines for the Management of Degenerative Cervical Myelopathy and Spinal Cord Injury: An Introduction to a Focus Issue. Global Spine Journal, 7(3 Suppl), :6S-7S. Visit Source.
  • Foran, S.J., Taran, S., Singh, J.M., Kutsogiannis, D.J. & McCredie, V. (2022). Timing of tracheostomy in acute traumatic spinal cord injury: A systematic review and meta-analysis. Journal of Trauma and Acute Care Surgery, 92(1):223-231. Visit Source.
  • Füssenich, W., Araujo S.H., Kowald, B., Hosmann, A., Auerswald, M. & Thietje, R. (2018). Discontinuous ventilator weaning of patients with acute SCI. Spinal Cord, 56(5), 461-468. Visit Source.
  • Galeiras, R., Mourelo, M., Bouza, M.T., Seoane, M.T., Ferreiro, M.E., Montonio, A., Salvador, A., Seoane, L. & Freire, D. (2018). Risk analysis based on the timing of tracheostomy procedures in patients with spinal cord injury requiring cervical spine surgery. World Neurosurgery, Aug;116: e655-e661. Visit Source.
  • Garshick, E. (2021). Respiratory physiologic changes following spinal cord injury. UptoDate, December 10, 2021. Accessed February 24, 2022. Visit Source.
  • Garshick, E. (2020). Respiratory complications in the adult patient with chronic spinal cord injury. UpToDate, December 10, 2020. Accessed February 24, 2022, Visit Source.
  • Guia, M., Ciobanu, L.D., Sreedharan, J.K., Abdelrahim, M.E., Gonçalves, G., Cabrita, B., Algahtani, J.S., Duan, J., El-Khatib, M., Diaz-Abad, M., Wittenstein, J., Karim, H.M.R., Bhakta, P., Ruggeri, P., Garuti, G., Burns, K.E.A., So Hoo, G.W., Scala R., Wsquinas, A. & International Association of Non-Invasive Ventilation. (2021). The role of non-invasive ventilation in weaning and decannulating critically ill patients with tracheostomy: A narrative review of the literature. Pulmonology, 27(1),43-51. Visit Source.
  • Guzel, S., Umay, E., Gundogdu, I., Bahtiycata, Z.T. & Cankurtaran, D. (2022). Effects of diaphragm thickness on rehabilitation outcomes in post-ICU patients with spinal cord and brain injury. European Journal of Trauma and Emergency Surgery, 48(1), 559-565. Visit Source.
  • Hachmann, J.T., Calvert, J.S., Grahn, P.J., Drubach, D.I., Lee, K.H. & Lavrov, I.A. (2017). Review of epidural spinal cord stimulation for augmenting cough after spinal cord injury. Frontiers in Human Neuroscience, Mar 28;11:144. Visit Source.
  • Hansebout, R.R. & Kachur, E. (2018) Acute traumatic spinal cord injury. UpToDate, July 18, 2018. Accessed February 24, 2022. Visit Source.
  • Hill, M, Jörgensen, S., Engström, G., Persson, M., Wollmer, P. & Lexell, J. (2022). Functional and structural impairments of the pulmonary system in middle-aged people with cervical and upper thoracic spinal cord injuries. Journal of Spinal Cord Medicine, Feb 23;1-10. Visit Source.
  • Hill, N.S. & Kramer, N.R. (2022). Noninvasive ventilation in adults with chronic respiratory failure from neuromuscular and chest wall diseases: Patient selection, alternative modes of ventilatory support. UpToDate. February 28, 2022. Accessed March 2, 2022. Visit Source.
  • Hyzy, R.C. & McSparron, J.I. (2021a). Tracheostomy: Rationale, indications, and contraindications. UpToDate. December 9, 2021. Accessed February 25, 2022. Visit Source.
  • Hyzy, R.C. & McSparron, J.I. (2021b) Noninvasive ventilation in adults with acute respiratory failure: Practical aspects of initiation. UpToDate. July 29, 2021. Accessed March 2, 2022. Visit Source.
  • Kaczmarek, C., Acch, M., Hoffman, M.F., Yilmaz, E., Waydhas, C., Schildhauer, T.A. & Hamsen, U. (2017). Early percutaneous dilational tracheostomy does not lead to an increased risk of surgical site infection following anterior spinal surgery. Journal of Trauma and Acute Care Surgery, 82(2), 383-386. Visit Source.
  • Ker, S., Leow, L.C. & Lee, Y.L. (2021). Mouthpiece noninvasive ventilation in a patient with traumatic cervical spinal cord injury: A case report. A & A Practice, May 27;15(6): e01480. Visit Source.
  • Kim, D.H., Kang, S.W., Choi, W.A., Oh, H.J. (2017). Successful tracheostomy decannulation after complete or sensory incomplete cervical spinal cord injury. Spinal Cord, 55(6), 601-605. Visit Source.
  • Levine, S., Ngyuen, T., Friscia, M.E., Budak, M.T., Rothenberg, P., Zhu, J., Sachdeva, R., Sonnad, S., Kaiser, L.R., Rubinstein, N.A., Powers, S.K. & Shrager, J.B. (2008). Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. New England Journal of Medicine, 358(13), 1327-1335. Visit Source.
  • Long, P-P., Sun, D-W., & Zhang, Z-F. (2022). Risk factors for tracheostomy after traumatic cervical spinal cord injury: A 10-year study of 456 patients. Orthopedic Surgery, 14(1), 10-17. Visit Source.
  • Luo, M. (2021). Toward an optimized strategy of using various airway mucus clearance techniques to treat critically ill COVID-19 patients. Biocell, 46(6),855-871. Visit Source.
  • McDonald, T., & Stiller, K. (2019). Inspiratory muscle training is feasible and safe for patients with acute spinal cord injury. Journal of Spinal Cord Medicine, 42(2), 220-227. Visit Source.
  • Marion, D.W. (2022). Pacing the diaphragm: Patient selection, evaluation, implantation, and complications. UpToDate. January 3, 2022. Accessed February 25, 2022. Visit Source.
  • Morrow, B., Argent, A., Zampoli, M., Human, A., Corten, L. & Toussaint, M. (2021). Cough augmentation techniques for people with chronic neuromuscular disorders. Cochrane Database of Systematic Reviews, 2021 Apr 22;4(4):CD013170. Visit Source.
  • Mubashir, T., Arif, A.A., Ernest, P., Maroufy, V., Chaudry, R., Balogh, J., Suen, C., Reskallah, A. & Williams, G.W. (2021). Early versus late tracheostomy in patients with acute traumatic spinal cord injury: A systematic review and meta-analysis. Anesthesia and Analgesia,132(2), 384-394. Visit Source.
  • Naqvi, U. & Sherman, A.l. Muscle Strength Grading. (2021). In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2022 Jan-Accessed February 24, 2022. Visit Source.
  • Nygren-Bonnier, M., Schiffler, T.A. & Lindholm, P. (2018). Acute effects of glossopharyngeal insufflation in people with cervical spinal cord injury. Journal of Spinal Cord Medicine, 41(1), 85–90. Visit Source.
  • Olivero, J.J. (2020). Caring for Patients with Spinal Cord Injuries. Methodist Debakey Cardiovascular Journal, 16(3), 250-251. Visit Source.
  • Pothirat, C., Chaiwong, W. & Phetsuk, N. (2015). Impact of direct substitution of arm span length for current standing height in elderly COPD. International Journal of Chronic Obstructive Pulmonary Disease, Jun 22;10, 1173-1778. Visit Source.
  • Qian, Z., Yang, M. & Chen, Y. (2018). Ultrasound assessment of diaphragmatic dysfunction as a predictor of weaning outcome from mechanical ventilation: a systematic review and meta-analysis. BMJ Open, Oct 4;8(9): e021189. Visit Source.
  • Raab, A.M., de Groot, S., Berlowitz, D.J., Post, M.W.M, Adriaansen, J., Hopman, M. & Mueller, G. (2019). Development and validation of models to predict respiratory function in persons with long-term spinal cord injury. Spinal Cord, 57(12),1064-1075. Visit Source.
  • Ramakrishnan, N., Singh, J.K., Gupta, S.K., Bhalla, V., Singh, D.K., Sheetal, R. & Kumari, A. (2019). Tracheostomy: Open surgical or percutaneous? An effort to solve the continued dilemma. Indian Journal of Otolaryngology and Head and Neck Surgery, 71(3), 320-326. Visit Source.
  • Randleman, M., Zholudeva, L.V., Vinit, S. & Lane, M.A. (2021). Respiratory training and plasticity after cervical spinal cord injury. Fronter in Cellular Neuroscience, Sep 21;15:700821. Visit Source.
  • Reardon, P.M., Wong, J., Fitzpatrick, A. Goligher, E.W. (2021). Diaphragm function in acute respiratory failure and the potential role of phrenic nerve stimulation. Current Opinions in Critical Care, 27(3), 282-289. Visit Source.
  • Reyes, M.R., Elmo M.J., Mehachem B. & Granda, S.M. (2020). A primary care provider's guide to managing respiratory health in subacute and chronic spinal cord injury. Topics in Spinal Cord Injury Rehabilitation, 26(2), 116-122. Visit Source.
  • Rybczynski, S., Celedon Flanders, X., Murphy, C., Hughes, D. & Rber, P. (2019). Case Report: Ventilator weaning, tracheostomy decannulation and noninvasive ventilation in an adolescent with autism spectrum disorder and new onset spinal cord injury. Spinal Cord Series and Cases, Dec 13;5:102. Visit Source.
  • Sánchez, J.A.S, Sharif S., Costa, F., Rangel, J.A.I.R, Nania, C.D. & Zileli, M. (2020). Early Management of Spinal Cord Injury: WFNS Spine Committee Recommendations. Neurospine, 17(4), 759-784. Visit Source.
  • Schreiber, A.F., Garlasco, J., Vieria, F., Lau, Y.H., Stavi, D., Lightfoot, D., Rigamonti, A., Burns, K., Friedrich, J.O., Singh, J.M. & Brochard, L.J. (2021). Separation from mechanical ventilation and survival after spinal cord injury: A systematic review and meta-analysis. Annals of Intensive Care, 24;11(1):149. Visit Source.
  • Schilero, G.J., Bauman, W.A. & Radulovic, M. (2018a). Traumatic spinal cord injury: Pulmonary physiologic principles and management. Clinics in Chest Medicine, 39(2), 411-425. Visit Source.
  • Schilero, G.J., Hobson, J.C., Singh, K., Spungen, A.M., Bauman, W.A. & Radulovic, M. (2018b). Bronchodilator effects of ipratropium bromide and albuterol sulfate among subjects with tetraplegia. Journal of Spinal Cord Medicine, 41(1), 42-47. Visit Source.
  • Soták, M., Roubik, K., Henlín, T. & Tyll, T. (2021). Phrenic nerve stimulation prevents diaphragm atrophy in patients with respiratory failure on mechanical ventilation. BMC Pulmonary Medicine, Oct 8;21(1):314. Visit Source.
  • Spinou, A. (2020). A review on cough augmentation techniques: Assisted inspiration, assisted expiration and their combination. Physiology Research, 27;69(Suppl 1), S93-S103. Visit Source.
  • Toki, A., Nakamura, T., Nishimura, Y., Sumida, M. & Tajima, F. (2021). Clinical introduction and benefits of non-invasive ventilation for above C3 cervical spinal cord injury. Journal of Spinal Cord Medicine, 44(1), 70-76. Visit Source.
  • Van Silfhout, L., Peters, A.E.J., Berlowitz, D.J., Schembri, R., Thijssen, D. & Graco, M. (2016). Long-term change in respiratory function following spinal cord injury. Spinal Cord, 54(9), 714-719. Visit Source.
  • Vashisht, R. & Chowdhury, Y.S. (2021). Diaphragmatic Pacing. [Updated 2021 Dec 14]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2022 Jan. Visit Source.
  • Vázquez, R.G., Sedes, P.R., Fariña, M.M., Marqués, A.M. & Velasco, M.E.F. (2013). Respiratory management in the patient with spinal cord injury. Biomedical Research International, 2013:168757. Visit Source.
  • Wang, H-C., Lin, Y-T., Huang, C-C., Lin, M-C., Liaw, M-Y., & Lu, C-H. (2021).  Effects of respiratory muscle training on baroreflex sensitivity, respiratory function, and serum oxidative stress in acute cervical spinal cord injury. Journal of Persian Medicine, May 5;11(5):377. Visit Source.
  • Wang, X., Zhang, N. & Xu, Y. (2020). Effects of respiratory muscle training on pulmonary function in individuals with spinal cord injury: An updated meta-analysis. Biomedical Research International, Feb 22; 2020:7530498. Visit Source.
  • Wijkstra, P.J., van der Aa, H., Hofker, H.S., Curto, F., Giacomini, M., Stagni, G., Agullo, M.A.D, Casanoves, F.X.C., Benito-Penalva, J., Martinez-Barenys, C. & Vidal, J. (2022). Diaphragm pacing in patients with spinal cord injury: A European experience. Respiration, 101(1), 18-24. Visit Source.
  • Winslow, C., Bode, R.K., Felton, D., Chen, D. & Meyer Jr., PR. (2002). Impact of respiratory complications on length of stay and hospital costs in acute cervical spine injury. Chest,121(5), 1548–1554. Visit Source.
  • Yonemitsu, T., Kinoshita, A., Nagata, K., Morishita, M., Yamaguchi, T. & Kato, S. (2021). Timely intubation with early prediction of respiratory exacerbation in acute traumatic cervical spinal cord injury. BMC Emergency Medicine, Nov 13;21(1):136. Visit Source.
  • Yu, W-K., Chen, Y-C., Chen, W-C., Su, V.Y-F., Yang, K-Y. & Kou, Y.R. (2022). Influencing factors for tracheostomy in patients with acute traumatic C3-C5 spinal cord injury and acute respiratory failure. Journal of the Chinese Medical Association JCMA, 85(2), 167-174. Visit Source.
  • Zakrasek, E.C., Nielson, J.L., Kosarchuk, J.J., Crew, J.D., Ferguson, A.R. & McKenna, S.L. (2017). Pulmonary outcomes following specialized respiratory management for acute cervical spinal cord injury: a retrospective analysis. Spinal Cord, 55(6):559-565. Visit Source.
  • Zambon, M., Greco, M., Bocchino, S., Cabrini, L., Beccaria, P.F. & Zangrillo, A. (2017). Assessment of diaphragmatic dysfunction in the critically ill patient with ultrasound: a systematic review. Intensive Care Medicine, 43(1), 29-38. Visit Source.
  • Zhu, Z., Li, J., Yang, D., Gao, F., Du, L. & Yang, M. (2021). Ultrasonographic evaluation of diaphragm thickness and excursion in patients with cervical spinal cord injury. Journal of Spinal Cord Medicine, 44(5), 742-747. Visit Source.
  • Zhu, Z., Li, J., Yang, D., Du, L. & Yang, M. (2019). Ultrasonography of diaphragm can predict pulmonary function in spinal cord injury patients: A pilot case-control study. Medical Science Monitor, Jul 20;25:5369-5374. Visit Source