Respiratory disorders are the leading cause of death for persons with both acute and chronic spinal cord injury (SCI), and much of the morbidity and mortality associated with respiratory disorders is related to acute respiratory infections. Pneumonia is the best recognized respiratory infection associated with mortality in this population. Recent evidence supports some management strategies that differ from those recommended for the general population. Upper respiratory tract infections and acute bronchitis may be precipitating factors in the development of pneumonia or ventilatory failure in patients with chronic SCI. This review emphasizes management principles for treatment and prevention of respiratory infections in persons with SCI.
Morbidity and mortality caused by respiratory infections
Respiratory disorders are the leading cause of death in persons with both acute and chronic spinal cord injury (SCI). Pneumonia occurs in 50% of patients with acute tetraplegia during acute hospitalization and rehabilitation . Respiratory disorders account for 28% of deaths in the first year after injury and 22% of deaths in later years . In patients who survive for at least 24 hours after injury, pneumonia or influenza causes 16.5% of all deaths . This contrasts with that of the general population of the United States, for which pneumonia and influenza account for only 2.5% of deaths and the two diseases in combination are the eighth leading cause of death . The standardized mortality ratio, a measure that adjusts for age, sex, and race, indicates that the rate of fatal pneumonia is elevated by a factor of 37 for people with SCI; persons with complete tetraplegia die from pneumonia at a rate that is 150 times higher than a matched population without SCI .
Respiratory disorders are also a leading cause of rehospitalization after SCI . Based on United States (US) Model SCI Systems (MSCIS) data, they are the third most common reason for hospitalization during the first year after SCI. A population-based study from Alberta, Canada found respiratory complications to be the leading cause of rehospitalization during the first 6 years after injury . For patients with C1 to C4 American Spinal Injury Association (ASIA) Impairment Scale A-C tetraplegia, they account for 30% of rehopitalizations across all years of follow-up .
In spite of the importance of respiratory infections as a cause of death in persons with SCI, few studies have examined the topic. The majority have reported on the incidence of respiratory complications during acute care and rehabilitation, in settings such as the MSCIS hospitals. Rehospitalization rates and causes of death in persons with chronic SCI have also been published using data from the US MSCIS as well as from other nations. More recently, data on outpatient respiratory infections in Veterans Affairs (VA) patients with SCI have been reported. The populations included in these studies may not be representative of all persons with SCI. Most have focused on epidemiologic aspects of respiratory infections. There remains a need to conduct clinical trials of preventive measures and treatments to reduce the morbidity and mortality associated with respiratory infections in this population.
Predisposing factors for persons with spinal cord injury
SCI can cause multiple alterations in normal physiology that may increase the likelihood of the development of respiratory infections (incidence) or increase the chance of dying from an infection (case fatality). The most obvious of these dysfunctions caused by SCI is weakness of the respiratory muscles. If the neurologic level is at C5 or rostral, there may be some degree of diaphragm weakness or even complete paralysis with higher level motor-complete injuries. At lower neurologic levels, diaphragm innervation is intact, and this normally is sufficient to maintain at least 60% of the predicted vital capacity. Ventilatory failure caused by inspiratory muscle weakness can occur immediately after injury or develop over the first week after the injury. Patients who require mechanical ventilation are susceptible to ventilator-associated pneumonia (VAP). Over the first weeks to months after injury, many patients with partially intact diaphragm innervation acquire the ability to spontaneously ventilate, which is in part caused by strength recovery in the diaphragm. Approximately 7% of persons with SCI will be ventilator dependent when discharged from rehabilitation . Patients with reduced inspiratory muscle strength are predisposed to microatelectasis, which may promote the development of pneumonia in atelectatic segments of the lung.
Severe expiratory muscle weakness is more prevalent in persons with SCI and is likely the most important factor increasing the incidence and case fatality for pneumonia. Expiratory muscle weakness, resulting in low voluntary cough peak expiratory flow, is strongly associated with unsuccessful extubation and increased in-hospital mortality in the general population . Because the primary expiratory muscles, the internal intercostals and abdominals, have thoracic innervation, they will be paralyzed completely in all patients with motor-complete tetraplegia. Expiratory strength increases incrementally with each additional neurologic level and is essentially normal at the T12 neurologic level and below; therefore, patients with high-level paraplegia have a similar degree of weakness to those with low-level tetraplegia. The main consequence of expiratory muscle weakness is a reduced peak cough flow, which is ineffective for clearance of bronchial secretions. With a peak cough flow of less than 2.7 L/sec (160 L/min), there is inadequate airflow to mobilize secretions out of the bronchi and trachea . To compensate for weak cough strength, aggressive multimodal respiratory therapy interventions are required for secretion mobilization . Measures to promote secretion mobilization are listed in Table 1 .
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Other than respiratory muscle weakness, additional factors predispose patients to respiratory complications. Reduced sympathetic innervation to the lungs occurs with injuries above the mid-thoracic level. The unopposed vagal parasympathetic input in patients with tetraplegia leads to bronchoconstriction and increased bronchial mucus secretion . In patients with acute tetraplegia, bronchial mucus production may exceed 1 L per day, and the secretions are often tenacious, likely because of an altered macromolecular composition . Aspiration is relatively common in patients with acute tetraplegia, especially those with predisposing factors such as mechanical ventilation, tracheostomy, anterior neck surgery, or brain injury . Autonomically mediated dynamic dysfunction of the pharynx and upper esophageal sphincter may be an additional contributing factor . In patients with chronic SCI, normal bacterial flora is altered for a number of reasons, including frequent treatment with antibiotics, autonomically mediated changes to the skin, or residence in health care settings, resulting in increased colonization with gram-negative and antibiotic-resistant organisms.
Subclinical adrenal insufficiency is common in this population, and this may blunt the response to sepsis once an infection is present. A diminished immune response in persons with tetraplegia has also been described, which could increase the susceptibility to infection . However, the antibody responses to both pneumococcal and influenza vaccinations in persons with SCI are similar to those in the general population .
Predisposing factors for persons with spinal cord injury
SCI can cause multiple alterations in normal physiology that may increase the likelihood of the development of respiratory infections (incidence) or increase the chance of dying from an infection (case fatality). The most obvious of these dysfunctions caused by SCI is weakness of the respiratory muscles. If the neurologic level is at C5 or rostral, there may be some degree of diaphragm weakness or even complete paralysis with higher level motor-complete injuries. At lower neurologic levels, diaphragm innervation is intact, and this normally is sufficient to maintain at least 60% of the predicted vital capacity. Ventilatory failure caused by inspiratory muscle weakness can occur immediately after injury or develop over the first week after the injury. Patients who require mechanical ventilation are susceptible to ventilator-associated pneumonia (VAP). Over the first weeks to months after injury, many patients with partially intact diaphragm innervation acquire the ability to spontaneously ventilate, which is in part caused by strength recovery in the diaphragm. Approximately 7% of persons with SCI will be ventilator dependent when discharged from rehabilitation . Patients with reduced inspiratory muscle strength are predisposed to microatelectasis, which may promote the development of pneumonia in atelectatic segments of the lung.
Severe expiratory muscle weakness is more prevalent in persons with SCI and is likely the most important factor increasing the incidence and case fatality for pneumonia. Expiratory muscle weakness, resulting in low voluntary cough peak expiratory flow, is strongly associated with unsuccessful extubation and increased in-hospital mortality in the general population . Because the primary expiratory muscles, the internal intercostals and abdominals, have thoracic innervation, they will be paralyzed completely in all patients with motor-complete tetraplegia. Expiratory strength increases incrementally with each additional neurologic level and is essentially normal at the T12 neurologic level and below; therefore, patients with high-level paraplegia have a similar degree of weakness to those with low-level tetraplegia. The main consequence of expiratory muscle weakness is a reduced peak cough flow, which is ineffective for clearance of bronchial secretions. With a peak cough flow of less than 2.7 L/sec (160 L/min), there is inadequate airflow to mobilize secretions out of the bronchi and trachea . To compensate for weak cough strength, aggressive multimodal respiratory therapy interventions are required for secretion mobilization . Measures to promote secretion mobilization are listed in Table 1 .
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Other than respiratory muscle weakness, additional factors predispose patients to respiratory complications. Reduced sympathetic innervation to the lungs occurs with injuries above the mid-thoracic level. The unopposed vagal parasympathetic input in patients with tetraplegia leads to bronchoconstriction and increased bronchial mucus secretion . In patients with acute tetraplegia, bronchial mucus production may exceed 1 L per day, and the secretions are often tenacious, likely because of an altered macromolecular composition . Aspiration is relatively common in patients with acute tetraplegia, especially those with predisposing factors such as mechanical ventilation, tracheostomy, anterior neck surgery, or brain injury . Autonomically mediated dynamic dysfunction of the pharynx and upper esophageal sphincter may be an additional contributing factor . In patients with chronic SCI, normal bacterial flora is altered for a number of reasons, including frequent treatment with antibiotics, autonomically mediated changes to the skin, or residence in health care settings, resulting in increased colonization with gram-negative and antibiotic-resistant organisms.
Subclinical adrenal insufficiency is common in this population, and this may blunt the response to sepsis once an infection is present. A diminished immune response in persons with tetraplegia has also been described, which could increase the susceptibility to infection . However, the antibody responses to both pneumococcal and influenza vaccinations in persons with SCI are similar to those in the general population .
Respiratory infections in outpatients
Pneumonia in the general population
Pneumonia is an acute infection of the pulmonary parenchyma, diagnosed by the presence of symptoms and either an infiltrate on chest radiograph or examination findings indicating consolidation. The most common and most widely studied epidemiologic category of pneumonia is termed community-acquired pneumonia (CAP). The most common CAP pathogen overall, as well as for fatal cases alone, is Streptococcus pneumoniae (pneumococcus). Other common pathogens include Hemophilus influenzae , Mycoplasma pneumonia , and Chlamydophila pneumoniae . Common risk factors for CAP include young or advanced age, medical comorbidities including chronic lung disease, smoking, immunosuppression, and alcoholism. Use of gastric acid-suppressive drugs (proton pump inhibitors and H2 blockers) also appears to be a risk factor for CAP .
Chest radiography is the primary test for establishing the diagnosis of CAP and distinguishing it from acute bronchitis. For patients who are hospitalized, it is recommended that they also have the following tests: complete blood count and differential, serum chemistry panel, liver function tests, oxygen saturation, and blood cultures . A sputum gram stain and culture has also been recommended, but its utility has been debated. A good-quality sputum with a predominant organism can only be obtained in 14% of patients. However, the presence of gram-positive diplococci on Gram stain is highly specific (98%) for pneumococcus .
Case fatality for CAP varies widely across studies with varying patient populations. Population-based data on patients receiving care in any setting (inpatient or outpatient) indicate a 1.5% to 2.3% mortality rate, whereas cohort studies indicate a 5.2% mortality rate . The Pneumonia Patient Outcome Research Team (Pneumonia PORT) derived an algorithm for determining whether adults with CAP should be hospitalized or treated in the community, based on short-term mortality risk . Patients are stratified into five severity classes, and outpatient treatment is generally recommended for the two lowest risk classes. To qualify for the lowest risk class, an adult would be age 50 years or less, have none of the important comorbidities (cancer, liver disease, congestive heart failure, renal disease, or cerebrovascular disease), have normal mental status, and have normal or only mildly abnormal vital signs. Patients in the two lowest risk categories are anticipated to have a short-term mortality risk of 0.5% or less. The rule is not meant to supersede clinical judgment, nor does it take into account other reasons for hospitalization besides the predicted risk of death from pneumonia. These could include the risk for other adverse events, the availability of support at home, and the likelihood of adherence to therapy and follow-up recommendations.
More recently, it has been recognized that specific outpatient populations with pneumonia are at increased risk for the same highly resistant bacterial pathogens that occur in hospitalized patients. In such cases, the pneumonia is more correctly defined as a health care–associated pneumonia (HCAP), rather than CAP . Risk factors for HCAP include the following: 2 or more days of acute care hospitalization in the prior 90 days; antibiotic therapy, chemotherapy, or wound care in the prior 30 days; residence in a nursing home or long-term care facility; or hemodialysis at a hospital or clinic. The etiologic pathogens in this population as well as treatment principles are thought to be similar to hospital-acquired pneumonia (HAP; see below).
Pneumonia in outpatients with spinal cord injury
Excess mortality caused by an acute condition in a specific population, as with pneumonia in persons with SCI, can be attributable to an increased incidence of the disorder, an increased case fatality when the disorder does develop, or a combination of both factors. There is limited evidence to support both an increased incidence and increased case fatality for pneumonia in persons with chronic SCI. The primary evidence comes from epidemiologic studies that used VA administrative data for persons with SCI.
Smith and colleagues determined outpatient visit rates for acute respiratory infections including pneumonia, based on administrative data for more than 8700 respiratory-related visits by a population of over 13,000 veterans with SCI. Annual outpatient visits for either pneumonia or influenza (nearly all of which were for pneumonia) averaged 29 to 35 per 1000 veterans. A smaller population-based study from Alberta, Canada reported a similar rate of 46 episodes of pneumonia per 1000 patients per year, during the first 6 years after injury. Comparable data for the overall US population indicate a rate of 10 cases of pneumonia per 1000 patients per year.
Using the same VA administrative data as in the study by Weaver and colleagues , the outcomes for pneumonia were estimated by determining hospitalization rates and all-cause mortality within 60 days of the visit. After outpatient visits for pneumonia, 46% of patients were hospitalized on the same day, and overall 7.9% of patients died within 60 days of the outpatient visit. By comparison, roughly 25% of the general population with pneumonia will be hospitalized for management . Because the VA study used administrative data, the link between pneumonia diagnosis and subsequent death was not clearly established. However, the case fatality appears to be much higher than the previously cited 1.5% to 2.3% case fatality seen in the general population .
Etiologic pathogens for CAP have also been examined using VA administrative data for all SCI veterans hospitalized for treatment of CAP during a 2-year period . The authors also determined whether identification of a causative pathogen for CAP was associated with outcomes in persons with SCI. Cases were identified as CAP if the hospital admission was preceded immediately by outpatient care with a diagnostic code for pneumonia. No significant association was found between the identification of a specific pathogen and mortality in 260 hospitalized SCI patients with CAP. The mean length of stay was 13.5 days, and the overall case fatality was 8.5%.
In that study, a causative pathogen was identified in 24% of cases, with pneumococcus the leading cause of pneumonia (32% of cases), as is true for the general population with CAP. Pseudomonas , which is an uncommon pathogen for CAP in the general population, was the second most commonly identified pathogen, occurring in 21% of cases. This finding should prompt clinicians to consider whether their patient with pneumonia has risk factors for HCAP rather than CAP. Pseudomonas colonization of the perineum, lower urinary tract, and urine collection system is common in persons with SCI and may be a risk factor for Pseudomonas pneumonia in this population . More well-recognized risk factors for gram-negative pneumonia, such as antibiotic treatment or hospitalization in the prior 30 days, pulmonary comorbidity, or aspiration , are relatively common in this population as well. In the general population, the relative risk of death is elevated by a factor of 2.6 to 6.4 with Pseudomonas pneumonia when compared with other pathogens .
An additional VA study characterized the clinical management of CAP at three VA hospitals with specialized SCI services . It used abstraction of individual electronic medical records for SCI veterans who received outpatient or inpatient treatment of CAP during the study period. Cases were identified initially from VA administrative databases using the same method used by Chang and coauthors , with the addition of cases that solely received an outpatient diagnosis of pneumonia but did not require hospitalization. Medical records were then reviewed to confirm the diagnosis of CAP, and detailed information on clinical presentation, diagnostic evaluation, and treatments were abstracted from the records. Of the 41 patients, 32 (78%) were hospitalized and only 9 (22%) were treated as outpatients. Because these patients were treated at hospitals with specialized SCI services, this may indicate that SCI specialists are more likely to recommend admission for treatment of HAP. The mean length of stay for hospitalized patients was 19.7 days. The antibiotic coverage received was in accordance with recommendations from the Infectious Disease Society of America for only one half of the patients . After accounting for the relatively high rate of fluoroquinolone resistance at the participating institutions, only 24% of patients received reliable antipseudomonal coverage. The in-hospital mortality rate was 7.3%, and after 3 years of follow-up, 42.1% of hospitalization survivors had died.
General population studies have been used to develop CAP treatment algorithms, involving decisions whether to hospitalize the patient and choice of empiric antibiotic coverage for the most common pathogens. Unfortunately, it is not clear which of these principles may be directly applied to the population with SCI residing in the community. For example, the Pneumonia PORT algorithm assigns no increased risk for either expiratory dysfunction or marginal ventilatory status that may be present because of SCI . Its use is not recommended for persons with SCI, because it is likely to underestimate mortality risk. Recommendations for management of CAP in persons with SCI are summarized in Table 2 .
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