Aging

Respiratory System

As a consequence of SCI, especially injury to the cervical and upper thoracic parts of the spinal cord, functioning of the respiratory muscles is disrupted, and leads to lowered lung volume parameters (Linn et al. 2000), in addition to other respiratory complications, such as decreases in compliance of the chest wall, changes in breathing patterns, sleep-disordered breathing (SDB), and ventilator dependency.

For individuals with SCI who have impaired autonomic function and impaired inspiratory muscle weakness, SDB may occur (Bonekat et al. 1990). In general, the incidence of SDB, characterized by sleep apnea, is estimated to be at least twice that reported in the general population (Schilero et al. 2009). Respiratory complications lead to significant morbidity and mortality in people with SCI (DeVivo et al. 1993; Cotton et al. 2005).

Among the general population, age associated changes in the respiratory system involve loss of elastic recoil of the lung. Similarly, among individuals with SCI, decreases in the compliance of the chest wall, and strength of the respiratory muscles are observed (Janssens et al. 1999; Janssens 2005). Complications resulting from SCI may therefore hold important respiratory implications as people age.

In this section, 5 longitudinal studies and 4 cross-sectional studies on the respiratory system after SCI are reviewed.

Table 6. Respiratory System

Author Year; Country Score Research Design Total Sample Size	Methods	Outcome
Van Silfhout et al. 2016; Australia Level 4 Retrospective N = 59	Population: 59 people with SCI (71% M, 29% F); mean age at injury (y)=40±16 (range 18-71); mean BMI in kg/m²= 28.2±6.8 (range 16.0-52.9); AIS ABC C1-C4 (17%), AIS ABC C5-C8 (51%), AIS ABC T1-S5 (15%), AIS D (15%) Methodology: People with SCI who previously have had at least 2 respiratory function tests (RFTs) were analyzed to study the effect of TSI on longitudinal respiratory function in people with SCI. Outcome Measures: Respiratory function, forced vital capacity (FVC).	There was no significant change in respiratory function measured in (forced) vital capacity ((FVC) after the initial drop in pulmonary function. People with a BMI>30kgm⁻² showed a decline in (FVC) over time.
Van Koppenhagen et al. 2014; The Netherlands Level 2 Longitudinal N = 130	Population: 130 persons with SCI (75% M), mean age 38.7±13.7; paraplegia (72%), tetraplegia (17.9%) Methodology: Measurements at the start of active rehabilitation, after 3 months, at discharge from inpatient rehabilitation, and 1 and 5 years after discharge were taken to examine the longitudinal relationship between wheelchair exercise capacity and life satisfaction in persons with SCI. Outcome Measures: Life Satisfaction Now (LS Now), Life Satisfaction Comparison (LS Comparison), Life Satisfaction Total (LS Total), peak O2 uptake (VO2peak), peak power output (POpeak)	Mean POpeak increased during the study from 32.9 to 55.9 Watts, mean VO2peak from 1.02 to 1.38 l/minute, An increase of POpeak of 10 W was associated with a 0.3-point increase of life satisfaction (P = 0.01). An increase of VO2peak with 0.1 l/minute was associated with a 0.1-point increase of life satisfaction
Postma et al. 2013; The Netherlands Prospective longitudinal Level 2 N=180	Population: 180 persons with SCI (73.9% male); mean (SD) age at start of active rehab (yrs): 39.7(13.7); mean (SD) YPI at start of active rehab (days): 101.8(62.1); Lesion level: 38.9% tetraplegia; Completeness: 66.7% motor complete (AIS A and B) Methodology: Pulmonary function (PF) was determined at the start of rehabilitation, at discharge, and 1 and 5 years after discharge. Outcome Measures: Forced vital capacity (FVC), forced expiratory volume in 1 second (FEV₁).	Overall, FVC improved a mean of 5.1% over the 5 yrs of observation. There was no change in FEV₁. There was no observed change in FVC or FEV₁from discharge to year 1, nor from year 1 to year 5.
Tamplin et al. 2011; Australia Prospective controlled trial Level 2 SCI N=6 Control N=6	Population: 6 individuals (4M 2F) with SCI; motor-complete C5-C7 tetraplegia; YPI >1 yr; age range 28-62 yrs. 6 AB age-matched controls. Methodology: Participants directed through phonatory exercises, standardized reading passages, and familiar songs. Outcome Measures: Maximal inspiratory and expiratory flow rates, timed lung volumes, surface electromyographic activity from accessory respiratory muscles, sound pressure levels during vocal tasks, Voice Handicap Index, Perceptual Voice Profile, ventilator function, upper airway function.	Participants with tetraplegia had smaller lung capacities, reduced respiratory pressures, and significantly greater vocal impairment. Significantly higher peak amplitude from participants with tetraplegia during loud and soft speech compared to control. AB Control participants had wider dynamic range compared to participants with tetraplegia. Control able to sustain vowel for longer than participants with SCI.
Ovechkin et al. 2010; USA Prospective controlled trial Level 2 N SCI=18 N Control=14	Population: 18 participants with SCI (15M 3F); 8 motor-complete, 10 motor-incomplete; ranging from C3 to L2. 14 AB controls (9M 5F). Methodology: Comparison of respiratory muscle control between SCI participants and AB controls through PFT (standard spirometry). Outcome Measures: Pulmonary function test (PFT); respiratory motor control assessment (RMCA) by surface electromyographic recording (sEMG).	Altered multi-muscle patterns in the SCI group produced Similarity Index (SI) values that were significantly lower (0.59±0.22) for expiratory tasks. SI values for expiratory tasks. Altered multi-muscle patterns were also significantly correlated with SCI levels and pulmonary function measures.
Berlowitz et al. 2005; USA Longitudinal Level 2 N=30	Population: 30 participants with acute tetraplegia (25M 5F); mean age 33.7, range 18-69 yrs. Methodology: Measured the incidence of sleep disordered breathing (SDB), and identified the relationship between SDB and previously postulated predictors. Outcome Measures: Apnea-Hyopnea Index; Incidence of sleep disordered breathing (SDB); overall respiratory function.	At 2 weeks, 60% had SDB; at 4 weeks, 62%; at 13 weeks, 62%; at 26 weeks, 83%; at 52 weeks, 62%. All participants had reduced respiratory function compared with normative population values.
Biering-Sorensen & Biering-Sorensen 2001; Denmark Case-control Level 3 N SCI=408 N controls=339	Population: 408 participants with SCI (331M 77F); mean(SD) age 42.5(14.1) yrs, range 17-86 yrs; mean(SD) YPI 12.1(6.3), range 2.5-45.1 yrs; age and gender matched AB controls. Methodology: Self-administered questionnaire. Outcome Measures: Nordic Sleep Questionnaire (NSQ) containing 21 questions.	Participants with SCI snored more often, louder, for more years, and started at younger ages compared to AB controls.
Bach & Wang 1994; USA Longitudinal Level 2 N=10	Population: 10 participants (9M 1F) with tetraplegia; mean(SD) age 41(12.3) range 34-77 yrs; mean(SD) YPI 7.7(5.8), range 6mos-19 yrs. Methodology: Comparison of oxygen desaturation. Ten participants were evaluated at least 6 months post injury and re-evaluated 5 years later. Outcome Measures: Oxygen desaturation, assessed through pulse oximetry.	At baseline, 6 participants (60%) had desaturation below 90%. At follow-up, 5 participants (50%) had an increased number of transient nocturnal oxygen desaturations.
Cahan et al. 1993; Australia Cross-sectional with AB controls Level 3 N SCI=16 N controls=12	Population: 16 men with tetraplegia; mean(SD) age 49(15) yrs, range 23-64 yrs; mean(SD) YPI 14(10), range 1-32 yrs; age and gender matched AB controls. Methodology: Comparison of oxygen desaturation. Outcome Measures: Pulse oximetry.	6 patients (38%) with tetraplegia had oxygen saturation levels below the normative range, indicative of SDB.
Loveridge et al. 1992; Canada Longitudinal Level 2 N=6	Population: 6 men with acute SCI; mean(SD) age 30(11) yrs; for persons with tetraplegia; mean age 32.6 yrs, range 21-50 yrs; mean time post-injury 38.6 months. Methodology: Comparison of lung function and breathing patterns. Outcome Measures: Lung function parameters including, force vital capacity, inspiratory capacity, residual volume, forced expiratory capacity, functional residual capacity, and maximum inspiratory mouth pressure; Breathing pattern indicators including, Inspiratory time, tidal volume, and expiratory time; assessed in both sitting and supine positions, at 2, 6, and >12 months post-injury.	Seating position resulted in greater stress on the respiratory system and breathing patterns in the group with tetraplegia compared to the AB control group. Over time, breathing patterns of the group with tetraplegia improved and were comparable to those of the AB control group.
Wicks & Menter 1986; USA Longitudinal Level 2 N=134	Population: 134 participants with tetraplegia (118M 16F). Methodology: Review of patients’ medical records over 10 yrs in order to determine the number of patients who could be weaned off mechanical ventilation and to assess their long-term survival rate. Outcome Measures: Medical records between1974-1983; mortality rates, ventilation status.	Individuals over 50 yrs of age had less successful weaning attempts and higher mortality rates than younger individuals despite similar levels of injury.

Discussion

Several of the identified studies highlight that SDB and other respiratory complications are higher in persons with SCI than in the general population and appear to increase with age. In a five-year longitudinal study to assess changes in SDB, Bach and Wang (1994) measured oxygen desaturation, which is characteristic of sleep apnea, in 10 individuals with tetraplegia; six individuals had oxygen desaturation below 90%. At the five-year follow-up, 5 of the 10 individuals had increased patterns of oxygen desaturation, leading to the conclusion that oxygen desaturation is common among people with tetraplegia and increases with age. In another longitudinal study (Berlowitz et al. 2005) sleep apnea, defined as an apnea-hypopnea index (AHI) of >10 events per hour, was found in 62% of the sample in the first month, peaking at 83% at 13 weeks, and falling to 68% and 62% at weeks 26 and 52 respectively.

Snoring is another important indicator of sleep apnea and appears to be age related. In a large case-control study, 29% of men (N = 331) and 21% of women with SCI (N = 77) snored daily or almost daily compared to 18.2% of the control group (N = 339) representing the normal population of Denmark (Biering-Sorensen & Biering-Sorensen 2001). In addition, those who snored daily or almost daily in the SCI group were significantly older than those with SCI who snored less frequently. After SCI, there are temporal changes in pulmonary functioning. Forced vital capacity (FVC), inspiratory capacity (IC), and maximum inspiratory mouth pressure (Pimax) are lowered in the acute stage of SCI, and then gradually improve over time. In a five-year longitudinal study, Postma et al. (2013) showed improvements to FVC. Loveridge and colleagues (1992) showed that seated positioning imposes greater stress on the respiratory system in the acute stages of SCI than the supine position. While breathing patterns in the supine position at all measured time points one-YPI were comparable to the controls (N= 18), breathing patterns in the seated position had to be adjusted in order to maintain minute ventilation. Over time, however, improved breathing patterns were observed in the seated position, so much so that differences initially observed between the seated and supine positions became insignificant. Such improved breathing pattern is speculated to be due to increased accessory muscle function, improved chest wall stability, thoraco-abdominal coupling, or a combination of these factors over time.

An increasingly shallow breathing pattern resulting from a lack of deep breaths, and other factors associated with SCI such as obesity and decreased chest wall compliance, may lead to hypercapnia, or excessive amounts of carbon dioxide in the blood, and possibly ventilatory failure (Bach & Wang 1994). Despite these results from this prospective longitudinal study, it is unclear if breathing patterns change as a result of the injury or due to aging with SCI. The former may be the case as the study followed adjustments only during the first YPI.

Sustaining a SCI often leads to an initial respiratory insufficiency and necessitates a need for long-term mechanical ventilation. In some instances, individuals may be weaned from the ventilator. Wicks and Menter (1986) conducted a 10-year retrospective study of ventilator-dependent patients with tetraplegia (N = 134) to determine factors associated with weaning and long-term survival rate. Despite similar levels of injury, patients over 50 years of age had a 20% mortality rate compared to 6% for those younger than 50, and that ventilator weaning is less successful for those over the age of 50. This suggests that ventilator-dependency among SCI individuals who are older than 50 possess a much greater risk of negative health outcomes (Wicks & Menter 1986).

Although there are additional factors that can affect respiratory health long-term for the individual with SCI (i.e. level and completeness), there are several preventative activities that can be done to minimize the aging of the respiratory system, such as not smoking, minimizing exposure to polluted air, and controlling body weight (Wilmot & Hall 1993). Further research is needed to better understand SDB in persons aging, especially in terms of their implications for for cardiovascular health.

Conclusion

There is Level 4 evidence from two longitudinal studies (Bach & Wang 1994; Berlowitz et al. 2005) support that SDB may either increase or persist with the aging process.

There is Level 2 evidence from a longitudinal study with AB controls (Loveridge et al. 1992) that seated breathing patterns are compromised immediately post injury but recover over time. As well, persons with tetraplegia do not take deep breaths as often as AB individuals.

There is Level 4 evidence from a longitudinal study that adults over the age of 50 who are aging with ventilator dependency are at greater risk of death and are less likely to be weaned from their ventilators than younger adults aging with a ventilator (Wicks & Menter 1986).

There is Level 4 evidence from one longitudinal study (Postma et al. 2013) that forced vital capacity improves 5 years after inpatient rehabilitation.

Sleep disordered breathing may increase or persist with the aging process in persons with SCI.

Seated breathing patterns after tetraplegia appear compromised early post-injury but may recover over time.

Adults who are older (50 years +) and ventilator dependent have a higher mortality rate and lower weaning rate than adults who are younger and who are ventilator dependent.