1. Introduction
The International Air Transport Association (IATA) expects 7.2 billion passengers to travel by air in 2035, a near doubling of the 3.8 billion passengers that travelled in 2016 [
1]. Within the U.S. Federal Aviation Administration’s (FAA) Air Traffic Control Organization alone, over 2.5 million airline passengers travel on 43,000 airline flights every day [
2]. Billions of passengers travel by air every year; however, compared to other forms of transportation, flying is the safest, with only 138 onboard and one external fatality worldwide in 2016 [
3].
As of 2017, there were an estimated total of 609,306 pilots within the FAA’s jurisdiction, including 159,825 airline transport pilots [
4]. Before an individual can become a pilot, they must obtain a medical certificate, which indicates that they are healthy enough to operate an airplane. Medication usage, medical history, use of corrective lenses, surgeries, and recent visits to health care professionals are all items that must be disclosed to the Aviation Medical Examiner (AME) by the applicant. Though having strict requirements of qualification, the actual performance and mental health of airplane pilots on the flight deck still warrants further intervention. An anonymous survey-based study showed that some pilots may suffer from depressive symptoms that they do not disclose to the AME or their primary care manager due to the fear of negative career impacts [
5]. Pilots’ attempts to protect their careers through non-disclosure of their symptoms prevents them from receiving proper treatment. Airline pilots also reported heightened self-rated fatigue and irregular sleep during international flights [
6,
7].
Pilots undergo a variety of physical, psychological, and physiological stressors that affects their performance during the flight. Examples include flight deck humidity, family illnesses or death, or fatigue and physical deconditioning. To ensure flight safety, it is necessary to have a deeper insight into the stress levels of pilots during flight, and how stress impacts their performance. The occupational stress and workload can be estimated through physiological indicators such as cortisol levels in saliva, respiration rate and heart rate variability (HRV) [
8,
9,
10]. A recent study [
11] indicated that the stress of pilots was elevated as indicated by lower HRV, when switching from analog to digital visual presentations of the flight and navigation data.
The stress response system is comprised of the autonomic nervous system (ANS) and the hypothalamic-pituitary-adrenal (HPA) axis [
12]. Activation of the sympathetic nervous system (SNS) with inhibition of the parasympathetic nervous system (PNS) triggers the acute response to both physical and psychological stress, also known as the fight-or-flight response [
13]. During the stress response, the HPA axis is initiated by the release of the corticotrophin-releasing hormone from the hypothalamus, which results in a series of endocrine changes that culminates with the release of cortisol from the adrenal cortex [
14]. The PNS plays an integral role in alleviating the stress response of individuals by inhibiting the SNS and HPA axis [
12,
15]. The PNS also regulates the “rest and digest” functions that calm the body down and dampen the stress response [
15,
16]. HRV is a measure of the variability in the length of time between heart beats, which serves as a proxy for the dynamic interplay between the parasympathetic and sympathetic branches of the ANS [
17]. Current neurobiological evidence suggests that HRV indices can be used as an objective physiological indicator of stress [
18]. HRV can be measured in both a time-domain and a frequency-domain [
19,
20]. Time-domain HRV indices represent the variability in the time intervals between successive heartbeats. SDNN (standard deviation of the normal to normal interval) and RMSSD (root mean square of successive differences between normal heartbeats) are the two most commonly-used HRV time-domain indices. SDNN reflects the total heart rate variability correlated with ANS activities, while RMSSD is more of a marker of parasympathetic regulation of heart. Both higher SDNN and RMSSD have been associated with physiological resilience against stress [
18,
21]; low variability could be attributed to pathologies such as hypertension, diabetes, and depression, all of which are associated with stress and decreased cognitive function [
22,
23].
Frequency-domain measurements describe the power distribution of HRV as a function of frequency. The low frequency (LF) component (0.04 to 0.15 Hz) of HRV is produced by both SNS and PNS activities. An increased LF power may reflect increased sympathetic activity during mental stress and exercise [
20]. The high frequency (HF) component (0.15 to 0.4 Hz) of HRV is primarily produced by PNS activity and highly correlated with the RMSSD time-domain measures [
24]. Lower HF power is correlated with higher stress, panic, anxiety or worry [
19]; therefore, the ratio of LF power to HF power (LF/HF ratio) can be used to estimate the balance between SNS and PNS activity [
23]. A low LF/HF ratio reflects the dominance of PNS activity, when people conserve energy and engage in tend-and-befriend behaviors. Conversely, a high LF/HF ratio indicates sympathetic dominance, which occurs when people engage in fight-or-flight behaviors or parasympathetic withdrawal.
The performance of pilots may also be affected by environmental conditions on the flight deck such as temperature, aircraft vibration, noise, air quality and ventilation. The flight deck has been under studied, however; nearly all of the research to date on these environmental factors in airplanes, has focused on conditions in the airplane cabin [
25,
26,
27,
28,
29]. Specific to air quality, a focus of our current study, one study of 179 U.S. domestic flights, Cao et al. [
30] found an average CO
2 concentration of 1353 ± 290 ppm (mean ± SD) during all flight phases, but as high as nearly 3000 ppm during boarding, a time when the flight deck door is usually open. The equivalent outside air ventilation rates could only meet the minimum value of 4.7 L/s/p as required by Federal Aviation Regulations [
31] 42% of time during boarding and 73% of time during flying. Data for conditions on the flight deck are more limited. The European Aviation Safety Agency (EASA) measured the CO
2 concentrations in the cockpits of eight B787 airplanes and 61 other types of airplanes [
32]. The mean CO
2 concentration on the B787 flight deck was 603 ppm with a range of 473 to 1229 ppm. On the flight deck of other airplanes, the mean CO
2 concentrations were 835 ppm (629–1918 ppm) and 753 ppm (594–1976 ppm) for short-haul and long-haul flights, respectively.
Exposure to CO
2 at these levels has been shown to be associated with detrimental effects on cognitive function and increasing prevalence of health symptoms in other indoor settings [
33,
34,
35,
36]. Further, our recent study that focused on CO
2 and airplane pilots [
37] demonstrated that CO
2 concentrations impact airline pilot performance at levels occasionally observed on the flight deck. Compared to segments at a CO
2 concentration of 2500 ppm, the odds of passing a maneuver in flight simulations were 1.52 (95% CI: 1.02–2.25) times higher when pilots were exposed to 1500 ppm and 1.69 (95% CI: 1.11–2.55) times higher when exposed to 700 ppm [
37]. Based on prior studies showing the potential for elevated CO
2 in the airplane and an impact of CO
2 on pilot performance, the aims of our present study were to: further investigate the stress response of pilots when conducting flight maneuvers of varying difficulty at different CO
2 concentrations during the flight simulations; and to evaluate how sympathetic stress response, as indicated by HRV metrics impact, the performance of pilots. Using a crossover repeated measures study design, we recruited thirty active commercial airline pilots and had them complete a series of three simulated flights in an FAA-certified A320 flight simulator at three CO
2 conditions: 700 ppm, 1500 ppm, and 2500 ppm. Pilots had HRV monitored for the duration of the flight, and the flight performance of pilots was rated by FAA designated pilot examiners. We sought to examine the effects of different influencing factors on pilots’ HRV, and in turn the effect of HRV on the flight performance.
4. Discussion
Active airline pilots were flying the simulator under high stress levels as indicated by their lower variability and higher LF/HF ratio, compared with the normative values of healthy adults [
42]. The stress of the pilots was generally higher when performing maneuvers during the takeoff, approach and landing phases. Their stress was reduced during the ‘Gap’ periods, which may represent the cruise phase when the pilots are not performing active maneuvers. Lower HRV was associated with aging, high BMI and performing hard maneuvers with low passing rates. Overall, the pilots performed better on maneuvers as rated by the examiners during the flight simulations when their stress was lower, as indicated by the increase of SDNN and RMSSD and decrease of LF/HF ratio, controlling for CO
2 condition and flight maneuver difficulty.
The findings on the impact of age and BMI on HRV are consistent with other studies. Previous studies of short-term HRV [
43,
44,
45,
46] have suggested inverse relationships between age and the time-domain HRV indices. The LF/HF ratio tends to increase with age in population of age <44 years [
43], but possibly decrease with aging for elderly subjects of age >44 years [
47] or >65 years [
48]. Respiratory sinus arrhythmia is a normal physiologic process that becomes less prominent as people age, partly because of decreases in baroreflex sensitivity. This may account for some of the changes in HRV observed in aging populations [
49]. The ANS activity is also related to the body weight regulation [
50]. In a study of 25 healthy adults [
51], increasing BMI is correlated to increased sympathetic activity (higher LF power) and lower parasympathetic activity (lower HF power). It could be speculated that obesity yields to increased energy expenditure as modulated by sympathetic activity. A study of 786 young men [
52] also showed that increased BMI was associated with a shift in sympathovagal balance trending towards sympathetic dominance in young adults.
In this study, the relationship between CO
2 condition and HRV was not significant, which was probably caused by concentrations in the flight simulator at or below 2500 ppm, a level not associated with HRV impacts in prior studies. For example, Kaye et al. [
53] investigated the impact of acute CO
2 exposure on cardiovascular and psychological responses to stress in healthy adults with concentrations from 5% to 35%. They concluded that a single breath of 35% CO
2 could produce sympathetic and HPA axis activation, indicating the anxiogenic response to hypercapnia by the tested subjects. Lower doses of CO
2 exposures did not show any significant effects on cardiovascular parameters. Elevating the end-tidal CO
2 from 5% to 6% could increase HF and LF components of HRV in awake volunteers under both spontaneous and mechanical ventilation [
54]. A recent study of indoor air quality and cardiovascular health [
55] indicated that no association was observed between HRV and CO
2 concentration in homes. The CO
2 concentrations in airplane cabins are much lower than the effect levels [
53,
54]. For this reason, the ANS activities were not likely on the causal pathway between CO
2 and cognition of pilots, yet HRV has an independent relationship with the odds of passing a maneuver.
The interaction between stress and pilot performance on different maneuvers may have two aspects. On the one hand, exposure to stress may be detrimental in performing executive-function tasks. Recent studies have signified the relationships between HRV and cognitive function [
56]. Reduced cognitive performance associated with lower HRV may be a consequence of the failure of the ANS to properly regulate brain perfusion [
57]. More importantly, vagally-mediated HRV has been related to the prefrontal cortex functioning, which is involved in the inhibition of SNS activation [
58,
59]. Attenuated SNS activity and increased PNS activity are associated with higher prefrontal cortex activity level [
58]. Prefrontal cortex activity is correlated with many important cognitive functions such as working memory, sustained attention, behavioral inhibition and general mental flexibility [
56,
60,
61]. All of these cognitive functions are essential for human executive functions that have to do with plan, direct action and self-regulation to perform goal-directed behavior. As a consequence, HRV is also related to cognitive performance of executive tasks. Hansen et al. [
62] reported the subjects with higher RMSSD performed better on executive function such as working memory and attention tasks. The following study showed that physically-trained subjects had higher HF component and better cognitive performance on executive tasks than de-trained subjects who did no physical activity for a four week period [
63]. A cross-sectional study of 4763 elder participants [
64] showed that reduced total variability was associated with poorer cognitive performance as indicated by lower Montreal cognitive assessment (MOCA) score. ZAl Hazzouri et al. [
22] collected the short-term ECG data of 2118 middle-age participants and correlated the HRV metrics with their cognitive test performance five years later with a prospective study design. They concluded that higher quartile of SDNN was associated with better executive function as indicated by higher Stroop test score. A study using visuospatial working memory (VSWM) test also showed that the decrement in HRV would lead to poor cognitive performance with an increase in memory load [
65]. All of this evidence suggests that stress could profoundly impair goal-directed behavior with increased HPA-axis and SNS activity [
66,
67], and may contribute to the cognitive deficits observed in mental disorders and extreme environments [
56]. As such, we can infer that stress could be detrimental to pilot performance on the hard maneuvers composed of challenging executive tasks being conducted under stressful conditions.
On the other hand, stress could be associated with improved cognitive performance on non-executive function tasks. Exposure to stress may have a positive effect on non-executive function that is driven reflexively by stimulation. Luft et al. [
68] studied the differences in athletes’ HRV between executive tasks and non-executive tasks. They found that lower time-domain HRV measures, which means higher stress, was related to faster reaction time on non-executive tasks. The subjects with lower HRV showed faster mean reaction time on a non-executive or easy task under the threat-of-shock condition in which participants were threatened to receive an uncomfortable, but not painful, electric shock through the hand [
69]. Stress is thought to be able to enhance memory formation but to impair memory retrieval [
70]. Stress can facilitate the processing of sensory information caused by an increase in attention mediated by cortical arousal [
71]. Acute exposure to stress may be beneficial to the instructed stimulus-response learning with moderate working memory demand [
72]. As such, in some cases, necessary hyper vigilance or so-called eustress possibly make the pilots more alert, enhancing their reaction and cognitive adaptation to maneuvers. For example, the pilots performed well on the ‘Takeoff: Normal’ maneuver, though they had high LF/HF ratios.
In this study, the LF/HF ratio was used as a marker of sympathovagal balance. However, the interpretation of LF remains actively debated, which is considered by some researchers as a measure of sympathetic regulation [
73] and by others as a parameter of both sympathetic and vagal regulation [
74]. Another interpretation is LF can serve as a marker of sympathetic modulation in some contexts, and more represent parasympathetic activity in other contexts [
74,
75]. We further analyzed the influencing factors of the LF power and HF power of HRV, as shown in
Figure S2 and
Table S3. The results show that the changes in LF and HF power were basically in the same direction but with different magnitude. As the GAMM results, an interquartile range (IQR) increase in LF (944 ms
2) and HF (266 ms
2) was associated with an increase of 17% and 23% in the odds of passing a maneuver, respectively. The above results indicate that the HF component is highly correlated with the RMSSD measures, both as markers of parasympathetic regulation of heart; the LF component is likely to be influenced by both sympathetic and parasympathetic activity. Consequently, the LF/HF ratio could reflect sympathovagal balance to some extent, but the interpretation of LF and LF/HF ratio still warrants further elucidation.
There are several limitations to consider when interpreting the results of this study. While we had a baseline measurement of HRV before the simulation, the measurements were likely impacted by the stress of the impending simulations. Therefore, the HRV values of pilots may not be directly comparable to the normative HRV values derived from a literature review [
42]. A number of studies have revealed large inter-personal variation for the majority of HRV measures [
19,
42]. The underlying factors for the discrepant values mainly include demographic of subjects, breathing protocols and spectral power analysis methods. In addition, the stress level and performance of pilots presented in this study could be different from those on an actual flight. These simulated flights were not conducted under an actual ‘check ride’ or actual ‘in-flight emergency’. In both of these cases where the pilot’s license and job, and possibly life, is on the line while performing these maneuvers, their stress level could be even higher than what we have demonstrated in this study. Though complying with the PTS standards, the examined maneuvers, such as one engine inoperative and glide slope inoperative, are generally much more challenging than the maneuvers occurred on normally functioning airplanes. As we were interested in the impact on pilot performance, we had the pilots controlling the simulator manually without any auto-pilot aid. Under these conditions, the pilots may more prone to error when conducting difficult maneuvers than during normal flight operations. Our research findings were solely based on male pilots. This reflects the current distribution of pilots in the workforce (94% male), but limit the generalizability to female pilots.
The HRV data that we have collected from airline pilots reflected their physiologic response produced by stressful situations in flight. This is a rare opportunity to evaluate the real-time stress response of pilots in an FAA-approved flight simulator under varying environmental conditions. Studying HRV data in this way can help us better understand how active pilots respond to stress physiologically. The implications of occupational stress and physiologic response can be applied to other workers in high-stress occupations.