Does Pre-Flight Cigarette Smoking Affect the Military Aviator's Attention at a Simulated Altitude of 18,000 Feet Created by A

• 268 • Taiwanese Journal of Psychiatry (Taipei) Vol. 25 No. 4 2011 Original Article

Does Pre-ﬂ ight Cigarette Smoking Affect the Military Aviator’s Attention at a Simulated Altitude of 18,000 Feet Created by a Hypobaric Chamber?

Yu-Ming Cheng, M.D.1,5, Ching-Hui Loh, Ph.D.2 , Chien-Bai Sha, M.D.1, Yi-Chang Wu, Ph.D.3, Hui-Nien Yang, M.D.1, Wei-An Lin, Ph.D.1,4

Objectives: Cigarette smoking affects performance and attention, but its relationship is unclear. Aviators require sustained, focused attention to maintain aviation safety, but they are frequently exposed to high-altitude environments. In this study, we intended to investigate whether pre-ﬂ ight cigarette smoking would affect the attention of military aviators at a simulated altitude of 18,000 feet created by a hypobaric chamber. Methods: We evaluated 96 (72 smokers and 24 non-smokers) aviators with the visual search and the incompatibility task. All participants took part in two tasks in a hypobaric chamber at ground level. We randomly chose 48 participants in the smoking group to receive a piece of cigarette with a nicotine dose of 1.0 mg; the other participants in the smoking group (n = 24) received a piece of cigarette with a nicotine dose of 0.1 mg (smoker group 2). After we gave the smoking participants a piece of cigarette, the smokers who received the 1.0 mg nicotine dose were equally divided into two groups (smoker groups 1 and 3; n = 24 each). All aviators except those in smoker group 3 (at ground level for the whole procedure) were subjected to altitude of 18,000 feet. Participants undertook the two tasks again. Results: In smokers, cigarette smoking was found to have a positive effect on reaction time in both visual search and incompatibility tasks, regardless of altitude. The trend was not clear about attitude and attention since no difference was found among smoker group 1 and 3. Conclusion: Cigarette smoking facilitates attention during the visual search and incompatibility tasks in smokers at 18,000 feet of altitude.

Key words: cigarettes, visual search, incompatibility, hypobaric chamber (Taiwanese Journal of Psychiatry [Taipei] 2011; 25: 268-78)

1 Department of Military Operational Psychiatry, Beitou Armed Forces Hospital, Taipei 2 Department of Family and Community Health, Tri-services General Hospital, Taipei 3 Institute of Aerospace Medicine, National Defense Medical Center, Taipei 4 School of Pharmacy and Graduate Institute of Pharmacy, National Defense Medical Center, Taipei 5 Department of Crime Prevention and Correction, Central Police University, Taoyuan Received: August 5, 2011; revised: September 8, 2011; accepted: October 10, 2011 Address correspondence to: Dr. Wei-An Lin, Beitou Armed Forces Hospital, No. 60, Sinmin Road, Taipei 11243, Taiwan Cheng YM, Loh CH, Sha CB, et al. • 269 •

Another study result shows that cigarette Introduction smoking only improves some kinds of attention [13]. Nicotine improves alertness, but does not Cigarette smoking is one of the most promi- improve spatial attention in non-smokers [14]. nent worldwide public health problems. The most Nicotine does not infl uence any aspect of atten- common cause of death in the world is hyperten- tion in people who have never smoked [15]. sion, and tobacco use is the second most common Furthermore, the nicotine direct effect in improv- cause of death globally. In a report of the 2010 ing cognition and attention remains controversial, World Health Organization, more than fi ve mil- and the relationship between nicotine and cogni- lion people die prematurely each year due to tive function is still unclear [16]. smoking, and this habit is currently responsible Aviators with smoking habits cannot smoke for 1 in 10 adult deaths. The prevalence of tobacco on board of an aircraft. When the altitude of an dependence remains high because it is a chronic, airplane is below the 18,000-feet level (FL180), remitting, and relapsing condition. Nearly 40% of whether due to an accident, a forced landing, or a smokers try to quit each year, but only 4%-7% drop in altitude, the key to a safe landing is the successfully stop smoking in the United States of aviator’s attention [17, 18]. According to a America [1]. A previous study has shown that PubMed search, no study has devoted to investi- fl ight crews smoke at a much higher rate (50.9%) gating the relationship between pre-fl ight cigarette compared to the ground crews (23.2%) [2]. In a smoking and attention, either at high altitudes or 2004 survey, the smoking prevalence for the in a simulated high-altitude environment (e.g., in Republic of China Air Force aircrew is found to a hypobaric chamber). In this study, we intended be 45%, which is also higher compared to that of to investigate whether pre-fl ight cigarette smok- other military servicemen (32.4%) [3]. ing would affect aviator’ attention of military ser- Smoking among commercial and military vicemen at a simulated altitude of 18,000 feet cre- aviators is a health hazard in the cockpit. Aviators ated by a hypobaric chamber. who are required to abstain before and during their fl ight, may suffer from a decreased cockpit perfor- Methods mance [4]. Cigarette smoking also causes damage to cardiopulmonary function that is critical for The apparatus performance at high altitudes [5]. Thus, piloting Participants performed the tasks (see below) an aircraft is an occupation that requires sustained at ground level on a laptop computer running E- attention and a healthy body, which may be the prime version 1.0 while in a hypobaric chamber most important factor in aviation safety [6]. (1957 Granite Inc., Chicago, Illinois, USA; capac- Nicotine in cigarettes affects cognitive func- ity: eight people). The laptop computer was placed tions including attention. Many studies have shown on a table about 60 cm in front of the participant, that in humans, nicotine has a positive effect in im- and the LCD screen was set at the participant’s proving selective attention [7], visual search per- line of vision. Participants used a chin rest to avoid formance [8] as well as inspection time [9]; and that head and body movements. All laptops performed in rats nicotine administration improves attention the task smoothly even under the high-altitude [10, 11] and visual signal detection [12]. conditions of the hypobaric chamber. We used • 270 • Smoking Facilitates Attention at FL180

carbon monoxide (CO) breath-meter (Bedfront Study participants Micro Smokerlyzer Breath Carbon Monoxide To prevent medical factors-especially those Monitoring, Rochester, United Kingdom) to mea- related to visual problems-from infl uencing our sure the recent smoking of the aviators and to dis- study, we recruited aviator volunteers from the R. tinguish them between the smoker and non-smok- O.C. Air Force Academy to join our study during er groups. general physiological training. These participants had the same level of education. As shown in The altitude Table 1, we randomly chose 72 male aviators for According to U.S. Federal Aviation the smoking groups and 24 male aviators for the Regulations (FAR; Part § 91.159), FL180 (18,000 non-smoking group. All aviators were about the feet in Aeronautics; ≅ 5486.57 m) is the boundary same age and had the same level of education. between the high altitude routes (Jet Route or J- Aviators in the smoking group who smoked 10.1 ± route) and the low altitude routes (Victor airways 1.6 pieces of cigarettes per day and had been or V-route) as well as the boundary between visual smokers for 5.1 ± 1.9 years. The nicotine yield fl ight rules (VFR) and instrument fl ight rules from the participant preferred cigarette brands (IFR). In general, the aviator must fl y an IFR fl ight was ranged from 0.8 mg to 1.0 mg per cigarette. plan above FL180 without special permission All participants had excellent visual acuity with- from air traffi c control (ATC). Furthermore, out correction by any refraction lenses, and no FL180 is the standard altitude for general physio- aviator had an eye-related disorders. All partici- logical training conditions in the U.S. and Taiwan pants were licensed aviators who operated mili- air forces, and the pressure at this altitude is 380 tary fi xed-wing aircraft (the T-34 made by Beech mmHg (0.5 ATM). According to military rules, Aircraft [USA] or the AT-3 advanced jet trainer aviators must successfully complete this training [Taiwan]). Participants were given course credit every three years in Taiwan; otherwise, aviators for their participation. We obtained written in- have been grounded until training is completed. formed consent at the beginning of the session and To mimic the experience of fl ight, participants fully debriefed all participants at the end of the performed attention tasks at a simulated altitude session. The institutional review board at Tri-ser- of 18,000 feet created by a hypobaric chamber (a vices General Hospital in Taipei approved the dark environment). study protocol.

Table 1. Demographic data

Group Smoker 1 Smoker 2 Smoker 3 Non-smoker Age (year) 22.3 ± 0.25 22.2 ± 0.27 22.1 ± 0.28 22.4 ± 0.52 Height (cm) 172.5 ± 3.5 172.3 ± 3.1 171.8 ± 3.2 171.3 ± 2.8 Body weight (kg) 65.3 ± 5.2 64.3 ± 5.8 64.1 ± 4.8 66 ± 4.2 Expiratory carbon monoxide (ppm) 12.3 ± 4.2*** 12.8 ± 4.1*** 12.5 ± 4.6*** 1.0 ± 0.5

*** p < 0.001. The concentration of expiratory carbon monoxide between smokers and non-smokers were signiﬁ cantly different. Cheng YM, Loh CH, Sha CB, et al. • 271 •

The attention task with their left index fi nger when the arrow pointed We chose the visual search and incompatibil- left, regardless of whether the arrow appeared to ity tasks to assess study participant’s attention, the left or right of the fi xation point. Therefore, and these tasks were adapted from Zimmermann when the arrow was displayed on the side that cor- and Fimm’s Battery for the Assessment of responded to the answering hand, the arrow and Attention. Both tasks were shown on a 15” LCD side were compatible. Conversely, an incompati- computer screen. All responses were recorded. bility arose when the hand required to type and the Visual search is a perceptual task that re- arrow direction was on opposite sides. Participants quires attention and typically involves in an active did 60 (15 compatible and 15 incompatible) trials scan of the visual environment for a particular ob- in each visual hemi-fi eld. ject or feature (i.e., the target) among other objects The tasks began once the participants’ eyes or features (i.e., distracters). We used the visual had adapted to the darkness, and the order of the search task to measure aviator’s visual scanning tasks was counterbalanced between participants, ability in our study. By displaying a 5×5 matrix who were tested together (each with his own com- of squares on the computer screen. As shown in puter) in a dark hypobaric chamber to simulate the Figure 2, each square was nicked on one of its fl ight. To diminish practice effects, we designed four sides. Participants detected whether the target all task signals to appear randomly on the com- (a square nicked on its upper side) was present puter screen. within the matrix as quickly as possible. We presented 100 trials, 50% of the trials contained the The procedure target. As shown in the schematic presentation of The incompatibility task is to assess sensitiv- Figure 1, all participants arrived at the hypobaric ity to interference (i.e., incompatibility between chamber center before 10: 00 p.m. the day before the stimulus and response) and the aviator’s judg- the test. They were requested to abstain from eat- ment, capacity, and focused attention [13]. In each ing irritating food and drinking caffeine-contain- trial, an arrow pointing to the right or the left was ing beverages, or alcohol. presented on the right or the left side of a fi xation At 8: 00 a.m. on the testing day, the partici- point. Participants reacted to the arrow direction pants who smoked habitually stopped smoking by pushing the “J” key with their right index fi n- their own cigarettes two hours before the task ger when the arrow pointed right and the “F” key [19]. During those two hours, we showed partici-

Figure 1. The schematic illustration of the study procedure • 272 • Smoking Facilitates Attention at FL180

Target

Figure 2. Example of the visual search task pants examples of the matrices in the visual search Force. To monitor any feelings of discomfort or and incompatibility tasks and explained instruc- participant problems, we elevated the altitude to tions to them. All participants entered the hypo- the FL50 at 2,000 feet per minute (2.5 minutes) baric chamber and completed the fi rst two tasks followed by a return to ground level at the same (recorded as Test 1) at ground level conditions at rate. If participants felt at ease with this procedure, 10: 00 a.m. After exiting the hypobaric chamber, we elevated the altitude to reach the FL180 at a each participant in the smoking group received rate of 2,000 feet per minute. The altitude reached their assigned cigarette at 10: 30 a.m. FL180 after 9 minutes. At the 15-minute mark We randomly selected 48 participants from (10: 45 a.m.), the participants performed the sec- the smoking group to receive a cigarette with a ond task (recorded as Test 2) again. After fi nishing nicotine dose of 1.0 mg, whereas the other smok- the two tasks, we returned the participants to ing participants (n = 24) received a control ciga- ground level conditions at the same rate. The en- rette with an ineffective nicotine dose of 0.1 mg tire procedure took about 30 minutes per group. (smoker group 2; Table 1) [20]. We randomly di- Smoker group 3 re-entered the hypobaric vided the smokers who received 1.0 mg of nico- chamber, but the altitude was set at ground level tine into two groups (smoker groups 1 and 3; n = during the entire procedure. After 15 minutes (10: 24). 45 a.m.), they completed the second task again Except for smoker group 3, we divided all (recorded as Test 2) at ground level. participants (n = 72) into nine groups (the capacity of the hypobaric chamber is eight people) and ran- Statistical analyses domly selected eight participants from each group. A general linear model (GLM) and Tukey’s Smoker groups 1 and 2, as well as the non-smoker HSD compared the average reaction time of the group re-entered the hypobaric chamber. The pro- four groups at ground level and at FL180 level; an cedure followed the Type Six Hypobaric Chamber ANOVA compared the CO concentration among Flight of R.O.C. Air Force Aerospace Physiology four groups. A two-sided t-test assessed whether Program, the same program used by the U.S. Air Test 1 and Test 2 were signifi cantly different from Cheng YM, Loh CH, Sha CB, et al. • 273 •

each other (α = 0.05). We analyzed all data with that all smokers groups were signifi cantly slower Statistical Package for Social Science (SPSS, Inc, than the non-smoker group (Tukey’s HSD test, p < Chicago, Illinois, USA) software version 15.0 for 0.001); however, we did not fi nd a difference Windows. The differences between the groups among smoker groups 1, 2, and 3. We found sig- were considered signifi cant if p-values were nifi cant differences among all groups at Test 2 smaller than 0.05. (F(3, 92) = 213.69, p < 0.001). The average reaction time of smoker group 2 and the non-smoker group Results was signifi cantly slower than smoker groups 1 and 3 (Tukey’s HSD test, p < 0.001). We did not Demographic data fi nd a difference between smoker groups 1 and 3. We did not fi nd signifi cant differences among The reaction time of smoker group 2 was signifi - smoker group 1, smoker group 2, smoker group 3, cantly slower than the non-smoker group (p < and the non-smoker group with regard to age, 0.001). height, and body weight. The concentration of ex- Figure 3 illustrates the change of reaction piratory carbon monoxide between smokers and time between Test 1 and Test 2. A paired t-test an- non-smokers were signifi cantly different (p < alyzed the change of each group between Tests 1 0.001), but we did not fi nd differences among the and 2. The average reaction time for the non- smoker subgroups (Table 1). smoker group did not change signifi cantly between Tests 1 and 2. Conversely, the average reac- Visual search task tion time of smoker groups 1 and 3 was signifi cantly Table 2 reports the visual search task data. faster at Test 2 compared to Test 1 (p < 0.001), We observed signifi cant differences between all whereas for smoker group 2, the average reaction groups with regard to reaction time at Test 1 (F(3, time at Test 2 was signifi cantly slower than Test 1

92) = 22.438, p < 0.001). A post-hoc test showed (p < 0.001).

Table 2. Average reaction time (msec) in the visual search and incompatibility task.

Visual search task Test 1 Test 2 Smoker group 1 1580 ± 209.6*** 851 ± 183.6 Smoker group 2 1596 ± 194.8*** 1877 ± 178.3+++ Non-smoker group 1272 ± 158.1 1156 ± 167.7+++ Smoker group 3 1588 ± 199.1*** 770 ± 160.2 Incompatibility task Test 1 Test 2 Smoker group 1 512 ± 55.9*** 328 ± 49.8 Smoker group 2 512 ± 61.0*** 625 ± 44.1+++ Non-smoker group 424 ± 44.3 404 ± 39.4+++ Smoker group 3 515 ± 49.1*** 281 ± 59.9 *** p < 0.001. In the two tasks at Test 1, the average reaction time between smokers and non-smokers was signiﬁ cantly different. +++ p < 0.001. In the two tasks at Test 2, the average reaction time of smoker group 2 and the non-smoker group were slower compared to smoker groups 1 and 3. Smoker group 2 was slower than the non-smoker group. • 274 • Smoking Facilitates Attention at FL180

Figure 3. Reaction time for the visual search task *** p < 0.001

Incompatibility task Figure 4 illustrates the change in reaction Table 2 reports the data for the incompati- time between Tests 1 and 2. A paired t-test ana- bility task. We observed signifi cant differences lyzed the change between Tests 1 and 2 for each in reaction time among all groups at Test 1 (F(3,92) group. The average reaction time for the non- = 21.118, p < 0.001). The average reaction times smoker group did not change signifi cantly be- for smoker groups 1, 2, and 3 were signifi cantly tween Tests 1 and 2. Conversely, the average reac- slower compared to the non-smoker group tion time of smoker groups 1 and 3 were (Tukey’s HSD test, p < 0.001); however, we did signifi cantly faster at Test 2 compared to Test 1 (p not observe differences in reaction time among < 0.001), whereas for smoker group 2, the average smoker groups 1, 2, and 3. At Test 2, we observed reaction time was signifi cantly slower at Test 2 signifi cant differences in the reaction time among compared to Test 1 (p < 0.001). all groups (F(3, 92) = 286.67, p < 0.001). The average reaction time of smoker group 2 and the non- Discussion smoker group were signifi cantly slower than smoker groups 1 and 3 (Tukey’s HSD test, p < Mancuso et al. in 2001 showed that partici- 0.001); however, we found no differences be- pants who have consumed a piece of cigarette (0.9 tween smoker groups 1 and 3. Smoker group 2 mg of nicotine) respond faster in an eye-move- was signifi cantly slower than the non-smoker ment task [13]. Furthermore, they showed that al- group (Tukey’s HSD test, p < 0.001). though nicotine can improve a participant’s alert state, it has no effect on incompatibility and visual Cheng YM, Loh CH, Sha CB, et al. • 275 •

Figure 4. Reaction time for the incompatibility task *** p < 0.001 search tasks [13]. With the exception of the low- third, the simulated altitude or atmosphere may pressure and dark environment of the hypobaric also factor into this result. chamber, we used the same procedure to evaluate We found that the average reaction time of performance associated with the incompatibility smokers was slower than non-smokers in both and visual search tasks. Our results are not com- tasks at Test 1. After smoking their assigned ciga- patible with those obtained by Mancuso et al. [13]. rette, smoker group 2 (0.1 mg-nicotine dose) was In our study, a 1.0 mg-nicotine dose had a positive signifi cantly slower than smoker groups 1 and 3 effect on reaction time in both visual search and (1.0 mg-nicotine) as well as the non-smoker group incompatibility tasks at Test 2, regardless of alti- in both tasks at Test 2. The reaction time of smok- tude. Several possible reasons may explain this er groups 1 and 3 was faster than non-smoker, so difference. First, Mancuso et al. in 2001 studied that cigarette smoking (1.0 mg-nicotine dose) im- only 10 participants, far fewer than our study (n = proved visual search and incompatibility task at 96) and who had been deprived of tobacco for Test 2 signifi cantly. Because smoker group 2 re- three hours [19]. Second, smokers may have poor ceived an ineffective dose of nicotine (0.1 mg- night vision, especially after recently smoking nicotine dose), the reaction time of them was [21]. In our study, the participants were tested in a slower than smoker groups 1 and 3 at Test 2. All dark hypobaric chamber to simulate fl ight, and we participants abstained from cigarette smoking for will set the environment in light or dark to evalu- two hours before participating in our study. But, ate differences between lighting conditions. And the reaction time was not signifi cantly different • 276 • Smoking Facilitates Attention at FL180

among the smoker groups at Test 1. After 15 min- speaking, the trend is clear. Because we collected utes, the Test 2 reaction time for smoker group 2 only the reaction time before participants smoked, was slower than at Test 1 on both tasks. Perhaps we could not separate the relationship between al- nicotine withdrawal occurred at Test 1 but was titude and attention. Although this is our study counterbalanced in each smoker group. After 15 limitation, aviators cannot smoke on board an air- minutes, nicotine withdrawal was probably more craft in reality. Our study design refl ects the reality obvious, especially for smoker group 2, who re- of being an aviator. To investigate whether alti- ceived cigarettes with an ineffective 0.1 mg-nico- tude infl uences attention more clearly, we may tine dose. The nicotine withdrawal may have had add an additional study to compare reaction time the greatest effect on the results of the smoker at ground and FL180 after receiving a cigarette group 2 at Test 2. and increasing other aspects of attention in the fu- Nicotine withdrawal syndrome is classifi ed ture. Another study limitation with the design is under code 292.00 in the DSM-IV-TR and its failure to test the effects of cigarette on the non- symptoms include anxiety, diffi culty concentrat- smoker group. It has ethical issues, and other ma- ing, irritability, and restlessness, all of which can terial (e.g., nasal spray, nicotine patch) cannot re- affect performance during fl ight [22]. Determining fl ect actual smoking effect in our study [25]. when smokers are experiencing nicotine with- Hypoxia is another possible phenomenon drawal is diffi cult, although performance impair- that infl uences attention [26]. In Test 2, smoker ments have been observed after a few hours of groups 1 and 2 as well as the non-smoker group cigarette abstinence [23, 24]. Moreover, with- were slower at FL180 compared to smoker group drawal-induced performance defi cits, including 3 at ground level. Although no signifi cant differ- those related to attention, are not typically seen ences were found in each group compared to within two hours of tobacco deprivation [19]. To smoker group 3, this trend was visible in two tasks prevent the infl uence of nicotine withdrawal syn- (Figure 3 and Figure 4). In general, people need to drome on the evaluation of attention, we deprived be provided oxygen when the altitude is higher participants of tobacco for only two hours. In fu- than FL100. If people are not provided oxygen ture study, nicotine dependence severity (FTND), above this level, they can suffer from anoxia, abil- nicotine withdrawal measure, and expired CO ity loss, and death. Time of useful consciousness data collection after the task must be considered. (TUC), also referred to as effective performance Whether altitude infl uences the results of the time (EPT), is an important index for determining visual search and incompatibility tasks is an im- levels of hypoxia [27]. Generally speaking, TUC portant problem. Although the difference was not is relatively shorter with increases in body activity signifi cant, we found that smoker group 3 (1.0 or altitude. Various altitudes have corresponding mg-nicotine dose at ground level) responded fast- average TUC times. At FL180, oxygen pressure is er than smoker group 1 (1.0 mg-nicotine dose at 79 mmHg and TUC is approximately 20-30 min- FL180) on the visual search and incompatibility utes. In other words, a person will lose conscious- tasks of Test 2. Furthermore, the reaction time at ness after about 20-30 minutes at FL180. In this Test 2 was faster than Test 1 for the non-smoker study, each task required 2-3 minutes (5-6 minutes group. Thus, although change in altitude may not in total). Therefore, TUC likely had no infl uence have had any effect on attention statistically on our results. TUC length, however, varies from Cheng YM, Loh CH, Sha CB, et al. • 277 •

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