Reprint&Copyright9 by AerospaceMedicalAssociation,Washington,DC



# Sleep,Sleepiness,and Circadian Rhythmicity inAircrews Operating on Transatlantic Routes

HANS M. WEGMANN, ALEXANDER GUNDEL, MARTIN NAUMANN, ALEXANDER SAMEL, EDWIN SCHWARTZ, and MARTIN VEJVODA
D.F.V.L.R. Institute of Aviation Medicine, Cologne; and Deutsche Lufthansa AG, Frankfurt, West Germany

WEGMANNHM, GUNDELA, NAUMANNM, SAMELA, SCHWARTZE, VEJVODAM. Sleep, sleepiness, and circadian rhythmicityinaircrewsoperatingon transatlanticroutes.Aviat.Space Environ.Med. 1986;57(12, Suppl.):B53-64. This study was performed on B-747 aircrews operating on regular passenger flights between Frankfurt and the U.S.west coast (9 h time difference). In an initial phase, sleep behavior was surveyed by daily logs in 38 crewmembers. The results for the layover period indicate congruent sleep patterns with shifts in sleep onset distinctly lessthan 9 h. In comparison with preflight control data, sleepduration wassignificantly prolonged and, on average, no sleep deficits were experienced before commencingthereturn flight.Themain part ofthestudy consisted of polygraphic sleep recordings and multiple sleep latency tests (MSLT) applied to four complete cockpit crews (12 members total) in a baseline period, during layover, and after return to homebase. In addition, body temperature and ECG were continuously recorded. During layover, mean bed times were shifted by 4.5 h at maximum. Sleep was disturbed by early and prolonged awakenings which led to a reduction of sleep efficiency. In contrast, no sleep deficits nor increases in daytime sleepiness occurred. Night duty associated with the return flight causedsleepdeprivationwhich conversely resulted in goodsleep during the first night back in Germany. However, during the second night after return, impaired sleep was observed, at least in part caused by the rhythm disturbances. As predicted by our resynchronization model, ECGand rectal temperature recordings gave evidence for a desynchronization of the circadian system and an internal dissociation of different body functions. 

# I N PRINCIPLE, our investigationswere performedin two major phases. In a first step (Phase I) sleeplog surveyswere obtained from crews operating on the FRA-SFO and FRA-LAX routes. The latter route was included since the flight schedules of both routes are

Address reprintrequeststo: Dr. HansM.Wegmann,DFVLR InstitutfurFlugmedizin,Postfach906058, D-5000K61n90, West Germany. almostidentical.The primarypurpose ofthisphase was toobtainabetterunderstandingofindividualdailyhabits andstrategies.Asitsubsequentlyturnedout, thesesleep surveys also provided valuable information about the quantity of sleep and its deviation from "normal." The second phase (Phase II) served as the main part of our investigation and consisted of a battery of tests and measurements applied to a group of 12 volunteers operating as B-747 crews on scheduledpassenger flights between FRA and SFO. Like the other participating research groups, our centralpurpose wasto studysleep inaircrewsexposedto atimezoneconsiderablydifferent from their home base. However, since multiple time
zone transitions are known to affect sleep by circadian rhythm disturbances, additional efforts were aimed at defining changes in the 24-h fluctuations of selected variables. Therefore, besides studying sleep-EEG and daytime sleep latency (MSLT) in the laboratory, we continuously recorded body temperature and ECG and collected continuous urine samples. The additional measurements were conducted not only during preduty and layover (L/O) periods, but also during flight. Furthermore, we attempted to learn more about flight
crew readjustment to home time by continuing all measurements in the laboratory for approximately 2
more days after return to FRA. Fig. 1illustratestimelinesandthegeneralexperimental design. At the present time, the results are limited to sleep-EEG, MSLTs, body temperature and ECG records. The chemicalanalysisofurinaryhormones and electrolytes is still in process. MATERIALS AND METHODS During Phase I, 26 sleep logs were completed on the FRA-LAX route and 12 on the FRA-SFO route.
Aviation,Space,andEnvironmentalMedicine9 December,1986 B53SLEEP, SLEEPINESS, & RHYTHMICITY--WEGMANN ET AL.



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Fig. 1. Overview of time lines for the data collection of the flight schedule Frankfurt-San Francisco.

The two groups were labeled "LAX" and "SFI," respectively. In Phase II, 12 additional logs were obtained from the experimental group, "SF2." The Phase I sleep surveys extended from 2 days before flight duty until 2 days after return to home base, whereas Phase II logs extended up to 6 days before dutycommenced. To obtain better comparability between Phases, the additional 4 days were omitted from the analysis. Another difference was that Phase I crewmembers stayed in a hotel during their L/O and at home after the return flight. The experimental, Phase II group spent both periods in sleep laboratories. Phase II subjectswere fourcomplete cockpit crews (1 Capt, 1F/O, 1F/E) for a total of 12 subjects who were assembled from a group of volunteer crewmembers. The age for captains and flight engineers ranged from 44-53 years and for flight officers from 32-40 years. As Fig. 1 shows, measurements were conducted over a baseline period of36h in our Cologne sleeplaboratory, in most cases during the week before the flight. All measurements were carried out in September 1984, with each crew leaving for SFO on Wednesday and returning to FRA on Saturday. Scheduled flight times were (in GMT) FRA:0810-SFO:1935 for the outgoing and SFO:2145-FRA:0830 for the home-going flight. After arriving at SFO the crews stayed together in separate rooms at the Stanford sleep laboratory for the 48-h L/O period. After returning to FRA they were transported by helicopter to the Cologne laboratory, wheretheyremained foran additional44h (post-return). Table I summarizes allvariablesand methodsincluded in our investigation. Sleep EEG recordings were performed as described in detail in the introductory paper (Graeber 

### etal.). Contrary to the other research groups, respiration and legmovements were not recordedinthis study, and the pretrip measurements were conducted in the sequence: adaptation night, MSLTs, baseline night, i.e., the MSLTsdidnot followthebaseline sleepperiod. Sevenbaseline MSLTs were administered instead ofsix. ECG andrectaltemperature werecontinuouslyrecorded bymeans ofOxford Medilog tape recorders. Frequency analysis for the first harmonic was carried out on the

B54 TABLE I. OVERVIEW OF VARIABLES AND MEASURES.

Mood Sleepiness Sleep Rhythmicity (24h) Workload Pre-Sleep MSLT(EEG, EOG) EEG Temperature ECG Scales SSS EOG ECG Catecholamines

Fatigue Card EMG Urine Constituents 17-OHCS 10-cm Scale Sleep Log

Self-Ratings

SSS=Stanford Sleepiness Scale

Aviation, Space, andEnvironmental Medicine 9 December, 1986

### SLEEP, SLEEPINESS, & RHYTHMICITY--WEGMANN ET AL.

heart rate and temperature data, accordingto Bliss (1), by shifting a 24-h window by 1-h intervals over the entire experiment. The results from this analysis were compared with values predicted by a model for the estimation of resynchronization after time-zone flights (13). Urine samples were collected in approximately 2-h intervals and frozen for later chemical analysis. Subjective fatigue ratings (10) were obtained from the subjects at regular intervals during the awake periods. RESULTS 

### Sleep log surveys: Figs. 2 to 5 present those results from the sleep log surveys which relate to the selfratings of time and duration of sleep. Quality of sleep was also assessed by five different rating categories. These data will be published elsewhere. The means of sleep-onset and -end shown in Fig. 2 demonstrate that sleep timing under control conditions (days 1 and 2) can be considered quite normal. Thus, it can be concludedthat these aircrews, when at home, go to bed at about 2200 GMT and get up at about 0600 GMT. This is true for all three groups with only minor differences in the mean values. The sleep-end preceding flight duty on day 3 is earlier by 1-2 h, again in all three groups. As shown more clearly in the next figure, this results in a reduction of sleep duration, since sleep-onset on the prior evening is not adjusted correspondingly. During L/O, sleep timing is considerably shifted towards later hours, as would be expectedbythetimedifferenceof9h betweenFRA and SFO/LAX. However, crewmembers do not shift their sleep periods completely, i.e., on the average groups LAX and SF1 delayed their sleep by not more than 7-7.5 h (onset and end of sleep, respectively). Shifts of the experimental group are distinctly less (p<0.01), averaginga5-hdelayatthemost.Thus, theexperimental crews went to bed, fell asleep, and got up earlier than the crews staying at the hotel. After the return flight, sleep timing was immediately shifted back towards the habitual hours ofsleep at homebase. The experimental group (SF2) again differs from the others in that its
mean times exhibit a slower readjustment, especially sleep onset (p<0.001). In summary, Fig. 2 demonstrates similar sleep behavior patterns of the three groups before, during and afterthe dutyperiod. During L/O, shifts in sleep times on average were distinctly less than the difference in local time between FRA and SFO/LAX. Fig. 3presentstheresultsfromtheself-reportsofsleep duration for the different groups. The similarity of the patterns is evident. Compared with the sleep period on day 1 (control night), there is consistently a significant reductioninsleepdurationduringthenightimmediately precedingflightduty.Asdemonstratedpreviously,these shortersleepperiodsresultedprimarilyfromthe earlier wakeup times in preparation for the relatively early commencementof duty. Sleep duration is significantly extendedin all groups duringthe firstL/O, but onlyfor the experimental group during the second night. After the return-flight, significantchanges appear onlytwice: longer sleep on the first night for the LAX group and shorter sleep on the second night for the SF2 group. The pronounced reduction in the latter was, at least in part, caused by earlier arising at the end of the experiment due to an early pick-up time. As in the LAX group, a longer sleep duration occurred on the firstpost-return night for the SF1 group; however, this duration isnot significantlydifferentfromcontrollevels due to increased variance, probably caused by some substantially delayed return flights in this group. To summarize the findings of Fig. 3, it can be concluded that aircrews on the average slept less than "normal"
on the nightbeforecommencingduty, but considerably
more during the L/O period. Fig. 4 illustrates what we call "sleep balance," i.e., the sum of the deviations in sleep duration from control nights. Thus, the curves reflect sleep deficit or surplus accumulated each consecutive day over the entire experimental period. Again, the three groups exhibit almost identical patterns with a moderate sleep deficit on day 3, substantial surpluses during the L/O period, and dramatic deficits after the return flight. Obviously, thesedeficitsresultfromtheprecedingnight duty when normal sleep was not possible; however, if we take into accountthe afternoon sleep after arrival in

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~/ n= 12 GMT ;z i ' 6 1'2 ' 1; ~0 Fig.2. Subiectiveratings of beginning and end of sleep during control, layover, and post-return nights. Presentedare means (• S.D.) of the three different groups. (Numbers of days at the vertical axis refer to days beginning at 2400 GMT).

Aviation, Space, andEnvironmentalMedicine 9 December, 1986 

### B55SLEEP, SLEEPINESS, & RHYTHMICITY--WEGMANN ET AL.



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Fig.3. Subjective ratings of sleep duration during control, layover, and post-return nights (means • S.E.).*p <=0.05; **p<=O.01 for differences from sleep period of day 1.

[+h} 3 CGN, the sleep balance approaches zero. Althoughthe 2 practical implicationofcomputing sleep balance curves 1. may be debatable, they nevertheless demonstrate that 0 aircrews usually attempt to get enough sleep and that ~ 2" they succeed. 3. Finally, Fig. 5 combines the three groups' sleep ~. duration during the three major stages of the sleep log s. survey.Fromthedistributionofsleepdurationsitcanbe I-h] 6 concluded that under control conditions about 90% of sleep episodes were between 6 and 10 h. Sleep duration t.hl3-
was 5 h or less in only 5 out of98 cases, indicatingthat 2
1 severe sleepdeficitsdo occur, althoughveryrarely.This 0 number of extremely short sleep periods remains the 1
same throughout duty and post-duty days. In addition, 2 for the 2 L/O nights the histogram clearly shows a shift a to longer sleep durations with maxima of 13 and 14 s h in four cases. During the 2 post-return days, sleep t-h] 6 periods show a tendency to normal length. The higher incidence in the 6-h class mainly reflects the enforced early termination of sleep during group SF2's last test night in Cologne. Sleep recording and MSLTs: In preparing to compare sleep parameters withbaseline (B2) values, we firsthad to check the latter for outliers. Any value deviating by more than 2 S.D. (2-sigma-limit) from the group mean was defined as an outlier. Indeed, one subject exhibited REM sleep lower than this limit and wake time and time in bed (TIB) longer than this limit. In addition,hissubjectivesleepqualityratingwasbelowthe 2-sigma-limit. He complained about a headache during the baseline night and took two aspirin. As an apparent outlier, this subject was excluded when comparisons with baseline data were made.
B56 Aviation, Space,andEnvironmental Medicine 9 December, 1986 [+hl 3 2 1
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S I-hi 6 2 3 ~ 5 6 "] 8 DAYS Fig.4. Sleep balance: accumulated deviations of subiectively rated sleep duration from control nights (day 1 and day 2). Values do not include short extra sleep periods (naps). Open circlesand dashed linesrepresent sleep balance includingsleep in the afternoon following return flight.SLEEP, SLEEPINESS, & RHYTHMICITY--WEGMANN ET AL.
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2 3 ~ 5 6 7 8 9 10 11 12 ' ' ' ' ' ' ' 3 14 [h] Fig. 5. Histogram of subjectively rated sleep duration of all three groups together. Combined are two nightseach from the control, layover, and post-return period. (Note: sleep period immediately preceding flight schedule not included). 0 4 8 12 16 20 GMT

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Fig. 6. Time schedule of sleep periods and flights. Time axis is chosenfrom 2000 to 2000 GMT. Barsfor sleep periods show standard deviation for light off and on. Baseline recordings were taken several days before flight to SFO.

The beginning and end of sleep periods were calculated as mean times (n--12) of lights-off and lightson and summarized in Fig. 6. Compared with baselines B1 and B2 when crewmembers went to bed at about 2200 GMT, their mean bed times shifted by 3.2 h
on the first L/O night (SFO1) and by 4.5 h on the second (SFO2). These values generally agree with those obtained from the sleep logs for the same period. For both sleep periods the average TIB was longer than during baseline or post-return. Get-up times showed considerable interindividual variability, with a standard deviation about twice that for baseline and post-return sleep. Before leaving Stanford for the return flight, nine subjects tried to nap, seven of them fell asleep. After the return flight, which was a complete night flight according to FRA time, all crewmembers went to bed in the afternoon (CGN1). On the following 2 nights, sleep was delayed by 1.9 h (CGN2) and 1.0 h (CGN3), compared to baseline.

Fig. 7 shows the total sleep time (TST) as well as the percentages for different sleep stages. While TST was about7.0h forallnight-sleepperiodsinCologne (except for CGN3, as explained above), it increased to almost 8.0 h during L/O. The afternoon sleep following the return flight (CGN1) had a mean TST of 3.5 h. REM sleep (%) was nearly constant for all sleep periods, Fig. 7. Mean percentage of total sleep time (TST)for sleep stages. Means (n=12)areshownforseven sleep periods. Absolute TST value (rain) are given on top of the bars.

Aviation, Space, andEnvironmentalMedicine 9 December, 1986 B57

### SLEEP, SLEEPINESS, & RHYTHMICITY--WEGMANN ET AL.

TABLE II. COMPARISON OF BASELINE (B2) SLEEP PARAMETERS (n= 11) WITH THOSE FROM 40-49-YEAR-OLD MALES (Williams) AND FROM ADAPTATION (B1), LAYOVER, AND POST-TRIP RECORDINGS.
Source Minutes Percentage TIB TST S 1 $2 $3+ $4 REM

B2 460.20 414.60 9.24 57.98 10.48 22.30 Williams 429.10 389.10 8.07a 58.41 a 9.13a 24.39a B1 494.50* 420.40 12.38" 57.86 6.90 22.85 SFO1 572.30** 477.50* * 11.93* 55.59 10.13 22.35 SFO2 529.80** 461.90"* 10.19 57.48 9.38 22.96 CGN1 219.10"* 208.70** 6.67 56.23 23.47** 13.63"* CGN2 469.80 429.90 7.22 56.84 8.32 27.61 * * CGN3 409.40 342.90 9.86 55.75 13.12 21.27
*p<0.05; **p<0.01
ao~ SPT values given by Williams were transformed to % TST 

### except for a decrease during CGN1 and an increase in CGN2. While stage 2 sleep (%) was also fairly constant, slow wave sleep (stages 3 +4, SWS) displayed a greater variability between sleep periods and a strikingly higher portion in CGN1. Large differences were also observed for stage 1.

Table II compares the baseline (B2) sleep parameters of our group with data reported by Williams et al. 

### (14) for a group ofmales (n= 10) ranging in age from 40-49 years. TIB, TST, as well as sleep stage percentages do not differ significantly. In addition, this table compares all sleep periods with baseline sleep B2. As might be expected, the adaptation night (B1) produced a longer meanTIB (p<0.05) and more stage 1sleep. During L/O nights, TIB andTST were significantly longerwithmore stage 1 sleep (%) in SFO1. The afternoon sleep CGN1 had more SWS(%) and less REM sleep (%), while the following night (CGN2) showed enhanced REM sleep.

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Fig. 8. Median (n =12) latencies to the first 10 minutes of persistent sleep, to slow-wave sleep ($3), and to REM sleep. Significant differences from baseline values (B2) are indicated (*p<O.OS, **p<O.01. Wilcoxon-matched-pairs-signed-rank test).


### B58 Aviation, Space, andEnvironmental Medicine 9 December, 1986 MEDIAN SUBJECTIVE SLEEP QUALITY

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### SLEEP, SLEEPINESS, & RHYTHMICITY--WEGMANN ET AL.
Median latencies to sleep onset, slow-wave sleep ($3), and REM sleep are shown in Fig. 8. Though the interindividual variability was rather high, the following comparisons to baseline were statistically significant: longer latencies to sleep onset and REM during adaptation, reduced latency to $3 for the CGN1 day sleep, and delayed sleep onset on the second postreturn night (CGN3).

Fig. 9 presents median values of several sleep quality parameters. The number ofawakenings varied between 5 (CGN1) and 11.5 (B1). In comparison with B2, sleep was less efficient during B1, SFO1, and CGN3, but more efficient during CGN1. Subjective sleep quality ratings also suggest poorer sleep during B1, SFO1, and CGN3. Computationsofcorrelationsbetween sleep qualityparameters and age revealed significantnegative coefficients (r---0.63, p<0.05) for sleep efficiency during each L/O night, but not for total sleep time.

Individual sleep patterns and MSLT results for baseline, L/O, and post-return are presented in Fig. 10. Most of the crewmembers underwent one SLT after arrival at Stanford and 5-9 MSLTs between the major sleep periods. For sleep SFO1, subjects went to bed at verydifferenttimes, andthisrankorderremainedalmost the same for SFO2. One subject (row 6) had relatively long naps in addition to his short sleep periods and

Fig. 10. Sleep pattern and multiple sleep latency test (MSLT). Sleep periods in black, waketimes in white. Vertical lines between sleep periods represent MSLT;their height is sleep latency in minutes. (Top left=Baseline; top right--L/O; lower left--Postreturn).

Aviation, Space, andEnvironmentalMedicine 9 December, 1986 

### B59SLEEP, SLEEPINESS, & RHYTHMICITY--WEGMANN ET AL.

Fig. 11. Mean MSLT after sleep periods B1, SFO1, SFO2, CGN2. 20- rain

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seemedtostayonhome-basetime. Shiftsofsleepperiods were more obvious for other subjects who exhibited longer TIB. As this figure clearly indicates, reduced sleep efficiency resulted from long waking times a) in the second half of SFO1 sleep and b) in the beginning of CGN3 sleep. Mean SLTvalueswerecalculatedonlyifatleast seven subjects performed the SLT at the corresponding time. In the home time zone, these mean values revealed 381
a general pattern of long latencies immediately after 

# J sleep, short latencies in the afternoon, and longer 36 again in the early evening (Fig. 11). During L/O, 38] when measurements were extended until late evening, 

# J the MSLT showed the typical biphasic contour. The 36 longest onset latencies were alwaysfound afterthe main sleep periods (B1, SFO1, SFO2, CGN2), regardless 381 of how far they were shifted. Comparison of MSLT 

# J latencies revealed the following significant differences 36 (Wilcoxon test): a) increase between 1600 and 1800 381 GMT for baseline (p<0.05) and L/O (p<0.10); b) 

# 1 increase between 1600 and 2000 GMT for baseline 36 (p<0.05), L/O (p<0.01), and post-return (p<0.05); c) 38] and a decrease between 2000 and 2400 GMT for L/O (p<0.05). In addition, latencies of the MSLTs at 1800 36 GMTwere significantly different (p<0.05) betweenL/O 381 and post-return. 36

# ] Temperature and ECG: As compared with baseline data, temperature and heart rate curvesrevealeddistinct 381 phase shifts during L/O and after return to FRA. 36

# ] The curves in Fig. 12 represent mean values from all experimental subjects. Computed minima (1), as well 38]
as minima predicted by our model (13), are marked 36

# J differently in the figure. Vertical lines illustrate where theminima wouldbeexpectedifsubjectshad completely adapted to SFO time. The temperature rhythm was shifted by 3.75 h on the first and by 5 h on the second day of the L/O period (both relative to baseline), while after return to home base the shift was 3.25 h relative to the last day in SFO (or 2.75 h relative to baseline). The rhythm of heart rate was shifted even more: 6.25 h on the first day in SFO and 7.0 h on the second; after return to FRA a shift of 6.0 h relative to SFO2 occurred, which corresponds to a time difference of 1 h relative to the baseline rhythm.

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20 22 24 02 04 06 08 10 12 14 16 18 20 9actual and 9predicted minimaof temperature
v actuoland a predicted minimaof heartfrequency Fig. 12. Means for temperature (upper curves) and heart rate (lower curves) before, during and after flights. Vertical lines indicate position of minima during baseline and after complete shift by 9 h (solid lines:temperature; dashed lines: heart rate).

B60 Aviation,Space,andEnvironmentalMedicine 9 December,1986SLEEP, SLEEPINESS, & RHYTHMICITY--WEGMANN ET AL.

TABLEIII.ESTIMATED24 h MEANSAND AMPLITUDESOF HEARTRATE AND TEMPERATURECOMPUTEDFROMAVERAGECURVES [AfterBliss(1)].

SOURCE HEARTRATE TEMPERATURE

(L-min-I) (~ Mean Amplitude Mean Amplitude
B1/B2 68.5 13.0 36.8 0.55 SFO1 71.5 19.5 36.75 1.00 SFO2 72.5 17.5 36.8 0.60

As a consequenceofthe differentadjustment speeds, internal dissociation can be observed. The phase difference between heart rate and temperature rhythms
was -1 h duringbaseline periods and changedto + 1.5 h during the first and + 1.0 h during the second day in SFO.Duetothefasterreadaptationoftheheartrate, the phase differencebecame -2.75 h after return to home base. Noactualminimafromharmonicanalysisaregiven for the return-flight day, because of the irregularities in the sleep-wake cycle. According to FRA time this flight was a total night flight. Even if related to the shifted circadian rhythm (delayby 5 h), it must still be considered as night duty, at least in part. Inspection of the curves demonstrates that, though the firstcircadian trough occurred in the second part of the duty period, heartrateandtemperaturealreadyincreasedagainabout 2 h before landing. Theperiodicaldecreaseofheartrate andtemperature every 2 h during awake time in Fig. 12 was most likely caused by the reduction of activity during MSLTs. Compared with the heart rate oscillations, the temperature fluctuations were delayed by 20-30 min. While the 24-h means of the circadian rhythms show only minor variation, the amplitudes are considerably higher during L/O as compared with baseline and postreturn periods (Table III). In our view, this is mainly caused by a masking effect. From the longer sleep durationsonecouldexpectanincreaseinamplitudesince longer periods of inactivityresult in longer sections of lowervalues in heart rate and temperature rhythms. At the same time, this would also lead to a decrease in the 24-h mean, butinourcasesuchaneffectiscompensated by the higher physical activity of most subjects during the day at Stanford (e.g., bicycling and jogging). Of course, these activities enhance the rhythm amplitudes
even more by adding sections of values higher than normal to the rhythm curves. In order to interpret the circadian results in more detail, shifts in acrophases of temperature and heart rate as well: as those predicted by our model are presented in Fig. 13, along with the subjects' mean daily bedtimes. All parameters indicate a clear shift towards the corresponding hours of the new time-zone (by a delay during L/O and by an advance after return to CGN). However, heart rate adapts faster, mainly due to the simultaneous shift of the rest-activity cycle. Temperature acrophases shift more slowly, and their adjustmentpattern corresponds well with the bedtimes, except for day CGN3. Fig. 13 also demonstrates that changes in temperature rhythm acrophase, after either westward or eastward flight, can be correctlypredicted by our model of resynchronization. DISCUSSION Our experimental design was based initially on the following hypothesis: Due to the considerable time differencebetweenFRA and SFO, aircrews performing dutyonthisroutewouldsufferfromrhythmdisturbance oftheircircadian system.As a directconsequence, they wouldalsoexperiencesleepdifficulties,aproblemwhich hasrepeatedlybeen a matter of serious concern among aircrews and safety researchers (5,7,8). Furthermore, sleep difficultieswould be manifestedby sleep loss and reducedsleepquality,bothintermsofsubjectiveratings and objective EEG recordings.

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Fig. 13. Shifts in acrophases relative to baseline position.

Aviation, Space, andEnvironmentalMedicine 9 December, 1986 B61SLEEP, SLEEPINESS, & RHYTHMICITY--WEGMANN ET AL.

Sleep loganalysis: Clearly, the results from our sleeplog surveys do not support the above hypothesis. In contrast, there is convincing evidence that our pilots slept significantly more during the L/O period and did not suffer at all from sleep loss, as compared with their normal sleep habits at home base. It is not possible to determine whether this was achieved by conscious attempts or by efforts and conditions beyond the subjects' direct control. From personal communications, however, we are inclined to conclude that the majority ofthe pilotpopulation iswellaware of this problem and takes serious measures to get enough sleep. No doubt, the results from the sleep-log surveys demonstrate that they succeed; however, the findings presented in this paper do not rule out the possibility that sleep deficits may occur in individual cases. The presented results deal only with computed means and, thus, merelyreflectaverage behavior. There are already indications that severe sleepdeficitsmaybeexperienced by some crewmembers. In at least five cases, sleep was 5h orlessduring L/O aswellasduring control and postreturn periods (with a 3-h minimum in one case). A
more detailed analysis is planned to settle this question of individual problems. There is another, more general, but also quite unexpected result that the sleep-log surveys are disclosing. Initially, all participating research groups were concerned about whether the sleep laboratory would be an adequate setting to obtain realistic information about "true" L/O behavior in the hotel environment. Comparison ofthe three sleep-loggroups reveals strong evidence that we were well "on the safe side," in
essence for two reasons: a) the patterns of sleep timing and duration were almost identical; in fact, statistical analysis (Kruksal-Wallis test) did not detect any general difference when the data sets (entities of 8 days) as a whole were compared, and b) during the first L/O, night sleep duration in the laboratory was significantly shorter than in the hotel environment (U-test); again, this wasin contrast to what had been expected. Despite the quiet, isolated surroundings ofthe sleepfacility, our subjectgroup didnot sleeplongerthan aircrewstayingin thecommercial atmosphere ofthecityhotel. Inaddition, during both post-return nights, the laboratory group reported distinctly shorter sleepdurations than the other groups sleeping at home. Thus, the data clearly refute the argument that sleep deficits could be anticipated in the realistic world even though they had not been observed in the laboratory. Of course, conclusions drawn from subjective ratings may give cause for criticism. However, subjective estimates of sleep duration, i.e., time between onset and end, correlate well with objective measurements. This is not necessarily true for the amount of sleep, since number and time of awakenings are frequently misjudged, thus leading to major discrepancies between subjective and objective assessments oftotal sleeptime. Theoretically, our sleep-log data could have indicated longer sleep periods despite a decrease in the amount of sleep, if our subjects had suffered from longer awakenings than accounted for by the surplus in sleep duration. In fact, the sleep-EEG recordings in our experimental group disclosed considerably prolonged awake periods during L/O sleep. Nevertheless, total sleep time was distinctly longer than under baseline conditions. To us, there appears to be little evidence that this should be different in the two other groups. In particular, the impressive and consistent similarities between the three groups in almost all sleep-log results support this view. Sleep recording and MSLT analysis: As a prerequisite for discussing details of the sleep-EEG and MSLT results it is important to know whether there are any differences between crewmembers' usual habits and their behavior in the laboratory, and how such differences may influence final conclusions about the study. Each time subjects left the sleep laboratories, questionnaires were administered asking for general sleep quality and a comparison between their usual sleeping conditions and those of the laboratory. In general, the answers to each question were equivalent after the baseline, L/O, and post-return periods. On a 5- point scale from "very poor" to "very good," the subjects consistently rated their sleep quality as being good. Quantity of sleep, daytime drowsiness, and quantity of meals were judged as comparable with the usual conditions. Upon leaving the Cologne laboratory after the post-return phase, all crewmembers were interviewed. Six claimed that their sleepwasbetter than at home, and six reported no difference. The improved sleep was attributed to the darkness and silence of the laboratory and to the absence offamilydisturbances. In contrast to what we inferred from the sleep-log surveys, these findings could mean that conclusions regarding sleepqualitydrawn fromthe experimental results should be rather conservative with regard to sleep in the usual world, where flight crews are sometimes faced with a more disturbing environment. The experimental part of the sleep investigations revealed a clearpattern ofsleepperiodswith onlyminor individual differences. During L/O, the onset of the two main sleep periods was shifted ahead by 3.2 and 4.5 h, respectively, as compared with baseline data. Our results cannot distinguish whether these shifts were due to a phase shift of an autonomous circadian sleep rhythm, orwhether theyreflecta consciouscompromise between increased fatigue and an adjustment to the social environment of the new time zone. If the crewmembers delayed sleep completely by 9 h, they would be much more tired during the presleep hours. Even withonlyapartial sleepdelay, Stanford SleepinessScale (SSS)ratings and MSLTresultsindicatethat the subjects
were more tired before L/O sleep than before baseline
or post-return sleep. After the return flight, which according to FRA local time was a complete night flight, crewmembers retired in the afternoon for a recovery sleep of several hours. For the night-sleep periods, theywent to bedmore than 1 h later than during baseline. As there was no social need, this behavior may be explained by a circadian phase delay resulting from the preceding adjustment to the SFO time zone. However, another reason is also conceivable: it might be assumed that recovery sleep in

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the afternoon leads to delayed tiredness in the evening and consequently to a later sleep time. Objective sleep quality may be conceived as a matter ofthe amount and continuity of sleep. Accordingly, the typical disturbance of sleep during the adaptation night
was manifested by decreased sleep efficiency, a higher number ofawakenings, alonger sleep-onsetlatency, and
a longer latency to REM sleep. Despite this impaired sleepquality, there wasno increase ofoverall sleepiness during the day. In fact, the MSLT results provided no indication of an abnormal increase in sleep tendency during any phase of the study. On the first L/O night subjects slept less efficiently and rated their sleep subjectivelyworse. The efficiency
was reduced by relatively long awakenings during the second half ofthe night. Probably, the circadian system forced them to awake too early, e.g., because they felt hungry or had to use the bathroom. Possibly due to training or experience, they were able to fall asleep again and to compensate somewhat for the effects of shifted sleep by staying in bed longer. Thus, at the end they got even more total sleep than during the baseline night. The sleep disturbances seen during SFO1 were not as pronounced for SFO2. However, from correlational analysis, we found that difficultiesin sleepcontinuity during L/O increased with age, sothat oldercrewmembershadtostayinbedlonger than younger ones in order to get enough sleep. The majority of the crewmembers took a nap before thereturn flighthome. This short extra sleepmost likely improved alertness for the following night shift (6,9). During the return flightthe subjectsincurred a sleeploss whichmayaccountforthegoodsleepexperiencedduring the afternoon and first night after arrival in Germany. The afternoon sleep was characterized by a rebound of SWS, i.e., a short latency to stage 3 sleep and more SWS(%) than observed during baseline. During the following night a rebound of REM sleep was observed. These effects are well known as consequences of sleep deprivation. During the second night, objective as well
as subjective sleep quality was reduced, very likely due to rhythm disturbances, some of which were detected in MSLT and body temperature. The MSLT results closely reflect the 24-h profiles reported by Richardson et al. (11). Nevertheless, the interpretation of MSLT results turned out to be more complicated. At least two factors seem to influence daytime sleepiness. The first is related to the time since the preceding sleep. Thus, long sleep latencies were observedwheneversubjectshadrecentlyawakenedfrom
a major sleep regardless of time of day. After pilots awoke, they were unlikely to fall asleep during the following SLT. A second factor reflects a circadian influence on sleep tendency. It is characterized by relativelyhigh sleepiness around midday and an increase in sleep latency in the late afternoon. The increase occurred at the same time (GMT) during the baseline and L/O periods. Consequently, we conclude that the underlying sleepiness rhythm might have shifted too slowly to be disclosed after the westbound flight. The observation of an SLT-rhythm delay after the return flight supports the viewthat the delayed nocturnal sleep in Cologne is related to the observed delay in the circadian rhythmicity of other physiological functions. Rhythm disturbances: As expected, our results provided evidence that the time-zone transition associated with flight duty on the FRA-SFO route leads to a) desynchronization of internal body time from the external timing system, and b) an internal dissociation between the circadian rhythms of different body functions. Both effects influence sleep behavior. This wasmost clearly shown bythe early and prolonged awakenings of the first L/O sleep period. Most likely theseawakenings weretriggered bythe circadian system, which was out of phase with the new local time by an advance of more than 5 h (according to the acrophase ofthe temperature rhythm). Due to progressive synchronization, awakenings occurred atlaterhours and became shorter or disappeared during the second nocturnal sleepperiod. Incontrast to awakenings, sleeponset time is influenced by other factors in addition to circadian rhythmicity, e.g., activation, consciousefforts, and in particular the duration of the preceding awake period. Therefore, the advance of sleep-onset during L/O may not reflect the "true" shift of the underlying rhythm, but more probably is the result of several influences. This could also explain our findings from the sleep surveysthat sleep-onset time in the laboratory
was earlier than in the hotel. For the post-return period we were also able to demonstrate a desynchronization of circadian rhythms fromlocaltime. In contrast tothe SFOL/O, however, it was a delay and the extent was less pronounced (ca. 2 h). Theoretically, this again should affect sleep; but awakenings would be expected at the beginning of the sleep period, or a delayed onset of sleep should occur. As already mentioned, our EEG data confirmed this assumption for the second night, whereas the findings for the first nocturnal sleep were confounded by the effectsofsleep deprivation and the preceding afternoon sleep. Our rhythm results reveal one other important operationally relevant fact. Due to the relatively short L/O period, synchronization with SFO time was not completed. In fact, the circadian systemhad onlyshifted byabout 5 h beforethe return flight commenced. Thus, readaptation to home-base time would be comparable to conditions after the transition of five time zones. As aresult, desynchronization onthe secondpost-return day was not more than about 2.5 h, which is below the limit (3 h) that is accepted as critical in terms of operational significance (13,15).

CONCLUSIONS We were able to show that the time zone transition associated with FRA-SFO flight duty leads to a desynchronization ofthe circadian system. According to our hypothesis, rhythm disturbances would cause major difficulties for sleep quality and quantity. However, from our subjective and objective sleep data we must conclude that the observeddesynchronization produced only moderate effects upon sleep. During L/O, early and extended awakenings led to a reduction of sleep

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efficiency, but did not cause sleep deficits. Sleepiness during the diurnal phase was not elevated, but quite normal. Night duty during the return flight caused sleep deprivation which in turn resulted in good sleep during the first night at homebase; however, impaired sleep occurred on the second night, at least in part caused by desynchronization. Nevertheless, resynchronization to homebase time appears fast enough that pilots can achieve a reasonable readjustment before commencing flight duty again. Obviously, these conclusions cannot be generalized. In the present form, our results consider only mean values and do not address individual cases where the situation may be far less favorable than on the average, Finally, our conclusions apply only to a duty schedule that isrelatively short and not especially complex. There
are other duty patterns that require operations with much more complex schedules involving many more days away from home base and more transit stops in different time zones. From these we may anticipate a quite different picture as to sleep problems and rhythm disturbances. Finally, it should be mentioned that the present results fit well into the line of our previous studies in aircrews and complement the results that have been obtained from short-haul (4) as well as from longhaul flight schedules (2,3,12).

ACKNOWLEDGMENTS The authors are very much obliged to the staff of the Stanford University Sleep Research Center who carried out the sleep and MSLT recordings during the L/O period in the U.S. We wish to express our sincere gratitude to the participating crewmembers for their exceptional motivation and outstanding cooperation. Special thanks go to Ute Brandl, Gabriele Kraus, and Paul Esser for their valuable assistance. This research was supported by the U.S. National Aeronautics and Space Administration (NASA Cooperative Agreement NCC2-302with Stanford University School of Medicine) and the German Ministry of Transport. REFERENCES 1. BlissCL. Statistics in biology. New York: McGraw Hill, 1970. 2. Klein KE, Bruner H, Ruff S. Untersuchungen zur Belastung des Bordpersonals auf Fernflugen mit Dusenmaschinen. Bericht uber die Ergebnisse aufder Nordatlantikroute. DLRForschungs-bericht 1965;65-44:1-68. 3. KleinKE,BrunerH,Holtmann H,RehmeH, StolzeT, Steinhoff WD, Wegmann HM. Circadian rhythm of pilot's efficiency and effects of multiple time zone travel. Aerospace Med. 1970; 41:125-32. 4. Klein KE, Bruner H, Kuklinski K, Ruff S, Wegmann HM. Bericht uber die Auswertung von Untersuchungen am fliegenden Personal der DLH zur Frage der beruflichen Beanspruchung aufder europaischen Kurzstrecke. Koln-Porz: DFVLR-Institut fur Flugmedizin. Interner Bericht 1974;335 -74/2:1-42. 5. Klein KE, Wegmann HM~ Significance of circadian rhythms in aerospace operations, AGARDograph No. 247. NeuillySur-Seine: NATO-AGARD, 1980. 6. Mullaney DJ, Kripke DF, Fleck PA, Johnson LC. Sleep loss and nap effects on sustained continuous performance. Psychophysiology 1983;20:643-51. 7. Nicholson AN. Duty hours and sleep patterns in aircrew operating world-wide routes. Aerospace Med. 1972;43:138 -41. 8. Nieholson AN, Stone BM, Borland RG, Spencer MB. Adaptation to irregularity of rest and activity. Aviat. Space Environ. Med. 1984;55:102-12. 9. Nicholson AN, Pascoe PA, Roehrs T, Roth T, Spencer MB, StoneBM,ZorickF. Sustainedperformance withshortevening and morning sleeps. Aviat. SpaceEnviron. Med. 1985;56:105 -14. 10. Pearson RG, Byars GE. The development and validation of a checklist for measuring subjective fatigue. USAF School Aerospace Med. Tech. Rept. 1956;SAM-TR-56-115. Randolph AFB, TX. 11. Richardson GS, Carskadon MA, Orav EJ, Dement WC. Circadian variation in sleep tendency in elderly and young adult subjects. Sleep 1982;5(Suppl. 2):82-94. 12. Wegmann HM, Klein KE, Goeters KM, Samel A. Flugmedizinische Untersuchungen zur DLH Non-Stop-Route Frankfurt-Rio de Janeiro. Koln-Porz: DFVLR-Institut fur Flugmedizin. Interner Bericht 1981;316-81-01:1-29. 13. Wegmann HM, Klein KE, Conrad B, Esser P. A model for prediction of resynchronization after time-zone flights. Aviat. Space Environ. Med. 1983;54:524-7. 14. WilliamsRL, Karacan I, Hursch CJ. EEG of human sleep. New York: John Wiley and Sons, 1974. 15. Zweite Durchfuhrungsverordnung zur Betriebsordnung fur Luftfahrtgerat (2.DVOLuftBo). Frankfurt (Main): Bundesanstalt fur Flugsicherung, 1981.

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