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Clinical Studies |
Department of Obstetrics and Gynecology, Northwestern University Medical School, Chicago, Illinois 60611; and the U.S. Army Research Laboratory, Aberdeen Proving Ground, Aberdeen, Maryland 21005
Address all correspondence and requests for reprints to: Robert T. Chatterton, Ph.D., Department of Obstetrics and Gynecology, Northwestern University Medical School, 333 East Superior Street, Chicago, Illinois 60611.
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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In the studies of stress responses to parachuting reported in the monograph by Levine et al. (2), a primary focus was on modification of the physiological effects of parachute jumping after successive experiences. That is, those investigators sought to evaluate the coping ability of the participants. In the present study our primary interest was in the period of time preceding the jump, the time when psychological forces alone are acting. Other studies of this type (3, 4, 5, 6, 7, 8) have not compared the period immediately before the stress event with hormone levels and psychological measures determined in control subjects. Although parachute jumping has been considered primarily a psychological stressor, the acceleration forces involved are a physical stressor that may alter blood flow within the body and cause substantial increases in plasma cortisol and catecholamine levels. Centrifugal forces have been shown to produce 2- to 3-fold increases in plasma cortisol and catecholamines (9).
Anticipatory coping responses may occur before a major inevitable stressor, such as a surgical procedure (10) or aircraft landings at sea (11), particularly before the actual physical preparation for the event (10) or when the outcome is in another person’s hands (11). In the present study naive volunteers were informed that they would be skydiving with an instructor; however, the degree of control that was theirs was not made known until the prejump instruction. Psychological perception of stress was assessed at intervals before and after the jump, and hormone levels in blood and saliva were measured to monitor physiological responses.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Subjects were male students and staff recruited from the Northwestern University Medical Center in Chicago. The average age of the 26 volunteers was 26.4 yr (range, 22–36 yr). None had previously parachuted or skydived from an airplane. All had had a physical examination within the year before they volunteered, and all were in good health. All subjects completed the trait and state portions of the State-Trait Anxiety Inventory (STAI) (12) and the Multiple Affect Adjective Checklist–Revised (MAACL-R) (13) and provided single blood and saliva samples at a mean time of 1400 h, 3–5 days before the day of the skydive was scheduled. The study was approved by the institutional review board of Northwestern University, and all subjects signed the informed consent form before participation in the study.
On any given day between one and three subjects participated in the study. Recruits had an indwelling catheter with a heparin lock inserted into an antecubital vein before leaving the medical center at 0745 h for a 45-min ride to the skydiving school. On the way to the site, four samples of heparinized blood and saliva were collected from the volunteers, one sample every 15 min. Saliva flow was stimulated by chewing sugarless gum, and saliva was collected by expectoration into a 30-mL plastic beaker and stored on ice. Additional samples were obtained after the 1-h classroom instruction, just before entering the airplane (time zero). After an approximately 30-min flight, the subjects jumped with an instructor. The altitude of the plane at the time of the jump was 9,000–10,000 ft; the student and instructor were attached by a harness with the instructor behind the student, and they experienced free fall for 4,000–5000 ft before the parachute was opened. It was the student’s responsibility to pull the rip cord to open the parachute. Immediately after the subjects touched the ground, a blood sample was drawn from the indwelling catheter, and saliva was collected. Additional blood and saliva samples were obtained at 15-min intervals for the next 45 min. Samples were placed in sealed containers and kept on ice until being returned to the medical center in the afternoon.
The state portions of the psychological instruments were administered to the volunteers between the first and second blood and saliva collections on the morning of the jump (0800–0815 h), just before boarding the plane (1230 h), and after returning to the skydiving center after the jump (1345–1400 h) to assess their perceptions of anxiety, hostility, depression, and overall stress levels.
Control subjects were also recruited from the medical center. Blood was collected from an indwelling catheter, and saliva was collected in the same manner as in the subjects who volunteered for the skydiving lesson. The timing of the three samples was calculated to correspond to 1) the mean time of the fourth sample of the morning, 2) the sample taken just before subjects entered the plane, and 3) the last sample of the day. Subjects read, watched television, or walked in the area. The average age of the 17 control subjects was 26.4 yr (range, 22–36 yr).
Psychological assessment
Trait measures. The following instruments were administered 3–5 days before the scheduled skydive: the MAACL-R, general form (13); the STAI, form Y-2 (12); and the SSS, form V (1). The respondents were instructed to check all the words or phrases that described how they "generally" feel.
State measures. The following instruments were administered on the control day and three times on the day of the jump: the Today form of the MAACL-R (13); form Y-1 (State form) of the STAI (12); the Subjective Stress Scale (Subj) of Kerle and Bialek (14), a list of 15 adjectives from which the subjects selected one word best describing how they felt; the Specific Rating of Events scale (SRE), in which subjects rate (on a scale of 0 for "not at all stressful" to 100 for "most stress possible") how stressed they feel "right now" or how stressful an event or time period was to them (15).
Biochemical measures
-Amylase assay.
Saliva was diluted 500-fold with 0.154
mol/L NaCl. Assay kits, obtained from Sigma Chemical Co. (St. Louis,
MO), were used. They used 1.0 mmol/L 4,6-ethylidene
(-D-maltoheptaside)7-p-nitrophenyl
as the substrate with 25,000 U/L -1,4-glucan glucohydrolase (EC
3.2.1.3) in a pH 7.0 phosphate buffer containing 10 mmol/L
MgCl2 and 50 mmol/L NaCl. The p-nitrophenol
product was measured spectrophotometrically at 405 nm after a 2-min
incubation at 37 C. The quality control for the assay was prepared from
a pool of saliva that was collected from unstressed volunteers. The
pool was divided into 1.0-mL aliquots and frozen in sealed vials. One
vial was thawed and run with each assay. The interassay coefficient of
variation (CV) of the quality control preparation was 8.5%.
Plasma cortisol. Plasma cortisol was assayed by RIA without extraction after a 1/100 dilution in 0.1 mol/L citrate, pH 4.0, buffer as performed previously (16). The interassay CV was 14%; the intraassay CV was 11% (mean, 309 nmol/L). The sensitivity of the assay at this dilution was 47 nmol/L.
Salivary cortisol. Salivary cortisol was assayed by RIA without extraction after a 1:10 dilution in 0.1 mol/L citrate buffer, pH 4.0. The antiserum and labeled cortisol were previously described (16). The interassay CV was 14%; the intraassay CV was 12% (mean, 11 nmol/L). The sensitivity of the assay at this dilution was 68 pmol/L.
Plasma PRL. Plasma PRL was assayed by RIA with materials obtained from the National Hormone and Pituitary Program of the NIDDK, NIH, at the University of Maryland according to recommendations provided with the material. The reference and iodination materials for PRL assay were NIDDK human (h) PRL RP-1 and NIDDK hPRL I-7, respectively. The antiserum was NIDDK anti-hPRL-3. The sensitivity of the assay was 2.1 ng/mL. The interassay CV was 22% (mean, 9.0 ng/mL), and the intraassay CV was 17.6% (mean, 9.1 ng/mL).
Plasma testosterone. Plasma testosterone was assayed by RIA by a direct method without extraction. Materials, including [125I]testosterone, for this procedure were obtained from Pantex (Santa Monica, CA). Antibody-bound testosterone was precipitated from solution by the addition of a second antibody in polyethylene glycol. The sensitivity of the assay (2 SD at the lowest standard) was 368 pmol/L. The interassay CV (mean, 1747 pmol/L) was 15%; the intraassay CV was 9.9%.
Salivary testosterone. Salivary testosterone was measured by RIA without extraction. Antiserum was prepared in this laboratory. Cross-reactivities with dihydrotestosterone and androstenedione were 13% and 0.2%; those for androsterone, etiocholanolone, estradiol, and dehydroepiandrosterone were all less than 0.1%. The interassay CVs were 10.5% for the low reference (0.13 nmol/L) and 16.7% for the high reference (0.40 nmol/L). The intraassay CV was 14.1%. The sensitivity was 0.028 nmol/L.
LH. LH was assayed by RIA with materials supplied by the National Hormone and Pituitary Program of the NIDDK. Iodination with 125I, purification of the iodinated hormone, and separation of the antibody-bound hormone from unbound hormone were performed as described by Midgley, Jr. (17). The interassay CV (mean, 12 mIU/mL) was 15%; the intraassay was 26%. The sensitivity of the assay was 2.4 mIU/mL.
GH. GH was assayed by RIA with materials obtained from the National Hormone and Pituitary Program, NIDDK. The standard and iodination materials were hGH RP-1 and hGH I-1, respectively. The sensitivity of the assay was 1.2 ng/mL. The interassay CV (mean, 5.2 ng/mL) was 15%; the intraassay CV was 12%.
Statistical analyses
Comparisons between the control group and skydiving group were made by ANOVA with repeated measures using the Systat statistical package for the microcomputer (Systat, Evanston, IL) (18). For this purpose there were three time intervals for the comparison, as listed in the description of the control subjects’ participation. Multiple stepwise regression with the psychological trait as dependent variable and hormones/amylase at the time of landing as the independent variables was also carried out using Systat. The significances of both the between-treatment difference and the treatment by time interaction are reported.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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, as are the
results of the STAI, Subj, and SRE instruments. The level of anxiety
perceived at the beginning of the day was not significantly higher than
that of the subjects themselves on the control day or that of the
control subjects (data not shown) on either of the anxiety scales.
However, there were significant changes in the anxiety perceived by the
subjects as the time for the skydive drew near. Significant increases
in the MAACL-R anxiety scale and the STAI scales were recorded shortly
before the subjects entered the airplane (Table 1). Hostility and
depression were not significantly elevated on the MAACL-R at the
beginning of the day in skydivers, and no significant differences
occurred in these measures during the day. The Subj was elevated
relative to the control day and the early morning scores just before
entering the airplane. The SRE was the only psychological measure that
showed a significant increase in scores from the control day to the
0800 h assessment on the day of the skydive.
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and 2). The mean plasma cortisol value in skydivers
themselves on the control day (226 ± 18 nmol/L), 3–5 days before
the jump, was not different from that in the control group at the same
time of day. There was no anticipatory increase in cortisol; levels did
not increase significantly until the skydivers landed. Cortisol levels
in plasma and saliva then continued to rise over the next 15 min before
starting to fall. The interaction between treatment and time was
significant (P < 0.001).
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). However, amylase levels in the subjects
themselves on the control day (369 ± 44 U/mL) were similar to the
levels on the morning of the jump.
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). As with amylase levels, plasma PRL levels on the
morning of the jump were not lower than those on the control day
(7.3 ± 0.6 ng/mL) in subjects who volunteered to skydive, but
were slightly lower than those in the control group. Plasma PRL levels
in skydivers greatly exceeded preflight and control levels upon landing
(P < 0.01).
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). The mean level on the control day (2.0 ± 0.4)
was similar to that in the control group at the same time of day. There
was no significant interaction with time.
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). The mean value in skydivers on the control day
was 19.3 ± 1.3 nmol/L, slightly higher but similar to that in the
control group at the same time of day. It tended to be lower upon
entering the plane, but the ANOVA with repeated measures was not
significant. On the other hand, salivary testosterone concentrations
were significantly lower by ANOVA throughout the day (P
< 0.001), particularly at the time just before boarding the plane
(Fig. 7). The mean salivary testosterone value in
skydivers on the control day was higher (0.36 ± 0.03 nmol/L) than
the mean value in the control group at the same time of day. Thus, the
suppression may have been even greater than that between the control
group and the skydivers.
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). No significant interaction with the control group
occurred at the times when control samples were collected.
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). PRL was a significant component of the
regressions in each case, but in one case it was negative, and in the
others it was positive. The only other hormones that contributed
significantly to the regressions were testosterone and cortisol. The
relationships were not improved when the psychological state measures
were evaluated against the same hormonal variables.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The low levels of plasma cortisol in the morning before the jump were also unexpected. Previous studies (4, 5, 7) did not compare basal levels with prejump levels on the day of parachuting. Nevertheless, Levine et al. (5) have made the argument that when an individual is coping with stress, there is little or no elevation in plasma cortisol. For example, a situation has been described in which soldiers waiting for an enemy attack had lower than normal glucocorticoid production, whereas the responsible officers had high levels (20). Similarly, radio officers on planes involved in practice landings on aircraft carriers did not have elevated urinary glucocorticoids, but the pilots who were conducting the landings did, despite the fact that the radio officers were as much at risk as the pilots (11). In the present study it may be assumed that the subjects who volunteered to skydive were coping, at least until the actual event. The fact that they were jumping while attached to an experienced instructor relieved them of the responsibility for their own safety, much as the soldiers and radio officers were relieved. Nevertheless, experiencing the actual sensation of falling was evidently more than their coping mechanisms were prepared to handle. This is similar to the situation faced by patients waiting for surgery. In the study of Czeisler et al. (10), patients had no increase in plasma cortisol until the actual physical preparation for surgery was conducted. During surgical preparations, denial of the impending procedure may have been impossible, causing coping mechanisms to fail and plasma cortisol levels to increase greatly.
In the present study measurements of salivary cortisol reflected the plasma levels, as has been shown in previous studies (21, 22), suggesting that salivary measures can be satisfactorily substituted for plasma assays of cortisol.
PRL levels have been shown in some studies to be increased by anxiety. This has been shown to occur in students about to take an examination (23, 24), although there is not complete agreement on this (25). In the present study the high levels of anxiety expressed just before entering the airplane were associated with a subsequent surge in plasma PRL concentrations. It is clear in this study that anxiety preceded the rise in plasma PRL levels. Generally, plasma PRL levels paralleled those of cortisol, except that the PRL response to the jump was more rapid than that of cortisol. PRL had reached peak values by the time of landing or before, as shown previously (8), whereas cortisol had not yet reached a peak upon landing. The observation that the group who had volunteered to skydive had significantly higher levels of amylase 3–5 days before the day of the skydive is interesting and must be evaluated further. It cannot be determined whether these subjects had a higher than normal level persistently, or if the anticipation of the skydive produced an effect at the time when the control sample was taken.
Plasma GH was generally increased, but not uniformly among individuals, by the skydiving stressor. Shedlowski et al. (4) also examined the change in plasma GH from shortly before to immediately after parachuting and found no difference; Richter et al. (7) found a small, but significant, increase. In the study of Weitzman et al. (26) when the plasma GH level after parachuting was compared with that on a control day, a rather large increase was seen. Our data are consistent with these studies. The increase from immediately before the jump to immediately after was not significant, but when comparing the GH concentrations in control subjects with the levels after the jump, the increase was significant.
Plasma testosterone levels were not different from those in controls before the jump and were not greatly decreased at the time of landing. However, the difference in the salivary concentrations of testosterone in the same subjects was remarkable. The skydivers appeared to have a decrease in salivary testosterone as the time for boarding the airplane approached. After the jump, a fairly complex pattern appeared: a small rise upon landing when the other hormones were rising, and then a fall. Nevertheless, the precision of the pattern after landing cannot be established from a single study. The failure to find a significant decrease in plasma testosterone levels may reflect a change in the unbound fraction. This must be investigated further. However, the changes in concentration cannot be attributed to dilution effects, as the concentration of salivary cortisol, measured in the same specimens, did not change during the time when testosterone levels declined.
An anticipatory decline in salivary testosterone has not been reported previously to our knowledge, although many studies have shown that testosterone declines after a stressful event. Ghanadian et al. (6), measuring testosterone before and after surgery in men, found that by comparison with levels 2 days before surgery, the lowest levels were found 2 days after surgery (70% decrease); complete recovery required a month. Shorter intervals were not studied. In addition, in a study of acute responses to exercise, plasma testosterone was found to be increased immediately after an exercise regimen; 2 h later there was a significant decrease, which persisted for more than 8 h (27). The results of the latter study appear to be similar to those we observed after the subjects had landed. Nevertheless, the prejump suppression that was evident from the salivary testosterone measurements demonstrates a purely psychological cause of the decrease in testosterone.
Although not conclusive because of the sampling frequency, the finding that plasma LH was elevated after the skydive suggests that the cause of the suppression of testosterone secretion was not the result of a decrease in gonadotropin stimulation, but may be the result of a direct action on the testis.
As administration of cortisol has been shown to suppress plasma testosterone levels in men (28), it may be presumed that cortisol is responsible for the decline in testosterone in the present study. However, this cannot be the explanation, because the decrease in testosterone occurred during the time when plasma cortisol levels were suppressed. The mechanism by which a psychological stressor inhibits testosterone secretion in man is an interesting observation that should be investigated further.
In an attempt to determine whether there is an association between personality traits and hormone responses, a stepwise multiple regression was performed. Highly significant relationships were found for the STAI, the SSS, and the SRE measured 3–5 days before the skydive and hormones measured immediately after the skydive. For the latter scale, 44% of the variability could be attributed to salivary testosterone and plasma PRL. Inclusion of other hormonal variables or amylase did not increase the closeness of this relationship. Surprisingly, measures of the psychological state on the day of skydiving could not be predicted with greater precision from concurrent hormone levels than could the psychological trait scores. The precise relationships cannot be determined with confidence from a single study of this magnitude, but this may be a fruitful avenue of future investigation.
In summary, as indicated by the low levels of cortisol and the low reported levels of anxiety on standardized psychological instruments, the subjects were coping with the situation early on the morning of the jump. However, within minutes before entering the airplane, it is apparent that personal defenses broke down, anxiety and subjective stress levels rose, and the low to normal levels of cortisol, amylase, PRL, and GH increased rapidly to very high levels. We conclude that the process of coping with anxiety and fear in this situation is characterized in men by specific hormone patterns, particularly elevated catecholamines and suppressed levels of cortisol and testosterone.
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Footnotes |
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Received February 28, 1997.
Revised April 15, 1997.
Accepted April 23, 1997.
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References |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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-amylase as a measure of endogenous
adrenergic activity. Clin Physiol. 16:433–448.[Medline]
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