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Transcript of Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A., Hucklebridge, F., & Der, G. (2006)....
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
Stressful Life Events Are Associated with Low Secretion Rates
of Immunoglobulin A in Saliva in the Middle-Aged and Elderly
Anna C. Phillips1, Douglas Carroll1, Phil Evans2, Jos A. Bosch1,
Angela Clow2, Frank Hucklebridge2, and Geoff Der3
1School of Sport and Exercise Sciences, University of
Birmingham, Birmingham, England2Psychophysiology and Stress Research Group, University of
Westminster, London, England3MRC Social and Public Health Sciences Unit, University of
Glasgow, Glasgow, Scotland
Correspondence: Anna C. Phillips, MSc, School of Sport and
Exercise Sciences, University of Birmingham, Birmingham,
England. Tel 00 44 121 414 7240; Fax 00 44 121 414 4121;
email [email protected]
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
Abstract
Whether chronic stress experience is related to down-
regulation of secretory immunoglobulin A (S-IgA) was tested in
two substantial cohorts, one middle-aged (N = 640) and one
elderly (N = 582), comprising similar numbers of men (N = 556)
and women (N = 666) and manual (N = 606) and non-manual (N =
602) workers. Participants indicated from a list of major
stressful life events up to six they had experienced in the
previous two years. They also rated how disruptive and
stressful the events were, at the time and now, as well as
their perceived seriousness; the products of these impact
values and event frequency were adopted as measures of stress
load. From unstimulated 2-minute saliva samples, saliva
volume and S-IgA concentration were measured, and S-IgA
secretion rate determined as their product. There was a
negative association between the stress load measures and S-
IgA secretion rate, still evident following adjustment for
such variables as smoking and saliva volume. The associations
also withstood adjustment for sex, cohort, and household
occupational status. Although these associations are small in
terms of the amount of variance explained, they nonetheless
suggest that chronic stress experience either decreases IgA
production by the local plasma cells or reduces the efficiency
with which S-IgA is transported from the glandular
interstitium into saliva. Given the importance of S-IgA in
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
immune defence at mucosal surfaces and the frequency with
which infections are initiated at these surfaces, S-IgA down-
regulation could be a means by which chronic stress increases
susceptibility to upper respiratory tract infection.
Keywords: Life events stress; secretory immunoglobulin A;
saliva volume; smoking; age; sex; household occupational
status.
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
1. Introduction
There is now convincing evidence linking measures of
chronic psychological stress, most noticeably the experience
of stressful life events, to upper respiratory tract infection
and disease (see, e.g., Cohen, Tyrell & Smith, 1991; 1993).
Up to 95% of all infections are initiated at the mucosal
surfaces (Bosch, Ring, de Geus, Veerman & Amerongen, 2002).
These surfaces are protected by the secretion of various
proteins from the exocrine glands, including the salivary
glands. Prominent among such secretory proteins are
immunoglobulins, the most predominant of which is secretory
immunoglobulin A (S-IgA) (Hood, Weissman & Wood, 1978).
Accordingly, S-IgA may be an important mediator in the link
between chronic stress and upper respiratory tract infection.
There is now fairly convincing evidence that acute
psychological stress whether naturalistic or contrived in the
laboratory is associated with increases in S-IgA concentration
and/or secretion rate (e.g., (Bosch, de Geus, Kelder, Veerman,
Hoogstraten & Amerongen, 2001; Carroll, Ring, Shrimpton,
Evans, Willemsen & Hucklebridge, 1996; Kugler, Reintjes, Tewes
& Schedlowski, 1996; Ring, Drayson, Walkey, Dale & Carroll,
2002; Willemsen, Ring, Carroll, Evans, Clow & Hucklebridge,
1998; Willemsen, Ring, McKeever & Carroll, 2000; Zeier,
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
Brauchli & Joller-Jemelka, 1996). Further, the inconsistent
findings from the numerous studies of examination stress
become well reconciled to the model above when the distinction
is drawn on temporal grounds between test or examination
stress - the acute stress of an imminent or ongoing
examination, and academic stress - more chronic exposure to an
extended examination period (Bosch, de Geus, Ring, Nieuw
Amerongen & Stowell, 2004; Bosch et al., 2002). All six
studies of the former report increases in S-IgA concentration
or secretion rate (Bosch, Brand, Ligtenberg, Bermond,
Hoogstraten & Nieuw Amerongen, 1998; Bristow, Hucklebridge,
Clow & Evans, 1997; Evans, Bristow, Hucklebridge, Clow & Pang,
1994; Huwe, Hennig & Netter, 1998; McClelland, Ross & Patel,
1985; Spangler, 1997). In sharp contrast, of the seven
studies that have investigated the latter, five (Deinzer and
Schuller, 1998; Jemmott, Borysenko, Borysenko, McClelland,
Chapman, Meyer & Benson, 1983; Jemmott and Magloire, 1988; Li,
Ziu, Qian & Tang, 1997; Mouton, Fillion, Tawadros & Tessier,
1989) have found decreases in S-IgA.
Academic stress aside, the rest of the evidence
linking chronic stress and S-IgA down regulation is less than
compelling. Most of the studies have examined minor events or
daily hassles in small samples of students or female nurses.
Of the six studies that have been published to date, only
three report negative associations between hassle frequency or
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
change in frequency and S-IgA concentration or secretion rate.
The problems with these studies have been enumerated elsewhere
(Bosch et al., 2002). Aside from modest sample size, some
have used instruments for measuring stress that have little
psychometric pedigree and all failed to control for health
behaviours, particularly smoking, now known to be related to
both S-IgA (Evans, Der, Ford, Hucklebridge, Hunt & Lambert,
2000) and chronic stress (Heslop, Davey Smith, Carroll,
Macleod, Hyland & Hart, 2001). Thus, although the balance of
evidence tends to favour the hypothesis that chronic stress
exposures down-regulate S-IgA, numerous methodological
problems counsel caution.
Data from the West of Scotland Twenty-07 Study
on a large adult community sample, in which both S-IgA ((Evans
et al., 2000) and major life events were measured, permitted a
more convincing test of the hypothesis that chronic stress
experience is related to down-regulation of S-IgA. In
addition, any putative associations between stress and S-IgA
could be adjusted for smoking, as well as for age, sex, and
household occupational status.
2. Method
2.1. Participants
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
Data are derived from the middle and eldest of the three
age cohorts of the West of Scotland Twenty-07 Study.
Individuals were all from the Glasgow area and have been
followed up at regular intervals since the baseline survey in
1987 (Ford, Ecob, Hunt, Macintyre & West, 1994). Members of
the middle cohort were all around 44 years old and members of
the older cohort were all around 63 years old at the third
follow-up when data on life events were collected and a saliva
sample taken. The optimum sample size was 1477. However,
missing data and improperly collected saliva reduced the
sample with full data to 1222, comprising 640 from the middle
cohort and 582 from the eldest cohort. The mean age of the
middle cohort was 44.6 (SD = 0.84) years and 63.6 (SD = 0.61)
years for the eldest cohort. Overall, there were 556 (45%)
men and 666 (55%) women, and 606 (50%) of the participants
came from manual and 602 (50%) from non-manual occupational
households. The sex ratios for the two cohorts were virtually
identical: 285 (45%) men and 355 (55%) women for the middle
cohort and 271 (47%) men and 311 (53%) women for the older
cohort. However, the distribution of participants from
manual and non-manual occupational households differed
significantly between cohorts (χ2 (1) = 21.81, p < 001); in the
middle cohort, 275 (44%) came from manual and 354 (56%) from
non-manual occupational households, whereas for the elder
cohort the figures were 331 (43%) and 248 (57%), respectively.
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
2.2 Apparatus and procedure
Participants were tested in a quiet room in their own
homes by trained nurses. Demographic information was obtained
by interview. Household socioeconomic position was classified
as manual and non-manual from the occupational status of the
head of household, using the Registrar General’s (1980)
classification system of occupations. Head of household was
either the participant or his/her partner, depending on which
of the two held or had held the highest status occupation.
Major life events over the past two years and their
initial and current impact were assessed by presenting
participants with eight cards each of which listed a number of
major life events in one particular domain. The domains were
as follows: health (e.g. serious illness diagnosed), marriage
(e.g. living apart or divorce), relationships (e.g. serious
disagreement within family), deaths (e.g. spouse died), work
(e.g. unemployment), housing (e.g. problem with landlord),
finance (e.g. problems paying bills), and general (e.g.
burglary or theft). Participants were asked to indicate up to
six events which had happened either to them or to someone
they cared about. The present analyses focussed on those
events that had happened directly to the participant.
Following identification of the events, participants were
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
asked to specify, for each event, how much the event disrupted
or changed their life and how stressful it was at the time of
occurrence, as well as how disruptive and stressful it was
now. All of these responses were scored on a 5-point scale,
where 1 = a very great deal and 5 = not at all; for the
analyses, the values were reversed so that the greater the
impact the higher the score. In addition, participants were
asked for each event to indicate how serious the event was on
a 10-point scale, where 1 = ‘something really small and
unimportant’ and 10 = ‘the worst thing that could happen to
you’. The present assessment method is based on the well-
established Life Events and Difficulties Schedule (Brown and
Harris, 1989) and included the same domains of personal
experience. As concern lay with the overall stress load on
participants, four measures were derived from the sums of the
product of each life event experienced and its disruptiveness
and stressfulness, both at the time of its occurrence and now.
In addition, a similar measure was derived from the number of
events times their rated seriousness.
Smoking behaviour was determined by responses to the
question, ‘Do you ever smoke tobacco now? I am thinking of a
pipe, cigars and your own roll ups as well as cigarettes you
might buy.’ If the answer was ‘No’, participants were asked,
‘Did you ever used to smoke any kind of tobacco?’ On this
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
basis, participants were characterised as ‘never smokers’, ex
smokers’, or ‘current smokers’.
Saliva samples were taken at the end of the interview,
using standard salivettes (Sarstedt Ltd, Leicester, UK).
Participants were instructed to swallow hard to dry out the
mouth and then immediately to place the swab under the tongue.
They were asked to hold the swab as still as possible for 2
minutes, timed precisely by the nurse interviewers using
portable digital timers. After exactly 2 minutes,
participants removed the swab, returning it to the salivette
case. It should be conceded that the use of absorbent cotton
materials to collect saliva has been observed to produce lower
S-IgA concentrations (Shirtcliff, Granger, Schwartz & Curran,
2001); however, it is reasonable to consider that any such
reduction would be a constant error. All samples were frozen
within 2 hours of collection and remained frozen at -20
degrees C until assay. Samples were dispatched from Glasgow
to London by air for assay in four batches and recovered after
thawing by centrifugation at 1000g for 10 minutes. Double
antibody sandwich ELISA, described in detail elsewhere
(Carroll et al., 1996), was used to determine S-IgA
concentration. Intra-assay % coefficient of variation was 3.8
and inter-assay % coefficient of variation was 7.6. Prior to
assay, saliva volume was determined gravimetrically. Saliva
sample collection and volume determination for S-IgA analysis
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
conformed to a procedure described previously (Zeier et al.,
1996). The focus of analysis was S-IgA secretion rates
(μg/2min), which were calculated as the product of saliva
volume (ml) and S-IgA concentration (μg/ml). Given the
distribution of S-IgA secretion rate values in this sample
(Evans et al., 2000), a natural log transformation was applied
prior to statistical analyses.
2.3 Data analyses
Analysis was undertaken using SPSS version 12.
ANOVA was used to compare life events scores between cohorts,
sexes, household occupational groups, and smoking status
groups. Eta-squared (η2) was derived as the ratio of the
independent variable sums of squares and the total sums of
squares, and used as an indicator of effect size. Similar
analyses were applied to the log n transformed S-IgA secretion
rate values. To test the main hypothesis, linear regression
was conducted, with log n transformed S-IgA secretion rate
values as the dependent variable. Initially, simple linear
regression was used to establish whether there were
indications of an association between stressful life events
exposure and secretion rate. In subsequent hierarchical
regression analyses, assay batch, saliva volume, and smoking
behaviour were entered at step 1. Since the batch variable
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
reflected inter-assay variation, it could be a potential
confounder. Adjustment for saliva volume would help establish
whether any associations between S-IgA secretion rates and
stressful life events exposure were driven by variations in
saliva volume or reflected a link with actual variations in S-
IgA production and/or transport (Willemsen et al., 1998). The
importance of controlling for smoking behaviour when examining
possible relationships between psychosocial variables and S-
IgA has already been demonstrated (Evans et al., 2000). In
these analyses, the life events measures were entered at step
2. In subsequent analyses, batch, smoking, and saliva volume
were again entered at step 1, with possible moderating
variables, sex, age cohort, and household occupational status,
entered at step 2, and the life events variables being
relegated to step 3. The main results of these regressions
are presented in Tables.
3. Results
3.1 Life Events
The median number of major stressful life events
happening to the participants over the last two years was 1
(interquartile range = 2). Although very few events were
experienced, they were clearly regarded as serious; the
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
average seriousness score was 7.12 (SD = 9.21) on a scale of
1-10. With regard to the stress load, the mean total
disruption scores at the time of the event and now were 3.65
(SD = 4.85) and 2.52 (SD = 3.61) respectively, and the mean
total stressfulness scores then and now were 4.10 (SD = 5.22)
and 2.53 (SD = 3.62).
The middle cohort identified more stressful life
events than the elder cohort, F (1,1220) = 8.81, p = .003, η2 =
.007, and their total stress load at the time of exposure was
higher, in terms of disruption, F (1,1220) = 7.79, p = .005, η2
= .006, stress, F (1,1220) = 8.75, p = .003, η2 = .007, and
seriousness, F (1,1220) = 4.89, p = .03, η2 = .004. Men and
women did not differ in the number of events exposed to or in
terms of the total contemporary and present stress load
arising from such exposures, nor did manual and non-manual
occupational household groups. The summary data are
presented in Table 1.
There were 420 (34%) current smokers in the sample,
330 (27%) ex smokers, and 472 (39%) never smokers. The life
events data for smokers, ex smokers, and never smokers are
presented in Table 2. Smokers had been exposed to more life
events than current non smokers, F (2,1219) = 5.21, p = .006,
η2 = .008, rated them as more serious, F (2,1219) = 7.73, p
< .001, η2 = .013, , experienced more disruption then, F
(2,1219) = 5.99, p = .003, η2 = .010, and now, F (2,1219) =
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
5.24, p = .005, η2 = .009, and experienced more stress at the
time, F (2,1219) = 5.78, p = .003, η2 = .009, and now, F
(2,1219) = 3.40, p = .03, η2 = .006.
3.2 Secretory Immunoglobulin A
Logn S-IgA secretion rates were significantly higher in
the middle than the older cohort, F (1,1220) = 12.04, p = .001,
η2 = .010; this would appear to be driven largely by cohort
differences in saliva volume, F (1,1220) = 23.82, p < .001, η2
= .019. Men had higher logn S-IgA secretion rates than women,
F (1,1220) = 18.45, p < .001, η2 = .015, again with
significantly higher saliva volumes, F (1,1220) = 6.27, p
= .01, η2 = .005. Non-manual occupational household groups had
higher secretion rates than manual occupational household
groups, F (1,1206) = 5.38, p = .02, η2 = .004, which again
appeared to be driven by differences in saliva volume, F
(1,1206) = 6.21, p = .01, η2 = .005. The summary data are
presented in Table 3. Finally, logn S-IgA secretion rates were
attenuated, F (2,1219) = 8.73, p < .001, η2 = .014, in current
smokers (M = 3.32, SD = 1.70) compared to ex smokers (M =
3.61, SD = 1.55) and never smokers (M = 3.62, SD = 1.46), and
assay batch also affected logn S-IgA secretion rate, F (3,1218)
= 10.81, p <.001, η2 = .026, with higher values being recorded
for the earlier batches. Finally, as would be expected, logn
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
S-IgA secretion rate and logn S-IgA concentration, r(1220)
= .66, p < .001, and logn S-IgA secretion rate and saliva
volume, r(1220) = .68, p < .001, were strongly correlated. The
positive correlation between logn S-IgA concentration and
saliva volume was more modest, but still statistically
significant, r(1220) = .07, p = .01.
[Insert Tables 1, 2, and 3 about here]
3.3 Life events and Secretory Immunoglobulin A Secretion Rate
Simple linear regression revealed statistically
significant negative associations between the five stressful
life events variables and log n S-IgA secretion rate: for
disruption then, β = -.06, t = 1.99, p = .05, R2 = .003; stress
then, β = -.06, t = 2.24, p = .03, R2 = .004; disruption now, β =
-.06, t = 2.17, p = .03, R2 = .004; stress now, β = -.06, t =
2.14, p = .03, R2 = .004; and seriousness, β = -.07, t = 2.30, p
= .02, R2 = .004.
In multiple hierarchical regressions models in
which assay batch, saliva volume, and smoking was entered at
step 1 and the life events variables at step 2, the negative
associations between stressful life events experience and S-
IgA secretion rate were attenuated, but all bar one remained
statistically significant. As might be expected from the
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
analyses above, the step 1 variables were all significantly
associated with log n S-IgA secretion rate: for batch, β =
-.14, t = 6.78, p < .001; for saliva volume, β = .67, t =
32.87, p < .001; for smoking β = -.09, t = 4.13, p <.001. The
step 1 model, incorporating all three variables accounted for
almost half the variance in log n S-IgA secretion rate, ΔR2
= .487. The associations between log n S-IgA secretion rate
and the life events variables emerging at step 2 in these
models are summarised in Table 4. Although for the most part,
remaining statistically significant, it is important to note
that the residual associations like the original bivariate
associations are small in terms of the amount of variance they
explain. In the next set of multiple hierarchical regression
models, batch, saliva volume and smoking were entered at step
1. In these models, though, the major demographic variables,
age cohort, sex, and household occupational status, were
entered at step 2, with the life events variables entered at
step 3. Only sex emerged from step 2 entry as a significant
predictor of log n S-IgA secretion rate, β = -.10, t = 3.70, p
< .001. The full step 2 model accounted for around %1, ΔR2
= .012, of additional variance in log n S-IgA secretion rate.
The associations between log n S-IgA secretion rate and the
life events variables emerging at step 3 in these models are
also summarised in Table 4; the associations are virtually
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
unchanged from those that emerged from the previous two-step
hierarchical models.
[Insert Table 4 about here]
4. Discussion
The present analyses testify to a negative association
between the experience of stressful life events and S-IgA
secretion rate. As such, they support the contention (Bosch
et al., 2002) that in contrast to the S-IgA enhancing effects
of acute psychological stress (Bosch et al., 2001; Carroll et
al., 1996; Kugler et al., 1996; Ring et al., 2002; Willemsen
et al., 1998; Willemsen et al., 2000; Zeier et al., 1996),
chronic stress might effect a down-regulation of S-IgA. Aside
from the evidence from the specific chronic exposure of
academic stress (Bosch et al., 2002), support for down-
regulation has largely relied on studies reporting a negative
relationship between S-IgA and university students’ experience
of daily hassles and fairly minor irritants (Evans, Bristow,
Hucklebridge, Clow & Walters, 1993; Farne, Boni, Corallo,
Gnugnoli & Sacco, 1992; Martin and Dobbin, 1988). To our
knowledge, the present study is the first to show that the
experience of serious and major life events over a protracted
period in substantial cohorts of middle aged and elderly men
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
and women is negatively related to S-IgA secretion rates. In
addition, it is clear from these analyses that these
associations embrace impact both currently and at the time of
exposure.
The importance of controlling for smoking
behaviour in this context has been emphasised elsewhere (Bosch
et al., 2002; Evans et al., 2000). In the present sample,
current smokers had lower S-IgA secretion rates than ex
smokers and never smokers. Smoking would also in turn seem to
vary with variations in psychological stress (Heslop et al.,
2001). In the present study, smokers had higher life events
scores than non smokers. Thus any relationship between
chronic stress and S-IgA may be confounded by variations in
smoking behaviour. However, the negative associations between
our life events measures and S-IgA largely withstood
adjustment for smoking, as well as for assay batch and saliva
volume. That assay batch has a substantial effect on S-IgA
secretion rate has been reported in prior aggregate analyses
of all three cohorts from this study (Evans et al., 2000).
The current analyses confirm the importance of controlling for
inter-assay variability in large scale epidemiological studies
of immune parameters.
By statistical adjustment we were able to establish
that the observed relationships between life events and S-IgA
secretion rate were not, for the most part, driven by
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
variations in saliva volume. This is important because it
permits us to eliminate one fairly parsimonious but less
interesting explanation that for those participants with a
high stress load the glands simply release less saliva into
mouth. The earlier analyses of all three cohorts from this
study indicated that the positive association between S-IgA
secretion rates and household occupational status were
essentially the result of lower salivary flow in the lower
household occupational status groups (Evans et al., 2000).
That this was not the case in the present analyses indicates
that life events stress either decreases IgA production by the
local plasma cells or reduces the efficiency with which S-IgA
is transported from the glandular interstitium into saliva.
The value of measuring total S-IgA levels, as opposed to
antigen-specific S-IgA, has been the subject of considerable
debate (Jemmott and McClelland, 1989; Stone, Cox,
Valdimarsdottir, Jandorf & Neale, 1987). This debate stems
from the common misconception that S-IgA is a measure of
adaptive immune responses, i.e., responses that are driven by
exposure to a previously encountered antigen. If this were
indeed the case then only the levels of S-IgA molecules that
are specifically directed against particular antigens would
matter for host protection rendering the measurement of total
S-IgA levels less meaningful. However, total S-IgA consists,
for the most part, of so-called ‘natural antibodies’ (Bos,
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
Cebra & Kroese, 2000). These natural antibodies have a
broader specificity to recognize many different types of
antigen, and their levels are independent of re-exposure to
specific antigens (Stoel, Jiang, van Diemen, Bun, Dammers,
Thurnheer, Kroese, Cebra & Bos, 2005). Hence, total
immunoglobulin levels are the key to monitoring this aspect of
immunity. This perspective is consistent with evidence
showing that total S-IgA levels are predictive of
susceptibility to respiratory, oral, and aural infections
(Evans, Hucklebridge, Clow & Doyle, 1995; Jemmott and
McClelland, 1989; Kuby, 1997). Thus, measuring total S-IgA
levels is an immunologically meaningful measure of mucosal
host resistance.
The present study suffers from a number of limitations.
First, although the present life events scale has a sound
pedigree and a paper using it has been published elsewhere
(Carroll, Phillips, Ring, Der & Hunt, 2005), the manner of its
administration could have imposed an arbitrary cap on the
total stress load scores derived. Participants were permitted
to select up to six life events only, rather than being free
to nominate as many events as had occurred. However,
participants on average selected only a small number of events
and only nine (1%) reported having experienced six events,
whereas 1061 (87%) reported between zero and two events, which
strongly suggests that the methodology was not unduly
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constraining. Second, only one measure of S-IgA was taken, a
concern given circadian variation (Hucklebridge, Clow & Evans,
1998). However, in a large cohort study, more comprehensive
monitoring was not practicable. Further, S-IgA would appear
to reasonably stable from around three hours after wakening
(Hucklebridge et al., 1998), and early morning testing was
rare. In addition, individual differences in S-IgA has been
found to show good test-retest reliability across two to four
days (Ring et al., 2002), one to two weeks (Bosch et al.,
2001), and four weeks (Willemsen et al., 1998). Third, it
should be conceded that the associations that emerged from the
present analyses are small in terms of the amount of variance
explained. However, they are consistent and remain
significant in four out of five cases following adjustment for
assay batch, saliva volume, and smoking that account for
around half the variance in S-IgA secretion rate. Further,
they are of the same order of magnitude as the effect sizes
reported in a recent meta-analysis of life events and
immunoglobulins (Segerstrom and Miller, 2004); it would appear
that samples of the current size are needed for such
associations to achieve statistical significance.
Nevertheless, their size does raise the question as to whether
associations of this magnitude are of idiopathic clinical
significance.
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
. In conclusion, the experience of major life events
both at the time and now was negatively associated with S-IgA
secretion rate. This association would not appear to be
driven by variations in saliva volume. As such, a high life
stress load would seem to compromise either production or
transport. Given the prominent role of S-IgA in immune
defence at mucosal surfaces and the frequency with which
infections are initiated at these surfaces, it is plausible
that S-IgA affords a pathway by which chronic stress increases
susceptibility to upper respiratory tract infection.
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Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
Table 1
Life Events Descriptive Statistics by Age Cohort, Sex and
Household Occupational Status
Middle Eldest Men Women Manual
Non-
manual
Mean
(SD)
Mean
(SD)
Mean
(SD)
Mean
(SD)
Mean
(SD)
Mean
(SD)
Number of
events
1.16
(1.37)
0.95
(1.15)*
1.07
(1.27)
1.05
(1.28)
1.04
(1.23)
1.08
(1.31)Disruption
then
4.02
(5.22)
3.25
(4.37)*
3.59
(4.75)
3.71
(4.93)
3.55
(4.61)
3.72
(5.03)Stressful
then
4.52
(5.61)
3.64
(4.71)*
3.94
(4.96)
4.24
(5.42)
4.02
(5.10)
4.16
(5.29)Disruption
now
2.67
(3.71)
2.35
(3.50)
2.52
(3.68)
2.51
(3.56)
2.52
(3.63)
2.49
(3.58)Stressful
now
2.70
(3.66)
2.34
(3.56)
2.47
(3.59)
2.59
(3.64)
2.55
(3.70)
2.49
(3.49)Seriousness 7.68
(9.82)
6.51
(8.45)*
6.91
(8.92)
7.29
(9.45)
7.06
(8.89)
7.11
(9.40)
* p < .05
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Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
Table 2
Life Events Scores according to Smoking Status
Current
Smoker Ex Smoker Never Smoker
Mean (SD) Mean (SD) Mean (SD)
Number of
events1.22 (1.34) 0.98 (1.21)
0.97 (1.24)
Disruption
then4.31 (5.11) 3.30 (4.66)
3.31 (4.68)
Stressful
then4.80 (5.52) 3.74 (5.05)
3.74 (4.99)
Disruption
now 2.97 (3.88) 2.22 (3.17)
2.31 (3.63)
Stressful now 2.90 (3.78) 2.28 (3.28) 2.38 (3.67)Seriousness 8.54
(10.04)6.43 (8.63)
6.34 (8.68)
Post-print, not final published version. Cite this article as:Phillips, A.C., Carroll, D., Evans, P., Bosch, J.A., Clow, A.,Hucklebridge, F., & Der, G. (2006). Stressful life events areassociated with low secretion rates of immunoglobulin A in saliva in the middle-aged and elderly, Brain, Behavior and Immunity, 20, 191-197.* http://dx.doi.org/10.1016/j.bbi.2005.06.006 IF 4.91
Table 3
Salivary Descriptive Statistics by Age Cohort, Sex and
Household Occupational Status
Middle Eldest Men Women Manual
Non-
manual
Mean
(SD)
Mean
(SD)
Mean
(SD)
Mean
(SD)
Mean
(SD)
Mean
(SD)
Saliva volume
(ml)
0.74
(0.59)
0.58
(0.52)*
0.71
(0.57)
0.63
(0.55)*
0.62
(0.55)
0.70
(0.57)*
S-IgA secretion rate (μg/2min)
102(384)
84 (162) 100(163)
88 (377) 83 (148) 105(399)
log n S-IgA secretion rate
3.63(1.49)
3.32(1.66)*
3.70(1.53)
3.31(1.60)*
3.38(1.63)
3.59(1.53)*
* p < .05
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Table 4
Associations between Secretory Immunoglobulin A Secretion Rate
and Life Experience following Adjustment for Potential
Confounding Variables
.
Step β t ΔR2
Step 1: Assay Batch,
Saliva Volume, and SmokingStep 2: Disruption
then
-.04 2.10* .002
Stressful
then
-.04 1.99* .002
Disruption
now
-.04 2.04* .002
Stressful
now
-.04 1.76# .001
Seriousness -.04 2.02* .002
Step 2: Age Cohort, Sex,
and Household Occupational
StatusStep 3: Disruption
then
-.05 2.21* .002
Stressful -.04 2.03* .002
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thenDisruption
now
-.05 2.17* .002
Stressful
now
-.04 1.84# .001
Seriousness -.04 2.08* .002
* p < .05# p < .08