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We examined the relation of academic stress and social support to salivary concentrations of secre-
tory immunoglobulin A (S-IgA), an antibody class that plays an important role in mucosal defense
against acute upper respiratory tract infections. We assayed whole, unstimulated saliva samples col-
lected from 15 healthy undergraduates 5 days before their final exam period, during their exam
period, and 14 days after their last final exam for S-IgA concentrations by single radial immuno-
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
diffusion. The students rated the university's general psychological climate as being more stressful
This document is copyrighted by the American Psychological Association or one of its allied publishers.
during the exam period compared with the two other periods. Paralleling this, their salivary concen-
trations of S-IgA were lower during the exam period. Students who reported more adequate social
support at the preexam period had consistently higher S-IgA levels than did their peers reporting
less adequate social support. This latter finding is consonant with the social support direct effects
hypothesis, which states that social support enhances health outcomes irrespective of whether the
individual is exposed to stressful experiences.
That stressful circumstances may heighten vulnerability to 1982). Most infectious agents enter the body through mucosal
infection is suggested by several studies (e.g., Friedman & Glas- surfaces, and the presence of S-IgA antibodies in the secretions
gow, 1966; Kasl, Evans, & Neiderman, 1979; McClelland, Alex- that bathe these surfaces provides a first line of defense against
ander, & Marks, 1982; McClelland, Floor, Davidson, & Saron, infections, particularly those of the upper respiratory, gastroin-
1980; Meyer & Haggerty, 1962; Plaut & Friedman, 1981). In an testinal, and urino-genital systems. Considerable evidence indi-
effort to understand this connection between stress and infec- cates that S-IgA antibodies interfere with bacterial and viral ad-
tion, researchers in the emerging field of psychoneuroimmunol- herence to mucosal surfaces and consequently limit coloniza-
ogy(Ader, 1981; Jemmott, 1985)have begun to study immuno- tion of these surfaces by pathogens. Should this local mucosal
logic functioning in relation to stress. The immune system is immunologic defense be overcome, resistance would depend on
the body's chief mechanism of defense against diseases (Hood, systemic immune mechanisms, including serum antibody, par-
Weissman, & Wood, 1978; Mims, 1982). The basic hypothesis ticularly immunoglobulin M and immunoglobulin G (Mc-
is that if stress increases susceptibility to infection, it may do so Ghee, Mestecky, & Babb, 1978; Mims, 1982; Tomasi, 1976; To-
at least in part by impairing features of immunologic defense. masi & Grey, 1972; Waldman & Ganguly, 1974; Williams &
Although the literature is small and contains exceptions to Gibbons, 1972).
the general trend, evidence suggests that stress may alter aspects
of immunologic functioning (Borysenko & Borysenko, 1982;
Measuring Salivary Secretory Immunoglobulin A
Jemmott & Locke, 1984;Monjan, 1981;Palmblad, 1981; Rog-
ers, Dubey, & Reich, 1979). Studies on humans have tied stress
Several studies have assayed S-IgA levels in whole saliva as an
to reduced natural killer cell activity (e.g., Kiecolt-Glaser, Gar-
index of mucosal immune functioning. Although Stone, Cox,
ner, et al., 1984; Locke et al., 1984). Others have linked it to Valdimarsdottir, Jandorf, and Neale (1987) have argued that
decreased lymphocyte proliferation responses to specific viral there are difficulties with this approach, close examination of
antigens (Kiecolt-Glaser, Speicher, Holliday, & Glaser, 1984) or the issue suggests that their concerns are overstated (Jemmott,
to nonspecific B- or T-lymphocyte mitogens (Bartrop, Lock- 1987; Jemmott & McClelland, 1988). Specifically, Stone et al.
hurst, Lazarus, Kiloh, & Penny, 1977; Dorian, Keystone, Gar- (1987) cited Brandtzaeg's (1971) finding of an inverse relation
finkel, & Brown, 1982; Schleifer, Keller, Camerino, Thortyon, between salivary flow and S-IgA concentration as evidence that
& Stein, 1983). Still others have tied stress to lower levels of measurement of salivary S-IgA is problematic. An obvious so-
secretory immunoglobulin A (Jemmott et al., 1983; McClel- lution to this problem is to take salivary flow into account when
land et al., 1982; McClelland et al., 1980). This latter immuno- measuring S-IgA levels. For instance, one might assess the S-
logic parameter is of particular interest in this article. IgA secretion rate (e.g., Jemmott et al., 1983)—the amount of
S-IgA per unit time—as suggested by Brandtzaeg, Fjellanger,
Secretory Immunoglobulin A
and Gjeruldsen (1970) and Tomasi (1976) in their careful con-
Secretory immunoglobulin A (S-IgA) is the predominant an- sideration of this issue. One might also assess S-IgA concentra-
tibody class in bodily secretions (Hood et al., 1978; Mims, tions partialing out effects of salivary flow (e.g., McClelland &
Kirschnit, 1988). Stone et al. also asserted that proteases in the
Correspondence concerning this article should be addressed to John mouth break down S-IgA and could bias immune measure-
B. Jemmott HI, Department of Psychology, Green Hall, Princeton Uni- ments when whole saliva (i.e., taken directly from the mouth)
versity, Princeton, New Jersey 08544. is used. The trouble with this assertion is that Stone et al. did
803
804 JOHN B. JEMMOTT lit AND KIM MAGLOIRE
not specify the nature or magnitude of the putative bias or cite stress and S-IgA levels within a substantially shorter time inter-
evidence documenting it and that the significance, if any, of val than was used in the Jemmott et al. (1983) study.
these proteases in resistance to infection is unknown (Kornfeld
& Plaut, 1981). Moreover, the measurement of S-IgA concen-
Social Support
tration in whole saliva is highly reproducible and stable over
time, as data from this study documents. A third comment by The second issue of concern is whether people who have more
Stone et al. is that total S-IgA concentration is not correlated adequate social support have higher S-IgA levels than do other
with disease incidence. However, recent narrative (Jemmott, people. Considerable research suggests that social support is re-
1987) and meta-analytic reviews (Jemmott & McClelland, lated to positive health outcomes (Cobb, 1976; S. Cohen &
1988) indicate that total S-IgA levels of healthy individuals are Wills, 1985; House, 1981; Wortman, 1984). Two models of the
related to susceptibility to infection. One carefully controlled effects of social support have been posited: The buffering
experiment reported that men who had higher concentrations model, which holds that social support has beneficial effects on
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
of total S-IgA in their secretions prior to inoculation with a live health only or chiefly when individuals are exposed to stress,
This document is copyrighted by the American Psychological Association or one of its allied publishers.
influenza virus showed a more rapid rise in antibodies specific and the main or direct effects model, which holds that social
to the virus and a lower incidence of the signs and symptoms of support is salubrious irrespective of whether individuals are ex-
upper respiratory tract infection following inoculation, com- posed to stress. Studies can be marshalled to corroborate both
pared with their counterparts who had relatively lower S-IgA models. However, most of them bear on the relation of social
concentrations (e.g., Rossen et al., 1970). Finally, Stone et al. support to mental health; hence, research on the relation of so-
proposed an alternative measure of S-IgA: the ratio of a specific cial support to susceptibility to infection and physical disease
S-IgA antibody (i.e., rabbit albumin S-IgA antibody) to the con- is greatly needed (S. Cohen & Wills, 1985).
centration of total S-IgA. The trouble with this measure is that That social support may relate to such susceptibility is inti-
the ratio is independent of the absolute amount of specific anti- mated by evidence (e.g., Berkman & Syme, 1979; House, Rob-
body, yet it is the amount of the specific antibody that would bins, & Metzner, 1982) that social support is associated with
affect resistance to a specific pathogen. In addition, the ratio diminished death rates due to cancers and respiratory diseases,
does not have a predictable relation to stress. Because there is conditions the immune system defends against. Moreover, vari-
no reason to believe that stress differentially affects different ables bearing conceptual affinity to social support seem to be
specific antibodies, there is no reason to believe that the ratio related to immunologic functions. Studies have linked reduced
of one specific antibody to total S-IgA would vary with degree lymphocyte proliferation to both bereavement, which could be
of stress. In short, the concerns posited by Stone et al. are over- seen as a loss of social support, and self-reported loneliness,
stated and there is no empirical or logical reason to prefer the which could reflect low social support (e.g., Bartrop et al., 1977;
measurement of another aspect of immunity to total S-IgA con- Kiecolt-Glaser, Garner, et al., 1984; Schleifer et al., 1983).
centration in whole saliva. Other researchers (e.g., Jemmott et al., 1983, 1988) have tied
affiliation motivation, which may relate to higher social sup-
port, to greater S-IgA levels and natural killer cell activity
Stress and Secretory Immunoglobulin A (NKCA). None of these studies, however, directly measured so-
cial support; hence, the extent of social support's empirical re-
Several investigations intimate that psychosocial factors, in- lation to these variables or to immunologic functioning is un-
cluding stress, may alter S-IgA levels (for a meta-analysis see known. This study measured social support.
Jemmott & McClelland, 1988). Studies by McClelland et al. In summary, we examined the relation of academic stress and
(1980, 1982) suggest that individuals who are above average in social support to S-IgA concentrations. We sampled college stu-
self-reported life stress and power motivation have lower levels dents' salivary concentrations of S-IgA 5 days prior to their final
of S-IgA. Both studies operationalized stress with a life-events exams, during the exam period, and about 2 weeks after their
measure. Another way to examine stress is to identify an objec- last final exam. We hypothesized that academic stress would be
tively stressful event and then to record whether its occurrence associated with reduced S-IgA concentrations and that social
is marked by decreased S-IgA levels. Jemmott et al. (1983), us- support would be associated with higher S-IgA concentrations.
ing this strategy, assayed students' S-IgA secretion rates at According to the buffering model, the latter relation should hold
differentially stressful periods of their first year in dental school: only or chiefly during the high-stress period; the direct effects
at an initial low-stress period in September of their first year, at model asserts that it should hold regardless of the stress level.
three high-stress periods (during November, April, and June)
when they had important exams, and at a low-stress period just Method
before the start of their second year in school (July). As ex-
pected, S-IgA secretion rates were lower in the high-stress peri- Subjects
ods compared with the low-stress periods.
The subjects were 15 healthy Princeton University undergraduates (8
However, it might be argued that the reported variations in
men and 7 women), recruited via a sign-up sheet posted in the psychol-
S-IgA over time may in part reflect seasonal variations in S-IgA ogy building for "a study of the relation between psychological stress
secretion because the data collections were spread over an 11- and the functioning of the immune system." Most (80%) of the subjects
month period. Had the study been conducted within a shorter were juniors or seniors. All had exams scheduled during the university's
time frame, this explanation would not be tenable. To address designated final-exam period in each of their four courses. We told them
this issue, we examined the relation between acute academic that they would provide saliva samples and complete psychological
STRESS, SOCIAL SUPPORT, AND S-IGA 805
questionnaires. We did not specifically mention social support. Subjects of the correspondence between the type of support and the person's
received $5 for their participation. needs, satisfaction with support, and adequacy of support are consistent
with this theoretical position (e.g., Henderson, Byrne, & Duncan-Jones,
198 l;Procidano& Heller, 1983;Sandler&Barrera, 1984; I. G. Sarason,
Procedure
Levine, Basham, & Sarason, 1983).
We studied each student on three occasions. The first, a low-stress In this study we conceptualized social support as the degree to which
period, was about 5 days before the student's first final exam of the fall an individual's needs for support were met by others and assessed it
semester; the second, a high-stress period, was on the day of the student's with the Social Relationships Questionnaire. It is an adaptation of an
third final exam; and the third, a low-stress period, was during the first instrument Turner (1981; Turner & Noh, 1983) used in four studies
week of the spring semester, about 14 days after the student's last final of social support and psychological well-being. The Turner instrument
exam. On each occasion, they rated the stressfulness of the university's contains seven items measuring the amount of social support. Each
psychological climate and provided a saliva sample to be assayed for S- item consists of three descriptions of stimulus persons who have varying
IgA. At the initial session they also completed a social support question- amounts of social support. Stimulus persons are described to whom
others are devoted, who others let know they are wanted, with whom
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
others spend time, who have close friends they can count on, in whom
This document is copyrighted by the American Psychological Association or one of its allied publishers.
others have faith and confidence, who belong to a network of others, and
Perceptions of the University's Psychological Climate who are praised and admired in varying degrees. The respondent rates
how similar he or she is to the stimulus persons. To measure desire or
To examine whether our designation of the three periods as differen-
need for social support, Jemmott and Locke (1988) developed seven
tially stressful was in line with the students' perceptions of them, we
additional items. Each of these was paired with one of the items measur-
asked students at each data collection session to "Rate the extent to
ing amount of support. Table 1 shows an example of an item used to
which each adjective describes your perceptions of Princeton's general
measure amount of support and an example of a parallel item used to
psychological climate over the past couple of days." The adjectives were
measure need for support. The two types of items are combined to cre-
demanding, anxiety-provoking, competitive, supportive, warm, and
ate an adequacy of support score in which need for support is partialed
stressful. Ratings were made on scales ranging from 1 (not at all) to 7
from amount of support (J. Cohen & Cohen, 1983, pp. 414^t21).
(very much). Jemmott et al. (1983), using a similar procedure, reported
Higher scores indicate more adequate social support, a greater amount
that such ratings corresponded to a priori objective academic stress.
of support relative to the person's needs.
The only difference between the measure used by Jemmott et al. (1983)
Jemmott and Locke (1988), studying 100 middle-class men in Bos-
and the one we used in this study was the substitution of stressful for
ton, found that men who had more adequate social support (a) listed a
professional, which Jemmott et al. (198 3) used.
greater number of people they could turn to in times of need on the
Social Support Questionnaire's (I. G. Sarason et al., 1983) Number of
Secretory Immunoglobulin A Assay Available Others scale; (b) registered greater satisfaction with their per-
ceived available support on its Social Support Satisfaction scale; and (c)
We obtained timed, 2-min samples of whole unstimulated saliva at evidenced greater affiliation tendencies on McAdams's (1980; Mc-
each collection point, recording the volume (ml) of saliva in each vial. Adams, Healy, & Krause, 1984) test of the need for intimacy. In addi-
We always made collections at about 3:00 p. m. to minimize variation tion, replicating a common finding in social support research (S. Cohen
caused by circadian rhythms. The saliva was stored frozen. After thaw- & Wills, 1985; B. R. Sarason et al., 1987), more adequate support was
ing, we centrifuged and assayed the saliva for S-IgA concentration by related to psychological well-being, as revealed by low scores on both
single radial immunodiffusion (Mancini, Carbonara, & Heremans, the Depression-Dejection scale of the Symptom Checklist and the De-
1965) in 16-well agar plates containing monospecific goat antihuman pression scale of the Profile of Mood States. The partialed support score
IgA (Kallestad Laboratories, Inc., Chaska, MM). Five microliters of had reasonably good test-retest reliability (i.e., .63) over a 6-month in-
three reference S-IgA sera and the saliva samples were dispensed in du- terval for a social support index (cf. Turner, 1981; Schaefer, Coyne, &
plicate into wells by a micropipette delivery system and incubated in Lazarus, 1981). It has sufficient stability for the brief time interval of
duplicate at room temperature for 48 hr. Observers, who were unaware this study. Coefficient alphas were in the .81 to .85 range for both the
of the collection point and subject identity, measured precipitin ring amount of support and the need for support items on both occasions.
diameters with an ocular micrometer. We constructed a reference curve
by plotting the square of the ring diameters of the reference sera against
their concentrations. We multiplied the IgA concentrations in saliva de-
Results
termined from the standard curve by 3.25, the factor for converting Perceptions of the University's Psychological Climate
serum levels to secretory IgA levels (Brandtzaeg et al., 1970). The two
extreme reference concentrations were 4 mg/dl and 60 mg/dl for serum; Analyses revealed that the students' perceptions of the uni-
hence, the assay was sensitive between concentrations of 13 mg/dl and versity's psychological climate during the three periods were in
195 mg/dl for saliva. All of the concentrations were within this range. agreement with our designation of those periods as differen-
tially stressful. We analyzed the students' perceptions using re-
Measuring Social Support peated measures analyses of variance (ANOVAS) and a planned
contrast (Rosenthal & Rosnow, 1985) testing the hypothesis
Social support has been conceptualized and operationalized in di- that the climate was perceived as being more stressful at the
verse ways (S. Cohen & Wills, 1985; B. R. Sarason, Shearin, Pierce, &
second period compared with the other two periods.1 We did
Sarason, 1987; Wortman, 1984). Several theorists and researchers have
reasoned that it is not sufficient to measure the amount of social support
1
(e.g., S. Cohen & Wills, 1985; Kaplan, Cassel, & Gore, 1977; Thoits, A Sex of Subject (male and female) X Time Period (preexam, exam,
1982). Whether a given amount of support is adequate to the person's and postexam) mixed-model analysis of variance with repeated mea-
support needs must be considered, for there are individual and group sures on the second variable performed on the perceived-stress index
differences in the quantity and kind of support needed depending on revealed no significant sex-of-subject main effect or Sex of Subject X
such factors as individuals' characteristics and circumstances. Measures Time Period interaction.
806 JOHN B. JEMMOTT III AND KIM MAGLOIRE
Time Period
Table 1
Figure 1. Mean perceived stressfulness of the university's
A Sample Amount of Support and Need for Support Item psychological climate.
Amount of support
JD>
able.
This document is copyrighted by the American Psychological Association or one of its allied publishers.
30-
Discussion
respiratory tract infection (Jemmott & McClelland, 1988). do more general criticisms of life-events methodology (e.g.,
Whether an infection would actually occur and whether it Minter & Kimball, 1978; Rabkin & Struening, 1976). Expo-
would remain subclinical or lead to clinically significant illness sure to academic stress was independent of the students' social
depends on many factors, including exposure to a pathogen to support. Still, this study links more adequate social support to
which the person is susceptible and the amount of such expo- reduced disease susceptibility.
sure. Recent evidence indicates that the amount of social support
Other researchers have also reported that academic stress is an individual receives is related to personality characteristics
associated with diminutions in aspects of immunologic func- (e.g., Dunkel-Schetter, Fblkman, & Lazarus, 1987). Future re-
tioning. Dorian et al. (1982), comparing 5 psychiatry residents search must identify particular personality characteristics or
undergoing an examination with 9 controls, found lower lym- circumstances that systematically influence individuals' long-
phocyte proliferation to mitogens among the residents prior to or short-term needs for social support. The factors affecting so-
the exam. Kiecolt-Glaser, Speicher, et al. (1984) reported re- cial support receipt might well differ from those that influence
need for support. It is also possible that the same factors affect
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
ropositive medical students on the first day of their final exams individuals' need for support and amount of support, but in
compared with a month earlier and a week after their return different ways. Consider, for example, the case of the patient
from summer vacation. In addition, Kiecolt-Glaser, Garner, et with acquired immune deficiency syndrome who is abandoned
al. (1984) observed lower NKCA in 75 medical students on the by friends, coworkers, and relatives. Social support receipt may
first day of final exams compared with a month earlier. How- be lowest at the very time an individual's need for support is
ever, significant relations between academic stress and decreases greatest.
in aspects of immunity have not been found in every study (e.g., In this study we measured social support at the initial data
McClelland, Ross, & Patel, 1985), and these decreases may oc- collection point and prospectively linked it to S-IgA levels as-
cur in some aspects of immunity while not occurring in others sessed in a more state fashion. Future research could also assess
(e.g., Dorian et al., 1982). Moreover, such conflicting findings undulations in individuals' support need and supply over time
are not limited to the effects of academic stress or to studies on in relation to immune functioning.
humans. Why they occur is not well understood (Jemmott & Reviews of the social support literature have highlighted the
Locke, 1984; Monjan, 1981; Rogers etal., 1979). need to research mechanisms underlying the relation between
social support and the incidence of disease (e.g., S. Cohen &
Wills, 1985; Wortman, 1984). Our study suggests one such
Social Support mechanism. A lack of adequate social support may reduce S-
We also found that adequacy of social support was related to IgA levels, rendering the individual more vulnerable to infec-
S-IgA concentrations. Students who had greater social support tion. What needs to be considered in future studies are potential
relative to their needs for social support had consistently higher mediators of a social support-immune function linkage. People
S-lgA levels compared with other students. When we analyzed who have more adequate social support may experience less de-
amount of social support, ignoring needs for support, the rela- pression and anxiety and smaller increases in corticosteroids
tion was positive but not significant, suggesting the value of tak- and catecholamines (S. Cohen & Wills, 1985) when threatened
ing individual differences in need for social support into ac- by stressful events such as academic exams. The release of corti-
count. Two images of the individual who has a high degree of costeroids and catecholamines can be immunosuppressive
social support have been posited. One image, drawn by the di- (Borysenko & Borysenko, 1982). In addition, there is evidence
that depression is associated with decrements in immune func-
rect effects theorists, suggests a person who is continually less
tioning (Kronfol et al., 1983; Linn, Linn, &Jenson, 1982). One
vulnerable to disease than are his or her peers. The other, drawn
particularly pertinent study is that by Linn et al. (1982), who
by buffering effect theorists, suggests an individual who is less
reported that men scoring relatively high on the Depression
vulnerable to disease, but chiefly during periods of relatively
scale of the Symptom Checklist had lower lymphocyte prolifer-
high stress. Inasmuch as students who reported more adequate
ation responses than did other men. Inasmuch as Jemmott and
support had consistently higher S-IgA, our results favor the di-
Locke (1988) found that less adequate social support, as opera-
rect effects model.
tionalized in this study, was associated with higher scores on
We operationalized stress with an academic exam, a discrete
this same Depression scale, it is possible that depression medi-
objective event, as opposed to a serf-report, life-events index,
ates the effects of adequacy of support on immune functioning.
the norm in research on stress and social support (S. Cohen &
Alternatively, people who have more adequate social support
Wills, 1985). Whereas the life-events approach (e.g., Dohren-
may engage in fewer behaviors that increase their risk for dis-
wend & Dohrenwend, 1974; Holmes & Rahe, 1967) has ad-
ease. For instance, they may be less apt to get an inadequate
vanced understanding of the effects of stress, several criticisms
amount of sleep, to have a poor diet, or to engage in substance
have been leveled at its use in social support research. It has
abuse. All of these possibilities must be considered. By conduct-
been asserted that lack of social support might have occasioned
ing research along these lines, a fuller understanding of the rela-
the occurrence of the stressful events in some studies or that the
tion of psychological stress and social support to disease suscep-
occurrence of the events might have triggered the lack of social
tibility may be achieved.
support (Thoits, 1982). In addition, some life-events instru-
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