Prolonged reduction of salivary immunoglobulin A (sIgA) after a major academic exam

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Abstract

Objective: In a previous study we observed a continuous reduction of salivary IgA concentration ([sIgA]) during a period of academic stress. This reduction of sIgA concentration exceeded the stress period by at least 1 week. The present study aimed to replicate and extend our previous finding. In particular, we wanted to examine the time of recovery of [sIgA] alterations associated with academic stress. Method: Twenty-seven participants in a major medical exam and 27 controls not participating in any exam during the study provided daily saliva samples (immediately after awakening), from the 6th day prior to their last exam until the 14th day afterwards, for analysis of salivary IgA. Data were averaged for the last weeks of exams and the first and second week after exams, respectively. Results: A prolonged reduction of sIgA in exam students as compared to controls was observed. Fourteen days post-stress sIgA concentrations of exam students were still significantly lower than control levels (P=0.004). No recovery was observable. At the same time exam students and controls did not differ in terms of self-reported stress and recovery. Conclusions: Psychological and immunological stress effects may be dissociated, the latter considerably exceeding the stress period. A closer look at the temporal dynamics of stress-induced immune alterations might increase our understanding of psychoimmuno relationships.

Introduction

Secretory Immunoglobulin A is an antibody found in high concentrations on all mucosal surfaces of the human body including the respiratory tract. It is thought to serve as a first line of defense against invading organisms and thus, to play a key role in prevention of infectious disease (Tomasi, 1970, Tomasi, 1992, Ogra et al., 1971, Mestecky et al., 1986, Jemmott and McClelland, 1989, Mestecky and Russell, 1997, Lamm, 1998). Stress is thought to play a role in mucosal infections like upper respiratory tract infection or periodontal inflammation (Marcenes and Sheiham, 1992, Cohen, 1995, Deinzer et al., 1998, Deinzer et al., 1999, Deinzer et al., in press). For these diseases it is known that IgA is involved in the host’s defense against their pathogens (Tomasi, 1970, Tomasi, 1992, Ogra et al., 1971, Ebersole et al., 1986, Mestecky et al., 1986, Jemmott and McClelland, 1989, Ogawa et al., 1991, Nieminen et al., 1993, Somer et al., 1993, Mestecky and Russell, 1997, Lamm, 1998).

Secretory IgA, especially salivary IgA (sIgA) became a focus of interest in psychoimmunological research since it has been shown to be sensitive to variations in subjective and objective stress levels. Acute challenges like assessed seminar presentations (Evans et al., 1994, Bristow et al., 1997), competition stress in soccer coaches (Kugler et al., 1996), 100-min working sessions of air traffic controllers (Zeier et al., 1996) and a laboratory computer game task (Carroll et al., 1996), have all been shown to be associated with sIgA increases. sIgA levels and secretion rates were found to be related to desirability of daily events (Evans et al., 1993, Stone et al., 1994), an effect suggested to be mediated at least in part by mood: negative mood tends to be associated with lower sIgA (Stone et al., 1987a, Stone et al., 1987b, Stone et al., 1996). Decreases in sIgA have been observed at parturition (Annie and Groer, 1991) and during prolonged periods of academic stress (Jemmott et al., 1983, Jemmott and Magloire, 1988, Deinzer and Schüller, 1998) although there is some inconsistency in reports on academic stress effects (McClelland et al., 1985, Bosch et al., 1996; see Section 4 of this paper).

By now, much is known about the immediate effects of stress on salivary IgA. The significance of stress-induced immune alterations, however, would be better understood if we knew more about their temporal dynamics. That is, when do stress effects on sIgA peak and for how long do they persist? Little is known about these questions, so far. In a recent paper we analyzed the effects of a major academic exam on sIgA from the 7th day prior to the exam until the 6th day afterwards (Deinzer and Schüller, 1998). The most striking result of this study was that sIgA concentration not only decreased at exam days but dropped further afterwards. Within the 6 days post-stress period we assessed, sIgA concentration remained below baseline; no recovery was observable. The present study aimed to replicate and extend the results of our earlier study. Most importantly, we now extended our post-stress assessment period to 14 days, expecting sIgA concentration to recover at least in part within that period.

Academic stress appears to be an ideal setting for the assessment of temporal dynamics of stress-induced immune alterations. The immediate immunological effects of academic stress are well known (Jemmott et al., 1983, Kiecolt-Glaser et al., 1984, Glaser et al., 1985, Glaser et al., 1990, Glaser et al., 1991, McClelland et al., 1985, Vassend and Halvorsen, 1987, Jemmott and Magloire, 1988, Mouton et al., 1989, Bosch et al., 1996, Deinzer and Schüller, 1998). The stressor is of high ecological validity and defined exam conditions guarantee some degree of standardization. Subjects as well as adequate control persons are easily available. Additionally, as the termination of the objective stressor is clearly defined (i.e. the exam or last exam within a prolonged exam period), one can also study immunological post-stress effects.

There have been suggestions that alterations within the post-stress period may account for development of disease (Deinzer, 1992) though it is not clear today whether this should be due to immunological alterations. However, the data of our previous study strongly support the notion that mucosal immune function is compromised particularly during the post-stress period. The aim of the present study was to add further data relevant to this finding and thus, to improve our understanding of immunological post-stress effects.

Section snippets

Subjects

Fifty-four medical students (27 exam students and 27 controls) provided a full set of valid data for this study. At the beginning of the study, subjects were asked about their age, number of semesters they studied medicine, exercise, regular nicotine consumption, use of oral contraceptives and whether they had a regular partner. These data are provided in Table 1. Groups did not differ on any of these variables.

Recruitment of subjects was done during their seminars; in addition, fliers

Results

The exam was a potent stressor in terms of psychological self-report as can be seen from Fig. 1 which shows the results of the recovery-stress-questionnaire. Exam students reported more stress and less recovery in the last week of exams while control group values remained constant. Within 3 days post-examination exam students recovered to control values in all but the success scales. At that time they even reported less lack of energy, less somatic complaints and more social relaxation than

Discussion

The present study replicates and extends results of a previous study from our laboratory (Deinzer and Schüller, 1998). During a prolonged period of academic stress, sIgA concentrations after awakening were reduced as compared to baseline and to control values. Furthermore, no recovery of sIgA concentration could be observed within 14 days post-stress even though students recovered very soon in terms of self-reported stress and recovery. Recovery in sIgA concentration showed a tentative relation

Acknowledgements

We greatly appreciate the excellent technical assistance of Mrs. Schulten in running the sIgA analyses.

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