Negative affect, absorption, and immunity

Physiology&Behavior,Vol.53, pp. 449-457, 1993

0031-9384/93 $6.00 + .00 Copyright© 1993 PergamonPressLtd.

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Negative Affect, Absorption, and Immunity J O H N D. C. S H E A , *l R O B E R T B U R T O N t

AND AFAF GIRGISt

*Psychology Department, University of Newcastle, N S W Australia and i-Medical Faculty, University of Newcastle, N S W Australia Received 18 July 1991 SHEA, J. D. C., R. BURTON AND A. GIRGIS. Negativeaffect, absorption, and immunity. PHYSIOL BEHAV 53(3) 449-457, 1993.--Relationships between the psychological characteristics absorption and neuroticism, and in vitro and in vivo measures of cell-mediated immunity were examined. Thirty-nine female subjects responded to questionnaires, donated blood for analysis of T-cell numbers, and were tested for delayed hypersensitivity skin responses. Consistent with the experimental hypothesis, subjects classified as repressors of negative affect (low absorption/low neuroticism), or extreme expressors of negative affect (high absorption/high neuroticism), showed lower immune responses than other groups of subjects. For the in vitro T-cell measures and the in vivo skin induration measures, there were also pervasive main effectsof neuroticism, with subjects higher in neuroticism showing higher immunity than subjects lower in neuroticism. Personality and immunity Psychoimmunology Negative affect and immunity NA and immunity

Behavioral immunology

Psychosocial factors and immunity

of research in this area concerns the observation that emotionally reactive people tend to report greater levels of symptomatic distress but do not always show changes in behavioral indicators such as absenteeism, doctors' visits, extent of current disability, general fitness and lifestyle variables, biological markers such as blood pressure, serum risk factors, immune system functioning, or objective evidence of dysfunction such as mortality rates (8,46). If anything, people low in NA may be more subject to cardiac problems (46), and may be more likely to develop cancer and to have lower survival rates once it is diagnosed [e.g., (9,19,44)]. A recent study (38) examined relationships between measures of trait and state NA and life changes, and a variety of cell-mediated immune responses in a small group of medical students facing acute examination stress. The findings tended to contradict the idea that high NA is associated with relatively depressed immunity. Low scorers on state and trait measures often had poor immune responses. One popular explanation for such effects utilises the concept of repression, and the idea that high NA scorers reduce the effects of stressors on themselves through the expression of negative emotion, but that repression may actually exacerbate it's effects [e.g., (6,11,32,45)]. This viewpoint allows for the possibility also that the group next most seriously affected by external stressors involves individuals who are high in NA, since their emotional responsiveness indicates relatively poor coping with the stressors (17). Giving support to the first of these theories are studies in which significant immunological and long-term health improvements have been noted to occur subsequent to therapies which reduced emotional inhibition and enhanced self-disclosure or feelings of emotional control [e.g., (17,18,24,28,33)].

THE idea that some individuals and not others may be prone to immune suppression has received considerable attention over recent years (39,42). A common proposition is that some people, through learning or biology, are more emotionally reactive than others, as a result of which prolonged nervous arousal and fatigue occurs (14,27). It has been proposed that such patterns of response are associated with health problems including immune deficits. Such people are said to score high on trait measures of negative affect (NA) such as neuroticism, anxiety, or emotionality measures. NA has been causally related to a variety of minor (headaches, nausea, ache) and major (ulcers, coronary heart disease, arthritis, asthma, diabetes) health problems (2,3,10,13,21,22,34). Power motivation, a concept apparently related to NA, has been consistently associated with higher levels of trait anxiety and depression, and with decreased concentrations of S-IgA (poorer immunity is assumed) during exams. A greater amount of self-reported illness, particularly of upper respiratory tract infections, has also frequently been noted within these studies [for reviews, see (22,29)]. Relatively enduring mood changes, decreases in trait NA, with concomitant reductions in physical symptoms and health clinic visits as well as apparent improvements in immunity measures, seem apparent in intervention studies using relaxation therapy (16,25,37). Thus, people high in negative affect should show immune deficits, with or without the immediate presence of external stressors. However, relationships between trait NA and immunity have rarely been investigated, and available data often contradict the hypothesis of a negative relationship, finding no relationship with trait NA (26) or negative effects (3,40). A major criticism

, Requests for reprints should be addressed to John D. Shea, PhD., Psychology Department, University of Newcastle, Shortland, NSW 2308, Australia.

449

450 An alternative proposal suggests that genuinely low-anxious subjects arc at risk from environmental stressors, due to their reduced ability to perceive stress and to become habituated or immune to it in the long term (11). Conversely, high trait anxiety or neuroticism give health protection (e.g., from cancer) under conditions of chronic stress through such habituation processes. Some NA effects appear to be mediated by self-attention style (46). For subjects low in private self-consciousness, but not for subjects high in this characteristic, stressful life events have been shown to be predictive of illness within a 2-month period (30,41). Thus, it would be of interest to measure self-attention when evaluating the effects of NA on health or immunity. Because there may be several kinds of self-consciousness which may interact with each other to affect an individual's health (49), it may be useful to examine a measure of self-attention different from the one used in the above studies. One such measure is absorption, the capacity for focussed attention. People scoring high on this measure have a greater capacity to attend to internal cues (43), and to bring about bodily changes; they are readily able to achieve relaxation after a simple direction to do so, without any special training or biofeedback, and their principal strategy for achieving this change is the use of appropriate mental imagery (35). These attributes would seem to make absorption an appropriate variable to use in exploring relationships between self-attention and immunity, An obvious point of concern is that since high absorbers can control their bodies" arousal levels more readily than others, questions arise concerning possible baseline differences in arousal (including negative affect) and in immunity between high and low absorbers. There are other reasons tbr choosing absorption as an appropriate measure of self-attention. It is of direct concern here, firstly because some authors have suggested that, like neuroticism, a key concept in the area of NA, it is a major dimension of personality (43), and secondly, because it is the single best predictor of hypnotic talent (31 ). Hypnosis is of relevance in the psychoimmunology area as a result of studies using hypnosis or relaxation [e.g., (16,18,20,23,25,37)] in efforts to change immunity specifically, or an immune-related illness such as cancer. One strategy for examining NA and absorption which might clarify areas of overlap between the two characteristics and test theoretical positions noted above, is to create a matrix of groups of extreme high and low scorers on the two measures. Those subjects who are low in both absorption and NA are, by definition, low in self-awareness and in reports of negative emotionality. These are key characteristics of repressors. On the other hand, subjects who are high in both absorption and in NA seem to exemplify the introspective, ruminative types who show extremes of psychosomatic distress (46). They are an extreme expressive group in terms of NA concepts. Since individuals who have low scores on absorption and high scores on NA are clearly not repressors of emotion, and do not fit neatly with the idea of the self-focussed symptom seeking personality that is said to characterise those showing extremes of psychosomatic distress (46), there is no reason to expect that they will show deleterious immune effects from the stressors of everyday life. Their high NA scores may reflect an accurate assessment of life experience, true negative affect, but low absorption scores suggest that they are unlikely to give undue attention to the effects of these stressors. They may, therefore, cope better with external stressors. Individuals who have high scores in absorption and low scores on NA, while self-reflective, do not attend excessively to negative physical and psychological symptoms. Their low NA scores may result from a relative absence of life stressors, or from positive personal self-attributions that may occur with higher levels of self-awareness (5), or both. In any

S[-IEA, BURTON ANI) (51ROIS event, these stable self-absorbed individuals might be expected to show better health and higher immunity. Accordingly, following the notion that individuals who cope poorly with stressors will experience immune deficits, and that two groups who are likely to show such effects are repressors of NA and extreme expressors of NA, it is hypothesised that both low absorption/low NA subjects (repressors) and high absorption/high NA (extreme expressors) subjects will show lower baseline immune responses than low absorption/high NA (true negative affect) and high absorption/low NA groups (stable selfabsorbed). METHOD

Subjects and Psychometric Pmcedure~ Subjects were female volunteers from an Introductory Psychology class. Two hundred and two female students filled out a number of questionnaires at the beginning of the academic year for the study which was described as dealing with psychological factors and the immune response. Five psychometric procedures were used, the Tellegen-Atkinson Absorption scale (43), the Willoughby Neuroticism scale (47), the Coopersmith Self-Esteem scale (7), the Rotter Locus of Control scale (36), and the General Health Questionnaire or GHQ (15). These were all scored according to standard procedure. Subjects were asked also to give their age, and to estimate the number of cigarettes they smoked each day. The Willoughby Neuroticism scale was used as a measure of NA because it has been described (47,48) as the best indicator of clinically significant stress. The Coopersmith scale and the Locus of Control scale were included because these measures are related to the concept of NA. The GHQ is included as a measure of state stress. The Tellegen-Atkinson Absorption scale was used for reasons mentioned above. Forty-eight extreme responders on absorption and neuroticism were selected from the subject pool in four equal groups; low absorption/low neuroticism (labelled repressors), low absorption/high neuroticism (labelled true negative affect), high absorption/low neuroticism (labelled stable self-absorbed), and high absorption/high neuroticism (labelled extreme expressors). After being informed of what was required of them, subjects were invited to participate further. Some of the potential subjects had dropped out of psychology classes by this time, and they and some others did not make contact with the researchers. A final group of 39 subjects participated in the complete study. The mean absorption scores and neuroticism scores of both the total student group and the final subject group were approximately 22 and 42, respectively. Table 1 shows the mean ages, absorption scores, neuroticism scores, and the average number of cigarettes smoked per day in the four experimental groups.

Procedure jbr Measurement o[Immune Responses After details of the procedures were explained, subjects donated blood and were exposed to antigens to test for skin hypersensitivity at the same occasion. This was on a weekday morning between 0900 and 1000 h. This standard time was chosen to control for diurnal changes in lymphocyte distribution and other responses. Samples of blood (0.10 ml) were taken from each subject by a qualified medical practitioner. Before administering the skin hypersensitivity test, the procedure was explained to subjects at length. This served the dual purpose of informing them about the tasks required of them, and ensuring that there were no untoward side effects from the blood sampling procedures. Following this, the cell mediated immunity multitest

NEGATIVE AFFECT, ABSORPTION, IMMUNITY

451

TABLE 1 MEAN AGE, ABSORPTION,AND NEUROTICISMSCORES (ROUNDED), NUMBEROF CIGARETTESSMOKEDDALLY,AND NUMBER FOR THE FOUR EXPERIMENTALGROUPS Low A b ~ r ~

Neuroticism Low High

n

Age

11 8

19.27 19.75

Absorption

14 16

High A b m r ~

Neuroticism

27 50

device was applied to the forearms of subjects following procedures recommended by Institut Merieux. Blood samples were collected in heparinized tubes, and lymphocytes isolated following established procedures (4). The 10 ml specimens were divided into two 5 ml samples and diluted l:l with PBS and underlaid with 5 ml (each) of Ficoll-Hypaque (Pharmacia Fine Chemicals, Piscataway, N J). Samples were centrifuged at room temperature for 30 min at 1200 rpm. Mononuclear cells were harvested from the interface and washed twice with PBS to remove all Ficoll-Hypaque. Final cell pellets were resuspended in RPMI medium supplemented with 5% fetal calf serum, 2% penicillin streptomycin, 1% L-glutamine, and 0. 1% 2-mercaptoethanol. Cell concentration was determined by haecytometer and concentration adjusted by adding additional media. The cells prepared in this manner were then divided and used to determine T-cell numbers. Staining of T-cells was carried out using the monoclonal antibodies (supplied by Ortho Pharmaceuticals, Raritan, N J) recognizing total T-lympbocytes (OKT3), the helper/inducer subset (OKT4), and the cytotoxic/suppressor subset (OKT8), and measurements obtained using a Spectrum III automated flow cytometer (Ortho Diagnostics, Westwood, MA) (4). This procedure allowed for the estimation of absolute lymphocyte count, the specified T-Cell numbers, and the ratio of T4:T8 cells. Delayed hypersensitivity skin (DHS) tests were conducted using the Institut Merieux CMI multitest. This device contains antigens to seven active agents and a glycerin control. The active antigens (using the numbering applied by Institut Merieux) were, l tetanus, 2 diphtheria, 3 streptococcus, 4 tuberculin, 6 candida, 7 trichophyton, 8 proteus; the glycerin control substance was in the fifth position. The numbers corresponding to the antigens and the glycerin control were written on the subjects' forearms when the test was administered. Measurement of skin induration were carried out 48 h after initial exposure to the CMI Muititest, using recording forms provided by Institut Merieux. Induration of the skin was measured in millimetres across the longest diameter and then across another diameter at right angles to the first. This procedure provided eight separate measures of induration for the skin sites tested, as well as scores for the number of sites showing measurable induration reactions, and a compound score (total) of induration responses per subject. Higher scores on immunity variables were taken to be indicators of better immune responding. For instance, circulating T4-cell numbers of more than 400 are less likely to be associated with a clinically significant problem than lower T4-cell numbers. Thus, larger T-cell numbers in general and greater skin induration in response to antigens were considered to be better immunologlcally than smaller numbers and less induration. An exception is very high T4:T8 ratios which are commonly seen as an indicator of intercurrent viral infection. Thus, both very low and very high T4:T8 ratios may be indications of health problems.

Smoking

n

Age

0.0 6.6

8 12

20.25 19.33

Absorption

28 29

Neuroticism

30 58

Smoking

1.4 2.7

RESULTS Analysis of covariance, multivariate analysis of variance, and correlation were used to examine the data. Analyses ofcovariance using absorption (two levels, low and high) and neuroticism (two levels, low high) as independent variables, and all possible immune measures as dependent variables, were carried out. Covariates were age and number of cigarettes smoked on a daily basis. There were many significant effects revealed in these analyses.

Measures of Cell Numbers It should be noted that T4- and T8-cell numbers are subsets of T3-cells numbers which, in turn, is a subset of absolute lymphocyte count. Thus, these measures overlap to a considerable degree. There were no significant main effects in these analyses of covariance, but there were several significant absorption X neuroticism interaction effects. These effects are summarised in Table 2. Newman-Keuls post hoc analysis indicated that for absolute lymphocyte count (ALC), and T3-cell numbers, the low absorption/high neurotic (true negative affect) groups had significantly higher cell numbers than the low absorption/low neurotic (repressors) groups and the high absorption/high neurotic (extreme expressors) groups (all p < 0.05). Table 2 shows that ALC and T3-cell numbers for the high absorption/low neurotic (stable self-absorbed) group were closer to the true negative affect group than to any other group. For T4-cell numbers the covariate smoking showed significant effects, F(1, 33) = 4.48, p < 0.05. Accordingly, cell numbers corrected for the effects of the covariates age, and smoking are shown in Table 2. There was also a significant interaction effect (Table 2). Post hoc analysis indicated that the true negative affect group had higher cell numbers than the repressors group (p < 0.05). Table 2 shows that the cell number for the extreme expressors group is similar to that for the repressors group, and the cell number for the stable self-absorbed group is similar to that of the true negative affect group. For T8-cell numbers, Newman-Keuls analysis showed that the true negative affect group and the stable self-absorbed group had significantly higher cell numbers than the other two groups; p < 0.01 for the true negative affect comparisons, and p < 0.05 for the stable self-absorbed comparisons. For the ratio of T4:T8 ceils, the covariate smoking showed significant effects, F(1, 33) = 5.08, p = 0.031. Ratios corrected for the effects of the covariates are shown in Table 2. There was also a significant absorption X neuroticism interaction (Table 2). Post hoc analysis showed that the stable self-absorbed group had a significantlylower ratio than the extreme expressors group (p < 0.05). The T4:T8 ratio for the true negative affect group is almost identical to that of the stable self-absorbed group (Table 2).

452

SHEA. B U R T O N , \ N I ) G I R ( i l S

TABLE 2 S I G N I F I C A N I A B S O R P T I O N ': N E U R O T I C I S M E F F E ( ' I S W H ' H ('ELL N U M B E R S

AI.C

Low N High N

T3 cell number

Low N High N

T4 cell number*

Low N High N

T8 cell number

Low N High N

T4:8 ratio*

Low N High N

l.ow Absorbers

ltigh Absorbers

Interaction

1684 [1 l] (SD 515) 2635 [8] (SD 604) 963 (SD 246) 1649 (SD 447) 586 (SD 174) 841 (SD 260) 358 (SD 144) 630 (SD 247) 1.83 (SD 0.61) 1.47 (SD 0.71)

2300 [8] (SD 923) 1760 [12] (SD 482) 1466 (SD 661) 1026 (SD 347) 805 (SD 346) 622 (SD 229) 560 (SD 196) 309 (SD 122) 1.44 (SD 0.31) 2.30 (SD 1.04)

FI 1, 33) 13.76 p 0.0008

F( 1, 33) = 15.26 p ~ 0.0004

F(1, 33) = 7.45 p - 0.01 F(1, 33) ~ 22.61 p < 0.00001

F( l, 33) = 6.67 p

0.0145

Numbers in brackets are cell numbers. * Means are adjusted for the significant effects of covariates age and smoking.

Delayed Hypersensitivity Skin (DHS) Tests Analyses for the skin test data showed several significant main effects, particularly for neuroticism, and significant interaction effects. These effects are summarized in Table 3. As expected, the glycerin control condition produced no significant effects. Neither were there any significant induration effects for the tetanus or diphtheria antigens. With streptococcus, there was a significant neuroticism main effect and an interaction effect for skin induration. High neurotics showed larger induration responses than low neurotics. However, examination of means shows that this difference is due primarily to the greater induration in the true negative affect group. Post hoc analysis indicated that this group was significantly different from the repressors group (p < 0.01). For the tuberculin antigen there was a significant neuroticism main effect for skin induration (Table 3). The high neurotics showed larger induration responses than low neurotics. Examination of the means in Table 3 shows that most of this effect was contributed by the very large scores in the true negative affect group. For the candida antigen, there was a highly significant absorption main effect with induration. The low absorbers showed greater skin responses than the high absorbers (Table 3). There was a significant main effect for neuroticism with the number of induration responses per subject (Table 3). High neurotics showed a greater number of induration responses than low neurotics.

Multivariate Analysis Since a large number of skin induration responses were used in the analyses of covariance described, multivariate analysis of variance was used to investigate the possibility that there was a relationship between the personality measures and skin induration responses in general. There were significant multivariate

main effects for both absorption [TSQ = 32.4304, F(7, 29) = 2.77, p < 0.025] and neuroticism [TSQ = 24.6817, F(7, 29) = 2.92, p < 0.02]. The F values of the individual analyses may be used as a guide to the nature of these effects. For absorption, the F values from the individual analyses were: candida, 8.48; tuberculin, 1.77; trichophyton, 1.58: diphtheria, 0.97; streptococcus, 0.83; proteus, 0.71; tetanus, 0.68. Clearly, reactions to the candida antigen are the best indication of the nature of absorption effects in the multivariate analyses. Thus, low absorbers generally had larger induration skin response than high absorbers. For neuroticism the F values from the individual analyses of covariance were as follows: streptococcus, 7.42; tuberculin, 6.79; proteus, 2.53: candida, 1.31; tetanus, 1.10; diphtheria, 0.16; trichophyton, 0.04. Accordingly, responses to the streptococcus and tuberculin antigens (Table 3) may be taken as the best indication of neuroticism effects in the multivariate analysis. High neurotics had larger skin induration responses than low neurotics. Relationships between the personality variables, neuroticism in particular, and skin induration responses were further explored by combining some of the individual induration responses to create an overall induration score. Using the F values of the individual analyses of covariance as a guide, and setting an arbitrary selection criterion of an F value greater than 2.5, three induration measures, streptococcus, tuberculin, and proteus were pooled to provide a single induration score that was used in an absorption × neuroticism analysis of covariance with age, smoking, and responses to the glycerin control as the covariates. Table 4 shows the means, corrected for the effects of the covariates, for the interaction and the main effects. There was a trend for an absorption effect, F(1, 32) = 3.02, p = 0.09, a significant neuroticism effect, F(1, 32) = 17.27, p < 0.0002, and a significant interaction effect, F(I, 32) -- 4.55, p = 0.041. There were no significant effects of the covariates. Table 4 shows that the lowest induration response for this set of measures came from the repressors group, and the highest from the true negative

N E G A T I V E AFFECT, A B S O R P T I O N , I M M U N I T Y

453

TABLE 3 SIGNIFICANT ABSORPTION AND NEUROTICISM EFFECTS FOR DHS INDURATION RESPONSES Low Absorption

High Absorption

Main Effects

Interactions

N, F(I, 33) = 7.42 p < 0.01

F(1, 33) = 7.16 p < 0.012

N, F(1, 33) = 6.79 p < 0.014

NS

A, F(I, 33) = 8.48 p < 0.007

NS

N, F(I, 33) = 5.19 p < 0.03

NS

Streptococcus

Low N

0.00 (0.00)

0.58 (1.40)

Tuberculin

High N Low N

1.59 (1.62) 0.27 (0.90)

0.54 (0.99) 0.36 (0.87)

Candida

High N Low N

2.68 (3.02) 3.05 (2.22)

1.13 (1.76) 1.50 (1.79)

High N Low N

4.33 (1.11) 1.82 (1.47)

2.17 (1.76) 1.38 (1.41)

High N

3.13 (1.36)

2.42 (1.51)

Number of induration response

* Means shown are in millimetres; standard deviations are in parentheses.

affect group, with the other two groups falling in between these extremes.

Correlations Considering firstly, correlations between age and cigarette smoking and i m m u n e responses, there were significant relationships between number of cigarettes smoked daily and T4-cell numbers (r = 0.37, p < 0.05), and the T4:T8 ratio (r = 0.36, p < 0.05). O f the two psychological variables examined, absorption was negatively correlated with the induration response to the candida antigen (r = -0.39, p < 0.05), and neuroticism was positively correlated with the number of induration responses (r = 0.37, p < 0.05). Within the independent T-cell measures (T4-cells and T8cells), T4-cell numbers correlated with T8-cell numbers (r = 0.57, p < 0.01), but there were no significant correlations between these two measures and skin responses. Within the induration responses to the seven antigens used in the study, induration responses to tetanus antigen correlated with responses to candida (r = 0.37, p < 0.05), and induration responses to diphtheria antigen correlated with responses to tuberculin and trichophyton antigens (respectively, r = 0.39, p < 0.05; r = 0.47, p < 0.01). There were no other significant correlations.

Exploratory Analyses A further set of covariance analyses and a multivariate analysis of variance were carried out with the T-cell data and the induration responses, using two levels of absorption (low and high) and three levels of neuroticism (low, medium, and high). Although these analyses involved cell sizes as low as five in some instances, they allowed for further examination of the effects of variation from the mean on relationships between neuroticism and i m m u n e responses. The mean values for main effects and interactions in the analyses of covariance are shown in Table 5. Comparison with Table 2 shows that almost all the significant effects from the 2 × 2 analyses are repeated, the exception being the T4-cell measure. With regard to the T-cell measures, although there is some increase in cell numbers between low and medium neurotics who are low in absorption, there is a greater difference between the medium and high neurotic groups. Effects are less clear for the high absorption subjects. There are indications that the effects of neuroticism, in interaction with absorption, are not linear, though within absorption groups greater divergence from the mean is associated with more extreme (greater or lesser) neuroticism effects. The situation is much clearer with the induration responses. In almost every case shown in Table 5, for both low and high absorbers successively higher neuroticism scores are associated with greater induration responses. DISCUSSION

TABLE 4 MEAN OVERALL INDURATION, FOR COMBINED STREPTOCOCCUS, TUBERCULIN, AND PROTEUS SCORES IN MILLIMETRES, AS A FUNCTION OF ABSORPTION AND NEUROTICISM;CORRECTED (AFTER ANALYSIS OF COVARIANCE)FOR THE EFFECTS OF AGE, SMOKING AND RESPONSES TO A GLYCERINE CONTROL

Neuroticism Low High Overall

Low Absorption

High Absorption

Overall

0.24 [11] 1.70 [8] 0.85 [19]

0.31 [8] 0.79 [12] 0.60 [20]

0.27 [19] 1.15 [20]

Numbers in brackets are number of cells.

It should be noted that the test situation was one of high acute stress. This conclusion was reached after the observation that about 40% of the subjects fainted, felt faint, blanched, or were otherwise visibly distressed at the prospect of having blood taken from them via a needle. Though this phenomenon is recognised in the clinical context, and seems age related (l), it is not noted in the literature reviewed above. Yet it is difficult to imagine any other stressful circumstance with such powerful effects. Thus, conclusions reached about relationships between personality measures and immunity based on the present data relate to conditions of acute environmental stress. In the discussion that follows, higher scores on immunity variables are taken to be indicators of better immune responding. That is, larger T-cell numbers and greater skin induration in

454

SHEA, BURTON ANI) GIRGIS

TABLE 5 EFFECTS OF ABSORPTION (LOW AND HIGH, CUTPOINT A'I' 22) AND NEUROTICISM (LOW MEDIUM AND HIGH, CUTPOtNIS AT 33 AND 48) IN ANALYSES OF COVARIANCE, USING AGE, AND CIGARETTES SMOKED AS COVARIATES, AND T-CELL AND INDURATION MEASURES AS DEPENDENT VARIABLES Absorption

Low N

Medium N

High N

ALC

Low

1691 (n = 8)

1812(n-: 5)

2837(n : 6)

T3 Cells

High Low

2202 (n = 6) 982

1946 (n - 5) 1091

1842 (n -: 91 1745

T4 Cells

High Low

1368 571

l 199 678

1092 895

T8 Cells

High Low

700 342

684 382

684 721

Ratio T4:T8

High Low

537 1.81

452 1.88

300 1.38

Streptococcus

High Low

1.32 0.00

1.52 0.90

2.59 1.37

Tuberculin

High Low

0.10 0.38

1.30 0.80

0.44 2.90

Candida

High Low

0.07 3.00

0.90 3.40

1.28 4.52

High Low

0.92 1.90

1.90 1.89

2.56 3.40

High

0.74

2.30

2.66

Number induration response

Significant Effect AN, f 5.83 p 0.007 AN, F = 5.38 p - 0.(1099 NS

AN, F = 12.08 p = 0.0001 AN, F - 6.07 p = 0.006 N, F -- 3.56 p - 0.043 N, F-- 4.53 p = 0.0188 A, F = 8.13 p = 0.0077 N, F-= 4.54 p = 0.0186

Cell measures are the actual number of the cells named, and induration measures are given in millimetres.

response to antigens are considered to be better immunologically than smaller numbers and less induration. When the T-cell n u m b e r s for the experimental groups are compared with normative data from a similar population (Table 6) it is evident that the T4-cell n u m b e r s in the repressors group and the extreme expressors group are below the normal range

(4). T4-cell n u m b e r s are monitored as a predictor o f impending symptomatic disease in HIV positive subjects (12). Clinical disease is associated with circulating T4-cell n u m b e r s less than 400. F r o m the present results it seems reasonable to believe that the two groups in question are relatively less i m m u n o c o m p e t e n t than the other groups. The same two groups also have low T8-

TABLE 6 T

LYMPHOCYTE SUBSETS IN YOUNG FEMALES; DATA FROM PRESENT SUBJECTS, AGE 18-30" COMPARED WITH NORMATIVE DATA. AGE 16-25 (64) ALC

T3

T4

T8

4:8 Ratio

(174) (260) (346) (229)

358 (144) 630 (247) 560 (196) 309 (122)

1.71 (0.6) 1,68 (0.7) 1,38 (0.3) 2,32 (1.03)

969 (321) 1185 (320)

564 (201) 623 (146)

1.90 (0.5) 1.90 (0,5)

Present Study Low A/Low N Low A/Hi N Hi A/Low N Hi A/Hi N

1684 (515) 2635 (604) 2300 (923) 1760 (482)

963 (246) 1649 (447) 1466 (661) 1026 (347)

555 903 771 632

Normative Data Nonsmoker Smokers

1908 (580) 2241 (589)

1467 (543) 1862 (486)

Standard deviations are shown in parentheses. * No corrections are made for the effects of age or smoking.

NEGATIVE AFFECT, ABSORPTION, IMMUNITY

cell numbers, by comparison with the normative group, which is consistent with this conclusion. The lowest T8-cell number occurs in the extreme expressors group, and was responsible for this group having the highest T4:T8 ratio, a level considerably above the normative group. The most common explanation for such high T4:T8 ratios is the presence of intercurrent viral infection. In other words, this group might be more susceptible than others to such infection. Overall, the true negative affect group had the highest circulating T-cell numbers, which leads to the prediction that this group would be the most reactive in a T-cell challenge such as delayed type hypersensitivity tests (DHS). Thus, the T-cell data would suggest that repressors individuals would do worst in DHS tests, because of low numbers of T4and TS-cells, and that the low absorption/high neurotic group would do best, because of relatively high numbers of T4- and TS-cells. The Extreme expressors group may score higher in DHS tests than their low T-cell numbers might suggest because the high T4:T8 ratio suggests existing reaction to antigen threat. These predictions are generally borne out by the data on skin induration. The multivariate analysis of variance examines the effects of the independent variables absorption and neuroticism on the whole set of seven induration measures. A particular advantage of this analysis is that it helps to overcome the problem of possible prior exposure of some subjects to some of the test antigens. By its very nature the multivariate analysis gives an indication of the subjects' overall immune responses. If the immune response can be considered a unitary response, the reliability of the measure is increased by using several scores to contribute to an overall measure. The multivariate analysis, some of the individual analyses of covariance, and the analysis using scores from the combined set of antigens (streptococcus, tuberculin and proteus) show that the lowest induration responses to the test antigens occurs with the repressors group, and the highest responses occur with the true negative affect group. Consistent with the idea that high T4:T8 ratio may be associated with some other ongoing immune response, the extreme expressors group showed induration responses in between the extremes, but closer to the true negative affect group. The reliability that is provided by the similarity of findings from the in vitro and in vivo data suggests that the idea of relationships between personality qualities and immunity must be taken very seriously. The experimental hypothesis predicted that repressors and extreme expressors subjects would show lower immune responses than true negative affect and stable self-absorbed subjects. This prediction was founded on the notion that the first two groups are those individuals who are most likely to be deleteriously affected by environmental stressors; firstly, those who are repressors of negative emotions, and secondly, those who are extreme in their expression of such emotions. Other groups of subjects who do not fall into these extreme categories were expected to show more favourable immunity because of presumed better coping with environmental stressors. The data already noted in this discussion provide partial support for the experimental hypothesis. The subject groups assumed to be repressors and extreme expressors, showed significantly lower immune responses in many cases. Most often the extreme contrast was between these groups and the true negative affect group. At least with the T-cell data the stable self-absorbed group was usually very similar in immune response to the latter group. Analyses of the DHS data showed some effects similar to the T-cell analyses, with the extreme induration groups generally being the true negative affect subjects, who showed superior skin responses, and repressor subjects who showed inferior skin responses. However, the extreme expressors group's responses were

455

not always of the same order as those from the repressors group, generally being somewhat higher, and the stable self-absorbed group showed responses that were not of the same order as those from the true negative affect subjects, generally being considerably lower. As a consequence of these effects, significant neuroticism effects are often shown in which high neurotics appear to have superior immune responses compared to low neurotics. Clearly, some qualification of this comment is required. If it is accepted, as suggested above, that the induration response of the extreme expressors group occurs because of a higher rate of intercurrent infection, the high absorbers/high neurotics are doing relatively poorly in immunological terms, consistent with the experimental hypothesis. The pooling of the induration responses across the two high neuroticism subgroups may provide a meaningless figure in view of the very different T4:T8 ratio of the two groups. The induration response means something different for the two groups; it means greater immunocompetence for the true negative affect group, and implies less immunocompetence in the extreme expressors group. Accordingly, the only group which does not fit the predictions of the experimental hypothesis most of the time is the stable self-absorbed group. The predictions are met for this group with the T-cell data, and Table 6 shows that for the most part, their T-cell responses fall comfortably in the normal range. However, with induration responses, this group most often shows low immune responses comparable with the repressors group. It may be useful to examine this discrepancy in the context of the broader issue of the relatively poor immunity of high absorbers as a group. The greater immune responses for low absorbers with regard to induration responses to antigens was unexpected. Given findings from other research that individuals higher in private self consciousness had better health than individuals low in such self-attention (30,41 ), observations that high absorbers have better control over bodily processes that are normally under autonomic nervous system control (35), and that high hypnotisable subjects may respond immunologically more favourably to hypnosis than others (20), it might have been expected that high absorbers rather than low absorbers would have higher immune responses. Interpreting the data from the present study in the context of such other research requires the recognition that the poorer immune response of the high absorbers is largely attributable to the subgroup who are low neurotics, and the better immune response of the low absorbers is restricted almost exclusively to those who are high neurotics. Examination of the means in the 2 X 2 analyses shows that the group which stands out as different from the rest is the true negative affect group. However, it may be more useful to adopt the viewpoint that it is the relatively poor immunity of the other three groups that requires explanation. There has already been some comment about the performance of the repressor subjects, and the extreme expressor subjects. What is the explanation for the poor immune response (at least with regard to induration responses) shown by the stable self-absorbed subjects? Part of the answer may lie in the differences between the absorption scale and the private self-consciousness scale in describing individual self awareness. Although higher absorption may indicate a potential for physiological self-change, some process of positive guidance or direction (instructions, or hypnosis) may be required before this potential is fulfilled. For high absorbers, the kind of prompting that is required for them to initiate self-change in physical functions, as with the relaxation response for example, may be much more subtle than the stimuli required by low absorbers. A simple initiating instruction or a hypnotic suggestion may be quite sufficient for the high absorbers, while

456

SHEA, B U R T O N AND ( i l R ( i l S

the constant encouragement of biofeedback may be necessary for the low absorber (31,35). Just as they are more susceptible to relatively subtle guidance in the experimental situation, high absorbers may be more susceptible to either positive or negative suggestions, such as the threat of discomfort, that occur spontaneously in their life experience. That is, high absorbers may respond unfavourably to the negative cues implicit in situations of environmental stress, and show decreased i m m u n o c o m p e tenee as a result. In the present study, the acute stress of venipuncture obviously presents a situation of m a x i m u m negative expectancy. High absorbers may be susceptible to such expectancies experiencing a lowering of immunity as a consequence. Though speculative, this explanation for the unexpected lower immunity of the high absorbers in the present study is consistent with current theory about absorption. Obviously, further research is required to clarify this issue. In conclusion, with regard to the issue of relationships between NA and biological measures such as i m m u n e responses, the present study has provided an unequivocal indication of positive relationships. When extreme groups were compared, high neurotics showed better immunity than low neurotics. Exploratory analyses with low, medium, and high groups of neurotics suggested a negative relationship between neuroticism and immunity with several immune measures. Thus, the psychological variable NA is related to variation in circulating T-lymphocytes in females as are the physiological variables age, gender, pregnancy, and cigarette smoking (4). However, the effects of NA, as measured by the Willoughby Neuroticism scale, seem to be moderated by a measure of self-attention, absorption. A case can be made to explain most of the effects reported in this study in terms of stress-linked i m m u n e deficits. This argument, which maintains that environmental stress has harmful health effects in general and harmful i m m u n e effects in particular, follows the assumptions

1. that individuals who score low on the absorption measure of sell-attention, and low on a measure of ncuroticism. are actually much more vulnerable to stressful stimuli than they themselves recognise; they are actually repressing their awareness of emotional response t~ stressors, thereby exaggerating the effects on themselves of those stressors: 2. that people who score highly on both the absorption measure of self-attention and neuroticism may be seen as extreme expressors of emotion, and insofar as this is a poor way of coping with stressors, are likely to be vulnerable to their effects, and 3. individuals who fall between these extremes of self-awareness and negative affect are likely to cope better with environmental stressors, and will, therefore, show better health and immunity. While the data presented are more or less consistent with this explanation, they are not unequivocal. One of the experimental groups, high absorbers/low neurotics (stable self-absorbed) scored lower than expected on some in vivo i m m u n e measures, thereby contributing to a statistically significant overall neurotieism effect on some induration measures, rather than the predicted interaction of absorption and neuroticism. These observations suggest that the alternative theoretical position about the general protective value of high neuroticism with regard to health and i m m u n i t y (11) should not be abandoned just yet. Much more research needs to be done to clarify the characteristics of those people who have been classified into the subgroups examined in this project. However, this study has demonstrated very reliable relationships between psychological variables and i m m u n e responses and, therefore, uncovers a little further the fascinating prospect of being able to predict i m m u n i t y and perhaps even health experience on the basis of psychological examination.

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