556107 research-article2014
JIVXXX10.1177/0886260514556107Journal of Interpersonal ViolenceRomero-Martínez et al.
Article
High Immunoglobulin A Levels Mediate the Association Between High Anger Expression and Low Somatic Symptoms in Intimate Partner Violence Perpetrators
Journal of Interpersonal Violence 1–11 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/0886260514556107 jiv.sagepub.com
A. Romero-Martínez,1 M. Lila,2 S. Vitoria-Estruch,1 and L. Moya-Albiol1
Abstract It has been hypothesized that anger expression may be associated with increased salivary immunoglobulin A (sIgA) levels, which is associated with decreased somatic symptoms, and therefore anger expression may be associated with reduced somatic symptoms in intimate partner violence (IPV) perpetrators. This study tested the potential mediating effect of sIgA levels on the relationship between anger expression and respiratory and gastrointestinal symptoms in IPV perpetrators and non-violent controls. The sample consisted of IPV perpetrators (n = 19) and controls (n = 21). Saliva samples were collected for assessing sIgA levels. The State-Trait Anger Expression Inventory–2 was used to assess anger expression and the Revised version of the Somatic Symptoms Scale developed by Sandín and Chorot to measure somatic symptoms. High anger expression was associated with low levels of respiratory and gastrointestinal symptoms in IPV perpetrators
1University
of Valencia, Spain of Social Psychology, Valencia University, Spain
2Department
Corresponding Author: L. Moya-Albiol, Department of Psychobiology, University of Valencia, Avenida Blasco Ibañez, 21, 46010 Valencia, Spain. Email: [email protected]
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mediated through high sIgA levels but the same was not true for non-violent controls. This finding supports the hypothesis that for IPV perpetrators, anger expression may be physiologically and psychologically rewarding. Future research examining other immunological parameters is needed to further test this hypothesis. Such effort may illuminate why some IPV perpetrators continue to use violence against their partners. Keywords anger expression, gastrointestinal symptoms, intimate partner violence, immunoglobulin A, respiratory symptoms
Introduction Higher levels of antibodies have been described in aggressive populations, especially in adults with conduct disorders when compared with non-aggressive controls (Fetissov et al., 2006; Pajer, Rabin, & Gardner, 2002). Such findings are consistent with those obtained in non-human primates, in which aggressive individuals have been found to have stronger immune systems than non-aggressive peers (Granger, Booth, & Johnson, 2000). For this reason, high immunocompetence could be a compensatory mechanism to protect aggressive individuals, given their high risk of exposure to immune stimuli (Granger et al., 2000). Intimate partner violence (IPV) perpetrators use physical and/or psychological abuse to control their partners and obtain a dominant status (Antai, 2011). Such behaviors may contribute to improving their health at the expense of that of the battered partner (Inslicht et al., 2006), who are in a subordinate position. Furthermore, levels of immune function have been observed to increase more after arguing in couples with higher baseline hostility than those with lower baseline hostility (Kiecolt-Glaser et al., 2005). Increases in the levels of salivary immunoglobulin A (sIgA) have been observed after the induction of anger (Tsuboi et al., 2008). In line with this, in a previous study, IPV perpetrators showed higher sIgA levels than controls in response to stress, this response being modulated by anger expression and testosterone levels (Romero-Martínez, Lila, Conchell, González-Bono, & Moya-Albiol, 2014). Moreover, several studies have demonstrated that high levels of sIgA are associated with a low incidence of disease and susceptibility to upper infectious diseases such as respiratory tract and gastrointestinal infections (Jemmott & McClelland, 1989; Kalha & Sellin, 2004; McClelland, Alexander, & Marks, 1982; Rein, Atkinson, & McCraty, 1995). To our
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knowledge, however, no studies have analyzed the relationship between anger expression, sIgA levels, and respiratory and gastrointestinal symptoms in aggressive individuals, such as men convicted of IPV. To address this gap in the literature, this study tested the potential mediating effect of sIgA levels on the relationship between anger expression and respiratory and gastrointestinal somatic symptoms in aggressive individuals, specifically, IPV perpetrators. We hypothesized that high anger expression would be related to low levels of respiratory and gastrointestinal somatic symptoms in IPV perpetrators which would, in turn, be mediated by baseline sIgA levels.
Method Participants The final sample was composed of 40 healthy male volunteers: 19 IPV perpetrators and 21 control volunteers. The IPV perpetrators were recruited from the participants in the CONTEXTO psycho-educational and communitybased treatment program (mandatory for male abusers) at the Department of Social Psychology, University of Valencia. They had been sentenced to less than 2 years in prison and had no previous criminal record, and therefore received a suspended sentence on the condition that they attend this type of intervention program (Lila, Oliver, Galiana, & Gracia, 2013). Before inclusion in the study, all participants gave informed consent, having been informed that they would need to attend a total of three sessions, anthropometric measurements would be taken and a saliva sample would be collected to assess biological traits, and two questionnaires would be administered. The study was performed in accordance with the Declaration of Helsinki and approved by the University of Valencia Ethics Committee. More detailed descriptions of the program have been published previously in Romero-Martínez, González-Bono, Lila, and Moya-Albiol’s (2013) and Romero-Martínez, Lila, Sariñana-González, González-Bono, and MoyaAlbiol’s (2013) works.
Procedure Each participant attended three sessions on 3 consecutive days in the psychobiology laboratories of the University of Valencia. In the first sessions, participants were interviewed to exclude any individuals with organic diseases. The second and third sessions all took place between 4:00 and 7:00 p.m. After arriving at the laboratory, participants were taken to a room with constant lighting conditions that was sound-attenuated and temperature-controlled (21 ± 2 °C)
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where they signed informed consent forms, and anthropometric data (height and weight) were obtained. A single saliva sample was collected (for assessing sIgA levels). Finally, in the last session, participants completed the State-Trait Anger Expression Inventory–2 (STAXI-2) and Spanish Revised Somatic Symptoms Scale (ESS-R). For further details of the procedure, see Romero-Martínez, González-Bono, et al. (2013) and Romero-Martínez, Lila, et al. (2013).
Anger and Somatic Symptoms Measurements Anger expression was measured by an adapted version (Miguel-Tobal, Casado, Cano-Vindel, & Spielberger, 2001) of the STAXI-2 (Spielberger, 1999). This test is distributed into four subscales: Anger Expression Out (describing the extent to which people express their emotional experience of anger in an outwardly negative and poorly controlled manner; therefore, this anger expression may involve physical and verbal aggressive actions), Anger Expression In (measuring the extent to which people hold things in or suppress anger when they are angry), Anger Control Out (assessing the expenditure of energy to monitor and control the physical or verbal expressions of anger), and Anger Control In (measuring how often a person attempts to relax, calm down, and reduce angry feelings before he or she loses control), all rated on a 4-point Likert-type scale (1 = not at all to 4 = very much so). To reduce the number of tests, increase the effect size (and hence the power), and aid interpretation within a conceptual framework, we generated a general anger expression index (anger index). This provides an overall estimate of the person’s tendencies to express anger, and was calculated by summing the scores of the two expression subscales, subtracting the scores of the two control scales, and finally adding 36 units to avoid negative scores. The Cronbach’s alpha ranged from .67 to .89. Somatic symptoms were assessed with the ESS-R created by Sandín and Chorot (1995). This instrument explores reported symptoms over the last 2 years and is composed of 80 items. In this study, we considered Respiratory (repetitive sneezing or breathing problems during exercise?) and Gastrointestinal (diarrhea or stomach ache?) subscales. A total score for symptoms is calculated. Each scale is composed of 10 items scored on a 5-point Likert-type scale from 0 (never) to 4 (more than 5 times in the last 2 years), with reliability coefficients ranging from .79 to .84.
Immune Marker Measurements Given the large number of biological samples that needed to be taken and to avoid stress-induced variation in hormonal and immunological measurements
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produced by the venipuncture method (Kirschbaum, Kudielka, Gaab, Schommer, & Hellhammer, 1999), the biomarker was measured from saliva samples. Specifically, IgA levels were measured in saliva samples collected with a Salivette cotton dental roll (Sarstedt, Rommersdolf, Germany) held in the mouth for 2 min. The samples were frozen at −20 °C immediately after collection until analysis in the laboratory by nephelometry (BN II Nephelometer II Analyzer, Siemens Dade Behring, Marburg, Germany). In immunochemical reactions, proteins form immune complexes with specific antibodies. These complexes scatter a beam of light passed through the sample. The intensity of the light scattered at a certain wavelength is proportional to the concentration of the relevant protein in the sample. Finally, the results obtained are compared with standard concentrations. The reactant used was OSAR15 anti-IgA (N antiserum produced in rabbits by immunization, from Siemens Dade Behring, Marburg, Germany). Although the acceptable limit for the coefficient of variation for replicate measurements was fixed at 10%, the intra-and inter-assay variation coefficients obtained were 3.3% and 3.7%, respectively, and the sensitivity was 0.2 mg/dL. In addition, two trained researchers measured the salivary flow volume twice and the Cronbach’s alpha for the measures was .98. This good reliability justifies the calculation of the ratio between IgA levels and salivary flow volume.
Data Analysis After confirming the normality of the data distribution using the Kolmogorov– Smirnov test, t tests with Levene’s test for equality of variances were used to check for significant differences in age, body mass index, impulsivity, and IgA levels between groups (IPV and controls). Mediation was conducted by examining the statistical significance of the associations between the independent variable and the mediator (a path), between the mediator and dependent variable controlling for the independent variable (b path), and, finally, by computing ab cross-product. Testing ab cross-product is established as the most accurate and reliable approach to test mediation (Preacher & Hayes, 2004), as it allows calculating the significance of the difference between the total effect (c path) and the direct effect (c′ path), which represents the impact of the independent variable on the dependent variable adjusting for the effect of the mediator. First, a linear regression was conducted to test the direct association between anger index (independent variable) and somatic symptoms (respiratory and gastrointestinal; dependent variable). Next, mediation analysis was conducted to test the mediation effect of sIgA levels on the association between anger index and somatic symptoms (respiratory and gastrointestinal).
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Data analyses were performed using IBM SPSS (Version 21.0; SPSS IBM), and p ≤ .05 was considered significant. Average values are expressed as mean ± standard deviation.
Results Sample Characteristics, Anger, IgA Levels, and Somatic Symptoms IPV perpetrators did not differ significantly from controls in age (39.47 ± 3.12 and 35.81 ± 1.47; t25.75 = 1.06, p = .30, d = .41, respectively), body mass index (27.17 ± 0.80 and 27.55 ± 0.63 kg/m2; t38 = −0.377, p = .71, d = .12, respectively), or anger index (18.95 ± 2.33 and 21.57 ± 1.75; t38 = −0.912, p = .37, d = .29, respectively). Moreover, there were no significant differences between groups in sIgA (11.12 ± 2.65 and 6.81 ± 1.49 mg/dL, t28.56 = 0.190, p = .85, d = .07, for IPV perpetrators and controls, respectively). However, groups differed in ESS-R respiratory (9.26 ± 7.92 and 4.81 ± 4.46; t38 = 2.22, p = .033, d = .72) and gastrointestinal (9.00 ± 9.11 and 4.71 ± 4.15; t38 = 1.95, p = .050, d = .63) scores, with IPV perpetrators reporting higher levels of respiratory and gastrointestinal somatic symptoms than controls. Are anger expression index scores associated with respiratory and gastrointestinal somatic symptoms in IPV perpetrators? Do sIgA levels mediate this association? First, considering sIgA levels and respiratory symptoms (displayed in Figure 1a), the direct effect of anger index on sIgA levels was statistically significant (β = .82, SE = .19, p = .001), as were the direct effects of sIgA levels and of anger index on respiratory symptoms (β = −.44, SE = .18, p = .026; and β = −.42, SE = .15, p = .016, respectively). In addition, when accounting for the effect of sIgA levels, the effect of anger index on respiratory symptoms reduced to non-significant levels (β = −.06, SE = .20, p = .735). Results of the bootstrap analysis indicate that there was a mediating effect (M = −.35, SE = .12, 95% confidence interval [CI] = [−.66, −.13]). Hence, it can be concluded that the association between anger index and respiratory symptoms in IPV perpetrators was mediated by their sIgA levels. Second, considering sIgA levels and gastrointestinal symptoms (shown in Figure 1b), the significant associations were similar, namely, the direct effect of anger index on sIgA levels was also statistically significant (β = .82, SE = .19, p = .001), as were the direct effects of sIgA levels and of anger index on
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Figure 1. Anger expression as reflected in AEI (anger index) scores as a predictor of (a) ESS-R respiratory symptoms and (b) ESS-R gastrointestinal symptoms mediated by IgA levels in IPV perpetrators. Note. AEI = anger expression index; ESS-R = Spanish Revised Somatic Symptoms Scale; IgA = immunoglobulin A; IPV = intimate partner violence. *p < .05. **p < .01. ***p < .001.
gastrointestinal symptoms (β = −.48, SE = .21, p = .040 and β = −.44, SE = .19, p = .032, respectively). Likewise, when accounting for the effect of sIgA levels, the effect of anger index on gastrointestinal symptoms reduced to
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non-significant levels (β = −.05, SE = .25, p = .852). Again, results of the bootstrap analysis indicate that there was a mediating effect (M = −.40, SE = .14; 95% CI [−.69, −.12]). Hence, as with respiratory symptoms, the association between anger index and gastrointestinal symptoms in IPV perpetrators was mediated by their sIgA levels. All analyses were also carried out for controls, and there were no significant regressions between those variables.
Discussion IPV perpetrators in our study present more respiratory and gastrointestinal symptoms than controls. High anger expression was only associated with low level of respiratory and gastrointestinal symptoms in IPV perpetrators. Moreover, this relationship was mediated by sIgA levels. There were, however, no differences between groups in sIgA levels. It has been previously described that the expression of anger reduces the population of immune cells on the mucosal surfaces in the general population; this, in turn, would increase susceptibility to the onset and development of infectious diseases (Bosch, de Geus, Veerman, Hoogstraten, & Nieuw Amerongen, 2003). Nonetheless, our results in this study are not consistent with this pattern. IPV perpetrators did not differ from controls in anger expression or sIgA levels although they reported higher levels of respiratory and gastrointestinal symptoms than controls. Previous research revealed that IPV perpetrators have lower self-esteem than controls, but the imbalance between testosterone and cortisol levels, which predisposes individuals to behaving violently, increases their self-esteem and reduces their psychopathological symptoms (Romero-Martínez, González-Bono, et al., 2013). As our data indicated that anger expression mediated the inverse relationship between sIgA levels and the levels of respiratory and gastrointestinal symptoms, we hypothesize that anger expression against their partners by IPV perpetrators could benefit their mucosal immunity and, consequently, be rewarding for them. The major limitation of the study is the small sample size and the crosssectional and non-experimental design, which mean that we cannot infer causal relationships; for this reason, the findings should be considered preliminary. Further research is needed to explore these patterns in larger samples and test mediational models. Moreover, the lack of data on pro-inflammatory cytokines limits the interpretation of the interaction in the immune–endocrine network. Another limitation is that sIgA is very different in structure and function from IgA in plasma (Tomasi, 1970). For these reasons, it is important to be cautious with our interpretation of the findings. Moreover, it should be noted known that the STAXI-2 tends to asses anger
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expression in general (including IPV). For that, future studies should consider acute instruments that specifically measure the IPV to test the proposed hypothesis of our study. However, our data are novel, as no studies have examined sIgA response to psychological stress in the context of IPV, and potentially important. Moreover, it is a nonequivalent two-group design, with no random assignment. Thus, differences found in comparisons between the groups could be due to factors associated with their experiences other than IPV perpetration or it is possible that the observed results reflect a reluctance to admit symptoms rather than real differences in symptoms. Finally, to test the hypothesis of the beneficial effects of dominating a female partner through physical aggression, the effect should be explored in other contexts such as men who dominate in their social circle. In conclusion, our study reveals that sIgA levels mediate the association between high anger expression and a low level of somatic symptoms. Hence, anger expression could benefit mucosal immunity of IPV perpetrators and improve their actual and perceived health. Our hypothesis is useful to understand why IPV perpetrators may relapse into violent behavior against their partners after treatment programs, namely, it suggests that they could obtain positive benefits. In our opinion, findings from this study warrant further research to determine whether biological indicators could be used to improve IPV prevention and treatment programs. Acknowledgments The authors wish to thank the Spanish Home Office Prison Services (Instituciones Penitenciarias, Ministerio del Interior) for their cooperation in this research. They also wish to thank Sara de Andrés-García and Patricia Sariñana-González for their help with the IgA and salivary flow volume measurements. Furthermore, they are grateful to Ideas Need Communicating Language Services for improving the use of English in the article.
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interests with respect to the research, authorship, and/or publication of this article.
Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Regional Government of Valencia’s program for researchers in training (Programa VALi+d para investigadores en formación, ACIF/2011/075); the Spanish Ministry of Health, Social Services and Equality, National Drug Plan (2012/001); the Ministry of Economy and Competitiveness (PSI2011-25434); and the research groups and
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networks of excellence of the Committee for Business, Research and Science of the Regional Government of Valencia (PROMETEO/2011/048; ISIC/2013/001).
References Antai, D. (2011). Controlling behavior, power relations within intimate relationships and intimate partner physical and sexual violence against women in Nigeria. BMC Public Health, 29, 11-511. Bosch, J. A., de Geus, E. J., Veerman, E. C., Hoogstraten, J., & Nieuw Amerongen, A. V. (2003). Innate secretory immunity in response to laboratory stressors that evoke distinct patterns of cardiac autonomic activity. Psychosomatic Medicine, 65, 245-258. Fetissov, S. O., Hallman, J., Nilsson, I., Lefvert, A. K., Oreland, L., & Hökfelt, T. (2006). Aggressive behavior linked to corticotropin-reactive autoantibodies. Biological Psychiatry, 60, 799-802. Granger, D. A., Booth, A., & Johnson, D. R. (2000). Human aggression and enumerative measures of immunity. Psychosomatic Medicine, 62, 583-590. Inslicht, S. S., Marmar, C. R., Neylan, T. C., Metzler, T. J., Hart, S. L., Otte, C., . . . Baum, A. (2006). Increased cortisol in women with intimate partner violencerelated posttraumatic stress disorder. Annals of the New York Academy of Sciences, 1071, 428-429. Jemmott, J. B., III, & McClelland, D. C. (1989). Secretory IgA as a measure of resistance to infectious disease: Comments on Stone, Cox, Valdimarsdottir, and Neale. Behavioral Medicine, 15, 63-71. Kalha, I., & Sellin, J. H. (2004). Common variable immunodeficiency and the gastrointestinal tract. Current Gastroenterology Reports, 6, 377-383. Kiecolt-Glaser, J. K., Loving, T. J., Stowell, J. R., Malarkey, W. B., Lemeshow, S., Dickinson, S. L., & Glaser, R. (2005). Hostile marital interactions, proinflammatory cytokine production, and wound healing. Archives of General Psychiatry, 62, 1377-1384. Kirschbaum, C., Kudielka, B. M., Gaab, J., Schommer, N. C., & Hellhammer, D. H. (1999). Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosomatic Medicine, 61, 154-162. Lila, M., Oliver, A., Galiana, L., & Gracia, E. (2013). Predicting success indicators of an intervention programme for convicted intimate-partner violence offenders: The Contexto Programme. European Journal of Psychology Applied to Legal Context, 5, 73-95. McClelland, D. C., Alexander, C., & Marks, E. (1982). The need for power, stress, immune function, and illness among male prisoners. Journal of Abnormal Psychology, 91, 61-70. Miguel-Tobal, J. J., Casado, M., Cano-Vindel, A., & Spielberger, C. D. (2001). Adaptación española del Inventario de Expresión de Ira Estado-Rasgo STAXI-II [The Spanish version of the State-Trait Anger Expression Inventory, STAXI-2]. Madrid, Spain: Tea Ediciones.
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Pajer, K., Rabin, B., & Gardner, W. (2002). Increased IgG 3:4 ratios in adolescent antisocial females: Evidence of Th1/Th2 imbalance? Brain, Behavior, and Immunity, 16, 747-756. Preacher, K. J., & Hayes, A. F. (2004). SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behavior Research Methods, Instruments, & Computers, 36, 717-731. Rein, G., Atkinson, M., & McCraty, R. (1995). The physiological and psychological effects of compassion and anger. Journal of Advancement in Medicine, 8(2), 87-105. Romero-Martínez, A., González-Bono, E., Lila, M., & Moya-Albiol, L. (2013). Testosterone/cortisol ratio in response to acute stress: A possible marker of risk for marital violence. Social Neuroscience, 8, 240-247. Romero-Martínez, A., Lila, M., Conchell, R., González-Bono, E., & Moya-Albiol, L. (2014). Immunoglobulin A response to acute stress in intimate partner violence perpetrators: The role of anger expression-out and testosterone. Biological Psychology, 96, 66-71. Romero-Martínez, A., Lila, M., Sariñana-González, P., González-Bono, E., & MoyaAlbiol, L. (2013). High testosterone levels and sensitivity to acute stress in perpetrators of domestic violence with low cognitive flexibility and impairments in their emotional decoding process: A preliminary study. Aggressive Behavior, 39, 355-369. Sandín, B., & Chorot, P. (Eds.). (1995). Escala de síntomas somáticos revisada (ESS-R) [Somatic Symptoms Scale Revised]. Madrid, Spain: Universidad Nacional de Educación a Distancia. Spielberger, C. D. (1999). Manual for the State-Trait Anger Expression Inventory–2. Odessa, FL: Psychological Assessment Resources. Tomasi, T. B., Jr. (1970). Structure and function of mucosal antibodies. Annual Review of Medicine, 21, 281-298. Tsuboi, H., Hamer, M., Tanaka, G., Takagi, K., Kinae, N., & Steptoe, A. (2008). Responses of ultra-weak chemiluminescence and secretory IgA in saliva to the induction of angry and depressive moods. Brain, Behavior, and Immunity, 22, 209-214.
Author Biographies A. Romero-Martínez is a neuroscience PhD at the Department of Psychobiology, Valencia University (Spain). M. Lila is a full professor at the Department of Psychobiology, Valencia University (Spain). S. Vitoria-Estruch is a neuroscience PhD student at the Department of Psychobiology, Valencia University (Spain). L. Moya-Albiol is a full professor at the Department of Psychobiology, Valencia University (Spain).
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JIVXXX10.1177/0886260514556107Journal of Interpersonal ViolenceRomero-Martínez et al.
Article
High Immunoglobulin A Levels Mediate the Association Between High Anger Expression and Low Somatic Symptoms in Intimate Partner Violence Perpetrators
Journal of Interpersonal Violence 1–11 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/0886260514556107 jiv.sagepub.com
A. Romero-Martínez,1 M. Lila,2 S. Vitoria-Estruch,1 and L. Moya-Albiol1
Abstract It has been hypothesized that anger expression may be associated with increased salivary immunoglobulin A (sIgA) levels, which is associated with decreased somatic symptoms, and therefore anger expression may be associated with reduced somatic symptoms in intimate partner violence (IPV) perpetrators. This study tested the potential mediating effect of sIgA levels on the relationship between anger expression and respiratory and gastrointestinal symptoms in IPV perpetrators and non-violent controls. The sample consisted of IPV perpetrators (n = 19) and controls (n = 21). Saliva samples were collected for assessing sIgA levels. The State-Trait Anger Expression Inventory–2 was used to assess anger expression and the Revised version of the Somatic Symptoms Scale developed by Sandín and Chorot to measure somatic symptoms. High anger expression was associated with low levels of respiratory and gastrointestinal symptoms in IPV perpetrators
1University
of Valencia, Spain of Social Psychology, Valencia University, Spain
2Department
Corresponding Author: L. Moya-Albiol, Department of Psychobiology, University of Valencia, Avenida Blasco Ibañez, 21, 46010 Valencia, Spain. Email: [email protected]
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mediated through high sIgA levels but the same was not true for non-violent controls. This finding supports the hypothesis that for IPV perpetrators, anger expression may be physiologically and psychologically rewarding. Future research examining other immunological parameters is needed to further test this hypothesis. Such effort may illuminate why some IPV perpetrators continue to use violence against their partners. Keywords anger expression, gastrointestinal symptoms, intimate partner violence, immunoglobulin A, respiratory symptoms
Introduction Higher levels of antibodies have been described in aggressive populations, especially in adults with conduct disorders when compared with non-aggressive controls (Fetissov et al., 2006; Pajer, Rabin, & Gardner, 2002). Such findings are consistent with those obtained in non-human primates, in which aggressive individuals have been found to have stronger immune systems than non-aggressive peers (Granger, Booth, & Johnson, 2000). For this reason, high immunocompetence could be a compensatory mechanism to protect aggressive individuals, given their high risk of exposure to immune stimuli (Granger et al., 2000). Intimate partner violence (IPV) perpetrators use physical and/or psychological abuse to control their partners and obtain a dominant status (Antai, 2011). Such behaviors may contribute to improving their health at the expense of that of the battered partner (Inslicht et al., 2006), who are in a subordinate position. Furthermore, levels of immune function have been observed to increase more after arguing in couples with higher baseline hostility than those with lower baseline hostility (Kiecolt-Glaser et al., 2005). Increases in the levels of salivary immunoglobulin A (sIgA) have been observed after the induction of anger (Tsuboi et al., 2008). In line with this, in a previous study, IPV perpetrators showed higher sIgA levels than controls in response to stress, this response being modulated by anger expression and testosterone levels (Romero-Martínez, Lila, Conchell, González-Bono, & Moya-Albiol, 2014). Moreover, several studies have demonstrated that high levels of sIgA are associated with a low incidence of disease and susceptibility to upper infectious diseases such as respiratory tract and gastrointestinal infections (Jemmott & McClelland, 1989; Kalha & Sellin, 2004; McClelland, Alexander, & Marks, 1982; Rein, Atkinson, & McCraty, 1995). To our
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knowledge, however, no studies have analyzed the relationship between anger expression, sIgA levels, and respiratory and gastrointestinal symptoms in aggressive individuals, such as men convicted of IPV. To address this gap in the literature, this study tested the potential mediating effect of sIgA levels on the relationship between anger expression and respiratory and gastrointestinal somatic symptoms in aggressive individuals, specifically, IPV perpetrators. We hypothesized that high anger expression would be related to low levels of respiratory and gastrointestinal somatic symptoms in IPV perpetrators which would, in turn, be mediated by baseline sIgA levels.
Method Participants The final sample was composed of 40 healthy male volunteers: 19 IPV perpetrators and 21 control volunteers. The IPV perpetrators were recruited from the participants in the CONTEXTO psycho-educational and communitybased treatment program (mandatory for male abusers) at the Department of Social Psychology, University of Valencia. They had been sentenced to less than 2 years in prison and had no previous criminal record, and therefore received a suspended sentence on the condition that they attend this type of intervention program (Lila, Oliver, Galiana, & Gracia, 2013). Before inclusion in the study, all participants gave informed consent, having been informed that they would need to attend a total of three sessions, anthropometric measurements would be taken and a saliva sample would be collected to assess biological traits, and two questionnaires would be administered. The study was performed in accordance with the Declaration of Helsinki and approved by the University of Valencia Ethics Committee. More detailed descriptions of the program have been published previously in Romero-Martínez, González-Bono, Lila, and Moya-Albiol’s (2013) and Romero-Martínez, Lila, Sariñana-González, González-Bono, and MoyaAlbiol’s (2013) works.
Procedure Each participant attended three sessions on 3 consecutive days in the psychobiology laboratories of the University of Valencia. In the first sessions, participants were interviewed to exclude any individuals with organic diseases. The second and third sessions all took place between 4:00 and 7:00 p.m. After arriving at the laboratory, participants were taken to a room with constant lighting conditions that was sound-attenuated and temperature-controlled (21 ± 2 °C)
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where they signed informed consent forms, and anthropometric data (height and weight) were obtained. A single saliva sample was collected (for assessing sIgA levels). Finally, in the last session, participants completed the State-Trait Anger Expression Inventory–2 (STAXI-2) and Spanish Revised Somatic Symptoms Scale (ESS-R). For further details of the procedure, see Romero-Martínez, González-Bono, et al. (2013) and Romero-Martínez, Lila, et al. (2013).
Anger and Somatic Symptoms Measurements Anger expression was measured by an adapted version (Miguel-Tobal, Casado, Cano-Vindel, & Spielberger, 2001) of the STAXI-2 (Spielberger, 1999). This test is distributed into four subscales: Anger Expression Out (describing the extent to which people express their emotional experience of anger in an outwardly negative and poorly controlled manner; therefore, this anger expression may involve physical and verbal aggressive actions), Anger Expression In (measuring the extent to which people hold things in or suppress anger when they are angry), Anger Control Out (assessing the expenditure of energy to monitor and control the physical or verbal expressions of anger), and Anger Control In (measuring how often a person attempts to relax, calm down, and reduce angry feelings before he or she loses control), all rated on a 4-point Likert-type scale (1 = not at all to 4 = very much so). To reduce the number of tests, increase the effect size (and hence the power), and aid interpretation within a conceptual framework, we generated a general anger expression index (anger index). This provides an overall estimate of the person’s tendencies to express anger, and was calculated by summing the scores of the two expression subscales, subtracting the scores of the two control scales, and finally adding 36 units to avoid negative scores. The Cronbach’s alpha ranged from .67 to .89. Somatic symptoms were assessed with the ESS-R created by Sandín and Chorot (1995). This instrument explores reported symptoms over the last 2 years and is composed of 80 items. In this study, we considered Respiratory (repetitive sneezing or breathing problems during exercise?) and Gastrointestinal (diarrhea or stomach ache?) subscales. A total score for symptoms is calculated. Each scale is composed of 10 items scored on a 5-point Likert-type scale from 0 (never) to 4 (more than 5 times in the last 2 years), with reliability coefficients ranging from .79 to .84.
Immune Marker Measurements Given the large number of biological samples that needed to be taken and to avoid stress-induced variation in hormonal and immunological measurements
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produced by the venipuncture method (Kirschbaum, Kudielka, Gaab, Schommer, & Hellhammer, 1999), the biomarker was measured from saliva samples. Specifically, IgA levels were measured in saliva samples collected with a Salivette cotton dental roll (Sarstedt, Rommersdolf, Germany) held in the mouth for 2 min. The samples were frozen at −20 °C immediately after collection until analysis in the laboratory by nephelometry (BN II Nephelometer II Analyzer, Siemens Dade Behring, Marburg, Germany). In immunochemical reactions, proteins form immune complexes with specific antibodies. These complexes scatter a beam of light passed through the sample. The intensity of the light scattered at a certain wavelength is proportional to the concentration of the relevant protein in the sample. Finally, the results obtained are compared with standard concentrations. The reactant used was OSAR15 anti-IgA (N antiserum produced in rabbits by immunization, from Siemens Dade Behring, Marburg, Germany). Although the acceptable limit for the coefficient of variation for replicate measurements was fixed at 10%, the intra-and inter-assay variation coefficients obtained were 3.3% and 3.7%, respectively, and the sensitivity was 0.2 mg/dL. In addition, two trained researchers measured the salivary flow volume twice and the Cronbach’s alpha for the measures was .98. This good reliability justifies the calculation of the ratio between IgA levels and salivary flow volume.
Data Analysis After confirming the normality of the data distribution using the Kolmogorov– Smirnov test, t tests with Levene’s test for equality of variances were used to check for significant differences in age, body mass index, impulsivity, and IgA levels between groups (IPV and controls). Mediation was conducted by examining the statistical significance of the associations between the independent variable and the mediator (a path), between the mediator and dependent variable controlling for the independent variable (b path), and, finally, by computing ab cross-product. Testing ab cross-product is established as the most accurate and reliable approach to test mediation (Preacher & Hayes, 2004), as it allows calculating the significance of the difference between the total effect (c path) and the direct effect (c′ path), which represents the impact of the independent variable on the dependent variable adjusting for the effect of the mediator. First, a linear regression was conducted to test the direct association between anger index (independent variable) and somatic symptoms (respiratory and gastrointestinal; dependent variable). Next, mediation analysis was conducted to test the mediation effect of sIgA levels on the association between anger index and somatic symptoms (respiratory and gastrointestinal).
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Data analyses were performed using IBM SPSS (Version 21.0; SPSS IBM), and p ≤ .05 was considered significant. Average values are expressed as mean ± standard deviation.
Results Sample Characteristics, Anger, IgA Levels, and Somatic Symptoms IPV perpetrators did not differ significantly from controls in age (39.47 ± 3.12 and 35.81 ± 1.47; t25.75 = 1.06, p = .30, d = .41, respectively), body mass index (27.17 ± 0.80 and 27.55 ± 0.63 kg/m2; t38 = −0.377, p = .71, d = .12, respectively), or anger index (18.95 ± 2.33 and 21.57 ± 1.75; t38 = −0.912, p = .37, d = .29, respectively). Moreover, there were no significant differences between groups in sIgA (11.12 ± 2.65 and 6.81 ± 1.49 mg/dL, t28.56 = 0.190, p = .85, d = .07, for IPV perpetrators and controls, respectively). However, groups differed in ESS-R respiratory (9.26 ± 7.92 and 4.81 ± 4.46; t38 = 2.22, p = .033, d = .72) and gastrointestinal (9.00 ± 9.11 and 4.71 ± 4.15; t38 = 1.95, p = .050, d = .63) scores, with IPV perpetrators reporting higher levels of respiratory and gastrointestinal somatic symptoms than controls. Are anger expression index scores associated with respiratory and gastrointestinal somatic symptoms in IPV perpetrators? Do sIgA levels mediate this association? First, considering sIgA levels and respiratory symptoms (displayed in Figure 1a), the direct effect of anger index on sIgA levels was statistically significant (β = .82, SE = .19, p = .001), as were the direct effects of sIgA levels and of anger index on respiratory symptoms (β = −.44, SE = .18, p = .026; and β = −.42, SE = .15, p = .016, respectively). In addition, when accounting for the effect of sIgA levels, the effect of anger index on respiratory symptoms reduced to non-significant levels (β = −.06, SE = .20, p = .735). Results of the bootstrap analysis indicate that there was a mediating effect (M = −.35, SE = .12, 95% confidence interval [CI] = [−.66, −.13]). Hence, it can be concluded that the association between anger index and respiratory symptoms in IPV perpetrators was mediated by their sIgA levels. Second, considering sIgA levels and gastrointestinal symptoms (shown in Figure 1b), the significant associations were similar, namely, the direct effect of anger index on sIgA levels was also statistically significant (β = .82, SE = .19, p = .001), as were the direct effects of sIgA levels and of anger index on
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Figure 1. Anger expression as reflected in AEI (anger index) scores as a predictor of (a) ESS-R respiratory symptoms and (b) ESS-R gastrointestinal symptoms mediated by IgA levels in IPV perpetrators. Note. AEI = anger expression index; ESS-R = Spanish Revised Somatic Symptoms Scale; IgA = immunoglobulin A; IPV = intimate partner violence. *p < .05. **p < .01. ***p < .001.
gastrointestinal symptoms (β = −.48, SE = .21, p = .040 and β = −.44, SE = .19, p = .032, respectively). Likewise, when accounting for the effect of sIgA levels, the effect of anger index on gastrointestinal symptoms reduced to
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non-significant levels (β = −.05, SE = .25, p = .852). Again, results of the bootstrap analysis indicate that there was a mediating effect (M = −.40, SE = .14; 95% CI [−.69, −.12]). Hence, as with respiratory symptoms, the association between anger index and gastrointestinal symptoms in IPV perpetrators was mediated by their sIgA levels. All analyses were also carried out for controls, and there were no significant regressions between those variables.
Discussion IPV perpetrators in our study present more respiratory and gastrointestinal symptoms than controls. High anger expression was only associated with low level of respiratory and gastrointestinal symptoms in IPV perpetrators. Moreover, this relationship was mediated by sIgA levels. There were, however, no differences between groups in sIgA levels. It has been previously described that the expression of anger reduces the population of immune cells on the mucosal surfaces in the general population; this, in turn, would increase susceptibility to the onset and development of infectious diseases (Bosch, de Geus, Veerman, Hoogstraten, & Nieuw Amerongen, 2003). Nonetheless, our results in this study are not consistent with this pattern. IPV perpetrators did not differ from controls in anger expression or sIgA levels although they reported higher levels of respiratory and gastrointestinal symptoms than controls. Previous research revealed that IPV perpetrators have lower self-esteem than controls, but the imbalance between testosterone and cortisol levels, which predisposes individuals to behaving violently, increases their self-esteem and reduces their psychopathological symptoms (Romero-Martínez, González-Bono, et al., 2013). As our data indicated that anger expression mediated the inverse relationship between sIgA levels and the levels of respiratory and gastrointestinal symptoms, we hypothesize that anger expression against their partners by IPV perpetrators could benefit their mucosal immunity and, consequently, be rewarding for them. The major limitation of the study is the small sample size and the crosssectional and non-experimental design, which mean that we cannot infer causal relationships; for this reason, the findings should be considered preliminary. Further research is needed to explore these patterns in larger samples and test mediational models. Moreover, the lack of data on pro-inflammatory cytokines limits the interpretation of the interaction in the immune–endocrine network. Another limitation is that sIgA is very different in structure and function from IgA in plasma (Tomasi, 1970). For these reasons, it is important to be cautious with our interpretation of the findings. Moreover, it should be noted known that the STAXI-2 tends to asses anger
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expression in general (including IPV). For that, future studies should consider acute instruments that specifically measure the IPV to test the proposed hypothesis of our study. However, our data are novel, as no studies have examined sIgA response to psychological stress in the context of IPV, and potentially important. Moreover, it is a nonequivalent two-group design, with no random assignment. Thus, differences found in comparisons between the groups could be due to factors associated with their experiences other than IPV perpetration or it is possible that the observed results reflect a reluctance to admit symptoms rather than real differences in symptoms. Finally, to test the hypothesis of the beneficial effects of dominating a female partner through physical aggression, the effect should be explored in other contexts such as men who dominate in their social circle. In conclusion, our study reveals that sIgA levels mediate the association between high anger expression and a low level of somatic symptoms. Hence, anger expression could benefit mucosal immunity of IPV perpetrators and improve their actual and perceived health. Our hypothesis is useful to understand why IPV perpetrators may relapse into violent behavior against their partners after treatment programs, namely, it suggests that they could obtain positive benefits. In our opinion, findings from this study warrant further research to determine whether biological indicators could be used to improve IPV prevention and treatment programs. Acknowledgments The authors wish to thank the Spanish Home Office Prison Services (Instituciones Penitenciarias, Ministerio del Interior) for their cooperation in this research. They also wish to thank Sara de Andrés-García and Patricia Sariñana-González for their help with the IgA and salivary flow volume measurements. Furthermore, they are grateful to Ideas Need Communicating Language Services for improving the use of English in the article.
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interests with respect to the research, authorship, and/or publication of this article.
Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Regional Government of Valencia’s program for researchers in training (Programa VALi+d para investigadores en formación, ACIF/2011/075); the Spanish Ministry of Health, Social Services and Equality, National Drug Plan (2012/001); the Ministry of Economy and Competitiveness (PSI2011-25434); and the research groups and
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networks of excellence of the Committee for Business, Research and Science of the Regional Government of Valencia (PROMETEO/2011/048; ISIC/2013/001).
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Author Biographies A. Romero-Martínez is a neuroscience PhD at the Department of Psychobiology, Valencia University (Spain). M. Lila is a full professor at the Department of Psychobiology, Valencia University (Spain). S. Vitoria-Estruch is a neuroscience PhD student at the Department of Psychobiology, Valencia University (Spain). L. Moya-Albiol is a full professor at the Department of Psychobiology, Valencia University (Spain).
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