- Email: [email protected]
Saliva testosterone and criminal violence among women
Person. individ. Diz
0191-8869 88 53.00+ 0.00 PergamonPressplc
Vol. 9. No. 2, pp. 269-275, 1988
Rimedin GreatBritain
SALIVA TESTOSTERONE AND CRIMINAL AMONG WOMEN JAMESM. DABBSJR,’ R.
BARRY RUBACK,’
ROBERT L. FRADY,’
and DEMETRIOSS.
VIOLENCE
CHARLES H. HOPPER’
SGO~TAS’
‘Department of Psychology, Georgia State University, University Plaza, Atlanta, GA 30303, Diagnostic Unit, Georgia Industrial Institute, Alto, GA 30596 and ‘Department of Pathology and Laboratory Medicine, Emory University, Atlanta, GA 30322, U.S.A. (Received
8 Muy
1987)
Summary-Free testosterone concentrations were measured in the saliva of 84 female inmates and 15 female college students. Testosterone differed among inmates convicted of unprovoked violence,defensive violence, theft, drugs, and a set of other crimes. It was highest with unprovoked violence and lowest with defensive violence, where inmates had reacted violently after being physically assaulted. Testosterone was also related to number of prior charges and to Parole Board decisions about length of time to serve before being released on parole. Mean testosterone levels were similar for inmates and college students.
INTRODUCTION
Testosterone is the principal male sex hormone, affecting sexual development in urero and during adolescence (Kandel and Schwartz, 1981). Throughout life it affects the functioning of numerous organ systems in both sexes (Kupperman, 1965). Its physical effects are both anabolic (high lean-fat ratios) and masculinizing (baldness, body hair, low voice pitch). It is also related to behavior, especially involving sex and aggression. In studies of male animals and human beings, testosterone has been related to libido (Kupperman, 1965), activity level (Broverman, Klaiber, Kobaysahi and Vogel, 1968), persistence at goal-directed behaviors (Andrew and Rogers, 1972; Archer, 1977), sensation seeking (Daitzman and Zuckerman, 1980), intolerance of frustration (Olweus, 1983), dominance (Mazur, 1985), and positive affect (Dabbs and Ruback, 1987). Testosterone affects behavior and in turn is affected by experience. It rises in male monkeys who win fights (Bernstein, Rose and Gordon, 1974) and men who win wrestling or tennis matches (Elias, 1981; Mazur and Lamb, 1980), and it drops in male monkeys who lose fights (Bernstein et al., 1974). Women have less testosterone than men, but its effects are much the same. Experimental administration of testosterone to women increases interest in sex (Sherwin, Gelfand and Brender, 1985), and frequency of sexual activity in married couples is correlated with the females’ characteristic testosterone levels (Morris, Udry, Kahn-Dawood and Dawood, 1987). Among women, testosterone levels have been associated with a friendly sociability (Persky, Lief, Strauss, Miller and O’Brien, 1978), and an adrenal precursor of testosterone (DHEA-S) has been associated with an expansive personality (Hermida, Halberg and de1 Pozo, 1985). Testosterone has also been related to personality characteristics of masculinity and femininity (Baucom, Besch and Callahan, 1985). Serum testosterone is reportedly higher among female students and professional, managerial, and technical workers than among clerical workers and housewives (Purifoy and Koopmans, 1979). Similarly, saliva testosterone is higher among female lawyers than among athletes, teachers and nurses (Schindler, 1979). Several studies have related testosterone to criminal violence among men (Dabbs, Frady, Carr and Besch, 1987; Ehrenkranz, Bliss and Sheard, 1974; Kreuz and Rose, 1972), and the present study extends this work to women. Women commit less violent crime than men do, but women who commit violent crimes may have more testosterone than those who do not. Such a finding would not imply a necessary tie between violence and testosterone, because a person could be high in testosterone and not violent, but it would suggest that testosterone sometimes contributes to violent behavior in both sexes. Most studies of testosterone have involved serum assays, which require the drawing of blood by medical personnel, and sample sizes have tended to be small. Saliva measurements are well suited to behavioral studies, because they are easy to obtain and reliable. In serum, most testosterone is 269
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bound to sex hormone binding globulin. Only a small percentage remains ‘free’ and thus biologically active, which means it is able to enter target cells and bind with specific receptors throughout the body (Vermeulen and Verdonck, 1972). Only the free testosterone can pass through the saliva glands (Vining and McGinley, 1984), and as a result there is a high correlation between concentrations of saliva testosterone and serum free testosterone (Vittek, L’Hommedieu, Gordon, Rappaport and Southren, 1985).
METHOD Testosterone measures Data collection. Subjects were 84 female inmates in a state prison and 15 female undergraduate college students. The inmates had been recently admitted and were housed in a diagnostic unit where all inmates spend their first month. Saliva samples were collected in group sessions of 20-25 inmates, held between 3:00 and 4:00 p.m. on 2 days a month apart, in April and May of 1986. About 12 inmates declined to participate, and saliva samples from two others were too small to assay. The college students participated as part of a course requirement. Their samples were collected in group sessions of 3-5 students, held at 10:00 a.m. on several days in April and May. No students declined to participate. Subjects rinsed their mouths with water before the session. The nature of testosterone and the purpose of the study was explained, and subjects were given consent forms to sign. Included with the consent forms were questions on age, number of children, and menstrual cycle history. Subjects were asked to write down any other information they thought might be relevant to reproductive function (e.g. hysterectomy). Each subject was given 20-ml polyethylene vial with a serial number of the cap. Subjects collected saliva in their mouths and deposited it into the vial, filling the vial to a 5-ml mark on the side. Subjects remained together in their group for l&15 min, until all had finished. Radioimmunoassays. Saliva samples were frozen and delivered to the Department of Pathology and Laboratory Medicine at Emory University. Radioimmunoassay (RIA) was performed using a commercial kit for serum testosterone from Leeco Diagnostics (Southfield, MI 48075). The antiserum was raised in rabbits against testosterone-3-(O-carboxymethyl)oxime-bovine serum albumin. Cross reaction is significant (16%) only with 5cr-dihydrotestosterone; other steroids give less than 2% cross reaction. The tracer was a testosterone-3-[‘251]iodohistamine ligand (sp. act. 2000 Ci/mmol). The Leeco kit and method were modified and optimized for saliva testosterone as follows. Standards in the kit were diluted with phosphate buffer to yield an assay range of 1400 pg/ml. Saliva was heated for 30 min at 55°C and then centrifuged to remove debris, and 0.5 ml volumes were mixed in tubes with equal volumes of water and extracted with 5 ml diethyl ether. For optimum extraction (95-98% recovery), the tubes were shaken for 5 min at high speed on a multivortex shaker. The aqueous phase was frozen by immersing the tubes in an ethanol-solid CO, mixture. The ether extract (the organic phase) was decanted into new tubes, and 4-ml volumes of the ether extract were transferred into appropriate RIA tubes. The ether was then evaporated under nitrogen in a warm water bath. When dry, the RIA tubes received 0.05 ml tracer, 0.1 ml antiserum diluted 3-fold with phosphate buffer, and 0.1 ml phosphate saline buffer. The mixture was incubated at room temperature overnight, and 0.5 ml of precipitating reagent antiserum diluted 2-fold with phosphate buffer was added. The mixture was centrifuged at 4°C for 30min. The supematant was decanted and the precipitate counted in a gamma counter. Sensitivity of the assay, defined as the quantity of unlabeled hormone required to inhibit binding of the tracer by an amount equal to 2 SD, as compared with inhibition in the absence of unlabeled hormone, was determined to be 5 fmol. Accuracy of the assay was estimated by adding testosterone standards to female saliva treated with charcoal to remove testosterone. When the saliva was extracted and treated as above,, the results were indistinguishable from what would be expected in the absence of saliva. For quality control purposes, duplicate assays were performed on each sample, and the coefficient of variation (CV: the standard deviation expressed as a percent of the mean) between
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duplicates was computed. Laboratory personnel did not know whether samples came from inmates or students. Samples were assayed a second time, again in duplicate, whenever the initial CV was greater than 25% or when laboratory personnel judged the results questionable for any reason. Where the CV did not improve markedly from the first to the second assay, the combined mean of the duplicates for both assays was taken as the subject’s score. The testosterone score for each subject was reported in units of nanograms per 100 milliliters (ng/lOO ml). Mean CV for the 99 samples was 8.8%. Stability of individual d&zrences. The present work employed a single measure of saliva testosterone from each inmate. Reliability is known to be high for single measurements of serum testosterone from male subjects, about r = 0.80 (Dai, I&Her, LaPorte, Gutai, Falvo-Gerard and Caggiula, 1981; Olweus, 1983). We assumed reliability would be lower for saliva measurements from females, because female saliva testosterone levels are so low as to approach the limits of assay sensitivity, but we did not know exactly what the reliability would be. We subsequently assayed saliva samples collected on 2 days from 22 male and 25 female students participating in a panel study at the University of North Carolina (Latane, 1987), finding reliability to be r = 0.79 for males and r = 0.51 for females. Based upon these data, we think reliability in the present study was about r = 0.50. Reliability was sufficiently high to reveal a number of significant relationships, as described below. For further research with female subjects, however, we suggest scores be based on the mean of two or three saliva samples. Applying the Spearman-Brown formula, reliability of r = 0.50 for a single measurement will increase to r = 0.67 for the mean of two measurements and to r = 0.75 for the mean of three measurements. Behavioral
data
The study focused upon each inmate’s current crime, but we also examined prior criminal charges, behaviour in prison, and Parole Board decisions about parole. This information was obtained from Department of Corrections computer files and Parole Board computer and paper files. Current crime. Because the study was an extension of earlier work on criminal violence in male inmates, our primary focus was on whether or not each inmate was currently incarcerated for a violent crime. Department of Corrections computer records indicated the crime for which each inmate was convicted, but sometimes persons commit violent crimes and are convicted of nonviolent crimes (usually through plea bargaining; e.g. assault might lead to a “reckless conduct” conviction). Parole Board records included a narrative description of the crime in a post-sentence investigation report in each inmate’s paper file. We determined the exact nature of each inmate’s current crime from this post-sentence investigation. Criminal history. Criminal histories are often confusing. A single conviction can lead to probation, probation violation, incarceration, parole, parole violation, and incarceration again. Legal records are scattered among jurisdictions. Parole Board personnel examine court records in countries where each subject has resided, and a list of all prior charges is included in each inmate’s post-sentence investigation. Parole Board files contained Post-Sentence Investigations for 8 1 of the 84 inmates. For each inmate we counted the total number of charges, including the current one, except that when the same charge appeared more than once it was counted only once. The same inmate might have charges as diverse as forgery, assault, and drug sale, or as similar as forged check and bad check, or marijuana sale and cocaine sale. We considered coding schemes that would simplify the list, such as grouping charges into four categories (person, property, drugs and other), but these coding schemes appeared to add no useful information beyond that given by the number of charges alone. Behavior in prison. Disciplinary reports for infractions in prison are placed in each inmate’s paper file and are also coded and entered into computer records of the Department of Corrections. These records show the infraction that took place and the punishment for it. Approximately 8 months after the saliva samples had been collected, we examined these computer records for each inmate and counted the total number of infractions, number of infractions involving assaultive behavior, and punishments received for the infractions. Parole Board treatment. Finally, we examined Parole Board recommendations on how much time each inmate was to serve before being released on parole. The Parole Board uses a Decision
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Guidelines grid that summarizes in an objective fashion the severity of each crime and the likelihood of recidivision. The Guidelines recommend a length of time in prison that ranges from 4 to 102 months. Parole Board members also examine cases individually, and they sometimes depart from Guidelines recommendations to increase or decrease the length of time an inmate must serve. Such departures usually indicate aggravating or mitigating circumstances, extensive criminal history, medical problems, or, less frequently, misbehavior in prison. We assigned a score of - 1, 0, or + 1 to indicate whether the Parole Board gave each inmate less, the same, or more time than the Guidelines recommendation. This score could be regarded as a measure of “Parole Board severity.” RESULTS Subjects
Inmates ranged in age from 17 to 66 years (median age 28). Six had hysterectomies, one had an ovariectomy, and two were pregnant. Of the remainder, among those below age 40, 10% reported not having regular menstrual cycles. Students ranged in age from 18 to 26 (median age 18), and all reported having regular menstrual cycles. Testosterone
scores
Overall mean testosterone concentration was 2.18 ng/lOO ml. The difference between prison inmates (Mean = 2.17, SD = 0.83) and college students (Mean = 2.21, SD = 0.58) was not significant (t < 1). These mean scores are within the normal range for female subjects. In a previous unpublished study employing the same assay procedure as used here, D. Sgoutas obtained values of 2.45 (SD = 0.41) for 20 women with regular menstrual cycles and 2.50 (SD = 0.42) for 12 post-menopausal women. Current
crime
The 84 current crimes fell into four categories: violent (20), theft (40), drugs (14) and other (10). Violent crimes included homicide, assault, and robbery. Theft primarily included shoplifting, forgery, and bad checks. Drug crimes involved use of or trafficking in drugs or alcohol, The “other” category included crimes that are relatively infrequent among women, such as arson, firearms possession, burglary, running a gambling operation, and hindering apprehension of a felon. Initial analysis did not show inmates convicted of violent crimes to be significantly higher than other inmates in mean testosterone (t < l), However, perusal of the data revealed 13 inmates in the violent group above the prison median in testosterone, one at the median, and six below the median (P < 0.10 by sign test). Some of the inmates below the median were extremely low in testosterone. Descriptions of the circumstances of each crime showed the violent acts of five inmates had been in response to physical provocation. Two of these women were battered wives who killed their husbands, and three had retaliated against lovers or acquaintances who had attacked them. These five “defensive violent” inmates were significantly lower in testosterone than their remaining 15 “unprovoked violent” inmates, t (18) = 3.05, P < 0.01. We kept this distinction between unprovoked violence and defensive violence in the analyses that follow. Mean testosterone scores among inmates are summarized in Table 1. The overall difference among the five groups in the table was significant, F(4,79) = 3.82, P < 0.01. A Tukey multiple range test showed differences between specific groups, as summarized in the table. The unprovoked violent group was significantly higher than the defensive violent and theft groups. Table I. Mean testosterone concentrations (ng/lOil ml) among inmates convicted of five tytxs of crime Defensive Violent (n = 5)
Theft (n =40)
Drugs (n = 14)
Other (n = 10)
Unprovoked Violent (n = 15)
1.48
1.94
2.31
2.47
2.63
Note: Groups that do not share a common underline are significantly different from one another (P < 0.05) by Tukey test.
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Criminal history
The overall correlation between testosterone and number of charges did not reach significance, df = 80, P < 0.10. This correlation could be affected by crime type differences in testosterone or in number of charges. To control for this possibility, we computed the pooled within-group correlation, treating each score as a deviation from the mean for its crime type. The resulting pooled within-group correlation was significant (r = 0.27, df = 76, P < 0.05).
r = 0.20,
Behavior in prison
There was no apparent relationship between testosterone levels and disciplinary infractions. The total number of infractions was relatively low. Twenty-six of the 84 inmates had received reports for infractions of prison rules, and 13 of these had received punishment (isolation). Only 9 inmates had behaved in an assaultive manner in prison. Parole Board treatment
Parole Board computer records were checked eight months after collecting saliva samples. At this time, “Parole Board severity” scores were available on 54 inmates, showing whether the Board assigned less, the same, or more time than recommended by the Decision Guidelines. The remaining inmates had been released before being reviewed or were not scheduled for review by the Parole Board. The scores were correlated positively with inmates’ testosterone levels (r = 0.34, 53 df, P c 0.05). As with criminal history, we also computed the pooled within-groups correlation, which was significant (r = 0.27, df = 49, P < 0.05). For inmates whose testosterone concentrations were higher than average, the Parole Board tended to assign longer times to serve than provided by the Decision Guidelines. DISCUSSION As with men, women’s saliva testosterone concentrations were related to criminal violence, although the pattern was more complicated with women. Violent crimes among women included both unprovoked violence and defensive violence, typified by abused wives who killed their husbands. Defensive violence may be especially common among women; Browne and Flewelling (1986) argue that women who kill do so primarily in response to some kind of threat. Testosterone was lowest in defensive violence and highest in unprovoked violence. Testosterone also differed with other kinds of crime, being low in theft and high in drug offenses and a miscellaneous set of crimes atypical of women. Defensive violence was relatively rare in our sample, which limits to some extent our confidence regarding its link to low testosterone. However, low testosterone in physically abused women is reminiscent of low testosterone found in male rhesus monkeys defeated in fights (Bernstein et al., 1974). We do not know how subject’s testosterone levels might have changed in the past. Physical abuse could have led to lower testosterone, or lower testosterone could have increased the likelihood these women would be abused. Male serum testosterone levels are heritable, with correlations reported of r = 0.50 between fraternal twins and r = 0.69 between identical twins (Turner, Ford, West and Meikle, 1986), implying some stability within individuals. On the other hand, testosterone changes with experience, and levels can rise markedly within a few minutes (Hellhammer et al., 1985). We do not know how much chronic testosterone levels change with experience over periods of months or years. The issue might be pursued among women who are abused and then removed to safer surroundings, to see whether their testosterone is initially low and gradually moves to higher levels. The findings on defensive violence might appear at variance with those of Olweus (1983), who reported higher testosterone among subjects who engaged in defensive (which he called “provoked”) aggression. But Olweus worked with normal high school students, and he used “provoked” to refer to cases where subjects reacted against being frustrated or restricted. Using his frame of reference, most of our inmates might have been frustrated or restricted and therefore “provoked” to violence, either by persons or by circumstances. We have limited the term “defensive” to describe more extreme cases of reaction against physical attack. Perhaps high levels of testosterone stimulate subjects to resist frustration and mild provocation, as described by
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Olweus, while response to extreme physical provocation may be explained better by something other than high testosterone. Disciplinary infractions in prison were not related to testosterone concentrations. This may be partly because female inmates, in comparison to males, commit relatively few disciplinary infractions. But even among male inmates testosterone has not been clearly related to behavior in prison (Rose, 1978). In the present study, the total number of different charges in an inmate’s history reflected both amount and diversity of illegal activity, and this score was correlated with testosterone concentration. Inmates high in testosterone received more time in prison than called for by the Parole Board Decision Guidelines. This Parole Board treatment, as indicated above, may reflect more aggravating circumstances about the offenses and more extensive criminal histories among these women; women higher in testosterone did tend to have more charges in their histories. In this regard, Gillespie (1986) has noted that female inmates are more likely to be executed if they exhibit inappropriate sex role behavior in addition to committing the crime. One might expect more inappropriate sex role behavior from women who are high in testosterone. An explanation based upon testosterone would not diminish the injustice involved if women are being punished for behaving differently than other women. But it would raise the question of whether the punishment is actually for out-of-role behavior or more simply for extreme stereotypical “masculine” behavior. The present findings, along our earlier study of male prison inmates (Dabbs er al., 1987), suggest the Parole Board does not react favorably to inmates who are high in testosterone, regardless of whether the inmates are male or female. The present emphasis upon criminal violence should not distort our perspective on testosterone. Testosterone, as reviewed in the introduction, has effects on mood. behavior, and even cognitive processes that can be quite positive. The prison population represents a small minority of all men and an even smaller minority of all women. It may be that testosterone has more negative effects among women than among men; Vogel, Klaiber and Broverman (1978) reported testosterone levels three times higher among depressed than among normal women. But testosterone could have one effect in a context of frustration, hostility, and violence and another effect where there is opportunity, friendliness, and achievement. We need to understand the fundamental psychological and behavioral dimensions associated with testosterone and the factors that cause testosterone to have different effects in different conditions. wish to thank the Georgia Department of Corrections and the Georgia Board of Pardons and Paroles for making this research possible. In addition, we specifically extend thanks to Kathy Barry, Gary Black, Tim Carr and Ray Roberson (Department of Corrections) and to Sue Aiken, Tom Morris and Sheila Tyson (Board of Pardons and Paroles). We are indebted to Mary Richter and Laura Salter for coding inmate records and to Claire Anderson for performing the radioimmunoassays.
Acknowledgements-We
REFERENCES Andrew R. J. and Rogers L. (1972) Testosterone, search behavior and persistence. Nature 237, 343-346. Archer J. (1977) Testosterone and nersistence in mice. Anim. Behar. 25. 479-488. Baucom D. H.,‘Besch P. K. and Callahan S. (1985) Relation between testosterone concentration, sex role identification, and personality among females. J. Person. sot. Psycho/. 48, 12181226. Bernstein 1. S., Rose R. M. and Gordon T. P. (1974) Behavioral and environmental events influencing primate testosterone levels. J. Human Evol. 3, 517-525. Broverman D. M., Klaiber E., Kobaysahi Y. and Vogel W. (1968) Roles of activation and inhibition in sex differences in cognitive abilities. Psycho/. Rev. 75, 23-50. Browne A. and Flewelling R. (1986, October/November) Women as victims or perpetrators of violence. Paper presented as the meeting of the American Society of Criminology, Atlanta, GA. Dabbs J. M. Jr, Frady R. L., Carr T. S. and Besch N. F. (1987) Saliva testosterone and criminal violence in young adult prison inmates. Psychosom. Med. 49, 174-182. Dabbs J. M. Jr and Ruback R. B. (1987) Saliva testosterone and personality among male college students. Unpublished manuscripts, Georgia State University, Atlanta. Dai W. S., Kuller L. H., LaPorte R. E.. Gutai J. P., Falvo-Gerard L. and Caggiula A. (1981) The epidemiology of plasma testosterone levels in middle-aged men. Am. J. Epidemiol. 114, 804-816. Daitzrnan R. and Zuckerman M. (1980) Disinhibitory sensation seeking, personality and gonadal hormones. Person. individ. D$f
1, 103-110.
Ehrenkranz J., Bliss E. and Sheard M. H. (1974) Plasma testosterone: Correlation with aggressive behavior and social dominance in man. Psychosom. Med. 36, 469-475. Elias M. (1981) Serum cortisol, testosterone, and testosterone-binding globulin responses to competitive fighting in human males. Aggress. Eehav. 7, 215-224.
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Gillespie L. K. (1986, October/November). What must a woman do to be executed: A comparison study of executed and non-executed women. Paper presented at the meeting of the American Society of Criminology. Atlanta. GA. Hellhammer D. H., Hubert W. and Schurmeyer T. (1985) Changes in saliva testosterone after psychological stimulation in men. Psychoneuroendocrinology 10, 77-8 1. Hermida R. C., Halberg F. and del Pozo F. (1985) Chronobiologic pattern discrimination of plasma hormones, notably DHEA-S and TSH, classifies an expansive personality. Chronobiology 12, 103-136. Kandel E. R. and Schwartz J. H. (1981) Principles of Neural Science. Elsevier-North Holland, Amsterdam. Kreuz L. E. and Rose R. M. (1972) Assessment of aggressive behavior and plasma testosterone in a young criminal population. Psychosom. Med. 34, 321-332. Kupperman H. S. (1965) Male sex hormones. In Drill’s Pharmacology in Medicine (Edited by J. R. DiPalma). McGraw-Hill. New York. Latanb B. (1987) The state of social science: Why we should invest in infrastructure. Sot. Sci. 72, I-16. Mazur A. (1985) A biosocial model of status in face-to-face primate groups. Sot. Forces 64, 377402. Mazur A. and Lamb T. A. (1980) Testosterone, status, and mood in human males. Harm. Behar. 14, 236-246. Morris N. M., Udry J. R., Kahn-Dawood F. and Dawood M. Y. (1987) Marital sex frequency and midcycle female testosterone. Arch. sex. Behau. 16, 27-37. Olweus D. (1983) The role of testosterone in the development of aggressive antisocial behavior in adolescents. In Prospectice Sfudies of Crime and Delinquency (Edited by Van Dusen K. T. and Mednick S. A.). Kluewer-Nighoff, Boston. Persky H., Lief H. I., Strauss D., Miller W. R. and O’Brien C. P. (1978) Plasma testosterone level and sexual behavior of couples. Arch. sex. Behuc. 7, 157-173. Purifoy F. E. and Koopmans L. H. (1979) Androstenedione, testosterone, and free testosterone concentration in women of various occupations. Sot. Biol. 26, 179-188. Rose R. M. (1978) Neuroendocrine correlates of sexual and aggressive behavior in humans. In Psychopharmacology: A Generarion of Progress (Edited by Lipton M. A., DiMascio A. and Killian K. F.). Raven Press, New York. Schindler G. L. (1979) Testosterone concentration, personality patterns, and occupational choice in women (Doctoral Dissertation, University of Houston, 1979). Dissertation Abstracts Internofional, 40, 141 IA. (University Microfilms No. 79-19.403). Sherwin B. B., Gelfand M. M. and Brender W. (1985) Androgen enhances sexual motivation in females: A prospective. crossover study of sex steroid administration in the surgical menopause. Psychosom. Med. 47, 339-351. . . Turner C. W., Ford M. H., West D. W. and Meikle A. W. (1986) Genetic influences on testosterone, hostility, and Type A behavior in adult male twins. Poster presented at the meeting of the American Psychological Association, Washington. __ U.L.
Vermeulen A. and Verdonck L. (1972) Some studies on the biological significance of free testosterone. J. steroid Biochem. 3, 421-426. Vining R. F. and McGinley R. A. (1984) Transport of steroid from blood to saliva. In Ninfh Tenocuc workshop: Immunoassay of Sreroidr in S&u (Edited by Read G. F., Riad-Fahmy D., Walker R. R. and Griffiths K.). Alpha Omega, Cardiff, Wales. Vittek J., L’Hommedieu D. G., Gordon G. G., Rappaport S. C. and Southren A. L. (1985) Direct radioimmunoassay (RIA) of salivary testosterone: Correlation with free and total serum testosterone. f.ife Sci. 37, 71 I-716. Vogel W., Klaiber E. L. and Broverman D. M. (1978) Roles of the gonadal steroid hormones in psychiatric depression in men and women. Prog. Neuro-Psychopharmac. 2, 487-503.
0191-8869 88 53.00+ 0.00 PergamonPressplc
Vol. 9. No. 2, pp. 269-275, 1988
Rimedin GreatBritain
SALIVA TESTOSTERONE AND CRIMINAL AMONG WOMEN JAMESM. DABBSJR,’ R.
BARRY RUBACK,’
ROBERT L. FRADY,’
and DEMETRIOSS.
VIOLENCE
CHARLES H. HOPPER’
SGO~TAS’
‘Department of Psychology, Georgia State University, University Plaza, Atlanta, GA 30303, Diagnostic Unit, Georgia Industrial Institute, Alto, GA 30596 and ‘Department of Pathology and Laboratory Medicine, Emory University, Atlanta, GA 30322, U.S.A. (Received
8 Muy
1987)
Summary-Free testosterone concentrations were measured in the saliva of 84 female inmates and 15 female college students. Testosterone differed among inmates convicted of unprovoked violence,defensive violence, theft, drugs, and a set of other crimes. It was highest with unprovoked violence and lowest with defensive violence, where inmates had reacted violently after being physically assaulted. Testosterone was also related to number of prior charges and to Parole Board decisions about length of time to serve before being released on parole. Mean testosterone levels were similar for inmates and college students.
INTRODUCTION
Testosterone is the principal male sex hormone, affecting sexual development in urero and during adolescence (Kandel and Schwartz, 1981). Throughout life it affects the functioning of numerous organ systems in both sexes (Kupperman, 1965). Its physical effects are both anabolic (high lean-fat ratios) and masculinizing (baldness, body hair, low voice pitch). It is also related to behavior, especially involving sex and aggression. In studies of male animals and human beings, testosterone has been related to libido (Kupperman, 1965), activity level (Broverman, Klaiber, Kobaysahi and Vogel, 1968), persistence at goal-directed behaviors (Andrew and Rogers, 1972; Archer, 1977), sensation seeking (Daitzman and Zuckerman, 1980), intolerance of frustration (Olweus, 1983), dominance (Mazur, 1985), and positive affect (Dabbs and Ruback, 1987). Testosterone affects behavior and in turn is affected by experience. It rises in male monkeys who win fights (Bernstein, Rose and Gordon, 1974) and men who win wrestling or tennis matches (Elias, 1981; Mazur and Lamb, 1980), and it drops in male monkeys who lose fights (Bernstein et al., 1974). Women have less testosterone than men, but its effects are much the same. Experimental administration of testosterone to women increases interest in sex (Sherwin, Gelfand and Brender, 1985), and frequency of sexual activity in married couples is correlated with the females’ characteristic testosterone levels (Morris, Udry, Kahn-Dawood and Dawood, 1987). Among women, testosterone levels have been associated with a friendly sociability (Persky, Lief, Strauss, Miller and O’Brien, 1978), and an adrenal precursor of testosterone (DHEA-S) has been associated with an expansive personality (Hermida, Halberg and de1 Pozo, 1985). Testosterone has also been related to personality characteristics of masculinity and femininity (Baucom, Besch and Callahan, 1985). Serum testosterone is reportedly higher among female students and professional, managerial, and technical workers than among clerical workers and housewives (Purifoy and Koopmans, 1979). Similarly, saliva testosterone is higher among female lawyers than among athletes, teachers and nurses (Schindler, 1979). Several studies have related testosterone to criminal violence among men (Dabbs, Frady, Carr and Besch, 1987; Ehrenkranz, Bliss and Sheard, 1974; Kreuz and Rose, 1972), and the present study extends this work to women. Women commit less violent crime than men do, but women who commit violent crimes may have more testosterone than those who do not. Such a finding would not imply a necessary tie between violence and testosterone, because a person could be high in testosterone and not violent, but it would suggest that testosterone sometimes contributes to violent behavior in both sexes. Most studies of testosterone have involved serum assays, which require the drawing of blood by medical personnel, and sample sizes have tended to be small. Saliva measurements are well suited to behavioral studies, because they are easy to obtain and reliable. In serum, most testosterone is 269
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bound to sex hormone binding globulin. Only a small percentage remains ‘free’ and thus biologically active, which means it is able to enter target cells and bind with specific receptors throughout the body (Vermeulen and Verdonck, 1972). Only the free testosterone can pass through the saliva glands (Vining and McGinley, 1984), and as a result there is a high correlation between concentrations of saliva testosterone and serum free testosterone (Vittek, L’Hommedieu, Gordon, Rappaport and Southren, 1985).
METHOD Testosterone measures Data collection. Subjects were 84 female inmates in a state prison and 15 female undergraduate college students. The inmates had been recently admitted and were housed in a diagnostic unit where all inmates spend their first month. Saliva samples were collected in group sessions of 20-25 inmates, held between 3:00 and 4:00 p.m. on 2 days a month apart, in April and May of 1986. About 12 inmates declined to participate, and saliva samples from two others were too small to assay. The college students participated as part of a course requirement. Their samples were collected in group sessions of 3-5 students, held at 10:00 a.m. on several days in April and May. No students declined to participate. Subjects rinsed their mouths with water before the session. The nature of testosterone and the purpose of the study was explained, and subjects were given consent forms to sign. Included with the consent forms were questions on age, number of children, and menstrual cycle history. Subjects were asked to write down any other information they thought might be relevant to reproductive function (e.g. hysterectomy). Each subject was given 20-ml polyethylene vial with a serial number of the cap. Subjects collected saliva in their mouths and deposited it into the vial, filling the vial to a 5-ml mark on the side. Subjects remained together in their group for l&15 min, until all had finished. Radioimmunoassays. Saliva samples were frozen and delivered to the Department of Pathology and Laboratory Medicine at Emory University. Radioimmunoassay (RIA) was performed using a commercial kit for serum testosterone from Leeco Diagnostics (Southfield, MI 48075). The antiserum was raised in rabbits against testosterone-3-(O-carboxymethyl)oxime-bovine serum albumin. Cross reaction is significant (16%) only with 5cr-dihydrotestosterone; other steroids give less than 2% cross reaction. The tracer was a testosterone-3-[‘251]iodohistamine ligand (sp. act. 2000 Ci/mmol). The Leeco kit and method were modified and optimized for saliva testosterone as follows. Standards in the kit were diluted with phosphate buffer to yield an assay range of 1400 pg/ml. Saliva was heated for 30 min at 55°C and then centrifuged to remove debris, and 0.5 ml volumes were mixed in tubes with equal volumes of water and extracted with 5 ml diethyl ether. For optimum extraction (95-98% recovery), the tubes were shaken for 5 min at high speed on a multivortex shaker. The aqueous phase was frozen by immersing the tubes in an ethanol-solid CO, mixture. The ether extract (the organic phase) was decanted into new tubes, and 4-ml volumes of the ether extract were transferred into appropriate RIA tubes. The ether was then evaporated under nitrogen in a warm water bath. When dry, the RIA tubes received 0.05 ml tracer, 0.1 ml antiserum diluted 3-fold with phosphate buffer, and 0.1 ml phosphate saline buffer. The mixture was incubated at room temperature overnight, and 0.5 ml of precipitating reagent antiserum diluted 2-fold with phosphate buffer was added. The mixture was centrifuged at 4°C for 30min. The supematant was decanted and the precipitate counted in a gamma counter. Sensitivity of the assay, defined as the quantity of unlabeled hormone required to inhibit binding of the tracer by an amount equal to 2 SD, as compared with inhibition in the absence of unlabeled hormone, was determined to be 5 fmol. Accuracy of the assay was estimated by adding testosterone standards to female saliva treated with charcoal to remove testosterone. When the saliva was extracted and treated as above,, the results were indistinguishable from what would be expected in the absence of saliva. For quality control purposes, duplicate assays were performed on each sample, and the coefficient of variation (CV: the standard deviation expressed as a percent of the mean) between
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duplicates was computed. Laboratory personnel did not know whether samples came from inmates or students. Samples were assayed a second time, again in duplicate, whenever the initial CV was greater than 25% or when laboratory personnel judged the results questionable for any reason. Where the CV did not improve markedly from the first to the second assay, the combined mean of the duplicates for both assays was taken as the subject’s score. The testosterone score for each subject was reported in units of nanograms per 100 milliliters (ng/lOO ml). Mean CV for the 99 samples was 8.8%. Stability of individual d&zrences. The present work employed a single measure of saliva testosterone from each inmate. Reliability is known to be high for single measurements of serum testosterone from male subjects, about r = 0.80 (Dai, I&Her, LaPorte, Gutai, Falvo-Gerard and Caggiula, 1981; Olweus, 1983). We assumed reliability would be lower for saliva measurements from females, because female saliva testosterone levels are so low as to approach the limits of assay sensitivity, but we did not know exactly what the reliability would be. We subsequently assayed saliva samples collected on 2 days from 22 male and 25 female students participating in a panel study at the University of North Carolina (Latane, 1987), finding reliability to be r = 0.79 for males and r = 0.51 for females. Based upon these data, we think reliability in the present study was about r = 0.50. Reliability was sufficiently high to reveal a number of significant relationships, as described below. For further research with female subjects, however, we suggest scores be based on the mean of two or three saliva samples. Applying the Spearman-Brown formula, reliability of r = 0.50 for a single measurement will increase to r = 0.67 for the mean of two measurements and to r = 0.75 for the mean of three measurements. Behavioral
data
The study focused upon each inmate’s current crime, but we also examined prior criminal charges, behaviour in prison, and Parole Board decisions about parole. This information was obtained from Department of Corrections computer files and Parole Board computer and paper files. Current crime. Because the study was an extension of earlier work on criminal violence in male inmates, our primary focus was on whether or not each inmate was currently incarcerated for a violent crime. Department of Corrections computer records indicated the crime for which each inmate was convicted, but sometimes persons commit violent crimes and are convicted of nonviolent crimes (usually through plea bargaining; e.g. assault might lead to a “reckless conduct” conviction). Parole Board records included a narrative description of the crime in a post-sentence investigation report in each inmate’s paper file. We determined the exact nature of each inmate’s current crime from this post-sentence investigation. Criminal history. Criminal histories are often confusing. A single conviction can lead to probation, probation violation, incarceration, parole, parole violation, and incarceration again. Legal records are scattered among jurisdictions. Parole Board personnel examine court records in countries where each subject has resided, and a list of all prior charges is included in each inmate’s post-sentence investigation. Parole Board files contained Post-Sentence Investigations for 8 1 of the 84 inmates. For each inmate we counted the total number of charges, including the current one, except that when the same charge appeared more than once it was counted only once. The same inmate might have charges as diverse as forgery, assault, and drug sale, or as similar as forged check and bad check, or marijuana sale and cocaine sale. We considered coding schemes that would simplify the list, such as grouping charges into four categories (person, property, drugs and other), but these coding schemes appeared to add no useful information beyond that given by the number of charges alone. Behavior in prison. Disciplinary reports for infractions in prison are placed in each inmate’s paper file and are also coded and entered into computer records of the Department of Corrections. These records show the infraction that took place and the punishment for it. Approximately 8 months after the saliva samples had been collected, we examined these computer records for each inmate and counted the total number of infractions, number of infractions involving assaultive behavior, and punishments received for the infractions. Parole Board treatment. Finally, we examined Parole Board recommendations on how much time each inmate was to serve before being released on parole. The Parole Board uses a Decision
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Guidelines grid that summarizes in an objective fashion the severity of each crime and the likelihood of recidivision. The Guidelines recommend a length of time in prison that ranges from 4 to 102 months. Parole Board members also examine cases individually, and they sometimes depart from Guidelines recommendations to increase or decrease the length of time an inmate must serve. Such departures usually indicate aggravating or mitigating circumstances, extensive criminal history, medical problems, or, less frequently, misbehavior in prison. We assigned a score of - 1, 0, or + 1 to indicate whether the Parole Board gave each inmate less, the same, or more time than the Guidelines recommendation. This score could be regarded as a measure of “Parole Board severity.” RESULTS Subjects
Inmates ranged in age from 17 to 66 years (median age 28). Six had hysterectomies, one had an ovariectomy, and two were pregnant. Of the remainder, among those below age 40, 10% reported not having regular menstrual cycles. Students ranged in age from 18 to 26 (median age 18), and all reported having regular menstrual cycles. Testosterone
scores
Overall mean testosterone concentration was 2.18 ng/lOO ml. The difference between prison inmates (Mean = 2.17, SD = 0.83) and college students (Mean = 2.21, SD = 0.58) was not significant (t < 1). These mean scores are within the normal range for female subjects. In a previous unpublished study employing the same assay procedure as used here, D. Sgoutas obtained values of 2.45 (SD = 0.41) for 20 women with regular menstrual cycles and 2.50 (SD = 0.42) for 12 post-menopausal women. Current
crime
The 84 current crimes fell into four categories: violent (20), theft (40), drugs (14) and other (10). Violent crimes included homicide, assault, and robbery. Theft primarily included shoplifting, forgery, and bad checks. Drug crimes involved use of or trafficking in drugs or alcohol, The “other” category included crimes that are relatively infrequent among women, such as arson, firearms possession, burglary, running a gambling operation, and hindering apprehension of a felon. Initial analysis did not show inmates convicted of violent crimes to be significantly higher than other inmates in mean testosterone (t < l), However, perusal of the data revealed 13 inmates in the violent group above the prison median in testosterone, one at the median, and six below the median (P < 0.10 by sign test). Some of the inmates below the median were extremely low in testosterone. Descriptions of the circumstances of each crime showed the violent acts of five inmates had been in response to physical provocation. Two of these women were battered wives who killed their husbands, and three had retaliated against lovers or acquaintances who had attacked them. These five “defensive violent” inmates were significantly lower in testosterone than their remaining 15 “unprovoked violent” inmates, t (18) = 3.05, P < 0.01. We kept this distinction between unprovoked violence and defensive violence in the analyses that follow. Mean testosterone scores among inmates are summarized in Table 1. The overall difference among the five groups in the table was significant, F(4,79) = 3.82, P < 0.01. A Tukey multiple range test showed differences between specific groups, as summarized in the table. The unprovoked violent group was significantly higher than the defensive violent and theft groups. Table I. Mean testosterone concentrations (ng/lOil ml) among inmates convicted of five tytxs of crime Defensive Violent (n = 5)
Theft (n =40)
Drugs (n = 14)
Other (n = 10)
Unprovoked Violent (n = 15)
1.48
1.94
2.31
2.47
2.63
Note: Groups that do not share a common underline are significantly different from one another (P < 0.05) by Tukey test.
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Criminal history
The overall correlation between testosterone and number of charges did not reach significance, df = 80, P < 0.10. This correlation could be affected by crime type differences in testosterone or in number of charges. To control for this possibility, we computed the pooled within-group correlation, treating each score as a deviation from the mean for its crime type. The resulting pooled within-group correlation was significant (r = 0.27, df = 76, P < 0.05).
r = 0.20,
Behavior in prison
There was no apparent relationship between testosterone levels and disciplinary infractions. The total number of infractions was relatively low. Twenty-six of the 84 inmates had received reports for infractions of prison rules, and 13 of these had received punishment (isolation). Only 9 inmates had behaved in an assaultive manner in prison. Parole Board treatment
Parole Board computer records were checked eight months after collecting saliva samples. At this time, “Parole Board severity” scores were available on 54 inmates, showing whether the Board assigned less, the same, or more time than recommended by the Decision Guidelines. The remaining inmates had been released before being reviewed or were not scheduled for review by the Parole Board. The scores were correlated positively with inmates’ testosterone levels (r = 0.34, 53 df, P c 0.05). As with criminal history, we also computed the pooled within-groups correlation, which was significant (r = 0.27, df = 49, P < 0.05). For inmates whose testosterone concentrations were higher than average, the Parole Board tended to assign longer times to serve than provided by the Decision Guidelines. DISCUSSION As with men, women’s saliva testosterone concentrations were related to criminal violence, although the pattern was more complicated with women. Violent crimes among women included both unprovoked violence and defensive violence, typified by abused wives who killed their husbands. Defensive violence may be especially common among women; Browne and Flewelling (1986) argue that women who kill do so primarily in response to some kind of threat. Testosterone was lowest in defensive violence and highest in unprovoked violence. Testosterone also differed with other kinds of crime, being low in theft and high in drug offenses and a miscellaneous set of crimes atypical of women. Defensive violence was relatively rare in our sample, which limits to some extent our confidence regarding its link to low testosterone. However, low testosterone in physically abused women is reminiscent of low testosterone found in male rhesus monkeys defeated in fights (Bernstein et al., 1974). We do not know how subject’s testosterone levels might have changed in the past. Physical abuse could have led to lower testosterone, or lower testosterone could have increased the likelihood these women would be abused. Male serum testosterone levels are heritable, with correlations reported of r = 0.50 between fraternal twins and r = 0.69 between identical twins (Turner, Ford, West and Meikle, 1986), implying some stability within individuals. On the other hand, testosterone changes with experience, and levels can rise markedly within a few minutes (Hellhammer et al., 1985). We do not know how much chronic testosterone levels change with experience over periods of months or years. The issue might be pursued among women who are abused and then removed to safer surroundings, to see whether their testosterone is initially low and gradually moves to higher levels. The findings on defensive violence might appear at variance with those of Olweus (1983), who reported higher testosterone among subjects who engaged in defensive (which he called “provoked”) aggression. But Olweus worked with normal high school students, and he used “provoked” to refer to cases where subjects reacted against being frustrated or restricted. Using his frame of reference, most of our inmates might have been frustrated or restricted and therefore “provoked” to violence, either by persons or by circumstances. We have limited the term “defensive” to describe more extreme cases of reaction against physical attack. Perhaps high levels of testosterone stimulate subjects to resist frustration and mild provocation, as described by
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Olweus, while response to extreme physical provocation may be explained better by something other than high testosterone. Disciplinary infractions in prison were not related to testosterone concentrations. This may be partly because female inmates, in comparison to males, commit relatively few disciplinary infractions. But even among male inmates testosterone has not been clearly related to behavior in prison (Rose, 1978). In the present study, the total number of different charges in an inmate’s history reflected both amount and diversity of illegal activity, and this score was correlated with testosterone concentration. Inmates high in testosterone received more time in prison than called for by the Parole Board Decision Guidelines. This Parole Board treatment, as indicated above, may reflect more aggravating circumstances about the offenses and more extensive criminal histories among these women; women higher in testosterone did tend to have more charges in their histories. In this regard, Gillespie (1986) has noted that female inmates are more likely to be executed if they exhibit inappropriate sex role behavior in addition to committing the crime. One might expect more inappropriate sex role behavior from women who are high in testosterone. An explanation based upon testosterone would not diminish the injustice involved if women are being punished for behaving differently than other women. But it would raise the question of whether the punishment is actually for out-of-role behavior or more simply for extreme stereotypical “masculine” behavior. The present findings, along our earlier study of male prison inmates (Dabbs er al., 1987), suggest the Parole Board does not react favorably to inmates who are high in testosterone, regardless of whether the inmates are male or female. The present emphasis upon criminal violence should not distort our perspective on testosterone. Testosterone, as reviewed in the introduction, has effects on mood. behavior, and even cognitive processes that can be quite positive. The prison population represents a small minority of all men and an even smaller minority of all women. It may be that testosterone has more negative effects among women than among men; Vogel, Klaiber and Broverman (1978) reported testosterone levels three times higher among depressed than among normal women. But testosterone could have one effect in a context of frustration, hostility, and violence and another effect where there is opportunity, friendliness, and achievement. We need to understand the fundamental psychological and behavioral dimensions associated with testosterone and the factors that cause testosterone to have different effects in different conditions. wish to thank the Georgia Department of Corrections and the Georgia Board of Pardons and Paroles for making this research possible. In addition, we specifically extend thanks to Kathy Barry, Gary Black, Tim Carr and Ray Roberson (Department of Corrections) and to Sue Aiken, Tom Morris and Sheila Tyson (Board of Pardons and Paroles). We are indebted to Mary Richter and Laura Salter for coding inmate records and to Claire Anderson for performing the radioimmunoassays.
Acknowledgements-We
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