This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Scuteri, A. Articles by Anderson, D. E. Search for Related Content PubMed PubMed Citation Articles by Scuteri, A. Articles by Anderson, D. E. Related Collections Personality Pulmonary Blood Pressure

Anger Inhibition Potentiates the Association of High End-Tidal CO₂ With Blood Pressure in Women

From the Laboratory of Cardiovascular Science (A.S., D.P., D.A.E.), National Institute on Aging, Baltimore, Maryland; and the Department of Medicine (M.A.C.), School of Medicine, University of California, San Francisco, California.

Address reprint requests to: David E. Anderson, PhD, Laboratory of Cardiovascular Science, National Institute on Aging, 5600 Nathan Shock Dr., Baltimore MD 21224. Email: AndersoD{at}grc.nia.nih.gov

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

 
OBJECTIVE: High resting end-tidal CO₂ (PetCO₂) has been shown to be an independent predictor of systolic blood pressure (SBP) in women, particularly older women. The study reported in this article investigated whether the tendency to experience, express, and/or suppress anger contributes to the association of PetCO₂ and SBP in women and in men.

METHODS: The Spielberger Anger Expression Inventory was administered to 403 healthy male and female participants in the Baltimore Longitudinal Study on Aging. Resting PetCO₂ was obtained by means of a respiratory gas monitor, and resting blood pressure was obtained with an oscillometric device. The associations of resting PetCO₂ and the anger scales with SBP and diastolic blood pressure (DBP) were investigated using multivariate regression analyses.

RESULTS: PetCO₂, as well as age and body mass index, was an independent predictor of SBP in women with low, but not high, trait anger and in women with low, but not high, anger-out. PetCO₂ was not an independent predictor of SBP in men with either high or low anger. In addition, PetCO₂ was not an independent predictor of DBP in either men or women.

CONCLUSIONS: The results of this study indicate that inhibition of anger potentiates the relationship of high PetCO₂ with SBP in women but not men. Additional studies are needed to determine the origins of the observed gender differences and the psychophysiological pathways by which high resting PetCO₂ contributes to elevated resting blood pressure in women.

Key Words: anger • breathing • blood pressure • end-tidal CO₂ • hypertension • women.

Abbreviations: BMI = body mass index; DBP = diastolic blood pressure; pCO₂ = partial pressure of CO₂; PetCO₂ = end-tidal CO₂; SBP = systolic blood pressure.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

 
One of the oldest hypotheses in the psychosomatic medicine literature, dating back more than a half century, is that chronic inhibition of anger can potentiate the development of hypertension (1). Since then many systematic attempts have been made to test this hypothesis. Most (2, 3) but not all (4) reviews of the resulting literature have concluded that the evidence points to a significant relationship. However, conclusions are generally qualified in terms of both conceptual and methodological complexities. In the 1950s, a distinction was first made about the direction of anger: outward toward the environment or inward toward the self (5). In the 1980s, the dimensions of state and trait anger were added, focusing on the frequency of occurrence of anger (6). In addition, reviews of the literature have concluded that the nature of the associations between anger and blood pressure depend on whether anger is determined from self-report or behavioral observation (3). When anger is assessed through self-report, positive correlations between anger expression and blood pressure tend to be observed, whereas when behavioral observations are made, inhibition of anger seems to be a predictor of higher blood pressure. One recent prospective study concluded that both self-reported high anger-in and high anger-out increased the probability of being diagnosed with hypertension 4 years later (7).

The physiological mechanism by which anger expression or suppression participates in long-term blood pressure regulation is typically presumed to involve sympathetic nervous system activity (8–10), and numerous studies of anger evocation in the laboratory have been associated with rapid increases in heart rate and blood pressure, which are likely to be mediated by autonomic arousal (11).

The possibility that the role of anger expression or suppression in the development of high resting blood pressure might be mediated through inhibition of breathing has received very little experimental attention. A significant contributing role of conditioned suppression of breathing in the development of hypertension has been suggested by a series of studies with genetically normotensive animals (12). For example, a combination of behavioral stress and high sodium intake can produce experimental hypertension that is not prevented by adrenergic antagonists (13). Development of this form of hypertension was accompanied by sustained sodium retention, which was not prevented by renal denervation (13). A pattern of conditioned suppression of breathing observed under these conditions was found to be associated with sustained increases in pCO₂ (14). Increases in pCO₂ can induce sodium retention through increased formation of carbonic acid with dissociation to hydrogen and bicarbonate ions, which increase renal sodium-hydrogen exchange and renal sodium reabsorption. Other studies have shown that increasing pCO₂ by voluntary slowing of breathing frequency at a normal tidal volume is also associated not only with sodium retention (15) but also with increased concentrations of endogenous digitalis-like factors that covary with plasma volume (16). Thus, inhibition of breathing and high pCO₂ might increase susceptibility to the hypertensive effects of a high sodium intake by expanding plasma volume.

The magnitude of the individual differences in resting PetCO₂ in humans is greater than the magnitude of within-subject variability over weeks and months (17). Recent studies have shown that high resting PetCO₂ in humans is a marker for blood pressure sensitivity to high sodium intake. Studies of older humans with a high incidence of sodium sensitivity (18) and of younger humans with a lower incidence of sodium sensitivity (19) have found a correlation between resting PetCO₂ and magnitude of blood pressure response to an increase in dietary sodium. In the older group, high resting PetCO₂ was associated with high levels of endogenous digitalis-like factors, both before and after sodium loading.

High resting PetCO₂ has also been associated with an increased tendency to worry and experience negative affect, as revealed by the Neuroticism Scale of the NEO Personality Inventory (17). A recent study also found that high resting PetCO₂ was a significant independent predictor of resting SBP in women, especially after age 50 (20), raising the question of whether the emotional state that characterizes humans with high resting PetCO₂ is relevant to the anger dimension that has been associated with high blood pressure.

The study reported here investigated the interdependence of trait anger, anger-in and anger-out, and resting PetCO₂ in blood pressure regulation. A series of healthy male and female participants in the Baltimore Longitudinal Study on Aging were administered the Spielberger State-Trait Anger Expression Inventory and had resting PetCO₂ and blood pressure recorded. It was hypothesized that anger expression style affects the association between resting PetCO₂ and blood pressure. In addition, it was hypothesized that this putative interaction may differ by gender.

	METHODS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

 
Subjects
The participants were 403 volunteers for the Baltimore Longitudinal Study on Aging, an open-panel multidisciplinary study of normal human aging conducted by the National Institute on Aging. Subjects are predominantly well educated (>75% have a bachelor’s degree or higher), and they are scheduled to visit the Gerontology Research Center at approximately 2-year intervals. Each visit involves 2.5 days of evaluation and testing, which includes a physical examination by a healthcare provider (ie, physician, physician’s assistant, or nurse practitioner), an inventory of medications used, and an intensive set of medical and physiological evaluations. Of the 403 subjects who participated in this study, 198 were male and 205 were female.

Exclusion criteria for this study included a history of stroke, myocardial infarction, pulmonary disease, renal disease, diabetes, congestive heart failure, or treatment with diuretics, antihypertensive medication, bronchodilators, oral hypoglycemic agents, nonsteroidal antiinflammatory drugs, central nervous system stimulants, or cigarette smoking within the past 12 months. The study was approved by the Institutional Review Board of The Johns Hopkins University School of Medicine.

Apparatus and Procedures
The participants were studied individually in the afternoon at least 2 hours after the previous meal. After the purpose of the study was described and informed consent was obtained, the subject was seated in a reclining chair for 25 minutes. PetCO₂ was monitored continuously by use of a nasal cannula attached to a respiratory gas monitor (Ohmeda, model 5250, Denver, CO). The subject was instructed to keep the mouth closed during the monitoring period, and an experimenter reminded the subject as necessary. Peak concentrations of expired CO₂ for each breath were detected by the gas monitor, and means over successive 1-minute intervals were recorded in a computer (model 3FGe, NEC Corporation, Santa Clara, CA). The respiratory gas monitor was recalibrated before each session using a cannister of 6% CO₂. Previous observations had shown that individual PetCO₂ does not drift significantly during 25 minutes of continuous resting observation.

Resting blood pressure was recorded every 5 minutes during the 25-minute session by means of an inflatable cuff placed around the nondominant arm and connected to an automated oscillometric device (Physiocontrol Lifestat 200, Redmond, WA). The first measurement was discarded, and the mean of the last four measurements was calculated.

The 31-item version of the Spielberger Anger Expression Inventory (21) assesses the disposition to experience anger (trait anger), express anger (anger-out), and suppress anger (anger-in). The frequency of anger experience is measured by answers to 10 questions. The tendency to hold anger in when experienced is measured from the answers to eight questions. The tendency to express anger outwardly when experienced is determined from the answers to eight. The test was given at the beginning of the monitoring period and required 5 to 10 minutes to complete.

Data Analysis
All analyses were performed using SAS computer programs (SAS Institute, Cary, NC).

Results are expressed as mean ± standard deviation. Zero-order correlations were calculated to assess the univariate associations of age, BMI, PetCO₂, trait anger, anger-in, and anger-out for men and women, with each gender subdivided into high and low trait anger on the basis of the median of the gender distribution. Forward stepwise multiple regressions of age, BMI, and PetCO₂ on SBP and DBP were performed separately for 1) women with trait anger above and below the median for gender, 2) women with anger-in above and below the median for gender, and 3) women with anger-out above and below the median for gender. First, age and BMI were entered as a block because of their known associations with blood pressure. These variables were followed by PetCO₂ to determine the extent to which it added incrementally to the variance.

	RESULTS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

 
Demographic Characteristics of Women and Men
Table 1 shows means and standard deviations of PetCO₂, trait anger, anger-in, anger-out, age, BMI, SBP, and DBP for women and for men. The anger-in scores (p < .02), BMI (p < .001), and SBP (p < .02) of men were higher than those of women in this sample. Table 2 shows the correlation coefficients between the anger scales for women and men. For both women and men, anger-in and anger-out were positively correlated with trait anger. Anger-in and anger-out were not significantly correlated for either women or men.

Table 2 also shows the univariate correlations of age, BMI, PetCO₂, and anger scores with SBP and DBP in women. Age, BMI, and PetCO₂ were each positively associated with SBP in women. The three anger scores were not significantly associated with SBP in women. Age was the only univariate associated with DBP in women.

Univariate Associations of Trait Anger, Anger-In, and Anger-Out
For men the univariate association of trait anger with anger-in was 0.41, and that with anger-out was 0.35. The univariate association of anger-in and anger-out was 0.19 for men.

For women the univariate association of trait anger with anger-in was 0.19, and that with anger-out was 0.60. The univariate association of anger-in and anger-out was -0.09 for women.

These correlations indicate that 60% to 90% of the variance of each scale was independent of the other scales.

Independent Predictors of SBP in Men and Women With High and Low Trait Anger
Table 3 shows the results of the stepwise multiple regression of age, BMI, and PetCO₂ on SBP in men and women with high and low trait anger. Age and BMI were independent predictors of SBP in men with high and low trait anger. The addition of PetCO₂ to the model did not add significantly to the variance explained for either high or low trait anger.

Independent Predictors of SBP in Men and Women With High and Low Anger-In
Table 4 shows the results of the stepwise multiple regression of age, BMI, and PetCO₂ on SBP in men and women with high and low anger-in. Age and BMI were independent predictors of SBP in men with high and low anger-in. The addition of PetCO₂ to the model did not add significantly to the variance explained for either high or low anger-in.

Independent Predictors of SBP in Men and Women With High and Low Anger-Out
Table 5 shows the results of the stepwise multiple regression of age, BMI, and PetCO₂ on SBP in men and women with high and low anger-out. Age and BMI were independent predictors of SBP in men with high anger-out, whereas BMI was the only independent predictor for men with low anger-out. The addition of PetCO₂ to the model did not add to the variance explained for either high or low anger-out.

	DISCUSSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

 
This study explored the relationship of trait anger and anger expression to PetCO₂ in blood pressure regulation. The results were consistent with findings of a previous study (20) showing that high resting PetCO₂ was an independent predictor of higher resting SBP in women but not men. In our study, the association was found to be specific to women with low trait anger and to women with low anger-out. The inverse univariate association of PetCO₂ with SBP in men was accounted for by the fact that PetCO₂ decreases with age in men (but not women), whereas SBP increases with age (in both men and women).

The classic psychosomatic hypothesis of Franz Alexander (1) postulated that essential hypertension is potentiated in persons who avoid the experience of anger, but at a cost of sustained physiological arousal. Consistent with this view, various experimental studies have found that hypertensive patients tend not to perceive aggression in others that is observed by nonhypertensive control subjects (eg, Ref. 22). In that formulation, anger is not merely held in or suppressed but is "repressed"; that is, it does not enter into conscious awareness and so would be underreported by hypertensive subjects on psychological tests. The findings for SBP in female subjects in the present study are consistent with this hypothesis and suggest that lack of anger plays a permissive role in the effects of high PetCO₂ on blood pressure. Other questionnaire studies using other methodologies, such as the Harburg Anger In/Anger Out Scale (23) or the Survey of Affective States (24), have observed positive associations between high anger experience and resting blood pressure. The relationships of the definitions of anger in those studies to those in the Spielberger inventory and whether other measures of anger would yield positive associations with blood pressure in women or men in the present sample remain to be clarified.

The observation that the association of PetCO₂ with SBP is manifest only in women with low trait anger or low anger-out raises the question of what it is about low trait anger or low anger-out that engenders this association. Low trait anger women in this study may be in settings that don’t arouse anger, may be able to manage anger effectively, or may be denying or repressing anger. We could not differentiate between these alternatives in this study. The previous study (17) showing that humans with high resting PetCO₂ tend to have high neuroticism scores on the NEO Personality Inventory suggest that some negative emotional state characterizes these individuals, but this state apparently is not conscious anger. It is tempting to extrapolate from the previously cited animal studies, in which quiet anticipation of the onset of an aversive task was associated with suppression of breathing and acute increases in pCO₂ (12). Those animals could be said to be in a state of "vigilance," a state of alertness prompted by the perceived possibility of harmful events in the external environment. It will be important to know whether the individual differences in resting PetCO₂ in the study reported here reflect differences in breathing patterns and whether those differences are due to history or genetic endowment. Previous research has found that humans with high resting PetCO₂ tend to breathe slowly and that those with low resting PetCO₂ tend to breathe more rapidly (25). When people become very anxious, breathing increases above the metabolic usage of O₂ and production of CO₂, resulting in decreases in pCO₂ (26). Resting PetCO₂ has been found to be lower in patients with panic disorders than in control subjects (27, 28). Because PetCO₂ tends to be lower in anxious individuals, it is unlikely that the emotional state identified by the neuroticism scale that accompanies high resting PetCO₂ is high trait anxiety. Possibly the emotional state associated with high PetCO₂ would be identified as stressful and aversive, but it is distinct from acute anxiety. Confirmation of the hypothesis that high PetCO₂ assesses vigilance awaits the development of suitable methodology for reliable measurement of this state.

Chronic interruption of breathing (ie, apnea) during sleep has been reported to be more prevalent among women than men, and hypertensive patients are known to have a greater prevalence of sleep apnea than normotensive control subjects (29). Interestingly, individuals with sleep apnea have been found to have a higher resting daytime pCO₂ than those without sleep apnea (30). The hypothesis that the set point for pCO₂ is a function of long-term breathing habits is consistent not only with the finding of a lower resting PetCO₂ in subjects with panic reaction (28) but also with the anecdotal observation that pearl divers tend to have high resting PetCO₂ (25). Blood pressure sensitivity to high sodium intake has been reported to be greater in older women than in older men (31), and high resting PetCO₂ is reportedly a marker for blood pressure sensitivity to high sodium intake (18, 19).

The origins of the gender differences in the association of high resting PetCO₂ with SBP remain to be clarified. In men resting PetCO₂ decreases progressively across the life span, whereas in women it remains stable across the life span (32). The association of resting PetCO₂ with SBP has been shown to be greater in older than in younger women (20). The observed gender difference may be related, therefore, to the fact that older men have lower resting PetCO₂ than older women. A recent study of patients with borderline hypertension who were not taking medication found that 24-hour ambulatory SBP was higher in women with high anger-in than in women with low anger-in (33). No such associations were found in male patients. In this regard, a recent theoretical article (34) has amassed evidence indicating gender differences in physiological responses to threat; the evidence indicates that females inhibit the characteristically male, sympathetically mediated "fight or flight" response and show parasympathetically mediated increases in oxytocin and reproductive hormones that support self-protective behaviors. It would be of interest to study whether breathing inhibition is associated with this self-protective response.

In summary, the results of this study are consistent with the view that elevations in resting blood pressure can be potentiated by either of two different behavioral/emotional states, one associated with anger and sympathetic nervous system arousal and another associated with a nonanger arousal, inhibition of breathing, and changes in blood gases. Both could affect blood pressure through their effects on renal regulation of sodium (15). Additional studies are needed to determine the origins of the gender differences in the association of PetCO₂ with SBP, the mechanism by which high PetCO₂ impacts sodium sensitivity, and its implications for the observed gender differences in the prevalence of hypertension across the life span.

Received for publication September 8, 1999.

	REFERENCES

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

 

1. Alexander F. Emotional factors in essential hypertension. Psychosom Med 1939; 1: 175–9.
2. Diamond EL. The role of anger and hostility in essential hypertension and coronary artery disease. Psychol Bull 1982; 92: 410–33.[Medline]
3. Jorgensen RS, Johnson BT, Kolodziej ME, Schreer GE. Elevated blood pressure and personality: a meta-analytic review. Psychol Bull 1996; 120: 293–320.[Medline]
4. Suls J, Wan CK, Costa PK. Relationship of trait hostility to resting blood pressure: a meta analysis. Health Psychol 1995; 14: 444–56.[Medline]
5. Funkenstein DH, King SH, Drolette ME. Mastery of stress. Cambridge (MA): Harvard University Press; 1957.
6. Johnson EH, Spielberger CD. Assessment of the experience, expression, and control of anger in hypertension research.In: Johnson EH, Gentry WD, Julius S, editors. Personality, elevated blood pressure, and essential hypertension. Washington DC: Hemisphere; 1992.p. 3–24.
7. Everson SA, Goldberg DE, Kaplan GA, Julkunen J, Salonen JT. Anger expression and incident hypertension. Psychosom Med 1998; 60: 730–5.[Abstract/Free Full Text]
8. Esler M. Biochemical evidence for sympathetic overactivity in human hypertension.In: Julius S, Bassett DR, editors. Handbook of hypertension. Vol 9: Behavioral factors in hypertension. New York: Elsevier; 1987.p. 75–94.
9. DeQuattro V, Sullivan P, Foti A, Schoentgen S, Kollch R, Verasales G, Levine D. Central neurogenic mechanisms in hypertension and in postural hypertension.In: Laragh J, Buhler F, Seldin D, editors. Frontiers in hypertension research. New York: Springer-Verlag; 1981.p. 301–5.
10. Perini C, Muller FB, Ruachfleisch U, Buhler FH. Hyperadrenergic borderline hypertension is characterized by suppressed aggression. J Cardiovasc Pharmacol 1986; 6: 53–6.
11. Steptoe A, Fieldman G, Evans O, Perry L. Cardiovascular risk and responsivity to mental stress: the influence of age, gender and risk factors. J Cardiovasc Risk 1996; 3: 83–93.[Medline]
12. Anderson DE. Experimental behavioral hypertension in laboratory animals.In: Julius S, Bassett DR, editor. Handbook of hypertension. Vol 9: Behavioral factors in hypertension. New York: Elsevier; 1987.p. 226–45.
13. Anderson DE. Operant conditioning, sodium loading and experimental hypertension. J Cardiovasc Pharmacol 1986; 8 (Suppl 5): S23–30.
14. Fedorova OV, French AW, Anderson DE. Inhibition of erythrocyte Na, K-ATPase activity during anticipatory hypoventilation in micropigs. Am J Hypertens 1996; 9: 1126–31.[Medline]
15. Anderson DE, Bagrov AY, Austin JL. Inhibited breathing decreases renal sodium excretion. Psychosom Med 1995; 57: 373–80.[Abstract/Free Full Text]
16. Bagrov AY, Fedorova OV, Austin-Lane JL, Dmitrieva RI, Anderson DE. Endogenous marinobufagenin-like immunoreactive factor and Na+, K+ ATPase inhibition during voluntary hypoventilation. Hypertension 1995; 26: 781–8.[Abstract/Free Full Text]
17. Dhokalia A, Parsons DJ, Anderson DE. Resting end tidal CO₂ association with age, gender, and personality. Psychosom Med 1998; 60: 33–7.[Abstract/Free Full Text]
18. Anderson DE, Dhokalia A, Parsons DJ, Bagrov AY. End tidal CO₂: association with blood pressure response to sodium loading in older adults. J Hypertens 1996; 14: 1073–9.[Medline]
19. Anderson DE, Dhokalia, A Parsons DJ, Bagrov AY. Sodium sensitivity in young humans with high end tidal CO₂. J Hypertens 1998; 16: 1015–22.[Medline]
20. Anderson DE, Parsons DJ, Scuteri A. End tidal CO₂ is an independent determinant of systolic blood pressure in women. J Hypertens 1999; 17: 1073–9.[Medline]
21. Johnson EH, Greene AE. The interview method for assessing anger: development and validation.In: Johnson EH, Gentry WD, Julius S, editors. Personality, elevated blood pressure, and essential hypertension. Washington DC: Hemisphere; 1992.p. 25–65.
22. Sapira JD, Scheib ET, Moriarty R, Shapiro A. differences in perception between hypertensive and normotensive patients. Psychosom Med 1971; 33: 239–50.[Abstract/Free Full Text]
23. Goldstein M, Edelberg R, Meier CF, Davis L. Relationship of resting blood pressure and heart rate to experienced anger and expressed anger. Psychosom Med 1988; 50: 321–9.[Abstract/Free Full Text]
24. Dimsdale JE, Harburg E, Cottingen EM, Johnson EH. Anger coping styles, blood pressure and all-cause mortality: a follow-up in Tecumseh, Michigan (1971–1983). Am J Epidemiol 1986, 124: 220–3.[Abstract/Free Full Text]
25. Schaefer KE. Respiratory pattern and respiratory response to CO₂. J Appl Physiol 1958; 13: 1–14.[Abstract/Free Full Text]
26. Ley R, Yelich G. Fractional end tidal CO₂ as an index of the effects of stress on math performance and verbal memory of test anxious adolescents. Biol Psychol 1998; 49: 83–94.[Medline]
27. Hegel MT, Ferguson RJ. Psychophysiological assessment of respiratory function in panic disorder: evidence for a hyperventilation subtype. Psychosom Med 1997; 59: 224–30.[Abstract/Free Full Text]
28. Roth WT, Wilhelm FH, Trabert W. Voluntary breath holding in panic and generalized anxiety disorders. Psychosom Med 1998; 60: 671–9.[Abstract/Free Full Text]
29. Silverberg DS, Oksenberg A, Iaina A. Sleep related breathing disorders are common contributing factors to the production of essential hypertension but are neglected, underdiagnosed, and undertreated. Am J Hypertens 1997; 10: 1319–25.[Medline]
30. Gold AR, Schwartz AR, Wise RA, Smith PL. Pulmonary function and respiratory chemosensitivity in moderately obese patients with sleep apnea. Chest 1993; 103: 1325–9.[Abstract/Free Full Text]
31. Nestel PJ, Clifton PM, Noakes M, MacArthur R, Howe PR. Enhanced blood pressure response to dietary salt in elderly women, especially those with small waist:hip ratio. J Hypertens 1993; 11: 1387–94.[Medline]
32. Frassetto L, Sebastian A. Age and systemic acid-base equilibrium: analysis of published data. J Gerontol 1996; 51: 691–9.
33. Helmers KF, Baker B, O’Kelly B, Tobe S. Anger expression, gender and ambulatory blood pressure in mild, unmedicated adults with hypertension. Ann Behav Med 2000; 22: 60–4.[Medline]
34. Taylor SE, Klein LC, Lewis BP, Gruenewald TL, Gurung RAR, Updegraff JA. Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol Rev 2000; 107: 411–29.[Medline]

This article has been cited by other articles:

				T. M. Starner and R. M. Peters Anger Expression and Blood Pressure in Adolescents The Journal of School Nursing, December 1, 2004; 20(6): 335 - 342. [Abstract] [Full Text] [PDF]

				I. Van Diest, S. Vuerstaek, I. Corne, S. De Peuter, S. Devriese, K. P. Van de Woestijne, and O. Van den Bergh Resting End-Tidal CO2 and Negative Affectivity Psychosom Med, November 1, 2003; 65(6): 976 - 983. [Abstract] [Full Text] [PDF]

				P. M. Eng, G. Fitzmaurice, L. D. Kubzansky, E. B. Rimm, and I. Kawachi Anger Expression and Risk of Stroke and Coronary Heart Disease Among Male Health Professionals Psychosom Med, January 1, 2003; 65(1): 100 - 110. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Scuteri, A. Articles by Anderson, D. E. Search for Related Content PubMed PubMed Citation Articles by Scuteri, A. Articles by Anderson, D. E. Related Collections Personality Pulmonary Blood Pressure