77
Journal ofAffective Disorders, 1 (1979) 77-92 0 Elsevier/North-Holland Biomedical Press
AFFECT
AND THE MENSTRUAL
LORRAINE
DENNERSTEIN
Department
of Psychiatry,
CYCLE
1 and GRAHAM University
D. BURROWS
of Melbourne,
2
Melbourne
(Australia)
SUMMARY Evidence from both retrospective and prospective studies suggests that many women do show cyclical changes in affect. Negative changes such as irritability, headache, tension, anxiety, sleep disturbance and depression are more frequent in the premenstrual and menstrual phases. Positive changes, pleasantness, increased vigour and elation are reported more often in the follicular or mid-cycle phases. Various theories have been suggested to explain these changes. These include psychodynamic, sociological and biological explanations. Although there is some evidence to support each theory no definite conclusions can be reached about the aetiological basis of most affective changes. Interpretation of studies attempting to link hormonal and affective fluctuations is limited by the many methodological problems outlined. Only one study appeared able to conclusively demonstrate a hormonal basis for a cyclical symptom. Suggestions are made for further research in this area.
HISTORICAL
Throughout the ages myths and superstitions have surrounded the menstrual cycle. A menstruating woman appears to have generally caused fear, evidenced in the taboos and regulations of many cultures (Ihalainen 1975). Ancient customs of the Yolngu Aborigines called for menstrual isolation, dietary restrictions and a spiritual cleansing by being passed through the fumes of a smokey fire at the conclusion of menstruation (Money et al. 1977). The Hebrews also isolated women during menstruation and for seven days thereafter and prescribed rituals for concluding the period of ‘uncleanness’. Wundt (1906) claimed that taboos have their origin in the fear of demonic powers. Menstruating women were credited with such powers in some cultures. The Natural History of Pliny (37-79 A.D.), Book VII, Chapter XV, asserts that such a woman sours wine, destroys the crops, dries
Reprint requests to: Dr. Lorraine Dennerstein, Melbourne Hospital, Melbourne, Victoria 3050, l Clinical Supervisor. z First Assistant.
Department Australia.
of Psychiatry,
c/o P.O. Royal
78
the garden, makes fruit fall from the trees and kills bees (Ricci 1943). The Folklore Archives of the Finnish Literature Society noted the belief that a woman cannot churn butter during menstruation (Ihalainen 1975). Recognition of the existence of a relationship between gonadal function and behavioural changes may be inferred from these and other folklore references. In France such beliefs have been embodied in legal statutes, so that a woman who commits a crime during her premenstrual period may use this fact in her defence, claiming temporary impairment of sanity (Katchadourian and Lunde 1975). The demonstration this century of the changing hormonal environment during the menstrual cycle has stimulated many studies attempting to correlate hormonal variations with behavioural and systemic changes (Southam and Gonzaga 1965). A review of the systemic changes associated with the menstrual cycle is not within the scope of the present paper which will focus on affect. DEFINITION
OF AFFECT
Affect refers to specific patterns of behavioural, subjective and physiological responses to underlying psychobiological states and includes both selfperception, or mood, and observable behavioural and physiological signs (Klerman 1977). TYPES OF AFFECTIVE
CHANGES
Minor premenstrual changes described by Greek physicians of the Hippocratic period included a sense of heaviness, headache, ringing in the ears and specks before the eyes (Ricci 1943). Frank (1931) reported that fatigue, irritability and lack of concentration were increased in the premenstruum. He introduced the term ‘premenstrual tension’ to describe a specific and severe affective syndrome present in the 10-7 days preceding menstruation. This was characterised by a ‘feeling of indescribable tension . . . unrest, ‘like jumping out of their skin’ and ‘a desire to find relief by irritability’, ‘Suicidal desire’ was present premenfoolish and ill-considered actions’. strually in two of the 15 cases he reported. Israel (1938) claimed that women suffering from premenstrual tension suffered ‘a cyclic alteration of personality’ during the lo-14 days prior to the expected menstruation. In addition to tension he described unreasonable emotional outbursts, ceaseless crying spells, insomnia, vertigo, headache and ‘nymphomania’. Both authors agreed that the syndrome disappeared dramatically with the onset of menstruation. Later authors have more broadly defined a premenstrual syndrome as a cluster of symptoms both psychological and physical, which appear episodically in relation to the phases of the menstrual cycle (Dalton 1964; Sutherland and Stewart 1965; Beumont et al. 1975). Although most common during the premenstruum, symptoms were sometimes present at ovulation or during the menses.
79
Some studies suggested that during the premenstruum and menstruation there was exacerbation of epilepsy and psychoses (Healey 1928), and an increase in acute psychiatric admissions (Dalton 1959; Janowsky et al. 1969), suicide (Ribeiro 1962) and attempted suicide (Dalton 1959). Others (Buckle et al. 1965; Holding and Minkoff 1973) found no association between attempted suicide and menstrual cycle phases. PREVALENCE
A number of studies have sought to estimate the frequency of cyclical affective symptoms. Kessel and Coppen (1963) and Sutherland and Stewart (1965) both found a high frequency of symptoms in the premenstruum. The latter study reported that some premenstrual mood change of irritability and/or depression occurred in nearly 70% of their subjects, while 32% complained of headaches. Only 13% reported no constant premenstrual molimina. The mood change was of a moderate to severe degree in up to 23% of women studied (Kessel and Coppen 1963). Actual estimates of the incidence of the premenstrual tension syndrome have varied from 30 to 79% depending on the definition of the syndrome, sampling procedures and method (Dalton 1964). As most of these studies were based on retrospective reporting via questionnaire surveys it is relevant to note that several authors have found discrepancies between retrospective reporting of menstrual cycle changes and actual findings from prospective data collected each day. McCance et al. (1937) reported these discrepancies to be so great as to ‘throw considerable doubt upon the value of any work on this subject based upon histories or a questionnaire’. May (1976) also reported finding no relationship between retrospective interview reporting of mood changes and daily records. Prospective studies of affective fluctuations during the menstrual cycle are of necessity small in sample size and consequently the sample is more likely to be biased. This type of investigation requires highly motivated and cooperative women. Not surprisingly, volunteers for such studies are most commonly tertiary students, health professionals or their wives, who are hardly representative of the general public. Some investigators have used patient groups. Benedek and Rubenstein (1939a) studied neurotic women who were being treated with psychoanalysis. Such studies are of limited value in demonstrating the prevalence of affective changes in the community. Their main usefulness has been to depict the pattern of affective fluctuations during the menstrual cycle so as to help ascertain their aetiology. PATTERN
OF AFFECTIVE
FLUCTUATIONS
Most prospective studies have presumed a hormonal aetiology of affective changes. The findings of 24 prospective studies of affective fluctuations during the menstrual cycle are summarized in Table 1. Unless otherwise
80 TABLE
1
AFFECTIVE Study
FLUCTUATIONS
and year
DURING
MENSTRUAL
CYCLE
n
Time (months)
Cycle marker
Method
167
6
standardised
ordinal
4-15
vaginal cytology
psychoanalysis dreams
of
?
vaginal cytology
psychoanalysis dreams
of
l-3
basal temperature
Gottschalk Verbal Anxiety Scale (VAS)
25
1
menses
movement and reaction times (on days 2, 8,18, 26).
26
2
menses
VAS (on days 14, 26).
8
2
standardised
Nowlis Mood Check List galvanic skin potential, flash threshold and time (on days 3,14, 24, 26, 28).
et al. (1969)
15
6
standardised
Moos Mental Distress Questionnaire (MDQ) Nowlis Mood Check List Plasma progesterone corticosteroid (on days 2, 7, 14, 19, 24, 25-28).
Morris and Udry (1970)
34
1-3
reverse cycle standardised
Paige (1971)
38
2
menses and basal temperature
VAS
6
2
plasma oestradiol and progesterone
migraine
11 40
1 1
menses menses
Watson-Glazer Critical Thinking (weekly)
11
l-2
reverse cycle
McCance
et al. (1937)
Benedek (1939a)
and Rubenstein
9
Benedek (1939b)
and Rubenstein
15
et al. (1962)
5
Gottschalk Pierson (1963)
and Lockhart
Ivey and Bardwick Kopell
Moos
(1968)
et al. (1969)
Somerville Sommer
Janowsky
(197 2) (1972)
et al. (1973)
day
day
mood
pedometer (days 4, 10, 16, 26).
Mood Scale weight 24-hour urinary K+/Na+
Test
81
Results
Presumed
menstrual
Premenstruum elation irritability fatigue headache tension depression intellectual
cycle Menses
phase Follicular
Mid-cycle
f
f 1 efficiency
no consistent c
well-being passive dependent neurotic conflicts
1‘
tension depression
:
anxiety
no change
reaction and movement times
no change
anxiety
t
time estimation other tests
no change
changes J
f
f
t
pleasantness anxiety aggression activation depression
t : no change
activity activity
no change t
anxiety hostility
:
migraine
t
intellectual performance
no change
negative weight K+/Na+
affect
:: t
t
f
f
Luteal
82 TABLE
1 (continued) _
Study
n
Time (months)
Cycle
Udry et al. (1973)
15
l-3
standardised
general
Zimmerman (1973)
14
menses and basal temperature
arm-hand steadiness galvanic skin response reaction time time estimation digitsymbol substitution self-rating mood mood - analogue scale urinary catecholamines
Patkai
and year
and Parlee
et al. (1974)
6
marker
Method
2
basal temperature and reverse cycle
Little and Zahn (1974)
12
1
basal temperature and reverse cycle
Nowlis List
Persky
21
1
menses and basal temperature
MMPI Hostility
(1974)
feelings
Mood
Check
anxiety depression lie Inventory
MDQ
Beck Depression Affect Check List Plasma oestradiol; progesterone; testosterone. (on days - menses - mid-cycle - premenstruum) Wuttke
et al. (1975)
Lewis and Burns Blackett-Smith
(1975) (1975)
16
1
plasma FSH, prolactin, progesterone, oestradiol.
2
3
menses
dream scoring (twice/week)
20
1
menses
mood questionnaire feminine-test arm-hand steadiness rod and frame test plasma oestradiol, progesterone,
LH,
reaction time calculation time EEG (every alternate day)
83
Results
Presumed
worse than usual better than usual arm-hand
all other
menstrual
cycle
Premenstruum
Menses
t
f
phase Follicular
Luteal
t
steadiness
tests
Mid-cycle
t
no significant
change
restlessness sleep length sleep disturbances urinary Ad, NAD depression elation vigour skin conductance “autonomic responsivity ” state
and trait
?: no change no change
tests
reaction time calculation time alpha band EEG frequency ’
no change
f
t
hostility fatigue other mood performance
t f and tests
no significant
changes
84 TABLE
1 (continued)
Study and year
n
Time (months)
Cycle marker
Method
testosterone, urinary total oestrogens (- follicular - mid-cycle - premenstruum) Beumont
et al. (1975)
32
1
menses
Beck Depression Symptom check - psychological - physical
list
plasma LH and progesterone for hysterectomised ? May (1976)
30
2
menses
elation -depression scale (on days 3, 14,
11
1
menses
MDQ
26) Wilcoxon
et al. (1976)
Nowlis Mood Check Pleasant Activities Schedule Personal Stress Inventory
indicated, data were collected daily during these studies. For ease of tabulation menstrual cycle phases were assigned as follows: menses-week beginning with onset of menses; follicular-week following menstrual week; mid-cycledays 14-15; luteal-week following mid-cycle; premenstruumweek preceding menses. Some cautious generalizations are possible. The majority of studies have found cyclical changes for negative moods. Irritability, restlessness, anxiety, tension, migraine, sleep disturbance, fatigue, impaired concentration, depression and increased neurotic conflicts were reported more frequently during the premenstrual and menstrual weeks. However some studies (for example, Little and Zahn 1974; Persky 1974) failed to find significant cyclical variations for many of these same moods, limiting any general conclusion. Positive moods were not assessed as frequently as negative moods. The data suggests increased feelings of well-being, elation, pleasantness and activation during the follicular and mid-cycle phases. No consistent pattern is evident from studies based on more objective tests of behaviour. Shortened calcula-
List
Results
Presumed
menstrual
Premenstruum
25 menstruating
Menses
Follicular
Mid-cycle
Luteal
t
1’ Q
7 hysterectomised
50% 40% 10%
phase
Q
Beck physical symptoms psychological symptoms
depression depression depression
cycle
Q Q Q
t
all tests no significant
t t
t
depression impaired concentration
:
t
stressful
f
t
events
changes
tion and reaction times during the premenstrual week were observed by Wuttke et al. (1975). Other studies report no significant cyclical changes in these or other tests (Pierson and Lockhart 1963; Kopell et al. 1969; Sommer 1972; Blackett-Smith 1975). AETIOLOGY
Various theories have been advanced ated with the menstrual cycle.
to explain
changes
in affect
associ-
Psychodynamic The perception of menstrual flow is claimed to intensify the woman’s preexisting conscious and unconscious conflicts about pregnancy, having a child, castration fears (mutilation, parturition and death), uncleanliness, lack of control of bodily function, aggression, penis envy and masturbation. In the presence of a vulnerable ego structure, neurotic or psychotic reactions
86
may occur (Deutsch 1944). Benedek and Rubenstein (1939b) using psychoanalytic techniques found that the premenstruum was associated with apprehension of what would happen to one’s body, fear of mutilation, recurrence of infantile sexual fantasies and intensification of neurotic conflicts. Other workers (Ivey and Bardwick 1968; Paige 1971) confirmed that the premenstrual phase in non-psychiatric populations was characterised by fears of mutilation and body change. Shainess (1961) suggested that premenstrual symptoms were a constant compulsive recapitulation of rejection of femininity and were directly related to unpleasant, humiliating or unloving experiences in relation to the mother. She found that women who had no symptoms of premenstrual tension had been prepared for the menarche by their mothers and were pleased at its occurrence. Berry and McGuire (1972) also found a significant negative association between physical symptoms of menstrual distress and role acceptance. Coppen and Kessel (1963) report that affective premenstrual symptoms were significantly correlated with neuroticism. Gruba and Rohrbaugh (1975) report similar findings.
Sociological Cyclical changes in affect may be socially learned. In a study of 255 women, Paulson (1961) found that 58% of the ‘high premenstrual tension’ group had mothers who suffered painful menstruation and premenstrual dysfunction while only 27% of the ‘low premenstrual tension’ group had symptomatic mothers. Parlee (1974) demonstrated the existence of stereotypic beliefs about menstruation. Both men and women reported expectations of women experiencing negative physical and affective changes in the premenstrual and menstrual phases. Koeske and Koeske (1973) demonstrated an attributional pattern, linking negative mood swings to the approach of menstruation. Further evidence of the influence of psychosocial factors on menstrual related symptoms was provided by Ruble (1977). She found that women who were led to believe that menses were due in one to two days reported a higher degree of distressing physical symptoms than those who believed they were intermenstrual. The two groups were in fact at identical phases of their cycles.
Biological The interesting report that almost all species of female primates observed in the field have cyclic irritability correlating with their fertility cycle (Janowsky et al. 1966) supports a biological basis for affective changes. Mechanisms proposed include the following: (a) High plasma oestrogen. Frank (1931) suggested that a high renal threshold for oestrogens resulted in ‘the continued circulation of an excessive amount of female sex hormone in the blood’. He reported that premenstrual tension was relieved by irradiation of ovaries. (b) Decreased progesterone production. Israel (1938) proposed that the
primary cause of premenstrual tension is a deficient ovarian luteinization. Both mechanisms (a) and (b) involve a postulated excess of oestrogen, either absolute or relative to available progesterone. The result is a high oestrogen to progesterone ratio. A major inconsistency is that the oestrogen to progesterone ratio is at its highest in the first half of the cycle when affective symptoms are most infrequent (Smith 1976). Backstrom and Carstensen (1974) report finding significantly higher oestrogen-progesterone ratios on days 6-3 before menstruation in women with premenstrual anxiety and irritability compared with a control group of healthy women. Smith (1976) reports that premenstrual depression sufferers had slightly lower progesterone levels than normal women during the seven days preceding menses. No difference was found in the oestrogen/progesterone ratio. Although progesterone has been claimed to alieviate premenstrual tension (Greenblatt et al. 1941; Dalton 1964) a double-blind study found that intramuscular progesterone was no more effective in the treatment of premenstrual depression than a placebo (Smith 1976). (c) Excessive aldosterone action. This may reflect increased aldosterone secretion or insufficient progesterone to antagonise aldosterone effects on renal sodium reabsorption (Dalton 1964), leading to accumulation of fluid. Janowsky et al. (1973) observed parallel changes in negative affect, weight and 24-h urinary potassium/sodium ratios. They postulated a renin-angiotensin-aldosterone hypothesis, suggesting that the causative factor of affective changes may be a substance fluctuating in parallel with aldosterone such as angiotensin which has been shown to affect central neurotransmitters. This may be activated by renin in response to elevated progesterone levels. Other workers (Bruce and Russell 1962) found no relationship between increased body weight and fluid retention and premenstrual symptoms. (d) Monoamine theory. Variation in levels of oestrogen and progesterone in the luteal phase of the menstrual cycle causes a decrease in brain serotonin and dopamine resulting in depression and an increase in serum prolactin sufficient to cause salt and water retention (Judd and McMurdo 1976). Animal studies have shown that the activity of monoamine oxidase changes cyclically in the rat hypothalamus, amygdala, adrenals and ovaries (Kamberi and Kobayashi 1970). Klaiber et al. (1971) found that plasma monoamine oxidase activity varied significantly with menstrual cycle phase. Increasing plasma oestrogen reduced monoamine oxidase activity whereas administration of oestrogen plus progestogen increased monoamine oxidase activity. A cyclic pattern of monoamine oxidase activity has also been observed in the uterine endometrium by Cohen et al. (1964). Using histochemical techniques they found more diffuse and intense monoamine oxidase activity later in the cycle. Women who suffer from premenstrual tension were found to have higher plasma prolactin levels than a control group (Halbreich et al. 1970). Whether this is cause or effect is not clear as the authors noted that prolactin levels
88
may be raised by stress. Graham et al. (1979) conducted a double blind study of a prolactin antagonist (bromocryptine). They found a significant improvement of affect in women treated with bromocryptine as compared with placebo. It is not known whether this effect was mediated by suppression of prolactin secretion or whether it reflected other effects of bromocryptine such as dopamine agonist actions. DISCUSSION
Seemingly contradictory findings may be partly explained by differences in methodology which limit any general interpretation of these studies. An example is the diversity of assessment techniques used. The types of measurement selected have often reflected different and conflicting theories of behaviour. For example, Benedek and Rubenstein (1939) used psychoanalytic techniques of dream interpretation and free association in an attempt to explore unconscious ‘instinctual’ changes. Persky’s approach reflected state and trait theories of personality and behaviour (Persky 1974). The validity of self-report as a tool to reflect the symptoms accompanying the menstrual cycle has been questioned by some workers. Few studies used a ‘cover story’ to minimize the subject’s awareness of the investigators’ objectives, despite the considerable evidence to indicate that subjects’ expectations can substantially influence behavioural findings in research (Orne 1962; Weber and Cook 1972). Beumont et al. (1975) attempted to control for subjects’ expectations by including a control group of 7 hysterectomized women. Other workers used indices of change that do not rely on subjective reports (Pierson and Lockhart 1963; Morris and Udry 1970). Some studies (McCance et al., 1939; Benedek and Rubenstein 1939) reported no statistical analysis of reports whereas later studies differentiated findings that had a low probability of occurring by chance (Beumont et al. 1975; Wilcoxon et al. 1976). An important aspect of analyses was highlighted by May (1976). He reported no change in mood when results of the women studied were averaged. When individual patterns of mood change were examined two main groups were identified; those women experiencing lowest mood at the premenstruum and those whose lowest mood coincided with menstruation. The greatest difficulty in interpretation relates to the differing and usually inadequate methods used of assigning behaviour to menstrual cycle phases. Many studies have used the onset of menses as the cycle marker. ‘If all women had the same length of menstrual cycle, with no inter- or intrapersonal variance, and if hormonal events could be presumed to proceed in an invariant pattern during every cycle, the menstrual marker would be an adequate reference point for the association of behavioural observations and hormonal events. There is, however, no such regularity’ (Udry and Morris 1977). Different methods have been used to organize data from cycles of disparate lengths. These techniques are based upon certain theoretical
89
assumptions about the procession of hormonal events in cycles. One example is to use a standardised cycle of an arbitrary length, usually 28 days, the assumption being that the pace of hormonal events is directly proportional to cycle length. Longer cycles are squeezed together while shorter cycles are proportionately lengthened (Kopell et al. 1969; Moos et al. 1969). Others have assumed that irregularities in cycle length occur before ovulation and that the time duration between ovulation and onset of next menstruation is a constant. The cycle phase is assigned by counting backwards from the onset of menses (reverse cycle day). That the use of these two differing techniques may influence the results obtained is demonstrated in the study of Morris and Udry (1970). When pedometer readings were analysed using reverse cycle day, no consistent change in physical activity was found. Significant changes in physical activity levels were evident on using the technique of standardised cycle day. The problem with these differing techniques which rely ultimately upon menstruation as the cycle marker, is that little can be deduced about actual hormonal events within the cycle. Some workers attempted to identify the menstrual cycle phases more accurately by using the basal temperature chart, the presumption being that the thermal nadir coincides with ovulation (Gottschalk et al. 1962). Lenton et al. (1977) were able to assess the accuracy of basal body temperature in predicting ovulation in 60 cycles for which both basal temperature charts and hormonal profiles were available. It was found that 80% of temperature charts were correctly interpreted as being ovulatory or anovulatory but the day of ovulation was predicted correctly in only 34% of cycles. The thermal nadir coincided with the luteinising hormone surge in 43% of the charts from normal subjects. It was concluded that predicting the day of ovulation from the temperature recording was unjustified. Udry and Morris (1977) suggested that fluctuations in steroid hormones and perhaps gonadotrophins must be assessed during the menstrual cycle in order to correlate any changes in behaviour patterns with the variations in levels of ovarian and pituitary hormones. That hormonal changes may underly certain affective changes was elegantly demonstrated by Somerville (1972), who studied 6 women who suffered a pattern of regularly recurring menstrual migraine. He demonstrated that falling levels of oestradiol, rather than progesterone, in some way triggered off migraine in susceptible women. The migraine attacks were not affected by injections of progesterone but could be postponed by maintaining high plasma oestradiol levels with injections of oestradiol valerate. In conclusion it is suggested that future studies in this area may be more useful in elucidating hormonal aetiology if, they meet the following criteria: adequate definition of, prospective; and measurement of subjective changes; intensive studies of women who suffer a particular change; determination of each woman’s pattern over several cycles; correlation of affective changes with day-by-day plasma levels of endogenous hormones; doubleblind investigations of subsequent hypotheses.
90 REFERENCES Backstrom, T. and Carstensen, H., Estrogen and progesterone in plasma in relation to premenstrual tension, J. Steroid Biochem., 5 (1974) 257-260. Benedek, T. and Rubenstein, B.B., The correlations between ovarian activity and psychodynamic processes, Part 1 (The ovulative phase), Psychosom. Med., 1 (1939a) 245270. Benedek, T. and Rubenstein, B.B., The correlations between ovarian activity and psychodynamic processes, Part 2 (The menstrual phase), Psychosom. Med., 1 (193913) 461485. Berry, C. and McGuire, F.L., Menstrual distress and acceptance of sexual role, Amer. J. Obstet. Gynecol., 114 (1972) 83-87. Beumont, P.J.V., Richards, D.H. and Gelder, M.G., A study of minor psychiatric and physical symptoms during the menstrual cycle, Brit. J. Psychiat., 126 (1975) 431434. Blackett-Smith, J.J., The Menstrual Cycle - Interactions Between Social Factors, Mood, Hormones and Task Performance, Unpublished B. Med. Sci. Thesis, Monash University, Victoria, Australia, 1975. Bruce, J. and Russell, G.F.M., Premenstrual tension-A study of weight changes and balances of water, sodium and potassium, Lancet, 2 (1962) 267-271. Buckle, R.C., Linnane, J. and McConachy, N., Attempted suicide presenting at the Alfred Hospital, Melbourne, Med. J. Aust., 1 (1965) 754-758. Cohen, S., Bitensky, L., Chayen, J., Cunningham, G.J. and Russell, J.K., Histochemical studies on the human endometrium, Lancet, 2 (1964) 56-59. Coppen, A. and Kessel, N., Menstruation and personality, Brit. J. Psychiat., 109 (1963) 711-721. Dalton, K., Menstruation and acute psychiatric illnesses, Brit. med. J., 1 (1959) 148-149. Dalton, K., The Premenstrual Syndrome, William Heinemann Medical Books Ltd., London, 1964. Deutsch, H., The Psychology of Women, Grune and Stratton, New York, NY, 1944. Frank, R.T., The hormonal causes of premenstrual tension, Arch. Neurol. Psychiat., 26 (1931) 1053-1057. Gottschalk, L.A., Kaplan, S.M., Gleser, G.C. et al., Variations in magnitude of emotion A method applied to anxiety and hostility during phases of the menstrual cycle, Psychosom. Med., 24 (1962) 300-311. Graham, J.J., Harding, P.E., Wise, P.H. and Berriman, H., Prolactin suppression in the treatment of premenstrual syndrome, Med. J. Aust., (1979) In press. Greenblatt, R.B., McCall, E. and Torpin, R., Oral progestin (anhydro-hydroxy-progesterone) in the treatment of dysmenorrhoea, Amer. J. Obstet. Gynecol., 42 (1941) 5053. Gruba, G.H. and Rohrbaugh, M., MMPI correlates of menstrual distress, Psychosom. Med., 37 (1975) 265-273. Halbreich, U., Assael, M., Ben-David, M. and Bornstein, R., Serum-prolactin in women with premenstrual syndrome, Lancet, 2 (1976) 654-656. Healey, F.H., Menstruation in relation to mental disorders, J. ment. Sci., 74 (1928) 488492. Holding, T.A. and Minkoff, K., Parasuicide and the menstrual cycle, J. psychosom. Res., 17 (1973) 365-368. Ihalainen, O., Psychosomatic aspects of amenorrhoea, Acta psychiat. stand., Suppl., 262 (1975). Israel, S.L., Premenstrual tension, J. Amer. med. Ass., 110 (1938) 1721-1723. Ivey, M.E. and Bardwick, J.M., Patterns of affective fluctuation in the menstrual cycle, Psychosom. Med., 30 (1968) 336-345.
91 Joanowsky, D.S., Gorney, R. and Kelley, B., The curse-vicissitudes and variations of the female fertility cycle, Psychosomatics, 7 (1966) 242-247. Janowsky, D.S., Berens, S.C. and Davis, J.M., Correlations between mood, weight and electrolytes during the menstrual cycle - A renin-angiotensin-aldosterone hypothesis of premenstrual tension, Psychosom. Med., 35 (1973) 143-154. Janowsky, D.S., Gorney, R., Castelnuovo-Tedesco, P. et al., Premenstrual-menstrual increases in psychiatric hospital admission rates, Amer. J. Obstet. Gynecol., 103 (1969) 189-191. Judd, S. and McMurdo, R., The premenstrual syndrome. In: J. Ellard (Ed.), Psychiatry for the Non-Psychiatrist, Geigy Pharmaceuticals, 1976, pp. 80-82. Kamberi, I.A. and Kobayashi, Y., Monoamine oxidase activity in the hypothalamus and various other brain areas and in some endocrine glands of the rat during the estrus cycle, J. Neurochem., 17 (1970) 261-268. Katchadourian, H.A. and Lunde, D.T., Fundamentals of Human Sexuality, 2nd edition, Holt, Rinehart and Winston, New York, NY, 1975, p. 100. Kessel, N. and Coppen, A., The prevalence of common menstrual symptoms, Lancet, 2 (1963) 61-64. Klaiber, E.L., Kobayashi, Y., Broverman, D.M. and Hall, F., Plasma monoamine oxidase activity in regularly menstruating women and in amenorrhoeic women receiving cyclic treatment with estrogens and a progestin, J. clin. endocrinol. Metab., 33 (1971) 630638. Klerman, G.L., Anxiety and depression. In: G.D. Burrows (Ed.), Handbook of Studies on Depression, Excerpta Medica, Amsterdam, 1977, pp. 49-68. Koeske, R.K. and Koeske, G.F., An attributional approach to moods and the menstrual cycle, J. pers. sot. Psychol., 31 (1973) 473-478. Kopell, B.S., Lunde, D.T., Clayton, R.B. and Moos, R.H., Variations in some measures of arousal during the menstrual cycle, J. nerv. ment. Dis., 148 (1969) 180-187. Lenton, E.A., Weston, G.A. and Cooke, I.D., Problems in using basal body temperature recordings in an infertility clinic, Brit. med. J., 1 (1977) 803-805. Lewis, S.A. and Burns, M., Manifest dream content - Changes with the menstrual cycle, Brit. med. J. Psychol., 48 (1975) 375-377. Little, B.C. and Zahn, T.P., Changes in mood and autonomic functioning during the menstrual cycle, Psychophysiology, 11 (1974) 579-590. McCance, R.A., Luff, M.C. and Widdowson, E.C., Physical and emotional periodicity in women, J. Hyg. Camb., 37 (1937) 571-605. May, R.R., Mood shifts and the menstrual cycle, J. psychosom. Res., 20 (1976) 125130. Money, J., Cawte, J.E., Bianchi, G.N. and Nurcombe, B., Sex training and traditions in Arnham Land. In: J. Money and H. Musaph (Eds.), Handbook of Sexology, Excerpta Medica, Amsterdam, 1977, pp. 519-541. Moos, R.H., Kopell, B.S., Melges, F.T. et al., Fluctuations in symptoms and moods during the menstrual cycle, J. psychosom. Res., 13 (1969) 37-44. Morris, N.M. and Udry, J.R., Variations in pedometer activity during the menstrual cycle, Obstet. Gynecol., 35 (1970) 199-201. Orne, M.T., On the social psychology of the psychological experiment-With particular reference to demand characteristics and their implications, Amer. J. Psychol., 17 (1963) 776-783. Paige, K.E., Effects of oral contraceptives on affective fluctuations associated with the menstrual cycle, Psychosom. Med., 33 (1971) 515-537. Parlee, M.B., Stereotypic beliefs about menstruation-A methodological note on the Moos Menstrual Distress Questionnaire and some new data, Psychosom. Med., 36 (1974) 229-240. Patkai, P., Johannson, G. and Post, B., Mood, Alertness and sympathetic-adrenal medullary activity during the menstrual cycle, Psychosom. Med., 36 (1974) 5033512.
92 Paulson, M.J., Psychological concomitants of premenstrual tension, Amer. J. Obstet. Gynecol., 81 (1961) 733--738. Persky, H., Reproductive hormones, moods and the menstrual cycle. In: R.C. Friedman (Ed.), Sex Differences in Behaviour, Wiley, New York, NY, 1974. Pierson, W.R. and Lockhart, A., Effect of menstruation on simple reaction and movement time, Brit. med. J., 1(1963) 796-797. Ribeiro, A.L., Menstruation and crime, Brit. med. J., 1 (1962) 640. Ricci, J.V., The Genealogy of Gynaecology, The Blakiston Company, Philadelphia, PA, 1943. Ruble, D.N., Premenstrual symptoms - A reinterpretation. Science, 197 (1977) 291292. Shainess, N., A re-evaluation of some aspects of femininity through a study of menstruation - A preliminary report, Compr. Psychiat., 2 (1961) 20-26. Smith, S.L., The menstrual cycle and mood disturbances, Clin. Obstet. Gynecol., 19 (1976) 391-397. Somerville, B.W., The role of estradiol withdrawal in the etiology of menstrual migraine, Neurology (Minneap.), 27 (1972) 355-365. Sommer, B., Menstrual cycle changes and intellectual performance, Psychosom. Med., 34 (1972) 263-268. Southam, A.L. and Gonzaga, F.P., Systemic changes during the menstrual cycle, Amer. J. Obstet. Gynecol., 91 (1965) 142-165. Sutherland, H. and Stewart, I., A critical analysis of the premenstrual syndrome, Lancet, l(l965) 1180-1183. Udry, J.R. and Morris, N.M., The distribution of events in the human menstrual cycle, J. Reprod. Fertil., 51 (1977) 419-425. Udry, J.R., Morris, N.M. and Waller, L., Effect of contraceptive pills on sexual activity of the luteal phase of the human menstrual cycle, Arch. sex. Behav., 2 (1973) 205-214. Weber, S.J. and Cook, T.D., Subject effects in laboratory research - An examination of subject roles, demand characteristics and valid inference, Psychol. Bull., 77 (1972) 273-295. Schrader, S.L. and Sherif, C.W., Daily self-reports on activities, life Wilcoxon, L.A., events, moods and somatic changes during the menstrual cycle, Psychosom. Med., 38 (1976) 399-417. Wundt, W., Mythus und Religion, Teil II (Volkerpsychologie, Band II), Leipzig, 1906. Quoted in S. Freud, Totem and Taboo, translated by J. Strachey, Routledge and Kegan Paul, London, 1972, p. 23. Wuttke, W., Arnold, P., Becker, D. et al., Circulating hormones, eeg, and performance in psychological tests of women with and without oral contraceptives, Psychoneuroendocrinology, l(l975) 141-151. Zimmerman, E. and Parlee, M.B., Behavioural changes associated with the menstrual cycle -An experimental investigation, J. appl. sot. Psychol., 3 (1973) 335-344.
Journal ofAffective Disorders, 1 (1979) 77-92 0 Elsevier/North-Holland Biomedical Press
AFFECT
AND THE MENSTRUAL
LORRAINE
DENNERSTEIN
Department
of Psychiatry,
CYCLE
1 and GRAHAM University
D. BURROWS
of Melbourne,
2
Melbourne
(Australia)
SUMMARY Evidence from both retrospective and prospective studies suggests that many women do show cyclical changes in affect. Negative changes such as irritability, headache, tension, anxiety, sleep disturbance and depression are more frequent in the premenstrual and menstrual phases. Positive changes, pleasantness, increased vigour and elation are reported more often in the follicular or mid-cycle phases. Various theories have been suggested to explain these changes. These include psychodynamic, sociological and biological explanations. Although there is some evidence to support each theory no definite conclusions can be reached about the aetiological basis of most affective changes. Interpretation of studies attempting to link hormonal and affective fluctuations is limited by the many methodological problems outlined. Only one study appeared able to conclusively demonstrate a hormonal basis for a cyclical symptom. Suggestions are made for further research in this area.
HISTORICAL
Throughout the ages myths and superstitions have surrounded the menstrual cycle. A menstruating woman appears to have generally caused fear, evidenced in the taboos and regulations of many cultures (Ihalainen 1975). Ancient customs of the Yolngu Aborigines called for menstrual isolation, dietary restrictions and a spiritual cleansing by being passed through the fumes of a smokey fire at the conclusion of menstruation (Money et al. 1977). The Hebrews also isolated women during menstruation and for seven days thereafter and prescribed rituals for concluding the period of ‘uncleanness’. Wundt (1906) claimed that taboos have their origin in the fear of demonic powers. Menstruating women were credited with such powers in some cultures. The Natural History of Pliny (37-79 A.D.), Book VII, Chapter XV, asserts that such a woman sours wine, destroys the crops, dries
Reprint requests to: Dr. Lorraine Dennerstein, Melbourne Hospital, Melbourne, Victoria 3050, l Clinical Supervisor. z First Assistant.
Department Australia.
of Psychiatry,
c/o P.O. Royal
78
the garden, makes fruit fall from the trees and kills bees (Ricci 1943). The Folklore Archives of the Finnish Literature Society noted the belief that a woman cannot churn butter during menstruation (Ihalainen 1975). Recognition of the existence of a relationship between gonadal function and behavioural changes may be inferred from these and other folklore references. In France such beliefs have been embodied in legal statutes, so that a woman who commits a crime during her premenstrual period may use this fact in her defence, claiming temporary impairment of sanity (Katchadourian and Lunde 1975). The demonstration this century of the changing hormonal environment during the menstrual cycle has stimulated many studies attempting to correlate hormonal variations with behavioural and systemic changes (Southam and Gonzaga 1965). A review of the systemic changes associated with the menstrual cycle is not within the scope of the present paper which will focus on affect. DEFINITION
OF AFFECT
Affect refers to specific patterns of behavioural, subjective and physiological responses to underlying psychobiological states and includes both selfperception, or mood, and observable behavioural and physiological signs (Klerman 1977). TYPES OF AFFECTIVE
CHANGES
Minor premenstrual changes described by Greek physicians of the Hippocratic period included a sense of heaviness, headache, ringing in the ears and specks before the eyes (Ricci 1943). Frank (1931) reported that fatigue, irritability and lack of concentration were increased in the premenstruum. He introduced the term ‘premenstrual tension’ to describe a specific and severe affective syndrome present in the 10-7 days preceding menstruation. This was characterised by a ‘feeling of indescribable tension . . . unrest, ‘like jumping out of their skin’ and ‘a desire to find relief by irritability’, ‘Suicidal desire’ was present premenfoolish and ill-considered actions’. strually in two of the 15 cases he reported. Israel (1938) claimed that women suffering from premenstrual tension suffered ‘a cyclic alteration of personality’ during the lo-14 days prior to the expected menstruation. In addition to tension he described unreasonable emotional outbursts, ceaseless crying spells, insomnia, vertigo, headache and ‘nymphomania’. Both authors agreed that the syndrome disappeared dramatically with the onset of menstruation. Later authors have more broadly defined a premenstrual syndrome as a cluster of symptoms both psychological and physical, which appear episodically in relation to the phases of the menstrual cycle (Dalton 1964; Sutherland and Stewart 1965; Beumont et al. 1975). Although most common during the premenstruum, symptoms were sometimes present at ovulation or during the menses.
79
Some studies suggested that during the premenstruum and menstruation there was exacerbation of epilepsy and psychoses (Healey 1928), and an increase in acute psychiatric admissions (Dalton 1959; Janowsky et al. 1969), suicide (Ribeiro 1962) and attempted suicide (Dalton 1959). Others (Buckle et al. 1965; Holding and Minkoff 1973) found no association between attempted suicide and menstrual cycle phases. PREVALENCE
A number of studies have sought to estimate the frequency of cyclical affective symptoms. Kessel and Coppen (1963) and Sutherland and Stewart (1965) both found a high frequency of symptoms in the premenstruum. The latter study reported that some premenstrual mood change of irritability and/or depression occurred in nearly 70% of their subjects, while 32% complained of headaches. Only 13% reported no constant premenstrual molimina. The mood change was of a moderate to severe degree in up to 23% of women studied (Kessel and Coppen 1963). Actual estimates of the incidence of the premenstrual tension syndrome have varied from 30 to 79% depending on the definition of the syndrome, sampling procedures and method (Dalton 1964). As most of these studies were based on retrospective reporting via questionnaire surveys it is relevant to note that several authors have found discrepancies between retrospective reporting of menstrual cycle changes and actual findings from prospective data collected each day. McCance et al. (1937) reported these discrepancies to be so great as to ‘throw considerable doubt upon the value of any work on this subject based upon histories or a questionnaire’. May (1976) also reported finding no relationship between retrospective interview reporting of mood changes and daily records. Prospective studies of affective fluctuations during the menstrual cycle are of necessity small in sample size and consequently the sample is more likely to be biased. This type of investigation requires highly motivated and cooperative women. Not surprisingly, volunteers for such studies are most commonly tertiary students, health professionals or their wives, who are hardly representative of the general public. Some investigators have used patient groups. Benedek and Rubenstein (1939a) studied neurotic women who were being treated with psychoanalysis. Such studies are of limited value in demonstrating the prevalence of affective changes in the community. Their main usefulness has been to depict the pattern of affective fluctuations during the menstrual cycle so as to help ascertain their aetiology. PATTERN
OF AFFECTIVE
FLUCTUATIONS
Most prospective studies have presumed a hormonal aetiology of affective changes. The findings of 24 prospective studies of affective fluctuations during the menstrual cycle are summarized in Table 1. Unless otherwise
80 TABLE
1
AFFECTIVE Study
FLUCTUATIONS
and year
DURING
MENSTRUAL
CYCLE
n
Time (months)
Cycle marker
Method
167
6
standardised
ordinal
4-15
vaginal cytology
psychoanalysis dreams
of
?
vaginal cytology
psychoanalysis dreams
of
l-3
basal temperature
Gottschalk Verbal Anxiety Scale (VAS)
25
1
menses
movement and reaction times (on days 2, 8,18, 26).
26
2
menses
VAS (on days 14, 26).
8
2
standardised
Nowlis Mood Check List galvanic skin potential, flash threshold and time (on days 3,14, 24, 26, 28).
et al. (1969)
15
6
standardised
Moos Mental Distress Questionnaire (MDQ) Nowlis Mood Check List Plasma progesterone corticosteroid (on days 2, 7, 14, 19, 24, 25-28).
Morris and Udry (1970)
34
1-3
reverse cycle standardised
Paige (1971)
38
2
menses and basal temperature
VAS
6
2
plasma oestradiol and progesterone
migraine
11 40
1 1
menses menses
Watson-Glazer Critical Thinking (weekly)
11
l-2
reverse cycle
McCance
et al. (1937)
Benedek (1939a)
and Rubenstein
9
Benedek (1939b)
and Rubenstein
15
et al. (1962)
5
Gottschalk Pierson (1963)
and Lockhart
Ivey and Bardwick Kopell
Moos
(1968)
et al. (1969)
Somerville Sommer
Janowsky
(197 2) (1972)
et al. (1973)
day
day
mood
pedometer (days 4, 10, 16, 26).
Mood Scale weight 24-hour urinary K+/Na+
Test
81
Results
Presumed
menstrual
Premenstruum elation irritability fatigue headache tension depression intellectual
cycle Menses
phase Follicular
Mid-cycle
f
f 1 efficiency
no consistent c
well-being passive dependent neurotic conflicts
1‘
tension depression
:
anxiety
no change
reaction and movement times
no change
anxiety
t
time estimation other tests
no change
changes J
f
f
t
pleasantness anxiety aggression activation depression
t : no change
activity activity
no change t
anxiety hostility
:
migraine
t
intellectual performance
no change
negative weight K+/Na+
affect
:: t
t
f
f
Luteal
82 TABLE
1 (continued) _
Study
n
Time (months)
Cycle
Udry et al. (1973)
15
l-3
standardised
general
Zimmerman (1973)
14
menses and basal temperature
arm-hand steadiness galvanic skin response reaction time time estimation digitsymbol substitution self-rating mood mood - analogue scale urinary catecholamines
Patkai
and year
and Parlee
et al. (1974)
6
marker
Method
2
basal temperature and reverse cycle
Little and Zahn (1974)
12
1
basal temperature and reverse cycle
Nowlis List
Persky
21
1
menses and basal temperature
MMPI Hostility
(1974)
feelings
Mood
Check
anxiety depression lie Inventory
MDQ
Beck Depression Affect Check List Plasma oestradiol; progesterone; testosterone. (on days - menses - mid-cycle - premenstruum) Wuttke
et al. (1975)
Lewis and Burns Blackett-Smith
(1975) (1975)
16
1
plasma FSH, prolactin, progesterone, oestradiol.
2
3
menses
dream scoring (twice/week)
20
1
menses
mood questionnaire feminine-test arm-hand steadiness rod and frame test plasma oestradiol, progesterone,
LH,
reaction time calculation time EEG (every alternate day)
83
Results
Presumed
worse than usual better than usual arm-hand
all other
menstrual
cycle
Premenstruum
Menses
t
f
phase Follicular
Luteal
t
steadiness
tests
Mid-cycle
t
no significant
change
restlessness sleep length sleep disturbances urinary Ad, NAD depression elation vigour skin conductance “autonomic responsivity ” state
and trait
?: no change no change
tests
reaction time calculation time alpha band EEG frequency ’
no change
f
t
hostility fatigue other mood performance
t f and tests
no significant
changes
84 TABLE
1 (continued)
Study and year
n
Time (months)
Cycle marker
Method
testosterone, urinary total oestrogens (- follicular - mid-cycle - premenstruum) Beumont
et al. (1975)
32
1
menses
Beck Depression Symptom check - psychological - physical
list
plasma LH and progesterone for hysterectomised ? May (1976)
30
2
menses
elation -depression scale (on days 3, 14,
11
1
menses
MDQ
26) Wilcoxon
et al. (1976)
Nowlis Mood Check Pleasant Activities Schedule Personal Stress Inventory
indicated, data were collected daily during these studies. For ease of tabulation menstrual cycle phases were assigned as follows: menses-week beginning with onset of menses; follicular-week following menstrual week; mid-cycledays 14-15; luteal-week following mid-cycle; premenstruumweek preceding menses. Some cautious generalizations are possible. The majority of studies have found cyclical changes for negative moods. Irritability, restlessness, anxiety, tension, migraine, sleep disturbance, fatigue, impaired concentration, depression and increased neurotic conflicts were reported more frequently during the premenstrual and menstrual weeks. However some studies (for example, Little and Zahn 1974; Persky 1974) failed to find significant cyclical variations for many of these same moods, limiting any general conclusion. Positive moods were not assessed as frequently as negative moods. The data suggests increased feelings of well-being, elation, pleasantness and activation during the follicular and mid-cycle phases. No consistent pattern is evident from studies based on more objective tests of behaviour. Shortened calcula-
List
Results
Presumed
menstrual
Premenstruum
25 menstruating
Menses
Follicular
Mid-cycle
Luteal
t
1’ Q
7 hysterectomised
50% 40% 10%
phase
Q
Beck physical symptoms psychological symptoms
depression depression depression
cycle
Q Q Q
t
all tests no significant
t t
t
depression impaired concentration
:
t
stressful
f
t
events
changes
tion and reaction times during the premenstrual week were observed by Wuttke et al. (1975). Other studies report no significant cyclical changes in these or other tests (Pierson and Lockhart 1963; Kopell et al. 1969; Sommer 1972; Blackett-Smith 1975). AETIOLOGY
Various theories have been advanced ated with the menstrual cycle.
to explain
changes
in affect
associ-
Psychodynamic The perception of menstrual flow is claimed to intensify the woman’s preexisting conscious and unconscious conflicts about pregnancy, having a child, castration fears (mutilation, parturition and death), uncleanliness, lack of control of bodily function, aggression, penis envy and masturbation. In the presence of a vulnerable ego structure, neurotic or psychotic reactions
86
may occur (Deutsch 1944). Benedek and Rubenstein (1939b) using psychoanalytic techniques found that the premenstruum was associated with apprehension of what would happen to one’s body, fear of mutilation, recurrence of infantile sexual fantasies and intensification of neurotic conflicts. Other workers (Ivey and Bardwick 1968; Paige 1971) confirmed that the premenstrual phase in non-psychiatric populations was characterised by fears of mutilation and body change. Shainess (1961) suggested that premenstrual symptoms were a constant compulsive recapitulation of rejection of femininity and were directly related to unpleasant, humiliating or unloving experiences in relation to the mother. She found that women who had no symptoms of premenstrual tension had been prepared for the menarche by their mothers and were pleased at its occurrence. Berry and McGuire (1972) also found a significant negative association between physical symptoms of menstrual distress and role acceptance. Coppen and Kessel (1963) report that affective premenstrual symptoms were significantly correlated with neuroticism. Gruba and Rohrbaugh (1975) report similar findings.
Sociological Cyclical changes in affect may be socially learned. In a study of 255 women, Paulson (1961) found that 58% of the ‘high premenstrual tension’ group had mothers who suffered painful menstruation and premenstrual dysfunction while only 27% of the ‘low premenstrual tension’ group had symptomatic mothers. Parlee (1974) demonstrated the existence of stereotypic beliefs about menstruation. Both men and women reported expectations of women experiencing negative physical and affective changes in the premenstrual and menstrual phases. Koeske and Koeske (1973) demonstrated an attributional pattern, linking negative mood swings to the approach of menstruation. Further evidence of the influence of psychosocial factors on menstrual related symptoms was provided by Ruble (1977). She found that women who were led to believe that menses were due in one to two days reported a higher degree of distressing physical symptoms than those who believed they were intermenstrual. The two groups were in fact at identical phases of their cycles.
Biological The interesting report that almost all species of female primates observed in the field have cyclic irritability correlating with their fertility cycle (Janowsky et al. 1966) supports a biological basis for affective changes. Mechanisms proposed include the following: (a) High plasma oestrogen. Frank (1931) suggested that a high renal threshold for oestrogens resulted in ‘the continued circulation of an excessive amount of female sex hormone in the blood’. He reported that premenstrual tension was relieved by irradiation of ovaries. (b) Decreased progesterone production. Israel (1938) proposed that the
primary cause of premenstrual tension is a deficient ovarian luteinization. Both mechanisms (a) and (b) involve a postulated excess of oestrogen, either absolute or relative to available progesterone. The result is a high oestrogen to progesterone ratio. A major inconsistency is that the oestrogen to progesterone ratio is at its highest in the first half of the cycle when affective symptoms are most infrequent (Smith 1976). Backstrom and Carstensen (1974) report finding significantly higher oestrogen-progesterone ratios on days 6-3 before menstruation in women with premenstrual anxiety and irritability compared with a control group of healthy women. Smith (1976) reports that premenstrual depression sufferers had slightly lower progesterone levels than normal women during the seven days preceding menses. No difference was found in the oestrogen/progesterone ratio. Although progesterone has been claimed to alieviate premenstrual tension (Greenblatt et al. 1941; Dalton 1964) a double-blind study found that intramuscular progesterone was no more effective in the treatment of premenstrual depression than a placebo (Smith 1976). (c) Excessive aldosterone action. This may reflect increased aldosterone secretion or insufficient progesterone to antagonise aldosterone effects on renal sodium reabsorption (Dalton 1964), leading to accumulation of fluid. Janowsky et al. (1973) observed parallel changes in negative affect, weight and 24-h urinary potassium/sodium ratios. They postulated a renin-angiotensin-aldosterone hypothesis, suggesting that the causative factor of affective changes may be a substance fluctuating in parallel with aldosterone such as angiotensin which has been shown to affect central neurotransmitters. This may be activated by renin in response to elevated progesterone levels. Other workers (Bruce and Russell 1962) found no relationship between increased body weight and fluid retention and premenstrual symptoms. (d) Monoamine theory. Variation in levels of oestrogen and progesterone in the luteal phase of the menstrual cycle causes a decrease in brain serotonin and dopamine resulting in depression and an increase in serum prolactin sufficient to cause salt and water retention (Judd and McMurdo 1976). Animal studies have shown that the activity of monoamine oxidase changes cyclically in the rat hypothalamus, amygdala, adrenals and ovaries (Kamberi and Kobayashi 1970). Klaiber et al. (1971) found that plasma monoamine oxidase activity varied significantly with menstrual cycle phase. Increasing plasma oestrogen reduced monoamine oxidase activity whereas administration of oestrogen plus progestogen increased monoamine oxidase activity. A cyclic pattern of monoamine oxidase activity has also been observed in the uterine endometrium by Cohen et al. (1964). Using histochemical techniques they found more diffuse and intense monoamine oxidase activity later in the cycle. Women who suffer from premenstrual tension were found to have higher plasma prolactin levels than a control group (Halbreich et al. 1970). Whether this is cause or effect is not clear as the authors noted that prolactin levels
88
may be raised by stress. Graham et al. (1979) conducted a double blind study of a prolactin antagonist (bromocryptine). They found a significant improvement of affect in women treated with bromocryptine as compared with placebo. It is not known whether this effect was mediated by suppression of prolactin secretion or whether it reflected other effects of bromocryptine such as dopamine agonist actions. DISCUSSION
Seemingly contradictory findings may be partly explained by differences in methodology which limit any general interpretation of these studies. An example is the diversity of assessment techniques used. The types of measurement selected have often reflected different and conflicting theories of behaviour. For example, Benedek and Rubenstein (1939) used psychoanalytic techniques of dream interpretation and free association in an attempt to explore unconscious ‘instinctual’ changes. Persky’s approach reflected state and trait theories of personality and behaviour (Persky 1974). The validity of self-report as a tool to reflect the symptoms accompanying the menstrual cycle has been questioned by some workers. Few studies used a ‘cover story’ to minimize the subject’s awareness of the investigators’ objectives, despite the considerable evidence to indicate that subjects’ expectations can substantially influence behavioural findings in research (Orne 1962; Weber and Cook 1972). Beumont et al. (1975) attempted to control for subjects’ expectations by including a control group of 7 hysterectomized women. Other workers used indices of change that do not rely on subjective reports (Pierson and Lockhart 1963; Morris and Udry 1970). Some studies (McCance et al., 1939; Benedek and Rubenstein 1939) reported no statistical analysis of reports whereas later studies differentiated findings that had a low probability of occurring by chance (Beumont et al. 1975; Wilcoxon et al. 1976). An important aspect of analyses was highlighted by May (1976). He reported no change in mood when results of the women studied were averaged. When individual patterns of mood change were examined two main groups were identified; those women experiencing lowest mood at the premenstruum and those whose lowest mood coincided with menstruation. The greatest difficulty in interpretation relates to the differing and usually inadequate methods used of assigning behaviour to menstrual cycle phases. Many studies have used the onset of menses as the cycle marker. ‘If all women had the same length of menstrual cycle, with no inter- or intrapersonal variance, and if hormonal events could be presumed to proceed in an invariant pattern during every cycle, the menstrual marker would be an adequate reference point for the association of behavioural observations and hormonal events. There is, however, no such regularity’ (Udry and Morris 1977). Different methods have been used to organize data from cycles of disparate lengths. These techniques are based upon certain theoretical
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assumptions about the procession of hormonal events in cycles. One example is to use a standardised cycle of an arbitrary length, usually 28 days, the assumption being that the pace of hormonal events is directly proportional to cycle length. Longer cycles are squeezed together while shorter cycles are proportionately lengthened (Kopell et al. 1969; Moos et al. 1969). Others have assumed that irregularities in cycle length occur before ovulation and that the time duration between ovulation and onset of next menstruation is a constant. The cycle phase is assigned by counting backwards from the onset of menses (reverse cycle day). That the use of these two differing techniques may influence the results obtained is demonstrated in the study of Morris and Udry (1970). When pedometer readings were analysed using reverse cycle day, no consistent change in physical activity was found. Significant changes in physical activity levels were evident on using the technique of standardised cycle day. The problem with these differing techniques which rely ultimately upon menstruation as the cycle marker, is that little can be deduced about actual hormonal events within the cycle. Some workers attempted to identify the menstrual cycle phases more accurately by using the basal temperature chart, the presumption being that the thermal nadir coincides with ovulation (Gottschalk et al. 1962). Lenton et al. (1977) were able to assess the accuracy of basal body temperature in predicting ovulation in 60 cycles for which both basal temperature charts and hormonal profiles were available. It was found that 80% of temperature charts were correctly interpreted as being ovulatory or anovulatory but the day of ovulation was predicted correctly in only 34% of cycles. The thermal nadir coincided with the luteinising hormone surge in 43% of the charts from normal subjects. It was concluded that predicting the day of ovulation from the temperature recording was unjustified. Udry and Morris (1977) suggested that fluctuations in steroid hormones and perhaps gonadotrophins must be assessed during the menstrual cycle in order to correlate any changes in behaviour patterns with the variations in levels of ovarian and pituitary hormones. That hormonal changes may underly certain affective changes was elegantly demonstrated by Somerville (1972), who studied 6 women who suffered a pattern of regularly recurring menstrual migraine. He demonstrated that falling levels of oestradiol, rather than progesterone, in some way triggered off migraine in susceptible women. The migraine attacks were not affected by injections of progesterone but could be postponed by maintaining high plasma oestradiol levels with injections of oestradiol valerate. In conclusion it is suggested that future studies in this area may be more useful in elucidating hormonal aetiology if, they meet the following criteria: adequate definition of, prospective; and measurement of subjective changes; intensive studies of women who suffer a particular change; determination of each woman’s pattern over several cycles; correlation of affective changes with day-by-day plasma levels of endogenous hormones; doubleblind investigations of subsequent hypotheses.
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