© 2013 John Wiley & Sons A/S Published by John Wiley & Sons Ltd.

Bipolar Disorders 2014: 16: 22–36

BIPOLAR DISORDERS

Review Article

Effects of the menstrual cycle on bipolar disorder Teatero ML, Mazmanian D, Sharma V. Effects of the menstrual cycle on bipolar disorder. Bipolar Disord 2014: 16: 22–36. © 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd. Objectives: Several lines of research suggest that reproductive events may affect the course of bipolar disorder (BD) in some women. With respect to the menstrual cycle, the focus has been on dysphoric symptoms [e.g., premenstrual dysphoric disorder (PMDD)], and the exacerbation of depression, in the premenstrual phase. This article reviews the literature on the potential effects of the menstrual cycle on BD. Methods: A systematic search for published case reports and research studies available through March, 2013 was conducted. Several combinations of search terms were entered into PubMed and PsycInfo. Results: Overall, 25 case reports, ten retrospective studies, and 11 prospective studies were identified. The majority (64%) of case reports involved hypomanic or manic episodes in the premenstrual phase. Retrospective results suggest that 25–77% and 15–27% of women with BD meet the criteria for premenstrual syndrome (PMS) and PMDD, respectively. Menstrual cycle-related mood changes were reported by 64–68% of women with BD in retrospective studies, and were displayed by 44–65% of women in prospective studies. Conclusions: Although research has focused on the premenstrual phase to the neglect of the periovulatory phase, it appears that a subgroup of women with BD, possibly those with hormonal sensitivity, experience menstrual cycle effects on depressive, hypomanic, and manic episodes. These phase-episode effects appear to be heterogeneous and may have implications for treatment. Whether they might best be described using course specifiers, similar to postpartum onset and rapid cycling, or as diagnostic entities, like PMDD, requires further study.

Research suggests that the prevalence rates of major depressive disorder (MDD), seasonal depressive episodes, mixed episodes, bipolar disorder (BD) type II, and rapid-cycling BD are higher among women than men (1, 2). Comparatively, the risk of hypomanic and manic episodes by sex is understudied and inconsistent (3). The phenomenology and clinical course of mood disorders may also differ between the sexes (2, 4, 5). For instance, the rates of depression among girls and boys are nearly equal, but there is a shift around mid-puberty to a two-to-one female-tomale ratio for depression until post-menopause

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Missy L Teateroa, Dwight Mazmaniana and Verinder Sharmab,c a

Health, Hormones, & Behaviour Laboratory, Department of Psychology, Lakehead University, Thunder Bay, bDepartment of Psychiatry and Obstetrics and Gynecology, Western University, c Perinatal Clinic, St. Joseph’s Health Care, London, ON, Canada

doi: 10.1111/bdi.12138 Key words: bipolar disorder – menstrual cycle – premenstrual dysphoric disorder – premenstrual syndrome Received 2 August 2012, revised and accepted for publication 1 July 2013 Corresponding author: Dr. Dwight Mazmanian Department of Psychology Lakehead University 955 Oliver Road Thunder Bay Ontario P7B 5E1 Canada Fax: 807-346-7734 E-mail: [email protected]

for women (6). Thus, between-sex variation in mood disorders has been hypothesized to be related to organizational (permanent) and activational (acute) effects of steroidal sex hormones on the nervous system (7). In some women, mood disorders, mood episodes, or affective instability co-occur with reproductive events or factors, characterized by precipitous hormonal changes, across the lifespan. Such events or factors include: menarche, the menstrual cycle, hormonal contraceptive use, hormone administration as part of in vitro fertilization, pregnancy, the postpartum period, the perimenopausal

Effects of the menstrual cycle on BD period, and hormone treatment for perimenopausal symptoms (7–9). For example, hormonal shifts across the menstrual cycle, particularly the decrease in both estrogen and progesterone levels in the late luteal phase, have long been thought to underlie premenstrual syndrome (PMS) and, more recently, premenstrual dysphoric disorder (PMDD) (10). The concurrent diagnosis of PMS or PMDD and a psychiatric or medical disorder that is exacerbated in the premenstrual phase has been termed premenstrual magnification (7). Unfortunately, there is a lack of agreed definitions and research criteria for menstrual cycle-related conditions (11). With respect to any effects of the menstrual cycle on BD, there are a number of non-mutually exclusive possibilities. Women with BD may also be more likely than other women to experience PMS or PMDD. Bipolar depressive, hypomanic, manic, or mixed episodes may be entrained (e.g., more likely to have onset in), or exacerbated in, one or more of the three main cycle phases (i.e., the menstrual, periovulatory, or premenstrual phase), particularly as a subset of women with PMDD also experience symptoms into the menstrual phase or during the periovulatory phase (1). Note that the onset of BD, regardless of first episode type, could also be entrained to the menstrual cycle, and episode entrainment or exacerbation (i.e., worsening) over the course of BD could be considered an exacerbation of the disorder itself. Although numerous publications have been devoted to specific issues in assessing and treating women with BD (4, 12), relatively little is known about BD in relation to PMS, PMDD, or the menstrual cycle more generally. However, there are four lines of research suggesting that there may be menstrual cycle effects on, or relationships with, BD in some women. First, both the disorder itself and treatment for BD (i.e., some anticonvulsants and antipsychotic agents) can be associated with reproductive dysfunction [e.g., polycystic ovary syndrome (PCOS), endometrial hyperplasia, anovulation, oligomenorrhea, and menstrual cycle irregularity] (13, 14). Menstrual cycle problems precede the diagnosis of BD in nearly 50% of cases (15, 16) and by analogy, women who experience menstrual cycle variability may be more likely to experience variability in mood across the cycle. While it is possible that the onset of BD or pharmacological treatment for BD deregulates the hypothalamic– pituitary–gonadal axis, resulting in the presentation of PMS, PMDD, or premenstrual exacerbation, the vast majority of menstrual cycle

research excludes women with irregular cycles, and the absolute levels of reproductive hormones do not seem to be anomalous among women with menstrual cycle- or postpartum-related mood disorders (17, 18). Overall, these studies indicate that hypersensitivity to normal hormone changes among a subgroup of women may underlie mood changes associated with reproductive events in both unipolar and bipolar mood disorders. Second, BD appears to be related to seasonality (19, 20). BD, seasonal affective disorder (SAD), and PMDD have all been found to be associated with increased sensitivity to light-induced melatonin suppression (21), suggesting that a common chronobiological mechanism may be involved in these disorders. Third, there is evidence from upwards of 80 case reports that psychosis linked to BD increases in the premenstrual phase in some women (22). Finally, other major reproductive events are known to increase the risk of onset of a mood disorder, or increase the risk of mood episodes in women with an existing mood disorder. Examples include the increased risk of sub-syndromal depressive episodes in up to 80% of new mothers, the onset of postpartum depressive episodes in 10–15% of new mothers (1), elation or hypomanic episodes in 10–18% of new mothers (23), and even the onset of manic and psychotic episodes in the postpartum period (24, 25). A later reproductive event, the menopausal transition, is associated with an increased risk of depression or mood instability in some women (7). There also appears to be substantial positive associations between the various ‘reproductive-related mood disorders’ (26–28). These findings are congruent with the notion that the course of BD could be affected by the menstrual cycle. The purpose of the present paper is to critically review the literature on the effects of the menstrual cycle on BD. The case reports and research studies on (i) the relationship between BD and both PMS and PMDD and (ii) menstrual cycle-related BD episodes or symptoms are examined. As discussed above, the menstrual cycle could affect the course of BD in 11 ways: (i) comorbidity between BD and PMS; (ii) comorbidity between BD and PMDD; (iii) premenstrual-related depressive episodes; (iv) menstrual-related depressive episodes; (v) periovulatory-related depressive episodes; (vi) premenstrual-related hypomanic or manic episodes; (vii) menstrual-related hypomanic or manic episodes; (viii) periovulatory-related hypomanic or manic episodes; (ix) premenstrual-related mixed episodes; (x) menstrual cycle-related mixed episodes; and (xi) periovulatory-related mixed episodes.

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Teatero et al. Methods

A systematic search for published case reports and research studies available through March, 2013 was conducted. The following terms were entered into PubMed and PsycInfo: bipolar disorder, mania, manic, and mixed episodes, along with menstrual cycle, ovulatory cycle, premenstrual syndrome, or premenstrual dysphoric disorder. The ancestry method was also used by examining the reference lists of all articles identified during the principal search. Although several partial reviews of the earlier reports on BD and the menstrual cycle (mean number of reports reviewed = 4) have been conducted (29–32), it is likely that the full body of literature on BD and the menstrual cycle is reviewed herein. There were no initial inclusion or exclusion criteria due to the sparse nature of the literature in this area. Therefore, the first author rated the quality of each case report and study based on methodological criteria (33). Each report was rated on a ten-point scale, with higher scores indicating higher quality, using the following factors: (i) clinical sample size (case report = 0, case series = 1, N of 8–108 = 2, N of 109 or above = 3); (ii) control case or group (no = 0, yes = 1); (iii) design (retrospective = 0, prospective = 1); (iv) controlled for at least one potential confound (e.g., medication use) (no = 0, yes = 1); (v) validated diagnostic instrument used to diagnose BD (no or not reported = 0, yes = 1); (vi) validated tool used to assess effects of the menstrual cycle (no or not reported = 0, yes = 1); (vii) number of menstrual cycle phases examined (two or less = 0, three or more = 1); and (viii) advanced statistical methodology (i.e., hierarchical linear modeling) (no = 0, yes = 1). Results

The findings were organized on the basis of case reports and research studies. Within each category, the findings were further grouped by episode type and menstrual cycle phase in order to assess the evidence for or against the 11 possible effects of the menstrual cycle on BD. Research studies were also separated by retrospective and prospective design. Case reports

Twelve case reports and four case series involving menstrual cycle-related BD episodes were identified. These reports are briefly summarized in Table 1. The total number of cases was 25 (age range = 16–47 years). The mean [standard deviation (SD)] quality rating for the case reports was

24

Table 1. Overview of case reports on the effects of the menstrual cycle on bipolar disorder

Study

N

Aalouane et al. 1 2010 (40) Al-Dabbas 2001 1 (41) Al-Habeeb 2003 1 (42) Becker et al. 1 2004 (48) 1 Conrad and Hamilton 1986 (39) D’Mello et al. 2 1993 (38) Ghadirian and 3 Kamaraju 1987 (45) Goldstein 1986 1 (34) Hendrick and 1 Altshuler 1998 (36) Hsiao and Lui 1 2002 (37) Hsiao and Liu 1 2007 (43) Kim and Staab 1 2005 (47) Kukopoulos 1 et al. 1985 (46) Matsunaga et al. 1 1986 (104); 2 Matsunaga and 3 Sarai 1993 1 (35)a McMeekin et al. 1 2003 (49) Sothern et al. 1 1993 (44) Phase-episode totalsb 8 1 0 12 3 1 5 0 1 0 0 0

Phase

Episode

Quality rating

Premenstrual

Hypomania

0.00

Premenstrual

Mania

1.00

Premenstrual

Mania

0.00

Menstrual Periovulatory Premenstrual

Depression Hypomania Mania

3.00

Premenstrual

Mania

1.00

Premenstrual Premenstrual

Depression Hypomania

1.00

Premenstrual

Depression

0.00

Premenstrual

Depression

2.00

Premenstrual N/A Premenstrual

Depression Hypomania Mania

3.00

Premenstrual



0.00

Premenstrual Premenstrual Premenstrual Menstrual Premenstrual Periovulatory

Depression Hypomania Depression Mania Mania Mania

3.00

Premenstrual

Mania

1.00

Premenstrual Menstrual

Mania Mania

3.00

Premenstrual Menstrual Periovulatory Premenstrual Menstrual Periovulatory Premenstrual Menstrual Periovulatory Premenstrual Menstrual Periovulatory

Depression Depression Depression Mania Mania Mania Hypomania Hypomania Hypomania Mixed Mixed Mixed

2.50 3.00 – 1.75 3.50 4.00 1.33 – 3.00 – – –

1.00

3.00

4.00

a It is unclear whether the ten cases reported by Matsunaga et al. (105) are also included in Matsunaga et al. (35). Based on patient characteristics and study results, it seems highly likely. b The mean quality ratings for each phase-episode combination are also presented.

1.63 (1.36). Only four cases involved exclusively depressive episodes entrained to, or exacerbated in, the premenstrual phase among women diagnosed

Effects of the menstrual cycle on BD with BD (34–37). In the first case, menstrual cyclerelated depression and PMS appeared to be comorbid with BD (34). While Hendrick and Altshuler (36) reported that PMDD may have been misdiagnosed as rapid-cycling BD type II, given that treatment with sertraline was successful but common BD medications were not, Hsiao and Lui (37) presented a case of a woman who developed hypomanic symptoms following treatment with paroxetine for PMDD. Overall, these case reports suggest that differentiating between menstrual cycle-related recurrent depression and BD may be difficult but has implications for patient care and outcome. There are approximately three times more published cases of hypomania or mania than bipolar depression or dysphoria entrained to, or exacerbated in, the premenstrual phase. In fact, 10 reports of exclusively hypomania and mania in the premenstrual phase have been published in the last 19 years (35, 38–43). Interestingly, Al-Habeeb (42) outlined diagnostic research criteria for premenstrual mania disorder (PMMD) as well as a case study. The proposed PMMD criteria are essentially those for a manic episode altered to reflect the criteria for PMDD. Two additional patients with BD in the controlled case series by Matsunaga and Sarai (35) were reported to have manic episodes that coincided with the menstrual phase (i.e., began on Day 1 of the cycle). By contrast, another woman experienced an episode of mania with psychotic features around ovulation (i.e., the periovulatory phase) (35). Sothern et al. (44) presented the case of a woman with schizoaffective disorder whose manic symptoms were related to two menstrual cycle phases. This case study is unique in that the patient had kept a menstrual cycle diary for 11 years. In total, this woman experienced 11 manic episodes, all of which occurred just before or during the follicular phase (the menstrual phase and up to ovulation). These reports, albeit a small number, suggest that there may be heterogeneous (i.e., a variety of) or alternative patterns of menstrual cycle-related effects on BD, rather than just premenstrual exacerbation of depressive episodes. Finally, seven reports that involved menstrual cycle-related changes in depression and hypomania or mania in the same woman were identified. At least four of these reports involved premenstrual onset or exacerbation of both depressive and hypomanic or manic episodes (45, 46). Kim and Staab (47) reported that episodes of BD, in general, were exacerbated in the premenstrual phase. By contrast, depressive episodes in the menstrual phase and hypomanic episodes around ovulation for

three to five days were present in one case (48). The details of an additional report are a bit unclear. McMeekin (49) reported that a woman with mixed, rapid-cycling mania and severe premenstrual discomfort experienced premenstrual exacerbation of mixed and depressive symptoms; however, it was also stated that the mood episode cycles often started following the menstrual phase, which is suggestive of the periovulatory phase. Several other findings within these case reports are worth noting. Of the six reports that presented the results of laboratory tests, three reported that they were within normal limits. These laboratory tests included blood count, pelvic ultrasound, ovarian hormone levels, electro-encephalogram, as well as kidney, liver, and thyroid function (37, 41, 42). Conversely, compared to a control group, Matsunaga and Sarai (35) found that eight women (67%) with menstrual cycle-related BD episodes or psychotic symptoms had elevated luteinizing hormone levels, six (50%) had lower follicle-stimulating hormone levels, six (50%) had higher testosterone levels, five (42%) had elevated androstenedione levels, and three (3%) had higher dehydroepiandrosterone sulfate (DHEA-S) levels. Nonetheless, testosterone and DHEA-S levels were lower in one and two cases, respectively. Given that ultrasonograph results consistent with PCOS were seen in 67% of patients, it was suggested that menstrual cycle abnormalities (which preceded diagnosis and treatment in three cases) may be related to changes in mood across the cycle. Two other reports indicated that lithium levels changed across the cycle, such that they were highest when mood was depressed and lowest when mood was hypomanic (46) or low in the premenstrual phase when BD episodes were exacerbated (39). These preliminary findings suggest that the pharmacokinetics of lithium may be related to the biological basis of menstrual cycle-related mood disorders. In summary, the majority of cases seemed to represent menstrual cycle phase onset entrainment of BD episodes. Fifty-six percent of the 25 reports involved hypomanic or manic episodes affected by the premenstrual phase. If PMDD is a reproductive subtype of unipolar depression and both MDD and BD are affected by menstrual cyclicity in some women, it seems highly plausible that there is a bipolar variant of PMS or PMDD, perhaps similar to Al-Habeeb’s (42) criteria for PMMD. Unfortunately, most case reports did not differentiate between BD comorbidity with a menstrual cycle-related disorder, such as PMS, and menstrual cycle-related BD episodes (i.e., onset entrainment). At the very least, it is clear that the diagnosis of a menstrual cycle-related mood disorder, particularly

25

Teatero et al. the differential diagnosis between a unipolar or bipolar diathesis, has treatment implications. Most women in these reports had experienced numerous drug trials. Additionally, antidepressant treatment, such as with selective serotonin-reuptake inhibitors (SSRIs), may induce a manic-type episode in some women who present with menstrual cycle-related depression (37). As Hendrick and Altshuler (36) pointed out, it is also important to distinguish between symptoms of hypomania and euthymic or elevated mood following depression. There are, of course, many limitations of case reports. It is largely unclear how any potential menstrual phase effects on mood were assessed. For instance, only one report involved phase confirmation using ovulation detection tests (48). In some cases, there was a lack of prospective methods such that diagnosis appeared to be made after one menstrual cycle (35). It is therefore possible that the association between menstrual cycle phase and BD was coincidental in some of these cases, increasing the false-positive rate. It is also unfortunate that Al-Habeeb’s (42) proposed criteria for PMMD do not seem to have had a major impact on the proceeding literature, as there is a striking lack of consistency in how different changes in mood across the cycle are assessed, diagnosed, and described. Although the extent to which these case reports can be generalized to subgroups of women is unclear, several research studies to which we can compare these individual reports have been conducted. Research studies

Ten retrospective or cross-sectional studies and 11 prospective studies on the effects of the menstrual cycle on BD were identified (see Table 2 for an overview). Four of the prospective studies also provided retrospective results (50–53). The mean (SD) quality ratings were 4.40 (1.26) for studies with retrospective results only and 6.36 (0.81) for studies with prospective results. Retrospective studies. Retrospective estimates of the proportion of women with BD who report PMS (i.e., increased somatic or psychological symptoms in the premenstrual phase) range from 25% to 77% (19, 51–56). Specifically, more women with BD type II than BD type I and age-matched controls reported moderate to severe PMS (52%, 23%, and 20%, respectively) (19), more women with rapidcycling BD than age-matched controls reported severe PMS (55), and patients with severe PMS tended to cycle more rapidly (55). Karadag et al. (52) found that significantly more women in the

26

control group reported PMS than women with treatment-responsive BD, while Diamond et al. (54) and Roy-Bryne et al. (56) did not find differences in premenstrual symptom reporting between clinical and control groups. Additionally, there were no differences in PMS among women with postpartum onset of BD compared to a control group (53), and women with BD compared to women with SAD (56). These studies suggest that retrospectively reported PMS may be associated with BD in a subgroup of women, namely those with BD type II or rapid cycling. With respect to a specific type of PMS, retrospective studies indicate that 15–27% of women with BD have a history of PMDD. These estimates are significantly higher than those found in a nonclinical subsample (19). Also, Fornaro and Perugi (57) reported that rates of BD type II, cyclothymia, obsessive-compulsive disorder, and body dysmorphic disorder were higher in women with PMDD, while rapid cycling, seasonality, psychotic features, melancholia, past hospitalization, and suicidality were similar between the clinical and control groups. If PMDD is more prevalent among women with BD than in the general population, some women with PMDD may have a BD diathesis with dysphoric episodes either exacerbated in the premenstrual phase or superimposed on the course of BD. Seven other retrospective studies examined the effects of the premenstrual phase on mood in women with BD. Overall, these studies suggest that 64–68% of women with BD report premenstrual changes in mood (50, 58–60). However, four of these studies did not distinguish between exacerbation of BD versus comorbidity between BD and a menstrual cycle-related disorder, as general oneitem or self-report measures were used, such as ‘[h] ave you ever noticed regular mood changes in the premenstrual or menstrual period?’ (59, p. 223). Payne and colleagues (59, 60) found that significantly fewer healthy female relatives (34%) reported such changes and that familial aggregation of premenstrual mood symptoms was not significant in women with BD or MDD. However, some additional problems with the measure used included that ‘mood change’ could refer to increased depression, decreased depression, increased mania, decreased mania, or euthymia, and it is not clear what proportion of the women who responded affirmatively may have experienced menstrual phase changes in mood. For instance, Diamond et al. (54) found that 17% of women reported menstrual symptoms. Moreover, although Wehr et al. (61) reported that BD episode cyclicity and menstrual cycle cyclicity did not

Effects of the menstrual cycle on BD Table 2. Overview of research studies on the effects of the menstrual cycle on bipolar disorder

Study Retrospective studies Blehar et al. 1998 (58)

Phase comparisons

N

Quality rating

Premenstrual/menstrual only

Premenstrual mood changes

3.00

Premenstrual only

PMS/PMDD

6.00

Premenstrual/menstrual only

n.s. (PMS)

4.00

Premenstrual only

Premenstrual mood swings

Premenstrual only

PMDD

Clinical: 17 Control: 16 Clinical: 34 Control: 35 Clinical: 50 Clinical: 777 Control: 163 Clinical: 435 Clinical:25 Control: 25 Clinical: 50 Control: 23 Clinical: 43 Control: 19 Clinical: 8 Control: 9

Premenstrual only

n.s. (PMDD)



Premenstrual only

n.s. (control group reported more PMS)



Premenstrual only Premenstrual/menstrual only

Premenstrual positive mood Premenstrual mood changes

2.00 5.00

Premenstrual/menstrual only

Premenstrual mood changes

5.00

Premenstrual only

PMS

5.00

Premenstrual only

n.s. (PMS)

6.00

N/A

n.s. (rapid-cycling bipolar disorder)

4.00

Premenstrual only

n.s. (control group reported more PMS)

Clinical: 293

Premenstrual only

7.00

Clinical: 17 Control: 16 Clinical: 34 Control: 35 Clinical: 25

Premenstrual only

Premenstrual mood swings related to a more symptomatic and relapseprone bipolar disorder course Progesterone and allopregnalone levels positivity associated with mixed symptom profiles n.s. (PMS)

6.00

Rasgon et al. 2003 (66)

Clinical: 45

Premenstrual versus menstrual

Rasgon et al. 2005 (5)

Clinical: 45

Premenstrual versus menstrual

Schoofs et al. 2011 (70) Shivakumar et al. 2008 (69)

Clinical: 52

Premenstrual versus nonpremenstrual Premenstrual versus follicular

Premenstrual depression Premenstrual euthymia Premenstrual hypomania Premenstrual depression Premenstrual euthymia Premenstrual hypomania Premenstrual depression Premenstrual euthymia Premenstrual hypomania Premenstrual binge eating n.s. (depression and mania)

6.00

Choi et al. 2011 (19)

Diamond et al. 1976 (54) Dias et al. 2011 (50) Fornaro and Perugi 2010 (57) Hardoy et al. 2006 (51)

Karadag et al. 2004 (52)

McClure et al. 1971 (62) Payne et al. 2007 (59)

Payne et al. 2009 (60) Price et al. 1986 (55)

Roy-Bryne et al. 1985 (56) Wehr et al. 1988 (61)

Wieck et al. 2003 (53) Prospective studies Dias et al. 2011 (50)

Hardoy et al. 2006 (51)

Karadag et al. 2004 (52)

Leibenluft et al. 1999 (65)

Clinical: 186 Clinical: 61 Control: 122 Clinical: 63 Control: 12 Clinical: 293 Clinical: 92

Menstrual cycle effect

Clinical: 41

Premenstrual versus postmenstrual Premenstrual versus menstrual

– 4.00



5.00

7.00

7.00

7.00

5.00

27

Teatero et al. Table 2. (Continued)

Study Sit et al. 2011 (71)

Wieck et al. 2003 (53) Whybrow et al. 2003 (67)

N Clinical: 11 Control: 10 Clinical: 8 Control: 9 Clinical: 45

Phase comparisons

Menstrual cycle effect

Quality rating

Premenstrual versus menstrual

n.s. (depression and mania)

7.00

Premenstrual versus menstrual

Premenstrual APO-GH response

7.00

Premenstrual versus menstrual

Premenstrual depression Premenstrual euthymia Premenstrual hypomania

6.00

APO-GH = apomorphine/growth hormone; n.s. = not significant (main effect of the menstrual cycle or interaction between menstrual cycle phase and clinical versus control group); N/A = not applicable; PMDD = premenstrual dysphoric disorder; PMS = premenstrual syndrome.

appear to be related because only 11% of women had cycle lengths that were similar to the duration of their rapid cycling, this does not negate the possibility that the course of BD is affected by the menstrual cycle. The only study to explicitly consider symptoms of mania found that 13 (26%) women calling a suicide prevention center reported that they were unusually active and felt better in the premenstrual phase (62). Some of these women reported symptoms consistent with hypomania just prior to premenstrual depression. Four out of five of these women reported a positive personal or familial history of BD. McClure et al. (62) concluded that premenstrual symptoms may be an indication of an underlying bipolar diathesis. Taken together, the 14 retrospective analyses indicate that 25–77% of women with BD, particularly BD type II perhaps report some form of PMS or premenstrual mood change. There was weak evidence that rapid-cycling BD may be particularly associated with the menstrual cycle (50, 55, 57), as well as that manic symptoms may be related to the premenstrual phase among some women (59, 62). It is important to recognize, however, the limitations of retrospective designs. Studies have shown that retrospective prevalence rates of PMS are inflated such that many symptom reports are not validated upon prospective assessment (63, 64). Prospective studies. Of the 11 prospective studies identified, only one examined PMS/PMDD. In 2003, Karadag et al. (52) found prospective menstrual cycle phase effects in 34 women with BD, responsive to mood stabilizers and thus, considered euthymic. With a 30% change criterion, total, depressive, and physical scores on a measure of PMS were higher in the premenstrual than the postmenstrual phase (i.e., Days 6–10 of a 28-day

28

cycle) across two consecutive cycles. However, significantly fewer women in the clinical group showed these changes (0.03% versus 2.9% for total PMS scores). It is important to note that three women who developed mood episodes in the premenstrual phase were excluded from analyses of menstrual cyclicity, but it is unclear as to why, as such selection criteria may reduce the probability of detecting a menstrual cycle effect. Seven of the prospective studies assessed the extent of menstrual cycle effects on symptom reporting. As in the corresponding retrospective studies, exacerbation of BD was not differentiated from comorbidity between BD and PMS as general one-item, visual analogue measures were most often employed (5, 53, 65–67). Although approximately 44% of women with rapid-cycling BD were found to exhibit a significant menstrual cycle effect, no systematic patterns were apparent (65). However, five of 25 women showed an increase in hypomania or a decrease in depression at the postmenstrual compared to the premenstrual phase, while six women showed the opposite pattern. It is notable that this study was conducted prospectively throughout three to 50 months and, thus, averaged ratings were used in the analyses. While averaged ratings tend to be more reliable, it is also possible that changes across any single cycle could be obscured when employing this strategy. Across three studies, Rasgon and colleagues (5, 66, 67) examined mood in the last seven days of the menstrual cycle in contrast to the first seven days (i.e., the menstrual phase) among women with BD. Data were collected prospectively using a computerized bipolar dimension from depression to mania across three months. Significant menstrual cycle changes in at least one cycle were found in 55–65% of women but there were no discernible patterns in any of the studies. However, Rasgon et al. (5) reported that 17 cycles showed

Effects of the menstrual cycle on BD higher, and 11 cycles showed lower, mood ratings in the premenstrual phase. In group analyses, women’s moods were less depressed (i.e., more euthymic) during the premenstrual phase for freecyclers [i.e., non-oral contraceptive (OC) users] but not OC users (66). In fact, free cycling women had lower overall mood scores, regardless of menstrual cycle phase, than OC users (5). Another study that compared the premenstrual and menstrual phases found that sad–happy ratings were not significantly different between women with postpartum BD and other parous women in either phase (53). If these studies had included the periovulatory phase, characterized by relatively high estrogen levels and increasing progesterone levels (68), it is possible that distinct menstrual cycle effects may have been discernible. More recently, Shivakumar et al. (69) examined depression and mania ratings across the menstrual, preovulatory, early-luteal, and late-luteal phases of the menstrual cycle. Based on a chart review of 41 women with BD, mood severity was not significantly related to the menstrual cycle. However, about 20% of women had greater depression scores, while 12% had higher mania scores, in the luteal phase compared to the follicular phase (i.e., the menstrual and preovulatory phases combined). There were no differences between the subgroup of women who exhibited a trend toward menstrual cyclicity and those who did not, including whether or not they had been diagnosed with rapid-cycling BD. This study (69) has three main limitations. It was not clear how mood symptoms were measured and thus how scores were determined retrospectively from life charts. Changes in any single cycle could have been masked as the data were collapsed across three consecutive months. Lastly, forward counting from Day 1 of menstruation was used to determine the four menstrual cycle phases. This is problematic because menstrual cycle length, and more specifically the length of the follicular phase, is variable. The reverse counting method, whereby the day before the first day of menstruation is 1, is more accurate for determining menstrual cycle phases (68). Lastly, the authors did not report how many women had lower depression and mania scores in the luteal phase or in the follicular phase. Two other studies examined menstrual cycle effects using specific symptom scales. Schoofs et al. (70) found that about 29% of women with BD that had been in remission for at least six months met the criteria for binge eating disorder. Moreover, binge eating symptoms and women’s self-reported weight were highest in the premenstrual phase compared to the rest of the cycle. These findings

suggest that symptoms other than mood may be exacerbated in the premenstrual phase among women with BD. Unfortunately, this study did not include a control group and so it cannot be concluded that the reported changes were specific to BD. While Sit et al. (71) included a control group, they determined that symptoms of depression, mania, generalized anxiety, and suicidality, as well as psychosocial functioning, perceived stress, and physical symptoms, did not change across the menstrual cycle in either group. However, women with PCOS, PMS, PMDD, unipolar depression, or an active hypomanic episode were excluded from the analyses, which potentially reduced the chance of observing a menstrual cycle effect. Finally, Dias et al. (50) was the only prospective study to have considered the effects of the menstrual cycle on the larger course of BD. Women from the Systematic Treatment Program for Bipolar Disorder (STEP-BD) who retrospectively reported premenstrual exacerbation, which was supported prospectively, were less likely to be in recovery and more likely to be in a depressed or sub-syndromal state at study entry. Over the course of one year, they also experienced a higher number of episodes, a shorter time until relapse (if recovered), and more overall depressive and mood elevation symptoms regardless of menstrual cycle phase. They were not, however, more likely to have rapid-cycling BD during this time. The results of this study suggest that premenstrual exacerbation may be a clinical marker of a severe phenotype of BD. This study is unique, in that it statistically controlled for three potential confounds: use of psychotropic medications and hormonal contraceptives, and menstrual cycle irregularity. With respect to differences in menstrual cycle characteristics, it is important to note that Hardoy et al. (51) found that blood serum levels of progesterone and allopregnalone, but not cortisol and 3a,21-dihydroxy-5a-pregnan-20-one, in the premenstrual phase were significantly higher among women with BD who retrospectively reported PMDD than those who did not. In the same sample, progesterone and allopregnalone levels were not associated with depressive and manic syndromes but rather a mixed symptom profile (72). In contrast, Karadag et al. (52) and Wieck et al. (53) did not find that levels of progesterone or estrogen differed between women with rapid-cycling BD or postpartum BD episodes, respectfully, and controls. However, women with postpartum BD episodes exhibited greater hypothalamic dopamine receptor sensitivity in the luteal phase, while the control group did not (53).

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Teatero et al. To summarize the results of the reviewed research studies, roughly 50% of women with BD experience significant menstrual cycle phase changes in mood. While some women who seem to have menstrual cycle-related BD exhibit premenstrual entrainment or exacerbation of depressive symptoms, others may demonstrate more atypical patterns (e.g., mania in the premenstrual phase). For instance, at least three studies were unable to discern any consistent menstrual cycle effects using analyses of individual cycles, but they only included premenstrual and menstrual phases. Several other methodological issues warrant mention. Distinctions between menstrual cycle exacerbation of BD episodes and comorbidity between BD and a menstrual cycle-related disorder were rarely made. Phase comparisons and methods for monitoring the menstrual cycle differed substantially across the studies. Most, if not all, women were receiving pharmacological treatment and few studies attempted to control for other possible confounds. Finally, all BD diagnoses tended to be grouped together and there was a definite focus on depressive symptoms as well as the premenstrual phase. Discussion and conclusions

In total, 25 case reports on the effects of the menstrual cycle on BD were identified. Although women are more likely to experience unipolar and bipolar depressive episodes than men (2, 5), the largest group of cases reported herein (64%) were of premenstrual hypomania or mania only. In fact, only four cases of bipolar depression associated with the premenstrual phase were found. Additionally, there were three cases of hypomanic or manic episodes entrained to the menstrual phase and one case of mania around ovulation. Six women presented with both depressive and manic episodes that changed with the menstrual cycle. BD episodes began in the premenstrual phase in two cases and manic episodes began in the periovulatory phase in one case. This means that only two cases of mood episodes entrained to the periovulatory phase were identified. There were no case reports of periovulatory-related depressive episodes, menstrual-related hypomanic episodes, or mixed episodes associated with any of the three phases. A comparable number of research studies (N = 21) was identified. In total, 14 studies included retrospective designs and 11 included prospective designs. With respect to comorbidity, results suggest that 25–77% of women with BD also report PMS. Most estimates were closer to the

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higher end of this range. Whether or not these results differ from the prevalence rate of PMS in the general population remains unclear, given that 40–80% of women report at least some premenstrual symptoms (73). Also, the only prospective study that examined the relationship between PMS and BD found that women with BD displayed less change in PMS symptoms than control participants (52). It is clear that more prospective research on PMS and BD is needed. For instance, women with BD type II may be more likely than women with BD type I to experience PMS (19). With respect to PMDD, even less research has been conducted. Two retrospective studies, and no prospective studies, examined the relationship between PMDD, a severe subtype of PMS, and BD. Approximately 15–27% of women with BD, particularly those with BD type II, may also meet the criteria for PMDD (57). By contrast, the prevalence rate of PMDD in the general population is 3–8% (1, 19). At this point, it is clear that women with BD may be more likely to report PMDD but whether or not they exhibit prospectively measured PMDD is an avenue deserving of future research. The vast majority of research studies did not differentiate between menstrual cycle entrainment or exacerbation and comorbidity of BD. In fact, there may be upwards of five possible overall menstrual cycle effects, which may represent subtypes of mood disorder (11, 74), regardless of episode type: (i) entrainment (i.e., episode onset); (ii) exacerbation; (iii) magnification defined as the diagnosis of BD with menstrual cycle exacerbation or entrainment and PMS/PMDD; (iv) comorbidity between BD and PMS/PMDD; and (v) reproductive mood disorder (i.e., distinct clinical entities like PMDD). The reviewed studies (N = 14) indicate that 64–77% of women with BD retrospectively report, while 44–65% of women with BD display using prospective assessment, mood changes in the premenstrual phase. These rates appear to be greater than those found among control groups (59, 60) but this difference has yet to be examined prospectively (71). Consistent with previous research, it appears that retrospective reports tend to overestimate the number of women with BD who may experience menstrual cycle-related changes in mood (75); that is, roughly 49% of women with BD may prospectively demonstrate menstrual cycle-related change in mood symptoms, although, at a conceptual level, the findings are obfuscated by a lack of consistent terminology with respect to menstrual cycle-related phenomena or syndromes. Rates of mood change in the menstrual phase or exacerbation of mania in the premenstrual phase appear to be 17% and 26%, respectively (54, 62).

Effects of the menstrual cycle on BD Overall, it can be concluded that there appears to be a subgroup or subgroups of women who experience effects of the menstrual cycle on BD. It is likely that menstrual cycle effects are more common in women with BD type II than BD type I. As alluded to previously, an extreme sex ratio in rapid-cycling BD is a well-supported, robust finding (32). In fact, 70–90% of those diagnosed with this variant of BD are women (76). Considering that rapid cycling is defined by at least four mood episodes in 12 months (1), it seems logical to postulate that, of all mood disorder types, it might have the strongest relationship with the menstrual cycle. However, the results of the present review suggest that this may not be the case, at least when prospective assessment is employed. There is a dearth of research on other possible differences between women with BD who do and do not experience effects of the menstrual cycle. Three (50% of ) case reports stated that all laboratory tests were within normal limits. However, the hormonal profiles of some women with menstrual cycle-related BD episodes were similar to those seen among women with PCOS, including elevated levels of testosterone as well as the presence of polycystic ovaries and mild hirsutism (35). Also, elevated levels of progesterone and allopregnalone in the premenstrual phase have been reported to be particularly associated with mixed mood syndromes (51, 72), while there do not appear to be any differences in estrogen levels between women with and without BD (52, 53). Consistent with the hormonal sensitivity hypothesis of reproductive mood disorders (7), dopamine receptor sensitivity to normal menstrual cycle changes in hormones has been shown to be related to postpartum depression but not a history of PMS (53). Overall, there are no well-researched physiological markers of menstrual cycle-related BD. Normal hormonal changes across the entire lifespan may contribute to variance in the course and severity of BD. For instance, fluctuations in estrogen or progesterone may modulate neuroendocrine functioning and, thus, vulnerability to BD episodes. In general, endogenous estrogen seems to have a positive effect on mood, including positive affect (77). It is associated with an increase in neuronal excitability, including serotonin- and noradrenaline-enhancing effects (78). Conversely, progesterone appears to exert a negative effect on mood and cortical excitability. As an example, progesterone and its metabolite allopregnanolone modulate the gamma-aminobutyric acid (GABA) system (79). It is likely that a spectrum of hormonal sensitivity and symptom severity exists

among women (80). Other systems that have been implicated in the hormonal modulation of symptoms are GABA, serotonin, dopamine, and the hypothalamic–pituitary–adrenal axis (81). It has also been proposed that the effects of hormonal changes across the lifespan may be cumulative in those who are vulnerable (26, 82). Women with a hypersensitivity to changes in reproductive hormones as well as a predisposition for various psychological changes (e.g., unipolar depression or BD) may accumulate risk across the lifespan, with every reproductive event. The pathogenesis of reproductive mood disorders may therefore be related to electrophysiological kindling (83), which would have treatment implications such as a role for antiepileptics, as suggested by a preliminary study of PMDD (84). Indeed, some women seem to be particularly vulnerable to the activational effects of hormones on mood, from menarche to menopause. Moreover, subgroups of women may be hormonally primed to experience different menstrual cycle effects (85– 88); that is, the effects of the menstrual cycle on BD may be heterogeneous with respect to both episode type and phase (i.e., phenotype). This vulnerability or hormonal priming may be genetic, a result of the organizational effects of hormones, or both, among other things. For instance, two case reports reviewed herein suggested that BD developed right after menarche (39, 40) and, according to Labad et al. (89), the onset of BD tends to be closer to menarche than that of unipolar depression. There is a small body of evidence that a subgroup of women with BD experience mood change with at least one reproductive event (58, 90). While Payne et al. (59) found that symptom reports associated with the premenstrual and menstrual phases, the postpartum period, and the perimenopausal period were correlated among women with MDD but not BD, the BD group consisted only of those with BD type I, and medication use may have obscured the results (91). The vast majority of research on the effects of the menstrual cycle on mood disorders has focused on depressive or dysphoric symptoms in the premenstrual phase. Bipolar episodes, most notably mixed states, as well as the periovulatory phase, have received relatively less, if any, attention (92, 93). The effects of the menstrual cycle on affect and mood are just beginning to be understood. However, as alluded to previously, there is some evidence that menstrual cycle-related BD may have several presentations. By analogy, PMDD may also be a heterogeneous entity that includes both unipolar and BD cases, as suggested by several case reports, but further research is needed.

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Teatero et al. According to Moos (94), profiles of symptoms across the menstrual cycle allow for the examination of cyclic differences within and between women. The vast diversity of PMS symptoms as well as clusters of symptoms has led to the conclusion that there may be different profiles or types of menstrual cycle syndromes (85, 95). In addition to PMS and PMDD, there may be numerous other, perhaps more atypical, presentations or phenotypes of menstrual cycle-related conditions (96). According to the American Psychiatric Association (APA) (1), for example, some women with PMDD also experience symptoms during the periovulatory phase; that is, a subset of women may have dysphoria that co-occurs with more than one menstrual cycle phase. Overall, these findings indicate that there are individual differences in symptom patterns across the cycle, and that all the phases of the menstrual cycle are important in assessing psychological entrainments, whether they involve the exacerbation of an existing disorder like MDD and BD, the magnification of existing disorders, or a separate clinical entity like PMDD. As Sit et al. (71) outlined, research studies on the effects of the menstrual cycle on BD have been limited by several other methodological concerns, including retrospective reporting, small sample sizes, failure to control for current mood episode, and unclear methodology. The first two limitations appear to have been addressed to some extent, given that several studies with controlled withinsubjects designs have been conducted in different groups of women with BD (5, 52, 53, 70). However, few studies have controlled for psychotropic medication or hormonal contraceptive use, which may be problematic because these drugs have been shown to alter the reproductive system (91). In the present review, 67% of research studies seemed to have included hormonal contraceptive users. Given the null results among hormonal contraceptive users in the study by Rasgon et al. (66) and that OCs may stabilize mood in some women (97– 99), hormonal contraceptive use is likely to be a confound when examining menstrual cycle effects on BD. Also, although only five studies excluded women on the basis of menstrual cycle irregularity, the majority of studies did not include a longitudinal duration beyond one menstrual cycle or biological measures of menstrual cycle phase (e.g., ovulation tests or hormone assays), and four studies averaged menstrual cycle phase symptom ratings across several months. To summarize, interpretation of the existing studies on the effects of the menstrual cycle on BD are limited by: (i) a lack of conceptual clarity; (ii) the possibility of reduced menstrual cycle variability (e.g., averaging

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scores across multiple cycles and excluding participants on the basis of other menstrual cycle problems); (iii) the confounding effects of treatment and hormonal contraceptive use (i.e., mood stabilization); (iv) a lack of biological measures (e.g., hormone assays or ovulation detection) to confirm menstrual cycle phase; (v) under-investigation of the periovulatory phase; and (vi) the use of singleitem measures or measures with unknown psychometric properties. The excellent study by Dias et al. (50) should be highlighted as it controlled for current psychotropic medications, hormonal contraceptive use, and menstrual cycle regularity, among other factors. This study was also unique in examining the course of BD over one year as a function of premenstrual exacerbation. In line with several case reports and other prospective findings, the results of Dias et al. indicate that ‘premenstrual exacerbation may be a clinical marker predicting a more symptomatic and relapse-prone phenotype in reproductive-aged women with bipolar disorder’ (50, p. 386). This study and the other five prospective studies with relatively high quality ratings listed in Table 2 should be built upon in future research. Specifically, we recommend the use of statistical techniques that test for variations in prospective effects (i.e., random effects) across individuals or groups. The present review suggests that the menstrual cycle likely affects the course of BD in some women, possibly those with hormonal sensitivity, but more rigorous research on BD and the entire menstrual cycle is warranted before any major conclusions can be drawn. For instance, the highest quality rating of the best prospective studies reviewed herein was seven out of ten. While the current evidence primarily supports a relationship between BD and premenstrual mood changes, we hypothesize that the periovulatory phase, when estrogen, neuronal excitability, and fertility are relatively high, may be particularly likely to be associated with hypomanic and manic episodes. By contrast, the premenstrual phase, when progesterone and allopregnanolone are relatively high and fertility and cortical excitability are low, seems most likely to be associated with bipolar depressive episodes. Similarly, it has been suggested that ‘… the initial euthymic phase leading to ovulation is conducive to mating …’ (100, p. 1084) and that dysphoric symptoms in the premenstrual phase, during pregnancy, and in the postpartum period might have evolved because they keep women out of harm’s way when the survival of a child may depend on them. Possibly relevant to the findings reviewed herein regarding heterogeneity in phaseepisode relationships, Reiber (101) reported that

Effects of the menstrual cycle on BD women experience different menstrual cycle patterns of PMS-like changes that are dependent on whether their current conditions are advantageous for reproduction from an evolutionary perspective. For instance, a subgroup of women with a relatively low mean age, few resources, and higher parity, conditions considered to be unfavorable for having (more) children, was found to experience ‘pseudo-PMS’ in the periovulatory phase, followed by less negative states in the premenstrual phase. Thus, attempts should be made to distinguish between subgroups of women who experience various patterns of mood dysregulation related to the menstrual cycle. Finally, menstrual or ovulatory cycling in BD may be similar to rapid-cycling BD or episode onset in the postpartum period, in that they may all reflect specific course variations, and should be described with course specifiers. This might have important implications in terms of etiology and treatment outcomes (36, 91, 102, 103). We recommend that primary care physicians and obstetricians monitor all phases of the menstrual cycle, including the periovulatory phase; all aspects of BD, including hypomanic, manic, and mixed episodes; and mood stabilizer levels across the cycle in women who present with possible hormonal sensitivity, given that there may be 11 specific effects of the menstrual cycle on BD. Disclosures VS has received grant support from, participated on scientific advisory boards for, or served on the speakers’ bureaus of AstraZeneca, Bristol-Myers Squibb, Eli Lilly & Co., Janssen, Lundbeck, Pfizer, Sunovion, and Servier; however, none of these activities were related to the content of the current manuscript. MLT and DM have no conflicts of interest to declare.

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Effects of the menstrual cycle on bipolar disorder.

Several lines of research suggest that reproductive events may affect the course of bipolar disorder (BD) in some women. With respect to the menstrual...
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