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Association Between the Menses and Suicide Attempts: A Replication Study

From the Department of Psychiatry (E.B.G.,C.D.S., A.C., J.S.R.), Hospital Ramon y Cajal, University of Alcala, Madrid, Spain; Department of Statistics, Universidad Nacional, Medellin, Colombia (F.J.D.); and the Mental Health Research Center (F.J.D., J.d.L.), Eastern State Hospital, Lexington, Kentucky.

Address reprint requests to: Jose de Leon, MD, Mental Health Research Center, Eastern State Hospital, 627 West Fourth St., Lexington, KY 40508. Email: jdeleon{at}uky.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION Suicide and the Menstrual... METHODS RESULTS DISCUSSION ACKNOWLEDGMENTS REFERENCES

 
OBJECTIVE: In our prior (first) study, suicide attempts were associated with the menses. The main hypothesis of this replication (second) study is that the proportion of suicide attempters during the menses is significantly higher than the expected probability in the general population.

METHODS: Using the same methodology and setting, this replication naturalistic study included 120 fertile female suicide attempters with regular menstrual cycles during a 1-year period in the emergency room of a general hospital in Madrid, Spain, serving a catchment area of 500,000 people.

RESULTS: The significant increase in probability of attempting suicide during the menses for the first study was 1.61; for the second study, 1.72; and for both studies combined, 1.68 (95% confidence interval, 1.27–2.09). Thus, using the combined results, the probability of attempting suicide during the menses was 1.68 times higher than the overall probability of attempting suicide for any fertile women. In the catchment area, the population rate of fertile women arriving at the hospital after a suicide attempt was 166 per 100,000. The probability for women during the menses arriving at the hospital after a suicide attempt was significantly higher, 279 per 100,000 (1.68 x 166 per 100,000). The 95% confidence interval was 211 to 347 per 100,000.

CONCLUSIONS: Despite inherent limitations, this naturalistic study replicates a small but significant increase of suicide attempts during the menses.

Key Words: suicide, • suicide attempts, • menstrual cycle, • menstruation, • sexual hormones.

Abbreviations: AR = attributable risk;; CI = confidence interval;; DSM-IV = Diagnostic and Statistical Manual of Mental Disorders, 4th edition;; MINI = Mini International Neuropsychiatric Interview.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION Suicide and the Menstrual... METHODS RESULTS DISCUSSION ACKNOWLEDGMENTS REFERENCES

 
Suicide attempts are more frequent in women than in men (1, 2) . More importantly, suicide is the second leading cause of death worldwide after tuberculosis in young women aged 15 to 45 years (3). US women are estimated to be two times more likely to attempt suicide than US men (4). However, US men are four times more likely to complete it (1).

Vulnerability to suicide is probably best understood in the context of a model of stress-diathesis for suicidal behavior as described by Mann (5, 6) . Genetics, rearing, chronic illness, chronic substance abuse, and possibly cholesterol level influence the diathesis for suicidal behavior. Typical stressors include psychiatric illness, acute use of alcohol or sedatives, acute medical illness, and acute family and social stress.

	Suicide and the Menstrual Cycle

TOP ABSTRACT INTRODUCTION Suicide and the Menstrual... METHODS RESULTS DISCUSSION ACKNOWLEDGMENTS REFERENCES

 
In the last few years, there has been an interest in the relationship of the menstrual cycle with mood disorders (7–10) . The menstrual cycle may influence suicidal behavior. Most published studies on the association between the menstrual cycle and suicide attempts are rather outdated, lack sophisticated methodologies, and have inaccuracies due to using self-estimates of the menstrual cycle to divide the cycle into weeks instead of physiological phases. For the publication of our prior (first) study (11), we performed an extensive review of the literature. This review included 17 studies published during the last 40 years. Most of the studies suggested that the time around the menses is a critical period for suicidal behavior and that the menstrual cycle could be considered as another contributing factor for suicide. Forestié et al. (12) specifically hypothesized that low estrogen levels may contribute to suicide. Therefore, in Mann’s suicide model (5, 6) , the menstrual cycle acts as a stressor.

Our prior study was performed in a general hospital of the Spanish National Health System that provides free medical coverage for 500,000 people in Madrid. All suicide attempters from this catchment area receive medical attention in this hospital. We studied 134 female attempters who came to this emergency room from January 1996 to December 1997. Of the initial 134 female patients selected, 80 were 18 years of age or over, did not take oral contraceptives, and had regular menstrual cycles. Plasma hormone level assays (13) classified the menstrual cycle into the physiological phases: follicular, midcycle, and luteal. Additionally, the follicular phase was divided into menses and the nonmenstrual follicular phase. Using theoretical controls (expected frequencies) of the phase durations for statistical analyses, the menses (and the follicular phase) was significantly associated with suicide attempts. Premenstrual symptoms, by retrospective assessment, were not associated with suicide attempts (11).

There was a five-fold increase in suicide attempts during the follicular phase associated with a history of a major axis I diagnosis and a three-fold decrease of personality disorder diagnosis in the follicular phase vs. the luteal phase (14).

Recruiting suicide attempters in the emergency room is particularly difficult. Almost all prior published studies were conducted before written informed consent was required for clinical studies. Our prior study (11) was noteworthy for important improvements as compared with prior studies using self-report, but it, too, had limitations in several areas: 1) sampling: although the sample represented all suicide attempts from a catchment area, only 70% of patients were invited to consent; 2) controls: using theoretical controls (expected frequencies) of the duration of the menses for statistical analyses; 3) statistics: use of simple statistical analyses (chi-square tests) that do not allow for extrapolation to the population; and 4) diagnosis: use of "clinical diagnoses" instead of research diagnoses generated by diagnostic interviews.

This second study aims to replicate our finding that there is an association between suicide attempts and the menses in fertile women. The main hypothesis is that the proportion of suicide attempters during menses is significantly higher than the expected probability that a fertile woman from the general population would be in the menses. This replication’s improvements included using all consecutive subjects, calculating the duration of the menses by using control subjects, performing more sophisticated statistical analyses to extrapolate to the population, and using diagnostic interviews for psychiatric diagnoses.

	METHODS

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Sample
The collection of suicide attempts samples began on February 1, 1999, and ended on January 31, 2000. The methods were very similar to the prior study. This time, all attempters presenting to the Ramon y Cajal Hospital were approached for recruitment. As before, suicide attempts were defined as "a self-destructive behavior with intent to end one’s life independent of resulting damage" (15). The only inclusion criteria were meeting this definition and signing the consent form. The only exclusion criteria were unwillingness to consent, prior participation, and age younger than 18 years. There were 350 attempts by 315 patients. No patient from the prior study was included in the replication study. The total study sample size included 264 suicide attempters (182 or 69% women and 82 or 31% men). The number of consenting individuals was high, 84% (264 of 315). Sixty-six percent (120 of 182) of consenting women, not currently on hormonal contraceptives, with regular menstrual cycles were included in this article’s analysis. As in the first study, regular menstrual cycles were defined as lasting 28 ± 6 days in the last three cycles. Of the 62 (34% of 182) excluded, 8 (4% of 182) used hormonal contraceptives. The rest were mainly menopausal women or those with irregular menstrual cycles. Table 1 provides the demographic and clinical data for the 120 female suicide attempters studied.

Establishing the Normal Duration of Menses With Control Subjects
In our prior study, the association between the menses and suicide attempts was tested using a theoretical distribution expected in the general population. This was calculated by assuming an average expected duration of 4 days for the menses and of 28 days for the menstrual cycle (menses: 4/28 = 0.14 or 14%; nonmenstrual phase: 24/28 = 0.86 or 86%). This method is compatible with that published in a standard textbook of internal medicine: "The mean duration of the menstrual cycle is 28 ± 3 days" and "of the menstrual flow is 4 ± 2 days" (25). Some may argue that in our first study, the small significant increase of suicide attempts was due to an artifact of the individual variations of the duration of menses in female suicide attempters; therefore, control subjects were recruited for this current study. Moreover, the data from the prior study was recalculated using the duration of the menses in control subjects (0.155 or 15.5%, see below). The results continued to be significant.

The control sample to determine the duration of the menses and the menstrual cycle included 160 fertile female blood donors at the same hospital with no history of suicidal behavior or psychiatric disorders. As in the first study, blood samples for sex hormones were collected from control subjects and from attempters in the first 24 hours (11). The hospital laboratory analyzed sex hormones (estradiol, progesterone, follicle-stimulating hormone, and luteinizing hormone) by a chemoluminescent enzyme immunoassay (13). As shown by the overlap in 95% confidence intervals, the patients and control subjects had similar values (Fig. 1).

View larger version (21K): [in this window] [in a new window]   Fig. 1. Hormonal levels in control subjects and patients across menstrual cycle phases. FSH = follicle-stimulating hormone; LH = luteinizing hormone.

Extrapolation to the Population
The catchment area has a little more than 503,000 people, including 99,481 women older than 45 years of age and 93,613 aged 18 to 45 years. Almost all are Spanish and Caucasians. During the replication study year, 155 fertile adult women came to the hospital after a suicide attempt. Therefore, the population’s annual rate of fertile women treated after a suicide attempt was approximately 166 per 100,000.

SPSS (26) was used for statistical analyses. For the follicular phase, an expected probability of 0.39 (11/28) was used. A complex method using probabilistic notions was used to establish the increased risk of suicide attempt during the menses (see technical discussion using the multiplication law of probability (27) in a footnote of Table 2). The idea is to compute a number (called k in the statistical analysis) that compares the probability of attempting suicide during menses with the probability of attempting suicide for a fertile woman at any moment of the menstrual cycle. k is closely related to Levin’s population attributable risk (AR) (28) (see Table 2).

	RESULTS

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Increased Probability of Suicide Attempts During Menses
The observed proportions of suicide attempters during menses were 0.25 (95% CI = 0.15–0.36) for the first study and 0.27 (CI = 0.19–0.35) for the second study. The observed proportions in the follicular phase were 0.51 (CI = 0.41–0.62) for the first study and 0.62 (CI = 0.53–0.70) for the second study. Because of the overlap between the first and second study in the confidence intervals for menses (and the follicular phase), there were no significant differences between the results of both studies. Combining the first and second samples, the proportions of suicide attempters during the menses and follicular phases were 0.26 (CI = 0.20–0.32) and 0.57 (CI = 0.50–0.64), respectively.

The increased probability of attempted suicide during menses was 1.61 for the first study, 1.72 for the second study, and 1.68 for the two combined (Table 2). The increased probability of attempted suicide during the follicular phase was 1.31 for the first study, 1.58 for the second study, and 1.46 for both studies combined (Table 2). In summary, by combining the samples, the probability of attempting suicide during menses was 1.68 times higher than the overall probability of attempting suicide for fertile women. Similarly, it was 1.46 times higher during the follicular phase.

Public Health Implications
The annual population rate of fertile women treated after a suicide attempt was approximately 166 per 100,000 (see section on extrapolation to population). The rate for women during menses, obtained by combining both studies, was higher: 279 per 100,000 (279 = 1.68 x 166) (Table 2). That is, of 100,000 fertile women during the menses, 279 will arrive at the hospital because of a suicide attempt. The rate for women in the follicular phase was also higher, 242 per 100,000 (242 = 1.46 x 166) (Table 2). The AR associated with the menses and follicular phases were 13% and 29%, respectively (Table 2).

Lack of Interaction With Clinical Variables
The associations (found in the first study) between the follicular phase and attempts associated with an axis I diagnosis, and between the luteal phase and attempts associated with an axis II diagnosis (14), were not replicated. The frequency of women with a history of a major axis I diagnosis was 94% among those attempting suicide during menses and 93% among those attempting suicide during the rest of the menstrual cycle (p = 1.00). Eighty-nine percent of women attempting suicide both during menses and the rest of the menstrual cycle had an axis II diagnosis (p = 1.00).

The association between menses and suicide attempts was not significantly influenced by lethality, attempt impulsivity, impulsivity traits, major depression, life events, seasonality, or day-night period. These variables did not seem to influence the increased risk of suicide attempt during the menses. Therefore, this increased risk may occur across all diagnoses, all levels of lethality and impulsivity in the attempt, and impulsive traits.

	DISCUSSION

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Limitations
This study has all the limitations of naturalistic studies without an experimental design. Logically, completed suicides were not included in our study; one female attempter died in the hospital in that year. Moreover, the area death registry identified seven female deaths as suicides. The annual number of suicides per 100,000 women older than 18 years of age was 3.6 and for females of all ages was 2.9. The latter is similar to the Spanish rate in 1997: 3.5 per 100,000 females of all ages (29). This catchment area’s sample was highly representative of the suicide attempters seeking medical help. However, it did not reflect female attempters not seeking medical help or those not brought by their families or friends. It is impossible to conduct biological studies of subjects who, at the time of the attempt, are not taken to a hospital. A small number (16%) did not consent with the study; however, we think that an 84% cooperation rate is an extraordinarily high number considering the emergency and complexity of the situation.

Using a single determination to establish the menstrual cycle phase in attempters has some limitations, but it is a reasonable approach and is better than the self-reports used by most prior studies. Repeated hormonal assessment would have better established menstrual cycle phases. The first study demonstrated that patients were reticent to call in at the onset of the next menses after the suicide attempt; it would have been impossible to convince them to return for repeated hormonal assessments.

The limitations of using a single hormonal determination, and the limitations of any study on the relationship between the menstrual cycle and suicide, were previously discussed in detail (11). To summarize, three uncontrollable factors may influence the duration of the menstrual cycle: 1) irregular cycles, 2) stress, and 3) psychiatric medications (particularly antipsychotics). The lack of significant differences between duration of menses and the menstrual cycle, between patients and control subjects, suggests that prescribed psychiatric medications have no major influence on these durations (see next section). Excluding the attempters with irregular menstrual cycles may possibly have contributed to eliminating the most obvious cases of disturbances in the menstrual cycle associated with psychiatric medications, particularly antipsychotics.

Similar Durations of Menses in Suicide Attempters and Control Subjects
The two samples of suicide attempters and control subjects reported similar durations of the three last menses and menstrual cycles. In attempters, the average durations of the menses and menstrual cycles and ratios of these averages were, respectively, 4.2 days, 28.3 days, and 0.15 (4.2/28.3) in the prior study and 4.8 days, 27.6 days, and 0.17 (4.8/27.6) in the current study. The combined ratio from both studies of suicide attempters was 0.16 (4.6/27.9). This ratio is similar to the 16% (4.5/28.2) value calculated by using the reports of blood donor control subjects. The values are extremely close for all samples and provide very similar results in analyses. Moreover, the similarity of the ratios suggests that the durations of menses and cycles are not significantly different from those of control subjects. The next section further explains that the found significant differences cannot be explained by abnormal menstrual cycle duration in suicide attempters.

Robustness of the Increased Probability of Attempts During Menses
The proportion of suicide attempters during menses was significantly higher than the expected probability that a fertile woman from the general population is in menses. This implies that the probability of attempting suicide during menses is significantly higher than the overall probability of attempting suicide for fertile women and assumes no differences in the probability of being in menses between suicide attempters and control subjects.

Using the combined sample, the confidence interval for the proportion of suicide attempters during menses was 0.20 to 0.32, and it did not overlap with the confidence interval for a woman of the normal population during menses, 0.15 to 0.16. The very limited range of 0.01 (0.16 - 0.15 = 0.01), or 1% of probability, suggests that our estimation of menses duration in the general population is very accurate. As described in the prior section, the ratio calculated using reports from suicide attempters was 0.16 and within the confidence interval for control subjects (0.15–0.16).

In summary, the large difference between the confidence interval found in patients (0.20–0.32) and the confidence interval for the expected frequencies (0.15–0.16) suggests that our findings are quite robust and cannot be explained by variations in menses duration among women. Even supposing the average duration of menses in suicide attempters is as high as 5.5 days in a 28-day cycle (0.055/28 = 0.196), our results continue to suggest a significant increase of menses in suicide attempts (0.196 does not overlap with the confidence interval of 0.20–0.32).

Public Health Implications
The increased rate of 1.68 in suicide during menses is relatively small but significant. When extrapolated to the population, the annual rate increased from 166 to 279 per 100,000. The AR of the menses was 13%, suggesting that if a biological intervention is designed to completely prevent the menses effect in suicide attempters, the maximum decrease in suicide attempts will be 13%.

Extrapolating these results to other areas, including the United States, may be difficult. Like Spain, the United States does not have annual statistics on suicide attempts; the available annual statistics reflect only completed suicides. Crosby et al. (30) estimated that there are 700,000 reported suicide attempts in US adults per year and that 301,000 adults receive medical attention after a suicide attempt. Assuming that two thirds of the US suicide attempts are in women, approximately 198,660 women go to US hospitals after a suicide attempt yearly. Supposing that there are 85 million adult women in the US, 234 per 100,000 US adult females are receiving medical attention for a suicide attempt yearly. In our hospital, 94 adult females per 100,000 receive medical attention for a suicide attempt yearly. If the effect of menses is similar in US women, the increased rate of 1.68 of suicide attempts during menses will increase from 234 to 393 per 100,000.

Possible Explanations for Increased Probability of Suicide Attempts During Menses
Undeniably, low brain serotonergic activity is a biological factor related to suicidal behavior (5). It is the most replicated finding in modern biological psychiatry since the initial study was published more than a quarter of a century ago. Low serotonergic function is a stable marker of suicidal behavior risk independent of psychiatric diagnosis (5).

Most studies exploring the relationship between sexual hormones and serotonergic function have been performed in animals. Even in animal studies, it is uncertain if results from one area of the brain using a specific methodology can be extrapolated to the brain as a whole. However, it seems that estradiol may increase serotonergic and noradrenergic activity but may have antidopaminergic activity (31). Specifically, in the serotonin system, estradiol may increase serotonin synthesis, modify serotonin receptor balance, and decrease serotonin metabolism by inhibiting monoamine oxidase A (31). Progesterone and its metabolites function as neuroesteroids and bind to the -aminobutyric acid A (GABA-A) receptors, a system crucial for anxiety disorders. However, progesterone does not seem to influence serotonin synthesis (32).

Changes of brain serotonergic function associated with menses have not been well studied in the clinical setting (33, 34) . The results of one study suggested that plasma serotonin concentration has its lowest values at the onset of menstruation (35). Low levels of estrogens during the menses in vulnerable females may be associated with a further decrease in brain serotonergic activity, contributing to increased suicide risk. One old study hypothesized that the low estrogen levels during menses may contribute to suicide attempts (12).

Thus, results from animal studies suggest that the decrease of estradiol, rather than the decrease of progesterone, may explain a decrease of serotonergic function during menses that might be associated with our finding of increased suicide attempts during menses. Clinical studies also suggest the decrease of estradiol, rather than the decrease of progesterone, may be more likely to explain our findings since some data support that although estradiol may have antidepressive properties in some situations, progesterone and synthetic progestogens do not seem to have antidepressant activities (some synthetic progestogens may be depressogenic in some situations) (36, 37) .

New studies, measuring hormones and in vivo serotonergic function in representative samples of suicide attempters, are needed to verify this hypothesis. However, these studies will be difficult to perform in the emergency room unless new, simple, and valid measures of in vivo serotonergic function are developed.

Lack of Replication of the Influence of Psychiatric Diagnoses on the Association Between Menses and Suicide Attempts
We did not replicate the associations found in the prior study between the follicular phase and attempts associated with Axis I diagnosis and between the luteal phase and attempts associated with Axis II diagnosis. In the replication study, the research psychiatrist using the MINI diagnosed more than 90% of the patients with a current Axis I diagnosis. The more reliable replication study suggests that neither Axis I nor Axis II psychiatric diagnoses influence the association between the menstrual cycle and attempts.

Regarding possible interactions of depression with the menstrual cycle, a prospective study of many depressed women with a high risk of suicide is needed to properly test the possibility that depressive symptoms may peak in the luteal phase but may be associated with suicide attempts during menses, when the patients have more energy.

In conclusion, the reanalysis of the prior study data, using menstruation duration obtained from control subjects, still suggests that there is an increase of suicide attempts during menses. Our replication study verified this finding. Thus, both studies combined suggest that menses is associated with a significant increase of suicide attempts by a factor of 1.68. Using the data from the catchment area, the average risk of suicide attempt of 166 per 100,000 fertile females increases to 266 per 100,000 fertile females during menses. Replication of these results in other representative samples both in Spain and other countries is needed. Prospective longitudinal studies of the menstrual cycle in women at high risk for suicide attempts may alternatively explore the association between the suicide attempts and menses.

	ACKNOWLEDGMENTS

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This study was partly supported by two National Alliance for Research on Schizophrenia and Affective Disorders (NARSAD) Young Investigator Awards in 1998 and 2001 (Dr. Baca-Garcia). Dr. Diaz was supported by a grant from the Kentucky Department of Mental Health and Mental Retardation to the Department of Psychiatry, University of Kentucky, through the University Collaboration Project (Dr. de Leon). Margaret T. Susce, RN, MLT, helped with editing of this article. The authors are grateful to the Statistics Institute of the State of Madrid (Comunidad de Madrid) and to Dolores Nuñez in particular for help in obtaining the suicide mortality data.

Received for publication December 7, 2001.

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TOP ABSTRACT INTRODUCTION Suicide and the Menstrual... METHODS RESULTS DISCUSSION ACKNOWLEDGMENTS REFERENCES

 

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