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Gastrointestinal symptoms before and during menses in healthy women

Gastrointestinal symptoms before and during menses in healthy women Background: Little is known as to the extent gastrointestinal (GI) complaints are reported by women around menses. We aimed to describe GI symptoms that occurred premenstrually and during menses in healthy women, and to specifically assess the relationship of emotional symptoms to GI symptoms around menses. Methods: We recruited healthy, premenopausal adult women with no indication of GI, gynecologic, or psychiatric disease who were attending an outpatient gynecology clinic for well-woman care. They completed a survey that queried menstrual histories and the presence of GI and emotional symptoms. We compared the prevalence of primary GI symptoms (abdominal pain, diarrhea, constipation, nausea, vomiting), as well as pelvic pain and bloating, in the 5 days preceding menses and during menses, and assessed whether emotional symptoms or other factors were associated with the occurrence of GI symptoms. Results: Of 156 respondents, 73% experienced at least one of the primary GI symptoms either pre- or during menses, with abdominal pain (58% pre; 55% during) and diarrhea (24% pre; 28% during) being the most common. Those experiencing any emotional symptoms versus those without were more likely to report multiple (2 or more) primary GI symptoms, both premenstrually (depressed p = 0.006; anxiety p = 0.014) and during menses (depressed p < 0.001; anxiety p = 0.008). Fatigue was also very common (53% pre; 49% during), and was significantly associated with multiple GI symptoms in both menstrual cycle phases (pre p < 0.001; during p = 0.01). Conclusions: Emotional symptoms occurring in conjunction with GI symptoms are common perimenstrually, and as such may reflect shared underlying processes that intersect brain, gut, and hormonal pathways. Background Other research has examined emotional symptoms Many women describe having gastrointestinal (GI) symp- around menses, with many reporting that mood symp- toms around their menses, yet little research has been done toms such as depression can be exacerbated premenstru- to quantify the prevalence or nature of these symptoms, or ally [6-8]. Strine et al. found that 19% of American women to consider associated factors. The handful of studies that had menstrual complaints and those with menstrual com- have examined the occurrence of GI symptoms in relation plaints were more likely to also have mood symptoms [9]. to menses have enquired about a narrow range of symp- However, it is unknown whether women who experience toms (e.g. abdominal pain, bloating) or focused on individ- emotional symptoms around menses are any more likely uals with established GI disorders [1-4]. A recent study by to have concomitant GI symptoms. There is evidence that our group, in which women with inflammatory bowel dis- symptoms of depression and anxiety can influence the ease were compared with a sample of healthy women on a development and severity of GI symptoms within a variety range of upper and lower GI symptoms, found that peri- of GI conditions such as inflammatory bowel disease and menstrual GI symptoms were common both in women irritable bowel syndrome [10-12]. Nevertheless, there are with and without inflammatory bowel disease [5]. no studies to date which have assessed whether there is a relationship between mood and GI symptoms around menses in women with no history of GI disease. Although physical symptoms are known to accompany premenstrual * Correspondence: [email protected] Department of Clinical Health Psychology, Faculty of Medicine, University of syndrome, there has been little research undertaken to Manitoba, PZ350 - 771 Bannatyne Avenue, Winnipeg, MB R3E 3N4, Canada document which specific physical symptoms occur, and to Full list of author information is available at the end of the article © 2014 Bernstein et al.; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Bernstein et al. BMC Women's Health 2014, 14:14 Page 2 of 7 http://www.biomedcentral.com/1472-6874/14/14 what extent they relate to depressive or other emotional GI symptoms. The remaining two - bloating and pelvic symptoms [13]. pain – were considered to be possibly gynecologic in origin Our prior report [5] focused on GI symptoms and in the context of the perimenstrual period, and thus classi- menses in inflammatory bowel disease. In this report, fied as secondary GI symptoms; and (c) the presence of we aimed to explore relationships among GI symp- emotional symptoms (depressive symptoms, anxiety, ‘other’ toms and emotional symptoms occurring in the context emotional symptoms), and fatigue. The questionnaire was of menses in the cohort of healthy women. Discerning piloted with 20 women to assess clarity of the questions whether there is a relationship between emotional and and completion time, and adjustments were made as GI symptoms at a particular point in the menstrual cycle needed based on feedback. (i.e., premenstrually and during menses) may help clar- Participants were directed to consider their recent ify why some are more prone to GI upset during this menstrual experiences (defined as the previous three normal gynecological functioning. If there are interrela- menstrual cycles), and to report whether they had any of tionships, this may provide direction for potential under- the GI or emotional symptoms, either in the five days lying pathways relevant to psychiatric, gastroenterological before the onset of menses (pre-menstrual) and/or dur- and gynecological functioning. ing menses. Since this was an exploratory study with the goal of a brief survey to readily engage participants, we Methods did not ask more detailed questions at this point about Participants the severity of any reported symptoms, nor did we in- We recruited women from outpatient gynecology clinics clude specific pain measures, for example. While aspects in a large general hospital in Winnipeg, Canada. Individ- of medical history were reviewed to establish eligibility uals from a range of socioeconomic backgrounds attend for participation, participants were not clinically evalu- these urban hospital clinics, given universal access for ated regarding their medical history. health care. Consecutive premenopausal women over the age of eighteen who were being seen for routine Outcomes pelvic examinations and/or family counseling during a 3 The main outcome of interest was the proportion of month period in 2011 were invited to participate. Those women reporting any of the specific individual gastro- with any known GI diagnoses, including inflammatory intestinal or emotional symptoms either prior to or dur- bowel disease, irritable bowel syndrome, celiac disease, ing menses. We also calculated the proportion reporting those with active gynecological illness or symptoms 2 or more different primary gastrointestinal symptoms such as endometriosis or dysfunctional uterine bleeding, either prior to or during menses. Last, we stratified par- and those with known active psychiatric disorders such ticipants by the presence or absence of each of self- as depression, panic disorder, schizophrenia and post reported depressive symptoms, anxiety, fatigue, or history traumatic stress disorder, were excluded. All partici- of painful menses, and determined the proportion of per- pants completed a brief survey at the time of their clinic sons within each strata who reported any individual gastro- appointment. intestinal symptoms as well as those who reported 2 or All who took part were given information about the more gastrointestinal symptoms. study, and provided their consent. The study was ap- proved by the University of Manitoba Research Ethics Board. Statistical analyses Descriptive statistics were calculated detailing means, Questionnaire and design standard deviations, and proportions where appropriate. A questionnaire was developed to assess the range of Differences in proportions, comparing prevalence of physical and emotional symptoms that might occur spe- GI and emotional symptoms between the two men- cifically in conjunction with the premenstrual and menses strual phases, were assessed for statistical significance phases. As there were no validated measures that served with Fisher’s exact test. Similarly, differences in pro- that purpose, items were identified based on patient re- portions, comparing prevalence of GI symptoms for ports, literature review, and expert consensus from a team those with or without concurrent depressive symptoms, of gastroenterologists, gynecologists, and clinical psycholo- anxiety or fatigue, were each assessed for statistical sig- gists. Items were included that briefly queried (a) menstrual nificance using Fisher’s exact test. Finally, differences in history, including age at menarche, duration of menstrual proportions, comparing prevalence of GI symptoms for cycle, history of painful periods, and use of medicinal those with or without a history of painful menses, were contraception; (b) the presence of seven common GI assessed for statistical significance using Fisher’s exact test. symptoms, of which five - abdominal pain, constipation, P-values less than 0.05 were considered to be statistically diarrhea, nausea, and vomiting - were classified as primary significant. Bernstein et al. BMC Women's Health 2014, 14:14 Page 3 of 7 http://www.biomedcentral.com/1472-6874/14/14 Table 1 Respondent characteristics related to menstrual Results history (n = 156) Of the 225 women invited to participate, 89% (n = 220) Menstrual information Mean (SD) proceeded with the study. Of those, 156 healthy, pre- menopausal women met the eligibility requirements and Age at first menses 12.9 (1.8) provided completed data (Figure 1). The participants Menses duration in days 5.7 (3.3) were between the ages of 18 and 55, with a mean age of n (%) 32.3 years (standard deviation 9.9 years). The mean age Cycle duration at menarche was 12.9 and the mean number of days of <25 days 20 (13) menses was 5.2. Just over 50% reported that their men- 25–35 days 106 (68) ses were typically painful (Table 1). With regard to the prevalence of GI symptoms, nearly >35 days 30 (19) three-quarters of the sample (73%, n = 107) reported ex- History of painful menses 82 (53) periencing at least one of the primary GI symptoms pre- Using medicinal contraception 52 (33) menstrually, and about two-thirds (69%, n = 107) reported at least one GI symptom during menses (Table 2). Thirty- one percent had multiple primary GI symptoms, either symptoms were significantly more likely to report nausea premenstrually or during menses. The prevalence of each both before (38% vs 13%, p = 0.006) and during menses GI symptom was similar across the two phases, with (44% vs 11%, p = 0.002). Overall, individuals with emotional abdominal pain and diarrhea being the most common symptoms of either depression or anxiety, or those report- primary symptoms, and the secondary GI symptom of ing fatigue were significantly more likely to experience bloating being experienced most frequently overall. De- multiple primary GI symptoms, both prior to the onset of pressive symptoms were the most common emotional menses and during menses (p < 0.02 for all comparisons). symptoms reported in both the premenstrual and menses Participants who had a history of painful menses in phases. A significantly higher proportion reported de- general were also significantly more likely to experience pressive symptoms premenstrually (32%) than during men- ses (21%, P = 0.028). Fatigue was fairly pronounced, with Table 2 Proportion of women experiencing GI and about half endorsing that symptom in either phase (53% emotional symptoms, comparing prevalence rates in premenstrual; 49% during menses). premenstrual and menses phases Tables 3, 4, 5 and 6 detail the frequency of GI symp- Symptoms Premenstrual During toms in relation to emotional symptoms (Tables 3 and 4) p-value menses and fatigue (Tables 5 and 6), separately considering the Primary GI symptoms %% premenstrual and menstrual phases. Women experiencing Abdominal pain 58 55 0.73 depressive symptoms were significantly more likely to also Diarrhea 24 28 0.44 report diarrhea, both before (36% vs 19%, p = 0.028) and during menses (50% vs 23%, p = 0.004). Those with anxiety Nausea 17 14 0.53 Constipation 15 10 0.08 Vomiting 2 3 0.72 225 women were consecutively invited to Any primary symptoms 73 69 0.60 participate Multiple (≥2) primary 31 31 1.0 symptoms Secondary GI symptoms Bloating 62 51 0.07 200 (89%) completed the survey Pelvic pain 49 46 0.73 Any primary or secondary GI 83 83 1.0 symptoms Excluded: 17 due to concurrent gastrointestinal or gynecological Mood symptoms diagnosis; 27 due to menopause Depressed mood 32 21 0.028 Anxiety 15 10 0.30 Other 23 15 0.08 156 women in the final sample Any emotional symptoms 47 31 0.004 Figure 1 Flow diagram of participant recruitment in the Fatigue 53 49 0.50 outpatient clinics. Bolded p value denotes p < 0.05. Bernstein et al. BMC Women's Health 2014, 14:14 Page 4 of 7 http://www.biomedcentral.com/1472-6874/14/14 Table 3 Proportion (%) of women with GI symptoms premenstrually, comparing those with or without emotional symptoms Depressive symptoms Anxiety symptoms Yes No Yes No P value P value n = 50 n = 106 n = 24 n = 132 Primary GI symptoms %% % % Abdominal pain 68 53 0.118 62 58 0.88 Diarrhea 36 19 0.028 42 21 0.040 Nausea 28 11 0.012 38 13 0.006 Constipation 24 11 0.056 25 14 0.27 Vomiting 4 1 0.40 8 1 0.062 Any primary symptom 86 67 0.012 75 73 1.0 Multiple (≥2) primary symptoms 46 24 0.006 54 27 0.014 Secondary GI symptoms Bloating 82 52 <0.001 71 60 0.43 Pelvic pain 76 36 <0.001 58 47 0.42 Bolded p value denotes p < 0.05. primary GI symptoms. In the premenstrual phase, those pain was quite frequent, but around one-quarter of the with a history of painful menses were more likely to re- women also experienced bowel habit disturbance in the port abdominal pain (73% v 42%, p = 0.0001), diarrhea form of diarrhea. GI symptoms occurred at a similar rate (32% v 16%, p = 0.04), and nausea (27% v 5%, p = 0.0005) in both the premenstrual phase and during menses. than those without painful menses. In the menstrual However, therewas ahigherprevalenceofdepressedmood phase, those with a history of painful menses were more and fatigue premenstrually, compared to during menses. likely to report abdominal pain (73% v 34%, p < 0.0001) As well, GI symptoms occurred disproportionately more and nausea (24% v 3%, p = 0.0001), compared to those frequently with depressive or anxious emotional symptoms not reporting painful menses (data not shown). than when those were not present, both prior to and dur- ing menses. This significant co-occurrence was also ob- Discussion served for fatigue. In this study, we found the experience of one or more Studies that have assessed the prevalence of various GI GI symptoms was very common for healthy women both symptoms perimenstrually have generally concluded that before and during menses. Not surprisingly, abdominal GI symptoms were more common for those with GI Table 4 Proportion (%) of women with GI symptoms during menses, comparing those with or without emotional symptoms Depressive symptoms Anxiety symptoms Yes No Yes No P value P value n = 32 n = 124 n = 16 n = 140 Primary GI symptoms %% % % Abdominal pain 69 51 0.110 63 54 0.72 Diarrhea 50 23 0.004 50 26 0.074 Nausea 25 12 0.082 44 11 0.002 Constipation 19 7 0.085 13 9 0.94 Vomiting 6 2 0.187 13 1 0.053 Any primary symptom 81 66 0.144 81 68 0.42 Multiple (≥2) primary symptoms 59 23 <0.001 63 27 0.008 Secondary GI symptoms Bloating 78 44 0.001 69 49 0.186 Pelvic pain 72 39 0.001 69 43 0.064 Bolded p value denotes p < 0.05. Bernstein et al. BMC Women's Health 2014, 14:14 Page 5 of 7 http://www.biomedcentral.com/1472-6874/14/14 Table 5 Proportion (%) of women with GI symptoms and during menstruation [1,16,17] consistent with our premenstrually, comparing those with or without fatigue findings of a similar rate of GI symptom occurrence across Fatigue the premenstrual and menses phases. Bowel habit changes have not been as readily ad- Yes n = 83 No n = 73 P value dressed, but Kane and colleagues [14] described equiva- Primary GI symptoms %% lent rates of diarrhea (20%) and constipation (20%) Abdominal pain 63 53 0.32 premenstrually, and lower rates of altered bowel habit Diarrhea 34 14 0.005 during menses (diarrhea 10%; constipation 2%) in their Nausea 23 10 0.032 sample of healthy women. Two studies found that ap- Constipation 19 11 0.185 proximately one third of women experienced bowel Vomiting 4 0 0.51 habit changes during menses, with diarrhea being more common [1,4]. We also found diarrhea (24-28%) to be Any primary symptom 78 67 0.148 more common than constipation (10-15%), regardless of Multiple (≥2) primary 43 16 <0.001 the menses phase. The lower rates for the Kane study symptoms might relate to their recruitment approach as they posted Secondary GI symptoms ads on a university campus, whereas the other studies, Bloating 77 44 <0.001 including ours, recruited from outpatient clinics offering Pelvic pain 63 33 <0.001 routine gynecological care. Bolded p value denotes p < 0.05. There has been little work to examine potential pre- dictors of GI symptoms in relation to menses. Our ex- ploratory study identified that depressed mood, anxiety disorders than for healthy women [1,3,14,15]. It was evi- and fatigue were each significantly more likely to be as- dent in our study that GI symptoms were quite preva- sociated with primary GI symptoms. Similarly, women lent for healthy women as well, as over 70% experienced who had a history of painful menses were also more GI symptoms in conjunction with their menstrual cycle, likely to experience GI symptoms perimenstrually. Previ- even when potential gynecological symptoms such as ous work assessing the relationship between GI symp- bloating were excluded. Some studies focused just on toms and both enduring personality traits and acute menses, and when they included more than one phase, psychological symptoms with GI symptoms during men- they tended to report more frequent GI symptoms during struation did not find any significant relationship [1]. In menses than other phases [3,15], although one of these that study, women who reported their GI symptoms studies reported on intensity but not the prevalence of GI were exacerbated during their menses did not differ in symptoms [15]. Other prospective studies described ab- their psychological profiles from women who did not re- dominal pain, nausea, and bloating as the predominant GI port these symptoms [1]. Keisner and colleagues reported symptoms, and found they tended to increase just before a significant association between premenstrual depressive symptoms and a number of physical symptoms, of which Table 6 Proportion (%) of women with GI symptoms GI symptoms were included [13]. during menses, comparing those with or without fatigue Depression, pain, and gut motility may share similar Fatigue pathophysiological mechanisms including serotonin as Yes No an important neurotransmitter mediating those symp- P value toms [1]. A study that found women in the late luteal (n = 48) (n = 107) phase experienced reduced pain tolerance, using a cold Primary GI symptoms %% pressor test, provides some evidence for somatic neural Abdominal pain 61 49 0.197 changes related to the timing within the cycle [18]. Diarrhea 34 23 0.113 There has also been consideration of the effect of hor- Nausea 19 10 0.168 monal activity in local tissue, with a recent study sug- Constipation 13 6 0.179 gesting that physical symptoms, including GI symptoms, Vomiting 5 0 0.054 may indicate sensitivity to reproductive steroids, and that concurrent psychological symptoms may reflect neuro- Any primary symptom 72 66 0.478 logical sensitivity to these steroids, at a peak point in the Multiple (≥2) primary symptoms 41 21 0.010 menstrual cycle [19]. Prostaglandins may provide another Secondary GI symptoms %% pathophysiological link to understand the overlap between Bloating 63 39 0.003 menstrual pain and gastrointestinal symptoms. Premen- Pelvic pain 58 34 0.004 strually, uterine prostaglandin production may mediate an Bolded p value denotes p < 0.05. inflammatory response characterized by pain, and during Bernstein et al. BMC Women's Health 2014, 14:14 Page 6 of 7 http://www.biomedcentral.com/1472-6874/14/14 menses abnormally high levels of prostaglandins in men- Conclusions strual fluid may induce abnormal uterine contractions and In conclusion, the occurrence of GI symptoms in con- pain [17,20]. In the gut, prostaglandins can cause smooth junction with the premenstrual and menses phases is muscle contractions, as well as reduced absorption and in- fairly common, and is disproportionately more likely if duced secretion of electrolytes in the small bowel, all of there are also accompanying emotional symptoms. These which may enhance gastrointestinal pain and diarrhea co-occurring experiences may reflect underlying com- [21]. It is not known whether uterine prostaglandins mon mechanisms which can provide direction for symp- are transported to the gut, or whether parallel changes tom relief. Given the exploratory nature of the study, in uterine and GI smooth muscle prostaglandin levels prospective work tracking GI and emotional symptom occur during menses [17]. Further study will be neces- severity in the context of the menses phases will be im- sary to determine pathophysiological mechanisms for portant as a next step. It will be useful to discern whether mood changes within the cycle as well and the direc- GI symptoms contribute to the mood disorder that af- tion of the relationship of these changes between brain fects many women prior to and during menses or alter- and GI function. natively, whether depressive and anxiety symptoms are While these findings are preliminary, they suggest that predominately impacting on GI symptoms, as these rela- clinicians should be aware of the heightened potential tionships may have implications for managing the symp- for co-occurring gastrointestinal and emotional symp- toms therapeutically. toms perimenstrually, and could consider providing infor- Competing interests mation to their patients to help normalize the experience. Laura E Targownik is supported by a Canadian Institutes of Health Research If the GI symptoms become troubling or problematic, it New Investigator Award. The authors declare they have no competing interests. may be useful to consider prophylactic steps to alleviate the symptoms through use of medication or behavioral Authors’ contributions MT was involved in the concept, design, data acquisition, analyses and approaches, parallel to the approach used to manage interpretation of data, manuscript draft preparation, and revisions for critical gynecological symptoms during menses (e.g., analgesic content. LG was involved in the concept, design, analyses and interpretation medication for dysmenorrhea). of data, manuscript draft and revisions for critical content. LA was involved in the concept, design, data acquisition, manuscript draft preparation and There are limitations to the study. It was exploratory revisions for critical content. CP was involved in the data acquisition, analyses in nature, aiming to assess the presence of GI and emo- and interpretation of data, manuscript draft preparation and revisions for critical tional symptoms perimenstrually using participant obser- content. KP was involved in the data acquisition, manuscript draft preparation and revisions for critical content. LT was involved in the analyses and vation, with minimal participant burden. There were no interpretation of data, manuscript draft and revisions for critical content. All validated scales that included all the symptoms of interest, authors read and approved the final manuscript. so a brief history and symptom measure was developed for the study. This had the benefit of assessing the variables of Acknowledgements There were no external funds used to support this study. interest using the same response scale, for ready compari- son. However, the validity of the symptom measure was Author details not established, and further, the duration and severity of Department of Internal Medicine, University of Manitoba, Winnipeg, Canada. Department of Clinical Health Psychology, Faculty of Medicine, University of symptoms could not be determined as the measure simply Manitoba, PZ350 - 771 Bannatyne Avenue, Winnipeg, MB R3E 3N4, Canada. assessed presence/absence of symptoms. Subsequent inves- Department of Obstetrics and Gynecology, University of Manitoba, tigation of potentially relevant variables identified in this Winnipeg, Canada. preliminary study, such as depression, anxiety, and pain, Received: 31 January 2013 Accepted: 21 January 2014 should include validated measures. Second, participants Published: 22 January 2014 reported their perimenstrual symptoms retrospectively, which increases the likelihood of recall bias. Neverthe- References 1. 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Expert Rev Pharmacoecon Outcomes Res 2004, 4(2):159–163. doi:10.1186/1472-6874-14-14 Cite this article as: Bernstein et al.: Gastrointestinal symptoms before and during menses in healthy women. BMC Women's Health 2014 14:14. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Women's Health Springer Journals

Gastrointestinal symptoms before and during menses in healthy women

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Copyright © 2014 by Bernstein et al.; licensee BioMed Central Ltd.
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Medicine & Public Health; Gynecology; Maternal and Child Health; Reproductive Medicine
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Abstract

Background: Little is known as to the extent gastrointestinal (GI) complaints are reported by women around menses. We aimed to describe GI symptoms that occurred premenstrually and during menses in healthy women, and to specifically assess the relationship of emotional symptoms to GI symptoms around menses. Methods: We recruited healthy, premenopausal adult women with no indication of GI, gynecologic, or psychiatric disease who were attending an outpatient gynecology clinic for well-woman care. They completed a survey that queried menstrual histories and the presence of GI and emotional symptoms. We compared the prevalence of primary GI symptoms (abdominal pain, diarrhea, constipation, nausea, vomiting), as well as pelvic pain and bloating, in the 5 days preceding menses and during menses, and assessed whether emotional symptoms or other factors were associated with the occurrence of GI symptoms. Results: Of 156 respondents, 73% experienced at least one of the primary GI symptoms either pre- or during menses, with abdominal pain (58% pre; 55% during) and diarrhea (24% pre; 28% during) being the most common. Those experiencing any emotional symptoms versus those without were more likely to report multiple (2 or more) primary GI symptoms, both premenstrually (depressed p = 0.006; anxiety p = 0.014) and during menses (depressed p < 0.001; anxiety p = 0.008). Fatigue was also very common (53% pre; 49% during), and was significantly associated with multiple GI symptoms in both menstrual cycle phases (pre p < 0.001; during p = 0.01). Conclusions: Emotional symptoms occurring in conjunction with GI symptoms are common perimenstrually, and as such may reflect shared underlying processes that intersect brain, gut, and hormonal pathways. Background Other research has examined emotional symptoms Many women describe having gastrointestinal (GI) symp- around menses, with many reporting that mood symp- toms around their menses, yet little research has been done toms such as depression can be exacerbated premenstru- to quantify the prevalence or nature of these symptoms, or ally [6-8]. Strine et al. found that 19% of American women to consider associated factors. The handful of studies that had menstrual complaints and those with menstrual com- have examined the occurrence of GI symptoms in relation plaints were more likely to also have mood symptoms [9]. to menses have enquired about a narrow range of symp- However, it is unknown whether women who experience toms (e.g. abdominal pain, bloating) or focused on individ- emotional symptoms around menses are any more likely uals with established GI disorders [1-4]. A recent study by to have concomitant GI symptoms. There is evidence that our group, in which women with inflammatory bowel dis- symptoms of depression and anxiety can influence the ease were compared with a sample of healthy women on a development and severity of GI symptoms within a variety range of upper and lower GI symptoms, found that peri- of GI conditions such as inflammatory bowel disease and menstrual GI symptoms were common both in women irritable bowel syndrome [10-12]. Nevertheless, there are with and without inflammatory bowel disease [5]. no studies to date which have assessed whether there is a relationship between mood and GI symptoms around menses in women with no history of GI disease. Although physical symptoms are known to accompany premenstrual * Correspondence: [email protected] Department of Clinical Health Psychology, Faculty of Medicine, University of syndrome, there has been little research undertaken to Manitoba, PZ350 - 771 Bannatyne Avenue, Winnipeg, MB R3E 3N4, Canada document which specific physical symptoms occur, and to Full list of author information is available at the end of the article © 2014 Bernstein et al.; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Bernstein et al. BMC Women's Health 2014, 14:14 Page 2 of 7 http://www.biomedcentral.com/1472-6874/14/14 what extent they relate to depressive or other emotional GI symptoms. The remaining two - bloating and pelvic symptoms [13]. pain – were considered to be possibly gynecologic in origin Our prior report [5] focused on GI symptoms and in the context of the perimenstrual period, and thus classi- menses in inflammatory bowel disease. In this report, fied as secondary GI symptoms; and (c) the presence of we aimed to explore relationships among GI symp- emotional symptoms (depressive symptoms, anxiety, ‘other’ toms and emotional symptoms occurring in the context emotional symptoms), and fatigue. The questionnaire was of menses in the cohort of healthy women. Discerning piloted with 20 women to assess clarity of the questions whether there is a relationship between emotional and and completion time, and adjustments were made as GI symptoms at a particular point in the menstrual cycle needed based on feedback. (i.e., premenstrually and during menses) may help clar- Participants were directed to consider their recent ify why some are more prone to GI upset during this menstrual experiences (defined as the previous three normal gynecological functioning. If there are interrela- menstrual cycles), and to report whether they had any of tionships, this may provide direction for potential under- the GI or emotional symptoms, either in the five days lying pathways relevant to psychiatric, gastroenterological before the onset of menses (pre-menstrual) and/or dur- and gynecological functioning. ing menses. Since this was an exploratory study with the goal of a brief survey to readily engage participants, we Methods did not ask more detailed questions at this point about Participants the severity of any reported symptoms, nor did we in- We recruited women from outpatient gynecology clinics clude specific pain measures, for example. While aspects in a large general hospital in Winnipeg, Canada. Individ- of medical history were reviewed to establish eligibility uals from a range of socioeconomic backgrounds attend for participation, participants were not clinically evalu- these urban hospital clinics, given universal access for ated regarding their medical history. health care. Consecutive premenopausal women over the age of eighteen who were being seen for routine Outcomes pelvic examinations and/or family counseling during a 3 The main outcome of interest was the proportion of month period in 2011 were invited to participate. Those women reporting any of the specific individual gastro- with any known GI diagnoses, including inflammatory intestinal or emotional symptoms either prior to or dur- bowel disease, irritable bowel syndrome, celiac disease, ing menses. We also calculated the proportion reporting those with active gynecological illness or symptoms 2 or more different primary gastrointestinal symptoms such as endometriosis or dysfunctional uterine bleeding, either prior to or during menses. Last, we stratified par- and those with known active psychiatric disorders such ticipants by the presence or absence of each of self- as depression, panic disorder, schizophrenia and post reported depressive symptoms, anxiety, fatigue, or history traumatic stress disorder, were excluded. All partici- of painful menses, and determined the proportion of per- pants completed a brief survey at the time of their clinic sons within each strata who reported any individual gastro- appointment. intestinal symptoms as well as those who reported 2 or All who took part were given information about the more gastrointestinal symptoms. study, and provided their consent. The study was ap- proved by the University of Manitoba Research Ethics Board. Statistical analyses Descriptive statistics were calculated detailing means, Questionnaire and design standard deviations, and proportions where appropriate. A questionnaire was developed to assess the range of Differences in proportions, comparing prevalence of physical and emotional symptoms that might occur spe- GI and emotional symptoms between the two men- cifically in conjunction with the premenstrual and menses strual phases, were assessed for statistical significance phases. As there were no validated measures that served with Fisher’s exact test. Similarly, differences in pro- that purpose, items were identified based on patient re- portions, comparing prevalence of GI symptoms for ports, literature review, and expert consensus from a team those with or without concurrent depressive symptoms, of gastroenterologists, gynecologists, and clinical psycholo- anxiety or fatigue, were each assessed for statistical sig- gists. Items were included that briefly queried (a) menstrual nificance using Fisher’s exact test. Finally, differences in history, including age at menarche, duration of menstrual proportions, comparing prevalence of GI symptoms for cycle, history of painful periods, and use of medicinal those with or without a history of painful menses, were contraception; (b) the presence of seven common GI assessed for statistical significance using Fisher’s exact test. symptoms, of which five - abdominal pain, constipation, P-values less than 0.05 were considered to be statistically diarrhea, nausea, and vomiting - were classified as primary significant. Bernstein et al. BMC Women's Health 2014, 14:14 Page 3 of 7 http://www.biomedcentral.com/1472-6874/14/14 Table 1 Respondent characteristics related to menstrual Results history (n = 156) Of the 225 women invited to participate, 89% (n = 220) Menstrual information Mean (SD) proceeded with the study. Of those, 156 healthy, pre- menopausal women met the eligibility requirements and Age at first menses 12.9 (1.8) provided completed data (Figure 1). The participants Menses duration in days 5.7 (3.3) were between the ages of 18 and 55, with a mean age of n (%) 32.3 years (standard deviation 9.9 years). The mean age Cycle duration at menarche was 12.9 and the mean number of days of <25 days 20 (13) menses was 5.2. Just over 50% reported that their men- 25–35 days 106 (68) ses were typically painful (Table 1). With regard to the prevalence of GI symptoms, nearly >35 days 30 (19) three-quarters of the sample (73%, n = 107) reported ex- History of painful menses 82 (53) periencing at least one of the primary GI symptoms pre- Using medicinal contraception 52 (33) menstrually, and about two-thirds (69%, n = 107) reported at least one GI symptom during menses (Table 2). Thirty- one percent had multiple primary GI symptoms, either symptoms were significantly more likely to report nausea premenstrually or during menses. The prevalence of each both before (38% vs 13%, p = 0.006) and during menses GI symptom was similar across the two phases, with (44% vs 11%, p = 0.002). Overall, individuals with emotional abdominal pain and diarrhea being the most common symptoms of either depression or anxiety, or those report- primary symptoms, and the secondary GI symptom of ing fatigue were significantly more likely to experience bloating being experienced most frequently overall. De- multiple primary GI symptoms, both prior to the onset of pressive symptoms were the most common emotional menses and during menses (p < 0.02 for all comparisons). symptoms reported in both the premenstrual and menses Participants who had a history of painful menses in phases. A significantly higher proportion reported de- general were also significantly more likely to experience pressive symptoms premenstrually (32%) than during men- ses (21%, P = 0.028). Fatigue was fairly pronounced, with Table 2 Proportion of women experiencing GI and about half endorsing that symptom in either phase (53% emotional symptoms, comparing prevalence rates in premenstrual; 49% during menses). premenstrual and menses phases Tables 3, 4, 5 and 6 detail the frequency of GI symp- Symptoms Premenstrual During toms in relation to emotional symptoms (Tables 3 and 4) p-value menses and fatigue (Tables 5 and 6), separately considering the Primary GI symptoms %% premenstrual and menstrual phases. Women experiencing Abdominal pain 58 55 0.73 depressive symptoms were significantly more likely to also Diarrhea 24 28 0.44 report diarrhea, both before (36% vs 19%, p = 0.028) and during menses (50% vs 23%, p = 0.004). Those with anxiety Nausea 17 14 0.53 Constipation 15 10 0.08 Vomiting 2 3 0.72 225 women were consecutively invited to Any primary symptoms 73 69 0.60 participate Multiple (≥2) primary 31 31 1.0 symptoms Secondary GI symptoms Bloating 62 51 0.07 200 (89%) completed the survey Pelvic pain 49 46 0.73 Any primary or secondary GI 83 83 1.0 symptoms Excluded: 17 due to concurrent gastrointestinal or gynecological Mood symptoms diagnosis; 27 due to menopause Depressed mood 32 21 0.028 Anxiety 15 10 0.30 Other 23 15 0.08 156 women in the final sample Any emotional symptoms 47 31 0.004 Figure 1 Flow diagram of participant recruitment in the Fatigue 53 49 0.50 outpatient clinics. Bolded p value denotes p < 0.05. Bernstein et al. BMC Women's Health 2014, 14:14 Page 4 of 7 http://www.biomedcentral.com/1472-6874/14/14 Table 3 Proportion (%) of women with GI symptoms premenstrually, comparing those with or without emotional symptoms Depressive symptoms Anxiety symptoms Yes No Yes No P value P value n = 50 n = 106 n = 24 n = 132 Primary GI symptoms %% % % Abdominal pain 68 53 0.118 62 58 0.88 Diarrhea 36 19 0.028 42 21 0.040 Nausea 28 11 0.012 38 13 0.006 Constipation 24 11 0.056 25 14 0.27 Vomiting 4 1 0.40 8 1 0.062 Any primary symptom 86 67 0.012 75 73 1.0 Multiple (≥2) primary symptoms 46 24 0.006 54 27 0.014 Secondary GI symptoms Bloating 82 52 <0.001 71 60 0.43 Pelvic pain 76 36 <0.001 58 47 0.42 Bolded p value denotes p < 0.05. primary GI symptoms. In the premenstrual phase, those pain was quite frequent, but around one-quarter of the with a history of painful menses were more likely to re- women also experienced bowel habit disturbance in the port abdominal pain (73% v 42%, p = 0.0001), diarrhea form of diarrhea. GI symptoms occurred at a similar rate (32% v 16%, p = 0.04), and nausea (27% v 5%, p = 0.0005) in both the premenstrual phase and during menses. than those without painful menses. In the menstrual However, therewas ahigherprevalenceofdepressedmood phase, those with a history of painful menses were more and fatigue premenstrually, compared to during menses. likely to report abdominal pain (73% v 34%, p < 0.0001) As well, GI symptoms occurred disproportionately more and nausea (24% v 3%, p = 0.0001), compared to those frequently with depressive or anxious emotional symptoms not reporting painful menses (data not shown). than when those were not present, both prior to and dur- ing menses. This significant co-occurrence was also ob- Discussion served for fatigue. In this study, we found the experience of one or more Studies that have assessed the prevalence of various GI GI symptoms was very common for healthy women both symptoms perimenstrually have generally concluded that before and during menses. Not surprisingly, abdominal GI symptoms were more common for those with GI Table 4 Proportion (%) of women with GI symptoms during menses, comparing those with or without emotional symptoms Depressive symptoms Anxiety symptoms Yes No Yes No P value P value n = 32 n = 124 n = 16 n = 140 Primary GI symptoms %% % % Abdominal pain 69 51 0.110 63 54 0.72 Diarrhea 50 23 0.004 50 26 0.074 Nausea 25 12 0.082 44 11 0.002 Constipation 19 7 0.085 13 9 0.94 Vomiting 6 2 0.187 13 1 0.053 Any primary symptom 81 66 0.144 81 68 0.42 Multiple (≥2) primary symptoms 59 23 <0.001 63 27 0.008 Secondary GI symptoms Bloating 78 44 0.001 69 49 0.186 Pelvic pain 72 39 0.001 69 43 0.064 Bolded p value denotes p < 0.05. Bernstein et al. BMC Women's Health 2014, 14:14 Page 5 of 7 http://www.biomedcentral.com/1472-6874/14/14 Table 5 Proportion (%) of women with GI symptoms and during menstruation [1,16,17] consistent with our premenstrually, comparing those with or without fatigue findings of a similar rate of GI symptom occurrence across Fatigue the premenstrual and menses phases. Bowel habit changes have not been as readily ad- Yes n = 83 No n = 73 P value dressed, but Kane and colleagues [14] described equiva- Primary GI symptoms %% lent rates of diarrhea (20%) and constipation (20%) Abdominal pain 63 53 0.32 premenstrually, and lower rates of altered bowel habit Diarrhea 34 14 0.005 during menses (diarrhea 10%; constipation 2%) in their Nausea 23 10 0.032 sample of healthy women. Two studies found that ap- Constipation 19 11 0.185 proximately one third of women experienced bowel Vomiting 4 0 0.51 habit changes during menses, with diarrhea being more common [1,4]. We also found diarrhea (24-28%) to be Any primary symptom 78 67 0.148 more common than constipation (10-15%), regardless of Multiple (≥2) primary 43 16 <0.001 the menses phase. The lower rates for the Kane study symptoms might relate to their recruitment approach as they posted Secondary GI symptoms ads on a university campus, whereas the other studies, Bloating 77 44 <0.001 including ours, recruited from outpatient clinics offering Pelvic pain 63 33 <0.001 routine gynecological care. Bolded p value denotes p < 0.05. There has been little work to examine potential pre- dictors of GI symptoms in relation to menses. Our ex- ploratory study identified that depressed mood, anxiety disorders than for healthy women [1,3,14,15]. It was evi- and fatigue were each significantly more likely to be as- dent in our study that GI symptoms were quite preva- sociated with primary GI symptoms. Similarly, women lent for healthy women as well, as over 70% experienced who had a history of painful menses were also more GI symptoms in conjunction with their menstrual cycle, likely to experience GI symptoms perimenstrually. Previ- even when potential gynecological symptoms such as ous work assessing the relationship between GI symp- bloating were excluded. Some studies focused just on toms and both enduring personality traits and acute menses, and when they included more than one phase, psychological symptoms with GI symptoms during men- they tended to report more frequent GI symptoms during struation did not find any significant relationship [1]. In menses than other phases [3,15], although one of these that study, women who reported their GI symptoms studies reported on intensity but not the prevalence of GI were exacerbated during their menses did not differ in symptoms [15]. Other prospective studies described ab- their psychological profiles from women who did not re- dominal pain, nausea, and bloating as the predominant GI port these symptoms [1]. Keisner and colleagues reported symptoms, and found they tended to increase just before a significant association between premenstrual depressive symptoms and a number of physical symptoms, of which Table 6 Proportion (%) of women with GI symptoms GI symptoms were included [13]. during menses, comparing those with or without fatigue Depression, pain, and gut motility may share similar Fatigue pathophysiological mechanisms including serotonin as Yes No an important neurotransmitter mediating those symp- P value toms [1]. A study that found women in the late luteal (n = 48) (n = 107) phase experienced reduced pain tolerance, using a cold Primary GI symptoms %% pressor test, provides some evidence for somatic neural Abdominal pain 61 49 0.197 changes related to the timing within the cycle [18]. Diarrhea 34 23 0.113 There has also been consideration of the effect of hor- Nausea 19 10 0.168 monal activity in local tissue, with a recent study sug- Constipation 13 6 0.179 gesting that physical symptoms, including GI symptoms, Vomiting 5 0 0.054 may indicate sensitivity to reproductive steroids, and that concurrent psychological symptoms may reflect neuro- Any primary symptom 72 66 0.478 logical sensitivity to these steroids, at a peak point in the Multiple (≥2) primary symptoms 41 21 0.010 menstrual cycle [19]. Prostaglandins may provide another Secondary GI symptoms %% pathophysiological link to understand the overlap between Bloating 63 39 0.003 menstrual pain and gastrointestinal symptoms. Premen- Pelvic pain 58 34 0.004 strually, uterine prostaglandin production may mediate an Bolded p value denotes p < 0.05. inflammatory response characterized by pain, and during Bernstein et al. BMC Women's Health 2014, 14:14 Page 6 of 7 http://www.biomedcentral.com/1472-6874/14/14 menses abnormally high levels of prostaglandins in men- Conclusions strual fluid may induce abnormal uterine contractions and In conclusion, the occurrence of GI symptoms in con- pain [17,20]. In the gut, prostaglandins can cause smooth junction with the premenstrual and menses phases is muscle contractions, as well as reduced absorption and in- fairly common, and is disproportionately more likely if duced secretion of electrolytes in the small bowel, all of there are also accompanying emotional symptoms. These which may enhance gastrointestinal pain and diarrhea co-occurring experiences may reflect underlying com- [21]. It is not known whether uterine prostaglandins mon mechanisms which can provide direction for symp- are transported to the gut, or whether parallel changes tom relief. Given the exploratory nature of the study, in uterine and GI smooth muscle prostaglandin levels prospective work tracking GI and emotional symptom occur during menses [17]. Further study will be neces- severity in the context of the menses phases will be im- sary to determine pathophysiological mechanisms for portant as a next step. It will be useful to discern whether mood changes within the cycle as well and the direc- GI symptoms contribute to the mood disorder that af- tion of the relationship of these changes between brain fects many women prior to and during menses or alter- and GI function. natively, whether depressive and anxiety symptoms are While these findings are preliminary, they suggest that predominately impacting on GI symptoms, as these rela- clinicians should be aware of the heightened potential tionships may have implications for managing the symp- for co-occurring gastrointestinal and emotional symp- toms therapeutically. toms perimenstrually, and could consider providing infor- Competing interests mation to their patients to help normalize the experience. Laura E Targownik is supported by a Canadian Institutes of Health Research If the GI symptoms become troubling or problematic, it New Investigator Award. The authors declare they have no competing interests. may be useful to consider prophylactic steps to alleviate the symptoms through use of medication or behavioral Authors’ contributions MT was involved in the concept, design, data acquisition, analyses and approaches, parallel to the approach used to manage interpretation of data, manuscript draft preparation, and revisions for critical gynecological symptoms during menses (e.g., analgesic content. LG was involved in the concept, design, analyses and interpretation medication for dysmenorrhea). of data, manuscript draft and revisions for critical content. LA was involved in the concept, design, data acquisition, manuscript draft preparation and There are limitations to the study. It was exploratory revisions for critical content. CP was involved in the data acquisition, analyses in nature, aiming to assess the presence of GI and emo- and interpretation of data, manuscript draft preparation and revisions for critical tional symptoms perimenstrually using participant obser- content. KP was involved in the data acquisition, manuscript draft preparation and revisions for critical content. LT was involved in the analyses and vation, with minimal participant burden. There were no interpretation of data, manuscript draft and revisions for critical content. All validated scales that included all the symptoms of interest, authors read and approved the final manuscript. so a brief history and symptom measure was developed for the study. This had the benefit of assessing the variables of Acknowledgements There were no external funds used to support this study. interest using the same response scale, for ready compari- son. However, the validity of the symptom measure was Author details not established, and further, the duration and severity of Department of Internal Medicine, University of Manitoba, Winnipeg, Canada. Department of Clinical Health Psychology, Faculty of Medicine, University of symptoms could not be determined as the measure simply Manitoba, PZ350 - 771 Bannatyne Avenue, Winnipeg, MB R3E 3N4, Canada. assessed presence/absence of symptoms. Subsequent inves- Department of Obstetrics and Gynecology, University of Manitoba, tigation of potentially relevant variables identified in this Winnipeg, Canada. preliminary study, such as depression, anxiety, and pain, Received: 31 January 2013 Accepted: 21 January 2014 should include validated measures. Second, participants Published: 22 January 2014 reported their perimenstrual symptoms retrospectively, which increases the likelihood of recall bias. Neverthe- References 1. 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Expert Rev Pharmacoecon Outcomes Res 2004, 4(2):159–163. doi:10.1186/1472-6874-14-14 Cite this article as: Bernstein et al.: Gastrointestinal symptoms before and during menses in healthy women. BMC Women's Health 2014 14:14. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit

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