GASTROENTEROLOGY
1990;98:1485-1489
Evidence for Exacerbation of Irritable Bowel Syndrome During Menses WILLIAM E. WHITEHEAD, LAWRENCE J. CHESKIN, BARBARA R. HELLER, J. COURTLAND ROBINSON, MICHAEL D. CROWELL, CAROL BENJAMIN, and MARVIN M. SCHUSTER Departments of Medicine and Psychiatry, The Johns Hopkins University and the Francis Scott Key Medical Center, Baltimore, Maryland
Many women report that bowel symptoms are associated with menstruation, but neither the prevalence of these complaints nor their physiological basis is known. This study aimed to estimate prevalence, to determine whether patients with irritable bowel syndrome are more likely to make such complaints, and to determine whether bowel complaints during menstruation are attributable to psychological traits such as increased somatization. To estimate prevalence, 369 clients of Planned Parenthood of Maryland were asked whether gas, diarrhea, or constipation occurred during menstruation. These subjects were compared with women referred to a gastroenterology clinic and found to have irritable bowel syndrome or functional bowel disorder (abdominal pain plus altered bowel habits but not satisfying restrictive criteria for irritable bowel syndrome). Thirty-four percent of 233 Planned Parenthood clients who denied symptoms of irritable bowel syndrome or functional bowel disorder reported that menstruation was associated with one or more bowel symptoms. Gastroenterology clinic patients with irritable bowel syndrome were significantly more likely to experience exacerbations of each of these bowel symptoms, but especially increased bowel gas. Selfreports of bowel symptoms during menstruation were not associated with psychological traits or with menses-related changes in affect.
G
astrointestinal symptoms, including diarrhea and constipation, are well-established events associated with the menstrual cycle. Loose or more frequent stools occur with the onset of menstrual flow (l-3), and constipation may occur during the luteal phase (4), although this is not consistently reported (2,3,5). Estimates of the prevalence of these menses-related
School of Medicine,
changes in bowel function vary from 65%-9670, but these estimates are based on small, selected samples. The physiological basis for these bowel symptoms has not been established. With a few exceptions (4,6), controlled studies have failed to show a difference in mouth-to-cecum transit time ($5) or whole-gut transit time (l&5) between the luteal and the folicular phases of the cycle, ruling out progesterone as a cause of menses-related bowel symptoms. The most dramatic changes in bowel symptoms occur during the first day of menses when there are elevated levels of prostaglandins E, and F,, in menstrual fluid, and it has been suggested that these bowel symptoms may be mediated by prostaglandins (1,3). These substances are known to be powerful stimulants of contractile activity in the colon (7). However, prostaglandins are rapidly metabolized, and it is not know whether prostaglandins released in the uterus are carried by the circulation to adjacent gastrointestinal smooth muscle in sufficient quantities to stimulate contractions of the colon. Previous studies suggest that in patients with irritable bowel syndrome (IBS), the colon is hyperreactive to a variety of stimuli including mechanical distension of the bowel with a balloon (81, food stimulation (91, and emotional arousal (10). Patients with IBS might also show an exaggerated colon motility response to prostaglandins or other substances released during menstruation. The purposes of this study were [a] to obtain reliable estimates of the frequency with which women report
Abbreviations used in this paper: FBD, functional bowel disorder; IBS, irritable bowe1 syndrome; MDQ, Menstrual Distress Questionnaire; MANOVA, multivariate analysis of variance. E 1990 by the American Gastroenterological Association 0018-5085/90/$3.00
1486
WHITEHEAD ET AL.
GASTROENTEROLOGY
bowel symptoms during menses, (b) to determine whether women with IBS report exacerbation of bowel symptoms more frequently during menses than women without IBS, and (c) to determine whether the tendency to report menses-related exacerbation of bowel symptoms is caused by a neurotic tendency to overreport caused by somatic symptoms or by mood swings occurring during the menstrual cycle. Materials
and Methods
Subjects Two populations were sampled. The first group were clients attending the Planned Parenthood of Maryland clinics for contraceptive and general gynecology care. Over a 12-mo period, 369 nonpregnant women aged 20-40 yr agreed to complete a set of questionnaires for payment of $20. Demographic characteristics are given in Table 1. This study was reviewed and approved by the Committee for the Protection of Human Subjects of the Francis Scott Key Medical Center. To obtain a sample of women with IBS who were well-screened medically, consecutive women aged 18-40 yr who were referred to the division of digestive diseases at Francis Scott Key Medical Center were tested. A gastroenterologist evaluated these women by clinical history, physical examination, and laboratory tests as appropriate to their presenting complaints. Testing included a rectal examination, colon motility test, colonoscopy if not performed within 3 yr, and, when clinically indicated, a lactose tolerance test and test of stools for parasites. Women in the medical clinic who had no evidence of other disease were diagnosed as having IBS if they reported abdominal pain that was relieved by defecation and at least 2 of the following symptoms: looser stools with onset of pain, more frequent stools with onset of pain, abdominal distension, passage of mucus by rectum, and feeling of incomplete evacuation (11). Medical clinic patients were diagnosed as having functional bowel disorder (FBD) if they had negative medical evaluations and reported symptoms of abdominal pain plus constipation or diarrhea but did not satisfy the criteria for IBS given above. These diagnostic criteria for FBD are the criteria used in many clinics to diagnose IBS; we sought to compare patients meeting these inclusive criteria with patients meeting restrictive diagnostic criteria that identify a more homogeneous group of patients with IBS (12). Fifty-three women with IBS and 117 with FBD were studied; their demographic characteristics are given in Table I(
Table 1. Demographic
Characteristics
Planned Parenthood
Average age (yr] Age range (yr) Race (% block) % Married No. of subjects
of Subjects Gastroenterology clinic
Control
FBD
IBS
FBD
IBS
25.70 19-40 27 17 234
26.1 20-38 24 20 105
27.5 20-39 16 20 30
30.7 19-39 0 60 101
30.7 19-40 5 68 42
Vol. 98, No. 6
Gastroenterology clinic patients were screened to identify those who reported having undergone hysterectomies, and these women were eliminated from subsequent statistical analyses. Interestingly, 21% of IBS patients and 14% of FBD patients aged 18-40 yr had undergone hysterectomies. This is significantly higher than the national average of 5.5% (13). Women in the Planned Parenthood sample were also screened by a questionnaire to identify those who met bowel symptom criteria for the diagnosis of IBS or FBD. However, since these women were not screened medically, it is not possible to rule out other gastrointestinal disorders as accounting for their bowel symptoms. Planned Parenthood clients who denied having bowel symptoms formed the control group.
Procedures A bowel symptom questionnaire was designed that included the question, “Do your bowel symptoms change during your menses?” and provided places for the subject to check “constipation better,” “constipation worse,” “diarrhea better, ” “diarrhea worse, ” “flatus decreased,” and “flatus increased.” Subjects were instructed to check all items that applied. Subjects in both samples completed the same questionnaire. Subjects in the Planned Parenthood sample were asked to complete the NE0 Personality Inventory (14) to determine whether subjects who reported that bowel symptoms were exacerbated by menses were psychologically different from those who did not. The NE0 Personality Inventory is a 181-item questionnaire which is scored for 5 personality dimensions: neuroticism, extraversion, openness, agreeableness, and conscientiousness. The neuroticism domain is composed of 6 separate scales: anxiety, hostility, depression, self-consciousness, impulsiveness, and vulnerability. The last 38 patients from the gastroenterology clinic who met the criteria for IBS or FBD were also given the Hopkins Symptom Checklist (15) for the purpose of comparing psychological characteristics of patients who reported a mensesrelated exacerbation of bowel symptoms with those who did not. Except for being the last patients studied, patients undergoing psychometric testing in the medical clinic were unselected, and they are believed to be representative of the total pool of gastroenterology clinic patients with IBS or FBD. Variations in mood that may occur during the menstrual cycle (e.g., irritability) could account for reports that bowel symptoms are exacerbated during menses by predisposing women to be more observant or less tolerant of chronic bowel symptoms during menstruation. To test this, the Moos Menstrual Distress Questionnaire (MDQ) (16) was administered to women in the Planned Parenthood sample on a separate visit 3 mo after they completed the other questionnaires. The MDQ consists of 45 symptoms, the severity of which women are asked to rate during three phases of their most recent menstrual cycle: during the most recent flow, 4 days before, and during the remainder of the cycle. The 45 symptoms are grouped into 8 scales, but only 6 of these scales-pain, water retention, autonomic reactions, negative affect, concentration, and behavior change-show reliable covariation with the phase of the menstrual cycle. Two of
BOWEL SYMPTOMS DURING MENSES
)une 1990
Table 2. Effects
of Menstruation
on Bowel Symptoms
Planned Parenthood Control (7.1 Gas increased Gas decreased Diarrhea increased Diarrhea decreased Constipation increased Constipation decreased Anv GI svmutoms increased
14 2 19 1 11 16 34
scale. A a-factor MANOVA was then performed in which diagnostic groups (IBS vs. FBD vs. controls) and mensesrelated exacerbation formed the factors and the two MDQ change scores were dependent variables.
Gastroenterology clinic
FBD IBS (70) (70) 22” 2 38” 0 21” 18 48’
39” 11 32” 7 18” 36” 50”
FBD (701
IBS (701
26” 3 15 0 13 19 43”
48” 2 29” 2 24’ IO 47”
Results
“Significantly different from control (p < 0.05).
these scales-negative affect and behavioral change-are relevant to the question of whether hormonally mediated mood swings explain reports that bowel symptoms are exacerbated during menses.
Data Analysis Differences between groups in the proportion who reported exacerbation of their bowel symptoms during menses were tested for significance of differences between proportions (17). Multivariate analysis of variance (MANOVA) was used to compare women who reported menses-related exacerbation of bowel symptoms with those who did not with respect to psychological characteristics. For the Planned Parenthood sample, a Z-factor MANOVA was used in which diagnostic group (IBS vs. FBD vs. controls) was one factor, menstrual exacerbation was a scales of the NE0 second factor, and the 6 neuroticism Personality Inventory were the dependent measures. For the gastroenterology clinic sample, a Z-factor MANOVA was used in which diagnostic group (IBS vs. FBD) and menses-related exacerbation were factors and in which the 9 scales of the Hopkins Symptom Checklist were dependent measures. To determine whether changes in affect or behavior occurring within the menstrual cycle were related to report:3 of bowel symptom exacerbation, we first calculated the difference in the MDQ negative affect scores for the menstrual phase and the remainder of the cycle and computed a similar change score for the MDQ behavior change Table 3. Psychological
Symptoms
in Planned
Parenthood
Thirty-four percent of Planned Parenthood subjects who denied symptoms of IBS or FBD reported that menstruation caused at least one bowel symptom. Table 2 gives the frequency with which individual bowel symptoms were reported. IBS patients from the gastroenterology clinic were significantly more likely than controls to report mensesrelated worsening of each bowel symptom on the questionnaire, but increased bowel gas was the symptom that most clearly distinguished them from controls. Patients with FBD from the gastroenterology clinic were similar to controls except that they reported significantly more gas during menses. Subjects in the Planned Parenthood sample who reported bowel symptoms consistent with IBS and FBD were also evaluated to determine whether differences between gastroenterology clinic patients and controls could be replicated. As shown in Table 2, the proportion of Planned Parenthood subjects with IBS who reported exacerbation of gas, diarrhea, and constipation during menstruation was similar to the gastroenterology clinic sample. Unlike the gastroenterology clinic sample, however, a higher proportion of FBD subjects than controls from the Planned Parenthood sample reported menses-related exacerbation of diarrhea and constipation. Exacerbation of bowel symptoms during menstruation was unrelated to psychological test scores. The MANOVA analysis of the NE0 Personality Inventory data in the Planned Parenthood sample showed that the main effect for exacerbation of bowel symptoms was not statistically significant [F(6,358) = 1.33, p = 0.241. The se d a t a are shown in Table 3. Similarly, the MANOVA analysis of the Hopkins Symptom
Sample
[Mean
Anxiety Hostility Depression Self-Conscious Impulsiveness Vulnerability Neuroticism Extraversion Openness Conscientious Agreeableness
Exacerbated 16.23 + 5.41 12.69 f 4.85 14.31 + 6.18 15.50 + 4.54 18.45 + 4.52 11.28 + 4.30 88.45 + 22.84 115.59 + 16.47 122.43 + 19.30 46.70 + 8.56 47.96 % 7.32
Not exacerbated 16.08 zk4.90 13.18 -r-4.98 13.79 * 5.73 14.66 k 4.55 17.53 + 4.07 11.19 + 4.12 86.44 k 21.49 115.28 + 17.19 120.89 + 18.62 48.64 + 8.51 46.25 + 6.35
+ SD)
FBD
Controls Psychological scale
1487
Exacerbated 19.38 k 4.26 13.93 t 5.92 17.13 f 6.01 16.38 k 4.46 19.45 2 4.65 13.53 * 4.59 99.80 + 21.95 113.07 * 19.43 126.13 t 16.93 45.31 t 9.92 45.95 + 7.98
IBS
Not exacerbated 18.10 5 4.98 14.30 + 4.11 15.98 k 5.42 16.18 k 3.62 18.40 i- 4.41 12.52 +-3.63 95.48 k 18.78 116.20 k 18.33 125.72 f 20.95 46.58 t 7.61 46.84 zk6.08
Exacerbated 19.20 + 6.49 14.33 k 4.85 16.00 + 7.38 15.60 k 5.10 17.67 * 4.95 13.60 + 5.10 96.40 + 25.34 117.60 k 16.73 122.33 k 15.10 49.40 + 7.80 47.40 + 7.88
Not exacerbated 15.93 k 4.48 12.07 + 6.55 13.67 + 6.01 12.60 + 5.03 17.60 + 3.74 10.20 + 2.70 82.07 k 20.31 120.20 k 20.06 125.20 + 16.96 46.80 k 10.07 49.60 f 9.12
1488
WHITEHEAD
ET AL.
GASTROENTEROLOGY
Table 4. Psychological Symptoms in Gastroenterology
Clinic Sample [Mean f SD) IBS
FBD
Psychological scale
Not exacerbated
Exacerbated
Somatization Obsessive/Compulsive Interpersonal sensitivity Depression Anxiety Hostility Phobia Paranoia Psychoticism Global Symptom Index
0.81 + 0.66 0.62 zt0.64 0.72 + 0.76 1.10 * 1.18 0.59 k 0.64 0.40 + 0.42 0.43 f 1.08 0.48 k 0.45 0.34 + 0.49 0.69 + 0.65
Discussion Thirty-four percent of women who deny chronic bowel symptoms report that the onset of menstruation is associated with a change in bowel habits: either increased diarrhea (19%), increased gas (14%j, or increased constipation (11%). These estimates differ from the 64% of 67 women studied by Rees and
Menstrual Distress Questionnaire scales” Negative affect Behavior change Pain Water retention Arousal Concentration
Symptoms
in Planned
Parenthood
3.24 1.72 3.24 2.34 0.43 1.54
+ k k + + *
5.34 2.98 3.59 2.83 1.17 3.93
Not exacerbated
1.11 + 0.63 1.09 * 0.43 1.10 + 0.54 1.44 * 0.44 1.14 k 0.62 0.73 + 0.29 0.19 -t 0.24 0.56 t 0.39 0.26 +- 0.25 0.95 * 0.31
0.97 t 1.07 k 0.80 k 1.36 + 0.96 k 0.50 t 0.63 k 0.52 k 0.41 + 0.88 +
Sample (Mean -+ SD) FBD
Not exacerbated 2.47 0.81 2.44 1.86 0.27 0.86
k k t + k f
4.77 2.43 3.74 2.81 0.95 2.31
0.81 0.84 0.65 0.97 0.86 0.55 1.04 0.64 0.39 0.65
Rhodes (4) who reported a change in bowel habits with menses and the 96% of 25 women studied by Hinds et al. (1). These differences may be attributable to the study of unrepresentative samples by previous investigators. A higher proportion of women with IBS report a worsening of bowel symptoms during menstruation as compared to women without chronic bowel symptoms. These differences cannot be explained by a neurotic tendency to overreport symptoms because women who reported menses-related worsening of bowel symptoms were not different psychologically from women who denied these symptoms. These differences also cannot be attributed to changes in affect or behavior within the menstrual cycle that might lead women to be more aware of and less tolerant of bowel symptoms because changes in affect and behavior during the cycle were not associated with a greater tendency to report worsening of bowel symptoms during menstruation. We infer that these differences have a physiological basis and are a reflection of the hyperreactivity of colonic smooth muscle in IBS to a variety of stimuli (18). The greater prevalence of hysterectomy among women with IBS and FBD than among controls confirms previous findings (19,20]. Because we know of no reason to expect an excess incidence of pelvic disease
Controls Exacerbated
Exacerbated
1.01 + 0.87 0.76 + 0.70 0.80 t 0.60 1.03 + 0.81 0.52 _t0.56 0.68 * 0.79 0.29 + 0.53 0.64 -t 0.96 0.26 t 0.47 0.74 f 0.61
Checklist scores in the gastroenterology clinic sample showed that the main effect for exacerbation of bowel symptoms was not statistically significant [F(10,25) = 0.44, p = 0.911. These data are shown in Table 4. Variations in negative affect and behavior occurring within the menstrual cycle were similarly unrelated to reports that bowel symptoms were exacerbated during menses [Table 5). The MANOVA analysis showed that the main effect for exacerbation of bowel symptoms was not statistically significant [F(2,339) = 1.29, p = 0.281. Tab1 e 5 a 1so shows the relationship of other MDQ change scores to exacerbation of bowel symptoms during menses. Although not directly related to this study, it is interesting to note that women with IBS and FBD were significantly more likely to report increased pain during menstruation as compared to normal controls [univariate F(2,340) = 7.00, p < 0.011.
Table 5. Menstrual
Vol. 98. No. 6
Exacerbated 4.76 1.63 4.52 2.78 0.76 1.31
+ + + * + +
5.99 2.89 3.55 2.91 1.79 2.41
IBS
Not exacerbated 3.29 1.12 3.45 2.90 0.55 0.52
+ + * + * +
4.82 2.50 4.13 2.43 1.17 1.98
Exacerbated 3.44 2.32 5.28 2.96 0.92 2.00
* k k + 2 +
4.38 3.86 4.14 3.10 2.31 3.18
Not exacerbated 5.64 1.91 5.18 3.27 0.64 1.18
+ + k * + k
4.01 2.21 3.49” 2.00b 1.57 1.83
“The Moos (1985) Menstrual Distress Questionnaire was scarred by subtracting the symptom severity during the luteal phase of the menstrual cycle from the symptom severity during menstrual flow. bUnivariate analyses of variance showed that normal subjects reported significantly less menses-related pain and water retention than IBS patients. No other contrasts were statistically significant.
BOWEL SYMPTOMS DURING MENSES
June 19910
in wornen with IBS, these operations were probably performed as an empirical attempt to correct abdominopelvic pain. This interpretation is supported by a recent study (21) showing that many women with symptoms of IBS consult gynecologists rather than gastroenterologists and that few of them receive firm gynecologic diagnoses. Thus the presence of symptoms of IBS or FBD and their relation to menstruation may ble important in assessing patients’ need for and likely Iresponse to hysterectomy. Additional research is needed to compare colonic motility during the first day of menstruation with colonifc motility at other times and to correlate colonic motility and bowel symptoms to circulating levels of prostaglandins. Whether prostaglandin antagonists would be useful in IBS patients with menstrual exacerbation remains to be determined. References
10.
11.
12.
13.
14.
15.
16.
I. Hinds JP. Stoney B, Wald A. Doesgender or the menstrual cycle affect colonic transit? Am J Gastroenterol1989;84:123-126. 2. Heitkemper MM, Shaver JF, Mitchell ES. Gastrointestinal symptoms and bowel patterns across the menstrual cycle in dysmenorrhea. Nurs Res 1988;37:108-113. 3. Turnbull GK, Thompson DG. Day S, Martin J, Walker E, Lennard-Jones JE. Relationship between symptoms, menstrual cycle and orocaecal transit in normal and constipated women. Gut 1989;30:30-34. 4. Reas WDW, Rhodes JWT. Altered bowel habit and menstruation. Lancet 1976;2:475. 5. Kamm MA, Farthing MJG, Lennard-Jones JE. Bowel function and transit rate during the menstrual cycle. Gut 1989;30:605-608. 6. Wald A, VanThiel DH, Hoechstetter L, Gavaler JS, Egler KM, Verm R, Scott L, Lester R. Gastrointestinal transit: the effect of the menstrual cycle. Gastroenterology 1981;80:1497-1500. 7. Bennett A. Effects of prostaglandins on the gastrointestinal tract. In Karim SM. ed. The prostaglandins. Progress in research. New York: Wiley Interscience. 1972:205-221. 8. Whitehead WE, Engel BT. Schuster MM. Irritable bowel syndralme. Physiological and psychological differences between diarrhea-predominant and constipation-predominant patients. Dig Dis Sci 1980;25:404-413. 9. Sullivan MA, Cohen S, Snape WJ Jr. Colonic myoelectrical
17. 18.
19.
20. 21.
1489
activity in irritable-bowel syndrome. Effect of eating and anticholinergics. N Engl J Med 1978;298:878-883. Welgan P, Meshkinpour H, Beeler M. Effect of anger on colon motor and myoelectric activity in irritable bowel syndrome. Gastroenterology 1988;94:1150-1156. Manning AP, Thompson WG, Heaton KW, Morris AF. Towards a positive diagnosis of the irritable bowel. Br Med J 1978;2:653654. Whitehead WE, Bosmajian L, Zonderman AB, Costa PT Jr, Schuster MM. Symptoms of psychologic distress associated with irritable bowel syndrome. Comparison of community and medical clinic samples. Gastroenterology 1988;95:709-714. Nolan TF, Dry HW. Layde PM, Hughes JM, Greenspan JR. Cumulative prevalence rates and corrected incidence rates of surgical sterilization among women in the United States, 19711978. Am J Epidemiol1982;116:776-781. Costa PT Jr, McCrae RR. The NE0 Personality Inventory Manual. Odessa, Fla.: Psychological Assessment Resources, 1985. Derogatis LI. The SCL-90-R. Administration, scoring, and procedures manual, II. Towson, Md.: Clinical Psychometric Research, 1983. Moos RH. Perimenstrual symptoms: a manual and overview of research with the Menstrual Distress Questionnaire. Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Palo Alto, Calif. Bruning JL, Kintz BL. Computational handbook of statistics. Glenview, 111.:Scott Foresman, 1968. Whitehead WE, Schuster MM. Gastrointestinal disorders: behavioral and physiological basis for treatment. San Diego: Academic, 1985:155-177. Chaudhary NA, Truelove SC. The irritable colon syndrome: a study of the clinical features, predisposing causes, and prognosis in 130 cases. Q J Med 1962;31:307-323, Keeling PWN, Fielding JR. The irritable bowel syndrome: a review of 50 consecutive cases. J Ir Call Phys Surg 1975:4:91-94. Prior A, Whorwell PJ. Gynaecological consultation in patients with the irritable bowel syndrome. Gut 1989;30:996-998.
Received August 7,1989. Accepted November 21,1989. Address requests for reprints to: William E. Whitehead, Ph.D., Division of Digestive Diseases, Francis Scott Key Medical Center, 4940 Eastern Avenue, Baltimore, Maryland 21224. Supported in part by Grants ROI NR01369 from the Center for Nursing Research and K05 MHOO133from the National Institute of Mental Health.
1990;98:1485-1489
Evidence for Exacerbation of Irritable Bowel Syndrome During Menses WILLIAM E. WHITEHEAD, LAWRENCE J. CHESKIN, BARBARA R. HELLER, J. COURTLAND ROBINSON, MICHAEL D. CROWELL, CAROL BENJAMIN, and MARVIN M. SCHUSTER Departments of Medicine and Psychiatry, The Johns Hopkins University and the Francis Scott Key Medical Center, Baltimore, Maryland
Many women report that bowel symptoms are associated with menstruation, but neither the prevalence of these complaints nor their physiological basis is known. This study aimed to estimate prevalence, to determine whether patients with irritable bowel syndrome are more likely to make such complaints, and to determine whether bowel complaints during menstruation are attributable to psychological traits such as increased somatization. To estimate prevalence, 369 clients of Planned Parenthood of Maryland were asked whether gas, diarrhea, or constipation occurred during menstruation. These subjects were compared with women referred to a gastroenterology clinic and found to have irritable bowel syndrome or functional bowel disorder (abdominal pain plus altered bowel habits but not satisfying restrictive criteria for irritable bowel syndrome). Thirty-four percent of 233 Planned Parenthood clients who denied symptoms of irritable bowel syndrome or functional bowel disorder reported that menstruation was associated with one or more bowel symptoms. Gastroenterology clinic patients with irritable bowel syndrome were significantly more likely to experience exacerbations of each of these bowel symptoms, but especially increased bowel gas. Selfreports of bowel symptoms during menstruation were not associated with psychological traits or with menses-related changes in affect.
G
astrointestinal symptoms, including diarrhea and constipation, are well-established events associated with the menstrual cycle. Loose or more frequent stools occur with the onset of menstrual flow (l-3), and constipation may occur during the luteal phase (4), although this is not consistently reported (2,3,5). Estimates of the prevalence of these menses-related
School of Medicine,
changes in bowel function vary from 65%-9670, but these estimates are based on small, selected samples. The physiological basis for these bowel symptoms has not been established. With a few exceptions (4,6), controlled studies have failed to show a difference in mouth-to-cecum transit time ($5) or whole-gut transit time (l&5) between the luteal and the folicular phases of the cycle, ruling out progesterone as a cause of menses-related bowel symptoms. The most dramatic changes in bowel symptoms occur during the first day of menses when there are elevated levels of prostaglandins E, and F,, in menstrual fluid, and it has been suggested that these bowel symptoms may be mediated by prostaglandins (1,3). These substances are known to be powerful stimulants of contractile activity in the colon (7). However, prostaglandins are rapidly metabolized, and it is not know whether prostaglandins released in the uterus are carried by the circulation to adjacent gastrointestinal smooth muscle in sufficient quantities to stimulate contractions of the colon. Previous studies suggest that in patients with irritable bowel syndrome (IBS), the colon is hyperreactive to a variety of stimuli including mechanical distension of the bowel with a balloon (81, food stimulation (91, and emotional arousal (10). Patients with IBS might also show an exaggerated colon motility response to prostaglandins or other substances released during menstruation. The purposes of this study were [a] to obtain reliable estimates of the frequency with which women report
Abbreviations used in this paper: FBD, functional bowel disorder; IBS, irritable bowe1 syndrome; MDQ, Menstrual Distress Questionnaire; MANOVA, multivariate analysis of variance. E 1990 by the American Gastroenterological Association 0018-5085/90/$3.00
1486
WHITEHEAD ET AL.
GASTROENTEROLOGY
bowel symptoms during menses, (b) to determine whether women with IBS report exacerbation of bowel symptoms more frequently during menses than women without IBS, and (c) to determine whether the tendency to report menses-related exacerbation of bowel symptoms is caused by a neurotic tendency to overreport caused by somatic symptoms or by mood swings occurring during the menstrual cycle. Materials
and Methods
Subjects Two populations were sampled. The first group were clients attending the Planned Parenthood of Maryland clinics for contraceptive and general gynecology care. Over a 12-mo period, 369 nonpregnant women aged 20-40 yr agreed to complete a set of questionnaires for payment of $20. Demographic characteristics are given in Table 1. This study was reviewed and approved by the Committee for the Protection of Human Subjects of the Francis Scott Key Medical Center. To obtain a sample of women with IBS who were well-screened medically, consecutive women aged 18-40 yr who were referred to the division of digestive diseases at Francis Scott Key Medical Center were tested. A gastroenterologist evaluated these women by clinical history, physical examination, and laboratory tests as appropriate to their presenting complaints. Testing included a rectal examination, colon motility test, colonoscopy if not performed within 3 yr, and, when clinically indicated, a lactose tolerance test and test of stools for parasites. Women in the medical clinic who had no evidence of other disease were diagnosed as having IBS if they reported abdominal pain that was relieved by defecation and at least 2 of the following symptoms: looser stools with onset of pain, more frequent stools with onset of pain, abdominal distension, passage of mucus by rectum, and feeling of incomplete evacuation (11). Medical clinic patients were diagnosed as having functional bowel disorder (FBD) if they had negative medical evaluations and reported symptoms of abdominal pain plus constipation or diarrhea but did not satisfy the criteria for IBS given above. These diagnostic criteria for FBD are the criteria used in many clinics to diagnose IBS; we sought to compare patients meeting these inclusive criteria with patients meeting restrictive diagnostic criteria that identify a more homogeneous group of patients with IBS (12). Fifty-three women with IBS and 117 with FBD were studied; their demographic characteristics are given in Table I(
Table 1. Demographic
Characteristics
Planned Parenthood
Average age (yr] Age range (yr) Race (% block) % Married No. of subjects
of Subjects Gastroenterology clinic
Control
FBD
IBS
FBD
IBS
25.70 19-40 27 17 234
26.1 20-38 24 20 105
27.5 20-39 16 20 30
30.7 19-39 0 60 101
30.7 19-40 5 68 42
Vol. 98, No. 6
Gastroenterology clinic patients were screened to identify those who reported having undergone hysterectomies, and these women were eliminated from subsequent statistical analyses. Interestingly, 21% of IBS patients and 14% of FBD patients aged 18-40 yr had undergone hysterectomies. This is significantly higher than the national average of 5.5% (13). Women in the Planned Parenthood sample were also screened by a questionnaire to identify those who met bowel symptom criteria for the diagnosis of IBS or FBD. However, since these women were not screened medically, it is not possible to rule out other gastrointestinal disorders as accounting for their bowel symptoms. Planned Parenthood clients who denied having bowel symptoms formed the control group.
Procedures A bowel symptom questionnaire was designed that included the question, “Do your bowel symptoms change during your menses?” and provided places for the subject to check “constipation better,” “constipation worse,” “diarrhea better, ” “diarrhea worse, ” “flatus decreased,” and “flatus increased.” Subjects were instructed to check all items that applied. Subjects in both samples completed the same questionnaire. Subjects in the Planned Parenthood sample were asked to complete the NE0 Personality Inventory (14) to determine whether subjects who reported that bowel symptoms were exacerbated by menses were psychologically different from those who did not. The NE0 Personality Inventory is a 181-item questionnaire which is scored for 5 personality dimensions: neuroticism, extraversion, openness, agreeableness, and conscientiousness. The neuroticism domain is composed of 6 separate scales: anxiety, hostility, depression, self-consciousness, impulsiveness, and vulnerability. The last 38 patients from the gastroenterology clinic who met the criteria for IBS or FBD were also given the Hopkins Symptom Checklist (15) for the purpose of comparing psychological characteristics of patients who reported a mensesrelated exacerbation of bowel symptoms with those who did not. Except for being the last patients studied, patients undergoing psychometric testing in the medical clinic were unselected, and they are believed to be representative of the total pool of gastroenterology clinic patients with IBS or FBD. Variations in mood that may occur during the menstrual cycle (e.g., irritability) could account for reports that bowel symptoms are exacerbated during menses by predisposing women to be more observant or less tolerant of chronic bowel symptoms during menstruation. To test this, the Moos Menstrual Distress Questionnaire (MDQ) (16) was administered to women in the Planned Parenthood sample on a separate visit 3 mo after they completed the other questionnaires. The MDQ consists of 45 symptoms, the severity of which women are asked to rate during three phases of their most recent menstrual cycle: during the most recent flow, 4 days before, and during the remainder of the cycle. The 45 symptoms are grouped into 8 scales, but only 6 of these scales-pain, water retention, autonomic reactions, negative affect, concentration, and behavior change-show reliable covariation with the phase of the menstrual cycle. Two of
BOWEL SYMPTOMS DURING MENSES
)une 1990
Table 2. Effects
of Menstruation
on Bowel Symptoms
Planned Parenthood Control (7.1 Gas increased Gas decreased Diarrhea increased Diarrhea decreased Constipation increased Constipation decreased Anv GI svmutoms increased
14 2 19 1 11 16 34
scale. A a-factor MANOVA was then performed in which diagnostic groups (IBS vs. FBD vs. controls) and mensesrelated exacerbation formed the factors and the two MDQ change scores were dependent variables.
Gastroenterology clinic
FBD IBS (70) (70) 22” 2 38” 0 21” 18 48’
39” 11 32” 7 18” 36” 50”
FBD (701
IBS (701
26” 3 15 0 13 19 43”
48” 2 29” 2 24’ IO 47”
Results
“Significantly different from control (p < 0.05).
these scales-negative affect and behavioral change-are relevant to the question of whether hormonally mediated mood swings explain reports that bowel symptoms are exacerbated during menses.
Data Analysis Differences between groups in the proportion who reported exacerbation of their bowel symptoms during menses were tested for significance of differences between proportions (17). Multivariate analysis of variance (MANOVA) was used to compare women who reported menses-related exacerbation of bowel symptoms with those who did not with respect to psychological characteristics. For the Planned Parenthood sample, a Z-factor MANOVA was used in which diagnostic group (IBS vs. FBD vs. controls) was one factor, menstrual exacerbation was a scales of the NE0 second factor, and the 6 neuroticism Personality Inventory were the dependent measures. For the gastroenterology clinic sample, a Z-factor MANOVA was used in which diagnostic group (IBS vs. FBD) and menses-related exacerbation were factors and in which the 9 scales of the Hopkins Symptom Checklist were dependent measures. To determine whether changes in affect or behavior occurring within the menstrual cycle were related to report:3 of bowel symptom exacerbation, we first calculated the difference in the MDQ negative affect scores for the menstrual phase and the remainder of the cycle and computed a similar change score for the MDQ behavior change Table 3. Psychological
Symptoms
in Planned
Parenthood
Thirty-four percent of Planned Parenthood subjects who denied symptoms of IBS or FBD reported that menstruation caused at least one bowel symptom. Table 2 gives the frequency with which individual bowel symptoms were reported. IBS patients from the gastroenterology clinic were significantly more likely than controls to report mensesrelated worsening of each bowel symptom on the questionnaire, but increased bowel gas was the symptom that most clearly distinguished them from controls. Patients with FBD from the gastroenterology clinic were similar to controls except that they reported significantly more gas during menses. Subjects in the Planned Parenthood sample who reported bowel symptoms consistent with IBS and FBD were also evaluated to determine whether differences between gastroenterology clinic patients and controls could be replicated. As shown in Table 2, the proportion of Planned Parenthood subjects with IBS who reported exacerbation of gas, diarrhea, and constipation during menstruation was similar to the gastroenterology clinic sample. Unlike the gastroenterology clinic sample, however, a higher proportion of FBD subjects than controls from the Planned Parenthood sample reported menses-related exacerbation of diarrhea and constipation. Exacerbation of bowel symptoms during menstruation was unrelated to psychological test scores. The MANOVA analysis of the NE0 Personality Inventory data in the Planned Parenthood sample showed that the main effect for exacerbation of bowel symptoms was not statistically significant [F(6,358) = 1.33, p = 0.241. The se d a t a are shown in Table 3. Similarly, the MANOVA analysis of the Hopkins Symptom
Sample
[Mean
Anxiety Hostility Depression Self-Conscious Impulsiveness Vulnerability Neuroticism Extraversion Openness Conscientious Agreeableness
Exacerbated 16.23 + 5.41 12.69 f 4.85 14.31 + 6.18 15.50 + 4.54 18.45 + 4.52 11.28 + 4.30 88.45 + 22.84 115.59 + 16.47 122.43 + 19.30 46.70 + 8.56 47.96 % 7.32
Not exacerbated 16.08 zk4.90 13.18 -r-4.98 13.79 * 5.73 14.66 k 4.55 17.53 + 4.07 11.19 + 4.12 86.44 k 21.49 115.28 + 17.19 120.89 + 18.62 48.64 + 8.51 46.25 + 6.35
+ SD)
FBD
Controls Psychological scale
1487
Exacerbated 19.38 k 4.26 13.93 t 5.92 17.13 f 6.01 16.38 k 4.46 19.45 2 4.65 13.53 * 4.59 99.80 + 21.95 113.07 * 19.43 126.13 t 16.93 45.31 t 9.92 45.95 + 7.98
IBS
Not exacerbated 18.10 5 4.98 14.30 + 4.11 15.98 k 5.42 16.18 k 3.62 18.40 i- 4.41 12.52 +-3.63 95.48 k 18.78 116.20 k 18.33 125.72 f 20.95 46.58 t 7.61 46.84 zk6.08
Exacerbated 19.20 + 6.49 14.33 k 4.85 16.00 + 7.38 15.60 k 5.10 17.67 * 4.95 13.60 + 5.10 96.40 + 25.34 117.60 k 16.73 122.33 k 15.10 49.40 + 7.80 47.40 + 7.88
Not exacerbated 15.93 k 4.48 12.07 + 6.55 13.67 + 6.01 12.60 + 5.03 17.60 + 3.74 10.20 + 2.70 82.07 k 20.31 120.20 k 20.06 125.20 + 16.96 46.80 k 10.07 49.60 f 9.12
1488
WHITEHEAD
ET AL.
GASTROENTEROLOGY
Table 4. Psychological Symptoms in Gastroenterology
Clinic Sample [Mean f SD) IBS
FBD
Psychological scale
Not exacerbated
Exacerbated
Somatization Obsessive/Compulsive Interpersonal sensitivity Depression Anxiety Hostility Phobia Paranoia Psychoticism Global Symptom Index
0.81 + 0.66 0.62 zt0.64 0.72 + 0.76 1.10 * 1.18 0.59 k 0.64 0.40 + 0.42 0.43 f 1.08 0.48 k 0.45 0.34 + 0.49 0.69 + 0.65
Discussion Thirty-four percent of women who deny chronic bowel symptoms report that the onset of menstruation is associated with a change in bowel habits: either increased diarrhea (19%), increased gas (14%j, or increased constipation (11%). These estimates differ from the 64% of 67 women studied by Rees and
Menstrual Distress Questionnaire scales” Negative affect Behavior change Pain Water retention Arousal Concentration
Symptoms
in Planned
Parenthood
3.24 1.72 3.24 2.34 0.43 1.54
+ k k + + *
5.34 2.98 3.59 2.83 1.17 3.93
Not exacerbated
1.11 + 0.63 1.09 * 0.43 1.10 + 0.54 1.44 * 0.44 1.14 k 0.62 0.73 + 0.29 0.19 -t 0.24 0.56 t 0.39 0.26 +- 0.25 0.95 * 0.31
0.97 t 1.07 k 0.80 k 1.36 + 0.96 k 0.50 t 0.63 k 0.52 k 0.41 + 0.88 +
Sample (Mean -+ SD) FBD
Not exacerbated 2.47 0.81 2.44 1.86 0.27 0.86
k k t + k f
4.77 2.43 3.74 2.81 0.95 2.31
0.81 0.84 0.65 0.97 0.86 0.55 1.04 0.64 0.39 0.65
Rhodes (4) who reported a change in bowel habits with menses and the 96% of 25 women studied by Hinds et al. (1). These differences may be attributable to the study of unrepresentative samples by previous investigators. A higher proportion of women with IBS report a worsening of bowel symptoms during menstruation as compared to women without chronic bowel symptoms. These differences cannot be explained by a neurotic tendency to overreport symptoms because women who reported menses-related worsening of bowel symptoms were not different psychologically from women who denied these symptoms. These differences also cannot be attributed to changes in affect or behavior within the menstrual cycle that might lead women to be more aware of and less tolerant of bowel symptoms because changes in affect and behavior during the cycle were not associated with a greater tendency to report worsening of bowel symptoms during menstruation. We infer that these differences have a physiological basis and are a reflection of the hyperreactivity of colonic smooth muscle in IBS to a variety of stimuli (18). The greater prevalence of hysterectomy among women with IBS and FBD than among controls confirms previous findings (19,20]. Because we know of no reason to expect an excess incidence of pelvic disease
Controls Exacerbated
Exacerbated
1.01 + 0.87 0.76 + 0.70 0.80 t 0.60 1.03 + 0.81 0.52 _t0.56 0.68 * 0.79 0.29 + 0.53 0.64 -t 0.96 0.26 t 0.47 0.74 f 0.61
Checklist scores in the gastroenterology clinic sample showed that the main effect for exacerbation of bowel symptoms was not statistically significant [F(10,25) = 0.44, p = 0.911. These data are shown in Table 4. Variations in negative affect and behavior occurring within the menstrual cycle were similarly unrelated to reports that bowel symptoms were exacerbated during menses [Table 5). The MANOVA analysis showed that the main effect for exacerbation of bowel symptoms was not statistically significant [F(2,339) = 1.29, p = 0.281. Tab1 e 5 a 1so shows the relationship of other MDQ change scores to exacerbation of bowel symptoms during menses. Although not directly related to this study, it is interesting to note that women with IBS and FBD were significantly more likely to report increased pain during menstruation as compared to normal controls [univariate F(2,340) = 7.00, p < 0.011.
Table 5. Menstrual
Vol. 98. No. 6
Exacerbated 4.76 1.63 4.52 2.78 0.76 1.31
+ + + * + +
5.99 2.89 3.55 2.91 1.79 2.41
IBS
Not exacerbated 3.29 1.12 3.45 2.90 0.55 0.52
+ + * + * +
4.82 2.50 4.13 2.43 1.17 1.98
Exacerbated 3.44 2.32 5.28 2.96 0.92 2.00
* k k + 2 +
4.38 3.86 4.14 3.10 2.31 3.18
Not exacerbated 5.64 1.91 5.18 3.27 0.64 1.18
+ + k * + k
4.01 2.21 3.49” 2.00b 1.57 1.83
“The Moos (1985) Menstrual Distress Questionnaire was scarred by subtracting the symptom severity during the luteal phase of the menstrual cycle from the symptom severity during menstrual flow. bUnivariate analyses of variance showed that normal subjects reported significantly less menses-related pain and water retention than IBS patients. No other contrasts were statistically significant.
BOWEL SYMPTOMS DURING MENSES
June 19910
in wornen with IBS, these operations were probably performed as an empirical attempt to correct abdominopelvic pain. This interpretation is supported by a recent study (21) showing that many women with symptoms of IBS consult gynecologists rather than gastroenterologists and that few of them receive firm gynecologic diagnoses. Thus the presence of symptoms of IBS or FBD and their relation to menstruation may ble important in assessing patients’ need for and likely Iresponse to hysterectomy. Additional research is needed to compare colonic motility during the first day of menstruation with colonifc motility at other times and to correlate colonic motility and bowel symptoms to circulating levels of prostaglandins. Whether prostaglandin antagonists would be useful in IBS patients with menstrual exacerbation remains to be determined. References
10.
11.
12.
13.
14.
15.
16.
I. Hinds JP. Stoney B, Wald A. Doesgender or the menstrual cycle affect colonic transit? Am J Gastroenterol1989;84:123-126. 2. Heitkemper MM, Shaver JF, Mitchell ES. Gastrointestinal symptoms and bowel patterns across the menstrual cycle in dysmenorrhea. Nurs Res 1988;37:108-113. 3. Turnbull GK, Thompson DG. Day S, Martin J, Walker E, Lennard-Jones JE. Relationship between symptoms, menstrual cycle and orocaecal transit in normal and constipated women. Gut 1989;30:30-34. 4. Reas WDW, Rhodes JWT. Altered bowel habit and menstruation. Lancet 1976;2:475. 5. Kamm MA, Farthing MJG, Lennard-Jones JE. Bowel function and transit rate during the menstrual cycle. Gut 1989;30:605-608. 6. Wald A, VanThiel DH, Hoechstetter L, Gavaler JS, Egler KM, Verm R, Scott L, Lester R. Gastrointestinal transit: the effect of the menstrual cycle. Gastroenterology 1981;80:1497-1500. 7. Bennett A. Effects of prostaglandins on the gastrointestinal tract. In Karim SM. ed. The prostaglandins. Progress in research. New York: Wiley Interscience. 1972:205-221. 8. Whitehead WE, Engel BT. Schuster MM. Irritable bowel syndralme. Physiological and psychological differences between diarrhea-predominant and constipation-predominant patients. Dig Dis Sci 1980;25:404-413. 9. Sullivan MA, Cohen S, Snape WJ Jr. Colonic myoelectrical
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Received August 7,1989. Accepted November 21,1989. Address requests for reprints to: William E. Whitehead, Ph.D., Division of Digestive Diseases, Francis Scott Key Medical Center, 4940 Eastern Avenue, Baltimore, Maryland 21224. Supported in part by Grants ROI NR01369 from the Center for Nursing Research and K05 MHOO133from the National Institute of Mental Health.
