Risk Factors for Uterine Fibroids among Women Undergoing Tubal Sterilization
Chao-Ru Chen1,
Germaine M. Buck1,1,
Norman G. Courey2,
Kimberly M. Perez1,3 and
Jean Wactawski-Wende1,2
1 Department of Social and Preventive Medicine, School of Medicine and Biomedical Sciences, University at Buffalo, State of New York, Buffalo, NY.
2 Department of Gynecology-Obstetrics, School of Medicine and Biomedical Sciences, University at Buffalo, State of New York, Buffalo, NY.
3 Department of Community and Family Medicine, Dartmouth Medical School, Hanover, NH.
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ABSTRACT
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Uterine leiomyomas are reported to be the most common benign gynecologic tumors affecting premenopausal women, and they are often associated with considerable morbidity. The purpose of this study was to identify risk factors for uterine fibroids among women undergoing tubal sterilization. Cases comprised women aged 1744 years whose uterine fibroids were first visualized at the time of tubal sterilization (19781979 or 19851987) or who reported a history of uterine fibroids (n = 317). Controls were randomly selected from women with no laparoscopic evidence of or history of fibroids (n = 1,268). Adjusted odds ratios were estimated using unconditional logistic regression separately for White (n = 1,235) and African-American(n = 350) women. Risk factors for White women included: age 4044 years (odds ratio (OR) = 6.3; 95% confidence interval (CI): 3.5, 11.6),
5 years since last delivery (OR = 1.9; 95% CI: 1.1, 3.1), lifetime cigarette smoking of
1 pack/day (OR = 1.6; 95% CI: 1.1, 2.3), menstrual cycle length of >30 days (OR = 1.6; 95% CI: 1.1, 3.3), and menstrual bleeding for
6 days (OR = 1.4; 95% CI: 1.0, 2.0). Parous women were at reduced risk compared with nulliparous women (OR = 0.2; 95% CI: 0.1, 0.3). Advancing age was the only significant risk factor for African-American women (ages 4044 years, OR = 27.5; 95% CI: 5.6, 83.6). Current oral contraceptive use and elective abortion were not associated with fibroids.
ethnic groups; leiomyoma; risk factors; sterilization, tubal; uterine diseases
Abbreviations:
CI, confidence interval; OR, odds ratio
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INTRODUCTION
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Uterine leiomyoma is reported to be the most common benign gynecologic tumor affecting premenopausal women. In the United States, fibroids are a leading cause of hospitalizations for gynecologic disorders and the most frequent reason for hysterectomy (1
, 2
). Accurate prevalence figures are lacking, primarily because of limited population-based research, varying symptomatologies (3
), and differences in case definitions across studies. Most research conducted to date has focused on symptomatic White women, with limited study of African-American women (4
, 5
) or women with asymptomatic disease.
Although the etiology of fibroids remains unknown, the ovarian hormones estrogen and progesterone are hypothesized to enhance fibroid growth (6
, 7
). Reported risk factors consistent with the hormonal hypothesis include premenopausal status (8
10
), younger age at menarche (5
, 9
, 11
), and obesity (8
10
, 12
). Never having been married (5
) and higher educational attainment (9
, 10
) are also reported to be risk factors. History of infertility, young age at first birth, and current alcohol consumption have been associated with increased risk (5
, 11
). Reported protective factors include parity (8

11
, 13
) and oral contraceptive use (8

11
, 14
16
). Use of oral contraceptives at young ages was reported to be associated with an elevated risk in at least one study (11
). Cigarette smoking has been reported to be inversely related to risk in several studies (8
10
, 13
, 17
19
), but not all (12
). These findings stemmed largely from case-control studies among which eligibility criteria (i.e., age, race, marital status) varied, as did case definitions (i.e., self-reports; histologic, pathologic, or ultrasound/hysterectomy confirmation) (5
, 8


12
). The purpose of this study was to identify risk factors for fibroids among women who were undergoing tubal sterilization, and to assess the consistency of risk factors in White and African-American women.
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MATERIALS AND METHODS
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The referent study cohort comprised 3,303 women aged 1744 years who underwent tubal sterilization during the period 19781979 or 19851987 at one of five hospitals in Buffalo, New York, that performed sterilization procedures. The cohort was enrolled in a larger multicenter study in which the purpose was to assess the efficacy and safety of tubal sterilization (20
). Only women with "interval" sterilizations occurring apart from delivery were eligible for inclusion in the cohort. Trained nurses conducted in-person interviews with the women prior to surgery to obtain information on: 1) sociodemographic characteristics; 2) medical, reproductive, menstrual, and contraceptive histories (last 3 months prior to sterilization); and 3) select lifestyle characteristics, such as usual lifetime cigarette smoking and body mass index. Although surgeons were instructed as a part of the larger study (20
, 21
) to perform a specific type of tubal sterilization by clinical site, they were not given any further instructions regarding laparoscopic approach or the extent of visualization of the woman's pelvis.
For study purposes, a nested case-control design was utilized. One hundred and thirty-two women were excluded from the present study because their race was other than White or African-American (n = 129) or they were missing operative information on fibroids at sterilization (n = 3). Among the 3,171 women undergoing tubal sterilization, 317 women with fibroids were identified, including 196 women with fibroids newly diagnosed at surgery and 121 women with a history of fibroids. Forty-five percent (n = 55) of the latter group had fibroids noted at sterilization. Potential controls comprised women without any fibroid diagnosis either at or before sterilization (n = 2,854), and they were frequency-matched to cases according to race (White/African-American) and year of tubal sterilization at a ratio of approximately 4:1. Controls comprised 988 White women and 280 African-American women.
We investigated the association between presence of uterine fibroids and various sociodemographic, menstrual, reproductive, and lifestyle characteristics using unconditional logistic regression analysis. For each study variable, we used multivariate logistic regression to obtain partially and fully adjusted odds ratios with corresponding 95 percent confidence intervals (22
).
Since approximately half of the sample had missing information on parity, we used number of living children (which theoretically could include adopted children or exclude deceased children) as a proxy measure. These two variables were very highly correlated (r = 0.99) in women for whom parity information was available. Age and number of living children were categorized for inclusion in the models as follows: for age, <30, 3034, 3539, and 4044 years; for number of living children, 0, 1, and 2 or more. Women were asked about menstrual cycle characteristics, including cycle length, regularity, flow, pain, and spotting between cycles for the last three menstrual cycles prior to sterilization (21
). Heavy flow referred to self-reports of "heavy" or "very heavy" bleeding during the first 3 days of menstrual bleeding. Irregular menstrual cycles referred to "irregular" or "almost always irregular" menstrual cycles. Severe menstrual pain was defined as having pain or cramping which required analgesic use or severe pain or cramping during menstruation. Spotting between cycles was defined as any bleeding or spotting between periods. Time since last delivery referred to the interval between date of last delivery and sterilization; it was categorized in years, with nulliparous women being treated as one category. Type(s) of contraception used was assessed only for the 3 months prior to sterilization (20
, 21
). Valid responses included: none, oral contraceptives, intrauterine devices, and other methods.
Lifestyle characteristics considered included cigarette smoking and body mass index. Women were asked how many cigarettes they had smoked per day throughout their lifetime, on average. The following categories were devised for cigarette smoking: smoker, ex-smoker, and smoking of (on average) <1 or
pack per day. Body mass index was defined as weight (in kilograms) at tubal sterilization divided by the square of current height (in meters). Body mass index was dichotomized at the cutpoint of 27.3, consistently with the designation for obesity in women (23
).
Partially adjusted models for each independent variable were adjusted for age at sterilization and number of living children. To test for trends, we treated age, education, number of living children (among women with
1 child), duration of menstrual bleeding, menstrual cycle length, time interval between last delivery and sterilization, age at last delivery, and body mass index as continuous variables in separate models (22
). Women with missing or unknown data on menstrual cycle length were recoded as having unknown lengths and were included as such in partially and fully adjusted models (i.e., 19 and 100 White case and control women, respectively, and 4 and 21 African-American case and control women, respectively).
Separate unconditional logistic regression analyses were carried out for White and African-American women using the backward stepwise elimination procedure. The final model included all statistically significant variables whose removal would change the significance of the log-likelihood ratio of the model (p < 0.2) (24
). For White women, the final model included age, education, heavy menstrual flow, irregular menstrual cycles, duration of menstrual bleeding, cycle length, number of living children, years since last delivery, and cigarette smoking. For African-American women, the final model included age, marital status, heavy menstrual flow, and years since last delivery.
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RESULTS
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The sample comprised mostly White, married, educated women of reproductive age (table 1). The prevalence of fibroids was 9 percent (247/2,726) for White women and 16 percent (70/448) for African-American women. Prevalence decreased to 6 percent and 12 percent, respectively, when the analysis was restricted to women without a history of fibroids. Risk of uterine fibroids increased significantly with advancing age, regardless of race. Overall, White women aged 4044 years had a ninefold increase in risk (odds ratio (OR) = 9.3; 95 percent confidence interval (CI): 5.5, 15.8) compared with women under 30 years of age, while African-American women of similar age had an approximately 24-fold increase in risk (OR = 23.5; 95 percent CI: 7.3, 75.7). No significant associations with risk were observed for education or marital status in either group of women.
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TABLE 1. Risk of uterine fibroids according to selected sociodemographic characteristics for White and African-American women undergoing tubal sterilization during 19781979 and 19851987, Buffalo, New York
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Heavy menstrual flow was associated with an increased risk of uterine fibroids among both White women (OR = 1.4; 95 percent CI: 1.0, 1.8) and African-American women (OR = 1.4; 95 percent CI: 0.8, 2.5) after adjustment for age at sterilization and number of living children (table 2). There was a suggestion of a reduced risk for irregular menstrual cycles for both White (OR = 0.7; 95 percent CI: 0.4, 1.1) and African-American (OR = 0.7; 95 percent CI: 0.3, 2.1) women. Menstrual bleeding for
6 days was associated with an increased risk for White women (OR = 1.5; 95 percent CI: 1.1, 2.0) but not for African-American women (OR = 0.8; 95 percent CI: 0.3, 1.8). Increasing duration of menstrual bleeding (per day) was associated with a 13 percent increase in risk of fibroids for White women (OR = 1.13; 95 percent CI: 0.9, 1.2). However, trends were not statistically significant. Odds ratios were elevated for menstrual cycle length of >30 days in both groups of women (for Whites, OR = 1.7 (95 percent CI: 1.0, 2.9); for African-Americans, OR = 4.8 (95 percent CI: 0.9, 25.9)). Neither severe menstrual pain nor spotting between cycles was significantly associated with risk of fibroids for either racial group.
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TABLE 2. Risk of uterine fibroids according to selected menstrual cycle characteristics for White and African-American women undergoing tubal sterilization during 19781979 and 19851987, Buffalo, New York
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Number of living children (our proxy for parity) was inversely related to risk of fibroids only among White women (table 3). In fact, White women with two or more children had a 70 percent reduction in risk compared with White women without any living children (OR = 0.3; 95 percent CI: 0.2, 0.4). The risk of fibroids increased as the interval between last delivery and sterilization increased for White women. Among parous women, no significant trends were observed for age at last delivery and risk in either racial group. Oral contraceptive use before sterilization and history of elective abortion were not associated with an increased risk in either group of women. Current smoking of one or more packs of cigarettes per day was associated with an increased risk for White women (OR = 1.6; 95 percent CI: 1.1, 2.3) but not for African-American women (OR = 0.7; 95 percent CI: 0.2, 1.7). No trend was observed for body mass index and risk in either group, and obese women did not appear to be at greater risk.
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TABLE 3. Risk of uterine fibroids according to selected reproductive and lifestyle characteristics for White and African-American women undergoing tubal sterilization during 19781979 and 19851987, Buffalo, New York
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Table 4 presents the results of multivariate logistic regression analysis. Among White women, advancing age (4044 years) remained the strongest risk factor (OR = 6.3; 95 percent CI: 3.5, 11.6), followed by
5 years since last delivery (OR = 1.9; 95 percent CI: 1.1, 3.1), smoking of one or more packs of cigarettes per day (OR = 1.6; 95 percent CI: 1.1, 2.3), menstrual cycle length of >30 days (OR = 1.6; 95 percent CI: 1.1, 3.3), and menstrual bleeding of
6 days (OR = 1.4; 95 percent CI: 1.0, 2.0). Parous women (those with at least one living child) were at reduced risk compared with nulliparous women, and this trend achieved statistical significance (p < 0.001). Advancing age was the only statistically significant risk factor for African-American women (OR = 27.5; 95 percent CI: 5.6, 83.6); trends for age were significant for both groups of women. Parity was not retained in the model; hence, no reduction in risk was observed for African-American women.
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TABLE 4. Multivariate analysis of risk factors for uterine fibroids first diagnosed at tubal sterilization during 19781979 and 19851987, by race, Buffalo, New York
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DISCUSSION
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The overall prevalence of fibroids in this sample of women undergoing tubal sterilization was 10 percent, i.e., 317 out of 3,171 women. This figure decreased to 6 percent after we removed the 121 women with a prior physician diagnosis of fibroids. The extent to which this figure could be used to estimate asymptomatic fibroids is unknown, given the selectiveness of the study sample. Data from the National Fertility Survey and the National Survey of Family Growth have identified married, Protestant, and older women and those aged <20 years at first birth as being most likely to report tubal sterilization at interview (25
). Women with a college-level or higher education or who resided outside of the southern United States in 1995 were less likely to report sterilization (25
). Our sample may have underrepresented infertile women who do not seek tubal sterilization and who are reported to be at increased risk for fibroids (11
, 13
), although the relation between fibroids and fecundity remains equivocal (3
, 6
).
We observed a higher prevalence of fibroids in African-American women compared with White women, a finding that is consistent with some previous reports (3
5
) but not all (10
). Previous authors have postulated that the higher prevalence rate in Black women may be attributable to gene encoding or a positive family history of fibroids (3
), myometrial irritation following a pelvic infection, resulting in abnormal uterine growth (8
), or higher levels of estrogen (8
). Other possibilities include differences in parity, body mass index, use of oral contraceptives or other hormonal preparations, and childbearing patterns. Recent data upheld higher rates for Black women even after adjustment for several of these factors (5
). Given the design and sample size limitations of our study, we were unable to fully assess the relation between race and risk of fibroids. Many of the confidence intervals overlapped for White and African-American women. However, we have no a priori reason to assume that African-American women were systematically missed from our sampling frameespecially given the tremendous increase in the percentage of non-Hispanic African-American US women reporting sterilization between 1973 (20 percent) and 1995 (50 percent) (25
).
Within the confines of our study, our findings suggest that risk factors may vary by race. This is suggestive of a more complex or multifactorial etiology for fibroids than a simple familial or hormonal basis. Increasing age was the strongest risk factor for uterine fibroids, which is consistent with earlier reports (5
, 8
, 15
), despite the younger ages of our women. An inverse relation has been previously reported for parity and risk of fibroids (8

11
, 13
), and we observed this relation as well, but only for White women. Some authors have interpreted the reduction in risk for parity as supportive of the estrogen hypothesis (8
), while others argue that fibroids impair women's fecundity or fertility (6
). Still, recent data suggest that parity is independent of infertility (11
). Our definition of parity referred to number of living children, and it may not be directly comparable with the definitions of previous studies. Nulliparous women in our study may have included women who chose not to have children, and they may have differed from nulliparous women in other studies. However, national data indicate that approximately 6 percent of sterilized nulliparous women, as compared with 71 percent of parous women, cite the fact that they or their partner did not want children as the reason for sterilization (25
25); most nulliparous women are sterilized for medical reasons. The absence of an inverse association for parity among African-American women suggests that this relation may not be so simple. History of elective abortion did not confer an increased risk, which is consistent with a previous report (13
).
White women with a longer menstrual cycle length and duration of menstrual bleeding (>6 days) were observed to be at higher risk for uterine fibroids than those with shorter bleeding histories. Cramer et al. (17
) found a higher proportion of abnormal bleeding in women with fibroids than in those without them, but this increase did not reach statistical significance. The authors suggested that excessive injury to and repair of the endometrial lining may promote monoclonal expansion of smooth muscle cell populations in the uterine wall (i.e., myomas). Other authors have suggested that a longer duration of menstrual bleeding may be a clinical symptom of fibroid growth and may not be etiologically linked (3
, 6
). The association between cycle length and risk is less clear, especially given the absence of a significant trend. The extent to which cycle length or duration of bleeding is indicative of underlying pathophysiology, unrelated aging of reproductive processes, or growth of fibroids remains unknown.
We were unable to confirm results of previous studies which found an inverse relation between oral contraceptive use and risk of fibroids (8
, 10
, 11
, 13
). Risk was reduced 10 percent for White women who used oral contraceptives but was increased 70 percent for African-American women who used them; all confidence intervals included 1. Our inferences regarding the relation between fibroids and oral contraceptive use are limited, because we only had data on oral contraceptive use in the 3 months prior to sterilization. Some clinicians argue that oral contraceptive use is contraindicated in women who are "at risk" for developing fibroids (16
), which further complicates interpretation of this association. Unlike the case in previous studies (8
, 9
), we did not observe any consistent association between age at last delivery and risk of fibroids. Some authors focus on age at last full term birth (8
, 9
, 13
), while others select time since last delivery (11
). These two variables are often inversely correlated, as they were in our study, and we opted to include the latter variable in our multivariate model, given the young age distribution of our women and our inclusion of age at sterilization in the model. The trend was not significant, despite an increased risk for
5 years since sterilization.
Average lifetime smoking of one or more packs per day increased risk, contrasting with earlier reports of an inverse relation between cigarette smoking and risk of fibroids (8
10
). The inverse association with smoking was observed only for women with a low body mass index (
22.2) in a case-control study of any self-reported fibroids (10
). Women in our study were aged 1744 years, noticeably younger than women in previous studies (8
, 9
, 10
, 13
), and our results are in keeping with the suggestion that menopausal status may modify the relation between smoking and fibroids (12
). Our crude measure of smoking may also account for the lack of a protective effect. We observed no association for body mass index
27.3, which is consistent with the findings of previous investigators (9
, 10
).
The results of this study require careful interpretation, given that they stemmed from a select sample of women who chose to undergo surgical sterilization. If pregnancy or childbearing intentions and behaviors affect fibroid formation, these results may have limited external validity. Furthermore, we recognize that diagnosis of fibroids may vary across surgeons, resulting in misclassification bias. However, we have no reason to assume that this bias would be differential with respect to the risk factors under study. Compared with ultrasound, laparoscopy (via tubal sterilization) may underascertain fibroids that cannot be directly visualized. We do recognize that the temporal ordering between risk factors and fibroids may be inexact, since we do not know when the fibroids actually developed in relation to risk factors. Of 121 women with prior diagnoses, 55 (45 percent) were noted to have fibroids at sterilization. Women whose fibroids were not noted at sterilization tended to have higher parity and to more often report having a heavy menstrual flow prior to tubal sterilization than women in whom fibroids were noted at surgery. Among African-American women, there were no significant differences between women with a history of fibroids and women with fibroids newly diagnosed at sterilization in terms of age at sterilization, number of living children, duration of menstrual bleeding, cigarette smoking, education, and years enrolled. White women with a history of fibroids were less likely to be nulliparous than White women whose fibroids were first diagnosed at tubal ligation. We reanalyzed the data after excluding women who had had fibroids diagnosed prior to sterilization (n = 121) and observed few differences, other than slight changes in point or interval estimates (data not shown).
In summary, our findings identify age as a risk factor for fibroids in both White and African-American women with asymptomatic fibroids, which is consistent with earlier reports. Parity reduced risk, but only for White women. Thus, an understanding of the etiology of fibroids remains elusive. Our data, coupled with those from the available literature, suggest that age, menstruation, and possibly smoking deserve further study, along with the protective effects of parity.
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ACKNOWLEDGMENTS
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The authors thank Dr. Pauline Mendola for her helpful comments on an earlier version of this paper and Terri Raimondo for her technical assistance. Funding for this study was made possible by a Merck/Society for Epidemiologic Research Fellowship Award given to Dr. Germaine M. Buck.
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NOTES
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Reprint requests to Dr. Jean Wactawski-Wende, Department of Social and Preventive Medicine, 270 Farber Hall, School of Medicine and Biomedical Sciences, University at Buffalo, State of New York, Buffalo, NY 14214 (e-mail: jww{at}buffalo.edu).
Editor's note: An invited commentary on this article and on the previous two-part paper by Faerstein et al. appears on page 27. Chen et al.'s response appears on page 30.
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Received for publication January 7, 1999.
Accepted for publication May 1, 2001.