Abstract
The effect of uterine leiomyoma on fertility is subject to continuous debate. IVF provides a unique opportunity to examine the effect of leiomyoma on embryonic implantation rate. Over the last two decades, many studies were published associating fibroids and infertility. Taken together these publications indicate that the implantation rate and pregnancy outcome is impaired in women with uterine leiomyoma when they cause deformation of the uterine cavity. In such patients, surgical treatment should be considered prior to IVF because of the reduced implantation rate, however, there are few prospective controlled studies that test the hypothesis that myomectomy with its inherent risks can help. In patients with intramural leiomyoma not invading the uterine cavity, the confusion still persists. Furthermore, even if one accepts that a negative effect of such fibroids exists, there is no direct proof that myomectomy results offer a better prognosis.
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Release date: 1 May 2013; Expiration date: 1 May 2014
Learning objectives
Upon completion of this activity, participants will be able to:
• Describe the association of fibroids with infertility, based on a review
• Describe considerations of performing myomectomy before IVF based on fibroid location and uterine cavity deformation, according to a review
• Describe considerations of performing myomectomy before IVF based on fibroid size, according to a review
Financial & competing interests disclosure
EDITOR
Elisa Manzotti
Publisher, Future Science Group, London, UK
Disclosure: Elisa Manzotti has disclosed no relevant financial relationships.
CME AUTHOR
Laurie Barclay, MD
Freelance writer and reviewer, Medscape, LLC
Disclosure: Laurie Barclay, MD, has disclosed no relevant financial relationships.
AUTHORS AND CREDENTIALS
Zion Ben-Rafael
Department of Obstetrics and Gynecology, IVF Unit, Laniado Medical Center, Netanya, Israel
Disclosure: Zion Ben-Rafael has disclosed no relevant financial relationships.
Despite numerous publications and years of research, the relationship between uterine fibroids and infertility is still unsettled. The exact mechanism by which fibroids may affect infertility is not certain and includes: blockage of the fallopian tubes; alterations of tubal motility and prevention of sperm–egg assembly; prevention of proper sperm migration through the cervical canal; dyspareunia; and thin, vascularized endometrium Citation[1] and abnormal uterine peristalsis Citation[2]. Only the last two can directly affect implantation and assisted reproductive technologies (ART)/IVF results.
It is obvious that depending on the number, size and location, some fibroids may cause a variety of signs and nonpathognomonic symptoms including pelvic mass, pressure, pain, heavy vaginal bleeding, infertility, miscarriage and premature delivery Citation[1–4]. The symptoms are not indicative of a causal relationship between existing fibroid and failure to procreate. Furthermore, it is hard to appraise accurately if a detected fibroid may affect fertility fully or marginally, directly or indirectly. Occasional cases of large fibroids, encountered during delivery or caesarean section, including intracavity fibroids (author’s personal experience), add to the confusion of delineating clear roles and conclusions of which fibroids can cause pregnancy failure.
After two decades of research and dozens of publications, what should have been straightforward clinical knowledge and practice remains highly controversial and difficult to formulate. Fibroids of the uterus are common, they increase with advanced age and they are no doubt among the most common benign pelvic tumors, attaining an incidence of 25–40% in women during their reproductive years Citation[4]. The prevalence of fibroids in fertile women is estimated to be between 1 and 2.4% Citation[1,2,5,6]. While most women with fibroids are probably fertile, the association between fibroids and infertility increases with age such that at 40 years, when infertility and fibroids reach a peak of 60 and 40%, respectively, the coexistence of the two can reach 24% and naturally attracts the attention of infertility specialists.
Our knowledge of the effect of fibroids on infertility in the pre-IVF era or in the non-ART setting is based on heterogeneous sets of data – some are outdated, from the 1970s and 1980s – collectively indicating that surgical myomectomy in infertile women is associated with a success rate of approximately 50% Citation[7,8]. These studies, however, include fibroids of various sizes, numbers and different locations and they are all uncontrolled or non-randomized, which explains the high variability of the results between <10 to >70% success rate Citation[6,9]. No comparison was made between women who underwent myomectomy and a control group without any operation, hence a cause and effect association between myomectomy and subsequent fertility has never been scientifically established. Nevertheless, as a consequence of all these studies, it was generally accepted, even if not systematically proven, that regardless of the means by which myomectomy is performed (hysteroscopy, laparoscopy or laparotomy), excision of submucous myoma can improve the chances of conception, whereas myomectomy of large intramural fibroids can improve the overall outcome of pregnancy Citation[10]. Similarly, in the ART/IVF setting, after two decades of publications correlating the results of ART treatment with the presence of fibroids, there is still more confusion and few sound conclusions.
ART & fibroids
The current social trend to delay childbearing to the 4th or 5th decade of life, when fibroids and infertility are more prevalent, increases the chances of encountering this association in elderly infertile women and the tendency to assume that a cause and effect association exists. However, at this age, most women suffer from infertility due to low-quality oocytes, which is the determining factor even if coexisting fibroids are detected. Hence, clinically, it is not easy to separate between infertility that is due to an existing fibroid or to other factors.
Since most of these older infertile women are promptly directed to ART treatment, these facts have created a renewed interest in the effect of fibroids of all shapes, sizes and locations on IVF outcome. The use of high resolution ultrasound equipment and frequent vaginal tests during treatment further increases the detection rate of even small fibroids, whether symptomatic or asymptomatic. It is obvious that not all fibroids produce infertility and the risk is that any detected fibroid might get undeserved attention and surgical treatment which is costly, time-consuming and not risk-free for patients who have a narrowing timeline to successful pregnancy. Therefore, the challenge is to distinguish between fibroids that do not affect the results, those that can marginally affect the results and those that deserve surgical management before proceeding to IVF. In the ART setting, which bypasses all the natural steps before egg–sperm interaction, the main outcomes measured are implantation, miscarriage rate and take-home baby rate.
In 1995, in a retrospective controlled trial, the authors drew attention to the fact that implantation rates and pregnancy outcomes were not different in a group of 46 women with fibroids in comparison to women with mechanical infertility without fibroids Citation[11]. However, if in hysteroscopy the leiomyoma was found to distort the uterine cavity, implantation rate was affected. The authors also suggested that in such patients with an abnormal uterine cavity, surgical treatment should be considered prior to IVF due to the reduced implantation rate Citation[11].
The findings on the submucous fibroids were later confirmed by other non-randomized studies Citation[10,12,13]. However, some of these studies also reported that intramural fibroids, which supposedly lack an intrauterine component, may have a deleterious effect on IVF results. As a result, excision of such fibroids should be considered. This conclusion remained controversial and was not confirmed by others Citation[9], requiring further elucidation. Despite few randomized control trials, a provisional summary of the literature permitted one to conclude that fibroids that impinge on the uterine cavity may lower implantation rates, and thus myomectomy prior to IVF might solve the problem. Conversely, the effect of intramural fibroids not encroaching on the uterine cavity warrants further investigation Citation[14].
Management of intramural myoma or IVF: which comes first?
Despite the accumulation of new information, it is still not easy to solve the current dilemma of the possible ill effect that small intramural fibroids may have on pregnancy potential. Donnez and Jadoul Citation[9] reported on a meta-analysis of six studies Citation[10–13,15] and found a pregnancy rate of 9 and 33.5%, respectively, in women with fibroids that impinged on the uterine cavity compared with women with fibroids that did not have an intracavitary component versus 40% in the control groups. The authors concluded that the large variations among the publications, the lack of proper diagnosis methodology and agreed definitions of fibroid location casts doubts on the true weight of these publications. Check et al. found that implantation and pregnancy rates were statistically similar in patients with or without intramural fibroids smaller than 5 cm; however, a trend toward higher abortion and lower delivery incidence was observed Citation[16]. The authors indicated the need for larger randomized controlled trials to solve the dilemma of myomectomy before IVF. Oliviera et al. concluded that in patients with intramural fibroids smaller than 4 cm that do not encroach into the uterine cavity, there is no negative effect on implantation or miscarriage rate over one cycle follow-up, a fact that also represents the limitation of the study Citation[17].
In a study comprised of 606 cycles, Khalaf et al. evaluated the cumulative effect of small intramural fibroids (<5 cm) not distorting the uterine cavity on implantation, ongoing pregnancy and live birth rate in three successive treatment cycles Citation[18]. Pregnancy, ongoing pregnancy and live birth rates were 23.6, 18.8 and 14.8% in the study group, respectively, compared with 32.9, 28.5 and 24%, respectively, in the control group. Regression analysis showed an approximate 40% reduction in success rates (p < 0.05), which leads to the conclusion that small fibroids have a less distinctive effect that might be missed when studying a single cycle, but becomes statistically apparent when looked at in a cumulative manner over several cycles Citation[18].
Taken together, these and other studies show conflicting results on IVF outcome only with intramural fibroids that are smaller than 5 cm and lack an intracavity component. Meanwhile large intramural fibroids or fibroids that distort the uterine cavity were clearly shown to impact the results of IVF, and hence, these women may, theoretically, benefit from surgical removal prior to IVF treatment.
Whereas the first meta-analyses showed limited or no impact of intramural fibroids Citation[9,19], the latter ones have documented an impact of fibroids not impinging on the uterine cavity on the fertility performance Citation[14,19–22]. Sunkara et al., in a newer meta-analysis, reviewed 19 studies comprised of 6087 cycles and reported on a significant reduction in the live birth rate (relative risk: 0.79) and clinical pregnancy rate (relative risk: 0.85) Citation[22].
Somigliana et al. concluded in a recent prospective study that in asymptomatic patients with intramural fibroids smaller than 5 cm not invading the cavity, the results were not affected Citation[23]. They concluded that “future efforts should be aimed to identify the subgroup of women” in whom the fibroid can increase risk. However, like others, they do not advise as to how the authors should identify these patients other than by size and location Citation[23].
The differences between the various studies are probably due to the difficulty in evaluating the true location of the fibroids and their relationship to the uterine cavity rather than only to the size of the fibroids. Admittedly, it is difficult to comprehend how a 5 cm fibroid on a 2 cm thickness uterine wall can escape imprinting on the cavity. Clinically, we probably need to improve our capability to evaluate the relationships of the fibroids with the cavity by other tools such as 3D sonography or even MRI.
A different approach to study the effect of fibroids on the fertility potential was taken by Johnson et al. in a ‘right from the start’ study Citation[24]. They followed a group of 3000 pregnant women who underwent first trimester ultrasound to determine the presence and characteristics of leiomyoma and retrospectively correlated it to self-reported time to conception. Women treated for infertility were excluded. They found no association between leiomyoma presence, type, location, segment or size and the time to pregnancy in 324 women (11%). The authors recognized that their study lacks the power to comment on the association of location to infertility and measures of the clinical symptoms and, hence, that their population, which was younger, may have been different to the usual series reporting on infertile women Citation[24].
Is myomectomy the answer to submucous & intramural fibroids?
The other controversial unsettled issue is the role of myomectomy in these cases. The intuitive assumption that myomectomy can overcome the decreased fertility associated with certain fibroids is not supported by the published experience. This question has come under scrutiny following new prospective studies.
Earlier retrospective studies have looked into the determinates of pregnancy rate and outcome following laparoscopic myomectomy and concluded that fertility and pregnancy after laparoscopic myomectomy depends primarily on patient age, duration of infertility before myomectomy and existence of associated infertility factors Citation[25]. While this is in line with what is known, it does not prove that myomectomy was required in these patients in the first place.
The first study to report on myomectomy in an IVF setting compared the effect of surgical removal of fibroids before egg donation cycles and concluded that the results were similar in the normal controls and in the recipients that were operated on previously Citation[26,27]. Naturally, these results can be interpreted in two directions, the second being that the operation was not required altogether. In fact, the mere association of fibroids with lower pregnancy potential cannot support the interpretation that myomectomy is the solution. A newer Cochrane review has rightfully challenged the paradigm.
This review, published in 2012, examined the issue of whether myomectomy can result in improvement of fertility and what is the preferred mode of operation Citation[28]. They considered 243 studies for evaluation, of which 23 were recognized randomized studies but only three studies complied with the level of evidence that was set Citation[29–31]. The only study that qualified to answer the first question on the effects of fibroids on fertility included 170 patients and looked only at cases with one fibroid greater than 4 cm in diameter Citation[29]. Collectively, this Cochrane review based on one study found no improvement in fertility and no evidence of reduction in the miscarriage rate following myomectomy in infertile women regardless of whether the fibroids were submucous, intramural, or a combination of submucous and intramural or subserous and intramural.
As for the alternative surgical approaches, they identified two studies fulfilling the set criteria and found no difference if the myomectomy was performed by the classical route of laparotomy or laparoscopy Citation[30,31]. It is possible that laparoscopy, with its slower learning curve, may present a choice for the more experienced endoscopic surgeons, an issue that is not addressed in these studies. Rightfully, the authors have also questioned the issue of the effect of hysteroscopic myomectomy for submucous fibroids Citation[28], which is considered an accepted indication. Considering the fact that the only randomized trial has only looked at reproductive outcome collectively using hysteroscopy and laparoscopy, without real possibility to differentiate between the two, and that the risk of adhesions versus the benefit of operating on a small submucous fibroid may prove inconvenient Citation[29]. Yoshino et al. found that myomectomy decreases the abnormal uterine peristalsis Citation[32], which is reported to increase with the presence of intramural fibroids Citation[2]. However, this should not be taken as proof that myomectomy was indicated.
Conclusion
The current social trend to delay childbearing to the fourth or fifth decade of life, when fibroids and infertility are more prevalent, increases the chances of encountering this association in specific patients. At 40 years of age, infertility is mainly due to decreased ovarian reserve and lower quality eggs. While fibroids are very common, they infrequently exert a negative effect on pregnancy potential. With the high rate of association of these two problems and the lack of a gold standard to diagnose which fibroids affect the chances to conceive, it is not surprising that many physicians tend to lean towards myomectomy as the partial solution to the problem. However, the role of myomectomy remains ambiguous. The ultimate randomized study of patients with uterine leiomyoma of similar size and location, which have no other apparent infertility factors, is not easy to design and execute with significant numbers. Despite the lack of proper information, as of today, it is acceptable to perform myomectomy prior to IVF in women with submucous fibroids and fibroids that are encroaching into the uterine cavity. Considering that the uterine wall is no more than 2 cm in thickness, it is possible that all the intramural fibroids that are larger than 5 cm have some submucous component and therefore deserve surgical consideration.
On the other hand, it is not advisable to perform myomectomy on intramural fibroids that are smaller than 5 cm and definitely not on those smaller than 3 cm. The final decision on those cases remains at the discretion of the treating physician and the patient, based on personal experience with IVF and surgical skills in myomectomy, and the kind of pregnancy failure that they are experiencing. The less pronounced effect of intramural fibroids on the outcome is probably one of the reasons for the miscellaneous results; different studies with newer tools to evaluate the fibroids vis-à-vis the uterine cavity are urgently needed. This review does not discuss fibroids that are causing pain or bleeding in women desiring fertility. In these cases, a less invasive solution or a solution that offers temporary relief can also be considered.
Expert commentary
The delay in family planning, which is so characteristic of our time, increases the chances of encountering fibroids and infertility with no real tools to decide if there is a cause and effect or just an association. However, it is difficult to resolve if a specific fibroid of known size and location is capable of affecting implantation, causing miscarriage or premature delivery or will just go unnoticed. Furthermore, it is not known if a failure will necessarily repeat itself. On the other hand, older women who have a high prevalence of infertility and fibroids may wish to have a solution that includes ‘do something (myomectomies) before it is too late’. The accumulated literature from the last 20 years does not help to formulate when to operate and when to refrain from operating on intramural fibroids. New controlled studies that use the most accurate diagnostic tools and engage mainly experienced ‘reproductive surgeons’ to offset the variability inherent in surgery may help to solve the issue. Unfortunately, experience shows that it will take many years before more precise data will be accumulated.
Five-year view
Some clinical questions are not easy to solve, even with randomized controlled trials, especially when so many variables exist. Fibroids vary in the size, location, number, distance from the endometrium and the age of the patient. They can affect fertility, but not necessarily in every pregnancy. Adding the variabilities, such as the quality of the operation and the loss of time due to the operation, it is not impossible that 5 years from now, the author will still not be able to formulate what to do with an existing fibroid beyond what is known today. On the other hand, new conservative treatments, such as specific progesterone modulators, may prove to be useful in offering temporary control of the fibroid size to minimize the effect on fertility. It is questionable whether more invasive, non-operative procedures, such as embolization or focused ultrasound, can offer a solution in these cases.
Key issues
• Fibroids of all sizes, shape, location and number are common in women with advanced age, resulting in infertility.
• The challenge is to distinguish between fibroids that do not affect the results of IVF, those that can marginally affect the results and those that deserve surgical management before proceeding to IVF.
• Fibroids deforming the uterine cavity can cause fertility failure; in such cases, a myomectomy might be justified.
• Intramural fibroids might also affect fertility but there is real proof that myomectomy (of intramural fibroids) will result in better reproductive performance compared with patients who were not operated on or to infertile women without fibroids.
• The conflicting results between studies are probably due to the difficulty in evaluating the true location of the fibroids and their relationship to the uterine cavity, rather than just the size of the fibroids.
• The intuitive assumption that myomectomy can overcome the decreased fertility associated with certain fibroids is not supported by published experiences.
• In fact, the mere association of fibroids with lower pregnancy potential cannot support the interpretation that myomectomy is the solution.
• A Cochrane review from 2012, based on one study, found no improvement in fertility and no evidence of reduction in the miscarriage rate following myomectomy in infertile women, regardless of whether the fibroids were submucous, intramural or a combination of submucous and intramural or subserous and intramural.
References
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Should we operate on fibroids before IVF?
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Activity Evaluation: Where 1 is strongly disagree and 5 is strongly agree
1. Based on the review by Dr Ben-Rafael, which of the following statements about the association of fibroids with infertility is most likely correct?
□ A At 40 years of age, fibroids are the leading cause of infertility
□ B With aging, small but not large fibroids become more common
□ C Clinicians have a well-defined golden standard to determine which fibroids affect reproductive potential
□ D The role of myomectomy remains ambiguous
2. Your patient is a 42-year-old woman with infertility and leiomyoma. Based on the review by Dr Ben-Rafael, which of the following statements about considerations of performing myomectomy before IVF, based on fibroid location and uterine cavity deformation, is most likely correct?
□ A Implantation rate and pregnancy outcome are impaired in women with fibroids causing deformation of the uterine cavity
□ B Myomectomy offers a better prognosis in women with intramural fibroid not invading the uterine cavity
□ C A 2012 Cochrane review showed significant differences in improvement in fertility after myomectomy based on whether the fibroids were submucous, intramural, or a combination
□ D In women with submucous fibroids, myomectomy before IVF is contraindicated
3. Based on the review by Dr Ben-Rafael, which of the following statements about considerations of performing myomectomy before IVF based on fibroid size would most likely be correct?
□ A All intramural fibroids larger than 1.5 cm are likely to have some submucous component and should therefore be operated
□ B For intramural fibroids between 3 to 5 cm, the final decision regarding surgery should be based on the discretion of the treating physician and the patient
□ C A study showed no difference in abortion and delivery rates among patients with or without intramural fibroids smaller than 5 cm
□ D Findings of randomized trials of patients with fibroids of similar size and location and no other apparent infertility factor have given a clear size cutoff for performing myomectomy