Committee Opinion
Number 618, January 2015


Committee on Gynecologic Practice
This document reflects emerging clinical and scientific advances as of the date issued and is subject to change. The information should not be construed as dictating an exclusive course of treatment or procedure to be followed.


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Ovarian Reserve Testing

ABSTRACT: The main goal of ovarian reserve testing is to identify those individuals who are at risk of decreased or diminished ovarian reserve, commonly known as DOR. Although ovarian reserve testing cannot predict the end of one’s reproductive years, results outside the range expected for a patient’s age can encourage the individual to pursue more aggressive treatment options to achieve pregnancy. Ovarian reserve testing should be performed for women older than 35 years who have not conceived after 6 months of attempting pregnancy and women at higher risk of diminished ovarian reserve. When test results suggest decreased or diminished ovarian reserve, if appropriate, an infertility evaluation should be initiated. It is reasonable to counsel the woman that her window of opportunity to conceive may be shorter than anticipated, and attempting to conceive sooner rather than later is encouraged. Compared with women of similar age, women with diminished ovarian reserve commonly have regular menses but a reduced quantity of ovarian follicles and, thus, may have a limited response to ovarian stimulation with fertility medications and reduced fecundity (probability of achieving a live birth in a single reproductive cycle). At this time, ovarian reserve testing results cannot be extrapolated to predict the likelihood of spontaneous conception.


Conclusions and Recommendations

Based on the available data and expert opinion, the American College of Obstetricians and Gynecologists offers the following conclusions and recommendations:

  • Ovarian reserve testing should be performed for women older than 35 years who have not conceived after 6 months of attempting pregnancy and women at higher risk of diminished ovarian reserve, such as those with a history of cancer treated with gonado-toxic therapy, pelvic irradiation, or both; those with medical conditions who were treated with gonadotoxic therapies; or those who had ovarian surgery for endometriomas.
  • For general obstetrician–gynecologists, the most appropriate ovarian reserve screening tests to use in practice are basal follicle-stimulating hormone (FSH) plus estradiol levels or antimüllerian hormone (commonly known as AMH) levels. An antral follicle count, commonly known as an AFC, also may be useful if there is an indication to perform transvaginal ultrasonography.
  • It is important to recognize that a poor result from ovarian reserve testing does not signify an absolute inability to conceive and should not be the sole criteria considered to limit or deny access to infertility treatment.
  • The best surrogate marker for oocyte quality is age.
  • Female age and ovarian reserve test results are useful for discussing prognosis and recommending a treatment plan. Younger women with diminished ovarian reserve demonstrate reduced oocyte numbers but may have normal oocyte quality, whereas older women with normal ovarian reserve may have a good number of oocytes but an age-appropriate decrease in oocyte quality.
  • When test results suggest decreased or diminished ovarian reserve, it is reasonable to counsel the woman that her window of opportunity to conceive may be shorter than anticipated, and attempting to conceive sooner rather than later is encouraged.
  • Compared with women of similar age, women with diminished ovarian reserve commonly have regular menses but a reduced quantity of ovarian follicles and, thus, may have a limited response to ovarian stimulation with fertility medications and reduced fecundity (probability of achieving a live birth in a single reproductive cycle).

Background

Female reproductive aging is a process that follows the generally accepted theory that over time, oocytes decrease in quantity and quality and do not regenerate (1). The number of human oocytes in a female peaks at 6–7 million during fetal life (around midgestation), followed by profound atresia; approximately 1–2 million oocytes are present at birth, 300,000–500,000 at the start of puberty, and 1,000 at 51 years of age, which is the average age of menopause in the United States (2). Factors such as genetics, lifestyle, environment, and medical issues, including endometriosis, ovarian surgery, chemotherapy, and radiation, can influence the quantity and quality of a woman’s oocytes (3). Although this reproductive decline occurs with age, there is significant variation in fertility among women of similar age, which highlights the unpredictability and individuality of the reproductive aging process (4).

Table 1. Summary of the Value of Ovarian Reserve Screening Tests
Test Cutpoint

Poor Response to
Ovarian Stimulation



Sensitivity   Specificity

Nonpregnancy*



Sensitivity   Specificity
Reliability Advantages Limitations
FSH
(international
units/L)
10–20   10–80         83–100   7–58          43–100 Limited Widespread
use
Reliability
Low sensitivity
AMH (ng/mL) 0.2–0.7   40–97         78–92    †                 † Good Reliability Limit of
detectability
Two commercial
assays
Does not predict
nonpregnancy
AFC (n) 3–10    9–73         73–100   8–33          64–100 Good Reliability
Widespread use
Low sensitivity
Inhibin B (pg/mL) 40–45   40–80         64–90    †                 -- Limited -- Reliability
Does not predict
nonpregnancy
CCCT, day 10 FSH (international units/L) 10–22   35–98         68–98   23–61          67–100 Limited Higher sensitivity
than basal FSH
Reliability
Limited additional
value to basal FSH
Requires drug
administration

Abbreviations: AFC, antral follicle count; AMH, antimüllerian hormone; CCCT, clomiphene citrate challenge test; FSH, follicle-stimulating hormone.

Note: Laboratories ELISA.

*Failure to conceive

†Insufficient evidence

Testing and interpreting measures of ovarian reserve: a committee opinion. Practice Committee of the American Society for Reproductive Medicine. Fertil Steril 2012;98:1407–15.

The concept of “ovarian reserve” defines a woman’s reproductive potential as a function of the number and quality of her remaining oocytes (1). The general purpose of ovarian reserve testing is to assess the quality and quantity of the remaining oocytes in an attempt to predict reproductive potential. The ideal screening test should be reproducible with low intercycle and intracycle variability and demonstrate high specificity to minimize the risk of a false-positive determination of decreased ovarian reserve in a woman with normal ovarian reserve (1). See Table 1 for a summary of the value of ovarian reserve screening tests and Table 2 for a list of recommended screening tests.

Available tests of ovarian reserve include biochemical markers (ie, FSH, estradiol, antimüllerian hormone, and inhibin B) and ovarian ultrasound imaging (ie, antral follicle count and ovarian volume). These screening tests have been best studied as predictors of specific in vitro fertilization (IVF) outcomes: oocyte yield from ovarian stimulation and rate of pregnancy (5). A common indicator of poor reproductive outcomes is low ovarian response to stimulation, usually defined as fewer than 3–5 developing follicles during an IVF cycle. It is important to recognize that a poor result from ovarian reserve testing does not signify an absolute inability to conceive and should not be the sole criteria considered to limit or deny access to infertility treatment (1). Although these tests are used to assess oocyte quantity and quality, the best surrogate marker for oocyte quality is age (6). At this time, ovarian reserve testing results cannot be extrapolated to predict the likelihood of spontaneous conception.

Table 2. Tests Recommended to Assess Ovarian Reserve
Test Details
FSH plus estradiol
  • Serum level on cycle day 2–3
  • Variation between cycles possible
  • High FSH value is associated with poor response to ovarian stimulation
  • Does not predict failure to conceive
AMH
  • No specific timing for the test
  • Stable value within and between menstrual cycles
  • Low AMH value is associated with poor response to ovarian stimulation
  • Does not predict failure to conceive
AFC
  • Number of visible follicles (2–10 mm) during transvaginal ultrasound
  • Performed on cycle days 2–5
  • Number of antral follicles correlates with ovarian response to stimulation
  • Does not predict failure to conceive
Abbreviations: AFC, antral follicle count; AMH, antimüllerian hormone; FSH, follicle-stimulating hormone.

The main goal of ovarian reserve testing is to identify those individuals who are at risk of decreased or diminished ovarian reserve, commonly known as DOR. There is no consensus on the definition of diminished ovarian reserve (7). However, compared with women of similar age, women with diminished ovarian reserve commonly have regular menses but a reduced quantity of ovarian follicles and, thus, may have a limited response to ovarian stimulation with fertility medications and reduced fecundity (probability of achieving a live birth in a single reproductive cycle). Female age and ovarian reserve test results are useful for discussing prognosis and recommending a treatment plan. Younger women with diminished ovarian reserve demonstrate reduced oocyte numbers but may have normal oocyte quality, whereas older women with normal ovarian reserve may have a good number of oocytes but an age-appropriate decrease in oocyte quality. Although ovarian reserve testing cannot predict the end of one’s reproductive years, results outside the range expected for a patient’s age can encourage the individual to pursue more aggressive treatment options to achieve pregnancy. Ovarian reserve testing should be performed for women older than 35 years who have not conceived after 6 months of attempting pregnancy and women at higher risk of diminished ovarian reserve, such as those with a history of cancer treatment with gonadotoxic therapy, pelvic irradiation, or both; those with medical conditions who were treated with gonadotoxic therapies; or those who had ovarian surgery for endometriomas (see Box 1). For general obstetrician–gynecologists, the most appropriate ovarian reserve screening tests to use in practice are basal FSH plus estradiol levels or antimüllerian hormone (commonly known as AMH) levels. An antral follicle count, commonly known as an AFC, also may be useful if there is an indication to perform transvaginal ultrasonography (Table 1). When test results suggest decreased or diminished ovarian reserve, if appropriate, an infertility evaluation should be initiated. Furthermore, it is reasonable to counsel the woman that her window of opportunity to conceive may be shorter than anticipated, and attempting to conceive sooner rather than later is encouraged. During the evaluation of infertility, factors such as female age, infertility diagnoses, and ovarian reserve test results are used to counsel the individual or couple about their prognosis and to formulate an appropriate treatment plan.

Biomarkers of Ovarian Response

Biochemical tests for ovarian reserve attempt to identify signs of ovarian aging that may signify changes in oocyte quantity and quality. These screening tests involve basal measurements and provocative tests. Basal measurements include assessments of FSH, antimüllerian hormone, and inhibin B. An example of a provocative test is the clomiphene citrate challenge test.

Box 1. Risk Factors for Diminished
Ovarian Reserve

  • Advanced reproductive age (older than 35 years)
  • Family history of early menopause
  • Genetic conditions (eg, 45,X mosaicism)
  • FMR1 (Fragile X) premutation carrier
  • Conditions that can cause ovarian injury (eg, endometriosis, pelvic infection)
  • Previous ovarian surgery (eg, for endometriomas)
  • Oophorectomy
  • History of cancer treated with gonadotoxic therapy or pelvic irradiation
  • History of medical conditions treated with gonadotoxic therapies
  • Smoking

Data from Testing and interpreting measures of ovarian reserve: a committee opinion. Practice Committee of the American Society for Reproductive Medicine. Fertil Steril 2012;98:1407–15; Gurtcheff SE, Klein NA. Diminished ovarian reserve and infertility. Clin Obstet Gynecol 2011;54:666–74; te Velde ER, Pearson PL. The variability of female reproductive ageing. Hum Reprod Update 2002;8:141–54; and Ferraretti AP, La Marca A, Fauser BC, Tarlatzis B, Nargund G, Gianaroli L. ESHRE consensus on the definition of ‘poor response’ to ovarian stimulation for in vitro fertilization: the Bologna criteria. ESHRE working group on Poor Ovarian Response Definition. Hum Reprod 2011;26:1616–24.

Basal Follicle-Stimulating Hormone

Follicle-stimulating hormone is released by the pituitary gland in response to gonadotropin-releasing hormone from the hypothalamus and is also subject to central negative feedback from estradiol and inhibin B. With normal ovarian function, a developing cohort of follicles secretes estradiol and inhibin B, which suppress FSH, keeping it in the normal range. In the setting of a smaller follicular cohort and decreased estradiol and inhibin B levels, an increase in pituitary FSH secretion occurs, which can be identified as an elevated early follicular phase FSH level. This higher FSH level stimulates rapid ovarian follicular growth, which results in higher estradiol levels as well as a shorter follicular phase and reproductive cycle.

With advancing reproductive age, basal serum FSH concentrations increase on days 2–4 of the menstrual cycle. However, because of the inherent variability of each reproductive cycle, the basal FSH level can vary, so a single FSH value has limited reliability (8). Moreover, there is variability among different FSH assays that further complicates the interpretation of a result. Although basal FSH commonly is used to assess ovarian reserve, and high values (greater than 10–20 international units/L) are associated with diminished ovarian reserve and poor response to ovarian stimulation, the test is not predictive of failure to conceive (9). If FSH values are consistently elevated, a poor reproductive prognosis is likely; in contrast, a single elevated FSH value in women younger than 40 years predicts a lower oocyte yield during IVF but does not affect the rate of pregnancy (10).

Basal Estradiol

Estradiol is released from the ovary during follicular development. The estradiol level is usually low (less than 50 pg/mL) on days 2–4 of the menstrual cycle but demonstrates some cycle-to-cycle variability. However, an elevated value (greater than 60–80 pg/mL) in the early follicular phase can indicate reproductive aging and hastened oocyte development. Through central negative feedback, a high estradiol level can suppress an elevated FSH concentration into the normal range, so the value of obtaining an estradiol level is that it allows the correct interpretation of a normal basal FSH level. Basal estradiol has low predictive accuracy for poor ovarian response and failure to conceive; therefore, this test should not be used in isolation to assess ovarian reserve (5).

Antimüllerian Hormone

Antimüllerian hormone is a glycoprotein hormone that is produced by the granulosa cells of primary, preantral, and antral follicles 2–6 mm in diameter; thus, it reflects the size of the primordial oocyte pool (6). Because early follicles secrete antimüllerian hormone in a gonadotropin-independent state, the antimüllerian hormone concentration is fairly stable within and between menstrual cycles (11). As the number of ovarian follicles decreases with age, a concomitant decrease in antimüllerian hormone levels occurs, which reflects this age-related oocyte depletion (12). Although an undetectable antimüllerian hormone level suggests diminished ovarian reserve and can identify individuals at risk of poor ovarian response to stimulation, undetectable and low antimüllerian hormone levels (0.2–0.7 ng/mL DSL ELISA) are not predictive of failure to conceive (13). Furthermore, antimüllerian hormone levels may allow treatment to be tailored to each individual. In vitro fertilization protocols take into consideration that lower antimüllerian hormone levels are associated with reduced ovarian response to stimulation, and high levels raise concern for a brisk ovarian response to stimulation (13). Although the level of antimüllerian hormone is a good predictor of oocyte quantity, it may not provide information about egg quality. Thus, young women with low antimüllerian hormone levels may have a reduced number of oocytes but normal, age-appropriate oocyte quality (14).

One limitation of antimüllerian hormone level testing is the variability of results between the available assays and the inability to compare antimüllerian hormone levels when different assays are used. Therefore, in clinical practice, individual antimüllerian hormone level test results must be interpreted based on the normal range of the assay used, and standard cutpoints may differ based on the assay (1). Antimüllerian hormone level testing is a useful screening test in women at high risk of diminished ovarian reserve and in women undergoing IVF but has limited benefits in someone at low risk of diminished ovarian reserve (1).

With further research, antimüllerian hormone level testing may become increasingly valuable in assessing ovarian reserve for young women with cancer (15). Measuring antimüllerian hormone levels before and after chemotherapy allows detection of differences in ovarian toxicity among chemotherapy regimens and may help evaluate long-term ovarian function (15, 16). Further research on antimüllerian hormone may enable assessment of ovarian reserve before and after ovarian surgery and for women at high risk of primary ovarian insufficiency; this research may provide an accurate method of predicting the reproductive lifespan and the timing of menopause (6).

Inhibin B

Inhibin B is a glycoprotein hormone that is secreted primarily by preantral and antral follicles. The serum concentration of inhibin B decreases with the age-related decrease in the number of oocytes. Inhibin B has central negative feedback that controls FSH secretion; therefore, a decrease in inhibin B levels leads to increased pituitary FSH secretion and higher early follicular FSH levels. However, there is significant variability in inhibin B levels between menstrual cycles. This marker does not reliably predict a poor response to ovarian stimulation and, thus, is not a recommended test (17).

Clomiphene Citrate Challenge Test

The clomiphene citrate challenge test is performed by measuring serum FSH on cycle day 3, administering 100-mg clomiphene citrate daily on cycle days 5–9, and again measuring serum FSH on cycle day 10. In women with a reduced number of ovarian follicles, lower estradiol and inhibin B production leads to less central negative feedback of FSH secretion and an elevated FSH level after clomiphene stimulation. Therefore, an elevated FSH level on day 10 of the clomiphene citrate challenge test is suggestive of diminished ovarian reserve. However, there is cycle-to-cycle variability in ovarian biomarkers (ie, estradiol, inhibin B, and FSH) during the clomiphene citrate challenge test, which limits the reliability of this provocative test (8). The stimulated FSH level on cycle day 10 of the clomiphene citrate challenge test is predictive of poor ovarian response but is not predictive of failure to conceive (18). Compared with the basal FSH level and the antral follicle count, the cycle-day-10 FSH level does not improve the prediction for poor ovarian response (18). Therefore, the use of this test to assess ovarian reserve is not recommended (18).

Home Fertility Tests

Available home fertility tests use a urine sample to assess the FSH level on cycle day 3. These tests are marketed directly to consumers and claim high accuracy in determining a woman’s ability to conceive. The limitations of these tests include misinterpretation of instructions and results and the unavailability of a medical professional to interpret and explain the results (1). Although these tests are used commonly by women at low risk of diminished ovarian reserve, the results may provide false reassurance or raise unnecessary concern.

Ultrasound Evaluation of Ovarian Reserve

Antral Follicle Count

The antral follicle count records the number of visible ovarian follicles (2–10 mm mean diameter) that are observed during transvaginal ultrasonography in the early follicular phase (cycle days 2–5). The number of antral follicles correlates with the quantity of remaining follicles and with the ovarian response during controlled ovarian stimulation, and good intercycle and interobserver reliability has been demonstrated (9, 17). A low antral follicle count is considered 3–6 total antral follicles and is associated with poor response to ovarian stimulation during IVF, but it does not reliably predict failure to conceive; in a meta-analysis, a low antral follicle count was a mean of 5.2 (2.11 standard deviation) total antral follicles (9). There are limited data on the predictive capacity of antral follicle count for IVF patients, so it should not be the sole criterion used to plan treatment (1). When antral follicle count was compared with age, basal FSH, basal estradiol, antimüllerian hormone, inhibin B, and ovarian volume, antral follicle count and antimüllerian hormone were the most significant predictors of poor response to ovarian stimulation but were not predictive of failure to conceive (17).

Ovarian Volume

The calculation of ovarian volume requires ovarian measurements in three planes and the use of the formula for the volume of an ellipsoid: D1 × D2 × D3 × 0.52. Some ultrasound software may calculate this value automatically. Mean ovarian volume, the average volume calculated for both ovaries from the same individual, is the value used to assess ovarian reserve. With age, changes in ovarian volume are concordant with the age-related decrease in ovarian follicles. Although ovarian volume correlates with ovarian response to stimulation, it does not predict failure to conceive (9). When screening for diminished ovarian reserve with imaging, ovarian volume has limited value compared with antral follicle count for detection of diminished ovarian reserve (1, 17).

Combined Ovarian Reserve Tests

A variety of biochemical and imaging techniques can be used to evaluate ovarian reserve. Because no single assessment of ovarian reserve has 100% sensitivity and specificity, tests often are combined in an attempt to improve the prediction of poor outcomes. Antimüllerian hormone and antral follicle count are the most accurate predictors, but combinations of a few tests are only slightly better than a single test. Because of the heterogeneity of the tests and cutpoints used in research studies, models of combined ovarian reserve tests do not significantly improve the ability to predict poor reproductive outcomes over single ovarian reserve tests (1). Furthermore, the use of multiple ovarian reserve tests may complicate the understanding of an individual’s ovarian reserve and increase the expense of screening. Further research is needed to determine an optimal combination of tests. An improved understanding of the genetic basis of ovarian aging may enable the development of a panel of genetic tests for routine screening for ovarian aging.

Conclusion

The primary goal of ovarian reserve testing is to identify women at risk of decreased or diminished ovarian reserve (see Box 1 for a list of risk factors), with a secondary goal of individualizing treatment strategies for each woman. Although these tests may predict ovarian response to infertility treatment, they do not reliably predict failure to conceive (1, 5). See Table 2 for a list of recommended tests.

References

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Ovarian reserve testing. Committee Opinion No. 618. American College of Obstetricians and Gynecologists. Obstet Gynecol 2015;125:268–73.

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