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Optimal cutoff value of basal anti-mullerian hormone in iranian infertile women for prediction of ovarian hyper-stimulation syndrome and poor response to stimulation

Aghssa et al. Reproductive Health (2015) 12:85 DOI 10.1186/s12978-015-0053-4 Optimal cutoff value of basal anti-mullerianhormone in iranian infertile women forprediction of ovarian hyper-stimulationsyndrome and poor response to stimulation Malek Mansour Aghssa1, Azam Manshadi Tarafdari1*, Ensieh Shahrokh Tehraninejad1, Mohammad Ezzati2,Maryam Bagheri1, Zahra Panahi1, Saeed Mahdavi3 and Mehrshad Abbasi4 Aim: We intended to establish the threshold of Anti-Mullerian Hormone (AMH) for detection of OvarianHyper-Stimulation Syndrome (OHSS) and poor response to treatment in Iranian infertile women.
Methods: Pre-stimulation menstrual cycle day-3 hormonal indices including basal AMH values were measured in105 infertile women aged 32.5 ± 4.3 years. Patients underwent long GnRH agonist Controlled Ovarian Hyperstimulation(COH) in a referral infertility center (Tehran, Iran). The gonadotropin dose was determined based on the age and basalserum Follicular Stimulating Hormone (FSH) level. The IVF/ICSI cycles were followed and the clinical and sonographicdata were recorded.
Results: Sixteen cases developed OHSS. The prevalence of PCOS was higher in subjects with OHSS [62.5 %(38.8-86.2) vs. 17 % (9.2-24.9)]. The patients with OHSS had higher ovarian follicular count [23.7 (3.2) vs. 9.1 (0.5);p < 0.05], collected oocytes [13.5 (1.9) vs. 6.9 (0.5); p < 0.05] and AMH level [7.9 (0.7) vs. 3.6 (0.3); p < 0.05]. BasalAMH level and oocyte yields (but not age, BMI, and PCOS) correlated with occurrence of OHSS; and only the AMHlevels were associated with poor ovarian response (oocytes yield ≤ 4). The optimal cutoff value for the predictionof OHSS was 6.95 ng/ml (area under the receiver operating characteristics curve: 0.86; CI: 0.78-0.95; sensitivity: 75 %;specificity: 84 %; odds ratio for occurrence of OHSS: 9 and p < 0.001). The optimal cut point to discriminate poorresponse (oocytes ≤4) was 1.65 ng/ml ( AUC : 0.8; CI: 0.69-0.91; sensitivity: 89 % specificity : 71 %; and OR = 23.8and P value <0.001).
Conclusions: Iranian women with basal AMH level > 6.95 ng/ml are at high risk of developing OHSS and thosewith AMH level < 1.65 ng/ml are poor responders.
Keywords: Assisted Reproductive Technology, Ovulation induction, Ovarian hyper-stimulation syndrome,Anti-mullerian hormone * Correspondence: 1Vali-e-Asr Reproductive Health Research Center, Department of Obstetricsand Gynecology, Valiasr Hospital, Tehran University of Medical Sciences,1419433141 Tehran, IranFull list of author information is available at the end of the article 2015 Aghssa et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium,provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver applies to the data made available in this article, unless otherwise stated.
Aghssa et al. Reproductive Health (2015) 12:85 of the gonadotropin and diagnosed and managed OHSS Anti-Mullerian Hormone (AMH) is a granulosa cell irrespective of patients' participation in the study. The fol- derived hormone secreted from pre-antral and small an- licle count (≥14 mm) based on sonographic examination tral follicles. AMH substantially inhibits the initiation of on the day of HCG administration, the number of re- primordial follicle growth and contributes to normal trieved oocytes, and the final outcome of the IVF/ICSI folliculogenesis by enhancing the role of FSH in cyclic cycle were recorded.
recruitment of follicles Clinically, AMH can serve asa reliable ovarian reserve marker independent of go- Controlled ovarian hyperstimulation protocol nadotropins levels A particularly helpful aspect of Participants were recruited among those who underwent AMH, when used as an ovarian reserve marker, is that long GnRH agonist protocol irrespective of age, gonado- its serum levels remain relatively constant during normal tropin dosage, and history of OHSS or antral follicular menstrual cycles The reported variability during count. From day 21 of the pre-stimulation menstrual the menstrual cycles is not possibly clinically influential cycle, the patient received a daily subcutaneous injection In 2002, Seifer et al. underscored the association of of Boucerelin acetate (Superfact, Hoecht AG, Frankfurt, AMH levels with ovarian response to Controlled Ovar- Germany). The gonadotropin (GonalF, Serono, Switzerland) ian Hyperstimulation (COH) The recent meta- was added on day 2 or 3 of the IVF/ICSI cycle. Dosing analysis by Broer et al. highlighted 9 studies employing was determined by the chief treating gynecologist of the AMH to predict excessive responses during COH center mainly based on the age and basal FSH levels While the ability to predict excessive ovarian stimulation (ranged between 150 and 225 IU/day). Dosage of gonado- using basal AMH values is established, the optimal tropin was adjusted based on the degree of ovarian re- threshold of AMH to predict Ovarian Hyper-Stimulation sponse in interval sonographic examinations (data not Syndrome (OHSS) is controversial and subjected to this collected for this report). Patients were examined by daily trans-vaginal sonography starting on day 7 of stimulation.
HCG (250 mgr; Ovitrelle, Merck, Serono) was injec- ted subcutaneously when the sonographic examination A total of 105 infertile couples undergoing COH enrolled showed a minimum of two 18 mm follicles. Oocyte in this study. They were visited in a private referral infer- pickup was performed from posterior vaginal fornix tility center (Tehran, Iran) between March 2010 and 34 to 36 hours after HCG administration. Embryo February 2011. Subjects with any known systemic diseases was transferred within 2 days of oocyte pickup and or endocrine disorders including diabetes, hypothy- the patient received 400 mg of cyclogest (Alpharma, roidism, hyper-prolactinemia, and those who were receiv- Barnstaple, UK) every 12 hours during the first ing levothyroxine or cabergoline were excluded. Data of 12 weeks of gestation and 2 mg of estradiol valereate the first attempt was recorded for the patients who under- every 12 hours for 2 weeks. Serum βHCG was mea- went more than one IVF/ICSI cycle. The corresponding sured 15 days after embryo transfer. Biochemical demographic and infertility related data of the participants pregnancy was defined as βHCG value > 50 mIU/ml.
were collected and the baseline pre-stimulation AMH, Sonographic examination was performed 2 weeks later FSH, LH, testosterone, dehydroepiandrosterone sulfate, to confirm the presence of gestational Sac and then TSH, and prolactin plasma levels were measured on the 2 weeks afterward to confirm viability of the embryo.
third day of the previous menstrual cycle. Pre-stimulation The OHSS related symptoms and signs, including cycle(s) was/were induced in those without regular men- abdominal distension and discomfort, nausea, vomiting, ses with intramuscular injection of 100 mg progestron in diarrhea, ascites, plural effusion, edema, oliguria, hyper- oil (Iran Hormone, Tehran, Iran) and maintained with coagulative state, serum creatinine of 1.0-1.5 mg/ml, daily OCP from day 3 in those without history of regular hemoconcentration, and electrolyte imbalance were moni- menses after withdrawal bleed. Serum AMH was mea- tored. Suspected OHSS cases were examined by sonog- raphy to determine ovarian enlargement and ascites ].
Ireland, Inc., Galway, Ireland) with functional sensitivity of OHSS and the severity of the condition were defined ac- 0.2 ng/ml and intra and inter-assay coefficient of variabil- cording to the Navot et al. []. Those patients experien- ity of 8 and 12 %, respectively. Samples were centrifuged cing OHSS were managed by cycle cancellation, coasting, and the assays were done in serums after performing cali- or freezing the embryo for future IVF cycles with or with- brations according to the manufacturer instructions.
out additional cabergoline (dostinex) therapy.
Samling of the hemolyzed samples were repeated and no The ethical committee of the Faculty of Medicine particular strategy for handling Heterophile antibody was (Tehran University of Medical Sciences) approved the employed. The chief gynecologist of the center (i.e.
study and waved the need for written informed consent.
MMA) selected the stimulation protocol, type, and dose The data was handled and analyzed anonymously.
Aghssa et al. Reproductive Health (2015) 12:85 skewed. For the parametric tests the square root of the Independent sample T-tests and Chi square tests were AMH values was generated and employed (Kolmogorov- used to compare correspondingly the difference of con- Smirnov's P value of transferred data = 0.39).
tinuous values and the prevalence of categorical vari-ables between subjects with and without OHSS. A binary logistic regression model (enter method) was de- The subjects' characteristics are shown in Table Basal signed to study the multivariate correlation of OHSS AMH level as well as ovarian follicle and collected with age, BMI, basal biochemical indices (including oocytes counts but not age and BMI were higher in the AMH), sonographic findings (follicle count), and clinical subjects with OHSS. The mean basal AMH value of the outcomes (retrieved oocytes). Additionally, a univariate 105 studied cycles was 4.2 ng/ml [SD: 3.3, median: 3.5, general linear model (enter method) was employed to inter-quartile range: 1.4-7.0, range: 0.05-15.0]. Sixteen adjust the effect of covariates on the association of patients presented with moderate or severe OHSS OHSS and AMH level. Finally, a receiver operating char- (15.2 %) out of whom 4 cycles were canceled, oocytes acteristics (ROC) curve was created to classify subjects were collected for subsequent IVF attempts in 7 cases with and without OHSS according to AMH levels. Two (with additional dostinex therapy in one patient), ovula- different approaches were assessed to determine the op- tion induction was coasted in 2 patients (with additional timal cutoff value of AMH to classify OHSS: Youden dostinex therapy in one patient), and two subjects were index which is the maximum sensitivity - (1-specificity) treated with dostinex alone. Two cases with severe and the shortest distance on the ROC from the optimal OHSS were managed in the hospital setting. Forty-two sensitivity and specificity [(1 - sensitivity)2 + (1 - specifi- (40 %; CI: 30.6-49.4 %) IVF/ICSI cycles led to clinical city)2] [Sensitivity, specificity, positive likelihood pregnancies and 37 (35.2 %; CI: 26.1-44.4 %) live births.
ratio [PLR; sensitivity / (1 - specificity)], and negative The subjects with OHSS had a clinical pregnancy rate of likelihood ratio [NLR; (1 - sensitivity) / specificity] of the 3/16 in the studied cycles with only 2 live births both in cutoffs were also calculated A binary logistic re- subjects treated with dostinex alone. In 4 patients (25 %) gression model was also designed to predict poor re- the OHSS occurred early and severely enough to prevent sponse to stimulation with different variables including oocyte collection and 2 patients, out of 89 subjects AMH level. The response to stimulation was defined (2.2 %), without OHSS had no oocytes yield.
poor ≤4 collected oocytes or good > 4 collected oocytes Twenty-five subjects (23.8 %; CI: 15.7-32.0 %) had in this model.
PCOS with higher prevalence of OHSS (40 % vs. 7.6 %; The AMH values were not normally distributed p < 0.001), younger age [30.5(0.7) vs. 33.3 (0.5); p = (Kolmogorov-Smirnov's P value <0.001) and were positively 0.005] and higher basal AMH levels [7.1(0.7) vs. 3.3(0.3); Table 1 The characteristics of the subjects with and without ovarian hyper-stimulation syndrome Subjects without OHSS n = 89 Subjects with OHSS n = 16 Duration of infertility (yrs) Duration of stimulation (days) Number of follicles (HCG day) Number of retrieved oocytes Basal Anti-mullerian Hormone Basal Luteinizing Hormone Basal Follicle stimulating Hormone Thyroid stimulating hormone Basal Testosterone Polycystic ovary syndrome Clinical pregnancy Data are mean or percentages and standard error from the mean or 95 % confidence intervals in the parentheses.
† indicates significant difference between the values of subjects with and without ovarian hyper-stimulation syndrome (T-test or Chi squared test; p < 0.05).
Aghssa et al. Reproductive Health (2015) 12:85 p < 0.001]. Their pregnancy rate, however, was not statis- The total administered gonadotropin dose (but not tically different from other patients [28(10.4-45.6) vs.
total days of stimulation) correlated inversely with the 44.3(33.3-55.3); p = 0.1].
OHSS occurrence (OR for every additional 75 inter- The binary logistic regression model was designed national unit = 0.8, CI: 0.7-0.9; p = 0.002).
with age, BMI, number of previous OSCs, PCOS, FSH After adjustment for the effect of age, BMI, and PCOS; level, number of retrieved oocytes, and basal AMH level the AMH values were higher in the subjects with (square root) as independent variables to predict the consequent OHSS than in those without OHSS [7.7 OHSS (dependent variable). The number of retrieved (0.7) ng/ml vs. 4.7(0.4) ng/ml; df = 5, F (11.9) = 14.2, oocytes [OR: 1.3(95 CI: 1.1-1.6), Wald: 8.0, and P = eta2 = 0.1; P = 0.001]. No significant interaction effect 0.004] and basal AMH value [OR: 5.4 (95 CI: 1.1-27.9), was detected for the presence of PCOS on the asso- Wald: 4.1, and P = 0.04] (but not PCOS, age, and BMI) ciation of AMH levels and OHSS [F (11.9) =2.4 and were significant independent predicting factors of OHSS.
The square root of basal AMH levels were moderately AMH levels classified subjects with and without OHSS correlated with the number of retrieved oocytes (r = 0.5; with an area under the ROC curve (AUC) of 0.86 (0.78- p < 0.001). Another model was defined with follicle 0.95; Fig. the best AMH cutoff value to predict OHSS count instead of collected oocytes count (considering was 6.95 ng/ml (sensitivity: 75 %, specificity: 84 %, PLR: significant co-linearity). In this model, in addition to 4.7, NLR: 0.3; Fig. panel a). Patients with AMH values AMH level the follicle count was significantly associated higher than 6.95 ng/ml experienced a higher frequency with OHSS [OR: 1.5 (95 CI: 1.1-1. 9), Wald: 8.9, and of OHSS (5.1 % vs. 46.2 %; OR = 9, CI: 1.3-59.7, Chi2 P P = 0.003]. A binary logistic regression model was de- value < 0.001). In subjects without OHSS, those with fined with independent variables identical to those of AMH values over 6.95 (n = 14) compared to those with the previous models excluding collected oocyte or fol- AMH levels below 6.95 received significantly smaller licle counts. AMH level (square root) was the only gonadotropine doses per day [157 (17) IU vs. 197 (46); predictor of the response to stimulation [OR: 0.25 (95 p < 0.005] with higher collected oocytes [9.4 (1.0) vs. 6.4 CI: 0.11-0.59), Wald: 10.3, and P = 0.001].
(0.5); p < 0.05] and the equal follicle count [11.1 (0.7) vs.
Fig. 1 Age adjusted anti-mullerian hormone is higher in those with consequent ovarian hyper-stimulation syndrome in patients with and withoutpolycystic ovary syndrome Aghssa et al. Reproductive Health (2015) 12:85 Fig. 2 The Receiver Operating Characteristics (ROC) curves of basal anti-mullerian hormone values to predict ovarian hyper-stimulation syndrome.
AURC: Area Under the ROC Curve 8.7 (0.7); p < 0.067]. The cutoff value of AMH with the responders to ovarian stimulation (post-test probability: best prediction of poor response to controlled ovarian 75 %; OR = 23) and those with AMH levels >6.95 stimulation (oocytes ≤4) was 1.65 ng/ml with AUC of (almost the upper quartile) are at a higher risk for OHSS 0.8 (0.69-0.91) and sensitivity and specificity of 89 % (post-test probability: 46 %; OR = 9). With subclass ana- and 71 %, respectively (Fig. panel b). A poor response lysis of the administered gonadotropin dose, we suggest rate in those with an AMH value below and above that milder ovarian stimulation in high risk patients has the cut point (1.65) was 75 % and 13.7 %, respectively no detrimental effect on the COH main outcome (re- (OR = 23.8, CI: 6.0-94.1, Chi2 P value <0.001). The trieved oocyte count). Thus, we believe that based on cut points for detection of OHSS and poor response the proposed cut point of basal AMH levels (i.e. 6.95; were substantially the same after exclusion of subject roughly the upper quartile), reduced stimulation would with PCOS (data not shown).
be a safe and the reasonable method of preventing No significant association was found between basal OHSS and its consequences. This approach may decrease AMH level and the outcome of the IVF/ICSI procedure the severe OHSS cases with its unfavorable consequences (clinical pregnancy vs. failed cycle).
including hospitalization and cycle cancellation Afteradjustment for AMH levels, other pre-stimulation vari- ables including age, BMI, and PCOS did not correlate with Our results indicate an association between extreme OHSS or poor response to COH.
AMH levels and OHSS and poor response to controlled Our optimal cutoff value of AMH for the prediction of ovarian stimulation independent of the effect of age, OHSS is higher than the cut points suggested by previ- BMI, and a history of PCOS. According to our findings, ous studies (i.e. 1.6 ng/ml 2.1 ng/ml 3.4 ng/ml subjects with an AMH level <1.65 (almost the lower 3.5 ng/ml ] and 4.8 ng/ml Our results quartile of AMH values) are more likely to be poor are in line with the result of La Marca et al. with

Aghssa et al. Reproductive Health (2015) 12:85 Fig. 3 Sensitivity, specificity, Yuden index and distance to the optimal point on the ROC curve for the basal anti-mullerian hormone levels topredict ovarian hyper-stimulation syndrome (panel a) and poor response to the IVF cycle (panel b). Arrows indicate the most effective thresholdvalue of AMH (6.95 and 1.65 ng/ml for ovarian hyper-stimulation syndrome and poor response to ovarian stimulation, respectively) correspondingto both maximum Youden index and shortest distance on the ROC curve cutoff value of 7 ng/ml (75th percentile) for the classifi- []. Generally there is good correlation between the new cation of exaggerated responses. The threshold value of (i.e. Beckman-Coulter) and old AMH assay kits .
the study by Lee et al. was numerically lower but again In our study 15 % of cases had moderate to severe it was the 75th percentile of the AMH values of the stud- OHSS. Moderate OHSS is reported in 1 to 14 % of sub- ied population. Ebner et al. also reported the best jects with less than 1 % severe OHSS cases We had ovarian response was achieved when the basal AMH higher frequency of diagnosed OHSS compared to the value was between the 25th and 75th percentiles with studies by Lee et al. (8 %), Nardo (10 %) and Aramvit reduced oocyte quality of patients in the top quartile et al. (12 %). Nevertheless, the prevalence of severe cases (AMH level > 4.5 ng/ml). The cutoff point suggested by leading to hospitalization was relatively low . The Nardo et al. (3.5 ng/ml) is presumably the upper quartile risk of excessive ovarian response is a function of the of non-PCOS normal responders to COH. The differ- COH protocol and the health characteristics of the par- ences between the AMH thresholds for higher OHSS ticipants (including age and the prevalence of PCOS).
risk noted in this study as compared to other studies One may expect to encounter less exaggerated responses may be explained by the differences between the studied in the short COH protocols and in populations with populations (age, threshold for treatment of infertility, or lower PCOS. The prevalence of PCOS was high among frequency of PCOS), the definition of OHSS, and the the infertile population of this study (i.e. 23.8 %). The different AMH measurement methods. Roughly - also prevalence of PCOS among subjects undergoing COH not limited by the remarkable difference between the varies from 4 to 22 % The risk of OHSS in AMH readings of two older ELISA kits i.e. DSL and our study was dramatically high in patients with PCOS Immunotech - the patients with upper quartile AMH (40 %), which is consistent with the study by Aramvit values are at high risk for exaggerated ovarian response et al. in which about 45 % of the PCOS subjects Aghssa et al. Reproductive Health (2015) 12:85 experienced OHSS Interestingly the incidence of Washington Hospital Center, Washington, DC, USA. 3Saeed Medical OHSS associated with AMH high levels independent of Laboratories, Tehran, Iran. 4Department of Nuclear Medicine, Valiasr Hospital,Tehran University of Medical Sciences, Tehran, Iran.
the diagnosis of PCOS. Also after adjustment for the ef-fect of AMH there was no correlation between PCOS Received: 2 August 2014 Accepted: 4 July 2015 The clinical pregnancy rate was comparable and rather high in our study (40 %) as compared with the results of Nardo et al. (24 %) ], Kini et al. (34 %) ], and Lee Tremellen KP, Kolo M, Gilmore A, Lekamge DN. Anti-müllerian hormone as a et al. (41 %) . Relatively higher pregnancy rates ac- marker of ovarian reserve. Aust N Z J Obstet Gynaecol. 2005;45:20–4.
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