Colour Doppler ultrasound in controlled ovarian stimulation with Intrauterine Insemination
 

Colour Doppler ultrasound in controlled ovarian stimulation with Intrauterine Insemination

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To assess the endometrial receptivity in terms of endometrial thickness and vascularity and to assess the ...

To assess the endometrial receptivity in terms of endometrial thickness and vascularity and to assess the
potential relationship between perifollicular vascularity following ovulation inducing drugs and outcome in intrauterine insemination (IUI) using the Doppler ultrasonography.

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    Colour Doppler ultrasound in controlled ovarian stimulation with Intrauterine Insemination Colour Doppler ultrasound in controlled ovarian stimulation with Intrauterine Insemination Document Transcript

    • Colour Doppler Ultrasound in Controlled Ovarian Stimulation with Intrauterine Insemination
    • Apollo Medicine 2012 September Volume 9, Number 3; pp. 252e262 Case Report Colour Doppler ultrasound in controlled ovarian stimulation with intrauterine insemination Kavita Bhadauriaa,*, Reeti Sahnib, Sohani Vermab, Payal Q. Khatric ABSTRACT Aim: To assess the endometrial receptivity in terms of endometrial thickness and vascularity and to assess the potential relationship between perifollicular vascularity following ovulation inducing drugs and outcome in intrauterine insemination (IUI) using the Doppler ultrasonography. Materials and methods: Infertile couple in our hospital was subjected to colour Doppler ultrasound examination and the parameters were tabulated and analysed in terms of pregnant and not pregnant. Results: There were 23 pregnancies out of 100 cycles. The endometrial receptivity has a significant role in predicting successful outcome with thicker endometrium, multifocal zone 3/4 vascularity and with distinct five line appearance. The pregnancy rate was higher with grade 4 perifollicular vascularity. Copyright © 2012, Indraprastha Medical Corporation Ltd. All rights reserved. Keywords: Colour Doppler, Controlled ovarian stimulation, Intrauterine insemination, Endometrial receptivity, Perifollicular vascularity INTRODUCTION Infertility in today’s world has reached almost epidemic proportion with the treatment modalities and options developing almost compulsorily at exponential rates. Both IUI (intrauterine insemination) and IVF (in vitro fertilization) are now practiced in reasonably large numbers at most reported infertility centres. Intrauterine insemination (IUI) with or without controlled ovarian stimulation (COS) is a popular modality for treatment of subfertility. Although considerable discussion and debate have appeared in western literature regarding the utility of COS and IUI, lately the National Institute of Clinical Excellence (NICE), UK has revised the evidence for assessment and treatment of infertile couples and has recommended that IUI should be offered to couples with infertility because it is as effective as IVF, less invasive and requires fewer resources.1 The use of gonadotrophins in IUI is now widespread, and has been shown to improve significantly the odds of pregnancy. However, significant risks of ovarian hyperstimulation syndromedand in particular multiple pregnanciesdremain.2 Despite this, IUI has significant cost savings and is less invasive, without necessarily a reduction in effectiveness, compared with other forms of assisted reproduction treatment such as IVF or gamete intra-fallopian transfer (GIFT) in particular for non-tubal infertility.3 The rationale put forward in support of COS and IUI is that ovarian stimulation corrects subtle, unpredictable ovulatory dysfunction and there is increased probability of conception if increased density of motile spermatozoa is placed closer to multiple fertilizable oocytes.1 With the progressive standardization of these techniques it also becomes imperative to develop parameters to predict suitability and thus the success of the procedure. As in most gynaecological condition, sonography and Doppler are a Resident, bSenior Consultant, cAssociate Consultant, Department of Radiodiagnosis and AARU, Indraprashta Apollo Hospitals, New Delhi 110076, India. * Corresponding author. email: drkbhadauria@gmail.com Received: 14.5.2012; Accepted: 4.7.2012; Available online: 13.7.2012 Copyright Ó 2012, Indraprastha Medical Corporation Ltd. All rights reserved. http://dx.doi.org/10.1016/j.apme.2012.07.014
    • Colour Doppler ultrasound in controlled ovarian stimulation Case Report 253 Fig. 1 Longitudinal scans showing endometrial patterns. (a and b) Hazy five line appearance. powerful tools. Goswamy and Steptoe4 were the first to suggest that abnormal uterine artery blood flow might be associated with infertility and to develop a classification of uterine artery blood flow waveforms. Subsequently, other authors have confirmed a relationship of uterine and ovarian blood flow to unexplained infertility,5,6 and to successful implantation following IVF.7e10 Power Doppler or colour ultrasonography has been generating increasing clinical interest since its introduction.11 Despite the fact that the application of power Doppler in gynaecology remains in its infancy, recent studies suggest potential applications especially in relation to the assessment of uterine and perifollicular vascularity12,13 and outcome in IVF treatment cycles. Statistical models have been reported for predicting success rates in IUI which suggested that follicle number, endometrial thickness, duration of subfertility and semen parameters were the most significant variables in predicting outcome.14 The application of Doppler ultrasound in IUI has tended to relate uterine perfusion to outcome and few data exist on ovarian vascularity in these treatment cycles.15 This study was thus designed to collect statistically significant data in large numbers for IUI so as to achieve superior results and outcome. MATERIALS AND METHODS The cycles of ovarian-stimulationeintrauterine insemination (COSeIUI) treatment in infertile couples presenting to Apollo Assisted Reproduction Unit (AARU), from June 2009 to December 2010 were screened in our study. These patients were subjected to inclusion and exclusion criterias and 100 COSeIUI cycles were then analysed and assessed for the successful outcome of pregnancy. Inclusion criteria Women aged <42 years, primary or secondary infertility lasting for at least 12 months, tubal patency assessed by hysterosalpingography and/or laparoscopy with chromosalpingography, with at least one patent fallopian tube, normal semen analysis. Exclusion criteria Patients with coexisting disease such as bilateral tubal block, congenital uterine anomalies which are liable to affect outcome, associated male subfertility and infertility, patients who were started on ovulation induction regime Fig. 2 Longitudinal scans showing endometrial patterns. (a and b) Distinct five line appearance.
    • 254 Apollo Medicine 2012 September; Vol. 9, No. 3 Bhadauria et al. Fig. 3 Longitudinal scans showing endometrial patterns. (a and b) Thin endometrium with no layering. but were not subjected to IUI due to inappropriate follicular growth (follicular size less than 16 mm till 22nd day of the cycle) were excluded from our study, patients with multiple dominant follicles (four or more) were excluded from our study considering the risk for multifetal pregnancies. Ultrasound examination was carried out in all patients in each cycle of COSeIUI at day 2 (baseline). Each patient was informed and written consent was taken for COSeIUI as well as for colour Doppler US evaluation in addition to routine follicular monitoring US protocol. Patients were examined in lithotomy position and transvaginal ultrasound evaluation was done using transvaginal probe of 8 Hz (E8C). All studies were performed by a single operator on LOGIC 5 PRO (GE Healthcare) ultrasound machine. On day 2 of menstrual cycle, all patients were subjected to baseline US. The uterus was screened for endometrial lining (thickness and pattern), echogenicty of myometrium (fibroids, adenomyosis, past myomectomy). The uterine imaging was done to rule out congenital anomalies if any. The ovaries were evaluated to rule out presence of cysts, number of antral follicles in either ovaries. The Doppler US was done to evaluate the uterine and intraovarian arterial impedance as described below. On day 7, the patients were evaluated for follicular and endometrial growth and were examined thereon every alternate day till the follicle reached the size 14 mm or more and then everyday till ovulation. Patients were subjected to 5000 units of HCG administration intravenously when one or more follicles attained the size >16 mm and endometrial thickness was >7 mm. The IUI was done 48 h (or 24 h if follicle was ruptured earlier) after the HCG administration. Doppler US was carried and various parameters were recorded as described on subsequent patient visits. For colour and power Doppler study, the pulse repetition frequency (PRF) and wall filters were set at the lowest possible frequencies. We used wall filter 40 Hze75 Hz for evaluating low resistance intraovarian and endometrial vessels. The wall filters were 60 Hze115 Hz for evaluating the ascending branches of both uterine arteries. The pulse repetition frequency (PRF) was 45e60 Hz. The uterus was screened for 1) Size and configuration to rule out congenital anomalies if any. 2) The endometrium was evaluated for: Thickness of endometrium i) Measured from the myometrialeendometrial junction to the endometrialemyometrial junction in sagittal plane. ii) Layering of endometrium (endometrial echogenic pattern), distinct five line appearance, hazy five line appearance, or no layering (Figs. 1e3). iii) Endometrial blood flow The endometrial and periendometrial areas are divided into the following four zones16,17 (Figs. 4 and 5). Zone 1 e a 2 mm thick area surrounding the hyperechoic outer layer of the endometrium Zone 2 e the hyperechoic outer layer of the endometrium Zone 3 e the hypoechoic inner layer of the endometrium Zone 4 e the endometrial cavity 3) Uterine arteries. The ascending branches of both uterine arteries were examined at lower uterine segment and Doppler parameters were recorded as (Fig. 6): Fig. 4 Endometrial zones of vascularity.
    • Colour Doppler ultrasound in controlled ovarian stimulation Case Report 255 Fig. 5 Zone 3/4 endometrial vascularity with (a) sparse and (b) multifocal vascularity. i) ii) iii) iv) Peak systolic velocity (PSV) End diastolic velocity (EDV) Pulsatility index (PI) Resistive index (RI) THE FOLLICLES The number of dominant follicles (>16 mm) in each COSeIUI cycle were recorded and each follicle was assessed for perifollicular vascularity (Fig. 7). When more Fig. 6 Different waveforms of uterine artery. (a) Normal waveform with characteristic early diastolic notch with high PI value in (a) and low PI in (b). (c) Absent early diastolic flow and (d) absent diastole flow.
    • 256 Apollo Medicine 2012 September; Vol. 9, No. 3 Bhadauria et al. Fig. 7 (a) Normal ovary on base day 2, (b) follicular diameter measured in two perpendicular planes, (c) showing dominant follicle with cumulus oophorus (arrow), (d) rt ovary showing multiple3 follicles. than one follicle was observed, grading was performed for all of them, and the highest vascularity grade was recorded. The vascularity of each follicle was subjectively graded using Power Doppler imaging (according to the grading system by Chui et al, 1997)13 (Fig. 8). Grade 1: 25% of the circumference; Grade 2: 26e50%; Grade 3: 51e75%; Grade 4: >75%. THE OVARIES The intraovarian arterial supply was studied in the periovulatory and periluteal phase. The intraovarian arterial Doppler indices were recorded as (Fig. 9) i) Peak systolic velocity (PSV) ii) End diastolic velocity (EDV) iii) Pulsatility index (PI) iv) Resistive index (RI). RESULTS AND ANALYSIS (TABLE 1) A total of 100 women undergoing consecutive COSeIUI CYCLES were analysed in our study. There were 23 pregnancies with pregnancy rate being 23%. The youngest patient was 20 years old, with 2 years duration of infertility. The eldest female was 41 years old with 10 years of infertility. Twenty-three pregnant patients, 13 patients had endometrial thickness 8e10 mm, eight patients had endometrial thickness 10e12 mm, one patient had endometrial of 8 mm. We found significant relation between endometrial thickness and pregnancy rates, highest (42%) with endometrial thickness ranging from 10 to 12 mm (p < 0.05). However not all pts with thicker endometrium had positive outcome. In case endometrial thickness was 6e8 mm, it showed a significantly lower rates of pregnancy (p < 0.01). Correlation: Pearson coefficient between endometrial thickness and pregnancy is 0.31, it is a positive correlation which suggest that more the endometrial thickness more the pregnancy rate.
    • Colour Doppler ultrasound in controlled ovarian stimulation Case Report 257 Fig. 8 Grades of perifollicular vascularity (a)-grade 1 (<25% of circumference) (b)-grade 2 (25%e50%) (c)-grade 3 (50%e75%) (d)grade 4 (>75% of circumference). There is significant correlation between pregnancy rate and endometrial vascularity. Of 16 patients with multifocal vascularity in zone 3/4, 14 patients (88%) had positive outcome (highly significant p < 0.001). Whereas only 22% (9 out of 41) patients had conception with sparse vascularity in zone 3/4. No conception was reported in women having zone 1/2 endometrial vascularity (highly significant p < 0.001, significantly lower chances of pregnancy if in zone 2). Statistically higher pregnancy rate (40%) was reported in women with distinct five line appearance (p < 0.05). Patients with no endometrial layering had poor pregnancy rate (6%) and 19% pregnancy was seen with hazy five line appearance. Lesser the uterine artery impedance, more the number of pregnancies reported. No pregnancy was reported in women when uterine artery impedance PI was more than 2.99 (statistically significant p < 0.05). There was no significant difference in pregnancy rates when uterine arterial PI was low, 36% when PI was <2.19, 29% when PI was 2.2e2.49, 32% when PI was 2.5e2.75 and 13% with PI 2.75e2.99 (not significant > 0.05). The median number of pre-ovulatory follicles (>17 mm in diameter) on the IUI day among the pregnant patents was 2 (Æ1.6) and in non-pregnant cases was 1.79 (Æ1.2). In cycles with a single pre-ovulatory follicle (>17 mm in diameter) the pregnancy rate (17%) was significantly lower than in cycles with more follicles (35% and 36% respectively with two or three dominant follicles). The perifollicular vascularity was associated with better pregnancy rate. No pregnancy was achieved with perifollicular vascularity with grade 1 and grade 2 (which is highly significant p < 0.001). The pregnancy rate was 19% with grade 3 perifollicular vascularity (not significant) and was 68% with grade 4 perifollicular vascularity (which is highly significant p < 0.001). DISCUSSION Many studies have been conducted to evaluate the role of various ultrasound parameters in predicting pregnancy during ART18e20 but little information exists in the literature with regard to their role in predicting subsequent pregnancy outcomes.21 Our study was attempted to assess the prognostic uterine and ovarian IUI variables with regard to successful outcome (pregnant/non-pregnant) using colour Doppler transvaginal ultrasound so that the outcome
    • 258 Apollo Medicine 2012 September; Vol. 9, No. 3 Fig. 9 Intraovarian waveform pattern (a) In proliferative phase, and (b) In secretory phase. of subsequent COSeIUI cycles could be more accurately predicted than before. In our study pregnancy occurred in 23 patients (23%) of total 100 infertility COSeIUI cycles. In Mehrafza et al study undertaken on 336 IUI cycles, the overall pregnancy rate was 18.2%.22 In another study by Delgadillo et al the pregnancy rate was 21.7%23 which was similar to the results of our study. Yousefi et al had 27% pregnancy rate.24 However, the success rate in some studies was lower than ours, about 12%.25e27 As regards the diagnosis of infertility, the highest pregnancy rate (33%) was achieved in women with ovulatory disorders. No conception was reported in women suffering from endometriosis. Patients with unexplained infertility had second highest pregnancy rate (23%). Farimani and Amiri reported the highest pregnancy rate (23.1%) in women with ovulatory disorders and the lowest (7.7%) in women suffering from endometriosis.24 Most of studies did show higher pregnancy rates in patients with unexplained infertility and ovulatory disorders and significantly low pregnancy rates Bhadauria et al. in patients suffering from endometriosis.27,28 IUI should not be opted for patients having severe endometriosis. Endometrial thickness and pattern, as a predictor of outcome, have been investigated by numerous studies with variable results. While some study groups found a significant correlation between thickness and pattern of the endometrium and pregnancy rate, others reported no such relationship. In our study, the endometrial receptivity has a significant role in predicting outcome of pregnancy. No pregnancy was reported when endometrial thickness was less than 8 mm and when endometrial vascularity was less than zone 3. Pregnancy rate was highest (88%) with multifocal vascularity in zone 3/4 and 22% with sparse vascularity in zone 3/4. Number of pregnancies were highest when endometrial thickness was 10e12 mm. Friedler et al in their study of literature survey (concerning endometrial thickness, which included 25 reports comprising 2665 assisted reproduction treatment cycles) found that in 1203 cycles the difference in the mean endometrial thickness of conception and non-conception cycles was statistically significant, while in 331 cycles found no such significant difference. They found that an endometrial thickness <6 mm has a strong NPV for the subsequent occurrence of pregnancy.29 Strohmer et al proposed that endometrial thickness is mainly related to individual uterine size and therefore has no predictive value for implantation. Similarly, no correlation was found between implantation and the mean cross-sectional area of the endometrium.30 In the study of Katib reported that mean of endometrial thickness in infertile was 0.7 cm, and the mean of endometrial thickness in fertile women was 1.3 cm hence significant decrement in endometrial thickness at p < 0.05. In addition, pregnancy rates were higher when the endometrium was thicker than 10 mm. A periovulatory endometrial thickness more than 10 mm defined 91% of conception cycles. No pregnancy occurred when the endometrium measured less than 7.31 M. Aghahoseini et al found no significant difference in endometrial thickness between pregnant and nonpregnant groups.32 It seems that the correlation between endometrial thickness as a single parameter and pregnancy is controversial. In general, most authors agree that the PPV of endometrial thickness alone is low. The low predictive value of endometrial thickness could be explained by its weak relationship with uterine receptivity.33 In Chien et al study, although pregnancy and implantation rates were significantly higher in patients with zone 3 compared with zone 1 or 2 penetration, there was no significant difference between the groups with zone 1 and 2 penetrations were found.17 In our study the pregnancy rate was 40% with distinct five line endometrial pattern, 19% with hazy five line Endometrial pattern, and 6% with no endometrial layering. Pregnancy rate
    • Colour Doppler ultrasound in controlled ovarian stimulation Case Report 259 Table 1 Comparison between pregnant and non-pregnant patients. Parameter Pregnant Non pregnant Sample size 23 77 Age in years 31.00 ± 4.25 31.08 ± 4.69 Primary 17 65 Secondary 6 12 4.87 ± 2.07 5.18 ± 2.98 0.639 10.13 ± 1.47 8.94 ± 1.60 <0.001 Zone 1 0 7 Zone 2 1 35 Zone 3/4 (sparse) 7 34 Zone 3/4 (multifocal) 15 01 No layering 1 17 Hazy five line 10 43 Distinct five line 12 17 Type of infertility Duration of infertility(years) Endometrial thickness in mm Endometrial receptivity on day of IUI Endometrial layering Endometrial Vascularity Type of layering P value 0.943 0.557 <0.001 <0.05 Right 2.38 ± 0.32 2.64 ± 0.46 <0.01 Left 2.43 ± 0.28 2.70 ± 0.54 <0.01 Mean 2.40 ± 0.28 2.67 ± 0.44 <0.01 Uterine artery doppler (PI) No of follices 1 12 57 more than 2 6 11 17 mm 3 5 9 Grade 1 0 3 Perifollicular Grade 2 0 40 vascularity Grade 3 6 26 Grade 4 17 8 0.737 Follicles on day of IUI was higher in distinct five line endometrial appearance. Friedler et al in their study found that the difference in the endometrial patterns of conception and non-conception cycles was statistically significant in 2892 cycles, however in 844 cycles no such significance was noted.33 <0.001 Uterine artery impedance is inversely related to pregnancy outcome. No pregnancy was reported when uterine PI was >2.99. Pregnancy Rate was higher in women with uterine artery PI <2.19. However no significant difference was noted in patients with uterine arterial PI 2.19e2.99.
    • 260 Apollo Medicine 2012 September; Vol. 9, No. 3 The predictive value of the PI, calculated from the published data, using a PI upper limit of 3.0 or 3.3, the Doppler assessment of uterine blood flow had a high NPV and sensitivity (in the ranges 88e100 and 96e100% respectively) and a relatively higher range of PPV and specificity (44e56 and 13e35% respectively) compared with the other ultrasonic parameters.33 Tsai et al reported no pregnancy when the pulsatility index of the ascending branch of the uterine arteries was more than 3. The fecundity rate was 18% when the pulsatility index was less than 2 and was 19.8% when the pulsatility index was between 2 and 3 (not significant). The continuing pregnancy rate was 18% when the pulsatility index was less than 2, compared with 12.1% when the pulsatility index was between 2 and 3 (P < 0.05).34 In our study we found that PR was low in COSeIUI cycles with single pre-ovulatory follicles which was significantly lower than in cycles with more follicles. The perifollicular vascularity was associated with better pregnancy rate. No pregnancy was achieved when perifollicular vascularity was grade 1 or grade 2. The pregnancy rate was 19% with grade 3 perifollicular vascularity (not significant) and was 68% with grade 4 perifollicular vascularity (which is highly significant p < 0.001). Bhal et al in their study reported that the pregnancy rate was low in the low-grade perifollicular vascularity, and it was higher in cycles with grade 3 and grade 4 perifollicular vascularity.35 Ragini et al in their study reported that follicular vascularity did not appear to predict the chance of pregnancy in women undergoing mild COS and IUI cycles. Pregnancy rate in the low-, medium- and high-grade vascularity groups was 14.1, 10.0 and 11.8%, respectively.36 Stefano et al also confirmed that the perifollicular vascularity is related to good-quality oocytes.37 CONCLUSIONS The endometrial receptivity (thickness and vascularity) is a predeterminant in predicting the outcome of pregnancy in COSeIUI treatment cycles. The pregnancy rates were higher in women with thick, multilayered endometrium and zone 3/4 endometrial vascularity. No conception was reported when endometrial thickness was less than 8 mm and zone 1/2 vascularity. The importance of measuring endometrial receptivity at around the time of intrauterine insemination is to ensure the presence of a minimal thickness to permit implantation. An evaluation of endometrial pattern, simplified to multilayered and non-multilayered, may serve to postpone or cancel those cycles in which poor endometrial development is demonstrated. The measurement of the impedance in the uterine artery during Bhadauria et al. IUI has provided an indirect assessment of uterine receptivity. Colour Doppler analysis allows an assessment of the impedance of the vascular flow of the uterine artery and measurement of uterine perfusion. If a PI upper limit for the uterine artery of 3 is defined, Doppler blood flow has a high negative predictive value and sensitivity. The positive predictive value and the specificity of uterine vascularization remain low. In our study, no pregnancy occurred with uterine PI values of more than 2.99. However not all patients conceived with lower uterine PI. At this time, however, the usefulness of ultrasonographic parameters in monitoring improvements of uterine receptivity in COSeIUI still remains to be proved by controlled prospective studies. Perifollicular vascular perfusion appears to be an important factor in determining the outcome in stimulated IUI cycles, and may have clinical implications in assisted reproduction techniques. As there were no pregnancies in women with low-grade vascularity, the identification of these cycles would be valuable early in cycles (before HCG/IUI). This could allow cancellation of treatment after careful counselling and cancellation of the cycles, could be cost-effective both financially and emotionally. However more longitudinal data would be needed before this form of prospective management of treatment cycles could be applied clinically. CONFLICTS OF INTEREST All authors have none to declare. REFERENCES 1. Das V, Pandey A, Agarwal A, Mehrotra S, Pradeep Y. Intrauterine insemination experience in a government teaching. J Obstet Gynecol India. 2010;60(4):326e330. 2. Ombelet W, Cox A, Janssen M. Artificial insemination (AIH). Artificial insemination 2: using the husband’s sperm. In: Acosta AA, Kruger TF, editors. Diagnosis and Therapy of Male Factor in Assisted Reproduction. Carnforth: Parthenon Publishing; 1996: 397e410. 3. Robinson D, Syrop CH, Hammitt DG. After superovulation intrauterine insemination fails: the prognosis for treatment by gamete intrafallopian transfer/pronuclear stage transfer. Fertil Steril. 1992;57:606e612. 4. Goswamy RK, Steptoe PC. Doppler ultrasound studies of the uterine artery in spontaneous ovarian cycles. Hum Reprod. 1988;3(6):721e726. 5. Kurjak A, Kupesic US, Schulman H, Zalud I. Transvaginal color flow Doppler in the assessment of ovarian and uterine
    • Colour Doppler ultrasound in controlled ovarian stimulation 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. blood flow in infertile women. Fertil Steril. 1991;56: 870e873. Steer CV, Tan SL, Mason BA, Campbell S. Midluteal phase vaginal color Doppler assessment of uterine artery impedance in a subfertile population. Fertil Steril. 1994;61:53e58. Sterzik K, Grab D, Sasse V, Hütter W, Rosenbusch B, Terinde R. Doppler sonographic findings and their correlation with implantation in an in vitro fertilization program. Fertil Steril. 1989;52:825e828. Steer CV, Tan SL, Dillon D. Vaginal color Doppler assessment of uterine artery impedance correlates with immunohistochemical markers of endometrial receptivity required for the implantation of an embryo. Fertil Steril. 1995;63:101e108. Favre R, Bettahar K, Grange G, et al. Predictive value of transvaginal uterine Doppler assessment in an in vitro fertilization program. Ultrasound Obstet Gynecol. 1993;3:350e353. Balakier H, Stronell RD. Color Doppler assessment of folliculogenesis in in vitro fertilization patients. Fertil Steril. 1994;62:1211e1216. Arenson J, Allinson J. New technology shows promise of improving the Doppler image. Med Imaging Int. 1994: 16e17. Bhal PS, Pugh ND, Chui DK, Gregory L, Walker SM, Shaw RW. The use of transvaginal power Doppler ultrasonography to evaluate the potential relationship between perifollicular vascularity and outcome in IVF treatment cycles. Hum Reprod. 1999;14:939e945. Chui DK, Pugh ND, Walker SM, Gregory L, Shaw RW. Follicular vascularity e the predictive value of transvaginal power Doppler ultrasonography in an in-vitro fertilisation programme: a preliminary study. Hum Reprod. 1997;12: 191e196. Tomlinson MJ, Amissah-Arthur J, Thompson BK, Kasraie JK, Bentick B. Prognostic indicators for intrauterine insemination (IUI): statistical model for IUI success. Hum Reprod. 1996;11:1892e1896. Tohma H, Hasegawa I, Sekizuka N, Tanaka K. Uterine blood flow. 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Predicting and optimizing success in an intra-uterine insemination programme. Hum Reprod. 1995;9:2014e2021. 21. Ernest HYN, Carina CWC, Oi ST, William SBY, Pak CH. Endometrial and subendometrial vascularity is higher in pregnant patients with livebirth following ART than in those who suffer a miscarriage. Hum Reprod. 2007;22(4):1134e1141. 22. Mehrafza M, Nobakhti N, Atrkar Roushan Z, Dashtdar H, Oudi M, Hosseini A. The correlation between semen parameters and pregnancy outcome after intrauterine insemination. Iranian J Reprod Med. 2003;1(1):29e32. 23. Delgadillo JC, Rojas JC, Molina AC, et al. Prognostic factors of pregnancy in intrauterine insemination. Ginecol Obstet Mex. 2006;74(12):611e625. 24. Farimani M, Amiri I. Analysis of prognostic factors for successful outcome in patients undergoing intrauterine insemination. Acta Med Iranica. 2007;45(2):101e106. 25. Zhao Y, Vlahos N, Wyncott D, et al. Impact of semen characteristics on the success of intrauterine insemination. 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    • 262 Apollo Medicine 2012 September; Vol. 9, No. 3 34. Tsai YC, Chang JC, Tai MJ, Kung FT, Yang LC, Chang SY. Relationship of uterine perfusion to outcome of intrauterine insemination. J Ultrasound Med. 1996;15(9):633e636. 35. Bhal PS, Pugh ND, Chui DK, Gregory L, Walker SM, Shaw RW. Perifollicular vascularity as a potential variable affecting outcome in stimulated intrauterine insemination treatment cycles: a study using transvaginal power Doppler. Hum Reprod. 2001;14(4):939e945. Bhadauria et al. 36. Ragni G, Anselmino M, Nicolosi AE, Brambilla ME, Calanna G, Somigliana E. Follicular vascularity is not predictive of pregnancy outcome in mild controlled ovarian stimulation and IUI cycles. Hum Reprod. 2007;22(1): 210e214. 37. Stefano P, Tiziana R, Angela F, et al. Clinical use of the perifollicular vascularity assessment in IVF cycles: a pilot study. Hum Reprod. 2006;21(4):1055e1061.
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