colour doppler ultrasound in controlled ovarian stimulation with intrauterine insemination

Colour Doppler Ultrasound in Controlled Ovarian Stimulation with Intrauterine Insemination

Colour Doppler ultrasound in controlled ovarian stimulation withintrauterine 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 thepotential relationship between perifollicular vascularity following ovulation inducing drugs and outcome in intrauterineinsemination (IUI) using the Doppler ultrasonography.

Materials and methods: Infertile couple in our hospital was subjected to colour Doppler ultrasound examination andthe 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 predictingsuccessful 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 epidemicproportion with the treatment modalities and options devel-oping almost compulsorily at exponential rates. Both IUI(intrauterine insemination) and IVF (in vitro fertilization)are now practiced in reasonably large numbers at most re-ported infertility centres.

Intrauterine insemination (IUI) with or withoutcontrolled ovarian stimulation (COS) is a popular modalityfor treatment of subfertility. Although considerable discus-sion and debate have appeared in western literatureregarding the utility of COS and IUI, lately the NationalInstitute of Clinical Excellence (NICE), UK has revisedthe evidence for assessment and treatment of infertilecouples and has recommended that IUI should be offeredto couples with infertility because it is as effective asIVF, 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 ofpregnancy. However, significant risks of ovarian hyperstim-ulation syndromedand in particular multiple pregnan-ciesdremain.2 Despite this, IUI has significant costsavings and is less invasive, without necessarily a reductionin effectiveness, compared with other forms of assistedreproduction treatment such as IVF or gamete intra-fallo-pian transfer (GIFT) in particular for non-tubal infertility.3

The rationale put forward in support of COS and IUI isthat ovarian stimulation corrects subtle, unpredictableovulatory dysfunction and there is increased probabilityof conception if increased density of motile spermatozoais placed closer to multiple fertilizable oocytes.1

With the progressive standardization of these techniquesit also becomes imperative to develop parameters to predictsuitability and thus the success of the procedure. As in mostgynaecological condition, sonography and Doppler are

aResident, bSenior Consultant, cAssociate Consultant, Department of Radiodiagnosis and AARU, Indraprashta Apollo Hospitals, New Delhi110076, India.*Corresponding author. email: [email protected]: 14.5.2012; Accepted: 4.7.2012; Available online: 13.7.2012Copyright � 2012, Indraprastha Medical Corporation Ltd. All rights reserved.http://dx.doi.org/10.1016/j.apme.2012.07.014

Apollo Medicine 2012 SeptemberVolume 9, Number 3; pp. 252e262 Case Report

powerful tools. Goswamy and Steptoe4 were the first tosuggest that abnormal uterine artery blood flow might beassociated with infertility and to develop a classificationof uterine artery blood flow waveforms. Subsequently,other authors have confirmed a relationship of uterine andovarian blood flow to unexplained infertility,5,6 and tosuccessful implantation following IVF.7e10

Power Doppler or colour ultrasonography has beengenerating increasing clinical interest since its introduc-tion.11 Despite the fact that the application of powerDoppler in gynaecology remains in its infancy, recentstudies suggest potential applications especially in relationto the assessment of uterine and perifollicular vascu-larity12,13 and outcome in IVF treatment cycles.

Statistical models have been reported for predictingsuccess rates in IUI which suggested that follicle number,endometrial thickness, duration of subfertility and semenparameters were the most significant variables in predictingoutcome.14 The application of Doppler ultrasound in IUIhas tended to relate uterine perfusion to outcome and fewdata exist on ovarian vascularity in these treatment cycles.15

This study was thus designed to collect statisticallysignificant data in large numbers for IUI so as to achievesuperior results and outcome.

MATERIALS AND METHODS

The cycles of ovarian-stimulationeintrauterine insemina-tion (COSeIUI) treatment in infertile couples presentingto Apollo Assisted Reproduction Unit (AARU), fromJune 2009 to December 2010 were screened in our study.These patients were subjected to inclusion and exclusioncriterias and 100 COSeIUI cycles were then analysedand assessed for the successful outcome of pregnancy.

Inclusion criteria

Women aged <42 years, primary or secondary infertilitylasting for at least 12 months, tubal patency assessed byhysterosalpingography and/or laparoscopy with chromosal-pingography, with at least one patent fallopian tube, normalsemen analysis.

Exclusion criteria

Patients with coexisting disease such as bilateral tubalblock, congenital uterine anomalies which are liable toaffect outcome, associated male subfertility and infertility,patients who were started on ovulation induction regime

Fig. 1 Longitudinal scans showing endometrial patterns. (a and b) Hazy five line appearance.

Fig. 2 Longitudinal scans showing endometrial patterns. (a and b) Distinct five line appearance.

Colour Doppler ultrasound in controlled ovarian stimulation Case Report 253

but were not subjected to IUI due to inappropriate folliculargrowth (follicular size less than 16 mm till 22nd day of thecycle) were excluded from our study, patients with multipledominant follicles (four or more) were excluded from ourstudy considering the risk for multifetal pregnancies.

Ultrasound examination was carried out in all patients ineach cycle of COSeIUI at day 2 (baseline). Each patientwas informed and written consent was taken for COSeIUIas well as for colour Doppler US evaluation in addition toroutine follicular monitoring US protocol. Patients wereexamined in lithotomy position and transvaginal ultrasoundevaluation was done using transvaginal probe of 8 Hz(E8C). All studies were performed by a single operatoron LOGIC 5 PRO (GE Healthcare) ultrasound machine.

On day 2 of menstrual cycle, all patients were subjectedto baseline US. The uterus was screened for endometriallining (thickness and pattern), echogenicty of myometrium(fibroids, adenomyosis, past myomectomy). The uterineimaging 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 DopplerUS was done to evaluate the uterine and intraovarian arte-rial impedance as described below.

On day 7, the patients were evaluated for follicular andendometrial growth and were examined thereon every alter-nate day till the follicle reached the size 14 mm or more andthen everyday till ovulation. Patients were subjected to 5000units of HCG administration intravenously when one ormore follicles attained the size >16 mm and endometrialthickness was >7 mm. The IUI was done 48 h (or 24 h iffollicle was ruptured earlier) after the HCG administration.

Doppler US was carried and various parameters wererecorded as described on subsequent patient visits. Forcolour and power Doppler study, the pulse repetitionfrequency (PRF) and wall filters were set at the lowestpossible frequencies. We used wall filter 40 Hze75 Hzfor evaluating low resistance intraovarian and endometrialvessels. The wall filters were 60 Hze115 Hz for evaluatingthe ascending branches of both uterine arteries. The pulserepetition 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 endometriumi) Measured from themyometrialeendometrial junction to

the endometrialemyometrial junction in sagittal plane.ii) Layering of endometrium (endometrial echogenic

pattern), distinct five line appearance, hazy five lineappearance, or no layering (Figs. 1e3).

iii) Endometrial blood flowThe endometrial and periendometrial areas aredivided into the following four zones16,17

(Figs. 4 and 5).Zone 1 e a 2 mm thick area surrounding thehyperechoic outer layer of the endometriumZone 2 e the hyperechoic outer layer of theendometriumZone 3 e the hypoechoic inner layer of theendometriumZone 4 e the endometrial cavity

3) Uterine arteries. The ascending branches of bothuterine arteries were examined at lower uterine segmentand Doppler parameters were recorded as (Fig. 6):

Fig. 3 Longitudinal scans showing endometrial patterns. (a and b) Thin endometrium with no layering.

Fig. 4 Endometrial zones of vascularity.

254 Apollo Medicine 2012 September; Vol. 9, No. 3 Bhadauria et al.

i) Peak systolic velocity (PSV)ii) End diastolic velocity (EDV)iii) Pulsatility index (PI)iv) Resistive index (RI)

THE FOLLICLES

The number of dominant follicles (>16 mm) in eachCOSeIUI cycle were recorded and each follicle wasassessed for perifollicular vascularity (Fig. 7). When more

Fig. 5 Zone 3/4 endometrial vascularity with (a) sparse and (b) multifocal vascularity.

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.


than one follicle was observed, grading was performed forall of them, and the highest vascularity grade was recorded.

The vascularity of each follicle was subjectively gradedusing Power Doppler imaging (according to the gradingsystem 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 periovu-latory and periluteal phase. The intraovarian arterialDoppler 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 COSeIUICYCLES were analysed in our study. There were 23 preg-nancies with pregnancy rate being 23%. The youngest patientwas 20 years old, with 2 years duration of infertility. Theeldest female was 41 years old with 10 years of infertility.

Twenty-three pregnant patients, 13 patients had endome-trial thickness 8e10 mm, eight patients had endometrialthickness 10e12 mm, one patient had endometrial of 8 mm.

We found significant relation between endometrialthickness and pregnancy rates, highest (42%) with endome-trial thickness ranging from 10 to 12 mm (p < 0.05).However not all pts with thicker endometrium had positiveoutcome. In case endometrial thickness was 6e8 mm, itshowed a significantly lower rates of pregnancy (p < 0.01).

Correlation: Pearson coefficient between endometrialthickness and pregnancy is 0.31, it is a positive correlationwhich suggest that more the endometrial thickness more thepregnancy rate.

Fig. 7 (a) Normal ovary on base day 2, (b) follicular diameter measured in two perpendicular planes, (c) showing dominant folliclewith cumulus oophorus (arrow), (d) rt ovary showing multiple3 follicles.


There is significant correlation between pregnancy rateand endometrial vascularity. Of 16 patients with multifocalvascularity in zone 3/4, 14 patients (88%) had positiveoutcome (highly significant p < 0.001). Whereas only22% (9 out of 41) patients had conception with sparsevascularity in zone 3/4. No conception was reported inwomen having zone 1/2 endometrial vascularity (highlysignificant p < 0.001, significantly lower chances of preg-nancy if in zone 2).

Statistically higher pregnancy rate (40%) was reported inwomen with distinct five line appearance (p < 0.05).Patients with no endometrial layering had poor pregnancyrate (6%) and 19% pregnancy was seen with hazy fiveline appearance.

Lesser the uterine artery impedance, more the number ofpregnancies reported. No pregnancy was reported inwomen when uterine artery impedance PI was more than2.99 (statistically significant p < 0.05). There was nosignificant difference in pregnancy rates when uterine arte-rial PI was low, 36% when PI was <2.19, 29% when PIwas 2.2e2.49, 32% when PI was 2.5e2.75 and 13% withPI 2.75e2.99 (not significant > 0.05).

The median number of pre-ovulatory follicles (>17 mmin diameter) on the IUI day among the pregnant patents was

2 (�1.6) and in non-pregnant cases was 1.79 (�1.2). Incycles with a single pre-ovulatory follicle (>17 mm indiameter) the pregnancy rate (17%) was significantly lowerthan in cycles with more follicles (35% and 36% respec-tively with two or three dominant follicles).

The perifollicular vascularity was associated with betterpregnancy rate. No pregnancy was achieved with perifollic-ular vascularity with grade 1 and grade 2 (which is highlysignificant p < 0.001). The pregnancy rate was 19% withgrade 3 perifollicular vascularity (not significant) and was68% with grade 4 perifollicular vascularity (which is highlysignificant p < 0.001).

DISCUSSION

Many studies have been conducted to evaluate the role ofvarious ultrasound parameters in predicting pregnancyduring ART18e20 but little information exists in the litera-ture with regard to their role in predicting subsequent preg-nancy outcomes.21 Our study was attempted to assess theprognostic uterine and ovarian IUI variables with regardto successful outcome (pregnant/non-pregnant) usingcolour Doppler transvaginal ultrasound so that the outcome

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).


of subsequent COSeIUI cycles could be more accuratelypredicted than before.

In our study pregnancy occurred in 23 patients (23%) oftotal 100 infertility COSeIUI cycles. In Mehrafza et alstudy undertaken on 336 IUI cycles, the overall pregnancyrate was 18.2%.22 In another study by Delgadillo et al thepregnancy rate was 21.7%23 which was similar to theresults of our study. Yousefi et al had 27% pregnancyrate.24 However, the success rate in some studies was lowerthan ours, about 12%.25e27

As regards the diagnosis of infertility, the highest preg-nancy rate (33%) was achieved in women with ovulatorydisorders. No conception was reported in women sufferingfrom endometriosis. Patients with unexplained infertilityhad second highest pregnancy rate (23%). Farimani andAmiri reported the highest pregnancy rate (23.1%) in womenwith ovulatory disorders and the lowest (7.7%) in womensuffering from endometriosis.24 Most of studies did showhigher pregnancy rates in patients with unexplained infertilityand ovulatory disorders and significantly low pregnancy rates

in patients suffering from endometriosis.27,28 IUI should notbe opted for patients having severe endometriosis.

Endometrial thickness and pattern, as a predictor ofoutcome, have been investigated by numerous studieswith variable results. While some study groups founda significant correlation between thickness and pattern ofthe endometrium and pregnancy rate, others reported nosuch relationship. In our study, the endometrial receptivityhas a significant role in predicting outcome of pregnancy.No pregnancy was reported when endometrial thicknesswas less than 8 mm and when endometrial vascularitywas less than zone 3. Pregnancy rate was highest (88%)with multifocal vascularity in zone 3/4 and 22% with sparsevascularity in zone 3/4. Number of pregnancies were high-est when endometrial thickness was 10e12 mm. Friedleret al in their study of literature survey (concerning endome-trial thickness, which included 25 reports comprising 2665assisted reproduction treatment cycles) found that in 1203cycles the difference in the mean endometrial thickness ofconception and non-conception cycles was statisticallysignificant, while in 331 cycles found no such significantdifference. They found that an endometrial thickness<6 mm has a strong NPV for the subsequent occurrenceof pregnancy.29 Strohmer et al proposed that endometrialthickness is mainly related to individual uterine size andtherefore has no predictive value for implantation. Simi-larly, no correlation was found between implantation andthe mean cross-sectional area of the endometrium.30 Inthe study of Katib reported that mean of endometrial thick-ness in infertile was 0.7 cm, and the mean of endometrialthickness in fertile women was 1.3 cm hence significantdecrement in endometrial thickness at p < 0.05. In addition,pregnancy rates were higher when the endometrium wasthicker than 10 mm. A periovulatory endometrial thicknessmore than 10 mm defined 91% of conception cycles. Nopregnancy occurred when the endometrium measured lessthan 7.31 M. Aghahoseini et al found no significant differ-ence in endometrial thickness between pregnant and non-pregnant groups.32 It seems that the correlation betweenendometrial thickness as a single parameter and pregnancyis controversial. In general, most authors agree that the PPVof endometrial thickness alone is low. The low predictivevalue of endometrial thickness could be explained by itsweak relationship with uterine receptivity.33

In Chien et al study, although pregnancy and implanta-tion rates were significantly higher in patients with zone 3compared with zone 1 or 2 penetration, there was no signif-icant difference between the groups with zone 1 and 2 pene-trations were found.17

In our study the pregnancy rate was 40%with distinct fiveline endometrial pattern, 19%with hazyfive line Endometrialpattern, and 6%with no endometrial layering. Pregnancy rate

Fig. 9 Intraovarian waveform pattern (a) In proliferative phase,and (b) In secretory phase.


was higher in distinct five line endometrial appearance. Frie-dler et al in their study found that the difference in theendometrial patterns of conception and non-conceptioncycles was statistically significant in 2892 cycles, howeverin 844 cycles no such significance was noted.33

Uterine artery impedance is inversely related to preg-nancy outcome. No pregnancy was reported when uterinePI was >2.99. Pregnancy Rate was higher in women withuterine artery PI <2.19. However no significant differencewas noted in patients with uterine arterial PI 2.19e2.99.

Table 1 Comparison between pregnant and non-pregnant patients.

Parameter Pregnant Non pregnant P value

Sample size 23 77

Age in years 31.00 ± 4.25 31.08 ± 4.69 0.943

Primary 17 65Type of infertility

Secondary 6 12

0.557

Duration of infertility(years) 4.87 ± 2.07 5.18 ± 2.98 0.639

Endometrial thickness in mm 10.13 ± 1.47 8.94 ± 1.60 <0.001

Zone 1 0 7

Zone 2 1 35

Zone 3/4 (sparse) 7 34

Endometrial receptivity on day of IUI Endometrial

Vascularity

Zone 3/4 (multifocal) 15 01

<0.001

No layering 1 17

Hazy five line 10 43Endometrial layering

Type of layering

Distinct five line 12 17

<0.05

Right 2.38 ± 0.32 2.64 ± 0.46 <0.01

Left 2.43 ± 0.28 2.70 ± 0.54 <0.01Uterine artery

doppler (PI)

Mean 2.40 ± 0.28 2.67 ± 0.44 <0.01

1 12 57

2 6 11

No of follices

more than

3 5 9

0.737

Grade 1 0 3

Grade 2 0 40

Grade 3 6 26

Follicles on day

of IUI

Perifollicular

vascularity

Grade 4 17 8

<0.001

17 mm


The predictive value of the PI, calculated from the pub-lished data, using a PI upper limit of 3.0 or 3.3, the Dopplerassessment of uterine blood flow had a high NPV and sensi-tivity (in the ranges 88e100 and 96e100% respectively)and a relatively higher range of PPV and specificity(44e56 and 13e35% respectively) compared with the otherultrasonic parameters.33 Tsai et al reported no pregnancywhen the pulsatility index of the ascending branch of theuterine arteries was more than 3. The fecundity rate was18% when the pulsatility index was less than 2 and was19.8% 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 with12.1% when the pulsatility index was between 2 and 3(P < 0.05).34

In our study we found that PR was low in COSeIUIcycles with single pre-ovulatory follicles which was signif-icantly lower than in cycles with more follicles. The perifol-licular vascularity was associated with better pregnancyrate. No pregnancy was achieved when perifollicular vascu-larity was grade 1 or grade 2. The pregnancy rate was 19%with grade 3 perifollicular vascularity (not significant) andwas 68% with grade 4 perifollicular vascularity (which ishighly significant p < 0.001). Bhal et al in their study re-ported that the pregnancy rate was low in the low-gradeperifollicular vascularity, and it was higher in cycles withgrade 3 and grade 4 perifollicular vascularity.35 Raginiet al in their study reported that follicular vascularity didnot appear to predict the chance of pregnancy in womenundergoing mild COS and IUI cycles. Pregnancy rate inthe low-, medium- and high-grade vascularity groups was14.1, 10.0 and 11.8%, respectively.36 Stefano et al alsoconfirmed that the perifollicular vascularity is related togood-quality oocytes.37

CONCLUSIONS

The endometrial receptivity (thickness and vascularity) isa predeterminant in predicting the outcome of pregnancyin COSeIUI treatment cycles. The pregnancy rates werehigher in women with thick, multilayered endometriumand zone 3/4 endometrial vascularity. No conception wasreported when endometrial thickness was less than 8 mmand zone 1/2 vascularity. The importance of measuringendometrial receptivity at around the time of intrauterineinsemination is to ensure the presence of a minimal thick-ness to permit implantation. An evaluation of endometrialpattern, simplified to multilayered and non-multilayered,may serve to postpone or cancel those cycles in whichpoor endometrial development is demonstrated. Themeasurement of the impedance in the uterine artery during

IUI has provided an indirect assessment of uterine recep-tivity. Colour Doppler analysis allows an assessment ofthe impedance of the vascular flow of the uterine arteryand measurement of uterine perfusion. If a PI upper limitfor the uterine artery of 3 is defined, Doppler blood flowhas a high negative predictive value and sensitivity. Thepositive predictive value and the specificity of uterinevascularization remain low. In our study, no pregnancyoccurred with uterine PI values of more than 2.99. Howevernot all patients conceived with lower uterine PI. At thistime, however, the usefulness of ultrasonographic parame-ters in monitoring improvements of uterine receptivity inCOSeIUI still remains to be proved by controlled prospec-tive studies.

Perifollicular vascular perfusion appears to be an impor-tant factor in determining the outcome in stimulated IUIcycles, and may have clinical implications in assisted repro-duction techniques. As there were no pregnancies inwomen with low-grade vascularity, the identification ofthese cycles would be valuable early in cycles (beforeHCG/IUI). This could allow cancellation of treatment aftercareful counselling and cancellation of the cycles, could becost-effective both financially and emotionally. Howevermore longitudinal data would be needed before this formof prospective management of treatment cycles could beapplied 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 governmentteaching. 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 ofMale Factor in Assisted Reproduction. Carnforth: ParthenonPublishing; 1996: 397e410.

3. Robinson D, Syrop CH, Hammitt DG. After superovulationintrauterine insemination fails: the prognosis for treatmentby gamete intrafallopian transfer/pronuclear stage transfer.Fertil Steril. 1992;57:606e612.

4. Goswamy RK, Steptoe PC. Doppler ultrasound studies of theuterine artery in spontaneous ovarian cycles. Hum Reprod.1988;3(6):721e726.

5. Kurjak A, Kupesic US, Schulman H, Zalud I. Transvaginalcolor flow Doppler in the assessment of ovarian and uterine


blood flow in infertile women. Fertil Steril. 1991;56:870e873.

6. Steer CV, Tan SL, Mason BA, Campbell S. Midluteal phasevaginal color Doppler assessment of uterine artery impedancein a subfertile population. Fertil Steril. 1994;61:53e58.

7. Sterzik K, Grab D, Sasse V, Hütter W, Rosenbusch B,Terinde R. Doppler sonographic findings and their correlationwith implantation in an in vitro fertilization program. FertilSteril. 1989;52:825e828.

8. Steer CV, Tan SL, Dillon D. Vaginal color Dopplerassessment of uterine artery impedance correlates withimmunohistochemical markers of endometrial receptivityrequired for the implantation of an embryo. Fertil Steril.1995;63:101e108.

9. Favre R, Bettahar K, Grange G, et al. Predictive value oftransvaginal uterine Doppler assessment in an in vitro fertiliza-tion program. Ultrasound Obstet Gynecol. 1993;3:350e353.

10. Balakier H, Stronell RD. Color Doppler assessment offolliculogenesis in in vitro fertilization patients. Fertil Steril.1994;62:1211e1216.

11. Arenson J, Allinson J. New technology shows promise ofimproving the Doppler image. Med Imaging Int. 1994:16e17.

12. Bhal PS, Pugh ND, Chui DK, Gregory L, Walker SM,Shaw RW. The use of transvaginal power Doppler ultrasonog-raphy to evaluate the potential relationship between perifollic-ular vascularity and outcome in IVF treatment cycles. HumReprod. 1999;14:939e945.

13. Chui DK, Pugh ND, Walker SM, Gregory L, Shaw RW.Follicular vascularity e the predictive value of transvaginalpower Doppler ultrasonography in an in-vitro fertilisation pro-gramme: a preliminary study. Hum Reprod. 1997;12:191e196.

14. Tomlinson MJ, Amissah-Arthur J, Thompson BK,Kasraie JK, Bentick B. Prognostic indicators for intrauterineinsemination (IUI): statistical model for IUI success. HumReprod. 1996;11:1892e1896.

15. Tohma H, Hasegawa I, Sekizuka N, Tanaka K. Uterine bloodflow. Assessment in an intrauterine insemination program forunexplained infertility. J Reprod Med. 1997;42:463e466.

16. Applebaum M. The uterine biophysical profile. UltrasoundObstet Gynecol. 1995;5:67e68.

17. Chien LW, Au HK, Chen PL, Xiao J, Tzeng CR. Assessmentof uterine receptivity by the endometrial-subendometrialblood flow distribution pattern in women undergoing in vitrofertilization-embryo transfer. Fertil Steril. 2002;78(2):245e251.

18. Salle B, Bied-Damon V, Benchaib M, Desperes S,Gaucherand P, et al. Preliminary report of an ultrasonographyand colour Doppler uterine score to predict uterine receptivityin an in-vitro fertilization programme. Hum Reprod.1998;13(6):1669e1673.

19. Kupesic S, Bekavac I, Bjelos D, Kurjak A. Assessment ofendometrial receptivity by transvaginal color doppler andthree-dimensional power doppler ultrasonography in patientsundergoing in vitro fertilization procedures. J UltrasoundMed. 2001;20:125e134.

20. Plosker SM, Jacobson W, Amato P. Predicting and optimizingsuccess in an intra-uterine insemination programme. HumReprod. 1995;9:2014e2021.

21. Ernest HYN, Carina CWC, Oi ST, William SBY, Pak CH.Endometrial and subendometrial vascularity is higher in preg-nant patients with livebirth following ART than in those whosuffer 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 parame-ters and pregnancy outcome after intrauterine insemination.Iranian J Reprod Med. 2003;1(1):29e32.

23. Delgadillo JC, Rojas JC, Molina AC, et al. Prognostic factorsof pregnancy in intrauterine insemination. Ginecol ObstetMex. 2006;74(12):611e625.

24. Farimani M, Amiri I. Analysis of prognostic factors forsuccessful outcome in patients undergoing intrauterine insem-ination. Acta Med Iranica. 2007;45(2):101e106.

25. Zhao Y, Vlahos N, Wyncott D, et al. Impact of semen charac-teristics on the success of intrauterine insemination. J AssistReprod Genet. 2004;21(5):143e148.

26. Deng CY, Clark S. Superovulation and intrauterine insemina-tion in treatment of idiopathic infertility in 202 cycles. Zhong-guo Yi Xue Ke Xue Yuan Xue Bao. 2004;26(2):178e181.

27. Khalil MR, Rasmussen PE, Erb K, Laursen SB, Rex S,Westergaard LG. Homologous intrauterine insemination. Anevaluation of prognostic factors based on a review of 2473cycles. Acta Obstet Gynecol Scand. 2001;80:74e81.

28. Nuojua- HS, Tomas C, Bloigu R, Tuomivaara L,Martikainen H. Intrauterine insemination treatment in subfer-tility: an analysis of factors affecting outcome. Hum Reprod.1999;14:698e703.

29. Friedler S, Schenker JG, Herman A, Lewin A. The role ofultrasonography in the evaluation of endometrial receptivityfollowing assisted reproductive treatments: a critical review.Hum Reprod Update. 1996;2(4):323e335.

30. Strohmer H, Obruca A, Radnevk M, Feichtinger W. Relation-ship of the individual uterine size and the endometrial thick-ness in stimulated cycles. Fertil Steril. 1994;61:972e975.

31. Katib AR. Effect of endometrial thickness on fertility. KufaMed J. 2010;13(1):1e4.

32. Aghahoseini M, Tuba K, Marsousi V, Aleyasin A. Assess-ment of endometrial-subendometrial blood flow detected bycolor doppler sonography and uterine receptivity in infertilewomen. Acta Med Iranica. 2008;46(6):461e466.

33. Dickey PR. Doppler ultrasound investigation of uterine andovarian blood flow in infertility and early pregnancy. HumReprod Update. 1997;3(5):467e503.


34. Tsai YC, Chang JC, Tai MJ, Kung FT, Yang LC, Chang SY.Relationship of uterine perfusion to outcome of intrauterineinsemination. 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 variableaffecting outcome in stimulated intrauterine inseminationtreatment cycles: a study using transvaginal power Doppler.Hum Reprod. 2001;14(4):939e945.

36. Ragni G, Anselmino M, Nicolosi AE, Brambilla ME,Calanna G, Somigliana E. Follicular vascularity is not predic-tive of pregnancy outcome in mild controlled ovarianstimulation and IUI cycles. Hum Reprod. 2007;22(1):210e214.

37. Stefano P, Tiziana R, Angela F, et al. Clinical use of the peri-follicular vascularity assessment in IVF cycles: a pilot study.Hum Reprod. 2006;21(4):1055e1061.


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colour doppler ultrasound in controlled ovarian stimulation with intrauterine insemination

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