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DOI:10.2214/AJR.07.3957
AJR 2008; 191:1381-1385
© American Roentgen Ray Society


Technical Innovation

MR Hysterosalpingography with an Angiographic Time-Resolved 3D Pulse Sequence: Assessment of Tubal Patency

Elizabeth A. Sadowski1, Jennifer E. Ochsner2, Jody M. Riherd1, Frank R. Korosec1, Garima Agrawal1, Elizabeth A. Pritts3 and Mark A. Kliewer1

1 Department of Radiology, University of Wisconsin School of Medicine and Public Health, 600 Highland Ave., Madison, WI 53792-3252.
2 Present address: Department of Radiology, University of Washington, Seattle, WA.
3 Wisconsin Fertility Institute, Madison, WI.

Received March 7, 2008; accepted after revision June 5, 2008.

 
Address correspondence to E. A. Sadowski (esadowski{at}uwhealth.org).


Abstract
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. The purpose of our study was to determine if tubal patency can be assessed by MR hysterosalpingography (HSG) using a clinically available MR angiographic sequence (3D time-resolved imaging of contrast kinetics [TRICKS]). This capability would enhance the value of MRI in women with infertility.

CONCLUSION. MR HSG effectively shows tubal patency and can be considered when both conventional HSG and standard MRI are necessary for the evaluation of women with infertility, such as in women with suspected uterine anomalies or extrauterine disease.

Keywords: hysterosalpingography • infertility • MRI • tubal patency


Introduction
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Women presenting with infertility undergo many laboratory tests and imaging studies to exclude endocrine disturbances, congenital anomalies of the genital tract, uterine abnormality, and occlusion of the fallopian tubes. Current imaging techniques used to evaluate tubal patency include hysterosalpingography (HSG) under fluoroscopy and contrast-enhanced hysterosalpingosonography. However, these imaging examinations provide limited evaluation of congenital uterine malformation and extrauterine disease [1]. MRI, by contradistinction, can offer a comprehensive anatomic survey and, potentially, can assess for tubal patency [24].

Because women with infertility may be referred to MR for diagnosis of uterine or extrauterine abnormality, the ability to simultaneously assess tubal patency would be beneficial. The purpose of this study was to determine if MR HSG, using a clinically available MR angiographic sequence (3D time-resolved imaging of contrast kinetics [TRICKS]), can be used to reliably ascertain tubal patency.


Materials and Methods
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Subjects
This nonrandomized, HIPAA-compliant study was approved by our institutional review board, and written informed consent was obtained from all subjects. Seventeen women with infertility were recruited between August 2005 and August 2006. All subjects underwent clinically indicated conventional HSG under fluoroscopy before MR HSG. Average time between the MR HSG and conventional HSG was 76 days. The conventional HSG was performed as part of routine clinical care.

MRI Technique
MRI was performed on a 1.5-T system (Signa, GE Healthcare), using a four-element phased-array surface coil. T1-weighted and T2-weighted images using routine clinical parameters were obtained to assess for intra- and extrauterine abnormalities. Then the patient was taken out of the MR scanner and brought to a procedure room where an HSG catheter (Hystero-Salpingography Catheter 5F, Medi cal Device Technologies) attached to IV tubing (Clearlink System, 44-inch [111.8-cm] extension set, Baxter Healthcare), was placed by the radiologist or referring gynecologist. After catheter placement, the patient was returned to the MR scanner for the remainder of the examination.

For all 17 subjects, approximately 20–40 mL of a 1:100 mixture of gadodiamide (Omniscan, GE Healthcare) to normal saline (0.9%) was gently hand-injected during a multiphase acquisition using a clinically available, dynamic time-resolved T1-weighted angiographic sequence (3D TRICKS). The optimal dilution was determined through our institutional clinical experience with MR arthrography. An oblique axial plane through the pelvis to include the uterus, ovaries, and cul-de-sac was prescribed using the following parameters: TR/TE, 4.5/minimum; number of excitations, 0.7; matrix, 256 x 128; and field of view, 26–28 cm.

There were two sets of 1:100 gadodiamide and normal saline injections during two separate 3D TRICKS acquisitions; one set was acquired with a slice thickness of 4.4 mm and a temporal resolution of 2.2 seconds, and the second set was acquired with a slice thickness of 5.4 mm and a temporal resolution of 1.8 seconds. A final axial T1-weighted, fat-suppressed 3D spoiled gradient-echo series was obtained. After the study was complete, 20–40 mL of normal saline was used to flush the uterus. The entire MRI examination lasted 60 minutes or less, which included the time required to place the HSG catheter.


Figure 1
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Fig. 1A 27-year-old woman evaluated for infertility. Initial MR angiography image (A) from series of 32 subtracted dynamic MR angiographic sequence (time-resolved imaging of contrast kinetics [TRICKS]) shows small amount of dilute gadodiamide beginning to accumulate in endometrial canal (arrow). Subsequent MR angiography images (B–D) reveal more obvious accumulation of contrast material in endometrial canal, filling of fallopian tubes (arrowheads, B), and free bilateral spill (arrowheads, D). Conventional hysterosalpingography (E) shows bilateral spill (arrows). Axial T1-weighted 3D gradient-echo images (F–I) through pelvis after dilute gadodiamide injection from inferior in pelvis (F) to superior in pelvis (I) show contrast material posterior and inferior in relation to uterus on left (arrow, F and G) from left fallopian tube and anterior and superior to uterus on right (arrow, I) from right fallopian tube.

 


Figure 2
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Fig. 1B 27-year-old woman evaluated for infertility. Initial MR angiography image (A) from series of 32 subtracted dynamic MR angiographic sequence (time-resolved imaging of contrast kinetics [TRICKS]) shows small amount of dilute gadodiamide beginning to accumulate in endometrial canal (arrow). Subsequent MR angiography images (B–D) reveal more obvious accumulation of contrast material in endometrial canal, filling of fallopian tubes (arrowheads, B), and free bilateral spill (arrowheads, D). Conventional hysterosalpingography (E) shows bilateral spill (arrows). Axial T1-weighted 3D gradient-echo images (F–I) through pelvis after dilute gadodiamide injection from inferior in pelvis (F) to superior in pelvis (I) show contrast material posterior and inferior in relation to uterus on left (arrow, F and G) from left fallopian tube and anterior and superior to uterus on right (arrow, I) from right fallopian tube.

 


Figure 3
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Fig. 1C 27-year-old woman evaluated for infertility. Initial MR angiography image (A) from series of 32 subtracted dynamic MR angiographic sequence (time-resolved imaging of contrast kinetics [TRICKS]) shows small amount of dilute gadodiamide beginning to accumulate in endometrial canal (arrow). Subsequent MR angiography images (B–D) reveal more obvious accumulation of contrast material in endometrial canal, filling of fallopian tubes (arrowheads, B), and free bilateral spill (arrowheads, D). Conventional hysterosalpingography (E) shows bilateral spill (arrows). Axial T1-weighted 3D gradient-echo images (F–I) through pelvis after dilute gadodiamide injection from inferior in pelvis (F) to superior in pelvis (I) show contrast material posterior and inferior in relation to uterus on left (arrow, F and G) from left fallopian tube and anterior and superior to uterus on right (arrow, I) from right fallopian tube.

 


Figure 4
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Fig. 1D 27-year-old woman evaluated for infertility. Initial MR angiography image (A) from series of 32 subtracted dynamic MR angiographic sequence (time-resolved imaging of contrast kinetics [TRICKS]) shows small amount of dilute gadodiamide beginning to accumulate in endometrial canal (arrow). Subsequent MR angiography images (B–D) reveal more obvious accumulation of contrast material in endometrial canal, filling of fallopian tubes (arrowheads, B), and free bilateral spill (arrowheads, D). Conventional hysterosalpingography (E) shows bilateral spill (arrows). Axial T1-weighted 3D gradient-echo images (F–I) through pelvis after dilute gadodiamide injection from inferior in pelvis (F) to superior in pelvis (I) show contrast material posterior and inferior in relation to uterus on left (arrow, F and G) from left fallopian tube and anterior and superior to uterus on right (arrow, I) from right fallopian tube.

 


Figure 5
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Fig. 1E 27-year-old woman evaluated for infertility. Initial MR angiography image (A) from series of 32 subtracted dynamic MR angiographic sequence (time-resolved imaging of contrast kinetics [TRICKS]) shows small amount of dilute gadodiamide beginning to accumulate in endometrial canal (arrow). Subsequent MR angiography images (B–D) reveal more obvious accumulation of contrast material in endometrial canal, filling of fallopian tubes (arrowheads, B), and free bilateral spill (arrowheads, D). Conventional hysterosalpingography (E) shows bilateral spill (arrows). Axial T1-weighted 3D gradient-echo images (F–I) through pelvis after dilute gadodiamide injection from inferior in pelvis (F) to superior in pelvis (I) show contrast material posterior and inferior in relation to uterus on left (arrow, F and G) from left fallopian tube and anterior and superior to uterus on right (arrow, I) from right fallopian tube.

 


Figure 6
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Fig. 1F 27-year-old woman evaluated for infertility. Initial MR angiography image (A) from series of 32 subtracted dynamic MR angiographic sequence (time-resolved imaging of contrast kinetics [TRICKS]) shows small amount of dilute gadodiamide beginning to accumulate in endometrial canal (arrow). Subsequent MR angiography images (B–D) reveal more obvious accumulation of contrast material in endometrial canal, filling of fallopian tubes (arrowheads, B), and free bilateral spill (arrowheads, D). Conventional hysterosalpingography (E) shows bilateral spill (arrows). Axial T1-weighted 3D gradient-echo images (F–I) through pelvis after dilute gadodiamide injection from inferior in pelvis (F) to superior in pelvis (I) show contrast material posterior and inferior in relation to uterus on left (arrow, F and G) from left fallopian tube and anterior and superior to uterus on right (arrow, I) from right fallopian tube.

 


Figure 7
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Fig. 1G 27-year-old woman evaluated for infertility. Initial MR angiography image (A) from series of 32 subtracted dynamic MR angiographic sequence (time-resolved imaging of contrast kinetics [TRICKS]) shows small amount of dilute gadodiamide beginning to accumulate in endometrial canal (arrow). Subsequent MR angiography images (B–D) reveal more obvious accumulation of contrast material in endometrial canal, filling of fallopian tubes (arrowheads, B), and free bilateral spill (arrowheads, D). Conventional hysterosalpingography (E) shows bilateral spill (arrows). Axial T1-weighted 3D gradient-echo images (F–I) through pelvis after dilute gadodiamide injection from inferior in pelvis (F) to superior in pelvis (I) show contrast material posterior and inferior in relation to uterus on left (arrow, F and G) from left fallopian tube and anterior and superior to uterus on right (arrow, I) from right fallopian tube.

 


Figure 8
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Fig. 1H 27-year-old woman evaluated for infertility. Initial MR angiography image (A) from series of 32 subtracted dynamic MR angiographic sequence (time-resolved imaging of contrast kinetics [TRICKS]) shows small amount of dilute gadodiamide beginning to accumulate in endometrial canal (arrow). Subsequent MR angiography images (B–D) reveal more obvious accumulation of contrast material in endometrial canal, filling of fallopian tubes (arrowheads, B), and free bilateral spill (arrowheads, D). Conventional hysterosalpingography (E) shows bilateral spill (arrows). Axial T1-weighted 3D gradient-echo images (F–I) through pelvis after dilute gadodiamide injection from inferior in pelvis (F) to superior in pelvis (I) show contrast material posterior and inferior in relation to uterus on left (arrow, F and G) from left fallopian tube and anterior and superior to uterus on right (arrow, I) from right fallopian tube.

 


Figure 9
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Fig. 1I 27-year-old woman evaluated for infertility. Initial MR angiography image (A) from series of 32 subtracted dynamic MR angiographic sequence (time-resolved imaging of contrast kinetics [TRICKS]) shows small amount of dilute gadodiamide beginning to accumulate in endometrial canal (arrow). Subsequent MR angiography images (B–D) reveal more obvious accumulation of contrast material in endometrial canal, filling of fallopian tubes (arrowheads, B), and free bilateral spill (arrowheads, D). Conventional hysterosalpingography (E) shows bilateral spill (arrows). Axial T1-weighted 3D gradient-echo images (F–I) through pelvis after dilute gadodiamide injection from inferior in pelvis (F) to superior in pelvis (I) show contrast material posterior and inferior in relation to uterus on left (arrow, F and G) from left fallopian tube and anterior and superior to uterus on right (arrow, I) from right fallopian tube.

 
Data Analysis
A set of dynamic subtracted images was reconstructed with a slice thickness of 2.2–2.7 mm and evaluated similar to an MR angiographic examination. Both the subtracted series and the anatomic images were reviewed on a PACS system (Horizon Medical Imaging, version 11; McKesson Imaging Group) by a single reader blinded to the conventional HSG results who recorded tubal patency and any uterine abnormality visualized. The subtracted images were viewed by scroll ing through the series manually on the PACS workstation and were not viewed in cine mode. The diagnoses made on MR HSG were compared with the final diagnoses rendered at the time of conventional HSG examination.


Results
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
We successfully evaluated tubal patency in 16 women using MR HSG (Fig. 1A, 1B, 1C, 1D, 1E, 1F, 1G, 1H, 1I). There was one failed MR examination because of excessive patient motion. Table 1 compares the results from the MR HSG examinations to the results of conventional HSG. Of note, one patient, in whom neither fallopian tube appeared patent on the conventional HSG, did have patency of her left fallopian tube on MR HSG (Table 1, subject 13). In subject 11, on conventional HSG and the first injection of dilute gadodiamide contrast medium at MR HSG, the left fallopian tube appeared occluded; however, on the second injection of dilute gadodiamide contrast medium, there was free spillage of contrast medium on the left (Fig. 2A, 2B, 2C). In four additional patients, MR HSG showed free spill in fallopian tubes that appeared occluded on conventional HSG (Table 1, subjects 14–17). Despite visualizing obvious free spill of dilute contrast on MR HSG, it was difficult to visualize the actual fallopian tubes in their entirety in most patients.


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TABLE 1: Comparison of Conventional Hysterosalpingography (HSG) and MR HSG

 

Figure 10
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Fig. 2A 33-year-old woman evaluated for infertility. Conventional hysterosalpingography (HSG) shows normal contour of uterine canal and free spill of iodinated contrast material from right fallopian tube, with no spill on left (arrow).

 

Figure 11
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Fig. 2B 33-year-old woman evaluated for infertility. Subtracted dynamic 3D T1-weighted angiographic (time-resolved imaging of contrast kinetics [TRICKS]) MR HSG image of first injection of dilute gadodiamide contrast material, depicting normal endometrial canal contour, free spill of contrast material from right fallopian tube (arrow), and no spill on left.

 

Figure 12
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Fig. 2C 33-year-old woman evaluated for infertility. Subtracted dynamic 3D T1-weighted angiographic (TRICKS) MR HSG image of second injection of dilute gadodiamide contrast material with free spill from right and left fallopian tubes (arrows).

 

In the failed examination because of motion, the dynamic subtracted angiographic images were nondiagnostic; however, free dilute contrast was noted in the pelvis on the delayed fat-suppressed T1-weighted images. This would imply at least one fallopian tube is patent.

There were five subjects with deformity of the uterine cavity contour on conventional HSG. On MRI, the contour abnormalities were found to be large leiomyomas (three cases), an arcuate configuration to the uterus (one case), and a partial septate uterus (one case) (Fig. 3A, 3B, 3C, 3D, 3E, 3F). Furthermore, three women were found to have abnormalities on MRI that were not suspected on conventional HSG. These included a hydrosalpinx, an endometrioma, and an atrophic ovary. There was no appreciable difference in the appearance of images when comparing the dynamic subtracted sets of images with different slice thicknesses.


Figure 13
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Fig. 3A Images show uterine contour abnormalities on conventional and MR hysterosalpingography (HSG) studies in two women. Image from subtracted dynamic 3D T1-weighted angiographic series (time-resolved imaging of contrast kinetics [TRICKS]) in 45-year-old woman shows bilateral spill of contrast material and deformity of endometrial canal (arrow).

 

Figure 14
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Fig. 3B Images show uterine contour abnormalities on conventional and MR hysterosalpingography (HSG) studies in two women. Conventional HSG image shows bilateral spill of contrast material and deformity of endometrial canal (arrow).

 

Figure 15
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Fig. 3C Images show uterine contour abnormalities on conventional and MR hysterosalpingography (HSG) studies in two women. Axial T2-weighted fast recovery fast spin-echo MR image shows leiomyoma (arrow) causing deformity of endometrial canal seen on MR HSG and conventional HSG.

 

Figure 16
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Fig. 3D Images show uterine contour abnormalities on conventional and MR hysterosalpingography (HSG) studies in two women. In 31-year-old woman, subtracted dynamic 3D T1-weighted angiographic (TRICKS) MR HSG image shows indention of fundus (arrow).

 

Figure 17
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Fig. 3E Images show uterine contour abnormalities on conventional and MR hysterosalpingography (HSG) studies in two women. Conventional HSG shows endometrial contour abnormality (arrow) that could represent either bicornuate or partial septate uterine malformation.

 

Figure 18
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Fig. 3F Images show uterine contour abnormalities on conventional and MR hysterosalpingography (HSG) studies in two women. Coronal T2-weighted image through uterus shows normal contour along serosal surface of fundus with indentation of myometrium and endometrium into uterine canal, indicating partial septate uterus (arrow).

 


Discussion
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The current trend for couples to defer childbirth to later ages has resulted in an increasing number of couples presenting with infertility problems. Fallopian tube occlusion is a common cause of infertility, found in up to 40% of women being evaluated for the inability to conceive [5]. Conventional HSG under fluoroscopy remains the most commonly used procedure to diagnose fallopian tube patency in women [6]. However, conventional HSG exposes the reproductive organs of a potentially fertile woman to ionizing radiation. Furthermore, conventional HSG provides a limited evaluation of other causes of infertility, such as congenital uterine malformation, myometrial abnormalities (adenomyosis, leiomyomas), and extrauterine diseases (endometriosis, adhesions, pelvic infection, adnexal disease).

MRI is valuable in defining uterine disease and anomalies and in identifying extrauterine causes of infertility [24]. This study demonstrates the ability of MR HSG to assess tubal patency using a clinically available MR angiographic sequence (TRICKS). All fallopian tubes appearing to be patent by conventional HSG were shown as patent on MR HSG. MR HSG also demonstrated free peritoneal spill in more than half of the fallopian tubes thought to be occluded on the conventional HSG study. Notably, one patient who appeared to have bilateral occlusion of the fallopian tubes on conventional HSG revealed a patent left fallopian tube on MR HSG during injection of dilute 1:100 gadodiamide and saline.

An unexpected finding from the study was the increased number of patent fallopian tubes evident using MR HSG compared with conventional HSG. Possibly, opening of the fallopian tubes from contrast injection during conventional HSG accounts for this. However, MRI may be more sensitive to spillage of small amounts of contrast material because MRI has inherently superior contrast resolution compared with conventional radiography [7]. Further investigation in a randomized, blinded study would need to be performed to accurately determine the cause of this finding.

Previous attempts to assess tubal patency in women have been performed using T1-weighted and T2-weighted sequences with a maximum temporal resolution of 20 seconds per phase [810]. These previous investigators did adequately depict tubal patency in most (but not all) subjects on MRI. In the current study, we used the 3D TRICKS MR angiography sequence with dilute 1:100 gadodiamide and saline and successfully visualized contrast spillage from the fallopian tubes in all but one of our subjects (Table 1; subject 6). In this subject, patient motion during the injection rendered the subtracted angiographic images nondiagnostic. However, on the delayed axial fat-suppressed T1-weighted images, contrast material was seen in the pelvis, indicating free spill and patency of at least one fallopian tube in this subject.

Evaluating tubal patency with the 3D TRICKS MR angiography sequence using dilute 1:100 gadodiamide and saline has several advantages over other techniques. First, the 3D TRICKS angiography sequence is clinically available without specific requirements for vendor or physicist support. The parameters chosen provide adequate spatial resolution for visualization of fallopian tube contrast spillage, with superior temporal resolution of approximately 2 seconds per phase. This temporal resolution allowed documentation of progressive spillage from left and right tubes and, therefore, discrimination of contrast spill from the separate tubes. Patient motion is a potential problem, but the speed of the dynamic TRICK sequence allowed near-real-time resolution of the contrast spillage from the fallopian tubes in nearly all subjects.

Gadolinium-based contrast agents have been safely used for more than 15 years on millions of subjects with normal renal function in concentrations much higher than we have used. In women with normally functioning kidneys, the contrast material should be excreted in the urine, under the assumption that all the contrast material is resorbed from the peritoneum, uterus, and fallopian tubes [11].

This study shows that tubal patency can be effectively assessed with a clinically available MR angiographic sequence (3D TRICKS). This capability enhances the already established value of MRI for the evaluation of uterine and extrauterine abnormalities. MR HSG can be considered as a single comprehensive examination when both conventional HSG and standard MRI are necessary in the work-up of women with infertility.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

  1. Watrelot A, Hamilton J, Grudzinskas JG. Advances in the assessment of the uterus and fallopian tube function. Best Pract Res Clin Obstet Gynaecol 2003; 17:187 –209[CrossRef][Medline]
  2. Levine D. Solving the problem: pelvic ultrasound with magnetic resonance imaging. Ultrasound Q 2006;22 : 159–168[CrossRef][Medline]
  3. Woodward PJ, Wagner BJ, Farley TE. MR imaging in the evaluation of female infertility. RadioGraphics 1993;13 : 293–310[Abstract]
  4. Imaoka I, Wada A, Matsuo M, Yoshida M, Kitagaki H, Sugimura K. MR imaging of disorders associated with female infertility: use in diagnosis, treatment, and management. RadioGraphics2003; 23:1401 –1421[Abstract/Free Full Text]
  5. Winfield AC, Fleischer AC, Moore DE. Diagnostic imaging of fertility disorders. Curr Probl Diag Radiol1990; 19:1 –38
  6. Krysiewicz S. Infertility in women: diagnostic evaluation with hysterosalpingography and other imaging techniques. AJR 1992; 159:253 –261[Abstract/Free Full Text]
  7. Leiner T, Kessels AG, Schurink GW, et al. Comparison of contrast-enhanced magnetic resonance angiography and digital subtraction angiography in patients with chronic critical ischemia and tissue loss. Invest Radiol 2004;39 : 435–444[CrossRef][Medline]
  8. Frye RE, Ascher SM, Thomasson D. MR hysterosalpingography: protocol development and refinement for simulating normal and abnormal fallopian tube patency—feasibility study with a phantom. Radiology 2000;214 : 107–112[Abstract/Free Full Text]
  9. Rouanet De Lavit JP, Maubon AJ, Thurmond AS. MR hysterography performed with saline injection and fluid attenuated inversion recovery sequences: initial experience. AJR 2000;175 : 774–776[Free Full Text]
  10. Unterweger M, De Geyter C, Fröhlich JM, Bongartz G, Wiesner W. Three-dimensional dynamic MR-hysterosalpingography: a new, low invasive, radiation-free and less painful radiological approach to female infertility. Hum Reprod 2002;17 :3138 –3141[Abstract/Free Full Text]
  11. Joffe P, Thomsen HS, Meusel M. Pharmacokinetics of gadodiamide injection in patients with severe renal insufficiency and patients undergoing hemodialysis or continuous ambulatory peritoneal dialysis. Acad Radiol 1998; 5:491 –502[CrossRef][Medline]

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MR Hysterosalpingography Compared With Conventional Hysterosalpingography
Am. J. Roentgenol., June 1, 2009; 192(6): W350 - W350.
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