Diagnostic Performance of Magnetic Resonance Hysterosalpyngography: Initial Results

Original Article

A.A. Kohana,b,*, M.C Kucharczykc, N.T. Posadasa,d, M.N. Napolia, S. Gile, N.A. Fuentesf, R.D. García Mónacoa and C.R. Chacóna a Servicio de Radiología, Hospital Italiano de Buenos Aires, Ciudad Autónoma de Buenos Aires, Argentina b CERIM, Ciudad Autónoma de Buenos Aires, Argentina c Servicio de Radiología, Instituto Oncológico Alexander Fleming, Ciudad Autónoma de Buenos Aires, Argentina d Servicio de Radiología, Instituto Médico de Alta Complejidad, Salta, Argentina e Servicio de Ginecología, Hospital Italiano de Buenos Aires, Ciudad Autónoma de Buenos Aires, Argentina f Servicio de Medicina interna, Hospital Italiano de Buenos Aires, Ciudad Autónoma de Buenos Aires, Argentina Recibido el 15 de julio de 2016; aceptado el 24 de diciembre de 2016 *Correspondance author. E-mail: [email protected] (A.A. Kohan)

Abstract Objective: Determine the diagnostic performance of magnetic resonance histerosalpyngography (MR-HSG) using laparoscopy as a method of reference. Materials and Methods: 22 patients were included. MR-HSG was performed in a 1.5 Tesla MR scanner. Afterwards, patients underwent laparoscopic chromotubation. MR images were examined by two trained radiologist and tubal patency was determined in consensus. Descriptive and diagnostic performance analyses were performed. Results: MRHSG had a 91% success rate. Exam duration was 49±15min, injected volume 26±16 cm3 and pain scale 30±19 out of 100. Sensitivity and Specificity of MRHSG was 100% for global and left Cotte test and 25% and 93.3% for right Cotte test, respectively. Only 2 minor and no major complications were observed. Discussion: Our initial results have shown high sensitivity and specificity. Even though other studies have analyzed MR- HSGs potential for tubal patency assessment and have already yielded good results, the use of a flawed gold standard such as conventional HSG always left margin for a reasonable doubt, thus precluding a solid evidence based recom- mendation. Nevertheless, if we compare our results to those published, we can observe a high degree of agreement in that positive spillage is correctly diagnosed with specificities near or at 100%. Conclusion: MR-HSG is a feasible and safe alternative to conventional or virtual HSG, sonohisterography, and chromotubation. Key Words: Magnetic Resonance Imaging, Hysterosalpingography, Infertility, Laparoscopy, Tubal Obstruction

Introduction While hysterosalpingography (HSG) continues to be the Between 10 and 15% of couples have problems conceiving. method of choice for assessing tubal patency and the uterine Out of that population, 40-50% of the causes are second- cavity, there is an increasing number of published literature ary to the female reproductive system: peritoneum 20-25%, addressing the capability of MR to perform such task by us- 1, 8-15 uterus 2-5% and the fallopian tubes 10% as individual cause ing diluted gadolinium (Gd) . The main weakness of the and 25-40% as concomitant causes1, 2. available literature is the lack of a proper homogeneous gold Even if magnetic resonance (MR) imaging is able to detect standard to make comparisons with MR findings and to un- most of these pathologies, no hard evidence has yet been derstand the real diagnostic capabilities of MR hysterosalpin- provided to determine the real tubal patency assessment ca- gography (MR-HSG), as most published literature has used pabilities of this method2-5. The most widely used method for for comparisons HSG alone or a mixture of HSG and an oc- 8, 10-15 this condition is hysterosalpingography, although it is far from casional laparoscopy . being reliable, with sensitivities ranging approximately from If MR-HSG proved to be reliable in the diagnosis of tubal 53 to 65% and specificities ranging approximately from 80 to patency, a relatively important number of potential benefits 87%6, 7. Chromotubation (the current gold standard method) would become available for the target population. For once, requires a surgical procedure and general anesthesia. we could provide patients being evaluated for fertility issues

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with a single examination to assess all diseases: endometrio- [volumetric interpolated breath-hold examination] and T1- sis, uterine/vaginal malformations, leiomyomas, adenomyosis weighted three-dimensional [3D] angiographic sequence), and polycystic ovaries, among others. Considering the study during (TRU-FISP [true fast imaging with steady state preces- population, additional benefits would be the lack of ionizing sion] and T1-weighted 3D angiographic sequence) and after radiation, the use of a more innocuous contrast (gadolinium intrauterine injection (VIBE and T1-weighted 3D angiograph- vs. Iodine) and no requirement of general anesthesia. ic sequence). In the present study we intend to determine the diagnostic The diluted mixture was injected at a rate of 0.3ml per second performance of MR-HSG using laparoscopic chromotubation with an automatic stop if the pressure raised above 30 mmHg as the reference method. inside the uterine cavity. Initial injection volume was 20ml for all patients which was reduced if the patient triggered an alarm due to pain or extended if the physician performing Materials and Methods the procedure considered it insufficient for a diagnostic study. For this prospective research study, approval was obtained All the patients were dismissed with written instructions and from our institutional Ethics Committee for Research Studies. contact numbers in case of complications after they were All subjects included provided informed consent. asked to mark in a visual analog pain scale the degree of pain/discomfort felt during the study. No antibiotics were pre- Population scribed either before or after the procedure. Patients from the fertility section of the Gynecology depart- Three days after the examination, patients were telephoni- ment at our institution were prospectively enrolled in this cally contacted to inquiry about potential complications and ongoing protocol from July 2010 to May 2014. the acceptability of the examination. The main inclusion criterion for this protocol was that patient should be of childbearing age, referred for diagnostic MRI of the Image Analysis pelvis with subsequent laparoscopic surgery as standard of care. Assessment of tubal patency was done independently by Exclusion criteria were: active infection of the pelvis, any two experienced radiologists with 8 and 6 years of experi- type of gynecological cancer, impossibility of undergoing ence in gynecologic radiology by using RAIM Alma® (Alma IT MR examination, pregnancy, known allergy to Gd and any Systems, Barcelona, Spain). They were blinded to all relevant gynecologic procedure performed between both diagnostic clinical information about the fallopian tubes (hysterosalpin- methods. gography, surgical resection, etc.). Other imaging findings (endometriosis, uterine morphology, ovarian pathology, etc.) Magnetic Resonance were also recorded in a tabular way. MR imaging was performed in a 1.5 Tesla scanner (Siemens Uterine enlargement was determined by a subjective assess- Avanto®, (Erlangen, Germany) . Patients were requested to ment. When there was discrepancy between their findings, attend the radiology department at least an hour before the agreement was reached by a joint reading of the images. study. Upon arrival they were taken to a private medical of- fice were they changed and removed all metallic objects. Af- Laparoscopic Chromotubation terwards, while lying in a gurney, using sterile technique, a Patients were operated on no longer than three months af- 5Fr or 7Fr hysterosalpingography catheter (Angiotech™, PBN ter the MR examination. Chromotubation was performed Medicals, Denmark) was placed inside the uterus of the pa- according to the surgical technique before the main surgi- tients with the help of a speculum. After uterine canalization, cal procedure. The gynecologist was blind to the MR-HSG the patients were kept in the gurney until the MR scanner results. became available. Patient transfer from the gurney to the After placing the patient under general anesthesia and fol- exam table was done with the help of bed-sheets while the lowing insertion of the trocars and laparoscopic camera, the patients remained still to avoid dislodgement of the catheter. disposable uterine manipulator, VCare (ConMed, Utica, NY) Once the patient was placed in the MR scanner, the cath- was placed and 10-20ml of methylene blue was injected eter was connected to an automated infusion pump (Optistar through the device into the uterine cavity to confirm spillage Elite Injector™, Mallinckrodt, Dublin, Ireland) that contained of the dye in the pelvic cavity and, therefore, check for tubal 60 ml of Gd diluted in saline solution (1:100). A body sur- patency (Fig. 1). Data was recorded in a tabular way. face coil was placed over the pelvis of the patients and they were positioned for pelvic MR. The routine examination pro- Data analysis tocol is detailed in Table 1. The dynamic images detailed in Continuous variables were reported as mean and standard the intrauterine contrast phase were performed before (VIBE deviation or median and interquartile range, according to the

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distribution observed. Categorical variables were described Results as proportions. Sensitivity, specificity, positive predictive value From all 42 patients that had agreed to participate and had (PPV), negative predictive value (NPV), precision and likeli- given consent, only 22 patients had already undergone MR hood ratios (LH) were estimated for the global Cotte test, and laparoscopy by the time this paper was written (an eli- considered positive or negative depending on the presence or gibility criterion for this interim analysis). Mean and standard absence of contrast, respectively, in the peritoneum. For the deviation for age, examination duration, injected volume and individual Cotte test, each fallopian tube was identified as degree of pain are summarized in Table 2. permeable or clogged. All estimations were calculated with a Out of the 22 patients that were analyzed, 2 MR-HSG and 1 95% confidence interval (CI). chromotubation could not be performed, resulting in a 91% Pain or discomfort during the study, measured by visual analog success rate for MR-HSG and 95% success rate for chromo- scale, were analyzed with a Mann-Whitney U Test for paired tubation. MR-HSG failure in two patients was due to catheter samples, using SPSS 20.0 (IBM Corp, Armonk, New York). Re- dislodgement secondary to compliant cervical orifices, while sults were considered statistically significant if p<0.05. chromotubation failure in one patient was due to the need to

Table 1: Magnetic resonance examination.

Study Phase Sequence Plane Angulation Repetition Exposure Field of Thickness orientation time (ms) time (ms) view (mm) (mm)

Non-Contrast T1-weighted Axial -15° 638 8.8 230 4 fat-suppressed turbo spin echo T2-weighted Axial -15° 5120 125 230 4 turbo spin echo T2-weighted Coronal 0° 4400 125 230 4 turbo spin echo T2-weighted Sagittal 0° 4200 125 230 4 turbo spin echo Fluid Attenuation Axial 0° 6600 423 254 1.87 Inversion Recovery Three-dimensional

Intrauterine Gradient echo Axial -15° 5.91 2.74 300 2.5 Contrast Volumetric Interpolated (VIBE) True-FIST Uterus Variable 198.1 1.37 380 3.5 oriented T1-weighted Coronal Variable 3.42 1.27 320 0.7 3d time-resolved to uterine angiographic cavity sequences

Intravenous T1-weighted fat- Axial -15° 638 8.8 230 4 Contrast suppressed turbo spin echo T1-weighted fat- Sagittal 0° 638 8.8 230 4 suppressed turbo spin echo

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a b

c d

Fig. 1 Axial T2-weighted (a) and T1-weighted (b) fat-saturated image post-intrauterine injection and (c) 3D volumetric reconstruction of a successful MR-HSG with bilateral contrast spillage post-gadolinium injection (arrows in b), clearly visible in volume reconstruction. As with conventional HSG, MR-HSG is not free from air bubble formation (arrowheads -), but in this latter method, bubbles are easily identified. (d) Confirmation of bilateral tubal patency is observed with chromotubation. convert surgery into a laparotomy. ing) in 22 patients at 72-hour follow-up and no major com- Injected volume was significantly different between patients plications. The bleeding was referred as spotting during the with enlarged uterus due to leiomyomas and patients with first 24 hours that would spontaneously disappear after that normal sized uterus (Fig. 2 and Table 2). Examination dura- lapse of time. tion and pain were not significantly different. Patient acceptance of the method was high: 91% of patients Individual and overall sensitivity and specificity data of MR- stated that they would “surely” (77%) or “most probably” HSG are shown in Table 3 and agreement between MR-HSG (14%) repeat the study. In patients with previous experience and laparoscopy is shown in Table 4. of hysterosalpingography the percentage of acceptance was There were 2 minor complications (clinically irrelevant bleed- 86% (6/7).

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Table 2: Population Data and Comparison between Enlarged Uterus and Non-enlarged Uterus.

Global Enlarged Non-Enlarged Mann-Whitney Enlarged vs Non-Enlarged

Age (years) 35 (4) 33.38 (3.6) 37.57 (4.4) Study duration (min) 49 (15) 52 (17.5) 44 (8.6) 0.338 Injected Volume (ml) 26 (16) 35.29 (21.5) 18.7 (3) 0.026 Intrauterine Pressure (psi) 10 (9) 14 (14) 8.6 (3.6) 0.742 Pain Scale 30 (19) 20.86 (15.9) 36.54 (17.8) 0.145

Values are expressed as mean (standard deviation)

Table 3: Sensitivity and Speciﬁcity of Magnetic Resonance Hysterosalpingography.

Sensitivity 95% confidence Specificity 95% confidence interval interval

Global Cotte 100 2-100 100 94.5-100 Left Cotte 100 51-100 100 94.2-100 Right Cotte 25 0-91.9 93.3 74.2-100

According to chromotubation: 1/19 had bilateral tubal occlusion, 1/19 had left unilateral tubal occlusion and 3/19 had right unilateral occlusion.

a b c

d e f

Fig. 2 Axial and sagittalT2-weighted images and maximum intensity projection (MIP) reconstruction of a normal (a, c and e) and an enlarged (b, d and f) uterus. Leiomyomas (arrows in b and d) are clearly identiﬁed on MR imaging and enlarge the uterus as well as the uterine cavity, which is deformed in the MIP image, as the contour of the dominant leiomyoma is observed (arrowheads). Enlarged uteruses required more contrast injection than normal-sized uteruses for a successful MR-HSG in our study group.

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Table 4: Agreement between magnetic resonance hysterosalpingography and chromotubation.

Agreement

Uterine morphology (normal vs altered) 100% Type of morphology 100% Uterine Size 86% Myomas (Presence vs abscence) 95% Number of Myomas* 31% Adenomiosis* (Presence vs abscence) 95% Hydrosalpinx (Presence vs abscence) 91% Adherences† (Presence vs abscence) 50% Endometriosis (Presence vs abscence) 82% Non endometriotic ovarian pathology (Presence vs abscence) 91%

*MR showed more pathology than surgery †Chromotubation showed more pathology than MR

Discussion occlusion (n=3) and laparoscopy showed patency, unobstruc- Our initial results in the diagnostic performance of MR-HSG tion might have been reached by MR-HSG, but further stud- for tubal patency evaluation have shown high sensitivity and ies and a larger number of patients are needed to support specificity when compared to the true gold standard for tubal this assumption. patency assessment, laparoscopic chromotubation (Fig. 1 and Apart from the benefits of visualizing tubal patency without 3). Even when considering each fallopian tube individually, iodide and radiation, MR-HSG also helped to detect previ- and despite not being able to see in some of the patients the ously unknown diseases in our study population, as it has 11 contour of the tube itself, high sensitivity and specificity were also been reported in previous studies . Specifically, up to observed for the left fallopian tube and high specificity was 23% of our study population were found to have a condition seen for the right fallopian tube. The low sensitivity observed they were not aware of, (which reinforces the potential of in the latter remains unexplained and warrants further inves- this procedure to become the single examination required for tigation in a larger population sample. patients with fertility issues). Furthermore, most of the find- Even though other studies have analyzed MR-HSGs potential ings reported in MR-HSG correlated with those reported in for tubal patency assessment and have already yielded good surgery. Poor correlation between MR-HSG and surgery was results, the use of a flawed gold standard, such as conven- only found in the case of peritoneal adherences, as flimsy ad- tional HSG, left margin for a reasonable doubt in respect to herences could not be detected by MR sequences, resulting its true potential, thus precluding solid evidence-based rec- in an underestimation of pelvic endometriosis. ommendation1,8,10-15. Nevertheless, if we compare our results Although Gadolinium is not being currently marketed for in- to those published (which compare MR-HSG to conventional trauterine use, many reports have shown its safe use as a HSG alone or conventional HSG in combination with lapa- iodine surrogate for allergic patients in conventional HSG and roscopy), we can observe a high degree of agreement in that MR-HSG , and it has also been shown not to affect reproduc- 1,8,10-14,16-19 positive spillage is correctly diagnosed with specificities near tive function in animals . or at 100%11-13. In our study, gadolinium was used in a 1:100 dilution, as in Our results on tubal occlusion could not be compared with other published report, because of its good diagnostic perfor- 11,12 those obtained by other authors either because in those stud- mance at that concentration . It is worth noting that this ies MR-HSG was not the initial examination or because lapa- dilution is significantly lower than when used as a iodine sur- roscopy was not performed in patients with unilateral occlu- rogate (in this case no dilution is performed given the lower 17,18 sion11,12,15. Furthermore, some authors detected more patent density of Gd) . The mean volume used in this study was tubes with MR-HSG than with conventional HSG, which was 26 ml, although larger volumes (mean: 35.29 ml) were need- attributed to either higher tissue contrast or to a secondary ed for enlarged uterus. This variable should be considered outcome of the initial procedure11,12. We could also hypoth- when performing this test in myomatous uterus or enlarged esize that in our cases in which MR-HSG showed unilateral uterus due to other pathologies (e.g. adenomyosis).

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a b

Fig. 3 Maximum intensity projection (a) and volumetric reconstruction (b) in a 29-year-old patient with previous history of endometriosis and right adnexectomy. Lack of passage of gadolinium into the right fallopian tube is consistent with her medical history. Lack of spillage of contrast from the left fallopian tube, which appears slightly dilated. Chromotubation conﬁrmed our ﬁnding.

As regards study duration, our mean study duration was lon- This does not allow us to fully ascertain that the sensitivity ger than that reported in other published studies8. However, and specificity of MR-HSG are those shown by our findings. our examination protocol included a routine pelvic MRI that Furthermore, the small number of patients and the absence accounted for 80% or morte of the MR examination. We of false positives and false negatives in the estimation of hypothesize that once MR-HSG is introduced in our clinical global and left Cotte test sensitivity yield a large confidence routine, a fast examination protocol with three plane T2- interval. It is expected that his value will be similar to that weighted turbo spin echo and the sequences used for tubal reported in conventional HSG if in the future a larger number patency will be enough to evaluate 90% of patients in ex- of false positive and false negative results start to appear in aminations no longer than 15 minutes duration. Those cases patients in this ongoing study. However, no other MR-HSG requiring further testing could complete the MR-HSG with publication has compared all of their patients against chro- a full pelvic MRI protocol and intravenous Gd injection in a motubation, which is the currently accepted gold standard subsequent day. method for tubal patency and the one that was then used to In addition, in our study group, 3D fluid-attenuated inver- evaluate conventional HSG6. sion-recovery (FLAIR) sequence, of approximately 4 minutes, Another weakness of this study is that only a 1.5T scanner was was part of the examination protocol in order to evaluate used. This means that, although not expected to be worse, Rouanet De Lavit et al. data 20 on better visualization of en- our results might not be a reliable predictor of diagnostic per- dometrial tissue using this sequence, which also influenced formance of MR-HSGs performed with 3T scanners. our study times. Despite all this, no patient discontinued the Finally, even if a dynamic sequence was used to evaluate cor- examination due to the long study duration. rect gadolinium filling of the uterus, the great dynamic assess- Pain was assessed with a visual analog pain scale, which ment provided by radioscopy during conventional HSG with a showed great tolerability (mean 30/100) and good correla- global overview and the distinct contrast progression through tion with previously published literature reports, although each fallopian tube is missing. Nevertheless, we have observed none had evaluated pain as objectively13,14. The acceptance that individual fallopian tube assessment is not impossible rate of the procedure, assessed by a telephone interview in- without that information. , also It is expected that as MR tech- quiring whether patients would repeat the study in the fu- nology and sequences evolve, a proper sequence that might ture, is also consistent with previously published literature8. allow visualization and assessment of contrast progression The main weakness of this work is the small study population. through the fallopian tubes will become available.

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4. Troiano RN, McCarthy SM. Mullerian duct anomalies: imaging and clinical Conclusion issues. Radiology. 2004;233(1):19-34. In our study, MR-HSG has proved to be a feasible and safe al- 5. Woodward PJ, Wagner BJ, Farley TE. MR imaging in the evaluation of ternative to conventional or virtual HSG, sonohysterography, female infertility. Radiographics. 1993;13(2):293-310. 6. Swart P, Mol BW, van der Veen F, van Beurden M, Redekop WK, Bossuyt and chromotubation. This method has high overall sensitiv- PM. The accuracy of hysterosalpingography in the diagnosis of tubal pa- ity and specificity for tubal patency detection, a high success thology: a meta-analysis. Fertil Steril. 1995;64(3):486-91. 7. Broeze KA, Opmeer BC, Van Geloven N, Coppus SF, Collins JA, Den Har- rate and patient acceptance, being also capable of evaluating tog JE, et al. 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Furuhashi M, Miyabe Y, Katsumata Y, Oda H, Imai N. Magnetic resonance the Declaration of Helsinki. imaging with gadolinium-diethylenetriamine pentaacetic acid is useful in assessment of tubal patency in a patient with iodine-induced hypothyroid- Confidentiality of data. The authors declare that they have ism. Magn Reson Imaging. 1998;16(3):339-41. followed the protocols of their work center on the publica- 11. Ma L, Wu G, Wang Y, Zhang Y, Wang J, Li L, et al. Fallopian tubal patency diagnosed by magnetic resonance hysterosalpingography. J Reprod Med. tion of patient data. 2012;57(9-10):435-40. Right to privacy and informed consent. The authors have ob- 12. Sadowski EA, Ochsner JE, Riherd JM, Korosec FR, Agrawal G, Pritts EA, tained the informed consent of the patients and/or subjects et al. MR hysterosalpingography with an angiographic time-resolved 3D pulse sequence: assessment of tubal patency. AJR Am J Roentgenol. mentioned in the article. The corresponding author is in pos- 2008;191(5):1381-5. session of this document. 13. Unterweger M, De Geyter C, Frohlich JM, Bongartz G, Wiesner W. Three- dimensional dynamic MR-hysterosalpingography; a new, low invasive, radiation-free and less painful radiological approach to female infertility. Conflicts of interest Hum Reprod. 2002;17(12):3138-41. The authors declare no conflicts of interest, except for Dr. Ko- 14. Wiesner W, Ruehm SG, Bongartz G, Kaim A, Reese E, De Geyter C. Three- dimensional dynamic MR hysterosalpingography: a preliminary report. Eur han, who declares a possible conflict of interest as member Radiol. 2001;11(8):1439-44. of the Writing Committee of Revista Argentina de Radiología 15. Winter L, Glucker T, Steimann S, Frohlich JM, Steinbrich W, De Geyter C, et al. Feasibility of dynamic MR-hysterosalpingography for the diagnostic work-up of infertile women. Acta Radiol. 2010;51(6):693-701. 16. Belt MM, Rodenko G, Taylor K, Maguire C, Bello S. 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