{"paper_id":"9ce10168-b10d-4f40-912d-8258019e3490","body_text":"R E S E A R C H A R T I C L E Open Access\nComparison of uterine and tubal pathology\nidentified by transvaginal sonography,\nhysterosalpingography, and hysteroscopy\nin female patients with infertility\nCatherine H. Phillips 1*, Carol B. Benson 1, Elizabeth S. Ginsburg 2 and Mary C. Frates 1\nAbstract\nBackground: The causes of female infertility are multifactorial and necessitate comprehensive evaluation including\nphysical examination, hormonal testing, and imaging. Given the associated psychological and financial stress that\nimaging can cause, infertility patients benefit from a structured and streamlined evaluation. The goal of such a work\nup is to evaluate the uterus, endometrium, and fallopian tubes for anomalies or abnormalities potentially\npreventing normal conception. To date, the standard method for assessing these structures typically involves some\ncombination of transvaginal sonography (TVS), hysterosalpingography (HSG), and hysteroscopy (HSC). The goal of\nthis review is to compare the diagnostic accuracy of TVS, HSG, and HSC for diagnosing abnormalities in infertility\npatients to determine if all studies are necessary for pre-treatment evaluation.\nResults: We identified infertility patients prior to initiation of assisted reproductive technology who had baseline TVS,\nHSG, and HSC within 180 days of each other. From medical record review, we compared frequencies of each finding\nbetween modalities. Of the 1274 patients who received a baseline TVS over 2 years, 327 had TVS and HSG within\n180 days and 55 patients had TVS, HSG and HSC. Of the 327, TVS detected fibroids more often than HSG (74 vs. 5,\np < .0001), and adenomyosis more often than HSG (7 vs. 2, p = .02). HSG detected tubal obstruction more often than\nTVS (56 vs. 8, p = .002). Four (1.2 %) patients had endometrial polyps on both HSG and TVS.\nIn the 55 patients with HSG, TVS, and HSC, HSC identified endometrial polyps more often than TVS (10 vs. 1, p =. 0 0 0 1 )\nand HSG (10 vs. 2, p = .0007). TVS detected more fibroids than HSC (17 vs. 5, p < .0001). Tubal obstruction was identified\nmore often by HSG than HSC (19 vs. 5, p <. 0 0 0 1 ) .\nConclusions: TVS is superior for evaluation of myometrial pathology. HSG is superior for evaluation of tubal pathologies.\nEndometrial pathologies are best identified with HSC.\nKeywords: Infertility, Transvaginal sonography, Hysterosalpingography\nBackground\nInfertility is defined as the inability for a couple to con-\nceive a pregnancy following 1 year of unprotected vagi-\nnal intercourse [1]. It is estimated that 10 –15 % of\ncouples seek treatment for infertility [1 –3]. It is generally\nconsidered appropriate to evaluate a couple for causes of\ninfertility after 1 year of failed attempts at conception.\nHowever, given the inverse relationship of female fertility\nwith age, it is often recommended that women over\n35 years of age be evaluated after 6 months of failure to\nconceive, and women older than 40 be evaluated imme-\ndiately [1].\nA variety of factors may affect normal fertility includ-\ning patient age, anatomy, ovulatory status, and sperm\nquality. Potential causes of infertility can be divided into\nmale and female causes and include endocrine, ana-\ntomic, genetic, and behavioral conditions [4]. As a result,\nthe evaluation of the infertile couple is multifactorial,\n* Correspondence: chawley1@partners.org\n1Department of Radiology, Brigham and Women ’s Hospital, Harvard Medical\nSchool, 75 Francis Street, Boston, MA 02115, USA\nFull list of author information is available at the end of the article\n© 2015 Phillips et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0\nInternational License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and\nreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to\nthe Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver\n(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.\nPhillips et al. Fertility Research and Practice  (2015) 1:20 \nDOI 10.1186/s40738-015-0012-3\n\nnecessitating physical examination, hormonal testing, and\nimaging. Because the infertility population is under a great\ndeal of psychological and emotional stress, these patients\nbenefit from a structured and streamlined evaluation. In\nparticular, evaluation of the female partner attempting to\nconceive requires assessment of the uterus, endometrium,\nand fallopian tubes for anomalies or abnormalities poten-\ntially preventing normal conception. The best method for\nassessing these structures usually involves some combin-\nation of transvaginal sonography (TVS), hysterosalpingog-\nraphy (HSG), and hysteroscopy (HSC). Less often, pelvic\nmagnetic resonance imaging (MRI) and saline infusion\nsonohysterography (SIS) are used.\nThe objective of this paper is to compare the diagnos-\ntic accuracy of TVS, HSG, and HSC for diagnosing uter-\nine and tubal abnormalities in women with infertility to\ndetermine if all three modalities are necessary in the\nwork up of these patients.\nMethods\nWe identified all baseline TVS performed on women in\nour infertility program from October 12, 2011 to October\n12, 2013, prior to their initiation of assisted reproductive\ntechniques (ART). From this group, we narrowed our pa-\ntient population to those who had an HSG within 180 days\nof the TVS to maximize the likelihood of concordance\nbetween the studies. All TVS and HSG reports were\nreviewed for tubal, myometrial, or endometrial findings\nand anatomical variants.\nWe reviewed patient medical records to identify those\npatients who also had hysteroscopy (HSC) within 180 days\nof the baseline TVS, and we recorded the reported\nfindings.\nMyometrial abnormalities were categorized as fibroids\nor adenomyosis; endometrial abnormalities as polyps,\ncysts, cavity distortion (e.g., synechia, stricture), or non-\nspecific asymmetry; and tubal abnormalities as obstruc-\ntion. For each abnormality, the frequency of detection\nby each modality (TVS, HSG, HSC) was tabulated. For\nTVS, visualization of a hydrosalpinx was classified as an\nobstructed fallopian tube. Detection rates of abnormal-\nities were compared among the modalities using the\nFisher exact test, with a p-value of <0.05 considered\nsignificant.\nThis study was approved by the Brigham and Women ’s\nHospital Institutional review board, protocol number\n2014P000355.\nResults\nA total of 1274 patients received a baseline TVS as part\nof a work up for infertility during the study period.\nAmong these patients, 327 underwent a diagnostic HSG\nwithin a 180-day interval of the sonogram and comprise\nour study population. The time between TVS and HSG\nwas 94 ± 49 days (mean ± SD). Among our 327 study pa-\ntients, 55 also underwent HSC. The time (mean ± SD)\nbetween TVS and HSC was 61 ± 41 days and between\nHSG and HSC was 61 ± 50 days.\nAmong the study population of 327 patients (Table 1), 74\n(23 %) had fibroids and 7 (2 %) had adenomyosis as diag-\nnosed by either modality. Endometrial abnormalities were\nf o u n di n1 6( 5% )p a t i e n t s ,b a s e do nT V So rH S G .T u b a l\nobstruction was found in 56 (17 %) patients, more com-\nmonly unilateral (47 patients) than bilateral (9 patients).\nTVS detected myometrial abnormalities significantly\nmore often than did HSG, identifying fibroids in 74 pa-\ntients while HSG only identified 5 (Fig. 1), and detecting\nadenomyosis in 7, while HSG detected only 2 ( p < .0001\nfor both comparisons). Both HSG and TVS diagnosed\nendometrial polyps in the same 4 patients. HSG detected\n6 patients with cavity distortion, while TVS found none\nof these ( p < 0.002). With respect to tubal abnormalities,\nHSG performed significantly better than TVS, detecting\ntubal obstruction in all 56 (Fig. 2), while ultrasound only\ndiagnosed 8 ( p < .0001) (Fig. 3).\nAmong the subset of 55 patients who were evaluated\nby all three modalities, TVS, HSG, and HSC (Table 2),\n17 (31 %) had fibroids and 6 (11 %) had adenomyosis.\nEndometrial abnormalities were found in 13 (24 %) pa-\ntients and tubal obstruction in 19 (35 %).\nIn this group, TVS detected myometrial abnormalities\nsignificantly more often than did HSC, which identified\nonly 4 of the 17 patients with fibroids ( p < .0001) and\nnone of the patients with adenomyosis. With respect to\nendometrial abnormalities, HSC outperformed TSV and\nHSG, identifying 10 polyps, while TVS only detected 1\nTable 1 Myometrial, endometrial, and tubal abnormalities\ndetected by transvaginal ultrasound and/or\nhysterosalpingography ( N = 327)\nCategory TVS HSG Statistical significance\nMyometrium\nFibroids 74 (23 %) 5 p < .0001\nAdenomyosis 7 (2 %) 2 p < .0001\nCesarean scar 1 0\nEndometrium\nPolyps 4 4\nCysts 4 0\nCavity distortion 0 6 p < 0.002\nNonspecific asymmetry 0 2\nTubes\nTotal obstructed 8 56 (17 %) p < .0001\nUnilateral 7 47\nBilateral 1 9\nAnomalies 4\nAbbreviations: TVS transvaginal ultrasound, HSG hysterosalpingography\nPhillips et al. Fertility Research and Practice  (2015) 1:20 Page 2 of 6\n\n(p = .0001) and HSG only 2 ( p = .0007). HSG outper-\nformed HSC for tubal obstruction, which only detected\n5 of the 19 patients with unilateral or bilateral obstruc-\ntion (<0.0001)\nDiscussion\nDiagnostic imaging plays an important role in the as-\nsessment of women with infertility. Although no consen-\nsus protocol for work up of these patients exists, the\nmajority of infertility patients undergo a baseline TVS\nand HSG. TVS is used for evaluating ovaries, fallopian\ntubes, and the adnexa and is a favored imaging modality\nin the infertility population because it is readily available,\nrelatively low cost, and does not use ionizing radiation.\nTVS is the test of choice for diagnosing polycystic ovary\nsyndrome [5], and is helpful for identifying endometri-\nosis and the sequelae of PID. In addition, TVS is invalu-\nable for monitoring ovarian folliculogenesis during\ntreatment with ART [6 –8]. In contrast, HSG provides\ninformation about tubal patency and uterine cavity ab-\nnormalities such as anomalies, polyps, synechiae, and\nadhesions, any of which could interfere with embryo im-\nplantation [9]. However, HSG offers limited evaluation\nof the cervix and myometrium and does carry the small\nrisks of contrast reaction and of ionizing radiation ex-\nposure [10]. Besides TVS and HSG, supplemental evalu-\nation with SIS and hysterosalpingo-contrast sonography\n(HyCoSy) is sometimes performed. These imaging pro-\ncedures are becoming more popular because of their\nability to combine TVS adnexal evaluation with HSG-\nlike assessment of the uterine cavity, without the risks of\ncontrast reactions and radiation exposure [11 –13], but\nare not yet universally available.\nMRI of the pelvis offers multi-planar imaging and does\nnot require the use of ionizing radiation. It is an excel-\nlent modality for detecting endometriosis [5] and is\nhelpful for determine the nature of uterine duplication\nanomalies, leiomyomas, and adenomysis [14 –18]. MRI is\nalso employed for evaluating intracranial causes of infer-\ntility, such as pituitary adenomas. However, due to its\nhigh cost and limited access, MRI is not typically used in\nthe infertility assessment except for a specific indication\nrequiring such imaging.\nFig. 1 a 38-year-old G1P1 female with a history of infertility presenting for baseline assessment prior to initiation of ART. Coronal transvaginal\nsonographic image through the uterus demonstrates a 6.0 × 4.2 × 3.9 cm left sided mass with heterogenous echotexture and an echogenic rim,\nconsistent with a large calcified intramural fibroid. b HSG demonstrates a normal endometrial cavity without filling defects to suggest fibroids as\nseen on TVS. The fallopian tubes are normal in caliber and demonstrate free intraperitoneal spill of contrast bilaterally\nFig. 2 36 year-old G2P1A1 female with a history of infertility ×\n3 years, presenting for baseline assessment of tubal patency prior to\ninitiation of ART. HSG demonstrates normal contour of the endometrial\ncavity. The left fallopian tube opacifies normally and demonstrates free\nintraperitoneal spill. The right fallopian tube fills with contrast, but\nterminates abruptly near its terminus (arrowhead). No right sided\ncontrast spill is identified, diagnostic of distal tubal obstruction. This\ntubal obstruction was not appreciated on TVS or HSC\nPhillips et al. Fertility Research and Practice  (2015) 1:20 Page 3 of 6\n\nAt our institution, we begin the infertility assessment\nwith an HSG. If there is evidence of an abnormal uterine\ncavity from etiologies such as uterine septa, submucosal\nfibroids, synchiae, or polyps, HSC is then typically per-\nformed [19 –21]. The standard practice at our institution\nis to perform HSC in the office setting, reserving opera-\ntive HSC and laparoscopy for patients who are not able\nto tolerate office based procedures and for situations for\nwhich surgical correction is required, such as septoplasty\nfor the correction of a subseptate uterus. Hysteroscopy\nis also preformed prior to ART if there is a 6 month or\ngreater delay between the HSG and ART. TVS is ob-\ntained when patients begin ART, and continues during\nfolliculogensis.\nOur results indicate that TVS is superior to HSG for\ndetection of myometrial pathology, including fibroids\nand adenomyosis. These results make intuitive sense, as\nTVS uses high frequency sound waves to evaluate the 3\ndimensional volume and echotexture of the uterine tis-\nsue, while HSG uses radiographs and contrast dye to\noutline the endometrial cavity. By assessing the contour\nof the contrast-filled cavity, information about the sur-\nrounding myometrium can be inferred, but not diag-\nnosed, because the tissue itself is not imaged directly.\nHSG may detect submucosal fibroids, but other myome-\ntrial pathology, such as intramural or subserosal fibroids,\nare likely to be missed. Similarly, TVS is superior to\nHSC, which visualizes the walls of the uterine cavity but\ncannot assess for lesions within the myometrium.\nOur results also indicate that HSG is the superior mo-\ndality for detection of tubal pathology, specifically tubal\nobstruction. This finding is in keeping with the functional\ncomponent of HSG, which allows the operator to visualize\nin real-time contrast medium passing through the tubes\nand most importantly, spilling into the surrounding peri-\ntoneum. TVS can only infer tubal obstruction when a\nFig. 3 a 38-year-old G2P2 female with history of male factor infertility presenting for baseline assessment prior to initiating ART. Transvaginal\ngrey-scale image of the left adnexa demonstrates an anechoic tubular structure (calipers), measuring 43 × 31 × 19 mm, separate from the left\novary (not shown) and consistent with hydrosalpinx. b HSG demonstrates contrast pooling within a dilated, blind ending fallopian tube (arrows),\nconfirming the presence of a left sided hydrosalpinx. The right fallopian tube is normal in caliber and demonstrates free intraperitoneal spill of\ncontrast, indicating tubal patency\nTable 2 Myometrial, endometrial, and tubal abnormalities\ndetected by each modality ( N = 55)\nCategory TVS HSG HSC Statistical\nsignificance\nMyometrium\nFibroids 17 (31 %) 6 4 p < .0001\n(TVS vs HSC)\nAdenomyosis 6 (11 %) 0 0\nEndometrium\nPolyps 1 2 10 p = .0001\n( HSC vs TVS)\np = .0007\n(HSC vs HSG)\nCysts 1 0 0\nCavity distortion 0 4 2\nNonspecific asymmetry 0 2 1\nTubes\nTotal Obstructed 6 19 (35 %) 5 <0.0001\n(HSG vs HSC)\nUnilateral 6 16 5\nBilateral 0 3 0\nAnomalies 0 1 31\nAbbreviations: TVS transvaginal ultrasound, HSG hysterosalpingography,\nHSC hysteroscopy\nPhillips et al. Fertility Research and Practice  (2015) 1:20 Page 4 of 6\n\nhydrosalpinx is present, therefore obstructed but nondis-\ntended fallopian tubes will be missed with sonography\nalone. Endometrial pathologies, specifically endometrial\npolyps, were more frequently identified on direct\nvisualization with HSC than on TVS and HSG combined.\nIt is possible that, for some of our patients, the HSC pre-\nceded the TVS and/or HSG and, thus, polyps could have\nbeen removed by the time of imaging evaluation. While\nTVS and HSG are both potential screening modalities for\nendometrial lesions, HSC is required for optimal diagnosis\n(Fig. 4), and one reason why flexible office hysteroscopy\nremains the gold standard for endometrial assessment.\nA weakness in our study is that we did not assess SIS as\na method to evaluate the endometrium. This procedure is\nincluded in some protocols during the work up of women\nwith infertility, but is not part of the routine assessment at\nour institution. SIS has been shown to be superior to TVS\nfor identifying endometrial abnormalities including polyps\nand cavity distortion [11, 13, 22 –27]. Some reports have\nalso shown SIS to be comparable to the gold standard of\nHSC for evaulation of intrauterine abnormalities including\npolyps, submucosal fibroids, adhesions and uterine anom-\nalies, with a sensitivity and specificity for detection of 88\nand 94 %, respectively [28, 29]. In addition, none of our\npatients were evaluated by HyCoSy, a procedure that uses\naerated saline or contrast to assess tubal patency with\nTVS. HyCoSy has been shown to be comparable to HSG\nwith regards to assessing tu bal patency, with sensitiv-\nity ranges from 75 –96 % and specificity from 67 –100 %\n[12, 13, 30, 31]. SIS and HyCoSy can be done in a single\nvisit and together provide information about the uterine\ncavity and the patency of the fallopian tubes, similar to\nHSG, but with added information about the myometrium\nfrom the TVS component, all without exposure to ioniz-\ning radiation or iodinated contrast. Despite these advan-\ntages, HyCoSy does not provide anatomical information\nabout the fallopian tubes, which limits its utility.\nGiven the lack of a single all encompassing imaging\ntool for accurately diagnosing endometrial, tubal, and\nmyometrial causes of infertility, it could be helpful to\noutline one ste p-wise approach for use of the TVS, HSG,\nand HSC. Although there is tremendous variability be-\ntween practices, at our institution most infertility pa-\ntients undergo both a TVS and HSG prior to initiating\nART. Others have found that SIS and HyCoSy provide\ncomparable information as TVS and HSG combined. If\nfindings of these tests suggest an abnormality within the\nuterine cavity, which could prevent implantation of a vi-\nable gestational sac, the patient will be referred for a\nHSC for direct inspection and possible treatment. How-\never, the management of abnormal tubal pathology on\nHSG will vary depending on plan for reproductive ther-\napy. If the patient is an In-vitro Fertilization (IVF) candi-\ndate, tubal obstruction is not of much consequence, as\nthe embryo is directly implanted into the uterus. However,\nif the patient is not a candidate for IVF , tubal obstruction\ncan be further managed with surgical interventions such\nas tuboplasty or salpingostomy.\nConclusion\nOur study compared the results from TVS, HSG, and\nHSC in a cohort of female infertility patients. TVS was\nsuperior for detecting myometrial pathology, HSG was\nsuperior for evaluating tubal patency, and HSC detected\nFig. 4 a 44 year-old G0P0 female with inability to conceive for 4 years presents for baseline assessment prior to IVF. TVS demonstrates an 11 ×\n11 × 10 mm echogenic lesion within the left aspect of the endometrial cavity (calipers). Flow was demonstrated within the lesion with color\nDoppler, raising the possibility of endometrial polyp. b Corresponding HSG demonstrates a depended rounded filling defect within the left\naspect of the endometrial cavity, which persisted on multiple projections, suggestive of a polyp. The fallopian tubes are normal in caliber and\npatent. The patient went on to HSC, where the lesion proved to be a submucosal fibroid\nPhillips et al. Fertility Research and Practice  (2015) 1:20 Page 5 of 6\n\nmore endometrial polyps than HSG and TVS. No single\nmodality provided accurate identification of all different\npathologies. Complete work up of women with infertility\nmay include all modalities, given the unique information\nobtained from each. However, with knowledge of the\nunique specificity of each imaging test to detect specific\npathologies, a combination of HSG, HSC and TVS could\nbe selected based on the clinical presentation of patients.\nCompeting interests\nThe authors declare that they have no competing interests.\nAuthors’ contribution\nCP helped to conceive of this study, lead data collection, reviewed the\nliterature, and drafted this manuscript . CB participated in statistical analysis\nas well as reviewing the manuscript. EG helped to select references and\naided in interpretation of hysteroscopic reports. MF conceived of the study\nand participated in its design and coordination as well as helped to draft the\nmanuscript. All authors read and approved the final manuscript.\nAcknowledgements\nNo other persons, besides those mentioned in the authorship, significantly\ncontributed towards this study. There were no sources of funding for this\nresearch paper, all authors dedicated their academic time towards the\npreparation and design of this study.\nAuthor details\n1Department of Radiology, Brigham and Women ’s Hospital, Harvard Medical\nSchool, 75 Francis Street, Boston, MA 02115, USA. 2Department of Infertility\nand Reproductive Surgery, Obstetrics and Gynecology, Brigham and\nWomen’s Hospital, Harvard Medical School, 75 Francis Street, Boston, MA\n02115, USA.\nReceived: 9 November 2015 Accepted: 15 December 2015\nReferences\n1. McLaren JF. Infertility evaluation. Obstet Gynecol Clin North Am.\n2012;39:453–63.\n2. Chandra A, Martinez GM, Mosher WD, Abma JC, Jones J. Fertility, family\nplanning, and reproductive health of U.S. women: data from 2002 National\nSurvey of Family Growth. Vital Health Stat. 2012;23:1 –160.\n3. Chandran A, Copen CE, Stephen EH. 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Luciano DE, Exacoustos C, Luciano AA. Contrast ultrasonography for tubal\npatency. J Min Invasive Gynecol. 2014;21:994 –8.\n•  We accept pre-submission inquiries \n  Our selector tool helps you to find the most relevant journal\n  We provide round the clock customer support \n  Convenient online submission\n  Thorough peer review\n  Inclusion in PubMed and all major indexing services \n  Maximum visibility for your research\nSubmit your manuscript at\nwww.biomedcentral.com/submit\nSubmit your next manuscript to BioMed Central \nand we will help you at every step:\nPhillips et al. Fertility Research and Practice  (2015) 1:20 Page 6 of 6","source_license":"CC0","license_restricted":false}