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  Sonographic evaluation of first-trimester bleeding Raj Mohan Paspulati, MD*, Shweta Bhatt, DMRD, DMRE, Sherif Nour, MD  Department of Radiology, University Hospitals of Cleveland, Case Western Reserve University, 11100 Euclid Avenue,Cleveland, OH 44106, USA Vaginal bleeding in the first trimester of preg-nancy is a common presentation in emergency carefacilities. About 25% of all gestations present withvaginal spotting or frank bleeding in the first fewweeks of pregnancy; half of these progress intomiscarriage or abortion[1].The acuity of these symptoms may vary from occasional spotting to se-vere hemorrhage, associated with cramping and ab-dominal pain. The bleeding often is self-limited andis most likely caused by implantation of the concep-tus into the endometrium. The important causes of first-trimester bleeding are spontaneous abortion, ec-topic pregnancy, and gestational trophoblastic dis-ease. The clinical assessment of pregnancy outcomeis unreliable and ultrasound (US) evaluation com- bined with quantitative beta human chorionic gonado-tropin ( b -hCG) is an established diagnostic tool inthese patients. This article reviews the role of ultra-sonography in the evaluation of patients presentingwith first-trimester bleeding. Sonographic anatomy The uterus is a pear-shaped, muscular organ that varies greatly in size and shape depending on age and prior pregnancies. The normal postpuberty uterus inan adult measures approximately 7.5 to 8 cm inlength, 4 to 5 cm in width, and about 2 cm in an-teroposterior dimension. The normal cervix is 3.5 to4 cm in length. The cervix is comprised of internaland external cervical os. The internal os is the junction of the uterine cavity and the cervical canaland the external os is the junction of the cervicalcanal and the vagina. Transvaginal US (TVUS) of thenormal myometrium reveals three distinct layers.Arcuate vessels separate the thin outer layer fromthe thick middle layer, and both layers are homoge-neous with the outer layer more hypoechoic relativeto the middle layer [2].The inner layer consists of a thin hypoechoic halo that surrounds the endometriumand corresponds to the junctional zone seen on MR imaging. The endometrial thickness measurementsare optimally made on sagittal (long-axis) images of the uterus; this measurement should be performedon the thickest portion of the endometrium excludingthe hypoechoic inner myometrium(Fig. 1).The en- dometrial thickness should be reported as the ‘‘dou- ble thickness’’ measurement [3].If endometrial fluid is present, its diameter should be omitted; in suchcases the endometrial thickness should be reportedas the sum of the measurements obtained from theanterior and posterior endometrial walls. An endo-metrial thickness of 4 to 14 mm is normal in an adult  premenopausal woman. Endometrial thickness andappearance vary with the phase of the menstrualcycle[4].The position of the ovaries is variable but they areusually found in the posterior fold of the broadligament, posterior and distal to the fallopian tubes.On sonography the ovaries can be localized anterior to the internal iliac vessels. The postpubertal ovarymeasures approximately 3 cm in length, 2 cm inwidth, and 1 cm in anteroposterior dimension. Theupper limit for normal ovarian volume is highest inyoung adult women measuring approximately 9.8 to14 mL and declines with increasing age[5].Normal 0033-8389/04/$ – see front matter  D 2004 Elsevier Inc. All rights reserved.doi:10.1016/j.rcl.2004.01.005* Corresponding author.  E-mail address: paspulati@uhrad.com (R.M. Paspulati).Radiol Clin N Am 42 (2004) 297–314  fallopian tubes cannot be visualized with current USimaging equipment  Scanning technique Ultrasound evaluation of the female pelvis isconducted with a real-time scanner, preferably usinga sector or curvilinear transducer. The scanner isadjusted to operate at the highest clinically appropri-ate frequency, realizing that there is a trade-off  between the resolution and beam penetration.Transabdominal pelvic US is performed with afull bladder using transducer frequencies of 3.5 MHzand above. Adequate distention of the bladder dis- places the bowel from the field of view. Transab-dominal US gives an initial overview of the uterus,adnexa, and any intra-abdominal free fluid. TVUS is performed with the patient’s bladder being empty,using a transducer frequency of 5 to 7.5 MHz. TVUSgives detailed information about the uterus and theadnexa. Higher-frequency transvaginal probes can be positioned closer to the pelvic organs resulting inimproved spatial resolution and diagnostic accuracy.Currently available transducers of 10 MHz and abovecan identify the finer details of intrauterine gestationand have greatly contributed to the early diagnosis of abnormal gestation and to the management of first-trimester bleeding. Color flow Doppler and pulsedDoppler may be added to the examination, as indi-cated by the gray-scale US findings. It is important to bear in mind that the energy output of Doppler US issubstantially higher than that used for imaging and it may have potentially harmful effects on the concep-tus[6].Because of this risk, caution has been expressed over the routine use of Doppler US inearly pregnancy evaluation. While performing Dopp-ler US in early pregnancy, the concept of ‘‘as low asreasonably achievable’’ is important [7]and the advantages of the Doppler US should outweigh the potentially harmful effects on the conceptus. Normal first-trimester sonography Scanning in the first trimester may be performedeither transabdominally or transvaginally. TVUS is preferred and is the community standard. The f irst-trimester milestones are given inTables 1 and 2.A gestational sac can be identified with TVUS at 5 weeks of gestational age, when it measures 5 mm.The yolk sac should always be seen by TVUS whena gestational sac measures greater than 10 mm and by transabdominal US when the mean sac diameter is greater than 20 mm[8,9].An embryo with car- diac activity should be seen transvaginally when thegestational sac measures greater than 18 mm, andtransabdominally when the gestational sac measures2.5 cm. These discriminatory criteria should be usedas guidelines. If the findings of the US examinationare equivocal and the examination is technicallydifficult, a follow-up examination should be obtained. Gestational sac The blastocyst implants into the endometrium byapproximately 23 days of menstrual age[10].It mea- sures 0.1 mm and is too small to be visualized onTVUS. Demonstration of peritrophoblastic flow bytransvaginal color flow Doppler at this focal decidualthickening has improved the diagnostic sensitivity of intrauterine pregnancy (IUP) from 90% with TVUSalone to 99% using transvaginal color flow Dopp-ler [11,12].The peritrophoblastic flow has a charac- teristic high-velocity and low-impedance flow caused by shunting of blood from the spiral arteries into theintervillous spaces. According to Emerson et al[11], the peak systolic velocity of peritrophoblastic flowin a normal IUP ranges from 8 to 30 cm/second, be-fore the visualization of the gestational sac. Yeh et al Fig. 1. Sagittal TVUS of the uterus demonstrates a normalendometrial lining ( arrowheads ).Table 1First-trimester scanning milestonesParameter Transabdominal US Transvaginal USGestational sac — Present at 5 wk (5 mm)Yolk sac Always present if GS > 20 mmAlways present when GS > 10 mmCardiac activity GS > 2.5 cm GS > 18 mm  Abbreviations: GS, gestational sac; US, ultrasound.  R.M. Paspulati et al / Radiol Clin N Am 42 (2004) 297–314 298  [13]described a focal, eccentric, anechoic area in theendometrium caused by the embedded blastocyst asthe ‘‘intradecidual sign.’’ They described this sign asearly as 3.5 weeks of menstrual age on transabdomi-nal US and reported a sensitivity rate of 92%, aspecificity rate of 100%, and an accuracy rate of 93%. Laing et al[14]used TVUS to demonstrate thissign and found that the overall sensitivity, specificity,and accuracy for the intradecidual sign were only48%, 66%, and 45%, respectively. With currentlyavailable high-frequency transvaginal probes, a ges-tational sac as small as 2 to 3 mm can be demon-strated at 4 weeks of gestational age[15–17]. OnTVUS, the gestational sac is seen as a well-definedfluid-filled cavity with a surrounding hyperechoicrim, embedded eccentrically in the endometrial liningof the fundus or midbody of the uterus(Fig. 2).The sonographic term ‘‘gestational sac’’ represents theexocoelomic cavity of the blastocyst and the sur-rounding echogenic rim is caused by the developingchorionic villi and decidual tissue. The echogenic rimshould have a minimum thickness of 2 mm and itsechogenicity should exceed that of myometrium[1].The double decidual sac sign of intrauterinegestation was first described in 1982[18].The double decidual sac sign consists of two concentric echo-genic rings encasing a central anechoic focus that im- press on the endometrial stripe. The inner echogenicrim represents the decidua capsularis and chorionlaeve, whereas the outer echogenic rim representsthe decidua parietalis; these echogenic rims are sepa-rated by a thin rim of fluid in the endometrial cavity(Fig. 3).This is a useful sign of IUP between 4 and6 weeks of gestation. The crown-rump length (CRL)of the embryo is a more accurate indicator of gesta-tional age than the mean gestational sac diameter. Themean gestational sac diameter should be recorded,however, when an embryo is not identified.Because hCG production and gestational sacgrowth are related to trophoblastic function, there isexcellent correlation of the serum hCG level, sac size,and the stage of pregnancy[19].Kadar et al[20]first  introduced the concept of a discriminatory level of the b subunit of hCG. The range of the serum b -hCGlevel at which an intrauterine gestational sac isvisualized is the discriminatory zone. Although thediscriminatory range of  b -hCG varies from one labo-ratory to another, the widely accepted range is from Table 2Land marks of normal first-trimester pregnancyGestational age Embryologic change Sonographic appearance23 d Blastocyst implantation Blastocyst measures 0.1 mm and is too small to visualize3.5–4 wk Decidual changes at implantation siteFocal echogenic decidual thickening at implantation site4–4.5 wk Trophoblastic tissue High-velocity and low-impedance trophoblastic flow at the implantation siteon TVCFD4.5–5 wk Exocoelomic cavity of the blastocyst Gestational sac (a sonographic term) is always seen when it measures > 5 mmand the serum b -hCG is between 1000 and 2000 mIU/mL (IRP)5–5.5 wk Secondary yolk sac Yolk sac is seen as a thin-walled cystic structure within the gestational sac andshould always be seen when the GS is > 10 mm; it is the first sign of a truegestational sac before the visualization of embryo5–6 wk Embryo Seen as a focal echogenic area adjacent to the yolk sac; should always be seenwhen the GS is > 18 mm5–6 wk Embryonic cardiacactivityEmbryonic cardiac activity should always be seen when the embryo is > 5 mm;normal heart rate ranges from 100–115 beats/min between 5–6 wk of gestation  Abbreviations: CG, human chorionic goradotropin; GS, gestational sac; IRP, international reference preparation; TVCFD,transvaginal color flow Doppler.Fig. 2. Coronal TVUS of the uterus shows a gestational sacwith hyperechoic margins ( arrow ) and endometrial cavity( curved arrow ).  R.M. Paspulati et al / Radiol Clin N Am 42 (2004) 297–314 299  1000 to 2000 mIU/mL international reference prepa-ration (IRP) for TVUS and 2400 to 3600 mIU/mL(IRP) for transabdominal US[10].In normal preg- nancy serum b -hCG should double or increase by at least 66% in 48 hours. Yolk sac The first structure to be seen within the gestationalsac is the secondary yolk sac, which is a reliableindicator of a true IUP with a positive predictivevalue of 100%. The primary yolk sac is not seen byUS because it shrinks at 4 weeks menstrual age andgradually disappears with the formation of the sec-ondary yolk sac[21].The secondary yolk sac is first  seen on TVUS as a thin-walled cystic structure by thefifth gestational week and is virtually always seen by5.5 weeks gestational age(Fig. 4)[22].The yolk sac is round, measures less than 6 mm, and should bevisualized by TVUS when a gestational sac measuresmore than 10 mm[10]. The yolk sac is involved innutritive, metabolic, hemopoietic, and secretive func-tions during early embryonic development and or-ganogenesis[23,24].Abnormalities in its size and appearance are predictors of abnormal gestation[25].  Embryo The embryo should always be visualized byTVUS when the gestational sac measures greater than18 mm, and transabdominally when the gestationalsac measures 2.5 cm(Fig. 5).With the currently available high-frequency transvaginal transducers,the embryonic disk is initially seen as a focal echo-genic area of 1- to 2-mm thickness adjacent to theyolk sac between 5 and 6 weeks of gestational age[26–29].Embryonic cardiac activity should always be seen when an embryo measures greater than 5 mm.Occasionally the heartbeat may be seen adjacent tothe yolk sac even before the embryo is clearly visible. Fig. 3. Double decidual sac sign. (  A ) Coronal TVUS of the uterus reveals an intrauterine gestational sac (  straight arrow ),decidua capsularis ( curved arrow ), decidua parietalis ( arrowhead  ), and effaced endometrial cavity ( asterisks ). (  B ) Correspondingline diagram.Fig. 4. TVUS of the uterus demonstrates a yolk sac ( thinarrow ) outside the amniotic membrane ( arrowhead  ), whichhas not yet fused with the chorion ( curved arrow ). Embryo( thick arrow ) is seen within the amniotic sac.  R.M. Paspulati et al / Radiol Clin N Am 42 (2004) 297–314 300
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