ORIGINAL RESEARCH

Setting up a Nuchal Translucency Clinic What Radiologists Need to Know Ifeanyi Onyeacholem, MD,* Beth Kleiner, MD,Þ Andrew D. Hull, MD,þ§ Jason Chibuk, MS,|| Lorene Romine, MD,*þ Tracy Anton, BS, RDMS, RDCS,þ§ and Dolores H. Pretorius, MD*þ Abstract: The purpose of this article was to discuss the process of setting up a nuchal translucency (NT) screening clinic in clinical practice, how to interpret the information in combination with other clinical tests, what to do if abnormal results are obtained, and to illustrate some of the fetal anomalies that are associated with an increased NT. The NT was initially implemented to predict the likelihood of a fetus with Down syndrome. Maternal age can be combined with fetal NT and maternal serum biochemistry (free A-hCG and PAPP-A) at 11 to 14 weeks to identify about 90% of affected fetuses. Setting up a clinic to perform the NT screening requires certified physicians and certified sonographers. Certification can be obtained for both physicians and sonographers through Nuchal Translucency Quality Review and Fetal Medicine Foundation. Cellfree DNA testing is now altering what our patients are choosing to evaluate fetuses at risk for chromosomal anomalies and congenital anomalies. Common pitfalls to performing, interpreting, and conveying results of the NT are illustrated in this article. Nasal bone measurement, fetal anatomy examination and fetal echocardiography are tools that add sensitivity to the detection of chromosomal abnormalities. Examples of fetal anomalies discovered during the NT screening are also illustrated. Screening for obstetric complications is an additional benefit to the NT clinic. Key Words: nuchal translucency, new clinic, genetic testing, fetal, maternal serum, chromosomal anomalies, fetal anomalies (Ultrasound Quarterly 2016;32:3Y14)

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outine screening of nuchal translucency (NT) is now recommended for all first trimester pregnancies, regardless of the age of the mother. The American College of Obstetrics and Gynecology, the American College of Radiology, and the American Institute of Ultrasound in Medicine now recommend that all women be offered NT in the first trimester to detect chromosomal abnormalities and fetal anomalies; it is also useful to assess for placental dysfunction. Down syndrome is the most common chromosomal anomaly; however, other chromosomal abnormalities and fetal anomalies can also

Received for publication November 5, 2014; accepted March 5, 2015. *University of California, San Diego, Department of Radiology, La Jolla; †Peninsula Diagnostic Imaging, San Mateo; ‡University of California, San Diego Maternal-Fetal Care and Genetics; §University of California, San Diego, Deparment of Reproductive Medicine; ||Sequenom Inc, John Hopkins Court, San Diego, CA. The authors declare no conflict of interest. Reprints: Dolores H. Pretorius, MD, 9300 Campus Point Dr, UCSD Thornton Hospital, La Jolla, CA 92037-7756 (e-fetoprotein (AFP),

FIGURE 9. Normal nasal bone ossification imaged during the NT.

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& Volume 32, Number 1, March 2016

FIGURE 10. Normal anatomy. From top left to right, Choroid, bladder, abdominal cord insertion (ACI). From bottom left to right, Stomach, arms, legs.

human chorionic gonadotropin (hCG), estriol, and Inhibin-A. Although this can be drawn between 15 and 20 weeks, we often recommend that it be drawn at approximately 16 weeks so that we avoid dating issues and obtain results as early as possible. The combination of the NT, QUAD screen, and first trimester biochemistry (A-hCG and PAPP-A) then provide an ‘‘integrated screen’’ that can be reported to the patient. Fifth, the patient should be referred for fetal echocardiography if the NT is greater than 3.5 mm. Sixth, the patient should be informed that the combination of a normal 18- to 20-week anatomy scan, normal fetal echocardiogram, and normal QUAD screen results in 95% probability of an unaffected fetus.15 Seventh, if the patient desires additional information, she may be referred to a genetic counselor or perinatologist. Additional testing is available for the patient with an abnormal NT screening examination. If the patient desires more invasive testing, CVS can be performed at 11 to 14 weeks. Amniocentesis can be performed as early as 15 to 16 weeks. Newer tests, such as microarray, have been used to detect microdeletions and duplications in a fetus with normal chromosomes, although it is more expensive. Recent advances in prenatal genetic testing have made noninvasive prenatal testing (NIPT) commercially available for the detection of aneuploidy in pregnancy by using a simple maternal blood test. In contrast to invasive diagnostic testing (CVS and amniocentesis), NIPT does not pose a risk of miscarriage to the pregnancy because it involves only a maternal blood sample, and thereby it has the potential to reduce the number of invasive diagnostic procedures and resulting fetal losses. In 1997, Lo et al16 made the discovery that that cell-free fetal DNA (cfDNA) exists in the maternal plasma, and efforts since then have focused on creating high-performance tests that can be offered to women in pregnancy to detect aneuploidy. The NIPT involves

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FIGURE 11. Two fetuses with abnormal NT. A, The NT measures 5.5 mm in this 12-week 1-day fetus later diagnosed with trisomy 21. B, The NT measures 10.7 mm in this 12-week 2-day fetus. Ascites, pleural effusions, and hydrops were found during NT screening. The fetus was later diagnosed with trisomy 18. * 2015 Wolters Kluwer Health, Inc. All rights reserved.

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Setting up a Nuchal Translucency Clinic

FIGURE 12. Congenital heart disease in a fetus with an abnormal NT. Increased NT of 3.1 mm in fetus found to have hypoplastic right heart on subsequent fetal echocardiography.

FIGURE 13. Abnormal NT in twin pregnancy. A, Dichorionic-diamniotic twin pregnancy. B, Twin A, NT measures 2.8 mm in this fetus with a of crownYrump length of 76.3 mm correlating to 14 weeks and 1 day. This was considered a borderline abnormal NT in the 95Y99th percentile. C, Twin B, normal NT measures 1.7 mm in this fetus with a crownYrump length was 81.5 mm correlating to 13 weeks and 6 days. Follow-up anatomy scan at 17 weeks was normal for both twins. * 2015 Wolters Kluwer Health, Inc. All rights reserved.

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FIGURE 14. Cystic hygroma found at an NT screening. This fetus had trisomy 18.

an examination of cfDNA in the maternal circulation to determine if there is an increased quantity of a particular chromosome as would be expected in a trisomy pregnancy. Detection rates for trisomy 21 (Down syndrome) are reported in excess of 98.6%, with false-positive rates of less than 0.2%.17Y19 Detection rates for trisomy 18 (Edward syndrome) and trisomy 13 (Patau syndrome) of 97.2% to 99.9% and 78.6% to 91.7%, respectively, are also very impressive.17,18 The technology is also reliable in multiple gestations and to test for sex chromosome

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aneuploidy.18,20 As this field continues to develop, it is highly likely that additional information about the fetal genome will be available through this novel noninvasive testing. Fetal echocardiography is recommended to all patients with an NT greater than 3.5 mm at our institution since these fetuses are at increased risk for congenital heart disease (Fig. 12). Souka et al15 reported that 30 fetuses from 3 combined studies were diagnosed with cardiac anomalies and of these fetuses, 83% had increased NT. Although fetal echocardiography is usually performed at 20 to 21 weeks at our institution, we often attempt to assess the fetal heart at 14 to 18 weeks in these highrisk patients; the age at assessment will depend on availability and expertise. Haak et al21 found a complete cardiac examination (4r chamber, aorta, and pulmonary artery) was successfully performed in 92% of cases at 13 weeks gestation. They also found that the best time to perform a first trimester complete cardiac examination was between 13 weeks 0 days and 13 weeks 6 days, although it could be performed anywhere between 12 and 20 weeks.21 A wide spectrum of cardiac malformations has been diagnosed in the first trimester.15

Multiple Gestations Multiple gestations require additional care in counseling because many of the parameters used for single gestations are different for multiple gestations. Twin gestations have increased over the years, which can be attributed to both

FIGURE 15. Normal NT in fetus with multiple anomalies at 12 weeks and 1 day. A, The NT measured 0.7 mm at a crownYrump length of 52.5 mm. At NT screening, omphalocele (B) and a club foot (C) were found. This fetus was found to have trisomy 18.

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increasing maternal age and increased use of fertility techniques. In monochorionic twins, the risk for aneuploidy is thought to be the same as for their singleton counterparts. For dichorionic twins, the age-related risk for aneuploidy is higher because each fetus carries an independent risk for Down syndrome.22 The maternal serum analysis and sonographic assessment is performed identically for multiple gestations, as it is for singletons; however, several factors must be taken into account. The interpretation of maternal serum values is difficult in multiple gestations because the normal co-twin can mask the serum markers for the affected fetus. In dichorionic twins at 11 to 13 weeks, the levels of maternal serum-free A-hCG and PAPP-A are about twice as high as in singleton pregnancies; but in monochorionic twins, the levels are lower than in dichorionic twins.23 It is important to diagnose the chorionicity of the gestation before correlating the risk with maternal serum analysis. The NT screening examination can also be useful in diagnosing the amnionicity and chorionicity if it was not determined earlier. Chorionicity can be determined by examining the location of the placenta(e) and the placenta-membrane junction. The L sign or twin peak, a projection of triangular chorionic tissue at the base of intertwin membrane, can be used between 11 and 14 weeks24 (Fig. 13). Similar to singleton pregnancies, the sonographic NT in multiple gestations has an essential role in improving the detection rate of fetal anomalies and chromosomal abnormalities. An NT screening of multiples requires skilled technique due to the interposition of fetal parts and position of fetuses. In dichorionic twins, patient-specific risks for trisomy 21 are calculated for each fetus based on maternal age and fetal NT, and the detection rate and the false-positive rate are similar to those in singleton pregnancies.23 In monochorionic twin pregnancies, the false-positive rate of NT screening is higher than in dichorionic twins because increased NT in at least one of the fetuses can be an early manifestation of twin-to-twin transfusion syndrome as well as a marker of chromosomal abnormalities.23 In the calculation of risk of trisomy 21 in monochorionic twins, the NT of both fetuses should be measured and the average of the 2 should be considered.25 If an abnormal NT is identified in one of the fetuses based on the 95th percentile, the same counseling and risk assessment should be performed taking into account the maternal age, maternal serum analysis, and the chorionicity (Fig. 13). The CVS is recommended over amniocentesis as it can be performed at an earlier time and provides results early enough to allow for safer selective pregnancy reduction if desired. Performing the NT provides a useful sonographic detectable marker and helps to ensure correct identification of the abnormal twin if selective termination is performed. ClearyGoldman et al22 showed that in twins, the addition of nasal bone to NT and biochemistry increased the Down syndrome detection rate from 79% to 89% at 5% false-positive rate. Death of a co-twin impacts interpretation of NT results in the live twin. An empty gestational sac has no effect on the serum analysis and therefore should be treated as a normal singleton pregnancy. The presence of a vanishing twin has different implications. The levels of A-hCG are not altered; however, the PAPP-A levels are elevated due to the fetal demise. The levels are also dependent on the interval from fetal

Setting up a Nuchal Translucency Clinic

demise to blood analysis since PAPP-A has a longer half-life during the first trimester.26 In the instance of a vanishing cotwin, it is recommended that NT alone or with free A-hCG levels should be used to calculate risk. At our institution, the California Genetic Disease Screening Program states that any twin demise makes screening in the first trimester unreliable; however, second trimester screening can be performed. Any demise at or greater than equal to 8 weeks makes both first and second trimester serum screening unreliable. Lastly, it is important to note that triplet pregnancies and beyond demonstrate even higher levels of A-hCG and PAPP-A in maternal serum. The fetuses can also demonstrate multiple combinations of chorionicity. Due to this, the maternal serum analysis cannot be taken into account when determining the probability of chromosomal abnormalities or fetal anomalies. The maternal age and NT screen are used together to assess the risk of aneuploidy in multiple gestations greater than twin gestations.

Fetal Anomalies Fetal anomalies and genetic syndromes can be identified in fetuses with normal and abnormal karyotypes at the time of NT screening.15 Anomalies of almost all organ systems have been identified but emphasis has included the central

FIGURE 16. Abnormal NT in fetus with omphalocele. A, NT measures 2.9 mm in this 12-week 0-day fetus with a crownYrump length of 52.7 mm. B, Omphalocele (long arrow) was seen at NT screening. Short arrow notates stomach. The maternal PAPP-A was low at 01.4 mm in a mother with advanced maternal age. The fetus was diagnosed with trisomy 18.

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nervous system, heart, anterior abdominal wall, urinary tract, and skeleton.15 It is important to assess the fetal anatomy when an abnormal NT is found, both at the time of the examination and on follow-up examinations. No guidelines for the gestational age for follow-up examinations have been adopted and it will be dependent on expertise in the community and maternal body habitus. Anomalies are generally identified on transabdominal imaging initially; however, transvaginal imaging often allows for further delineation of the anomalies as well as identification of additional anomalies. Cystic hygroma is a common anomaly found at NT screening. It is characterized by a spoked-wheelYshaped cystic structure that can be identified posterior and lateral in the soft tissues of the neck with a normal underlying cervical spine. More than 60% of cystic hygromas are associated with chromosomal abnormalities: although Turner syndrome is most common in the second trimester, other aneuploidies are common in the first trimester, with trisomy 21 being most common.3 The FASTER Trial found a 5-fold increase in the risk of aneuploidy, a 12-fold increase in the risk of cardiac malformations and a 6-fold increase risk of perinatal death27; when cystic hygroma is combined with hydrops, fetal demise is highly likely (Fig. 14). Abdominal wall defects can be detected in the first trimester. The diagnosis of omphalocele, gastroschisis, and

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limbYbody-wall complex should be made with caution before 12 weeks gestation or a crownYrump length of 45 mm or less, unless the anterior abdominal mass is greater than 7 mm or contains the liver, stomach, or heart.6 Abdominal wall defects can be discovered at the time of the NT screening with normal (Fig. 15) or abnormal NT (Fig. 16). It is important to remember that physiologic herniation of the midgut occurs at 8 to 11 weeks 6 days and is often visible on ultrasound. The incidence of gastroschisis is increasing, particularly in teenagers and is now able to be diagnosed at the time of nuchal screening (Fig. 17).28 Congenital heart disease is associated with increased NT and is discussed previously. Lastly, limb deformities can be identified at the time of the NT screening. The limbs buds are first identified on transvaginal ultrasound at 8 to 9 weeks gestation but limb abnormalities can be identified on transabdominal ultrasound imaging performed for NT screening. Ossification and limb movements should be seen by 11 weeks. 6 Many reported cases of skeletal defects in the first trimester have been associated with an increased NT. 29 Rice et al 30 recently reported that limb abnormalities detected in the first trimester are often associated with trisomy 18 (Fig. 18). Skeletal dysplasias, a heterogeneous group of bone abnormalities resulting in abnormal growth and

FIGURE 17. Fetal anomaly found at NT screening in triplets. A, Triplets at 12 weeks and 6 days. B, Triplet B was found to have gastroschisis. C, Triplet C for reference has a normal abdomen. D, Follow-up for Triplet B at 19 weeks demonstrating persistent gastroschisis.

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Setting up a Nuchal Translucency Clinic

FIGURE 18. Fetus with multiple congenital anomalies at 12 weeks and 4 days. A, NT measured 2.9 mm at a crownYrump length of 57.8 mm. B and C, Findings at NT screening included flexed wrist, cystic structure in the posterior fossa, flat face, and prominent forehead. C, Three-dimensional ultrasound shows the flexed wrists. Chorionic villus sampling revealed normal karyotype.

shape of the fetal skeleton, have also been reported with increased NT. 15

Placental Dysfunction A low PAPP-A, below the 5th percentile, at 11 to 13 weeks has been associated with obstetrical complications due to placental dysfunction as well as chromosomal anomalies.31 Obstetrical complications due to placental dysfunction include intrauterine growth restriction, extreme preterm delivery, preeclampsia, and stillbirth. PAPP-A is synthesized by the placenta, increases through pregnancy, and seems to promote placental growth and function. Proctor et al31 found the risk of complications continues to increase if an elevated AFP level is found at 15 to 18 weeks. If a low PAPP-A is seen with a normal NT measurement during screening, the clinician should have a heightened suspicion for placental dysfunction. Fetal growth should be monitored closely. Other sonographic measurements such as placental size, morphology, location, and uterine artery Doppler (at 24 weeks gestational age) can be used to assess placental function and fetal well-being.

Ultrasound Bioeffects When performing NT screening and any additional Doppler evaluation of the fetus, the radiologist should keep in mind the potential for ultrasound induced bioeffects of ultrasound especially during the first trimester. Currently, there is no evidence that links diagnostic ultrasound with harm to human or the developing fetus; however, with advances in

technology, increased power of newer generation equipment, and the growing need for ultrasound monitoring, it is important for the radiologist to have a clear understanding of diagnostic ultrasound parameters for the first trimester. Practitioners should use As Low As Reasonably Achievable (ALARA) guidelines for every examination, particularly prenatal examinations. Thermal (TI) and mechanical indices (MI) should be 0.5 or less if possible.12 The MI is an indicator of the relative potential for ultrasound to induce adverse bioeffect by a nonthermal mechanism, such as cavitation. The TI is an indicator of the relative potential for a tissue temperature to rise. Particular attentions should be paid to TI in cases of elevated maternal temperature. Concern for the connection between ultrasound in the first trimester and abnormal neuronal migration, neural tube defects, autism, and growth restriction continues to grow.32

CONCLUSIONS Setting up an NT clinic requires advanced certification, knowledge of the appropriate time and measurement to read both normal and abnormal NT studies, and ability to provide appropriate counseling and follow-up for the patient. The radiologist should be able to counsel the patients or if desired, refer them to genetic counselors or perinatologists if additional information is needed when an abnormal NT is detected. Nuchal translucency screening is a useful examination to increase the sensitivity of diagnosing chromosomal abnormalities, to identify other fetal anomalies, and to provide information regarding placental dysfunction.

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REFERENCES 1. Nicolaides KH, Sebire NJ, Snijders RJM. The 11-14-Week Scan: The Diagnosis of Fetal Abnormalities, London: Parthenon Publishing Group, 1999. 2. Orlandi F, Damiani G, Hallahan TW, et al. First-trimester screening for fetal aneuploidy: biochemistry and nuchal translucency. Ultrasound Obstet Gynecol. 1997;10:381Y386. 3. Snijders RJ, Noble P, Sebire N, et al. UK multicentre project on assessment of risk of trisomy 21 by maternal age and fetal nuchal translucency thickness at 10Y14 weeks of gestation. Lancet. 1998; 352:343Y346. 4. Souka AP, Snijders RJM, Novakov A, et al. Defects and syndromes in chromosomally normal fetuses with increased nuchal translucency thickness at 10Y14 weeks of gestation. Ultrasound Obstet Gynecol. 1998;11(6):391Y400. 5. AIUM. Practice guideline for the performance of obstetric ultrasound examinations. J Ultrasound Med. 2013;32(6):1083Y1101. 6. Fong KW, Toi A, Salem S, et al. Detection of fetal structural abnormalities with US during early pregnancy. Radiographics. 2004; 24(1):157Y174. 7. Otano L, Aiello H, Igarzabal L, et al. Association between first trimester absence of fetal nasal bone on ultrasound and Down syndrome. Prenat Diagn. 2002;22:930Y932. 8. Weingertner AS, Kohler M, Firtion C, et al. Interest of foetal nasal bone measurement at first trimester trisomy 21 screening. Fetal Diagn Ther. 2006;21(5):433Y438. 9. Has R, Kalelioglu I, Yuksel A, et al. Fetal nasal bone assessment in first trimester Down syndrome screening. Fetal Diagn Ther. 2008; 24(1):61Y66. 10. Cicero S, Curcio P, Rembouskos G, et al. Maxillary length at 11Y14 weeks of gestation in fetuses with trisomy 21. Ultrasound Obstet Gynecol. 2004;24(1):19Y22. 11. Cusick W, Shevell T, Duchan LS, et al. Likelihood ratios for fetal trisomy 21 based on nasal bone length in the second trimester: how best to define hypoplasia? Ultrasound Obstet Gynecol. 2007;30(3):271Y274. 12. Nelson TR, Fowlkes JB, Abramowicz JS, et al. Ultrasound biosafety considerations for the practicing sonographer and sonologist. J Ultrasound Med. 2009;28(2):139Y150. 13. Sepulveda W, Wong AE, Martinez-Ten P, et al. Retronasal triangle: a sonographic landmark for the screening of cleft palate in the first trimester. Ultrasound Obstet Gynecol. 2010;35(1):7Y13. 14. Chaoui R, Benoit B, Mitkowska-Wozniak H, et al. Assessment of intracranial translucency (IT) in the detection of spina bifida at the 11Y13-week scan. Ultrasound Obstet Gynecol. 2009;34(3): 249Y252. 15. Souka AP, von Kaisenberg CS, Hyett JA, et al. Increased nuchal translucency with normal karyotype. Am J Obstet Gynecol. 2005; 192(4):1005Y1021.

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16. Lo YMD, Corbetta N, Chamberlain PF, et al. Presence of fetal DNA in maternal plasma and serum. Lancet. 1997;350(9076):485Y487. 17. Palomaki GE, Kloza EM, Lambert-Messerlian GM, et al. DNA sequencing of maternal plasma to detect Down syndrome: an international clinical validation study. Genet Med. 2011;13(11):913Y920. 18. Bianchi DW, Platt LD, Goldberg JD, et al. Genome-wide fetal aneuploidy detection by maternal plasma DNA sequencing. Obstet Gynecol. 2012;119(5):890Y901. 19. Norton ME, Brar H, Weiss J, et al. Non-Invasive Chromosomal Evaluation (NICE) Study: results of a multicenter prospective cohort study for detection of fetal trisomy 21 and trisomy 18. Am J Obstet Gynecol. 2012;207(2):137.e1Y137.e8. 20. Canick JA, Kloza EM, Lambert-Messerlian GM, et al. DNA sequencing of maternal plasma to identify Down syndrome and other trisomies in multiple gestations. Prenat Diagn. 2012;32(8):730Y734. 21. Haak MC, Twisk JWR, Van Vugt JMG. How successful is fetal echocardiographic examination in the first trimester of pregnancy? Ultrasound Obstet Gynecol. 2002;20(1):9Y13. 22. Cleary-Goldman J, Rebarber A, Krantz D, et al. First-trimester screening with nasal bone in twins. Am J Obstet Gynecol. 2008;199(3):283.e1Y283.e3. 23. Nicolaides KH. Screening for fetal aneuploidies at 11 to 13 weeks. Prenat Diagn. 2011;31:7Y15. 24. Vayssiere C, Benoist G, Blondel B, et al. Twin pregnancies: guidelines for clinical practice from the French College of Gynaecologists and Obstetricians. Eur J Obstet Gynecol Reprod Biol. 2011;156:12Y17. 25. Vandecruys H, Faiola S, Auer M, et al. Screening for trisomy 21 in monochorionic twins by measurement of fetal nuchal translucency thickness. Ultrasound Obstet Gynecol. 2005;25:551Y553. 26. Spencer K, Staboulidou I, Nicolaides KH. First trimester aneuploidy screening in the presence of a vanishing twin: implications for maternal serum markers. Prenat Diagn. 2010;30(3):235Y240. 27. Malone FD, Ball RH, Nyberg DA, et al. FASTER Trial Research Consortium. Obstet Gynecol. 2005;106:288Y294. 28. Reid KP, Dickinson JE, Doherty DA. The epidemiologic incidence of congenital gastroschisis in Western Australia. Am J Obstet Gynecol. 2003;189(3):764Y768. 29. Souka AP, Krampl E, Bakalis S, et al. Outcome of pregnancy in chromosomally normal fetuses with increased nuchal translucency in the first trimester. Ultrasound Obstet Gynecol. 2001;18:9Y17. 30. Rice KJ, Ballas J, Lai E, et al. Diagnosis of fetal limb abnormalities before 15 weeks: cause for concern. J Ultrasound Med. 2011; 30(7):1009Y1019. 31. Proctor LK, Toal M, Keating S, et al. Placental size and the prediction of severe early-onset intrauterine growth restriction in women with low pregnancy-associated plasma protein-A. Ultrasound Obstet Gynecol. 2009;34(3):274Y282. 32. Abramowicz J. Prenatal exposure to ultrasound waves: is there a risk? Ultrasound Obstet Gynecol. 2007;29(4):363Y367.

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Setting up a Nuchal Translucency Clinic: What Radiologists Need to Know.

The purpose of this article was to discuss the process of setting up a nuchal translucency (NT) screening clinic in clinical practice, how to interpre...
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