AIUM Practice Parameter for the Performance of Detailed Diagnostic Obstetric Ultrasound Examinations Between 12 Weeks 0 Days and 13 Weeks 6 Days.

Abstract

Journal of Ultrasound in MedicineVolume 40, Issue 5 p. E1-E16 Practice ParameterFree Access AIUM Practice Parameter for the Performance of Detailed Diagnostic Obstetric Ultrasound Examinations Between 12 Weeks 0 Days and 13 Weeks 6 Days First published: 27 August 2020 https://doi.org/10.1002/jum.15477AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Introduction The American Institute of Ultrasound in Medicine (AIUM) is a multidisciplinary association dedicated to advancing the safe and effective use of ultrasound in medicine through professional and public education, research, development of clinical practice parameters, and accreditation of practices performing ultrasound. The AIUM Practice Parameter for the Performance of Detailed Diagnostic Obstetric Ultrasound Examinations Between 12 Weeks 0 Days and 13 Weeks 6 Days was developed by the AIUM in collaboration with other organizations whose members use ultrasound for performing this examination (see “Acknowledgments”). Recommendations for personnel requirements, the request for the examination, documentation, quality assurance, and safety may vary among the organizations and may be addressed by each separately. This practice parameter is intended to provide the medical ultrasound community with recommendations for the performance and recording of high-quality ultrasound examinations. The parameter reflects what the AIUM considers the appropriate criteria for this type of ultrasound examination but is not intended to establish a legal standard of care. Examinations performed in this specialty area are expected to follow the parameter with recognition that deviations may occur depending on the clinical situation. This specialized diagnostic examination is an extension of the standard sonographic fetal assessment described in the AIUM-ACR-ACOG-SMFM-SRU Practice Parameter for the Performance of Standard Diagnostic Obstetric Ultrasound Examinations and the American College of Obstetricians and Gynecologist practice bulletin Ultrasound in Pregnancy.1, 2 The detailed obstetric ultrasound examination in the late first trimester is an indication-driven examination for women at increased risk for fetal or placental abnormalities that are potentially detectable between 12 weeks 0 days and 13 weeks 6 days' gestation. Performance and interpretation of this examination require advanced training, knowledge, and imaging skills, as well as the ability to effectively communicate the findings to the patient and referring physician. Thus, the performance of the detailed first-trimester ultrasound examination should be rare outside referral practices with special expertise in the identification and diagnosis of fetal anomalies and placental implantation disorders in the first trimester. Genetic counseling and diagnostic testing services should be available for patients diagnosed with fetal anomalies in early gestation. Ultrasound imaging of the fetus was first introduced in the late first trimester as a component of risk assessment for aneuploidy and has been widely incorporated into prenatal care.3-6 In addition to aneuploidy assessment, imaging the fetus in this period promotes accurate dating and optimal assessment of amnionicity and chorionicity in multiple gestations and provides an opportunity to evaluate the structural integrity of the fetus. Many anomalies that were historically diagnosed in the second trimester can be identified in the latter part of the first trimester by sonographers and sonologists.7-17 The components of this examination promote a systematic method of assessing fetal anatomy that optimizes the detection of anomalies.17-22 Approximately 50% of major anomalies are detectable in singletons and 25% in twins in this gestational age window, although there is significant variability among organ systems.13, 14, 17-25 Some malformations, such as anencephaly, alobar holoprosencephaly, ectopia cordis, body stalk abnormalities, and large abdominal wall defects, are usually identified.14, 16, 17, 19-23, 25 Certain anomalies such as microcephaly and callosal agenesis are not sonographically detectable during this period. Anomaly detection rates increase with fetal size and may be enhanced by the use of transvaginal sonography, especially when the fetal anatomy is suboptimally visualized by the transabdominal approach.8, 11, 12, 19 While it is not possible to detect every abnormality, adherence to the following practice parameter will maximize the probability of detecting fetuses with major structural anomalies between 12 weeks 0 days and 13 weeks 6 days' gestation.21 Early detection of major anomalies allows the patient the opportunity to pursue genetic diagnostic testing, obtain comprehensive multidisciplinary counseling, and maximize reproductive choices. While a first-trimester detailed anatomic scan may detect many major anomalies, the natural history of some findings (eg, megacystis, micrognathia, abdominal cysts, and cardiac structures) is variable.13, 14, 26-28 In addition, similar to other screening paradigms, false-positive and false-negative results may occur.14, 17, 22, 27, 29, 30 It must be emphasized that a first-trimester ultrasound examination does not replace the second-trimester anatomic survey.16, 22, 31, 32 In ongoing pregnancies at increased risk for adverse outcomes, a second-trimester detailed anatomic evaluation should be considered and recommended when appropriate.1, 33 Late first-trimester fetal anatomic and placental imaging is rapidly evolving, requiring meticulous attention to advances in the literature and interpretation of findings. Qualifications and Responsibilities of Personnel Physicians interpreting or performing this type of ultrasound examination should meet the specified AIUM Training Guidelines in accordance with AIUM accreditation policies. Sonographers performing the ultrasound examination should be appropriately credentialed in the specialty area in accordance with AIUM accreditation policies. Physicians not personally performing the examination must provide supervision, as defined by the Centers for Medicare and Medicaid Services Code of Federal Regulations 42 CFR §410.32 . Request for the Examination The written or electronic request for an ultrasound examination must originate from a physician or other appropriately licensed health care provider or under the provider's direction. The clinical information provided should allow for the performance and interpretation of the appropriate ultrasound examination and should be consistent with relevant legal and local health care facility requirements. Indications A detailed late first-trimester obstetric ultrasound examination may be performed when there is an increased risk for a fetal or placental abnormality associated with anatomic findings, potentially identifiable by ultrasound in the first trimester. Indications include but are not limited to: Previous fetus or child with a congenital, genetic, or chromosomal anomaly.34, 35 Known or suspected fetal abnormality detected by ultrasound in the current pregnancy. Fetus at increased risk for a congenital anomaly based on the following: 35 years or older at delivery.34-37 Maternal pregestational diabetes. Pregnancy conceived via in vitro fertilization.38-41 Multiple gestation.42-45 Teratogen exposure.46-49 Enlarged nuchal translucency.50, 51 Positive screening test results for aneuploidy, including cell-free DNA screening and serum-only or combined first-trimester screening.52 Other conditions possibly affecting the pregnancy/fetus, including: Maternal body mass index of 30 kg/m2 or higher.53-55 Placental implantation covering the internal cervical os under a cesarean scar site or cesarean scar pregnancy diagnosed in index gestation.56, 57 Specifications of the Examination General Considerations The examination may be done transabdominally and/or transvaginally. The transabdominal examination provides a global view of the fetus, placenta, uterus, and adnexa. Higher-frequency transabdominal linear or curvilinear transducers have been used to visualize fetal anatomy, including fetal cardiac structures.58, 59 In most cases, transabdominal imaging may be sufficient; however, a transvaginal approach can optimize visualization by providing a higher resolution and is recommended if transabdominal imaging is suboptimal or an anomaly is suspected. A combined transabdominal and transvaginal approach has been reported to optimize the detection rate of fetal anomalies.10, 12, 13, 19 Attention should be given to adequate magnification, appropriate depth, sector size, and correct focal zone placement at the area of interest. Harmonic imaging, compound imaging, and speckle reduction may enhance the demonstration of fetal anatomy. Power and color Doppler imaging may be complementary to standard grayscale evaluation when appropriate. As in all clinical imaging situations, the patient's body habitus and the presence of other acoustic challenges (leiomyomata, uterine position, and surgical scars) may alter the ability to see all anatomic components despite using both a transabdominal and transvaginal approach. In some circumstances, such as a suspected anomaly, repeated imaging in 1 to 3 weeks should be considered, and in other situations, the nonvisualized structure(s) may be evaluated at the time of the second-trimester detailed anatomic scan. In women of a high body mass index, structural evaluation of the fetus in the later first trimester may be advantageous.53-55 Imaging Parameters Imaging parameters are listed in Table 1. Table 1. Detailed Fetal Anatomic and Placental Assessment Between 12 Weeks 0 Days and 13 Weeks 6 Days The detailed obstetric ultrasound examination in the late first trimester is an indication-driven examination for women at increased risk for fetal or placental abnormalities that are potentially detectable between 12 weeks 0 days and 13 weeks 6 days' gestation. Performance and interpretation of this examination require advanced training, knowledge, and imaging skills, as well as the ability to effectively communicate the findings to the patient and referring physician. • Images should be acquired with appropriate attention to magnification, depth, and focal zone. • Anatomic structures should be evaluated in at least 1 plane of imaging, although the specific plane(s) may vary depending on imaging conditions. • It is recognized that in some imaging situations, not all required landmarks will be visualized, and follow-up imaging may be recommended. Scanning Planes/Structures Required Required if Indicated or Suspicious Comments and Observations General Output display standard √ TI for bone ratio ≤0.7124 Cardiac activity √ M-mode or cine loop Heart rate √ M-mode Number of fetuses and gestational sacs √ If multiple gestation √ Amnionicity and chorionicity Biometry See text for description of technique Crown-rump length √ Report the mean of 3 acceptable measurements Biparietal diameter √ Head circumference √ Abdominal circumference √ Femoral length √ Fetal head A. Axial Transventricular Cranial bones (calvarium) √ Oval shape, no bulges, appropriate ossification Falx cerebri √ Anterior to posterior, symmetric hemispheres of equal size Choroid plexus √ Fill majority of lateral ventricle Ventricles √ Symmetrical Cortex √ Thin, seen mostly anteriorly Transthalamic Falx cerebri √ Thalami √ Third ventricle √ Posterior fossa √ Angle posterior-inferiorly B. Sagittal Thalami-midbrain √ Brain stem √ Fourth ventricle (intracranial translucency) √ Cisterna magna √ Facial structures A. Axial Orbits √ Size and position B. Sagittal Nasal bone √ Present/absent Profile (forehead, nasal contour, nasal bone, upper lip, mandible) √ Forehead appearance, intact upper lip Maxilla √ Evaluate for maxillary gap C. Coronal/tangential Retronasal triangle with ancillary bones (frontal process of the maxilla and alveolar ridge) √ Nasal bone may be evaluated in this view Mandible √ Evaluate for absence of mandibular gap Upper lip √ Intact and contiguous Orbits √ May also be evaluated on axial plane Lenses √ Ears √ Seen or not seen Neck A. Axial, sagittal, coronal Evaluation for cystic hygroma, dilated jugular lymphatic sacs, other abnormal fluid collections, or masses √ Subjective evaluation B. Sagittal Nuchal translucency evaluation √ Nuchal translucency measurement √ Comment A measurement of the nuchal translucency is required if it appears enlarged or is part of a screening protocol for aneuploidy risk assessment. A quality assessment program is recommended to ensure that false-positive and false-negative results are kept to a minimum.88, 89 Fetal thorax A. Axial Cardiac position and axis √ Subjectively assessed Cardiac axis (angle measurement) √ Normal axis (≈45° ± 15°), leftward 4-chamber view without color √ Symmetric chambers, presence or absence of pericardial effusion 4-chamber view with color √ Diastolic filling 3-vessel and trachea view with color √ Antegrade flow Symmetric lungs (may be evaluated in coronal plane) √ No masses or effusions Ribs with normal shape, length, and ossification √ Tricuspid valve flow √ B. Sagittal Aortic arch with color √ Antegrade flow Ductal arch with color √ Antegrade flow Diaphragm demarcation √ Contour Comment While the use of Doppler should be limited in the first trimester, color flow imaging is useful to evaluate the fetal heart, great vessels, and circulation; monitor the output display standard to keep TI for bone ≤0.7.124 C. Coronal Lungs √ Diaphragm demarcation √ Contour Fetal abdomen A. Axial (3 planes: at level of stomach, kidneys, and bladder/cord insertion) Stomach √ Fluid-filled structure on left side of abdomen Liver √ Right side Portal vein √ Coursing away from stomach Cord insertion into abdominal wall* √ Bladder with fluid √ Sagittal measurement recommended if suspicious for anomaly Color Doppler of umbilical arteries on each side of the bladder √ B. Sagittal Contour of anterior wall √ No hydrops/masses Ductus venosus flow √ C. Coronal Kidneys √ Axial and sagittal acceptable Color Doppler of renal vessels √ If kidneys not well seen Comment *Physiologic midgut hernia should not be seen after 12 weeks 6 days. May occasionally be present and resolve later in gestation. Genetic counseling should be considered. Extremities Confirm each of the 4 extremities √ Confirm 3 long bones are present and subjectively normal in each extremity √ Humerus/radius/ulna Femur/tibia/fibula Confirm presence of hands/feet √ Fingers/thumb/toes √ 3-dimensional assessment of extremities √ Spine A. Axial, longitudinal Vertebral elements/alignment √ Skin edge √ Presence of any bulges Scapula √ Placenta A. Axial, sagittal Position of the placenta, including relationship with lower uterine segment, internal cervical os, and cesarean scar site (if applicable) √ Placental position should be reported if centrally located over internal cervical os, history of cesarean delivery, or suspicion for PAS Umbilical cord insertion into placenta √ Echo texture of placenta √ Note heterogeneity, masses, cystic spaces, or lacunae Color Doppler evaluation √ Required if suspicious for PAS Myometrial thinning (subjective)/loss of retroplacental clear zone √ Bladder wall interface √ Uterine vesical vascularity √ Comment In cases of suspected PAS, transvaginal imaging through a partially full bladder is recommended. A previously documented low-lying gestational sac or cesarean scar pregnancy may expand toward the fundus with advancing gestation. If the placenta is anterior and under the cesarean scar site, the villi remain anchored in that location, a characteristic of PAS. Uterus, adnexa, cul-de-sac Myometrial masses (leiomyomata) √ Presence and number, size, and location of clinically significant masses Müllerian duct anomalies √ Intrauterine linear structures √ Synechiae, bands Ovaries √ Adnexa and cul-de-sac √ It is recognized that visualization of anatomic structures may be adequate in 1 or more planes. Fetal cardiac activity should be documented by M-mode or a cine loop. Fetal number should be determined. In cases of multiple gestation, amnionicity and chorionicity should be assigned. Fetal Biometry Assessment of gestational age is critical in pregnancy management, including scheduling of obstetric screening and surveillance tests, optimizing detection of fetal growth disorders, and consideration regarding timing of delivery. Aside from assisted reproductive technology, ultrasound imaging is the most reliable method of assessing gestational age in the first trimester.60, 61 Standardization of sonographic measurements is important in maintaining consistency. For each biometric measurement, the image should be magnified to fill the majority of the image space available without compromising image quality. Nomograms are available for fetal biometric measurements.61-70 Crown-Rump Length Crown-rump length (CRL) is the most commonly used and recommended sonographic method to establish or confirm gestational age up to 13 weeks 6 days.60 Variability in predicting menstrual age by CRL is ±8%.62 In spontaneously conceived pregnancies, ultrasound redating of a pregnancy based on CRL is supported when the CRL varies from menstrual dating by more than 7 days between 9 weeks and 13 weeks 6 days.60 The CRL measurement in the later first trimester may be affected by fetal position and image magnification. Standardization and consistency in obtaining this measurement are critical for accuracy in gestational dating as well as risk assessment for aneuploidy.71-77 The CRL may be smaller in fetuses with central nervous system abnormalities or chromosomal aberrations.78 Significant intertwin crown-rump discordance has been reported in association with an increased risk of fetal anomalies and pregnancy complications in monochorionic twins.79, 80 In spontaneously conceived multiple gestations, gestational age should be based on the results obtained from the largest fetus, so as not to overlook a growth-restricted fetus.81 Method of Measuring CRL Between 12 Weeks 0 Days and 13 Weeks 6 Days75, 82 Fetus fills at least two-thirds of the image space available. The long axis of the fetus should be perpendicular to the ultrasound beam. The fetus should be in the midsagittal position with the profile, spine, and rump visible. The entire CRL should be visible. The fetus should be in a neutral position with fluid between the fetal chin and anterior neck. The fetus should not be hyperextended (the angle between the chin and anterior neck should not be >90°). The caliper crossbars should be placed on the outer border of the skin on the fetal head and rump. The caudal caliper should not be on the distal spine or posterior thigh or include the limbs. The maximum length of the fetus from the cranial to caudal calipers should be measured in a straight line, parallel to the long axis of the fetus. The numeric value is reported as the mean of 3 acceptable measurements. Biparietal Diameter or Head Circumference Biparietal diameter (BPD) is a reliable method of assessing gestational age in the later first trimester and has been reported to be accurate with good reproducibility.61, 66, 67, 73 Biparietal diameter and head circumference (HC) may be measured as part of a detailed first-trimester anatomic examination. Biparietal diameter and/or HC should be assessed in situations in which the CRL is technically inadequate or when an anomaly is suspected.83, 84 When interpreting the BPD, attention to the method used in the nomogram is critical, as placement of the “far” caliper may be different (inner versus outer calvarial bone).63, 64, 67, 69 Method of Measuring BPD and HC An axial scan of the fetal head with the ultrasound beam perpendicular to the midline falx should be obtained and magnified to fill the majority of the image space without compromising image quality. The fetal calvarium should not be distorted by transducer pressure or adjacent structures. The brain and calvarium should appear symmetric with the midline falx centrally located. The thalami should be seen, and the third ventricle is typically visible. Measurements are made at the widest diameter of the calvarium, perpendicular to the midline falx. The skin should not be included in the measurement. For BPD, the crossbar of the “near” caliper should be placed on the outside edge of the bone. The crossbar of the “far” caliper may be placed on the inside edge of the bone (outer to inner) or on the outer edge of the bone (outer to outer) depending on the nomogram used. For HC, the measurement is made by placing an ellipse on the outer surface of the calvarium excluding skin. Abdominal Circumference The abdominal circumference may be helpful in certain clinical situations such as early asymmetric growth restriction (triploidy) and skeletal dysplasias.61, 64, 70 Method of Measuring Abdominal Circumference An axial scan of the fetal abdomen is obtained and magnified to fill the majority of the available image space without compromising image quality. The fetal stomach and, if possible, the intrahepatic portion of the portal vein should be seen. The kidneys and umbilical cord insertion into the fetus should not be in the image. One vertebral body should be identified, and a single rib on each side lateral to the spine should be seen to ensure that the abdomen is in a true axial plane and not oblique. Optimally, the cross-section of the spine is at 3 or 9 o'clock. Measurements should be made along the outer skin edge. This can be done by an ellipse or 2 perpendicular diameters. Femoral Length Femoral length is not used for assessing gestational age due to variability in the measurement; however, it may be useful in evaluating a fetus with a suspected skeletal dysplasia.61, 71, 85 Method of Measuring Femoral Length The femoral diaphysis should be magnified to fill the majority of the image space without compromising imaging quality. The ultrasound beam is perpendicular to the long axis of the femur. The calipers are placed at the proximal and distal ends of the ossified diaphysis. Spur artifacts at the end of the femur should not be included. The longest visible diaphysis is measured. Anatomy The comprehensive assessment of fetal anatomy will be dependent on a variety of imaging factors, including fetal gestational age (size) and position as well as external maternal factors such as uterine orientation, presence of leiomyomata, and maternal habitus. For each anatomic area of interest, the image should be magnified to fill the majority of the image space available without compromising image quality. Fetal Head The fetal head is evaluated in axial and sagittal planes without significant pressure from the transducer or surrounding anatomic structures. The fetal skull should be oval in appearance, and calvarial ossification should be evident. The falx cerebri divides the brain into equal-sized symmetric halves. In the transventricular plane, the choroid plexus on each side of the falx is hyperechoic and fills the ventricular space. The choroid plexuses are not necessarily the same size or shape.86, 87 A rim of cortex can be seen around the lateral ventricles, most notably in the anterior portion of the brain. The transthalamic plane demonstrates the thalami, the cerebral peduncles, and typically the third ventricle and aqueduct of Sylvius. Angling in the axial plane toward the posterior fossa results in visualization of the semilunar fluid-filled space of the fourth ventricle. This view is commonly seen best on transvaginal imaging. The midsagittal view of the fetal head is used at this stage in gestation for measuring the nuchal translucency.88, 89 Other critical landmarks that should be visualized in the midsagittal plane include the thalami, midbrain, brain stem, intracranial lucency (fourth ventricle), and future cisterna magna.90-94 Severe central nervous system anomalies, such as the anencephaly-acrania sequence, alobar holoprosencephaly, and large cephaloceles, will frequently be detected by a structured evaluation of the fetal head.13, 14, 16, 19, 21, 95 In the midsagittal view, a compressed or absent fourth ventricle or abnormal future cisterna magna may be an early sign of spina bifida; alternatively, fourth ventricle enlargement can be associated with the Dandy-Walker continuum.90-94 In the transthalamic view, the posterior displacement of the aqueduct of Sylvius may be a marker for spina bifida.96 Biometry of the fetal head (BPD and HC) may be smaller than expected in cases of central nervous system abnormalities such as holoprosencephaly or neural tube defects.83, 84, 97 Some structures such as the cavum septi pellucidi and corpus callosum are not visible sonographically in the late first trimester. Fetal Face and Profile Midsagittal and modified coronal views are most commonly used to identify structures in the fetal profile and face. The profile should be seen in its entirety. The fetal forehead, nasal bridge, nasal bone, maxilla, and mandible should be seen. The forehead should be a normal shape (not flattened or protruding), and the nasal bone should be present. The contour of the nose and upper lip should be intact and contiguous with no maxillary protuberance. The maxilla should be intact without a maxillary gap. The presence of a maxillary gap is suspicious for a cleft palate.98 The retronasal triangle can be used to identify the paired nasal bones, premaxillary processes, primary palate, and the mandible.99-102 The absence of the mandibular gap raises a concern for micrognathia.101 A sweep of the coronal planes can be used to demonstrate the orbits, lenses, and integrity of the upper lip. Fetal Neck The fetal neck should be evaluated for cystic hygroma, dilated jugular lymphatic sacs, or other abnormal fluid collections or masses in an axial or coronal view. The nuchal translucency should be evaluated and subjectively assessed in the midsagittal view. A precise measurement is required when it appears thickened or as part of a screening protocol for aneuploidy risk assessment. A quality assessment program is recommended to ensure that false-positive and false-negative results are kept to a minimum.88, 89 Fetal Thorax and Heart The heart and chest are initially evaluated with an axial view of the thorax. The ribs should appear of normal shape, length, and ossification. The fetal lungs should be symmetric without pleural effusion. Sagittal or coronal imaging will demonstrate the demarcation between the thorax and abdomen. The fetal heart should occupy approximately one-third of the chest. Two equal-sized cardiac ventricles, atria, and atrioventricular valves should be seen on the 4-chamber view. The cardiac position within the chest and cardiac axis should be subjectively assessed. If the cardiac axis appears abnormal, it should be measured (normal, ≈45° ± 15°).103 The use of color Doppler imaging is essential for cardiac evaluation in this gestational age range and requires optimization for this application.59, 104 Color Doppler evaluation of the 4-chamber view facilitates assessment of the cardiac axis, as it better defines the ventricular septum than grayscale imaging.58, 104-107 Furthermore, color Doppler imaging allows for the evaluation of chamber symmetry and demonstration of distinct mitral and tricuspid flow during diastole.23, 58, 104, 107 The three-vessel and trachea view should be demonstrated with color Doppler and grayscale imaging when technically feasible. In the three-vessel and trachea view, the transverse aortic arch/isthmus merging with the pulmonary trunk/ductus arteriosus with antegrade flow should be demonstrated to the left side of the trachea.58, 105-107 Extended cardiac views including the longitudinal aortic and ductal arches and pulsed wave Doppler flow across the tricuspid valve and within the ductus venosus may provide a more comprehensive evaluation in those patients with suspected cardiac abnormalities.59, 108, 109 Fetal Abdomen and Pelvis The abdomen is evaluated primarily in the axial plane at 3 levels: stomach, kidneys, and bladder. The stomach should be identified on the left and the liver on the right side of the abdomen. The portal vein may be seen coursing away from the stomach. The umbilical cord insertion into the anterior abdominal wall should be demonstrated. Power or color Doppler imaging may be used to show the umbilical arteries coursing on each side of the fetal bladder. Fluid should be seen within the fetal bladder. The fetal kidneys may be identified most easily on the coronal view, aided by the appearance of the central hypoechoic space of the renal pelvis. Power or color Doppler imaging of the renal arteries is recommended if visualization of the kidneys is inadequate. Unusual cystic collections within the fetal abdomen should be noted, as they may be harbingers of fetal anomalies.28, 110 A physiologic herniation of the bowel into the base of the umbilical cord may