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    Cardiothoracic Imaging in the Pregnant Patient

    Diana E. Litmanovich, MD,*  Dennis Tack, MD, PhD,w  Karen S. Lee, MD,*

    Maryam Shahrzad, MD,*  and Alexander A. Bankier, MD, PhD*

    Abstract: Cardiovascular imaging during pregnancy poses a uniquechallenge to clinicians in differentiating between physiologicalchanges mimicking pathology and true pathologic conditions, aswell as for radiologists in terms of image quality. This review articlewill focus on 3 goals: first, to familiarize radiologists with safetyissues related to imaging pregnant women using computed tomo-graphy and magnetic resonance imaging; second, to review thecurrent, evidence-based recommendations for radiology topicsunique and common to pregnant and lactating patients; and third,to provide practical algorithms to minimize risk and increase safety

    for both the pregnant woman and the fetus.

    Key Words:   pregnancy, cardiovascular, multidetector computed

    tomography, magnetic resonance imaging, radiation dose

    (J Thorac Imaging   2014;29:38–49)

    Cardiopulmonary disorders can compromise up to 4%of all pregnancies in the industrialized world due topreexisting conditions or conditions acquired during preg-nancy.1 In part, this is related to increased age at pregnancyand an increased proportion of women of child-bearing agewith congenital heart defects.2 In western countries, mater-

    nal heart disease is now the major cause of maternal deathduring pregnancy.2 Overall, the most frequent cardiopul-monary disorders complicating pregnancy are: pulmonaryembolism (PE), aortic dissection, acute coronary syndrome,hypertension, and pneumonia, with the incidence of thesedisorders varying according to patient age and demographics.3

    Pregnancy causes profound effects on the circulatorysystem, with most of them starting in the first trimester,peaking during the second, and reaching a plateau duringthe third trimester. The main parameters affected areplasma volume, cardiac output, heart rate, blood pressure,hematocrit level, and coagulability.4,5 During the first andsecond trimesters, cardiac output can increase between 30%and 50% secondary to increase in blood volume (plasma)

    and heart rate (commonly up to 10 to 15 bpm). Decrease insystemic vascular resistance caused by the low-resistancecircuit of the placenta and vasodilatation contributes todecreases in blood pressure by 10 to 15 mm Hg.5 Decreasein the hematocrit level is due to an increase in plasma

    volume (40% at 24wk gestation, disproportional toincrease in red cell mass). Finally, heart size increases by30% by the end of the second trimester.4,5 In the thirdtrimester, the supine position causes caval compression bythe gravid uterus that may lead to a decrease in venousreturn, that is, decreased cardiac output with subsequentsupine hypotension syndrome.5 Stroke volume decreases inthe third trimester due to partial vena cava obstruction.In addition, the Virchow triad (hypercoagulability, venousstasis, and vascular damage) contributes to altered

    hemodynamics.6For radiologists, cardiothoracic imaging of pregnant

    patients poses particular problems in terms of image quality.First, the physiological changes affect the quality of tissue/vessel enhancement. Another challenge for imaging duringpregnancy is the “2 in 1” setting, that is, the simultaneousimaging of the patient and the fetus, as imaging techniquesoptimal for the patient may be harmful for the fetus and viceversa. The “2 in 1” imaging implies unavoidable simulta-neous exposure of the patient and the fetus to radiation,ultrasonographic (US) waves, or magnetic field, with allcurrently available techniques for cardiovascular andpulmonary imaging—US, computed tomography (CT) andmagnetic resonance imaging (MRI)—having advantages

    and disadvantages when imaging pregnant women. The roleof vascular US and echocardiography in cardiovascularimaging during pregnancy has been extensively discussedpreviously,7–9 and it is beyond the scope of this review. Thismanuscript will focus on 4 aspects of “2 in 1” imaging: CTsafety, MRI safety, medico-legal issues, and practicalalgorithms.

    SAFETY ASPECTS OF CT IMAGINGGeneral concerns of radiation exposure in diagnostic

    imaging (caused by substantial increase in CT utilization inthe last decade) mainly focus on the relationship betweenradiation exposure and the associated lifetime attributable

    risk for cancer in the general population.10,11 In the contextof female individuals of child-bearing age, several pub-lications have addressed specific concerns, citing an increasein cancer risk of up to 0.8% for a 20-year-old womanundergoing chest CT angiography (CTA) and potentialincrease in relative risk for breast cancer of up to 4.2% persingle cardiothoracic CTA.11,12 Relatively sparse and ran-dom scientific data in humans assessing radiation risksassociated with imaging during pregnancy in both theradiology and nonradiology communities cause hesitationand apprehension.13–16

    However, given the increase in imaging of pregnantpatients for nonobstetric cardiopulmonary conditions,familiarity with the following topics is important: risk of 

    CT radiation exposure to the patient, risk of direct andindirect CT radiation exposure to the fetus, fetal andmaternal dosimetry, approach to CT imaging of pregnant

    From the *Department of Radiology, Beth Israel Deaconess MedicalCenter, Boston, MA; and   wDepartment of Radiology, EpicuraHospital, Baudour, Belgium.

    Diana E. Litmanovich is currently receiving grants from RadiologicalSociety of North America and Society of Thoracic Radiology.Alexander A. Bankier is currently receiving a consult fee fromSpiration/Olympus and has received royalties from Harvard Med-ical School-American Thoracic Society, Elsevier, and Amirsys. Theremaining authors declare no conflicts of interest.

    Reprints: Diana E. Litmanovich, MD, Department of Radiology, BethIsrael Deaconess Medical Center, 330 Brookline Ave-Shapiro 4,Boston, MA 02215 (e-mail:   [email protected]).

    Copyright r 2013 by Lippincott Williams & Wilkins

    REVIEW ARTICLE

    38   | www.thoracicimaging.com   J Thorac Imaging    Volume 29, Number 1, January 2014

    mailto:[email protected]:[email protected]

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    patients in typical clinical scenarios, and the currentlyavailable options for CT radiation dose reduction. Safety of iodinated contrast administration during pregnancy andlactation must also be addressed. It is critical to understandthat during pregnancy 2 individuals are exposed simulta-neously, the woman and the fetus, and that the intensity of 

    the exposure and potential consequences vary substantiallybetween the 2. American College of Radiology (ACR) andAmerican Congress of Obstetricians and Gynecologistsagree that the necessary imaging examination should beperformed after clinical workup, and the radiation levelshould be kept as low as reasonably achievable.17,18

    Radiation Exposure to the PatientIn pregnant women, all the organs exposed to diagnostic

    radiation as part of cardiopulmonary assessment are at riskfor carcinogenesis: lung, heart, bone marrow, thyroid, andbreast. For example, during most common cardiothoracicCT examinations, the radiation exposure to the lungapproaches 18 to 25 mGy, even with modern scanners.19

    Justifiably, radiation exposure of a pregnant woman is of higher concern than an age-matched nonpregnant femalebecause of increased sensitivity of glandular breast tissue.11,12

    Although minimal, radiation exposure to breasts exists evenwith a chest radiograph, at a range of 150mGy (15rad) such that, if reached, might require

    termination of pregnancy.24 Exposure to 100 to 500 mGycan induce spontaneous abortion, particularly at earlystages of pregnancy. At exposures

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    pulmonary angiography (CTPA) has estimated a fetal doseup to 0.2mGy in the first trimester, 0.8 mGy in the second,and 1.3 mGy in the third trimester, when 120 kVp and100 mA were used.26 Phantom-based experiments obtainedby Doshi et al27 are in agreement with the above estimates,with the calculated fetal dose in late pregnancy received fromCTPA being in the range of 0.6 to 2.3 mGy. Hurwitz et al25

    have reported even lower doses to the fetus regardless of gestation age from CTPA protocol: 0.24 to 0.47 mGy andapproximately 0.6mGy at 0 and 3 months of pregnancy,

    respectively, with scan parameters of 140kVp and 340 mA.With these data in mind, it would be clinically unreasonableto reject, delay, or substitute a necessary CT scan due toconcern for fetal radiation exposure.

    Patient and Fetal DosimetryBoth maternal and fetal exposure can be assessed

    using an array of dosimetry techniques.12,19,20,25 Thus, aradiologist and a physicist together can estimate or calcu-late fetal, breast, or lung doses, although if the study isconducted in the first 2 weeks of pregnancy, no such esti-mate is usually required for any of the studies, includingcardiothoracic examinations,28 given the all-or-nothing

    response.18 In the vast majority of clinical cases, dose esti-mation is done in a retrospective manner.28–30 Radiationdose information, including the dose length product (DLP),effective dose, and the new parameter size-specific doseestimate entered as part of the dosimetry report, is a sufficientdocumentation for quality assurance and risk-managementpurposes. In rare cases when prospective assessment of thefetal dose (with metal oxide semiconductor field effect tran-sistor technology or thermoluminescence dosimetry techno-logy) is required, detectors can be placed on the surface of thepatient over an appropriate area corresponding to the centerof the fetus (on the basis of the gestational age), andobstetrics and gynecology specialists may need to be con-sulted. Fetal dose is estimated to be about one third of the

    entrance dose of the average patient.31 Assessment of thepatient’s breast, lung, and thyroid doses can be obtained witha similar approach.16

    CT Safety to Patient and Fetus

    Dose Reduction Techniques to Patientand Fetus—General Concept

    As the goal of radiation safety is to deliver radiationaccording to the ALARA principle—“as low as reasonablyachievable”—the approach to radiation dose reduction inpregnant patients has particular emphasis on the followingmajor procedures: (a) No standard protocol should beused—protocols should be tailored for each patient,including adjustment of kVp on the basis of body weightand obligatory use of automatic tube current modulation.(b) When appropriate, low-kilovoltage setting for contrastopacification improvement should be applied, (c) Highpitch (>1) can be used in the vast majority of CT exami-nations while maintaining diagnostic accuracy when GEand Toshiba scanners are used. With Siemens and Phillipsscanners, careful selection of mAs is also recommended todecrease the effective tube current time product.32 (d)Appropriately limited length of the examination (z-axis) isimportant for both the patient and the fetus. Additionalmeasures such as incorporation of novel reconstructionalgorithms to reduce imaging noise and allow reduction inmilliamperage and increasing the noise index when appro-priate can substantially affect radiation dose.33,34 Imagingin multiple phases (such as noncontrast enhanced exami-nation before contrast administration in patients with sus-pected aortic dissection) should be avoided. Appropriate-ness criteria, CT protocols, and radiation dose should beestablished and monitored on each clinical practice basis.

    Intravenous Iodine Contrast Administration DuringPregnancy and Lactation

    Iodine contrast agents are hydrophilic and of moder-

    ate molecular weight, thus they can cross the placenta bypassive diffusion to be eventually excreted by fetal kid-neys.35,36 No teratogenic effects have been reported withiodinated contrast agents.22 Although there is a potential toinduce neonatal hypothyroidism by direct instillation intothe amniotic sac37 or by maternal use of iodine-containingmedications, no evidence exists of neonatal hypothyroidisminduced by clinical doses of iodinated contrast media.38

    Bourjeily et al39 have shown no clinical effect of in uteroexposure to a single high dose of water-soluble iodinatedcontrast material on neonatal thyroid function. Owing tothe lack of sufficient evidence that iodinated contrastmaterial poses no risk to the fetus, the 2013 ACR Manualon Contrast Media states that iodinated contrast media

    may be given to the pregnant patient only if absolutelynecessary.18 However, because of the theoretic concern thatfetal thyroid function may be affected, neonates of allwomen exposed to iodinated contrast media during preg-nancy should be screened for hypothyroidism.36 In manycountries, including the United States and other indus-trialized countries, newborns routinely undergo this test.

    In cases in which a nursing patient was to undergo CTexamination with an intravenous (IV) iodinated contrastagent, interruption of nursing was often suggested, usuallyfor 12 to 24 hours. The theoretic risks are allergic sensitivityor reaction, neither of which has been reported.22 Theestimated amount of iodinated contrast agent absorbedthrough the infant’s bowel is approximately 0.01% of the

    contrast agent administered to the patient, which is

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    milk has been estimated to be

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    with iterative reconstructions may decrease the DLP valueto

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    vehicle accidents, and trauma more commonly occurs in thethird trimester.30,56 Fetal death can occur with both minor

    and major trauma.56In pregnant trauma patients, priority is given to

    maternal survival, as there can be no fetal survival withoutmaternal survival. Cardiovascular imaging in trauma isusually part of the overall assessment of chest, abdomen,and pelvis focusing assessment of the great vessels, media-stinum, and lungs. No alteration should be done to thetrauma protocol that could potentially compromise thequality of the study. Moreover, given that the cardio-thoracic trauma examinations entail only indirect radiationto the fetus, pregnancy should neither deter nor delay thestudy.57,58 If the patient is in a critical condition, no alter-ations in technical parameters are necessary if this poten-tially delays the examination.

    CT of the Chest: Nodules, Masses, and OtherIndications

    Although chest CT for other indications is rarelyperformed during pregnancy,59 due to the increasing aver-age age of the pregnant population, its utilization hasincreased. The most frequent indication is to evaluate apulmonary nodule, pulmonary mass, or mediastinalabnormality suspected on a chest radiograph.59 All themodifications discussed for CTPA are relevant for chestCT. However, although the entire chest should be included,the lower margin of the scan should be at the level of thediaphragm to avoid primary beam radiation of the fetus.60

    Using current dose reduction methods for routine 64-slicechest MDCT, anthropomorphic phantom measurements of the doses delivered to the breast, the lung, and the pelvis wereobtained, and the breast and lung doses were found to besubstantially less than previously published: 11 to 15 mGy forthe breast and 18mGy for the lungs, using the currentstandard clinical chest CT protocol used at our institution.19

    The protocol operates at 120 kVp and uses automatic dosemodulation, ranging from 120 to 320mA, a noise index of 11.57, and a pitch of 0.984.19 This dose reduction is a com-bined effect of the consistent use of tube settings of 120 kV orless and an automatic dose modulation algorithm provided bythe manufacturer. Increasing the pitch above 1 (for example1.3) would substantially drop the radiation dose without sac-

    rificing image quality. Note that breast radiation, although stillhigher than that measured with dedicated PE pregnancy pro-tocol, is lower than previously reported by different

    investigators by at least 50%.20,61 The fetal dose delivered bychest CT is 10,000times greater than that of the earth (50mT).63 Although use of MRI has not been shown to have any deleterious effects onthe fetus, the safety of MRI during pregnancy has yet to be

    definitively established.22,64 There are 3 potential hazardouseffects MRI can have on the fetus63,65,66: (1) potential bio-logical damage related to cell migration, proliferation, anddifferentiation, possibly leading to miscarriage due to expo-sure to the static magnetic field; (2) tissue heating potentialand secondary damage, particularly with regard to organo-genesis due to energy deposition by radiofrequency pulses;and (3) potential damage to the fetal ear (especially after24 wk gestation) due to the high acoustic noise level invarying gradient electromagnetic fields, particularly withfast-acquisition sequences.67

    Given the lack of long-term data in human subjectsproving the safety of MRI for the fetus, the ACR White Paperon MR safety (2007) states that pregnant patients should

    undergo MRI only if: (1) the required information cannot beobtained through other nonionizing means; (2) the informa-tion is likely to alter patient care; and (3) the examinationcannot wait until after completion of the pregnancy.68

    TeratogenesisThe static magnetic field of MRI can potentially cause

    cell migration, proliferation, and differentiation within thefetus resulting in teratogenesis. However, multiple studiesshow no scientific evidence of teratogenesis in humans seenup to 9 years after exposure to MRI in utero.69 In terms of risks of MRI exposure, the ACR does not distinguishbetween the first trimester of pregnancy and the second and

    third trimesters.66,68 As per the ACR White Paper, at anystage during pregnancy, a risk-benefit analysis should beperformed before MRI.

    TABLE 3.   CTPA Acquisition Parameters for Pregnant Patients

    kVp 100mA Up to 200Scan range 1 cm above aortic arch to dome of the

    diaphragm

    Injectionparameters Automatic triggeringThreshold: 150 HUROI: main pulmonary artery

    Short scanduration

    Preferably 64-slices or more

    High iodine influx Increased flow >5 mL/minHigh iodine concentration >350 iodium/mL

    Respiration Suspended respiration

    ROI indicates region of interest.Adapted with permission from Lippincott Williams and Wilkins/Wolters

    Kluwer Health: Litmanovich et al.21

     J Thorac Imaging    Volume 29, Number 1, January 2014   Cardiovascular Imaging 

    r  2013 Lippincott Williams & Wilkins   www.thoracicimaging.com   | 43

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    Tissue HeatingExposure to radiofrequency pulses can cause tissue

    heating, with subsequent heating of fetal stem cells and, as aresult, potential teratogenesis. For all MRI examinations, tis-sue heating associated with MRI exposure is measured inspecific absorption rate units (SAR).66 SAR is a measure of the

    rate at which energy is absorbed by the body when exposed toa radiofrequency electromagnetic field. It is measured in W/kg,reflecting power absorbed per mass of tissue. SAR units forMRI are regulated by the Food and Drug Administration,which currently makes no specific recommendations forpregnant patients.70 SAR is influenced by a number of parameters such as static magnetic field strength, flip angle,number of radiofrequency pulses, and spacing between radi-ofrequency pulses. An increase in the first 3 parameters and adecrease in the last parameter can all cause an increase inSAR. In addition, radiofrequency refocusing pulses tend togenerate more magnetization and thus more heat because theflip angles utilized approach 180 degrees.71

    Single-shot echo-train spin-echo sequences (single-shot

    fast spin-echo) use a long train of 180-degree refocusingpulses, leading to high SAR, and in some instancesapproach SAR limits set by the International Commissionon Non-Ionizing Radiation Protection.72 It is important toremember, however, that the majority of heating created byMRI is superficial and absorbed by the maternal body withonly a fraction reaching the fetus.70 Further, in a study byHand and colleagues, fetal SAR and fetal temperature weredemonstrated to be within international safety limits forMRI procedures compliant with the International Elec-trotechnical Commission normal mode condition. Aninternational consensus states that MRI of pregnantpatients should also be performed with 3.0T magnets orless to minimize SAR.73 Another method to reduce SAR is

    to utilize gradient-recalled echo sequences, which have alower SAR compared with single-shot fast spin-echosequences.66 Some authors have suggested decreasing theroom temperature in the MRI suite to

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    MRI in pregnancy, radiologists should be aware that suchimaging involves potential medico-legal risk.82 To minimizethis potential, certain guidelines for imaging pregnantpatients with CT and MRI should be followed. Theseinclude: (1) an established process for evaluating pregnantpatients in a radiologic facility; (2) a written policy formanagement of pregnant and lactating women; (3) accessi-bility of radiologists knowledgeable about MRI/CT exposureeffects to patients and referring physicians; and (4) and doc-umentation in the radiology report of all discussions with

    patients about the risks/benefits of a specific CT examination.Four main questions have to be answered by the referring

    clinician and radiologist when planning CT or MRI during

    pregnancy: (1) Can the information be obtained without CT orMRI examinations? (2) Can the information be obtainedwithout IV contrast administration? (3) Will the informationobtained with imaging affect the care of the patient or fetusduring the pregnancy? and (4) Can imaging be safely deferreduntil after pregnancy?

    Informed ConsentAt our institution, informed consent is obtained for all

    studies involving ionizing radiation including conventional

    radiography, computer tomography, and MRI. While obtain-ing informed consent, the radiologist should explain the needfor imaging and the importance of the diagnosis for the

    Is CT the best modality for specific question?

    No

    Proceed with modality of choice

    Yes

    Yes No

    Image acquisition

    according to ALARA

    principle

    Clinician -Radiologist discussion

    Can the study be postponed?

    NoYes

    After informed consent obtained from the patient, proceed with CT examination as following:

    Low kVp(

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    patient’s care as well as a brief explanation of the orderedimaging test. While summarizing the estimated risk to thepatient and the fetus, the radiologist has the opportunity toconfirm the patient’s comprehension of the risks and benefits as

    well as alternative options before consenting.43 The emphasison a low risk of harm to the fetus by CT scanning (comparedwith the known 15% risk for spontaneous abortion and 1% to3% risk for major malformation) and no documented risk tothe fetus caused by MRI is important.

    Patient consent is essential before imaging is obtained.Discussion with patients about the risks/benefits should bedocumented in the radiology report, including: (a) need forimaging and the importance of the diagnosis for patient’scare; (b) brief explanation of the ordered imaging test; (c)summary of the estimated risks to the patient and the fetus;and (d) confirmation of the patient’s understanding of andconsent to the diagnostic test.

    A new approach has been recently suggested83 to assess

    the radiation dose in terms of background radiation equivalent(BRE). This approach compares radiation delivered by a cer-tain examination to the annual background radiation. Forexample, annual radiation exposure in the United States is3.1mSv/y, so when radiation delivered by a chest radiograph iscompared with this dose, it would be equivalent to 0.02 mSv ora BRE of 2.1 days. The substantially higher radiation deliveredby chest CTA of 3 to 6 mSv, depending on the protocol, wouldbe equivalent to a BRE of 1 to 2 years.

    PROPOSED PRACTICAL ALGORITHMS FORMDCT AND MRI SCANNING IN

    PREGNANT PATIENTS

    As stated previously, both MDCT and MRI can beobtained in pregnant patients for the purposes of car-diothoracic imaging if indicated, after careful discussion of 

    risks versus benefits with the referring clinician. Algorithm2 (Fig. 4) is designed to help determine whether MDCT isthe modality of choice for the female patient with suspectedcardiothoracic disease. After the study is completed, the

    report should include the following: the informed consentdiscussion that occurred before the study, description of theimaging findings, radiation dose recording from the reportgenerated by the MDCT scanner, and recommendation toobtain neonatal thyroid function check-up (routinelyobtained in all newborns in the United States). Algorithm 3(Fig. 5) is designed to help determine whether MRI is themodality of choice for the female patient with suspectedcardiothoracic disease. After the study is completed, thereport should include the following: informed consent dis-cussion, imaging findings, and whether or not IV gadoli-nium was administered. If gadolinium was administered,the report should state that no specific neonatal tests arenecessary after birth.

    SUMMARYDespite potential adverse implications of cardio-

    thoracic CT and MRI in pregnancy, they remain a crucialpart in a variety of potential clinical scenarios duringpregnancy. Combined efforts of a referring clinician andradiologist are essential for providing the best practice.When an acute problem is identified by a referring providerand the pregnant patient is referred to imaging with aspecific question related to cardiothoracic pathology, it isthe radiologist’s role to decide whether the diagnosticquestion can be answered with a nonionizing modality suchas US or MRI or whether CT is more appropriate. On the

    basis of feasibility and/or specific questions asked, it is theradiologist’s role to estimate fetal and maternal risk from aknown radiation dose in each specific case or the potential

    Clinician Radiologist discussion

    Can the study be postponed?

    Yes

    After informed consent obtained from the patient, obtained, proceed with study ensuring

    adequate technical parameters

    Is protocol adjustment possible? Is IV Gd necessary?

    Yes No NoYes/ Regular Gd dose

    Is the patient pregnant?

    Is MRI the best modality for specific question?

    YesNo

    Regular MRI study

    According to accepted standards

    No

    NoYes

    FIGURE 5.   Algorithm 3. Suggested approach to MRI examination in pregnancy.

    Litmanovich et al    J Thorac Imaging    Volume 29, Number 1, January 2014

    46   | www.thoracicimaging.com   r  2013 Lippincott Williams & Wilkins

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    adverse effects of MRI, as well as to structure the exami-nation without compromising diagnostic accuracy. Themost frequent indications such as suspected PE, aorticdissection, and, relatively rarely, trauma or parenchymalpathology should be properly addressed after discussionwith both the referring provider and the patient.

    The best practice for imaging of pregnant or potentiallypregnant patients with ionizing radiation is as follows: “Tomaintain a high standard of safety, particularly when imagingpotentially pregnant patients, imaging radiation must beapplied at levels as low as reasonably achievable (ALARA),whereas the degree of medical benefit must counterbalancethe well-managed levels of risk.” Necessary imaging exami-nation should be performed after clinical workup, and theradiation level should be kept as low as reasonably achiev-able. The patient should give informed consent before theprocedure. Careful approach to MRI during pregnancy withemphasis on minimizing potential acoustic damage and tissueheating is essential despite primarily theoretical potential fetaldamage from the procedure.

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