REVIEW ARTICLE

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 unique challenge to clinicians in dierentiating between physiological changes mimicking pathology and true pathologic conditions, as well as for radiologists in terms of image quality. This review article will focus on 3 goals: rst, to familiarize radiologists with safety issues related to imaging pregnant women using computed tomography and magnetic resonance imaging; second, to review the current, evidence-based recommendations for radiology topics unique 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;29:3849)

ardiopulmonary disorders can compromise up to 4% of all pregnancies in the industrialized world due to preexisting conditions or conditions acquired during pregnancy.1 In part, this is related to increased age at pregnancy and an increased proportion of women of child-bearing age with congenital heart defects.2 In western countries, maternal heart disease is now the major cause of maternal death during pregnancy.2 Overall, the most frequent cardiopulmonary disorders complicating pregnancy are: pulmonary embolism (PE), aortic dissection, acute coronary syndrome, hypertension, and pneumonia, with the incidence of these disorders varying according to patient age and demographics.3 Pregnancy causes profound eects on the circulatory system, with most of them starting in the rst trimester, peaking during the second, and reaching a plateau during the third trimester. The main parameters aected are plasma volume, cardiac output, heart rate, blood pressure, hematocrit level, and coagulability.4,5 During the rst and second 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 in systemic vascular resistance caused by the low-resistance circuit of the placenta and vasodilatation contributes to decreases in blood pressure by 10 to 15 mm Hg.5 Decrease in the hematocrit level is due to an increase in plasma
From the *Department of Radiology, Beth Israel Deaconess Medical Center, Boston, MA; and wDepartment of Radiology, Epicura Hospital, Baudour, Belgium. Diana E. Litmanovich is currently receiving grants from Radiological Society of North America and Society of Thoracic Radiology. Alexander A. Bankier is currently receiving a consult fee from Spiration/Olympus and has received royalties from Harvard Medical School-American Thoracic Society, Elsevier, and Amirsys. The remaining authors declare no conicts of interest. Reprints: Diana E. Litmanovich, MD, Department of Radiology, Beth Israel Deaconess Medical Center, 330 Brookline Ave-Shapiro 4, Boston, MA 02215 (e-mail: dlitmano@bidmc.harvard.edu). Copyright r 2013 by Lippincott Williams & Wilkins

volume (40% at 24 wk gestation, disproportional to increase in red cell mass). Finally, heart size increases by 30% by the end of the second trimester.4,5 In the third trimester, the supine position causes caval compression by the gravid uterus that may lead to a decrease in venous return, that is, decreased cardiac output with subsequent supine hypotension syndrome.5 Stroke volume decreases in the third trimester due to partial vena cava obstruction. In addition, the Virchow triad (hypercoagulability, venous stasis, and vascular damage) contributes to altered hemodynamics.6 For radiologists, cardiothoracic imaging of pregnant patients poses particular problems in terms of image quality. First, the physiological changes aect the quality of tissue/ vessel enhancement. Another challenge for imaging during pregnancy is the 2 in 1 setting, that is, the simultaneous imaging of the patient and the fetus, as imaging techniques optimal for the patient may be harmful for the fetus and vice versa. The 2 in 1 imaging implies unavoidable simultaneous exposure of the patient and the fetus to radiation, ultrasonographic (US) waves, or magnetic eld, with all currently available techniques for cardiovascular and pulmonary imagingUS, computed tomography (CT) and magnetic resonance imaging (MRI)having advantages and disadvantages when imaging pregnant women. The role of vascular US and echocardiography in cardiovascular imaging during pregnancy has been extensively discussed previously,79 and it is beyond the scope of this review. This manuscript will focus on 4 aspects of 2 in 1 imaging: CT safety, MRI safety, medico-legal issues, and practical algorithms.

SAFETY ASPECTS OF CT IMAGING

General concerns of radiation exposure in diagnostic imaging (caused by substantial increase in CT utilization in the last decade) mainly focus on the relationship between radiation exposure and the associated lifetime attributable risk for cancer in the general population.10,11 In the context of female individuals of child-bearing age, several publications have addressed specic concerns, citing an increase in cancer risk of up to 0.8% for a 20-year-old woman undergoing chest CT angiography (CTA) and potential increase in relative risk for breast cancer of up to 4.2% per single cardiothoracic CTA.11,12 Relatively sparse and random scientic data in humans assessing radiation risks associated with imaging during pregnancy in both the radiology and nonradiology communities cause hesitation and apprehension.1316 However, given the increase in imaging of pregnant patients for nonobstetric cardiopulmonary conditions, familiarity with the following topics is important: risk of CT radiation exposure to the patient, risk of direct and indirect CT radiation exposure to the fetus, fetal and maternal dosimetry, approach to CT imaging of pregnant J Thorac Imaging


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patients in typical clinical scenarios, and the currently available options for CT radiation dose reduction. Safety of iodinated contrast administration during pregnancy and lactation must also be addressed. It is critical to understand that during pregnancy 2 individuals are exposed simultaneously, the woman and the fetus, and that the intensity of the exposure and potential consequences vary substantially between the 2. American College of Radiology (ACR) and American Congress of Obstetricians and Gynecologists agree that the necessary imaging examination should be performed after clinical workup, and the radiation level should be kept as low as reasonably achievable.17,18

Radiation Exposure to the Patient

In pregnant women, all the organs exposed to diagnostic radiation as part of cardiopulmonary assessment are at risk for carcinogenesis: lung, heart, bone marrow, thyroid, and breast. For example, during most common cardiothoracic CT examinations, the radiation exposure to the lung approaches 18 to 25 mGy, even with modern scanners.19 Justiably, radiation exposure of a pregnant woman is of higher concern than an age-matched nonpregnant female because of increased sensitivity of glandular breast tissue.11,12 Although minimal, radiation exposure to breasts exists even with a chest radiograph, at a range of <0.04 mSv and should be multiplied by at least a factor of 200 as compared with multidetector CT (MDCT) radiation. Unlike abdomen and pelvis CT, cardiopulmonary CT examinations deliver direct breast radiation in the range of 10 to 50 mGy, depending on the protocol used,19,20 which is equivalent to 10 to 15 routine mammograms. The amount of radiation was shown to be even higher when a coronary CTA protocol is used (from 43 to 90 mGy), a rare but not unseen examination during pregnancy. Such doses were measured, with kVp ranging from 120 to 140 and mA approaching as high as 645.12 Even though more recent protocols with automatic exposure control (AEC) deliver a dose between 10 and 15 mGy or less,19,21 radiation exposure to the breast is an increasingly important consideration when planning any cardiothoracic CT examinations.12,20

Radiation Exposure to the Fetus

Radiation exposure to the fetus has stochastic and deterministic eects. Stochastic eect (also known as carcinogenesis) indicates the risk of the exposed fetus for carcinogenesis in childhood. This risk reects the potential consequences of ionizing radiation producing cellular damage through chemical and/or physical processes. This

damage can lead to nuclear DNA changes resulting in genetic mutations or carcinogenesis. The linear or no threshold approach to the stochastic eect postulates that it may occur with any amount of radiation exposure, and its severity is independent of the radiation dose.18 In other words, according to the linear or no threshold approach, there is no threshold radiation below which there would be no risk for the fetus. On the basis of probability calculations, exposure of 50 mGy (5 rad) may lead to doubling or even tripling the baseline risk for childhood carcinogenesis from 0.1% to 0.2%.18 Despite recent wide use of CT scanning, no documented fetal radiation eect has been reported at this level so far. Estimated fetal risk based on gestational age and magnitude of radiation exposure, in conjunction with practice guidelines for imaging pregnant patients, was published by ACR in 2013 (Table 1).18 The guidelines emphasize, however, that all the estimates are based on extrapolation from animal studies, atomic bomb survivors epidemiologic studies, and studies of groups exposed to medical radiation.18 Nonstochastic (deterministic) eect also known as the threshold eect is caused by radiation at higher doses exceeding certain thresholds and reects the risk for organogenesis and teratogenesis of the exposed fetus. These risks are predictable and represent the result of physical and/or chemical processes leading to either cellular death, resulting in morphologic changes, or changes in nuclear DNA, leading to carcinogenesis, chromosomal aberrations, and genetic mutations.22 The presence of a threshold following linear progression that increases in frequency and severity with increase in exposure dose is the main dierence compared with the stochastic eect.23 Organogenesis defects can be seen after exposure to radiation levels > 150 mGy (15 rad) such that, if reached, might require termination of pregnancy.24 Exposure to 100 to 500 mGy can induce spontaneous abortion, particularly at early stages of pregnancy. At exposures <100 mGy, no adverse eects have been documented, thus 100 mGy and below would be considered the no adverse eect level or NOAEL.23 The potential eects of dierent amounts of radiation exposure at dierent stages of pregnancy, with an emphasis on timing of exposure, are summarized in Table 2.

Fetal Diagnostic Radiation Exposure

Indirect fetal radiation exposure is caused by head, neck, and all types of cardiothoracic CT. For cardiothoracic CT, exposure is several magnitudes <0.5 mGy.12,19,25 MonteCarlobased assessment of fetal radiation dose from CT

TABLE 1. Summary of Potential Deterministic Effects on the Embryo and Fetus From Radiation Exposure

Potential Eect of Radiation Exposure Gestational Age (wk)

0-2 (before implantation) 3-4 (organogenesis) 5-10 (organogenesis) 11-17 (fetal period) 18-27 (fetal period) > 27 (fetal period)

<50 mGy
No No No No No No eect eect eect eect eect eect

50-100 mGy
No eect Probably none Uncertain Uncertain No eect No eect

>100 mGy
No eect Possible spontaneous abortion Possible malformations Possible IQ decit or MR IQ decit not detectable at diagnostic doses No eect applicable to diagnostic medicine

IQ indicates intelligence quotient; MR, mental retardation. Reprinted with permission of the American College of Radiology. No other representation of this material is authorized without expressed, written permission from the American College of Radiology.

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TABLE 2. Potential Teratogenesis Effects of Different Amounts of Radiation Exposure at Different Stages of Pregnancy

CT Safety to Patient and Fetus Dose Reduction Techniques to Patient and FetusGeneral Concept
As the goal of radiation safety is to deliver radiation according to the ALARA principleas low as reasonably achievablethe approach to radiation dose reduction in pregnant patients has particular emphasis on the following major procedures: (a) No standard protocol should be usedprotocols should be tailored for each patient, including adjustment of kVp on the basis of body weight and obligatory use of automatic tube current modulation. (b) When appropriate, low-kilovoltage setting for contrast opacication improvement should be applied, (c) High pitch (>1) can be used in the vast majority of CT examinations while maintaining diagnostic accuracy when GE and Toshiba scanners are used. With Siemens and Phillips scanners, careful selection of mAs is also recommended to decrease the eective tube current time product.32 (d) Appropriately limited length of the examination (z-axis) is important for both the patient and the fetus. Additional measures such as incorporation of novel reconstruction algorithms to reduce imaging noise and allow reduction in milliamperage and increasing the noise index when appropriate can substantially aect radiation dose.33,34 Imaging in multiple phases (such as noncontrast enhanced examination before contrast administration in patients with suspected aortic dissection) should be avoided. Appropriateness criteria, CT protocols, and radiation dose should be established and monitored on each clinical practice basis.

Gestational Age (wk)

0-2 3-8 8-15

Potential Eect of Radiation Estimated Exposure Dose Threshold (mGy)

All (death of embryo) or none Congenital multisystem anomalies Growth retardation Severe MR* (high risk)w IQ decit Microcephaly Severe MR (low risk) 50-100 200 200-250 60-310 25 IQ point loss per 1 Gy 200 250-280

16-25

*Period of rapid neuronal development and migration. wData based on results of animal studies, epidemiologic studies of atomic bomb survivors, and studies of groups exposed to radiation for medical reasons. IQ indicates intelligence quotient; MR, mental retardation. Modied from original version from Patel et al.15 r Radiological Society of North America.

pulmonary angiography (CTPA) has estimated a fetal dose up to 0.2 mGy in the rst trimester, 0.8 mGy in the second, and 1.3 mGy in the third trimester, when 120 kVp and 100 mA were used.26 Phantom-based experiments obtained by Doshi et al27 are in agreement with the above estimates, with the calculated fetal dose in late pregnancy received from CTPA 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 and approximately 0.6 mGy at 0 and 3 months of pregnancy, respectively, with scan parameters of 140 kVp and 340 mA. With these data in mind, it would be clinically unreasonable to reject, delay, or substitute a necessary CT scan due to concern for fetal radiation exposure.

Intravenous Iodine Contrast Administration During Pregnancy and Lactation

Iodine contrast agents are hydrophilic and of moderate molecular weight, thus they can cross the placenta by passive diusion to be eventually excreted by fetal kidneys.35,36 No teratogenic eects have been reported with iodinated contrast agents.22 Although there is a potential to induce neonatal hypothyroidism by direct instillation into the amniotic sac37 or by maternal use of iodine-containing medications, no evidence exists of neonatal hypothyroidism induced by clinical doses of iodinated contrast media.38 Bourjeily et al39 have shown no clinical eect of in utero exposure to a single high dose of water-soluble iodinated contrast material on neonatal thyroid function. Owing to the lack of sucient evidence that iodinated contrast material poses no risk to the fetus, the 2013 ACR Manual on Contrast Media states that iodinated contrast media may be given to the pregnant patient only if absolutely necessary.18 However, because of the theoretic concern that fetal thyroid function may be aected, neonates of all women exposed to iodinated contrast media during pregnancy should be screened for hypothyroidism.36 In many countries, including the United States and other industrialized countries, newborns routinely undergo this test. In cases in which a nursing patient was to undergo CT examination with an intravenous (IV) iodinated contrast agent, interruption of nursing was often suggested, usually for 12 to 24 hours. The theoretic risks are allergic sensitivity or reaction, neither of which has been reported.22 The estimated amount of iodinated contrast agent absorbed through the infants bowel is approximately 0.01% of the contrast agent administered to the patient, which is <1% of the permitted infant dose of 2 mL/kg.40 The expected absorbed dose by the infant from the ingestion of breast
r

Patient and Fetal Dosimetry

Both maternal and fetal exposure can be assessed using an array of dosimetry techniques.12,19,20,25 Thus, a radiologist and a physicist together can estimate or calculate fetal, breast, or lung doses, although if the study is conducted in the rst 2 weeks of pregnancy, no such estimate is usually required for any of the studies, including cardiothoracic examinations,28 given the all-or-nothing response.18 In the vast majority of clinical cases, dose estimation is done in a retrospective manner.2830 Radiation dose information, including the dose length product (DLP), eective dose, and the new parameter size-specic dose estimate entered as part of the dosimetry report, is a sucient documentation for quality assurance and risk-management purposes. In rare cases when prospective assessment of the fetal dose (with metal oxide semiconductor eld eect transistor technology or thermoluminescence dosimetry technology) is required, detectors can be placed on the surface of the patient over an appropriate area corresponding to the center of the fetus (on the basis of the gestational age), and obstetrics and gynecology specialists may need to be consulted. Fetal dose is estimated to be about one third of the entrance dose of the average patient.31 Assessment of the patients breast, lung, and thyroid doses can be obtained with a similar approach.16

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milk has been estimated to be <0.05% of the recommended dose of contrast agent if the infant were to undergo a contrast-enhanced imaging study. Thus, no interruption of lactation is required.36,41,42

Dose Reduction Techniques for CT Scanning in Pregnant Patients: Specific Clinical Scenarios
The most important and meaningful way to reduce radiation exposure is to prevent unnecessary study by appropriate patient selection and pretest probability evaluation, as well as by substituting radiation-bearing study with an appropriate no-radiation-exposure alternative. The following focuses on specic MDCT examinations and appropriate MDCT protocol variations.

the early stages of pregnancy tend to be lower than those of V/Q scanning, because of a lack of direct fetal radiation.19,25,44 The major shortcoming of CTPA is the signicantly higher breast radiation dose (10 to 90 mGy) compared with V/Q scan (0.28 mGy).44 Currently, the choice between CTPA and V/Q scanning is made according to accessibility, local expertise, necessity to exclude alternative diagnosis (done with CTPA), and radiation exposure consideration at dierent stages of pregnancy. Discussion regarding V/Q scan is beyond the scope of this manuscript. The following focuses on the overall decrease in the radiation dose to both the patient and the fetus and techniques for improving image quality of CTPA in pregnancy. Strategies to Decrease CT Radiation Dose Methods used to decrease radiation dose in CTPA in the general population can be applied in pregnant patients, with some modications: pitch >1 (preferably 1.5 to 2), increase in collimation (1.5 mm), and optimization of scan coverage (z-axis). Z-axis coverage from 1 cm above the aortic arch to the level of diaphragm can decrease the delivered dose by up to 40% compared with full-length chest CT.47 AEC allowing a relatively high noise index (16 or higher) for reconstruction in the soft tissue kernel, in combination with the maximum available mA of 200 protects from overexposure and is appropriate in the vast majority of patients with a body mass index of 35 or less.21 Low kilovoltage improved opacication of the vasculature, in particular the pulmonary arteries, while decreasing radiation dose (Fig. 3).48,49 Lowering kVp has the most signicant impact on radiation dose given their exponential relationship, with diagnostic accuracy achieved in both general and pregnant populations.50 Combination of decreased kVp and mAs decreased CTDIvol, DLP, and calculated eective dose by a factor of 4.21 CTDIvol of <5 mGy and DLP values not exceeding 150 mGy cm were routinely achieved. With this protocol, the radiation dose delivered to the breast and fetus were in the range of 4 to 6 mGy and 0.1 mGy, respectively, as measured using an anthropomorphic phantom, substantially lower than previously published,19 with a lung radiation dose of <8.1 mGy. Iterative reconstructing algorithms were applied to compensate for imaging noise caused by decrease in kVp and mA. Those algorithms allow additional radiation dose savings of up to 50%. Combination of low-dose kilovoltage

CTPA
To prevent mortality and morbidity from venous thromboembolism, a high index of clinical suspicion followed by a timely and accurate diagnostic approach is required.15,43 Diagnosis in the vast majority of cases is done with CTPA followed by ventilation-perfusion (V/Q) scanning, with the choice being dicult as both studies have demonstrated similar high sensitivity, specicity, and accuracy (Fig. 1).44 In addition, assessment of a pregnant patient with suspected PE with MRI can be potentially performed, although relatively few centers comprise the necessary expertise.45 Current Clinical Practice Guidelines for Assessment of Suspected PE in Pregnancy A multidisciplinary panel of major leaders in related medical elds has developed evidence-based guidelines for evaluation of suspected PE in pregnancy using the Grades of Recommendation, Assessment, Development, and Evaluation (GRADE) system.46 Although a substantial portion of underlying evidence for all recommendations was rated as very low or low, the panel provided ocial guidelines for assessment of PE in pregnant patients. The highlights of the GRADE recommendations46 stratifying the approach to assessment of pregnant patients with suspected PE are summarized in Figure 2 focusing on the ocial guidelines for assessment of PE in pregnancy. Radiation Exposure to Patient and Fetus Fetal radiation exposure is extremely low with CTPA and V/Q examinations (<1 mGy for both). CTPA doses at

FIGURE 1. A 27-week pregnant 31-year-old patient with chest pain and shortness of breath. Chest radiograph (A) demonstrates bilateral opacities and plural effusions, as well as potential consolidations. Given the abnormal chest radiograph, further assessment was done with CTPA and not V/Q scan. Axial soft tissue (B) and lung window (C) images show a combination of pulmonary edema, pleural effusion and consolidations, and normal opacification of pulmonary arteries. A kVp of 100 and a maximum mAs of 100 were used resulting in a DLP of 113 mGy cm.
r

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Suspected pulmonary embolism in pregnancy

Leg Symptoms

Yes

No

Ultrasound

Negative results

Radiography

Abnormal findings

Normal findings

CTPA

Nondiagnostic results

V/Q

FIGURE 2. Algorithm 1. Society of Thoracic Radiology and American Thoracic Society imaging guidelines for suspected PE in pregnancy. Reprinted with permission of the American Thoracic Society. Copyright r 2013 American Thoracic Society. Leung et al.46

with iterative reconstructions may decrease the DLP value to <80 mGy cm.51 Shielding of the breast tissue and fetus is a controversial topic that requires further research. Meanwhile, the suggested approach is as follows: both external and internal fetal shielding should be used. Although external shielding is not necessary given the miniscule dose delivered to the fetus, it may provide the patient more reassurance than actual risk reduction.30 Oral administration of 30% barium sulfate 20 to 30 min before the CT examination provides internal shielding from scattered radiation by distributing in the stomach, duodenum, and proximal small bowel.52 Currently, there has been only 1 study conducted using a phantom, and assessment in a clinical patient may be helpful. Breast shielding still remains debatable in pregnant patients similar to the general population. Although dose reduction up to 50% has been achieved with breast shielding, beam hardening artifacts and increased image noise remain a problem even more substantial for the pregnant population because of kVp and mA being lower than usual in pregnant CTPA protocols. In addition, timing of breast shield placing is crucial, as placement before

obtaining the scout view may increase the tube current due to AEC activation. Similar dose reduction can be achieved with the methods previously described for decreasing tube output, which have less impact on image quality.53 Methods to Improve Image Quality The combination of decreased vascular contrast enhancement in a hyperdynamic circulation and a change in the breathing pattern in pregnant women with an increased risk for Valsalva maneuvers can potentially cause suboptimal CTPA image quality in a substantial number of studies if standard CTA acquisition protocols are used.54,55 To improve image quality and to keep radiation as low as possible, adaptation of the protocol is necessary.43,53,55 The suggested modications are summarized in Table 3.

Chest CT for Trauma

Trauma is one of the leading nonobstetric causes of maternal and fetal death56 and aects up to 7% of pregnant patients, with physiological changes in pregnancy occasionally masking the severity of the maternal condition. The most common cause of trauma in pregnancy is motor

FIGURE 3. A 13-week pregnant 21-year-old patient with severe dyspnea, pleuritic chest pain, and fever. CTPA was obtained given patients history of asthma. Given the body mass index of 19, 80 kVp and maximum mAs of 100 were selected. Excellent opacification of the pulmonary arterial tree was demonstrated (A and B). B, Coronal reconstructions demonstrate limited field of view from 1 cm above the aortic arch till the dome of the diaphragm. As part of routine internal shielding, 2 cups of oral barium were administered, with barium seen in the stomach (white arrow, B). C, Combination of kVp, mAs, and adjusted z-axis resulted in a DLP of 52 mGy cm.

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TABLE 3. CTPA Acquisition Parameters for Pregnant Patients kVp mA Scan range Injection parameters 100 Up to 200 1 cm above aortic arch to dome of the diaphragm Automatic triggering Threshold: 150 HU ROI: main pulmonary artery Preferably 64-slices or more

investigators by at least 50%.20,61 The fetal dose delivered by chest CT is <0.2 mGy,19 which is lower than that reported for V/Q scintigraphy performed in pregnant patients with suspected PE.62 However, the dose is not zero, indicating the potential presence of a stochastic risk that should be considered when designing examination protocols according to the ALARA principle.

Short scan duration High iodine inux Increased ow >5 mL/min High 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

Cardiac CTA
Dedicated cardiac electrocardiogram (ECG)-gated CTA in pregnancy is rarely indicated, but given the rising age of pregnant patients, it might be consideredusually in cases of atypical chest pain in the presence of risk factors for coronary artery disease. In such cases, discussion with the referring cardiologist is obligatory to fully understand the indications for the study. If the decision to proceed with ECG-gated study is taken, all attempts should be made to minimize radiation: there is no need to obtain calcium scoring; all attempts to obtain the study using prospective ECG-gating should be made (might be challenging in pregnant patients because of physiologically elevated heart rates); and careful attention to the appropriate z-axis coverage is crucial to avoid overscanning too far distally.

vehicle accidents, and trauma more commonly occurs in the third trimester.30,56 Fetal death can occur with both minor and major trauma.56 In pregnant trauma patients, priority is given to maternal survival, as there can be no fetal survival without maternal survival. Cardiovascular imaging in trauma is usually part of the overall assessment of chest, abdomen, and pelvis focusing assessment of the great vessels, mediastinum, and lungs. No alteration should be done to the trauma protocol that could potentially compromise the quality of the study. Moreover, given that the cardiothoracic trauma examinations entail only indirect radiation to the fetus, pregnancy should neither deter nor delay the study.57,58 If the patient is in a critical condition, no alterations in technical parameters are necessary if this potentially delays the examination.

SAFETY ASPECTS OF MRI Potential Hazards in MRI

MRI is not associated with ionizing radiation exposure. However, it exposes the fetus to a magnetic eld >10,000 times greater than that of the earth (50 mT).63 Although use of MRI has not been shown to have any deleterious eects on the fetus, the safety of MRI during pregnancy has yet to be denitively established.22,64 There are 3 potential hazardous eects MRI can have on the fetus63,65,66: (1) potential biological damage related to cell migration, proliferation, and dierentiation, possibly leading to miscarriage due to exposure to the static magnetic eld; (2) tissue heating potential and secondary damage, particularly with regard to organogenesis due to energy deposition by radiofrequency pulses; and (3) potential damage to the fetal ear (especially after 24 wk gestation) due to the high acoustic noise level in varying gradient electromagnetic elds, particularly with fast-acquisition sequences.67 Given the lack of long-term data in human subjects proving the safety of MRI for the fetus, the ACR White Paper on MR safety (2007) states that pregnant patients should undergo MRI only if: (1) the required information cannot be obtained through other nonionizing means; (2) the information is likely to alter patient care; and (3) the examination cannot wait until after completion of the pregnancy.68

CT of the Chest: Nodules, Masses, and Other Indications

Although chest CT for other indications is rarely performed during pregnancy,59 due to the increasing average age of the pregnant population, its utilization has increased. The most frequent indication is to evaluate a pulmonary nodule, pulmonary mass, or mediastinal abnormality suspected on a chest radiograph.59 All the modications discussed for CTPA are relevant for chest CT. However, although the entire chest should be included, the lower margin of the scan should be at the level of the diaphragm to avoid primary beam radiation of the fetus.60 Using current dose reduction methods for routine 64-slice chest MDCT, anthropomorphic phantom measurements of the doses delivered to the breast, the lung, and the pelvis were obtained, and the breast and lung doses were found to be substantially less than previously published: 11 to 15 mGy for the breast and 18 mGy for the lungs, using the current standard clinical chest CT protocol used at our institution.19 The protocol operates at 120 kVp and uses automatic dose modulation, ranging from 120 to 320 mA, a noise index of 11.57, and a pitch of 0.984.19 This dose reduction is a combined eect of the consistent use of tube settings of 120 kV or less and an automatic dose modulation algorithm provided by the manufacturer. Increasing the pitch above 1 (for example 1.3) would substantially drop the radiation dose without sacricing image quality. Note that breast radiation, although still higher than that measured with dedicated PE pregnancy protocol, is lower than previously reported by dierent
r

Teratogenesis
The static magnetic eld of MRI can potentially cause cell migration, proliferation, and dierentiation within the fetus resulting in teratogenesis. However, multiple studies show no scientic evidence of teratogenesis in humans seen up to 9 years after exposure to MRI in utero.69 In terms of risks of MRI exposure, the ACR does not distinguish between the rst trimester of pregnancy and the second and third trimesters.66,68 As per the ACR White Paper, at any stage during pregnancy, a risk-benet analysis should be performed before MRI. www.thoracicimaging.com |

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Tissue Heating
Exposure to radiofrequency pulses can cause tissue heating, with subsequent heating of fetal stem cells and, as a result, potential teratogenesis. For all MRI examinations, tissue heating associated with MRI exposure is measured in specic absorption rate units (SAR).66 SAR is a measure of the rate at which energy is absorbed by the body when exposed to a radiofrequency electromagnetic eld. It is measured in W/kg, reecting power absorbed per mass of tissue. SAR units for MRI are regulated by the Food and Drug Administration, which currently makes no specic recommendations for pregnant patients.70 SAR is inuenced by a number of parameters such as static magnetic eld strength, ip angle, number of radiofrequency pulses, and spacing between radiofrequency pulses. An increase in the rst 3 parameters and a decrease in the last parameter can all cause an increase in SAR. In addition, radiofrequency refocusing pulses tend to generate more magnetization and thus more heat because the ip 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 refocusing pulses, leading to high SAR, and in some instances approach SAR limits set by the International Commission on Non-Ionizing Radiation Protection.72 It is important to remember, however, that the majority of heating created by MRI is supercial and absorbed by the maternal body with only a fraction reaching the fetus.70 Further, in a study by Hand and colleagues, fetal SAR and fetal temperature were demonstrated to be within international safety limits for MRI procedures compliant with the International Electrotechnical Commission normal mode condition. An international consensus states that MRI of pregnant patients should also be performed with 3.0 T magnets or less to minimize SAR.73 Another method to reduce SAR is to utilize gradient-recalled echo sequences, which have a lower SAR compared with single-shot fast spin-echo sequences.66 Some authors have suggested decreasing the room temperature in the MRI suite to <241C to diminish potential heating eects on the developing fetus.65

Acoustic Damage
By 24 weeks of pregnancy, the fetal ear develops to be able to hear noise.63 The MRI noise level can be as high as 80 to 120 dB, but the maternal body attenuates the noise substantially, by at least 30 dB. This results in <90 dB of noise reaching the fetal ear. It is noteworthy that 90 dB is suggested by the American Academy of Pediatrics as the upper limit beyond which permanent damage to the fetal ear might be expected.74,75 To date, no scientic evidence of acoustic damage in human fetuses has been reported in association with MRI exposure. Most authors, as well as the International Commission on Non-Ionizing Radiation Protection, suggest that MRI evaluation should be limited to the second and third trimesters of pregnancy, especially elective imaging.68,76 In contrast, because of the lack of documented deleterious eects of MRI on the developing fetus, ACR guidelines apply to the entire pregnancy term, with no dierentiation between the rst trimester of pregnancy and the second and third trimesters in terms of risks of MRI exposure.68

passive diusion across the chorionic epithelium in animal studies, it should be assumed to likewise cross the human placenta.67,77 It is ltered through the kidneys and subsequently excreted into the amniotic uid through the urine. On the basis of the animal studies, only 0.01% of the injected gadolinium dose was present in the fetus 4 hours after contrast medium injection, with only traces remaining after 24 hours; however, the actual half-life of the gadolinium in the human fetus is unknown.36 Women with impaired renal function have longer circulation times for contrast medium, so potentially the fetal dose may reach higher levels because of prolonged circulation times in the placenta. Concern is focused on the toxic free gadolinium ion, which can be formed by dissociation of the ion from the chelating agent. Although the stability of the gadolinium-chelate complex is unknown, 1 study showed that even in patients with severely reduced renal function, no free gadolinium ion could be measured in the blood 5 consecutive days after the administration of contrast medium.78 Mu hler et al79 have reported in pregnant mice the redistribution of gadoterate meglumine back to the woman after passing the placenta, with undetectable fetal concentrations after 48 hours. Gadolinium has been shown in animal studies to have teratogenic eects when administered at high and repeated doses.22,68 No human studies have been conducted to assess the teratogenic eect of gadolinium in pregnant women, but there have been no harmful events reported so far in human fetuses exposed to gadolinium-based contrast agents in utero. A series of 26 women who received gadopentetate dimeglumine in the rst trimester of pregnancy and 2 additional series of women who received gadolinium in the second and third trimesters of pregnancy have shown no adverse eect of gadolinium exposure on the fetus.80,81 In 2010, the ACR stated that gadolinium-based contrast agents may be given to a pregnant patient if needed, by joint decision of the radiologist and referring physician only when essential to the diagnosis, when no alternative imaging studies are available, and when delaying the MRI examination until after delivery would be impossible.22,68 IV gadolinium is classied as a category C agent in pregnant patients by the US Food and Drug Administration, meaning that, although animal studies have revealed adverse eects on the fetus at supraclinical doses, there have been no controlled studies in women, and it should only be administered in pregnancy if the potential benet justies the potential risk to the fetus.63 No specic neonatal tests are necessary after delivery, as no adverse eects, teratogenesis, or acoustic damage have been documented in association with the use of gadolinium-based contrast agents for medical imaging.36 Only minimal amounts of gadolinium-based contrast material are excreted through breast milk and absorbed by the infant bowel (0.01% of injected dose). This expected absorbed dose is <0.05% of the IV contrast amount recommended by the American Academy of Pediatrics for neonates undergoing a gadolinium-enhanced MRI study.40 Thus, as per the ACR Contrast Manual 2013, no interruption of lactation is required if IV gadolinium is administered to a nursing patient.40

Administration of IV Gadolinium-based Contrast Agents During Pregnancy and Lactation

Given that intravenously injected gadolinium-based contrast agents have been shown to cross the placenta by

MEDICO-LEGAL ISSUES Risk Management

Despite the widely established role of CT examinations in pregnant patients, and several decades of experience with
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Is CT the best modality for specific question?

Yes Is the patient pregnant?

No Proceed with modality of choice

Yes

No Image acquisition

Clinician -Radiologist discussion

according to ALARA principle

Can the study be postponed?

No Yes

Is protocol adjustment possible?

Is IV iodinated contrast necessary?

Yes

No (rare)

Yes/Regular contrast dose

No

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

Low kVp(<=100) Low mAs(<=100) Oral barium:1-2 cups 15-20 min prior to study Abdominal lead shielding Limited z-axis coverage: 1.CT chest: lung apices - diaphragmatic domes 2.CTPA:2CM above aortic arch-diaphragmatic domes

FIGURE 4. Algorithm 2. Suggested approach to MDCT examination in pregnancy.

MRI in pregnancy, radiologists should be aware that such imaging involves potential medico-legal risk.82 To minimize this potential, certain guidelines for imaging pregnant patients with CT and MRI should be followed. These include: (1) an established process for evaluating pregnant patients in a radiologic facility; (2) a written policy for management of pregnant and lactating women; (3) accessibility of radiologists knowledgeable about MRI/CT exposure eects to patients and referring physicians; and (4) and documentation in the radiology report of all discussions with patients about the risks/benets of a specic CT examination. Four main questions have to be answered by the referring clinician and radiologist when planning CT or MRI during
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pregnancy: (1) Can the information be obtained without CT or MRI examinations? (2) Can the information be obtained without IV contrast administration? (3) Will the information obtained with imaging aect the care of the patient or fetus during the pregnancy? and (4) Can imaging be safely deferred until after pregnancy?

Informed Consent
At our institution, informed consent is obtained for all studies involving ionizing radiation including conventional radiography, computer tomography, and MRI. While obtaining informed consent, the radiologist should explain the need for imaging and the importance of the diagnosis for the www.thoracicimaging.com |

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Is MRI the best modality for specific question?

Yes

No

Is the patient pregnant?

Yes Clinician Radiologist discussion Can the study be postponed?

No Regular MRI study According to accepted standards

No

Yes

Is protocol adjustment possible?

Is IV Gd necessary?

Yes

No

Yes/ Regular Gd dose

No

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

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

patients care as well as a brief explanation of the ordered imaging test. While summarizing the estimated risk to the patient and the fetus, the radiologist has the opportunity to conrm the patients comprehension of the risks and benets as well as alternative options before consenting.43 The emphasis on a low risk of harm to the fetus by CT scanning (compared with the known 15% risk for spontaneous abortion and 1% to 3% risk for major malformation) and no documented risk to the fetus caused by MRI is important. Patient consent is essential before imaging is obtained. Discussion with patients about the risks/benets should be documented in the radiology report, including: (a) need for imaging and the importance of the diagnosis for patients care; (b) brief explanation of the ordered imaging test; (c) summary of the estimated risks to the patient and the fetus; and (d) conrmation of the patients understanding of and consent 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 certain examination to the annual background radiation. For example, annual radiation exposure in the United States is 3.1 mSv/y, so when radiation delivered by a chest radiograph is compared with this dose, it would be equivalent to 0.02 mSv or a BRE of 2.1 days. The substantially higher radiation delivered by chest CTA of 3 to 6 mSv, depending on the protocol, would be equivalent to a BRE of 1 to 2 years.

risks versus benets with the referring clinician. Algorithm 2 (Fig. 4) is designed to help determine whether MDCT is the modality of choice for the female patient with suspected cardiothoracic disease. After the study is completed, the report should include the following: the informed consent discussion that occurred before the study, description of the imaging ndings, radiation dose recording from the report generated by the MDCT scanner, and recommendation to obtain neonatal thyroid function check-up (routinely obtained in all newborns in the United States). Algorithm 3 (Fig. 5) is designed to help determine whether MRI is the modality of choice for the female patient with suspected cardiothoracic disease. After the study is completed, the report should include the following: informed consent discussion, imaging ndings, and whether or not IV gadolinium was administered. If gadolinium was administered, the report should state that no specic neonatal tests are necessary after birth.

SUMMARY
Despite potential adverse implications of cardiothoracic CT and MRI in pregnancy, they remain a crucial part in a variety of potential clinical scenarios during pregnancy. Combined eorts of a referring clinician and radiologist are essential for providing the best practice. When an acute problem is identied by a referring provider and the pregnant patient is referred to imaging with a specic question related to cardiothoracic pathology, it is the radiologists role to decide whether the diagnostic question can be answered with a nonionizing modality such as US or MRI or whether CT is more appropriate. On the basis of feasibility and/or specic questions asked, it is the radiologists role to estimate fetal and maternal risk from a known radiation dose in each specic case or the potential
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PROPOSED PRACTICAL ALGORITHMS FOR MDCT AND MRI SCANNING IN PREGNANT PATIENTS
As stated previously, both MDCT and MRI can be obtained in pregnant patients for the purposes of cardiothoracic imaging if indicated, after careful discussion of

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adverse eects of MRI, as well as to structure the examination without compromising diagnostic accuracy. The most frequent indications such as suspected PE, aortic dissection, and, relatively rarely, trauma or parenchymal pathology should be properly addressed after discussion with both the referring provider and the patient. The best practice for imaging of pregnant or potentially pregnant patients with ionizing radiation is as follows: To maintain a high standard of safety, particularly when imaging potentially pregnant patients, imaging radiation must be applied at levels as low as reasonably achievable (ALARA), whereas the degree of medical benet must counterbalance the well-managed levels of risk. Necessary imaging examination should be performed after clinical workup, and the radiation level should be kept as low as reasonably achievable. The patient should give informed consent before the procedure. Careful approach to MRI during pregnancy with emphasis on minimizing potential acoustic damage and tissue heating is essential despite primarily theoretical potential fetal damage from the procedure. REFERENCES
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