Ailbhe C. O’Neill1 , Pamela J. DiPiro1 and Erica L. Mayer2
(1)
Department of Imaging, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, USA
(2)
Susan F. Smith Center for Women’s Cancers, Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, USA
Ailbhe C. O’Neill
Email: aoneill9@partners.org
Pamela J. DiPiro
Email: pdipiro@partners.org
Erica L. Mayer (Corresponding author)
Email: Erica_Mayer@dfci.harvard.edu
Keywords
Pregnancy-associated cancerBreast cancerImaging
Introduction
Imaging and image-guided biopsies play an important role in the diagnosis, staging, and management of cancer, and guidelines exist for the radiologic evaluations of patients diagnosed with a variety of malignancies [1]. Pregnancy-associated cancers are increasing in frequency, and due to possible risks to the developing fetus, practice guidelines may not be applicable to the situation of pregnancy [2]. Therefore, given the need to balance the clinical needs of the mother with any potential adverse effects to the child, clinical imaging paradigms for this patient population may deviate from established guidelines and may be highly individualized. This chapter will provide an overview of specific imaging modalities that can be considered in pregnant cancer patients, as well as imaging strategies for specific anatomic locations.
Radiation Risks from Imaging
When imaging a pregnant patient, especially when considering the use of ionizing radiation, one must carefully weigh the benefits of the modality versus the potential risks to the fetus. Ionizing radiation exposure may occur with common imaging modalities, including X-rays and computed tomography (CT). There are two main categories of risk from ionizing radiation – deterministic and stochastic. Deterministic effects involve damage to multiple cells and do not occur below certain threshold doses; their severity increases with increased radiation dose (Table 2.1). Deterministic effects in a fetus include malformations, growth retardation, mental retardation, and death. The International Committee on Radiological Protection concluded in a 2007 report that no deterministic effects of practical significance would be expected to occur below a dose of 100 mGy (milligray = a measure of the absorbed radiation dose), which is above the normal radiation exposure of a single diagnostic radiology or nuclear medicine study [3]. Deterministic effects, if they occur, are more significant in the earlier stages of pregnancy. During first trimester organogenesis, exposure above threshold values may lead to increased risk of deterministic effects, with less risk of toxicity in subsequent trimesters [4]. Stochastic effects occur due to damage of a single cell and can lead to carcinogenesis. Unlike deterministic effects, there is no threshold dose, though the risk of damage increases with escalating radiation dose. An additional risk of carcinogenesis of 1 in 10,000 is quoted with fetal radiation doses of up to 1 mGy [5]. The American College of Radiologists (ACR) describes the carcinogenesis risk at a dose of 10 mGy as increasing background rates of malignancy from 0.2–0.3 % to about 0.3–0.7 % [4]. Increased awareness of radiation doses, as well as improvements in imaging technology (including automatic exposure control software and iterative reconstruction algorithms), may contribute to reductions in the risk of both maternal and fetal radiation exposure [6].
Table 2.1
ACR summary of suspected in utero-induced deterministic effects [4]
|
Menstrual or gestational age (days) |
Conception age (days) |
<50 mGy |
50–100 mGy |
>100 mGy |
|
0–2 weeks (0–14) |
Before conception |
None |
None |
None |
|
3rd and 4th weeks (15–28) |
1st and 2nd weeks (1–14) |
None |
Probably none |
Possible spontaneous abortion |
|
5th to 10th week (29–70) |
3rd to 8th week (15–56) |
None |
Potential effects are scientifically uncertain and probably too subtle to detect clinically |
Possible malformation increasing in likelihood as dose increases |
|
11th to 17th week (71–119) |
9th to 15th week (57–105) |
None |
Potential effects are scientifically uncertain and probably too subtle to detect clinically |
Risk of diminished IQ or of mental retardation increasing in frequency and severity with increasing dose |
|
18th to 27th week (120–189) |
16th to 25th week (106–175) |
None |
None |
IQ deficits not detectable at diagnostic doses |
|
>27th week (>189) |
>25 week (>175) |
None |
None |
None applicable to diagnostic medicine |
Specific Imaging Modalities
Radiography involves the use of ionizing radiation with the associated risks as discussed previously. However, if the pelvis is outside the field of view, the fetal radiation dose is minimal. For example, the fetal radiation dose from a chest X-ray is estimated to be 0.002 mGy and from an extremity radiograph <0.001 mGy; these are both far less than the background radiation exposure from a transatlantic flight [7].
CT is associated with higher levels of radiation exposure, but again the dose to the fetus varies, with higher levels of radiation when the field of view is closer to the uterus. CT of the head, neck, and extremities can generally be safely performed during pregnancy regardless of the trimester; however, consideration of imaging modalities without radiation can be considered if appropriate for the specific anatomic location [8]. Shielding of the abdominopelvic region with a lead apron during a CT scan may reduce radiation dose from the minimal amount of external scattered radiation that comes from the exposed tissue or imaging equipment, however will not decrease internal scattered radiation [9].
Ultrasound (US) may be safely used during pregnancy with no adverse events to a fetus documented to date. Ultrasound is useful for a spectrum of focused clinical assessments, including in the evaluation of a palpable breast mass, the evaluation of adnexal lesions, and the assessment of the presence of hepatic metastases. There are limitations with obesity, operator dependence, and the presence of bowel gas, with decreased sensitivity in later pregnancy due to increase in abdominal girth and mass effect from the gravid uterus.
Magnetic resonance imaging (MRI) is an imaging modality that does not use ionizing radiation. No adverse effects to the fetus have been conclusively documented with MRI imaging exposure to date during any stage of pregnancy [10]. The primary safety concerns are the effects of noise on the fetus and the possible heating effects from radiofrequency pulses during an MRI [11]. Similar to the use of CT in pregnancy, the ACR recommends that before a pregnant patient undergoes MRI, the risks versus benefits in performing the examination during pregnancy should be weighed. MRI should be utilized only if (1) the information cannot be acquired by alternate nonionizing methods such as ultrasound, (2) the examination cannot wait until the patient is no longer pregnant, or (3) the imaging could potentially impact care for the patient or fetus during pregnancy [10].
Positron emission tomography–computed tomography (PET-CT) combines functional imaging provided by PET with cross-sectional anatomic information from CT. Due to its radiation dose, PET-CT is not recommended for oncology staging during pregnancy. The most common radiopharmaceutical used in PET imaging is fluoro-2-deoxy-D-glucose (F18-FDG), a radiolabeled glucose analog. PET-CT is commonly used in oncology imaging for staging disease and also for assessing response to therapy. However, PET-CT contributes ionizing radiation from both the injected radionuclide marker and the CT, leading to a potentially high fetal radiation dose; therefore, PET-CT is not recommended during pregnancy. In the ACR parameter guide for performing PET-CT in oncologic imaging, when appropriate, a pregnancy test to exclude pregnancy is necessary prior to performing a PET-CT [12]. Reducing the amount of radionuclide injected and changing CT parameters to impart less radiation may decrease the dose from PET-CT. There have been a few cases in the literature where PET-CT was used in pregnancy, with reported fetal doses as low as 1.1 mGy and as high as 21.8 mGy [13, 14].
Intravenous Contrast Administration in Pregnancy
Iodinated Contrast
Studies evaluating the safety of low osmolar contrast media (LOCM), which is the current type of iodinated intravenous CT contrast administered, are limited, and the sequelae of contrast exposure on fetal development are largely unknown. Iodinated CT contrast media given as part of a diagnostic CT has been shown to cross the placenta and enter the fetus [15]. There have been historic reports of hypothyroidism in infants, following administration of fat-soluble contrast during pregnancy as part of amniofetography, used to detect congenital malformations. However, fat-soluble contrast is no longer used in diagnostic imaging [16]. No mutagenic or teratogenic effects have been demonstrated during in vivo animal testing with LOCM [17]. No cases of neonatal hypothyroidism or other adverse effects have been reported from maternal administration of water-soluble contrast agents to date [18]. Due to insufficient evidence regarding the safety of LOCM to the fetus, it is recommended that prior to use in a pregnant patient, the potential added risks of contrast media should be considered and the administration of intravenous contrast be deemed essential for the planned study. In addition, informed consent potentially should be obtained from the mother, and consideration should be given to screening newborns for hypothyroidism, a paradigm that is already standard pediatric practice in North America and Europe [19].
Gadolinium Contrast
No adverse effects to the fetus have been reported when the clinically recommended doses of gadolinium-based contrast agents have been given to pregnant women [20]. However, the US Food and Drug Administration has classified gadolinium as category C, indicating that animal studies have revealed adverse effects on the fetus. Although there have been no controlled studies in pregnant women, potential benefits of using gadolinium may warrant its use despite potential risks, depending on the clinical situation. Gadolinium-based agents have been shown to cross the placenta, and the possibility of gadolinium in the amniotic fluid dissociating into toxic-free gadolinium ions cannot be excluded [19]. The ACR recommends using gadolinium only when the potential benefit to the patient or fetus outweighs the possible risks and should be reviewed on a case-by-case basis. Both the patient and the referring physician should be counseled as to the potential risks and benefits of gadolinium contrast prior to its administration [19].
Breast Imaging During Pregnancy
Ultrasound (US) is the primary imaging technique used in a pregnant patient presenting with a palpable breast mass. Ultrasound does not involve ionizing radiation and is highly sensitive and specific in imaging pregnancy-associated breast cancer [21, 22]. In locally advanced pregnancy-associated breast cancers, neoadjuvant chemotherapy may be indicated; in this scenario, ultrasound can be utilized to assess response [23]. Ultrasound can be used to guide core needle biopsy of any suspicious masses and to evaluate for axillary nodal disease.
Mammography is less sensitive during pregnancy due to increased parenchymal density in the breast secondary to hormonal effects. However, mammography can be useful in assessing suspicious microcalcifications that might not be visible sonographically in a patient diagnosed with breast cancer and can help determine the disease extent, as well as evaluate the contralateral breast (Fig. 2.1). Mammography can be performed safely during pregnancy with minimal fetal radiation exposure, with the dose to the uterus estimated as less than 0.03 mGy [24]. Lead apron shielding can be offered, but the majority of radiation to the uterus will be scatter radiation and lead shielding will have limited efficacy. Contrast-enhanced MRI is not recommended during pregnancy due to the unknown effects of gadolinium on the fetus.
Fig. 2.1
A 32-year-old at 20 weeks gestation palpated a nodule in the right lower breast. (a) US of the right breast demonstrates a 30 × 10 mm hypoechoic mass (arrow). Biopsy consistent with invasive ductal carcinoma. ER negative and PR and HER2-neu positive. (b) Right MLO spot magnification demonstrates clip in the biopsy-proven carcinoma (arrowhead) and a 5 mm separate cluster of pleomorphic calcification posteriorly (arrow). Biopsy of calcification consistent with DCIS
Image-guided biopsy is most often performed with US due to lack of ionizing radiation, though stereotactic biopsy and wire localization can be performed safely in pregnancy for lesions not visible sonographically. Core biopsy in pregnancy has a slightly increased risk of bleeding and infection due to increased breast vascularity. There is also a very small risk of a milk fistula, though there is more concern for this complication with open surgical procedures [25–27]. Subcutaneous anesthesia with lidocaine can be safely administered and does not have any adverse effect on the fetus.
Osseous Imaging During Pregnancy
Radiography and CT of the extremities, with the exception of the hip and pelvis, have little to no exposure to the fetus if the beam is properly collimated. Therefore, pregnancy status should not alter the decision to perform these examinations [4]. MRI of an extremity can be performed for assessing a primary bone tumor or a soft tissue tumor. In the evaluation of diffuse osseous metastases, whole body MRI without contrast can be safely performed [28].
Another method of assessing bone metastases is with bone scintigraphy (nuclear medicine bone scan), which is performed using technetium-99m, a short-lived radionuclide with a half-life of 6 h. An average dose in early pregnancy may have a fetal exposure of 4.7 mGy, decreasing to 1.8 mGy by 9 months [29]. Given the potential fetal dose, bone scans are not commonly performed in pregnancy though there are methods to further reduce the radiation dose including decreasing the amount of activity injected and encouraging maternal hydration and frequent voiding, as this radionuclide is excreted by the kidneys and accumulates in the bladder [30].
Head and Neck Imaging During Pregnancy
In a patient with a palpable neck mass, ultrasound is the preferred initial imaging modality and can also be used to guide biopsy. CT or MRI of the neck may also be performed for evaluation of a neck mass or lymphadenopathy, with minimal radiation or no radiation exposure to the fetus, respectively. CT of the neck has fetal radiation doses quoted of ≤1.0 mGy [4, 29, 31].
Ultrasound of both the thyroid gland and cervical lymph nodes is the preferred imaging modality for evaluation of a thyroid nodule. There are no definite features of thyroid malignancy; however, suspicious findings include a solid rather than cystic appearance, calcifications, irregular margins, and the presence of lymphadenopathy [32]. The typical size criterion for fine needle aspiration is usually >10 mm, as diagnosis of subcentimeter thyroid cancers does not improve life expectancy [33].
In imaging suspected central nervous system tumors, MRI of the brain is superior to CT for characterizing tumors, especially when using diffusion weighting and intravenous contrast (contrast allows for added features of perfusion and spectroscopy imaging). As MRI contrast is not recommended during pregnancy, characterization from a non-contrast MRI may be limited to diffusion weighting as well as T1 and T2 characteristics. CT of the brain is most useful in urgent cases of raised intracranial pressure and in excluding hemorrhage; there is minimal associated radiation exposure to the fetus [4, 7].
Thoracic Imaging During Pregnancy
Thoracic imaging in pregnancy may be performed in the evaluation of mediastinal masses and pulmonary masses or, more commonly, for assessment of metastatic disease. A chest radiograph has a negligible fetal dose, with estimates ranging from 0.0005 to 0.002 mGy [7, 29]. Chest CT is more sensitive in evaluating mediastinal structures, lymphadenopathy, and pulmonary parenchyma. Though fetal doses are slightly higher than with radiography, they remain relatively low, ranging between 0.01 and 0.66 mGy, when performed with pelvic shielding [29]. MRI of the chest has excellent contrast and spatial resolution, without radiation to the fetus or to the maternal breast tissue. While MRI is limited compared to CT for evaluating the pulmonary parenchyma, it has value in assessing lesions involving the mediastinum (Fig. 2.3), chest wall, pleura, lymph nodes, and spine, even without the use of intravenous contrast [34]. CT-guided biopsy of mediastinal and pulmonary pathology can be performed for diagnosis and has been shown to be accurate and technically feasible at low doses [35, 36]. When thoracic biopsies are performed in pregnancy, both tube voltage and tube current may be decreased to reduce the radiation dose, and the number of fluoroscopic images can also be limited to further reduce radiation.
The incidence of pulmonary embolism is higher both in pregnancy and in oncology patients compared to the general population. There is increased risk especially in patients with CNS tumors and pancreatic, upper GI, and lung cancers [37, 38]. For suspected pulmonary embolus, CT pulmonary angiogram (CTPA) or ventilation–perfusion scintigraphy (VQ) can be performed. The fetal radiation dose from both studies is low, with VQ conferring a fetal dose of approximately 0.1–0.5 mGy and CTPA 0.01–0.66 mGy [29]. There are conflicting data in the literature regarding the diagnostic accuracy of one test over the other, though one meta-analysis has shown CTPA to be better than VQ in an oncology population. CTPA also has the advantage of assessing other thoracic pathology, such as pulmonary metastases and thoracic nodal disease [39].
Abdominal and Pelvic Imaging During Pregnancy
Abdominopelvic imaging in pregnancy may be performed for evaluation of a primary malignancy, for assessment of nodal disease, or for evaluation of metastatic disease (including hepatic metastases). The use of CT for evaluation of the abdomen and pelvis during pregnancy is associated with high fetal doses of radiation. Estimated fetal dose for an abdominal CT ranges between 1.3 and 25 mGy and for a pelvic CT from 10 to 50 mGy [29]. Therefore, CT imaging of the abdomen and pelvis in pregnancy is not commonly utilized. MRI or US is preferred to evaluate the abdomen and pelvis (Fig. 2.2), particularly in evaluation for hepatic metastatic disease. Percutaneous biopsy of hepatic lesions may be performed with US or MRI guidance, if required to definitively stage cancer.
Fig. 2.2
A 35-year-old woman, 5 weeks pregnant with an incidental 7 cm pelvic wall mass at initial obstetric US. (a) Axial T2-weighted MRI performed at 5 weeks, demonstrating an early intrauterine pregnancy with a gestational sac (arrow). There is a low intensity mass arising from the left rectus abdominis muscles (curved arrow). (b) There is a 15 G introducer needle present in the abdominal wall mass (curved arrow). The biopsy result demonstrated desmoplastic fibroblastoma
Melanoma staging in pregnancy should initially involve the primary tumor site and local-draining lymph nodes. However, if metastatic, melanoma may spread hematogenously to the lungs, liver, adrenal glands, and small bowel. Less commonly, metastatic melanoma has been reported in the spleen, pancreas, kidneys, and gallbladder [40]. Whole body MRI is useful in the evaluation of melanoma, as well as lymphoma occurring in pregnancy (Fig. 2.3). Whole body MRI has shown higher sensitivity than PET-CT in detecting liver, splenic, and bony metastases, though is less sensitive for lung and nodal metastases [41].
Fig. 2.3
Whole body MRI performed in a 36-year-old patient with Hodgkin’s lymphoma at 23 weeks gestation. (a) Coronal T2-weighted image shows an anterior mediastinal mass (arrow). The fetus is visible in the lower abdomen inferior to the liver and stomach. (b) Axial T2-weighted image demonstrates bilateral internal mammary lymphadenopathy measuring 3.3 × 2.5 cm on the right and 1.2 × 1.0 cm on the left (arrows). The anterior mediastinal mass is also again demonstrated (curved arrow). (c) A sagittal STIR image in the same patient does not demonstrate pathology but shows how well delineated the cervical stroma is on MRI (arrows)
Cervical cancer is the most common malignancy occurring in pregnancy. Cervical cancer diagnosed in pregnancy tends to be detected at earlier stages, possibly due to the more frequent cervical examinations as part of prenatal care [42, 43]. Cervical cancer tends to spread by local extension, and staging of cervical cancer is optimally performed with pelvic MRI. This modality can evaluate the size of the primary tumor in three planes, as well as assess for parametrial or vaginal invasion, lymphadenopathy, and potential secondary complications, such as hydronephrosis, if there is bladder or ureteric invasion [44].
Conclusions
Radiologic imaging plays a crucial role in the diagnosis, staging, and monitoring of most malignancies. As with much of the clinical management of pregnant patients with cancer, the potential risks of imaging to the fetus, including exposure to ionizing radiation or intravenous contrast, must be balanced against the need for accurate diagnostic evaluation and effective treatment of the mother. Alternative imaging strategies that present fewer risks can be considered, such as MRI and US. A proposed general strategy for radiologic evaluation of the pregnant patient is presented in Fig. 2.4. However, optimal selection of imaging in pregnant patients with cancer may be best achieved through individualized multidisciplinary consultation with radiology colleagues.
Fig. 2.4
Possible algorithm for assessment of common cancers occurring during pregnancy (*Abdominal shielding can be placed during CT)
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