key: cord-0707265-ok63nf7r
authors: Nair, Anirudh Venugopalan; Ramanathan, Subramaniyan; Venugopalan, Prasanna
title: Chest imaging in pregnant patients with COVID-19: Recommendations, justification, and optimization
date: 2022-03-07
journal: Acta Radiol Open
DOI: 10.1177/20584601221077394
sha: 599c1c144bceec92ffa8eb020718f266cefa4004
doc_id: 707265
cord_uid: ok63nf7r

Evaluation of COVID-19 related complication is challenging in pregnancy, due to concerns about ionizing radiation risk to mother and the fetus. Although there are instances when diagnostic imaging is clinically warranted for COVID-19 evaluation despite the minimal risks of radiation exposure, often there are concerns raised by the patients and sometimes by the attending physicians. This article reviews the current recommendations on indications of chest imaging in pregnant patients with COVID-19, the dose optimization strategies, and the risks related to imaging exposure during pregnancy. In clinical practice, these imaging strategies are key in addressing the complex obstetrical complications associated with COVID-19 pneumonia.

Corona virus disease of 2019 (COVID-19) is a viral disease caused by severe acute respiratory syndrome-Coronavirus-2 (SARS-COV-2). 1 The disease first originated in the Hubei province of China, later sweeping through the continents and evolving to become a global pandemic. The detailed insights into the disease manifestations, heterogeneity, and physiological behavior of the virus, including pulmonary and extra pulmonary manifestations of COVID-19, are being better understood with new research studies and clinical experiences.

There is a relative higher risk of COVID-19 infection during the time of pregnancy, 2 thereby creating constraints and clinical dilemma on proceeding with the use of an appropriate radiological investigation. 3 The clinical pathway for evaluating COVID-19 and its associated complications in pregnancy is highly variable, depending on the institutional preferences, availability of resources, practice pattern of referring clinicians, and interpreting radiologist.

Imaging studies which involve radiation exposure like chest X-ray and chest CT scan are indispensable in the management of COVID-19 patients. Radiologists around the globe should be familiar with merits and limitations of various chest imaging modalities in evaluation of COVID-19 pneumonia and its complications during pregnancy. In this review, we aim to summarize the current recommendations on indications of chest imaging in pregnant COVID-19 patients including chest X-ray, CT chest, CT pulmonary angiogram, chest ultrasound, and cardiac MRI, with emphasis on imaging risks and dose optimization strategies.

Epidemiology Recent surveillance data from the Centers for Disease Control and Prevention (CDC), in the women aged between 15 to 44 years, showed pregnant women were more likely to be hospitalized, requiring an intensive care unit (ICU) care or ventilation. 4 However, large cohort study from the United Kingdom observed that the rates of ICU admission or maternal mortality in severe disease were similar to non-pregnant women in the reproductive age group. 5 Pregnant women are more susceptible to infections owing to the immunity changes during the time of pregnancy. 6 There are guidelines from the CDC, the American College of Obstetricians and Gynaecologists (ACOG), the Society for Fetal-Medicine (SMFM), and the Royal College of Obstetrics and Gynaecologists (RCOG) related to the management of COVID-19 in pregnancy. [7] [8] [9] [10] [11] [12] [13] Complications related to COVID-19 in pregnancy Chest complications related to COVID-19 in general include a spectrum of findings related to airway, alveolar, vascular, and cardiac involvement. Recent studies have shown an increased incidence of complications in pregnancy due to COVID-19, especially preeclampsia, eclampsia, HELLP syndrome, and increased risk for maternal mortality. 14 Furthermore, the complications are augmented with pre-existing or underlying comorbidities like obesity, diabetes mellitus, systemic hypertension, and cardiac diseases. 15 Diagnosis and clinical severity classification in pregnancy with COVID-19

RT-PCR is considered the reference standard for diagnosis of COVID-19 in pregnancy. 16 Prior studies have reported the RT-PCR positive rates in asymptomatic pregnant women between 50 and 89%, [17] [18] [19] while false negative rates varied from 17 to 63%. 20 The categorization of pregnant patients with COVID-19 based on the severity of illness is similar to other adult patients with COVID-19. They are categorized into asymptomatic, mild, moderate, severe or, critical 21 (Table 1) . There are instances when the initial clinical presentation related to an upper or lower respiratory tract infection related to bacterial or other non-COVID-19 viral infection may raise the suspicion for COVID-19, 22 the imaging in such a scenario may be tailored according to the disease severity, clinical suspicion, and the trimester.

(1) Utility of chest X-ray

Recommendations. The position statement by Fleischner society and ACOG recommends that routine imaging should not be used in asymptomatic or mild illness severity patients and also in intubated stable patients with COVID-19. 8, 23 The ACOG and SMFM recommends chest X-ray in patients with moderate clinical risk based on illness severity and underlying comorbidities in all trimesters, 10 while the RCOG recommends that the radiographic investigations such as chest radiograph and CT chest should be performed in pregnant patient with COVID-19 as for the non-pregnant adult and chest imaging should be performed when indicated and should not be delayed over concerns of fetal radiation exposure, as the maternal well-being is paramount. 13 In practice, chest X-ray should not be used for arriving at a diagnosis of COVID-19 in pregnant patients, instead it is recommended to rely on RT-PCR confirmation of the disease status. Follow-up chest Xray should be judiciously considered only when there is further clinical deterioration and situations that would impact patient care. Optimization strategies in chest x-ray. In routine chest X-ray, the pelvis or gravid uterus is generally not exposed to direct X-ray beam, and can be safely performed with optimization strategies. 24 However, in third trimester due to gravid uterus reaching the upper abdomen, parts of fetus can get exposed to a direct X-ray beam, and this needs to be taken care of using an appropriate technique. Dose optimization strategies to reduce the maternal and fetal dose include collimating on the lungs and avoiding upper abdomen as much as possible with an abdominal lead shield 25 placed over the abdomen or back depending on Antero-Posterior (AP) or Postero-Anterior (PA) radiographs, respectively, and also to limit the chest radiograph to frontal view and avoiding a lateral radiograph. 24 (2) Utility of CT Pattern of lung involvement in COVID-19 includes ground glass opacities (GGO), GGO with consolidation, and only consolidation are similar to non-pregnant patients. [26] [27] [28] [29] However, the imaging findings have close overlap with other viral lung infections like influenza virus, MERS-COV, SARS, H1N1, H5N1, and H7N9. 26, 27 Recommendations. The position statement by the American College of radiology (ACR) 30 recommends against the use of CT scan as a first-line investigation or for follow-up to assess progression of COVID-19. The Fleischner Society advocates CT scan only in patients with functional impairment, hypoxemia, or after recovery from infection. The SMFM, ACOG, and RCOG recommend that CT chest should not be withheld in pregnant patients when clinically indicated. 10, 13 Thus, in pregnant patients the CTchest should be undertaken only in instances where there is functional impairment, hypoxemia, or both. Unlike other lower respiratory tract viral infections, respiratory decompensation in COVID-19 pneumonia happens later in the disease. 31 Hypoxemia related to acute respiratory failure in pregnancy manifests with partial pressure of oxygen (PaO2) <60 mmHg on room air, that corresponds to oxygen saturation (SpO2) <90 mmhg on room air or sea level. 32, 33 Optimization and dose reduction strategies in CT. Although CT chest do not directly expose the pelvis or gravid uterus to ionizing radiation and can be performed in pregnancy after justification of the benefits, the radiologists should be aware of the dose reduction descriptors 34 and strategies while performing a CT chest or CT pulmonary angiogram for pregnant patients with COVID-19 (Tables 2 and 3 ). The most common strategies include reducing mA, kVp, Z-axis of acquisition, and iterative reconstruction algorithms. 21, [35] [36] [37] Reduction in exposure parameters to a certain level is possible with trade-off in image quality without altering the diagnostic accuracy of images. Dose reduction strategies unrelated to CT imaging parameters include reducing the length of scan with strict collimation from the lung apices to diaphragm to minimize maternal and fetal dose and use of lead shield coverage over the maternal abdomen and bismuth breast shield to maternal breasts. Although, the lead shielding to wrap the abdomen during the CT chest scan may reassure the patient of the safety of fetus, the fetal dose received due to CT chest is primarily related to internal scatter, which is not altered by abdominal shielding. 38 The use of breast shielding is controversial as it can degrade the image quality due to increased noise and make the automatic exposure control unpredictable. However considering the increased radiosensitivity of breast parenchyma in pregnancy, breast shielding can be selectively used with proper training. 39, 40 In such a scenario, the dose reduction strategies implemented in pregnant patients should be utilized in nonpregnant young females undergoing COVID-19 imaging as well.

Overall, the dose reduction strategies should be tailored depending on the resources available with the institution, and the focus should be on implementing a low dose or ultra-low dose strategies for CT imaging in pregnant patients with COVID-19 and to bring down the effective dose below 3 mSv. 41 

The International Society of Ultrasound in Obstetrics and Gynecology (ISUOG) recommends using an ultrasound for lung examinations in pregnant patients with COVID-19 as it has the advantage of being radiation free and can be performed at the same time along with obstetric ultrasound which in turn saves time and improves the clinical workflow. Also it can be considered as an alternate when chest radiograph or CT scan is not available. 42 On ultrasound, the normal horizontal "A-lines" (A-lines refers to horizontal echogenic reverberation artefacts that occur in normal lungs, beneath the pleural line at multiples of distance between the ultrasound probe and visceral-parietal pleural interface) are replaced by abnormal "B-Lines" when there is early loss of aeration but not completely consolidated (B-Lines refers to artefact in ultrasound caused as a result of loss of aeration in alveolar-interstitial space). While a consolidation results in absence of A-and B-lines, with a hyperechoic "white lungs".

Pulmonary embolism is reported to occur commonly in patients with COVID-19 with a reported incidence ranging from 0.7-57%, more often associated with severe disease. 43 Pregnancy is associated with a five-fold increased risk for developing pulmonary embolism, due to decreased fibrinolysis, hypercoagulability status, venous stasis, and prolonged bed rest. Pulmonary embolism is also a leading cause of maternal death during pregnancy, and the diagnosis during pregnancy has significant implications in planning of delivery and anticoagulation therapy. 44, 45 In planning an imaging for COVID-19 to rule out pulmonary embolism, all patients should have been thoroughly evaluated on the pretest probability of pulmonary embolism using Pulmonary embolism rule out criteria, 46 Wells score, 47 Geneva score, 48 and D-Dimer when indicated. The role of D-dimer assay is limited in pregnant patients as the value can arise above the reference levels as the pregnancy progresses. 49 However, normal D-dimer levels have a high negative predictive value in ruling out pulmonary embolism.

Diagnostic imaging with CT pulmonary angiography is considered a clinically warranted investigation in pregnant patients suspected of pulmonary embolism with COVID-19. 13 However, the initial workup should focus on non-ionizing imaging techniques like lower extremity color Doppler ultrasound. Although the prevalence of lower limb deep vein thrombosis with clinically suspected pulmonary embolism in COVID-19 is uncertain, the advantage of getting a positive deep vein thrombosis on duplex ultrasound is considered sufficient to justify the use of anticoagulation therapy, thereby eliminating the need for further CT pulmonary angiography. 50 If the initial tests are non-diagnostic, CT pulmonary angiography should be performed as a second line investigation. Figure 1 summarizes a practical diagnostic algorithm for evaluating a pregnant patient with suspected pulmonary embolism in COVID-19. 51 In a setting of COVID-19, the CT pulmonary angiography is preferred over V/Q scintigraphy as it can be used to assess the severity of lung changes for COVID-19 as well.

If there is a positive pulmonary embolism, deep vein thrombosis, or when there is maternal hypoxemia, an obstetric ultrasound for fetal growth, amniotic fluid, and color Doppler imaging should be performed when necessary to assess the extent of fetal hypoxemia. 52

The risks related to iodinated contrast material include the possibility of nephrotoxicity and allergic reactions, with similar relative risks for pregnant and general population. The contrast should not be administered when there is prior major allergic reaction to iodinated contrast material or an underlying impaired renal function. Although, the iodinated contrast crosses the placenta to reach the fetus, there are no reported risks for the fetus. There is a theoretical risk of contrast-induced thyroid dysfunction and hence thyroid function screening should be performed in neonates although there is no convincing evidence to support the same. 53, 54 The use of gadolinium should be restricted in pregnancy as few studies have shown association between gadolinium exposure in utero to still births and neonatal deaths. The US Food and Drug Administration (FDA) has categorized gadolinium as pregnancy class 3 drug. 55 Evaluation of myocarditis in pregnancy with COVID-19

There is evidence of varying manifestation of myocardial injury associated with ongoing or recently recovered COVID-19 patients, with myocarditis being the most common pattern (in 40% cases) while other complications include myocardial ischemia, right ventricular strain, cardiac thromboembolism etc. 56 Few studies have indicated that the mapping abnormalities and cardiac involvement can be picked up early in the disease with cardiac MRI. 57 Cardiac MRI has shown to be a safe imaging in pregnancy with no risk to the mother. Theoretical concerns of teratogenesis, acoustic damage, and tissue heating have not been sufficiently proven in humans. Moreover in cardiac MRI, field of view is away from the fetus, thereby further reducing the potential harm. 58 There is no different risk in relation to different trimesters as per the American College of Radiology (ACR). 59 The information related to utility of cardiac MRI in pregnant patients with COVID-19 is limited, and with the absence of specific recommendations, the use of cardiac MRI can be considered in pregnancy on a case-to-case basis, and also on the resource availability.

Evaluation of fetal hypoxemia due to maternal pulmonary compromise Hypoxemia due to maternal respiratory failure in COVID-19 leading to poor oxygenation to placenta and fetus can result in fetal distress. 60, 61 Although the emerging evidence suggests vertical transmission is probable, the significance of the same to the neonate is yet to be ascertained. There are emerging data that indicate that this viral infection causes inflammation, villitis, and arteriopathy in placenta. 62, 63 Fetal distress and preterm pregnancy are common obstetrical complications of COVID-19. 64 Assessment for acute placental insufficiency and fetal hypoxia can be easily assessed with obstetric Doppler ultrasound. 65, 66 The placental and fetal consequences of COVID-19 including the utility of functional MRI in fetal hypoxemia related to COVID-19 remain to be explored.

During the time of pregnancy, the permitted radiation exposure limits are up to 50mGy. The absorbed dose of radiation in a fetus whose mother undergoes chest X-ray and CT scan is 0.002mGy and 0.2mGy, respectively. 43, 67 Although the data on the fetal risks from radiation is widely variable in the literature, it is generally agreed that at doses less than 50 mGy, there is no evidence of an increased risk of fetal malformations, developmental delay, or loss of pregnancy (Table 4 ). There is reported small increased risk of childhood cancer, 1 in 1500 to 2000 versus the 1 in 3000 background rate. [68] [69] [70] In this context it is important to note that combined exposure to few chest 

Informed consent and patient counseling are important to alleviate the anxiety of patients, while undergoing imaging modalities with radiation exposure like the chest X-ray or CT scan. The attending physician should convey the outweighed benefits of doing an imaging to assess the disease status or to evaluate the complications of COVID-19, as opposed to the risk on the fetus leading to congenital anomalies, birth defects, and miscarriage although negligible for the radiation dose received by the patient. The attending physician and the radiologist should confirm the patients understanding of the estimated risk to mother and fetus. In practice, patient can be explained about the imaging-related radiation exposure by comparing it with background population risk which is approximately 4%, 10%, 10%, and 20% for malformations, genetic diseases, growth retardation, and pregnancy loss, respectively. 71

Chest radiograph and CT examinations for COVID-19 evaluation deliver minimal radiation dose to the mother and fetus, and rarely exceed the permissible limit of 50mGy. Although this knowledge should reassure pregnant women and attending physician on the greater benefits of undergoing an imaging for COVID-19 evaluation, over the minimal radiation risks, the management strategy should focus on keeping the radiation exposure to both mother and fetus as low as reasonably achievable according to ALARA principles. Radiologists should be aware of the lack of understanding about the radiation risk among the nonradiologist physician who would be requesting an imaging during the care of a pregnant COVID-19 patient, and it's the responsibility of radiologist to counsel the treating physician with regard to various options available for chest imaging including radiation-free modalities like chest USG and cardiac MRI when appropriate for evaluation of COVID-19 related chest complications in pregnancy and to improve patient care.

Article concept, design, manuscript drafting/editing/revision for important intellectual content and Literature research all authors. Final version of manuscript is approved by all authors.

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The publication of this article was funded by the Qatar National Library.

Informed consent was waived by IRB (Institutional Review Board) for this review article.

Anirudh Venugopalan Nair  https://orcid.org/0000-0001-7662-7668 Subramaniyan Ramanathan  https://orcid.org/0000-0002-4317-2414 

Diagnostic accuracy and interobserver agreement with the CO-RADS lexicon for CT chest reporting in COVID-19

What are the risks of COVID-19 infection in pregnant women?

Imaging in pregnant patients: examination appropriateness

Characteristics of Women of Reproductive Age with Laboratory-Confirmed SARS-CoV-2 Infection by Pregnancy Status -United States

Characteristics and outcomes of pregnant women admitted to hospital with confirmed SARS-CoV-2 infection in UK: national population based cohort study

Inflammation and pregnancy: the role of the immune system at the implantation site

COVID-19 Treatment Guidelines

COVID-19) | ACOG

Public health agency of sweden's brief report: pregnant and postpartum women with severe acute respiratory syndrome coronavirus 2 infection in intensive care in sweden

COVID-19) and pregnancy: what obstetricians need to know

Considerations for Inpatient Obstetric Healthcare Settings | CDC

COVID-19) and Pregnancy: What Maternal-Fetal Medicine Subspecialists Need to Know

COVID-19) infection in pregnancy information for healthcare professionals

Maternal and neonatal morbidity and mortality among pregnant women with and without COVID-19 infection

Clinical findings and disease severity in hospitalized pregnant women with coronavirus disease 2019 (COVID-19)

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) universal screening in gravids during labor and delivery

Universal screening for SARS-CoV-2 in women admitted for delivery

Universal screening for SARS-CoV-2 before labor admission during Covid-19 pandemic in Madrid

Pregnancy and postpartum outcomes in a universally tested population for SARS-CoV-2 in new york city: a prospective cohort study

Falsenegative testing for severe acute respiratory syndrome coronavirus 2: consideration in obstetrical care

Clinical Spectrum | COVID-19 Treatment Guidelines

The diagnosis of pneumonia in a pregnant woman with coronavirus disease 2019 using maternal lung ultrasound

The role of chest imaging in patient management during the COVID-19 pandemic: a multinational consensus statement from the Fleischner Society

PRACTICE PARAMETER 1 Pregnant or Potentially Pregnant Patients

Proposed imaging guidelines for pregnant women suspected of having COVID

CT imaging features of 2019 novel coronavirus (2019-NCoV)

Emerging 2019 novel coronavirus (2019-NCoV) pneumonia

Radiological findings from 81 patients with COVID-19 pneumonia in wuhan, china: a descriptive study

Clinical and CT imaging features of the COVID-19 pneumonia: Focus on pregnant women and children

CT) for Suspected COVID-19 Infection. ACR recommendations for the use of chest radiography and computed tomography

Statements/Recommendations-for-Chest-Radiography-and-CT-for-Suspected-COVID19-Infection

Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in wuhan, china

COVID-19: Overview of pregnancy issues -UpToDate

Correlation between the levels of SpO2and PaO2

How I do it: managing radiation dose in CT

State-of-the-art pulmonary CT angiography for acute pulmonary embolism

Pulmonary CT angiography as first-line imaging for PE: Image quality and radiation dose considerations

CT radiation dose optimization and estimation: an update for radiologists

Published on behalf of the lnternational Commission on Radiological Protection International Commission on Radiological Protection 198l-1985 Members of the Main Commission of the ICRP Subscription Rates Annual subscription, including postage and insurance

Does radiotherapy around the time of pregnancy for Hodgkin's disease modify the risk of breast cancer?

To shield or not to shield: application of bismuth breast shields

Imaging pregnant patients with suspected pulmonary embolism: what the radiologist needs to know

ISUOG interim guidance on 2019 novel coronavirus infection during pregnancy and puerperium: information for healthcare professionals

Pulmonary embolism and deep vein thrombosis in COVID-19: a systematic review and meta-analysis

Antenatal pulmonary embolism: risk factors, management and outcomes

British thoracic society guidelines for the management of suspected acute pulmonary embolism

Clinical criteria to prevent unnecessary diagnostic testing in emergency department patients with suspected pulmonary embolism

Excluding pulmonary embolism at the bedside without diagnostic imaging: management of patients with suspected pulmonary embolism presenting to the emergency department by using a simple clinical model and D-dimer

Prediction of pulmonary embolism in the emergency department: the revised geneva score

Pregnancy-induced changes in immune protection of the genital tract: defining normal

Imaging the pregnant patient for nonobstetric conditions: algorithms and radiation dose considerations

An official american thoracic society/society of thoracic radiology clinical practice guideline: evaluation of suspected pulmonary embolism in pregnancy

COVID-19 during pregnancy, delivery and postpartum period based on EBM

The use of iodinated and gadolinium contrast media during pregnancy and lactation

Thyroid function in very low birthweight infants after intravenous administration of the iodinated contrast medium iopromide. Arch Disease Childhood

Association between MRI exposure during pregnancy and fetal and childhood outcomes

Cardiac magnetic resonance imaging in coronavirus disease

Cardiac involvement in patients recovered from COVID-2019 identified using magnetic resonance imaging

Guidelines for computed tomography and magnetic resonance imaging use during pregnancy and lactation

ACR guidance document on MR safe practices

Findings and differential diagnosis of fetal intracranial haemorrhage and fetal ischaemic brain injury: what is the role of fetal MRI?

Severe fetal brain damage subsequent to acute maternal hypoxemic deterioration in COVID-19

Visualization of severe acute respiratory syndrome coronavirus 2 invading the human placenta using electron microscopy

Placental pathology in COVID-19

Effects of SARS-COV-2 infection on fetal pulmonary artery Doppler parameters

Fetal pulmonary artery doppler evaluation in pregnant women after recovery from COVID-19

Maternal and fetal effects of COVID-19 virus on a complicated triplet pregnancy: a case report

Novel screening and triage strategy in iran during deadly coronavirus disease 2019 (COVID-19) epidemic: value of humanitarian teleconsultation service

Guidelines for diagnostic imaging during pregnancy. unboundmedicine.com

Radiation exposure and pregnancy: when should we be concerned?

Guidelines for diagnostic imaging during pregnancy and lactation

Diagnostic imaging in pregnant and nursing patients -Up-ToDate