Decidual arteriopathy occurred in 7/15 cases, including atherosis and fibrinoid necrosis of maternal vessels (3/15) and mural hypertrophy of membrane arterioles (5/15). Collectively, these findings suggest that increased antenatal surveillance for women diagnosed with SARS-CoV-2 may be warranted. None of the COVID-19 patients in our study were severely ill or undergoing a “cytokine storm,” and it may be possible that CIP, including histiocytic intervillositis, could be induced in those cases of systemic inflammation. Placentas are only submitted for clinical examination when there is an indication—usually diseases in pregnancy or complications of labor and delivery. Online ISSN: 1472-4146 Print ISSN: 0021-9746. Five placentas were small for gestational age, 1 significantly (298 g, expected 409-589 g). For permissions, please e-mail: journals.permissions@oup.com, This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (. Patients were tracked using REDCap supported by NIH UL1TR001422. The premature infant remains admitted at the time of revision (DOL 14). Pregnant women with COVID-19 delivering between March 18, 2020, and May 5, 2020, were identified via the electronic health record and tracked using REDCap.19 From March 18, 2020, until April 7, 2020, only women with moderate to severe symptoms of COVID-19 underwent testing. Formal “topline” diagnoses of MVM were made in 2 of 15 cases, more commonly than in women with a history of melanoma (P = .012), but not all historical controls. Suggested criteria for examination included abnormal placenta and/or cord on examination in the delivery room; stillbirth; intrauterine growth restriction (<10th percentile); preterm delivery of 34 weeks or less gestation; premature rupture of membranes at less than 34 weeks gestation; severe preeclampsia; clinical concern for viral infection; clinical suspicion of chorioamnionitis; clinical suspicion of abruption; history of current/previous gestational trophoblastic disease; compromised clinical condition of neonate, including intensive care admission, cord pH less than 7.0, Apgar score of 5 or less at 5 minutes, ventilatory assistance, hematocrit less than 25%, hydrops fetalis, congenital anomalies, monochorionic twin gestation, and all higher order multiple gestations (eg, triplets); maternal cancer history (including melanoma); and retained placenta. Sixteen placentas from patients with SARS-CoV-2 were examined Table 1. Best cases from the ESC Clinical Case Gallery is an initiative launched by the ESC Education Committee, the ESC Clinical Case Task Force in collaboration with the European Heart Journal - Case Reports, which objective is to reward the best cases for their outstanding quality and educational content. The authors thank Dr Kruti Maniar (Northwestern Department of Pathology), staff in the Obstetric-COVID unit at Prentice Women’s Hospital, and the Northwestern Memorial Hospital Department of Pathology. The placentas of 3 women who delivered while acutely ill demonstrated increased perivillous or subchorionic fibrin, while in 2 women who had recovered from third trimester infection by the time of delivery, there were large zones of avascular villi, with one of the two additionally demonstrating a large villous infarct; both contained increased nucleated RBCs in the fetal circulation. Behavior Circulatory System Clinical Pathology and Procedures Digestive System Ear Disorders Emergency Medicine and Critical Care Endocrine System Exotic and Laboratory Animals Eye Diseases and Disorders ... Cases. Finally, our study does not formally test causality or the direct relationship between SARS-CoV-2 infection and development of placental pathology. Our hospital’s laboratory information system (Cerner Build List Id: 2014.08.1.36) was searched for all second and third trimester placentas between July 2011 and June 2018. Prior to April 7, 2020, testing was performed using a laboratory-developed version of the Centers for Disease Control and Prevention (CDC) SARS-CoV-2 reverse transcription polymerase chain reaction (RT-PCR) assay.20 Total RNA was extracted by Qiagen MinElute Virus Spin Kit. In determining which placental anomalies are attributable to SARS-CoV-2 infection, we would argue that statistically significant associations identified in controlled studies, such as this one, are the appropriate first step. No patient in the study period had such metastases, so they may be considered a random sample of the delivering population. Placental pathology demonstrated villous edema and a retroplacental hematoma. We report placental pathology from 16 patients with SARS-CoV-2 infection. Pathology reports were retrieved from the laboratory information system. The research goal in the Department of Pathology is to extend our knowledge of the mechanisms of disease, especially at the molecular level. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide, This PDF is available to Subscribers Only. An important placental sign of neonatal morbidity and mortality, Chorangiosis and chorangioma in three cohorts of placentas from Nepal, Tibet, and Japan, Placental pathology in women with gestational diabetes, Association of chorangiomas to hypoxia-related placental changes in singleton and multiple pregnancy placentas, The frequency and type of placental histologic lesions in term pregnancies with normal outcome, Correlation between placental bacterial culture results and histological chorioamnionitis: a prospective study on 376 placentas, Evidence for and against vertical transmission for SARS-CoV-2 (COVID-19), Manual of Pathology of the Human Placenta, © American Society for Clinical Pathology, 2020. Quantities are reported as mean ± standard deviation. In addition to original research, JCP publishes a wide range of other content types aimed at the trainee or practising pathologist, including review articles on hot topics, best practice articles for clinical investigations, detailed summaries of key genes and molecules in pathogenesis, and multi-disciplinary grand rounds cases. Maternal age, gestational age, and delivery mode were extracted from the clinical history within the pathology request. To describe histopathologic findings in the placentas of women with coronavirus disease 2019 (COVID-19) during pregnancy. Comparisons of categorical data with patients with history of melanoma use Fisher exact test. Editorial team. In this report, we present placental findings in 16 women with SARS-CoV-2 infection during pregnancy and compare results to historical controls. C, Intervillous thrombus showing lines of Zahn (×5). Most of the commonly circulating coronaviruses cause mild upper respiratory infection with occasional severe illness in immunocompromised individuals. As SARS-CoV-2 is a virus, it might be expected to induce inflammation.   However adverse perinatal outcomes have been reported, including increased risks of miscarriage, preeclampsia, preterm birth, and stillbirth.4. Search for other works by this author on: Department of Pediatrics, Division of Infectious Diseases, Ann and Robert H. Lurie Children’s Hospital of Chicago and Feinberg School of Medicine, Northwestern University, Feinberg School of Medicine, Northwestern University, Department of Obstetrics and Gynecology, Division of Maternal Fetal Medicine, Feinberg School of Medicine, Northwestern University. For patient safety and convenience, biopsies are usually performed on the posterior iliac crest. This study is subject to some limitations. The impact of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and the associated coronavirus disease 2019 (COVID-19) on pregnant women and infants is of particular interest to obstetricians, pediatricians, and patients. Micropathology Ltd provides a clinically supported service for the rapid diagnosis and management of infectious and genetic disease, DNA paternity testing, a forensic genetics service and undertakes biomedical research on human and veterinary pathology. All rights reserved. COVID-19 patients showed a significant increase in intervillous thrombi. We have grouped symptomatic, asymptomatic, and recovered patients; a larger study could treat these groups separately. Fifteen cases were compared with the 2 control populations described previously. As one of the few broad scope pathology journals, it enables the busy pathologist to keep up to date with the latest developments in all disciplines of pathology. Fourteen patients delivered at term (37-40 weeks), 1 delivered at 34 weeks, and 1 represented a 16-week intrauterine fetal demise (IUFD). Our cohort includes a 16-week IUFD, which was excluded from the subsequent statistical analysis. MVM, previously known as maternal vascular underperfusion, has been associated with oligohydramnios, fetal growth restriction, preterm birth, and stillbirth.23-26 Maternal hypertensive disorders, including gestational hypertension and preeclampsia, are the major risk factors for MVM.27,28 Surprisingly, only 1 of the patients in our study was hypertensive. Patients with a history of melanoma have been suggested as superior controls, as this indication is orthogonal to other pregnancy complications.22 A nested cohort of patients with a history of melanoma was created from the historical controls based on the presence of the word “melanoma” in the clinical history section of their pathology report. A case series of 5 women with MERS during pregnancy as well as subsequent case reports suggest that MERS is also associated with poor maternal and perinatal outcomes.2,3,9, Current case series have described clinical features and outcomes in pregnant women with COVID-19 in Wuhan, China, the original epicenter of infection.2,6,7 Taken together, the body of evidence does not currently suggest that pregnant women are subject to more severe disease, in contrast to both SARS and MERS. For full access to this pdf, sign in to an existing account, or purchase an annual subscription. Sixteen placentas from patients with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) were examined (15 with live birth in the third trimester, 1 delivered in the second trimester after intrauterine fetal demise). Categorical data are reported as actual values or percentages. The increased incidence of chorangiosis is notable as well. After April 7, 2020, patients were tested using the GeneXpert Dx Xpress SARS-CoV-2 RT-PCR assay (Cepheid). The most significant finding is an increase in the rate of features of MVM, most prominently decidual arteriopathy including atherosis and fibrinoid necrosis and mural hypertrophy of membrane arterioles. Four patients had COVID-19 remote from delivery (ie, infection diagnosed between 25-34 days prior to delivery), 2 were diagnosed 6 and 7 days prior to delivery, and the remaining 10 were diagnosed on presentation to labor and delivery Table 2. A, Maternal arteriole with atherosis and fibrinoid necrosis (×20). The rate of AIP is significantly lower than both melanoma (114/215, P = .001) and all historical (9,879/17,479, P = .0003) controls. Follow the journal via Twitter and Facebook. P values are not corrected for multiple comparisons. Thus, while MVM is a useful organizing feature, decidual arteriopathy specifically appears most strongly related to COVID-19, suggesting a different pathophysiology for a different etiology. All 5-minute Apgar scores were 9. The Department of Pathology is dedicated to understanding the basis of disease, to teach knowledge to others, and to apply our understanding to improve medical diagnoses and treatment of patients. We also report villous infarction in several placentas, reinforcing the significance of MVM lesions. Melanoma history is an indication for placental examination but is considered independent of pregnancy outcome, and therefore some have advocated using these patients as a control. All infants were negative for SARS-CoV-2 by nasopharyngeal and throat swab. The analytical sensitivity and specificity are reported by the manufacturer as 100% (87/87 samples) and 100% (30/30 samples), with a limit of detection of 250 copies/mL or 0.0100 plaque-forming units per milliliter.21 Positive SARS-CoV-2 test was considered an independent criterion for submission of placentas to pathology. The histologic changes of MVM are thought to represent some chronicity, though exact timing is unknown, and these features can be seen in women who develop preeclampsia only during or after childbirth. The intervillous space usually contains flowing maternal blood, yet 85% of thrombi are suggested to be of fetal origin.30 Intervillous thrombi are generally considered incidental findings, but have been associated with maternal hypertensive disorders or coincident infarctions.31-33 In the context of research suggesting an increase of thrombotic and thromboembolic disorders in COVID-19, these may represent placental formation or deposition of thrombi in response to the virus.34-36. No pathognomonic features are identified; however, there are increased rates of maternal vascular malperfusion features and intervillous thrombi, suggesting a common theme of abnormal maternal circulation, as well as an increased incidence of chorangiosis. Di Mascio D, Khalil A, Saccone G, et al.Â, Assiri A, Abedi GR, Al Masri M, et al.Â, Garcia AG, Fonseca EF, Marques RL, et al.Â, Martines RB, Bhatnagar J, Keating MK, et al.Â, Martines RB, Bhatnagar J, de Oliveira Ramos AM, et al.Â, Ribeiro CF, Silami VG, Brasil P, et al.Â, Hosier H, Farhadian S, Morotti R, et al.Â, Harris PA, Taylor R, Thielke R, et al.Â, Zhou YY, Ravishankar S, Luo G, et al.Â, Bustamante Helfrich B, Chilukuri N, He H, et al.Â, Weiner E, Feldstein O, Tamayev L, et al.Â, Freedman AA, Goldstein JA, Miller GE, et al.Â, Moldenhauer JS, Stanek J, Warshak C, et al.Â, Klok FA, Kruip MJHA, van der Meer NJM, et al.Â, Helms J, Tacquard C, Severac F, et al.Â, Daskalakis G, Marinopoulos S, Krielesi V, et al.Â. While there are no known placental findings associated with the common coronaviruses, Ng et al14 reported placental pathology in 7 women with SARS infection in Hong Kong. Our dedicated colleagues across the state are a vital part of the NSW and international response to COVID-19 disease. Comparisons were made between placentas of women with COVID-19 and historical controls as well as between placentas of women with COVID-19 and women with placental evaluation for a history of melanoma. A bone marrow aspiration should be performed as part of the same procedure. Whether systemic vascular changes due to maternal COVID-19 are responsible for the histologic changes of MVM cannot be determined. We do not see an increased incidence of AIP in our IUFD or overall in our cases. Maternal vascular malperfusion of the placental bed associated with hypertensive disorders in the Boston Birth Cohort, Placental histopathological lesions in correlation with neonatal outcome in preeclampsia with and without severe features, Seasonal variation of chronic villitis of unknown etiology, Identification of erythrocytes in intervillous thrombi: a study using immunoperoxidase identification of hemoglobins, Relationship between placental morphology and histological findings in an unselected population near term, The frequency and severity of placental findings in women with preeclampsia are gestational age dependent, Placental infarcts, intervillous fibrin plaques, and intervillous thrombi: incidences, cooccurrences, and epidemiological associations, Incidence of thrombotic complications in critically ill ICU patients with COVID-19, High risk of thrombosis in patients with severe SARS-CoV-2 infection: a multicenter prospective cohort study, Prevalence of venous thromboembolism in patients with severe novel coronavirus pneumonia, Chorangiosis: the potential role of smoking and air pollution, Chorangiosis. Information is also provided on editorial policies and open access. Our educational programs include ACGME-accredited residency program in both Anatomic and Clinical Pathology as well as a full range of subspecialty fellowships. Coronaviruses are single-stranded, encapsulated RNA viruses. Comparison with the reported features of 3 placentas in the Chinese language literature are of interest.16 In the previous study, the 3 patients had variably increased perivillous fibrin deposition in comparison to only 1 in our series. Placentas were examined and compared to historical controls and women with placental evaluation for a history of melanoma. PD-L1 expression by Tumor Proportion Score (TPS) and Combined Positive Score (CPS) are similar in non-small cell lung cancer (NSCLC), Role of PRPS2 as a prognostic and therapeutic target in osteosarcoma, Hospital laboratory experience with SARS-CoV-2 (COVID-19) molecular assay sample pooling method in New York City, Clinical and laboratory characteristics in outpatient diagnosis of COVID-19 in healthcare professionals in Rio de Janeiro, Brazil, Impact of COVID-19 on small biopsy diagnostic procedures and cancer resection surgeries in the North-West of Ireland, Clinical pathology resident education during the COVID-19 pandemic, Atypical lymphoid cells circulating in blood in COVID-19 infection: morphology, immunophenotype and prognosis value, Histopathological observations in COVID-19: a systematic review, Cross-reactivity of SARS-CoV-2 with HIV chemiluminescent assay leading to false-positive results, COVID-19 salivary signature: diagnostic and research opportunities, Gene of the month: the 2019-nCoV/SARS-CoV-2 novel coronavirus spike protein, Diagnostic approach in TFE3-rearranged renal cell carcinoma: a multi-institutional international survey, Laboratory assessment of vitamin K status, Inherited metabolic disorders and dyslipidaemia, Placental microbial–metabolite profiles and inflammatory mechanisms associated with preterm birth, Non-neoplastic colorectal disease biopsies: evaluation and differential diagnosis, Epigenetic-sensitive liquid biomarkers and personalised therapy in advanced heart failure: a focus on cell-free DNA and microRNAs, Real-world programmed death-ligand 1 prevalence rates in non-small cell lung cancer: correlation with clinicopathological features and tumour mutation status, Clinicopathological significance of CD47 expression in hepatocellular carcinoma, Development, internal validation and calibration of a risk score to predict survival in patients with EGFR-mutant non-small cell lung cancer, Methylation study of the Paris system for reporting urinary (TPS) categories, Non-amplification genetic alterations of HER2 gene in non-small cell lung carcinoma. SARS-CoV-2 nucleic acid testing was negative in the fetus but positive in placenta. The patients in this study differed from typical MVM patients in other ways. Rates of acute and chronic inflammation were not increased. These rates are not significantly different from melanoma (62/215, P = .246) or all historical (6,739/17,479, P = .082) controls. This case is not included in the cohort for statistical analysis, as the control population is of third trimester deliveries only. Chol, cholestasis of pregnancy; CoV, SARS-CoV-2 infection; Frag, fragmented placenta, weight unreliable; GDM, gestational diabetes mellitus; IUFD, intrauterine fetal demise; LGA, large for gestational age; NA, not applicable; PIH, pregnancy-induced hypertension; PPROM, preterm premature rupture of the membranes; SGA, small for gestational age.
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