Publications by authors named "Sara De Carolis"

60 Publications

Is Cardiomegaly an Indication of "Heart-Sparing Effect" in Small Fetuses?

Fetal Diagn Ther 2021 Oct 15:1-7. Epub 2021 Oct 15.

Fetal Medicine Unit, St. George's University Hospitals NHS Foundation Trust, London, United Kingdom.

Introduction: This study aimed to test the hypothesis that cardiac size is maintained in small fetuses presenting with cardiomegaly.

Materials And Methods: We identified singleton fetuses with estimated fetal weight <10th centile and with cardiomegaly without another more likely cardiac or extra-cardiac cause. We used Z-scores for cardiac and thoracic circumferences normalized for gestational age (GA), biparietal diameter (BPD), head circumference (HC), and femur length (FL), obtained from 188 normally grown fetuses.

Results: When comparing chest size, small fetuses had significantly lower thoracic circumferences median Z-scores (IQR) for GA = -4.82 (-6.15 to -3.51), BPD = -2.42 (-4.04 to -1.48), HC = -2.72 (-4.53 to -1.90), and FL = -1.60 (-2.87 to -0.71); p < 0.001 for all. When comparing heart size, small fetuses showed lower cardiac circumferences median Z-scores (IQR) for GA = -1.59 (-2.79 to -0.16); p < 0.001, similar cardiac circumferences Z-scores for BPD = 0.29 (-0.65 to 1.28); p = 0.284 and HC = 0.11 (-1.13 to 0.96); p = 0.953, and higher cardiac circumferences Z-scores for FL = 0.94 (-0.05 to 2.13); p < 0.001.

Conclusions: Our results show that in small fetuses with cardiomegaly, the heart maintains normal dimensions when normalized to cranial diameters and higher dimensions when normalized to long bones. This provides insight into cardiac adaptation to adverse intrauterine environment.
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http://dx.doi.org/10.1159/000519059DOI Listing
October 2021

Correction to: Acute liver failure in Still's disease relapse during pregnancy: case report and discussion of a possible trigger role of DILI.

BMC Gastroenterol 2021 Oct 1;21(1):358. Epub 2021 Oct 1.

Transplant Hepatology Unit - CEMAD Digestive Disease Center, Fondazione Policlinico Universitario "A. Gemelli" IRCCS, Università Cattolica del Sacro Cuore, Largo A. Gemelli 8, 00168, Rome, Italy.

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http://dx.doi.org/10.1186/s12876-021-01933-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8487132PMC
October 2021

Continuous Glucose Monitoring in Women with Normal OGTT in Pregnancy.

J Diabetes Res 2021 23;2021:9987646. Epub 2021 Aug 23.

Department of Obstetrics and Gynecology, Catholic University of Sacred Heart, Fondazione Polclinico Universitario Agostino Gemelli IRCCS, Rome, Italy.

Continuous glucose monitoring (CGM) might be an effective tool to improve glycemic control in gestational diabetes mellitus (GDM). Few data are available about its utilization as a diagnostic tool to find potential alterations of glycemia in subjects with normal oral glucose tolerance test (OGTT). In this preliminary prospective real-life observational study, we aimed to analyze the glycemic pattern in normal and gestational diabetes mellitus (GDM) women by continuous glucose monitoring (CGM) in order to detect potential differences between the two groups and glycemic alterations despite a normal OGTT. After the screening for GDM, subjects were connected to a CGM system for seven consecutive days. The areas under the curve of the first 60 minutes after each meal and 60 minutes before breakfast were analyzed. Women with normal OGTT that during CGM showed impaired glycemic values (more than 95 fasting or more than 140 one hour after meals or more than 120 two hours after meals) performed one week of self-monitoring of blood glucose (SMBG). After OGTT, 53 women considered normal and 46 affected by GDM were included. CGM parameters did not show any differences between the two groups with impaired glycemic excursions found in both groups. After CGM period, 33 women with normal OGTT showed abnormal glycemic patterns. These 33 women then performed one week of SMBG. After evaluation of one week of SMBG, 21 required diet therapy and 12 required insulin treatment and were followed until the delivery. An increase in gestational weight gain was observed in normal women with normal OGTT but this was not significant. No significant data were found regarding neonatal outcomes in the two groups of women. In conclusion, CGM use in pregnancy might help to detect glycemic fluctuations in women with normal OGTT, improving their treatment and outcomes.
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http://dx.doi.org/10.1155/2021/9987646DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8408006PMC
August 2021

Bleeding and antithrombotic therapy during pregnancy in women with poor aPL-related obstetric outcomes: A survey of 1075 cases from EUROAPS registry∗.

Eur J Anaesthesiol 2021 09;38(9):916-922

From the Systemic Autoimmune Disease Unit, Department of Internal Medicine, Vall d'Hebron University Hospital, Department of Medicine, Universitat Autonoma (JA-R, JP-G), Internal Medicine Department, Althaia Healthcare University Network of Manresa, Systemic Autoimmune Disease Unit, Manresa (EE-V), High Risk Unit, Obstetric Department, Quirón University Hospital, Barcelona (RF-O), Internal Medicine Department, Miguel Servet University Hospital, Zaragoza, Spain (LS-C), Haematology Unit, Hippokration Hospital of Thessaloniki, Greece (EL), AP-HP, Hôpital Saint-Antoine, Service de Médecine Interne and Inflammation-Immunopathology-Biotherapy Department (DHU i2B), Sorbonne Universités, UPMC University, Paris (AM), Vascular and Coagulation Department, University Hospital Angers, Angers, France (CB), Rheumatology Unit, Department of Clinical and Experimental Medicine Azienda Ospedaliera, University of Padua, Padua (AR), Rheumatology and Clinical Immunology Unit, Department of Clinical and Experimental Sciences, University of Brescia, Spedali Civili, Brescia (AT, CN), Department of Obstetrics and Gynaecology, Università di Torino, Torino, Italy (LM), Systemic Autoimmune Diseases Service, Hospital Clinic, Universitat de Barcelona, Barcelona, Spain (GE), Department of Gynaecology, Gemmelli Hospital, Catholic University, Rome, Italy (SDeC), Autoimmune, Thrombophilic Diseases and Pregnancy Division, Dr Carlos G Durand Hospital, Buenos Aires, Argentina (OL, US), Obstetrics and Gynaecology Department, High Risk Unit, University Hospital de la Santa Creu i Sant Pau, Barcelona, Spain (ELL), Immunorheumatology Research Laboratory, Istituto Auxologico Italiano (LT), Division of Rheumatology, Department of Clinical Sciences and Community Health, University of Milan, Milan, Italy (CC), Cardiology Unit, Department of Cardiac, Thoracic and Vascular Sciences, University of Padua, Padua (VP), Pregnancy and Rheumatic Diseases Clinic Unit of Medicine and Clinical Immunology IRCCS Ospedale San Raffaele Università Vita-Salute San Raffaele, Milano, Italy (PR-Q, VC), Department of Obstetrics, Medical University Graz, Graz, Austria (KM-P), Department of Systemic Rheumatic Disease, V.A. Nasonova Research Institute of Rheumatology, Moscow, Russia (TR), Department of Gynecology Obstetrics and Urology, "Sapienza" University of Rome, Rome, Italy (ST) and Clinical Research Unit, Althaia Healthcare University Network of Manresa, Barcelona, Catalonia Central University, Manresa-Vic, Spain (AA).

Background: The combination of low-dose aspirin (LDA) and low-molecular-weight heparin (LMWH) until the end of gestation are the currently the accepted standard of care for the treatment of antiphospholipid-related obstetric disorders. In refractory cases, hydroxychloroquine (HCQ) can be added to this standard of care.

Objective: To evaluate the haemostatic safety of LDA and LMWH (medium to high prophylactic doses) during pregnancy and the puerperium in women with both full-blown obstetric antiphospholipid syndrome (OAPS) (Sydney criteria) and noncriteria - incomplete - OAPS.

Study Design: Retrospective/prospective multicentre observational study. Obstetric background, laboratory categories, delivery mode, antithrombotic regimens and bleeding complications were compared.

Setting: A total of 30 tertiary European hospitals.

Patients: Mainly, Caucasian/Arian pregnant women were included. Other ethnicities were minimally present. Women were controlled throughout pregnancy and puerperium.

Main Outcome Measures: The primary end-point was to evaluate the number of major and minor haemorrhagic complications in this cohort of women. Neuraxial anaesthetic bleeding complications were particularly assessed. Secondly, we aimed to compare local/general bleeding events between groups.

Results: We studied 1650 women, of whom 1000 fulfilled the Sydney criteria of the OAPS and 650 did not (noncriteria OAPS). Data on antithrombotic-related complications were available in 1075 cases (65.15%). Overall, 53 (4.93%) women had bleeding complications, with 34 being considered minor (3.16%) and 19 major (1.76%). Neither obstetric complications nor laboratory categories were bleeding-related. Assisted vaginal delivery and caesarean section were related to local haemorrhage. Heparin doses and platelet count were not associated with major bleeding.

Conclusions: LDA and medium to high prophylactic LMWH during pregnancy in women with full-blown OAPS/noncriteria OAPS are safe. A slight increase in bleeding risk was noted in instrumental deliveries. No women who underwent spinal or epidural anaesthesia suffered bleeding complications. No haemorrhage was observed in cases where HCQ was added to standard therapy.
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http://dx.doi.org/10.1097/EJA.0000000000001484DOI Listing
September 2021

Acute liver failure in Still's disease relapse during pregnancy: case report and discussion of a possible trigger role of DILI.

BMC Gastroenterol 2021 Aug 6;21(1):317. Epub 2021 Aug 6.

Transplant Hepatology Unit - CEMAD Digestive Disease Center, Fondazione Policlinico Universitario "A. Gemelli" IRCCS, Università Cattolica del Sacro Cuore, Largo A. Gemelli 8, 00168, Rome, Italy.

Background: Still's disease is a rare systemic inflammatory disease with frequent but generally mild liver involvement. The most common cause of acute liver failure in western countries is drug-induced liver injury, while it has rarely been reported in subjects suffering from Still's disease.

Case Presentation: We report a case of a young woman presenting with SD reactivation in pregnancy and acute liver failure after delivery with a possible triggering role of drug induced liver injury.

Conclusions: The prompt recognition of Still's disease reactivation allowed early introduction of steroid therapy and resolution of the clinical picture. We discuss potential factors precipitating ALF in this case, and implications for the diagnosis and management of such patients.
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http://dx.doi.org/10.1186/s12876-021-01878-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8349071PMC
August 2021

"Non-criteria antiphospholipid antibodies": bridging the gap between seropositive and seronegative Antiphospholipid Syndrome.

Rheumatology (Oxford) 2021 May 10. Epub 2021 May 10.

Reumatologia, Dipartimento di Scienze Cliniche Internistiche, Anestesiologiche e Cardiovascolari, Sapienza Università Roma, Rome, Italy.

Objective: We aimed to analyze the prevalence of non-criteria anti-phospholipid (aPL) antibodies and their role in the diagnosis, treatment and prognosis in a cohort of patients with clinical features consistent with a diagnosis of antiphospholipid syndrome (APS), but persistently negative for criteria aPL-anti-cardiolipin antibodies (aCL), anti-β2-glycoprotein I antibodies (aβ2-GPI), and lupus anticoagulant (LA) - named seronegative APS (SN-APS).

Methods: Sera from SN-APS patients were tested for aCL by TLC-immunostaining, anti-vimentin/cardiolipin (aVim/CL) and anti-phosphatidylserine/prothrombin (anti-PS/PT) by ELISA. Control groups of our study were APS patients and healthy controls.

Results: We enrolled 114 consecutive SN-APS patients, 69 (60.5%) resulted positive for at least one non-criteria test in two occasions 12 weeks apart. Among the persistently positive patients to these tests, 97% resulted positive for aCL by TLC-immunostaining, 52.3% for aVim/CL and 17.4% for aPS/PT. SN-APS patients with double positivity (aCL by TLC-immunostaining and aVim/CL) showed a likelihood positive ratio of 8 to present mixed thrombotic and obstetrical features. Among SN-APS patients tested positive, after the therapeutic changes, 3 cases of recurrent thrombosis were observed [median follow-up 41 months (IQR 39.5)]. Twenty pregnancies were recorded in 17 SN-APS patients after the detection of unconventional aPL and 12 of them (60%) experienced a good outcome under conventional treatment for APS.

Conclusions: This is the largest monocentric study demonstrating that aCL tested by TLC-immunostaining and aVim/CL can detect aPL positivity in SN-APS. It may encourage clinicians to monitoring and providing adequate targeted therapy, which improve SN-APS prognosis.
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http://dx.doi.org/10.1093/rheumatology/keab414DOI Listing
May 2021

Autoimmune Congenital Heart Block: A Review of Biomarkers and Management of Pregnancy.

Front Pediatr 2020 22;8:607515. Epub 2020 Dec 22.

Fondazione Policlinico Universitario "A. Gemelli" IRCCS, Department of Obstetrics, Gynaecology and Pediatrics, Rome, Italy.

Autoimmune Congenital Heart Block (CHB) is an immune-mediated disease due to transplacental passage of circulating anti-Ro/SSA and anti-La/SSB autoantibodies. It occurs in 2% of anti-Ro/SSA-exposed pregnancies, and recurrence rate is nine times higher in subsequent pregnancies. Aim of this review is to identify biomarkers of CHB and treatment strategies. The Ro-system is constituted by two polypeptides targeted by the anti-Ro52 and anti-Ro60 autoantibodies. The central portion of Ro52 (p200), more than the full amino-acid sequence of Ro-52, is recognized to be the fine specificity of anti-Ro associated to the highest risk of cardiac damage. If anti-p200 antibody should be tested, as biomarker of CHB, over standard commercial ELISAs is still debated. Recent studies indicate that type I-Interferon (IFN) can activate fibroblasts in fetal heart. In the mother the anti-Ro/La antibodies activate the type I IFN-signature, and maternal IFN-regulated genes correlate with a similar neonatal IFN-gene expression. Evaluation of maternal IFN-signature could be used as novel biomarker of CHB. The measurement of "mechanical" PR interval with weekly fetal echocardiogram (ECHO) from 16 to at least 24 weeks of gestation is strongly recommended for CHB prenatal diagnosis. However, ECHO screening presents some limitations due to difficult identification of first-degree block and possible occurrence of a complete block from a normal rhythm in few days. Maternal administration of Hydroxychloroquine from the tenth week of gestation, modulating toll-like receptor and autoantibody-dependent type I IFN activation on the fetus, has an important role in preventing CHB in pregnant women with high risk for recurrent CHB.
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http://dx.doi.org/10.3389/fped.2020.607515DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7784711PMC
December 2020

Perinatal outcome in gestational hypertension: Which role for developing preeclampsia. A population-based cohort study.

Eur J Obstet Gynecol Reprod Biol 2020 Aug 1;251:218-222. Epub 2020 Jun 1.

UOC di Patologia Ostetrica, Dipartimento Scienze della Salute della Donna, del Bambino e di Sanità Pubblica, Fondazione Policlinico Universitario A. Gemelli IRCCS, Largo A. Gemelli 8, 00168, Roma, Italy; Istituto di Clinica Ostetrica e Ginecologica, Università Cattolica del Sacro Cuore, L.go Francesco Vito 1, Roma, Italy. Electronic address:

Objective: To analyze perinatal outcome in singleton pregnancies complicated by gestational hypertension (GH), to investigate the rate of women developing preeclampsia (PE) and to describe maternal features associated with progression to PE.

Study Design: This is a population-based retrospective cohort-study involving 514 singleton pregnancies with a diagnosis of GH at admission.

Results: In pregnancies with GH, a poorer pregnancy outcome in comparison to healthy controls was observed in terms of gestational age at delivery, birthweight and birthweight percentile. The observed overall rate of developing PE was 11.7 %. Of all pregnancies with GH at admission, two different groups were identified based on the diagnosis at delivery: GHPE, i.e. women who developed PE (60/514; 11.7 %), and GHnoPE, i.e. women who did not develop PE (454/514; 88.3 %). In the GHPE group it was observed that the 62 % of the women with diagnosis of GH earlier than 28 weeks developed PE while only 2% developed PE if the diagnosis of GH was performed later than 36 weeks. The observed rate of developing PE was 14.7 % in pharmacologically treated hypertensive women, whereas the diagnosis of PE has been made in only 3% of non-treated women.

Conclusion: Pregnant women with raised blood pressure are at risk of having a less favourable perinatal outcome. The risk is mainly associated with the progression to PE. Major determinants of the risk of developing PE are the earlier gestational age at diagnosis of GH, the necessity of treatment and the number of anti-hypertensive drugs needed for controlling blood pressure.
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http://dx.doi.org/10.1016/j.ejogrb.2020.05.064DOI Listing
August 2020

Postnatal Health in Children Born to Women After Bariatric Surgery.

Obes Surg 2020 Oct;30(10):3898-3904

Istituto di Clinica Ostetrica e Ginecologica, Università Cattolica del Sacro Cuore, Rome, Italy.

Introduction: The aim of this study is to evaluate short- and long-term consequences in children born to women after different bariatric surgery (BS) procedures.

Methods: A questionnaire survey was given to the mothers referred from 1994 to 2019 to our center for pregnancy and delivery management after BS procedures: (a) malabsorptive surgery, (b) restrictive procedures, and (c) combined restrictive-malabsorptive procedures.

Results: Data from 74 children born after BS, aged 0 month to 12 years, were analyzed. The prevalence of children with underweight was 5.4%, normal weight 59.5%, overweight 16.2%, and obesity 18.9%. The prevalence of obesity was higher in children pre-school aged than that in school-aged ones. Neurodevelopmental disorders were more frequent if maternal BMI before bariatric surgery was ≥ 41 kg/m (p = 0.008), as well as if the pregnancy occurred less than 18 months after BS (p = 0.028). In school-aged children conceived within 18 months after BS, the highest risk of neurodevelopmental disorders (p = 0.028) and overweight (p = 0.018) was observed. The prevalence of neurodevelopmental disorders was much higher for small for gestational age babies (p = 0.048). Children born after biliopancreatic diversion (BPD) showed less maternal breastfeeding, shorter breastfeeding duration, more overweight, and more occurrence of atopic dermatitis in comparison with children born after other bariatric procedures.

Conclusions: Postnatal health in children born to women after BS was impaired by long-term consequences and by other diseases later in life. Children born after BPD were particularly at higher risk for short and long term consequences when compared to children born after other BS procedures.
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http://dx.doi.org/10.1007/s11695-020-04738-3DOI Listing
October 2020

Impact of chorioamnionitis on maternal and fetal levels of proinflammatory S100A12.

Eur J Pediatr 2021 Jan 9;180(1):39-45. Epub 2020 Jun 9.

University Children's Hospital, Würzburg, Germany.

Histologic chorioamnionitis (HCA) may lead to the fetal inflammatory response syndrome (FIRS). The aim of this pilot study was to evaluate S100A12, a marker of innate immune activation, in mothers with or without HCA and in their infants. Concentrations of S100A12, interleukin 6 (IL-6), and C-reactive protein (CRP) were evaluated in maternal, cord, and neonatal blood of very preterm infants. Histologic examinations of the placenta and umbilical cords were performed. The 48 mother-neonate pairs enrolled were subdivided into two groups: HCA group (N = 15) and control group without HCA (N = 33). Maternal S100A12 levels were similar between HCA and control group. Similarly, S100A12 concentrations in cord and neonatal blood did not differ between the groups. However, high S100A12 concentrations were detected in cord and neonatal blood of two out of three neonates exposed to HCA associated with advanced funisitis. Concentrations of IL-6 and CRP were higher in maternal blood of the HCA group compared with controls (p < 0.05, p < 0.001; respectively), but no differences in cord or neonatal blood was found.Conclusion:S100A12 did neither identify mothers with HCA nor very preterm infants exposed to HCA. It is currently unknown if S100A12 may identify neonates with FIRS. What is known: • Histologic chorioamnionitis (HCA) may lead to the fetal inflammatory response syndrome (FIRS). • S100A12 represents an early, sensitive, and specific diagnostic marker of inflammatory processes. What is new: • S100A12 did neither identify mothers with HCA nor very preterm infants exposed to HCA. • It is currently still unclear if S100A12 has a potential in identifying preterm infants with FIRS.
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http://dx.doi.org/10.1007/s00431-020-03695-4DOI Listing
January 2021

Persistence of right umbilical vein: a singular case.

Turk J Pediatr 2020 ;62(2):338-342

Departments of Obstetrics, Gynaecology, Fondazione Policlinico Gemelli IRCCS, Università Cattolica del Sacro Cuore, Largo Francesco Vito 1, 00168 Rome, Italy.

Background: Persistent right umbilical vein (PRUV) is one of the most common prenatally detected venous anomaly. In the intrahepatic variant (I-PRUV) the right umbilical vein fuses with right portal vein and through the ductus venous drains into inferior vena cava, while in the uncommon extrahepatic variant (E-PRUV), the vein bypasses the liver completely. E-PRUV has a worse prognosis compared to I-PRUV, due either to severe hemodynamic effects or to the frequent association with other severe fetal malformations.

Case: Here we report a case of E-PRUV with good outcome. Prenatal fetal ultrasonography (US) performed at 33 weeks of gestation in 28-year old woman, highlights the presence of E-PRUV with right UV draining in inferior vena cava. In the male neonate born at 35 weeks of gestation by C-section, the Apgar Score was 95`- 1010 and no other associated malformations and hemodynamic decompensation were found. Postnatal abdominal US showed the presence of enlarged paraumbilical veins.

Conclusions: The association of E-PRUV draining into the inferior vena cava with shunt through paraumbilical veins, could have preserved offspring by severe cardiac overload, positively affecting prognosis.
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http://dx.doi.org/10.24953/turkjped.2020.02.024DOI Listing
August 2021

Pregnancy outcome and left ventricular ejection fraction in women with history of myocardial infarction.

Eur J Obstet Gynecol Reprod Biol 2020 Jul 29;250:74-75. Epub 2020 Apr 29.

Dipartimento Scienze della Salute della Donna, del Bambino, e di Sanità Pubblica, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Università Cattolica del Sacro Cuore, Largo Agostino Gemelli 8, Roma, Italy. Electronic address:

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http://dx.doi.org/10.1016/j.ejogrb.2020.04.052DOI Listing
July 2020

Comparative study of obstetric antiphospholipid syndrome (OAPS) and non-criteria obstetric APS (NC-OAPS): report of 1640 cases from the EUROAPS registry.

Rheumatology (Oxford) 2020 06;59(6):1306-1314

Clinical Research Unit, Althaia Healthcare University Network of Manresa, University of Vic - Central University of Catalonia, Barcelona.

Objectives: To compare clinical features, laboratory data and fetal-maternal outcomes between 1000 women with obstetric APS (OAPS) and 640 with aPL-related obstetric complications not fulfilling Sydney criteria (non-criteria OAPS, NC-OAPS).

Methods: This was a retrospective and prospective multicentre study from the European Registry on Obstetric Antiphospholipid Syndrome.

Results: A total of 1650 women with 5251 episodes, 3601 of which were historical and 1650 latest episodes, were included. Altogether, 1000 cases (OAPS group) fulfilled the Sydney classification criteria and 650 (NC-OAPS group) did not. Ten NC-OAPS cases were excluded for presenting thrombosis during follow-up. All cases were classified as category I (triple positivity or double positivity for aPL) or category II (simple positivity). Overall, aPL laboratory categories showed significant differences: 29.20% in OAPS vs 17.96% in NC-OAPS (P < 0.0001) for category I, and 70.8% in OAPS vs 82% in NC-OAPS (P < 0.0001) for category II. Significant differences were observed when current obstetric complications were compared (P < 0.001). However, major differences between groups were not observed in treatment rates, livebirths and thrombotic complications. In the NC-OAPS group, 176/640 (27.5%) did not fulfil Sydney clinical criteria (subgroup A), 175/640 (27.34%) had a low titre and/or non-persistent aPL positivity but did meet the clinical criteria (subgroup B) and 289/640 (45.15%) had a high aPL titre but did not fulfil Sydney clinical criteria (subgroup C).

Conclusion: Significant clinical and laboratory differences were found between groups. Fetal-maternal outcomes were similar in both groups when treated. These results suggest that we could improve our clinical practice with better understanding of NC-OAPS patients.
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http://dx.doi.org/10.1093/rheumatology/kez419DOI Listing
June 2020

Delivery room interventions to improve the stabilization of extremely-low-birth-weight infants.

J Matern Fetal Neonatal Med 2021 Jun 9;34(12):1925-1931. Epub 2019 Aug 9.

Department of Obstetrics and Gynecology, Policlinico Universitario Agostino Gemelli, Rome, Italy.

Objective: To retrospectively verify whether the positioning of the umbilical venous catheter (UVC) in the delivery room (DR) and the early start of the preheated infusion of 10% glucose solution conditioned temperature and glycemia values of ELBW neonates in the first hours of life.

Methods: Neonates ( = 137) were divided into two groups on the basis of timing of positioning of the UVC. In Group I the UVC was placed in DR, while in Group II after Neonatal Intensive Care Unit (NICU) admission. Data were assessed in different times: body temperature at neonatal admission to NICU (T); after 2 hours (T); then, every 2 hours until normothermia; glycemia value at NICU admission, every 1-2 hours in the first 12 hours, every 4 hours from 12 to 24 hours, and every 6-12 hours until normalization. Time slot childbirth was also detected since only in the morning shift there was a dedicated resuscitation team always present in DR, while during the afternoon and night it was available on-call. Preventive measures to limit heat dispersion were adopted in both Groups.

Results: In Group I respect to Group II, both at T and T: (a) the rate of normothermic neonates was higher and (b) the rate of neonates with moderate hypothermia was lower. The hourly temperature increase was similar between the groups and the time needed to reach normothermia was significantly lower in Group I than in Group II. Glycemic values at T were lower in Group II. In Group II, after UVC positioning and glucose solution administration, the 42.2% of infants immediately brought glycemia back to normal, while the 57.8% needed specific treatment. The majority of newborns of Group I was born during the morning shift.

Conclusions: The early UVC placement by a dedicated interdisciplinary team is a relevant intervention to carry out during the "Golden minutes" to improve the ELBW stabilization soon after birth.
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http://dx.doi.org/10.1080/14767058.2019.1651278DOI Listing
June 2021

Adult onset Still's disease and pregnancy.

Autoimmun Rev 2019 Sep 16;18(9):102356. Epub 2019 Jul 16.

Division of Rheumatology, Fondazione Policlinico Universitario A. Gemelli IRCCS, Roma-Università Cattolica del Sacro Cuore, Italy.

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http://dx.doi.org/10.1016/j.autrev.2019.102356DOI Listing
September 2019

Autoimmunity in obstetrics and autoimmune diseases in pregnancy.

Best Pract Res Clin Obstet Gynaecol 2019 Oct 18;60:66-76. Epub 2019 Mar 18.

UOC di Patologia Ostetrica, Dipartimento Scienze della Salute della Donna, del Bambino e di Sanità Pubblica, Fondazione Policlinico Universitario A. Gemelli IRCCS, Roma, Italy; Istituto di Clinica Ostetrica e Ginecologica, Università Cattolica del Sacro Cuore, Roma, Italy.

Autoimmune diseases (AIDs) are associated with strong female preponderance and often present before or during the reproductive years; consequently, pregnancy and breastfeeding are topics of major interest for these patients. AIDs show different responses to pregnancy: some ameliorate, while others remain unchanged, and several AIDs aggravate. The response of the AIDs to the hormonal and immunological alterations of pregnancy reflects the different pathophysiology of each disease. Systemic lupus erythematosus (SLE) and antiphospholipid syndrome (APS) are associated with multiple autoantibodies, multiorgan involvement, more aggressive therapy, and increased impact on pregnancy outcome. For the management of pregnancy in patients with SLE and/or APS, it is important to individuate the correct risk profile for each woman and timing for treatment. The optimal timing for starting or modulating treatment is at preconception assessment to influence the placentation. In this chapter, we discuss the management of pregnancy in patients with AIDs.
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http://dx.doi.org/10.1016/j.bpobgyn.2019.03.003DOI Listing
October 2019

The European Registry on Obstetric Antiphospholipid Syndrome (EUROAPS): A survey of 1000 consecutive cases.

Autoimmun Rev 2019 Apr 15;18(4):406-414. Epub 2019 Feb 15.

Clinical Research Unit, Althaia Healthcare University Network of Manresa, Manresa, Barcelona, Spain.

Aim: To analyse the clinical features, laboratory data and foetal-maternal outcomes, and follow them up on a cohort of 1000 women with obstetric antiphospholipid syndrome (OAPS).

Methods: The European Registry of OAPS became a registry within the framework of the European Forum on Antiphospholipid Antibody projects and was placed on a website in June 2010. Thirty hospitals throughout Europe have collaborated to carry out this registry. Cases with obstetric complaints related to antiphospholipid antibodies (aPL) who tested positive for aPL at least twice were included prospectively and retrospectively. The seven-year survey results are reported.

Results: 1000 women with 3553 episodes were included of which 2553 were historical and 1000 were latest episodes. All cases fulfilled the Sydney classification criteria. According to the laboratory categories, 292 (29.2%) were in category I, 357 (35.7%) in IIa, 224 (22.4%) in IIb and 127 (12.7%) in IIc. Miscarriages were the most prevalent clinical manifestation in 386 cases (38.6%). Moreover, the presence of early preeclampsia (PE) and early foetal growth restriction (FGR) appeared in 181 (18.1%) and 161 (16.1%), respectively. In this series, 448 (44.8%) women received the recommended OAPS treatment. Patients with recommended treatment had a good live-birth rate (85%), but worse results (72.4%) were obtained in patients with any treatment (low-dose aspirin (LDA) or low-molecular-weight heparin (LMWH) not on recommended schedule, while patients with no treatment showed a poor birth rate (49.6%).

Conclusion: In this series, recurrent miscarriage is the most frequent poor outcome. To avoid false-negative diagnoses, all laboratory category subsets were needed. OAPS cases have very good foetal-maternal outcomes when treated. Results suggest that we were able to improve our clinical practice to offer better treatment and outcomes to OAPS patients.
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http://dx.doi.org/10.1016/j.autrev.2018.12.006DOI Listing
April 2019

Antiphospholipid syndrome: An update on risk factors for pregnancy outcome.

Autoimmun Rev 2018 Oct 15;17(10):956-966. Epub 2018 Aug 15.

Department of Obstetrics, Gynaecology and Pediatrics, F.Policlinico Gemelli IRCCS, Università Cattolica del Sacro Cuore, Largo Francesco Vito 1, 00168 Rome, Italy.

Background: The optimal treatment of women with primary antiphospholipid syndrome (APS) is still debated. About 20-30% of women with APS remain unable to give birth to healthy neonates despite conventional treatment, consisting of prophylactic-dose heparin and low-dose aspirin. These cases are defined "refractory obstetric APS". The early identification of risk factors associated with poor pregnancy outcome could be the optimal strategy to establish criteria for additional therapies, such as hydroxychloroquine, steroids, intravenous immunoglobulin, and plasma exchange.

Purpose: The aim of the present study was to review current literature about risk factors for poor pregnancy outcome.

Search Methods: The PubMed database was used to search for peer-reviewed original and review articles concerning risk factors for pregnancy outcome in APS from 1st January 1990 to 15th January 2018.

Outcomes: History of pregnancy morbidity and/or thrombosis, the association with SLE and/or other autoimmune diseases are well known history-based predictive factors for obstetrical complications, such as miscarriage, maternal venous thromboembolism, intrauterine foetal demise, preeclampsia, and neonatal death. Moreover, laboratory findings associated with poor pregnancy outcome are:triple antiphospholipid antibodies aPL positivity, double aPL positivity, single aPL positivity, false-positive IgM for CMV, and hypocomplementemia. Triple positivity is confirmed as the most significant risk factor by a large body of evidence. Furthermore, the abnormal uterine arteries Doppler velocimetry results are confirmed to be strongly associated with poor pregnancy outcomes in APS. The good performance of the uterine arteries velocimetry, as a negative predictive factor, was reported by different studies. On the contrary, in case of abnormal uterine arteries results, the relevance of a careful surveillance is highlighted for the high risk of maternal-foetal complications. Nevertheless, this tool is a late indicator to suggest any additional treatments.

Conclusions: In order to prevent obstetrical complications and establish the optimal combination therapy, the knowledge at preconception or at the beginning of pregnancy of risk factors associated with poor pregnancy outcome could be a crucial step for management and treatment of APS. In addition, in the preconception assessment a regimen with low-dose aspirin, folic acid, and vitamin D supplementation should be offered, and a treatment strategy has to be established (conventional vs additional therapy). In fact, additional treatment has to be tailored for each patient.
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http://dx.doi.org/10.1016/j.autrev.2018.03.018DOI Listing
October 2018

A Monocentric Cohort of Obstetric Seronegative Anti-Phospholipid Syndrome.

Front Immunol 2018 20;9:1678. Epub 2018 Jul 20.

Dipartimento di Medicina Sperimentale, Sapienza Università di Roma, Rome, Italy.

The present study was conducted to diagnose obstetric anti-phospholipid syndrome (OAPS) in patients with clinical signs suggestive of anti-phospholipid syndrome (APS), but persistently negative for conventional anti-phospholipid antibodies (aPL). Sera from 61 obstetrical seronegative APS (SN-APS) patients were analyzed for anti-cardiolipin antibodies (aCL) using thin-layer chromatography (TLC)-immunostaining, for anti-cardiolipin/vimentin antibodies (aCL/Vim), anti-phosphatidylserine/prothrombin antibodies, IgA anti-βglycoprotein I antibodies (aβGPI), and IgA aCL antibodies by enzyme-linked immunosorbent assay. Taken together, our findings show that in 50 out of 61 SN-APS (81.9%) at least one aPL/cofactor antibody was detected using the assays under test. Results revealed that 76% of SN-APS patients resulted positive for aCL by TLC-immunostaining, 54% for aCL/Vim, 12% for aPS/PT, 4% for IgA aβGPI, and 2% for IgA aCL. Thirty-five out of 61 patients were followed up and the tests were repeated on two occasions, at least 12 weeks apart. Twenty-six out of 35 SN-APS (74.3%) were positive at least one non-conventional test; only 2 patients (5.7%) did not confirm the positivity to the second test. These findings suggest that non-conventional tests, mainly aCL/Vim and aCL detected by TLC-immunostaining, seem to be the most sensitive approaches for finding out aPL in patients with obstetric SN-APS. The use of these tests can be useful for accurate and timely diagnosis of patients with obstetrical APS who are negative for conventional laboratory criteria markers.
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http://dx.doi.org/10.3389/fimmu.2018.01678DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6062588PMC
July 2018

Effect of Additional Treatments Combined with Conventional Therapies in Pregnant Patients with High-Risk Antiphospholipid Syndrome: A Multicentre Study.

Thromb Haemost 2018 04 28;118(4):639-646. Epub 2018 Feb 28.

Louise Coote Lupus Unit, Guy's and St Thomas' NHS Foundation Trust, St Thomas' Hospital, London, United Kingdom.

The effect of additional treatments combined with conventional therapy on pregnancy outcomes was examined in high-risk primary antiphospholipid syndrome (PAPS) patients to identify the most effective treatment strategy. The study's inclusion criteria were (1) positivity to lupus anticoagulant alone or associated with anticardiolipin and/or anti-β2 glycoprotein I antibodies; (2) a history of severe maternal-foetal complications (Group I) or a history of one or more pregnancies refractory to conventional therapy leading to unexplained foetal deaths not associated with severe maternal-foetal complications (Group II). Two different additional treatments were considered: oral-low-dose steroids (10-20 mg prednisone daily) and/or 200 to 400 mg daily doses of hydroxychloroquine and parenteral-intravenous immunoglobulins at 2 g/kg per month and/or plasma exchange. The study's primary outcomes were live birth rates and pregnancy complications. A total of 194 pregnant PAPS patients attending 20 tertiary centres were retrospectively enrolled. Hydroxychloroquine was found to be linked to a significantly higher live birth rate with respect to the other oral treatments in the Group II patients. The high (400 mg) versus low (200 mg) doses of hydroxychloroquine ( = 0.036) and its administration before versus during pregnancy ( = 0.021) were associated with a significantly higher live birth rate. Hydroxychloroquine therapy appeared particularly efficacious in the PAPS patients without previous thrombosis. Parenteral treatments were associated with a significantly higher live birth rate with respect to the oral ones ( = 0.037), particularly in the Group I patients. In conclusion, some additional treatments were found to be safe and efficacious in high-risk PAPS pregnant women.
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http://dx.doi.org/10.1055/s-0038-1632388DOI Listing
April 2018

Comparative study between obstetric antiphospholipid syndrome and obstetric morbidity related with antiphospholipid antibodies.

Med Clin (Barc) 2018 09 20;151(6):215-222. Epub 2017 Dec 20.

AP-HP, Hôpital Saint-Antoine, service de médecine interne and Inflammation-Immunopathology-Biotherapy Department (DHU i2B), Sorbonne Universités, UPMC Univ Paris 06, F-75012, Paris, France.

Background And Objectives: To compare clinical, laboratory, treatment and live birth rate data between women with aPL-related obstetric complications (OMAPS) not fulfilling the Sydney criteria and women fulfilling them (OAPS).

Materials And Methods: Retrospective and prospective multicentre study. Data comparison between groups from The European Registry on Antiphospholipid Syndrome included within the framework of the European Forum on Antiphospholipid Antibody projects.

Results: 338 women were analysed: 247 fulfilled the Sydney criteria (OAPS group) and 91 did not (OMAPS group). In the OMAPS group, 24/91 (26.37%) fulfilled laboratory Sydney criteria (subgroup A) and 67/91 (74.63%) had a low titre and/or non-persistent aPL-positivity (subgroup B). Overall, aPL laboratory categories in OAPS vs. OMAPS showed significant differences: 34% vs. 11% (p<0.0001) for category I, 66% vs. 89% (p<0.0001) for category II. No differences were observed when current obstetric complications were compared (p=0.481). 86.20% of OAPS women were treated vs. 75.82% of OMAPS (p=0.0224), particularly regarding the LDA+LMWH schedule (p=0.006). No differences between groups were observed in live births, gestational, puerperal arterial and/or venous thrombosis.

Conclusions: Significant differences were found among aPL categories between groups. Treatment rates were higher in OAPS. Both OAPS and OMAPS groups had similarly good foetal-maternal outcomes when treated. The proposal to modify OAPS classification criteria, mostly laboratory requirements, is reinforced by these results.
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http://dx.doi.org/10.1016/j.medcli.2017.11.017DOI Listing
September 2018

Hydroxychloroquine as additional treatment in pregnant patients with refractory APS.

Am J Obstet Gynecol 2017 12 6;217(6):711-712. Epub 2017 Sep 6.

Department of Gynecology Obstetrics and Urology, Sapienza University of Rome, Piazzale Aldo Moro, 5, RM 00185 Rome, Italy.

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http://dx.doi.org/10.1016/j.ajog.2017.08.113DOI Listing
December 2017

Refractory obstetrical antiphospholipid syndrome: Features, treatment and outcome in a European multicenter retrospective study.

Autoimmun Rev 2017 Jul 4;16(7):730-734. Epub 2017 May 4.

AP-HP, Hôpital Saint-Antoine, service de médecine interne and Inflammation-Immunopathology-Biotherapy Department (DHU i2B), Sorbonne Universités, UPMC University Paris 06, F-75012 Paris, France.

Aim: To describe the consecutive pregnancy outcome and treatment in refractory obstetrical antiphospholipid syndrome (APS).

Methods: Retrospective multicenter open-labelled study from December 2015 to June 2016. We analyzed the outcome of pregnancies in patients with obstetrical APS (Sydney criteria) and previous adverse obstetrical event despite low-dose aspirin and low-molecular weight heparin LMWH (LMWH) conventional treatment who experienced at least one subsequent pregnancy.

Results: Forty nine patients with median age 27years (23-32) were included from 8 European centers. Obstetrical APS was present in 71%, while 26% had obstetrical and thrombotic APS. Lupus anticoagulant was present in 76% and triple antiphospholipid antibody (APL) positivity in 45% of patients. Pregnancy loss was noted in 71% with a median age of gestation of 11 (8-21) weeks. The presence of APS non-criteria features (35% vs 17% in pregnancies without adverse obstetrical event; p=0.09), previous intrauterine death (65% vs 38%; p=0.06), of LA (90% vs 65%; p=0.05) were more frequent in pregnancies with adverse pregnancy outcome, whereas isolated recurrent miscarriage profile was more frequent in pregnancies without any adverse pregnancy outcome (15% vs 41%; p=0.04). In univariate analysis considering all pregnancies (index and subsequent ones), an history of previous intrauterine death was associated with pregnancy loss (odds-ratio 2.51 (95% CI 1.274.96); p=0.008), whereas previous history of prematurity related to APS (odds-ratio 0.13 95%CI 0.04 0.41, P=0.006), steroids use during the pregnancy (odds-ratio 0.30 95% CI 0.11-0.82, p=0.019) and anticardiolipids isolated profile (odds-ratio 0.51 95% CI 0.26-1.03, p=0.0588) were associated with favorable outcome. In multivariate analysis, only previous history of prematurity, steroids use and anticardiolipids isolated profiles were associated with live-birth pregnancy.

Conclusion: The main features of refractory obstetrical APS were the high rates of LA and triple APL positivity. Steroids could be effective in this APS profile, but prospective studies are necessary.
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http://dx.doi.org/10.1016/j.autrev.2017.05.006DOI Listing
July 2017

Neonatal lupus: Follow-up in infants with anti-SSA/Ro antibodies and review of the literature.

Autoimmun Rev 2017 Apr 14;16(4):427-432. Epub 2017 Feb 14.

Department of Obstetrics and Gynaecology, Catholic University of Sacred Heart, Rome, Italy.

Neonatal Lupus Syndrome (NLS) is a distinct clinical entity caused by transplacental passage of maternal anti-SSA/Ro antibodies (Ab). Mothers may have systemic lupus erythematosus, Sjögren syndrome, or other connective tissue disease, or may be completely healthy at the time of giving birth. NLS includes several clinical manifestations: complete congenital heart block (CCHB) and cutaneous lupus are the most common, while hepatobiliary disease, hematological manifestations and central nervous system involvement may occur. Data from literature on the incidence of the different clinical manifestations of NLS are difficult to compare because they come mostly from retrospective studies or prospective studies, but up to date no systematic follow-up was carried out. We performed a large prospective single-center study with a systematic clinical and instrumental follow-up until 9months of life, in order to evaluate the incidence and the clinical impact of NLS features. From 2004 to 2014 all infants born in our center to mothers with anti-SSA/Ro Ab were enrolled in a specific diagnostic and follow-up (FU) program. At birth, 50 infants born to mothers with anti-SSA/Ro Ab were found positive for anti-SSA/Ro Ab. Infants were tested for anti SSA/Ro Ab at 3months of life, if positive they were re-tested at 6 and 9months. At 9months anti-SSA/Ro Ab were positive in 10% of children. In two cases (4%) a CCHB was identified during pregnancy and required pacemaker implantation at birth. In 10% of cases a transient ECG alterations was found during follow-up. Hematological NLS features (anemia, neutropenia, thrombocytopenia) were found at birth and during FU in several patients, in all cases without clinical manifestations and in most cases with complete normalization at 9months. Mild and transient elevation of aminotransferases between 3 and 6months of life were found in 56% and 40% of patient, respectively; non-specific ultrasound cerebral anomalies in absence of clinical neurological signs were found at birth in 9 patients (18%), subsequently normalized. Prenatal maternal screening is of primary importance in order to early detect CCHB, which requires maternal treatment and pacemaker implantation at birth. Infants born to mothers with anti-SSA/Ro Ab should be monitored for all NLS features at birth. However, during the first months of life, these infants seem to develop only mild, transient and self-limited clinical manifestations, which in most cases are completely solved at 9months of life. This consideration, together with the evidence that only 10% of infants had anti-SSA/Ro Ab persistent in blood at 9months, suggests that follow-up of these children can be performed until 6-9months of life with good clinical safety. Moreover, a clinical and laboratory monitoring at 3months of life, when the highest incidence of hematological features and liver tests alterations are observed, is strongly recommended. In the future, it would be clarified if a follow-up until adulthood would be indicated in cases with persistent anti SSA/Ro or in all infants born to mother with anti SSA/Ro.
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http://dx.doi.org/10.1016/j.autrev.2017.02.010DOI Listing
April 2017

Inherited thrombophilia in women with poor aPL-related obstetric history: prevalence and outcomes. Survey of 208 cases from the European Registry on Obstetric Antiphospholipid Syndrome cohort.

Am J Reprod Immunol 2016 08;76(2):164-71

Department of Medicine, Hôpital Saint-Antoine, Universite Est Parisien, Paris, France.

Aim: To analyse the prevalence and effects of inherited thrombophilic disorders (ITD) on maternal-foetal outcomes in cases of antiphospholipid antibody related to obstetric complications.

Methods: Women with obstetric complaints who tested positive for aPL and with inherited thrombophilia were prospectively and retrospectively included.

Results: ITD data were available in 208 of 338: 147 had obstetric antiphospholipid syndrome (OAPS) and 61 aPL-related obstetric morbidity (OMAPS). 24.1% had ITD. Laboratory categories I and IIa were more related to OAPS-ITD and IIb and IIc to OMAPS-ITD. No significant differences in obstetric complaints were observed. Regarding ITD carriers, treatment rates were higher in OAPS than in OMAPS for LMWH and LDA plus LMWH (P=.002).

Conclusion: Cases with aPL-related OAPS/OMAPS showed no differences in maternal-foetal outcomes regardless of the presence of one ITD. Maternal thrombotic risk was low, with ITD-positive cases included. Registry data concur with Sydney criteria, whereby aPL-ITD-positive patients are classified as having antiphospholipid syndrome.
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http://dx.doi.org/10.1111/aji.12534DOI Listing
August 2016

Fetal hypoxia secondary to severe maternal anemia as a causative link between blueberry muffin baby and erythroblastosis: a case report.

J Med Case Rep 2016 Jun 13;10(1):155. Epub 2016 Jun 13.

High Risk Pregnancies Unit, Department of Obstetrics, Gynaecology and Paediatrics, Catholic University of the Sacred Heart, Largo F. Vito, 1, 00168, Rome, Italy.

Background: Neonatal blueberry muffin lesions are rare cutaneous eruptions, presenting as transient, non-blanching, red-violaceous papules, mostly localized in the trunk, head and neck, attributable to a marked dermal hematopoietic activity. Congenital infections of the TORCH complex (toxoplasmosis, other, rubella, cytomegalovirus and herpes) and hematological disorders have been classically associated with this neonatal dermatological manifestation. We report for the first time an unusual presentation of blueberry muffin lesions in a neonate born from a mother affected by severe anemia during pregnancy.

Case Presentation: A male, white Caucasian, neonate showed a cutaneous rash at birth, suggestive of "blueberry muffin"-like lesions. These cutaneous lesions were associated with marked elevation of the circulating nucleated red blood cells, and with ultrasound findings of peculiar brain ischemic porencephalic lesions. The clinical features of spontaneous disappearance and the association with marked erythroblastosis strongly suggest that these dermatological findings may be the consequence of an extramedullary hematopoiesis unexpectedly evoked by the intrauterine chronic exposure to hypoxia caused by severe maternal anemia.

Conclusions: In conclusion, fetal hypoxia secondary to severe maternal anemia may play a causative and unreported role in the development of neonatal blueberry muffin lesions.
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http://dx.doi.org/10.1186/s13256-016-0924-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4904358PMC
June 2016

Development of a new fetal growth curve from a large sample of Italian population.

Minerva Pediatr 2017 Aug 10;69(4):245-250. Epub 2015 Sep 10.

Department of Obstetrics and Gynecology and Pediatrics, Catholic University of Sacro Cuore, Rome, Italy.

Background: Intrauterine growth curves are considered an essential instrument in prenatal medicine for an appropriate auxological classification of fetuses and they have a great importance in clinical practice. Nowadays, in Italy a national curve published in 1975, is the most used. It Is based on birth weights of 8458 newborns from physiological pregnancies. The aim of the present study was to develop a modern fetal growth curve based on accurately selection of 35 240 physiological singleton Italian pregnancies with sure gestational age confirmed by ultrasound.

Methods: This is a retrospective analysis of 35,240 pregnancies from "A. Gemelli" University Hospital in Rome and "S. Anna" University Hospital in Turin from January 2001 to December 2006. Non-resident pregnant women or coming from other countries, women with diabetes, hypertensive disorders of pregnancy, multiple pregnancies, fetuses with major malformations and/or chromosomal disorders and stillborn fetuses were excluded.

Results: An increasing trend of median neonatal weight, in comparison with the previous Italian National Curve drawn up in 1975, was found.

Conclusions: Combining data from two centers, a new fetal growth curve, in which the 10th and the 90th percentiles are clinically reliable, was performed, in order to have a better tool to evaluate the Italian fetal population. A trend towards an increase of birth weight was observed if compared to previous growth curve drawn up more than 30 years ago.
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http://dx.doi.org/10.23736/S0026-4946.16.04258-4DOI Listing
August 2017
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