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High Risk of Long‐Term Neurodevelopmental Impairment In Ultrasound Obstet Gynecol 2020; 55:39–46 Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/uog.20846 High risk of long-term neurodevelopmental impairment in donor twins with spontaneous twin anemia–polycythemia sequence L. S. A. TOLLENAAR1 ,E.LOPRIORE2,F.SLAGHEKKE1, D. OEPKES1, J. M. MIDDELDORP1, M. C. HAAK1,F.J.C.M.KLUMPER1,R.N.G.B.TAN2,M.RIJKEN2 andJ.M.M.VANKLINK2 1Division of Fetal Medicine, Department of Obstetrics, Leiden University Medical Center, Leiden, The Netherlands; 2Division of Neonatology, Department of Pediatrics, Leiden University Medical Center, Leiden, The Netherlands KEYWORDS: anemia; long-term outcome; monochorionic twins; neurodevelopmental impairment; twin anemia–poly- cythemia sequence CONTRIBUTION NDI. Outcome was compared between surviving donor and recipient twins. Logistic regression analysis was used What are the novel findings of this work? to assess risk factors for NDI. Donor twins of pregnancies complicated by sponta- neous twin anemia–polycythemia sequence (TAPS) have Results Forty-nine twin pregnancies complicated by four-fold higher odds of neurodevelopmental impairment spontaneous TAPS were eligible for inclusion. The compared with their recipient cotwins, are at increased perinatal survival rate was 83% (81/98) of twins. risk of cognitive delay and have a high rate of deafness. Neurodevelopmental assessment was performed in 91% What are the clinical implications of this work? (74/81) of surviving twins. NDI occurred in 30% (22/74) Based on our findings, we strongly advise that routine of TAPS survivors, and was found more often in donors long-term follow-up, including testing for hearing loss, (44%; 15/34) than in recipients (18%; 7/40) (odds ratio = should be an essential part of care of twins diagnosed (OR), 4.1; 95% CI, 1.8–9.1; P 0.001). Severe NDI was with spontaneous TAPS. detected in 9% (7/74) of survivors and was higher in donors compared with recipients (18% (6/34) vs 3% (1/40)), although the difference did not reach statistical ABSTRACT significance; P = 0.056). Donors demonstrated lower = Objectives To evaluate the long-term neurodevelopmen- cognitive scores compared with recipients (P 0.011). tal and behavioral outcomes in surviving infants of Bilateral deafness was identified in 15% (5/34) of donors = pregnancies with spontaneous twin anemia–polycythemia compared with 0% (0/40) of recipients (P 0.056). sequence (TAPS), to compare outcome between donors Parental concern regarding development was reported = and recipients, and to investigate potential risk factors for more often for donor than for recipient twins (P 0.001). neurodevelopmental impairment (NDI). On multivariate analysis, independent risk factors for NDI were gestational age at delivery (OR, 0.7; 95% CI, Methods This was a retrospective study of a consecutive 0.5–0.9; P = 0.003) and severe anemia (OR, 6.4; 95% CI, cohort of spontaneous-TAPS survivors delivered between 2.4–17.0; P < 0.001). 2005 and 2017 at the Leiden University Medical Center, The Netherlands. Neurological, motor, cognitive and Conclusion Surviving donor twins of pregnancies com- behavioral development were assessed at a median age plicated by spontaneous TAPS have four-fold higher odds of 4 years. The primary outcome was NDI, which was a of NDI compared with recipient cotwins, are at increased composite outcome of cerebral palsy, deafness, blindness risk of cognitive delay and have a high rate of deafness. and motor and/or cognitive delay. NDI was subdivided Copyright © 2019 ISUOG. Published by John Wiley & into two grades of severity: mild-to-moderate and severe Sons Ltd. Correspondence to: Ms L. S. A. Tollenaar, Department of Obstetrics, Leiden University Medical Center, Room J6-150, Zone J6-S, Albinusdreef 2, 2333 ZA, Leiden, The Netherlands (e-mail: [email protected]) Accepted: 9 August 2019 Copyright © 2019 ISUOG. Published by John Wiley & Sons Ltd. ORIGINAL PAPER 40 Tollenaar et al. INTRODUCTION median (MoM), which is suggestive of the imbalanced chronic fetofetal transfusion leading to fetal anemia and Twin anemia–polycythemia sequence (TAPS) is a form polycythemia. Postnatal diagnosis was based on a large of chronic imbalanced fetofetal transfusion through (> 8 g/dL) intertwin difference in hemoglobin with at minuscule placental anastomoses in monochorionic twin least one of the following criteria: reticulocyte count pregnancies, leading to anemia in the donor twin and ratio > 1.7 and the presence of only minuscule (diameter polycythemia in the recipient twin1. Unlike twin-to-twin < 1 mm) anastomoses at the placental surface, detected transfusion syndrome (TTTS), TAPS is not associated with by color dye injection7. TAPS was classified antenatally amniotic fluid discordance. TAPS occurs spontaneously in and postnatally from stages 1 to 5, in accordance with the 3–5% of monochorionic twin pregnancies (spontaneous previously published staging systems for TAPS6,8. TAPS) and can develop iatrogenically due to residual The following perinatal data were retrieved from our anastomoses in 2–16% of pregnancies treated with databases: gestational age at diagnosis, antenatal TAPS laser surgery for TTTS (post-laser TAPS)2,3. While the stage, antenatal treatment, gestational age at birth, sex, optimal antenatal management for TAPS is not known, birth weight, small-for-gestational age (SGA; birth weight management options include expectant management, < 10th percentile) or fetal growth restriction (FGR; birth induced preterm delivery, intrauterine blood transfusion rd (IUT) with or without partial exchange transfusion (PET), weight < 3 centile), according to the charts of Hoftiezer 9 fetoscopic laser coagulation of the placental anastomoses et al. , severe fetal anemia, hemoglobin and reticulocyte and selective feticide. values at birth, need for blood transfusion or partial Short-term outcome of TAPS varies from isolated exchange transfusion 1 day after delivery, severe neonatal hemoglobin differences to severe cerebral injury and morbidity, severe cerebral injury and perinatal death. neonatal death4. Due to an increasing number of Severe fetal anemia was defined as the need for IUT, fetal monochorionic twins being liveborn after a complicated MCA-PSV value > 1.7 MoM or need for blood transfu- pregnancy, attention is shifting from short-term perinatal sion at birth. Severe neonatal morbidity was defined as the outcome to long-term neurodevelopmental outcome, presence of at least one of the following conditions: respi- focusing more on survival without impairment and on ratory distress syndrome requiring mechanical ventilation quality of life. Only one previous study in a cohort of or surfactant, patent ductus arteriosus requiring medical post-laser TAPS twins evaluated the long-term outcome therapy or surgical closure, necrotizing enterocolitis grade of TAPS, and showed that severe neurodevelopmental ≥ 210, or severe cerebral injury. Severe cerebral injury was impairment (NDI) occurs in 9% of survivors5. However, diagnosed in cases with one of the following abnormalities in spontaneous TAPS, the long-term neurodevelopmental detected on cerebral imaging: intraventricular hemor- outcome is unknown, which hampers adequate parent rhage grade ≥ 311, cystic periventricular leukomalacia counseling. Moreover, knowledge of the long-term grade ≥ 212, ventricular dilatation ≥ 97th percentile13, outcome is of paramount importance for designing porencephalic cysts, or arterial or venous infarction. future randomized controlled trials to determine the best A follow-up appointment was scheduled at a minimum treatment option for TAPS. age of 24 months and consisted of a neurological and The aims of the current study were to evaluate cognitive assessment and a behavioral questionnaire. long-term neurodevelopmental and behavioral outcomes Cognitive development was assessed using three stan- in a large cohort of children of pregnancies complicated by dardized psychometric age-appropriate tests, providing spontaneous TAPS, to compare outcome between donors cognitive scores with a normal distribution with a mean and recipients and to identify potential risk factors for of 100 and SD of 15. For children aged 2–3 years, NDI. the Dutch version of the Bayley Scales of Infant and Toddler Development, third edition (Bayley-III-NL)14, was used. For those aged between 3 and 6 years, the METHODS Wechsler Preschool and Primary Scale of Intelligence, 15 All consecutive monochorionic twin pregnancies with third edition (WPPSI-III-NL) , was used. For children spontaneous TAPS evaluated at our center between aged 7 years or older, the Wechsler Intelligence Scale 16 2005 and 2017 were eligible for this study. The Leiden for Children, third edition (WISC-III-NL) , was used. University Medical Center (LUMC) is the national referral To investigate behavioral problems, parents completed center for complicated twin pregnancies and fetal therapy. the Child’s Behavior Checklist (CBCL) for 1.5–5 years The study was approved by the institutional ethics review or 6–18 years, as appropriate17,18.Incasesinwhichthe board and all parents gave written informed consent child presented with hearing loss, vision loss or cerebral for their children to participate. Monochorionic twin palsy, additional medical information from our center or pregnancies identified as having TAPS antenatally and/or peripheral hospitals was requested to determine the grade postnatally were eligible for inclusion. Antenatal diagnosis of severity of the impairment. Maternal educational level was based
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