Twin Anemia-Polycythemia Sequence (TAPS): From Basic Research to
Clinical Practice

Joana      da Silva Rocha; Luís      Guedes-Martins; Ana      Cunha
Abstract

Twin pregnancy is associated with an increased risk of perinatal and maternal complications, and early establishment of the chorionicity type defines this risk. In monochorionic (MC) pregnancies, the fetuses share the same placental mass and exhibit vascular anastomoses crossing the intertwin membrane, and the combination and pattern of anastomoses determine the primary clinical picture and occurrence of future complications.
Twin Anemia-Polycythemia Sequence (TAPS) was first described in 2006 after fetoscopic laser surgery in twin-to-twin transfusion syndrome (TTTS) twins, and in 2007, the first spontaneous cases were reported, recognizing TAPS as an individualized vascular identity in fetofetal transfusion syndromes. There are two types of TAPS: spontaneous (3-5%) and iatrogenic or postlaser (2-16%). TAPS consists of small diameter arteriovenous anastomoses (<1 mm) and low-rate, small-caliber AA anastomoses in the absence of amniotic fluid discordances. There are certain antenatal and postnatal diagnostic criteria, which have progressively evolved over time. New, additional secondary markers have been proposed, and their reliability is being studied. The best screening protocol for TAPS in MC twins is still a matter of debate.
This review provides a survey of the relevant literature on the epidemiology, vascular pathophysiology, underlying hemodynamic factors that regulate mismatched vascular connections, and diagnostic criteria of this condition. The aim is to increase awareness and knowledge about this recently identified and frequently unrecognized and misdiagnosed pathology.
Graphical Abstract

[1]
Santana D, Surita F, Cecatti J. Multiple pregnancy: Epidemiology and association with maternal and perinatal morbidity. Rev Bras Ginecol Obstet  2018; 40(9): 554-62.
 [http://dx.doi.org/10.1055/s-0038-1668117] [PMID:  30231294]

[2]
Murray SR, Stock SJ, Cowan S, Cooper ES, Norman JE. Spontaneous preterm birth prevention in multiple pregnancy. Obstet Gynaecol  2018; 20(1): 57-63.
 [http://dx.doi.org/10.1111/tog.12460] [PMID:  30008614]

[3]
Resnik RL, Moore CJ, Greene TR, Copel MF. Creasy and resnik’s maternal-fetal medicine: Principles and practice. In: Multiple Gestation: Clinical Characteristics and Management.  Elsevier Inc. 2020; pp. 654-675.e5.

[4]
Paepe MED. Examination of the twin placenta. Semin Perinatol  2015; 39(1): 27-35.
 [http://dx.doi.org/10.1053/j.semperi.2014.10.005] [PMID:  25455620]

[5]
Hubinont C, Lewi L, Bernard P, Marbaix E, Debiève F, Jauniaux E. Anomalies of the placenta and umbilical cord in twin gestations. Am J Obstet Gynecol  2015; 213(4): S91-S102.
 [http://dx.doi.org/10.1016/j.ajog.2015.06.054] [PMID:  26428508]

[6]
Miller JL. Twin to twin transfusion syndrome. Transl Pediatr  2021; 10(5): 1518-29.
 [http://dx.doi.org/10.21037/tp-20-264] [PMID:  34189110]

[7]
Verbeek L, Slaghekke F, Sueters M, et al. Hematological disorders at birth in complicated monochorionic twins. Expert Rev Hematol  2017; 10(6): 525-32.
 [http://dx.doi.org/10.1080/17474086.2017.1324290] [PMID:  28460542]

[8]
Sueters M, Oepkes D. Diagnosis of twin-to-twin transfusion syndrome, selective fetal growth restriction, twin anaemia-polycythaemia sequence, and twin reversed arterial perfusion sequence. Best Pract Res Clin Obstet Gynaecol  2014; 28(2): 215-26.
 [http://dx.doi.org/10.1016/j.bpobgyn.2013.12.002] [PMID:  24433823]

[9]
Baschat A, Oepkes D. Twin anemia-polycythemia sequence in monochorionic twins: Implications for diagnosis and treatment. Am J Perinatol  2014; 31 (Suppl. 1): S25-30.
 [http://dx.doi.org/10.1055/s-0034-1376391] [PMID:  24858317]

[10]
Arts NFT, Lohman AHM. The vascular anatomy of monochorionic diamniotic twin placentas and the transfusion syndrome. Eur J Obstet Gynecol  1971; 1(3): 85-93.
 [http://dx.doi.org/10.1016/0028-2243(71)90055-4]

[11]
Lewi L, Jani J, Blickstein I, et al. The outcome of monochorionic diamniotic twin gestations in the era of invasive fetal therapy: A prospective cohort study. Am J Obstet Gynecol  2008; 199(5): 514.e1-8.
 [http://dx.doi.org/10.1016/j.ajog.2008.03.050] [PMID:  18533114]

[12]
Gucciardo L, Lewi L, Vaast P, et al. Twin anemia polycythemia sequence from a prenatal perspective. Prenat Diagn  2010; 30(5): 2491.
 [http://dx.doi.org/10.1002/pd.2491] [PMID:  20373492]

[13]
Machin GA, Feldstein VA, Van Gemert MJC, Keith LG, Hecher K. Doppler sonographic demonstration of arterio-venous anastomosis in monochorionic twin gestation. Ultrasound Obs Gynecol  2000; 16(3): 214-7.
 [http://dx.doi.org/10.1046/j.1469-0705.2000.00231.x] [PMID:  11169284]

[14]
Lewi L, Deprest J, Hecher K. The vascular anastomoses in monochorionic twin pregnancies and their clinical consequences. Am J Obstet Gynecol  2013; 208(1): 19-30.
 [http://dx.doi.org/10.1016/j.ajog.2012.09.025] [PMID:  23103301]

[15]
van den Wijngaard JPHM, van Gemert MJC, Lopriore E, Vandenbussche FPHA, Nikkels PGJ, VanBavel E. Case report: twin-to-twin transfusion syndrome resulting from placental collateral artery development. Placenta  2008; 29(2): 220-3.
 [http://dx.doi.org/10.1016/j.placenta.2007.10.013] [PMID:  18068761]

[16]
Tollenaar LSA, Lopriore E, Oepkes D, Haak MC, Klumper FJCM, Middeldorp JM. Twin anemia polycythemia sequence: Knowledge and insights after 15 years of research. Maternal-Fetal Med  2021; 3(1): 33-41.

[17]
Lopriore E, Middeldorp JM, Oepkes D, Kanhai HH, Walther FJ, Vandenbussche FPHA. Twin anemia-polycythemia sequence in two monochorionic twin pairs without oligo-polyhydramnios sequence. Placenta  2007; 28(1): 47-51.
 [http://dx.doi.org/10.1016/j.placenta.2006.01.010] [PMID:  16516289]

[18]
de Paepe ME, Luks FI. What-and why-the pathologist should know about twin-to-twin transfusion syndrome. Pediatr Dev Pathol  2013; 16(4): 237-51.
 [http://dx.doi.org/10.2350/13-03-1315-MISC.1] [PMID:  23617829]

[19]
Zhao D, Lipa M, Wielgos M, et al. Comparison between monochorionic and dichorionic placentas with special attention to vascular anastomoses and placental share. Twin Res Hum Genet  2016; 19(3): 191-6.
 [http://dx.doi.org/10.1017/thg.2016.19] [PMID:  27068823]

[20]
Tollenaar LSA, Lopriore E, Middeldorp JM, et al. Prevalence of placental dichotomy, fetal cardiomegaly and starry‐sky liver in twin anemia–polycythemia sequence. Ultrasound Obstet Gynecol  2020; 56(3): 395-9.
 [http://dx.doi.org/10.1002/uog.21948] [PMID:  31856326]

[21]
Mabuchi A, Ishii K, Yamamoto R, et al. Clinical characteristics of monochorionic twins with large hemoglobin level discordance at birth. Ultrasound Obstet Gynecol  2014; 44(3): 311-5.
 [http://dx.doi.org/10.1002/uog.13343] [PMID:  24585685]

[22]
Lopriore E, Holtkamp N, Sueters M, Middeldorp JM, Walther FJ, Oepkes D. Acute peripartum twin-twin transfusion syndrome: Incidence, risk factors, placental characteristics and neonatal outcome. J Obstet Gynaecol Res  2014; 40(1): 18-24.
 [http://dx.doi.org/10.1111/jog.12114] [PMID:  23876159]

[23]
Nicholas L, Fischbein R, Aultman J, Ernst-Milner S. Dispelling myths about antenatal TAPS: A call for action for routine MCA-PSV doppler screening in the United States. J Clin Med  2019; 8(7): 977.
 [http://dx.doi.org/10.3390/jcm8070977] [PMID:  31277521]

[24]
Slaghekke F, Kist WJ, Oepkes D, et al. Twin anemia-polycythemia sequence: diagnostic criteria, classification, perinatal management and outcome. Fetal Diagn Ther  2010; 27(4): 181-90.
 [http://dx.doi.org/10.1159/000304512] [PMID:  20339296]

[25]
Couck I, Lewi L. The placenta in twin-to-twin transfusion syndrome and twin anemia polycythemia sequence. Twin Res Hum Genet  2016; 19(3): 184-90.
 [http://dx.doi.org/10.1017/thg.2016.29] [PMID:  27098457]

[26]
Lopriore E, Deprest J, Slaghekke F, et al. Placental characteristics in monochorionic twins with and without twin anemia-polycythemia sequence. Obstet Gynecol  2008; 112(4): 753-8.
 [http://dx.doi.org/10.1097/AOG.0b013e318187e1ff] [PMID:  18827116]

[27]
Zhao DP, Peeters SHP, Middeldorp JM, et al. Monochorionic placentas with proximate umbilical cord insertions: Definition, prevalence and angio-architecture. Placenta  2015; 36(2): 221-5.
 [http://dx.doi.org/10.1016/j.placenta.2014.11.016] [PMID:  25499682]

[28]
Tollenaar LSA, Slaghekke F, Lewi L, Ville Y, Lanna M, Weingertner A. Treatment and outcome of 370 cases with spontaneous or post-laser twin anemia-polycythemia sequence managed in 17 fetal therapy centers. Ultrasound Obstet Gynecol  2020; 56(3): 378-87.
 [http://dx.doi.org/10.1002/uog.22042]

[29]
Liu B, Kalafat E, Bhide A, Thilaganathan B, Khalil A. Performance of antenatal diagnostic criteria of twin-anemia-polycythemia sequence. J Clin Med  2020; 9(9): 1-12.

[30]
Han SJ, Lee SM, Oh S, et al. Short- and long-term outcomes of preterm spontaneous twin anemia-polycythemia sequence. J Perinat Med  2020; 48(4): 329-34.
 [http://dx.doi.org/10.1515/jpm-2019-0437] [PMID:  32229695]

[31]
Tollenaar LSA, Slaghekke F, Middeldorp JM, et al. Twin anemia polycythemia sequence: Current views on pathogenesis, diagnostic criteria, perinatal management, and outcome. Twin Res Hum Genet  2016; 19(3): 222-33.
 [http://dx.doi.org/10.1017/thg.2016.18] [PMID:  27068715]

[32]
de Villiers SF, Slaghekke F, Middeldorp JM, Walther FJ, Oepkes D, Lopriore E. Arterio-arterial vascular anastomoses in monochorionic placentas with and without twin–twin transfusion syndrome. Placenta  2012; 33(8): 652-4.
 [http://dx.doi.org/10.1016/j.placenta.2012.05.003] [PMID:  22652047]

[33]
de Villiers SF, Slaghekke F, Middeldorp JM, Walther FJ, Oepkes D, Lopriore E. Placental characteristics in monochorionic twins with spontaneous versus post-laser twin anemia-polycythemia sequence. Placenta  2013; 34(5): 456-9.
 [http://dx.doi.org/10.1016/j.placenta.2013.02.005] [PMID:  23481221]

[34]
Tollenaar LSA, Lopriore E, Faiola S, et al. Post-laser twin anemia polycythemia sequence: Diagnosis, management, and outcome in an international cohort of 164 cases. J Clin Med  2020; 9(6): 1759.
 [http://dx.doi.org/10.3390/jcm9061759] [PMID:  32517071]

[35]
Tollenaar LSA, Lopriore E, Middeldorp JM, Haak MC, Klumper FJ, Oepkes D. Improved prediction of twin anemia-polycythemia sequence by delta middle cerebral artery peak systolic velocity: New antenatal classification system. Ultrasound Obstet Gynecol  2019; 53: 788-93.
 [http://dx.doi.org/10.1002/uog.20096]

[36]
Tavares de Sousa M, Fonseca A, Hecher K. Role of fetal intertwin difference in middle cerebral artery peak systolic velocity in predicting neonatal twin anemia–polycythemia sequence. Ultrasound Obstet Gynecol  2019; 53(6)uog.20116; 
 [http://dx.doi.org/10.1002/uog.20116] [PMID: 30207009]

[37]
Tollenaar LSA, Zhao DP, Middeldorp JM, Oepkes D, Slaghekke F, Lopriore E. Can color difference on the maternal side of the placenta distinguish between acute peripartum twin–twin transfusion syndrome and twin anemia–polycythemia sequence? Placenta  2017; 57: 189-93.
 [http://dx.doi.org/10.1016/j.placenta.2017.07.008] [PMID:  28864011]

[38]
Glennon CL, Shemer SA, Palma-Dias R, Umstad MP. The history of treatment of twin-to-twin transfusion syndrome. Twin Res Hum Genet  2016; 19(3): 168-74.
 [http://dx.doi.org/10.1017/thg.2016.27] [PMID:  27203604]

[39]
Berger HM, de Waard F, Molenaar Y. A case of twin-to-twin transfusion in 1617. Lancet  2000; 356(9232): 847-8.
 [http://dx.doi.org/10.1016/S0140-6736(00)02665-9] [PMID:  11022944]

[40]
Slaghekke F, Zhao DP, Middeldorp JM, et al. Antenatal management of twin-twin transfusion syndrome and twin anemia-polycythemia sequence. Expert Rev Hematol  2016; 9(8): 815-20.
 [http://dx.doi.org/10.1080/17474086.2016.1200968] [PMID:  27322562]

[41]
Slaghekke F, Pasman S, Veujoz M, et al. Middle cerebral artery peak systolic velocity to predict fetal hemoglobin levels in twin anemia-polycythemia sequence. Ultrasound Obstet Gynecol  2015; 46(4): 432-6.
 [http://dx.doi.org/10.1002/uog.14925] [PMID:  26094734]

[42]
Mari G. Middle cerebral artery peak systolic velocity for the diagnosis of fetal anemia: the untold story. Ultrasound Obstet Gynecol  2005; 25(4): 323-30.
 [http://dx.doi.org/10.1002/uog.1882] [PMID:  15789353]

[43]
Brock CO, Bergh EP, Moise KJ Jr, et al. Middle cerebral artery doppler velocimetry for the diagnosis of twin anemia polycythemia sequence: A systematic review. J Clin Med  2020; 9(6): 1735.
 [http://dx.doi.org/10.3390/jcm9061735] [PMID:  32512796]

[44]
Khalil A, Gordijn S, Ganzevoort W, et al. Consensus diagnostic criteria and monitoring of twin anemia–polycythemia sequence: Delphi procedure. Ultrasound Obstet Gynecol  2020; 56(3): 388-94.
 [http://dx.doi.org/10.1002/uog.21882] [PMID:  31605505]

[45]
Robyr R, Lewi L, Salomon LJ, et al. Prevalence and management of late fetal complications following successful selective laser coagulation of chorionic plate anastomoses in twin-to-twin transfusion syndrome. Am J Obstet Gynecol  2006; 194(3): 796-803.
 [http://dx.doi.org/10.1016/j.ajog.2005.08.069] [PMID:  16522415]

[46]
Lucewicz A, Fisher K, Henry A, Welsh AW, Welsh AW. Review of the correlation between blood flow velocity and polycythemia in the fetus, neonate and adult: Appropriate diagnostic levels need to be determined for twin anemia polycythemia sequence. Ultrasound Obs Gynecol  2016; 47: 152-7.

[47]
Yokouchi T, Murakoshi T, Mishima T, et al. Incidence of spontaneous twin anemia-polycythemia sequence in monochorionic-diamniotic twin pregnancies: Single-center prospective study. J Obstet Gynaecol Res  2015; 41(6): 857-60.
 [http://dx.doi.org/10.1111/jog.12641] [PMID:  25510181]

[48]
Lopriore E, Slaghekke F, Middeldorp JM, Klumper FJ, Oepkes D, Vandenbussche FP. Residual anastomoses in twin-to-twin transfusion syndrome treated with selective fetoscopic laser surgery: localization, size, and consequences. Am J Obstet Gynecol  2009; 201(1): 66.e1-4.
 [http://dx.doi.org/10.1016/j.ajog.2009.01.010] [PMID:  19306965]

[49]
Habli M, Bombrys A, Lewis D, et al. Incidence of complications in twin-twin transfusion syndrome after selective fetoscopic laser photocoagulation: a single-center experience. Am J Obstet Gynecol  2009; 201(4): 417.e1-7.
 [http://dx.doi.org/10.1016/j.ajog.2009.07.046] [PMID:  19788973]

[50]
Slaghekke F, Lopriore E, Lewi L, et al. Fetoscopic laser coagulation of the vascular equator versus selective coagulation for twin-to-twin transfusion syndrome: an open-label randomised controlled trial. Lancet  2014; 383(9935): 2144-51.
 [http://dx.doi.org/10.1016/S0140-6736(13)62419-8] [PMID:  24613024]

[51]
Weingertner AS, Kohler A, Kohler M, Bouffet N, Hunsinger MC, Mager C. Clinical and placental characteristics in four new cases of twin anemia-polycythemia sequence. Ultrasound Obstet Gynecol  2010; 35(4): 490-4.
 [http://dx.doi.org/10.1002/uog.7508]

[52]
Bae JY, Oh JJ, Hong SY. Prenatal diagnosis of spontaneous twin anemia-polycythemia sequence and postnatal examination of placental vascular anastomoses. Obstet Gynecol Sci  2016; 59(6): 539-43.
 [http://dx.doi.org/10.5468/ogs.2016.59.6.539] [PMID:  27896259]

[53]
Donepudi R, Papanna R, Snowise S, Johnson A, Bebbington M, Moise KJ Jr. Does anemia-polycythemia complicating twin-twin transfusion syndrome affect outcome after fetoscopic laser surgery? Ultrasound Obstet Gynecol  2016; 47(3): 340-4.
 [http://dx.doi.org/10.1002/uog.14913] [PMID:  26033705]

[54]
Lopriore E, Middeldorp JM, Oepkes D, Klumper FJ, Walther FJ, Vandenbussche FPHA. Residual anastomoses after fetoscopic laser surgery in twin-to-twin transfusion syndrome: Frequency, associated risks and outcome. Placenta  2007; 28(2-3): 204-8.

[55]
Tollenaar LSA, Slaghekke F, Lewi L, Colmant C. Spontaneous twin anemia polycythemia sequence: diagnosis, management, and outcome in an international cohort of 249 cases. Am J Obstet Gynecol  2021; 224(2): 213.

[56]
Bajoria R, Wigglesworth J, Fisk NM. Angioarchitecture of monochorionic placentas in relation to the twin-twin transfusion syndrome. Am J Obstet Gynecol  1995; 172(3): 856-63.
 [http://dx.doi.org/10.1016/0002-9378(95)90011-X] [PMID:  7892875]

[57]
De Paepe ME, Shapiro S, Hanley LC, Chu S, Luks FI. Correlation between cord insertion type and superficial choriovasculature in diamniotic-monochorionic twin placentas. Placenta  2011; 32(11): 901-5.
 [http://dx.doi.org/10.1016/j.placenta.2011.08.001] [PMID:  21864904]

[58]
Slaghekke F, Kist WJ, Oepkes D, Middeldorp JM, Klumper FJ, Vandenbussche FPHA. TAPS and TOPS: Two distinct forms of feto-fetal transfusion in monochorionic twins. Z Geburtshilfe Neonatol  2009; 213(6): 248-54.

[59]
Zhao D, De Villiers SF, Oepkes D, Lopriore E. Monochorionic twin placentas: Injection technique and analysis. Diagnostico Prenat  2014; 25(2): 35-42.

[60]
Lanna MM, Consonni D, Faiola S, et al. Color-dye injection of monochorionic placentas and correlation with pregnancy complications. Placenta  2015; 36(10): 1095-9.
 [http://dx.doi.org/10.1016/j.placenta.2015.07.129] [PMID:  26278056]

[61]
Lopriore E, Slaghekke F, Middeldorp JM, et al. Accurate and simple evaluation of vascular anastomoses in monochorionic placenta using colored dye. J Vis Exp  2011; (55): e3208.
 [http://dx.doi.org/10.3791/3208] [PMID:  21912373]

[62]
De Paepe ME, DeKoninck P, Friedman RM. Vascular distribution patterns in monochorionic twin placentas. Placenta  2005; 26(6): 471-5.
 [http://dx.doi.org/10.1016/j.placenta.2004.06.014]

[63]
Chandrashekhar Veerabhadrappa H. Study of the vascular organization of the placenta. Int J Heal Sci Res  2013; 3(4): 35.

[64]
Nikkels PGJ, Hack KEA, van Gemert MJC. Pathology of twin placentas with special attention to monochorionic twin placentas. J Clin Pathol  2008; 61(12): 1247-53.
 [http://dx.doi.org/10.1136/jcp.2008.055210] [PMID:  18794196]

[65]
Denbow ML, Cox P, Taylor M, Hammal DM, Fisk NM. Placental angioarchitecture in monochorionic twin pregnancies: Relationship to fetal growth, fetofetal transfusion syndrome, and pregnancy outcome. Am J Obstet Gynecol  2000; 182(2): 417-26.
 [http://dx.doi.org/10.1016/S0002-9378(00)70233-X] [PMID:  10694346]

[66]
De Paepe ME, Shapiro S, Greco D, et al. Placental markers of twin-to-twin transfusion syndrome in diamniotic–monochorionic twins: A morphometric analysis of deep artery-to-vein anastomoses. Placenta  2010; 31(4): 269-76.
 [http://dx.doi.org/10.1016/j.placenta.2009.12.024] [PMID:  20064658]

[67]
van Gemert MJC, Sterenborg HJCM. Haemodynamic model of twin-twin transfusion syndrome in monochorionic twin pregnancies. Placenta  1998; 19(2-3): 195-208.
 [http://dx.doi.org/10.1016/S0143-4004(98)90009-1] [PMID:  9548187]

[68]
Umur A, Van Gemert MJC, Nikkels PGJ, Ross MG. Monochorionic twins and twin–twin transfusion syndrome: The protective role of arterio-arterial anastomoses. Placenta  2002; 23(2-3): 201-9.

[69]
van Meir H, Slaghekke F, Lopriore E, van Wijngaarden WJ. Arterio-arterial anastomoses do not prevent the development of twin anemia-polycythemia sequence. Placenta  2010; 31(2): 163-5.
 [http://dx.doi.org/10.1016/j.placenta.2009.11.009] [PMID:  19962758]

[70]
Bermúdez C, Becerra CH, Bornick PW, Allen MH, Arroyo J, Quintero RA. Placental types and twin-twin transfusion syndrome. Am J Obstet Gynecol  2002; 187(2): 489-94.
 [http://dx.doi.org/10.1067/mob.2002.124280] [PMID:  12193948]

[71]
Zhao DP, Cohen D, Middeldorp JM, et al. The role of veno-venous anastomoses in twin–twin transfusion syndrome. Placenta  2014; 35(5): 334-6.
 [http://dx.doi.org/10.1016/j.placenta.2014.03.002] [PMID:  24680292]

[72]
de Villiers S, Slaghekke F, Middeldorp JM, et al. Arterio-arterial vascular anastomoses in monochorionic twin placentas with and without twin anemia-polycythemia sequence. Placenta  2012; 33(3): 227-9.
 [http://dx.doi.org/10.1016/j.placenta.2012.01.009] [PMID:  22257747]

[73]
Sobreira I, Sousa C, Paiva C, Freitas S, Proença E, Carvalho C. Twin anemia-polycythemia sequence: The importance of an accurate diagnosis. Case Reports Perinat Med  2014; 3(2): 143-6.
 [http://dx.doi.org/10.1515/crpm-2013-0051]

[74]
Zhao DP, De Villiers SF, Slaghekke F, Walther FJ, Middeldorp JM, Oepkes D. Prevalence, size, number and localization of vascular anastomoses in monochorionic placentas. Placenta  2013; 34(7): 589-93.
 [http://dx.doi.org/10.1016/j.placenta.2013.04.005]

[75]
Favre R, Koch A, Weingertner AS, et al. Vascular pattern in monochorionic placentas with spontaneous TAPS and TTTS with residual anastomoses after laser: a case-control study. Prenat Diagn  2013; 33(10): 979-82.
 [http://dx.doi.org/10.1002/pd.4177] [PMID:  23744723]

[76]
Zhao D, Slaghekke F, Middeldorp JM, Duan T, Oepkes D, Lopriore E. Placental share and hemoglobin level in relation to birth weight in twin anemia-polycythemia sequence. Placenta  2014; 35(12): 1070-4.
 [http://dx.doi.org/10.1016/j.placenta.2014.09.019] [PMID:  25449031]

[77]
Verbeek L, Slaghekke F, Hulzebos CV, Oepkes D, Walther FJ, Lopriore E. Hypoalbuminemia in donors with twin anemia-polycythemia sequence: a matched case-control study. Fetal Diagn Ther  2013; 33(4): 241-5.
 [http://dx.doi.org/10.1159/000345716] [PMID:  23485951]

[78]
Diehl W, Glosemeyer P, Tavares De Sousa M, Hollwitz B, Ortmeyer G, Hecher K. Twin anemia-polycythemia sequence in a case of monoamniotic twins. Ultrasound Obstet Gynecol  2013; 42(1): 108-11.
 [http://dx.doi.org/10.1002/uog.12418] [PMID:  23361996]

[79]
Rossi AC, Prefumo F. Perinatal outcomes of twin anemia-polycythemia sequence: a systematic review. J Obstet Gynaecol Can  2014; 36(8): 701-7.
 [http://dx.doi.org/10.1016/S1701-2163(15)30512-0] [PMID:  25222165]

[80]
LeGallo R. Placental Vasculogenesis/Angiogenesis. In: Pathobiology of Human Disease: A Dynamic Encyclopedia of Disease Mechanisms. Amsterdam: Elsevier Inc. 2014.
 [http://dx.doi.org/10.1016/B978-0-12-386456-7.05003-6]

[81]
Chen D, Zheng J. Regulation of placental angiogenesis. Microcirculation  2014; 21(1): 15-25.
 [http://dx.doi.org/10.1111/micc.12093] [PMID:  23981199]

[82]
Reynolds LP, Redmer DA. Angiogenesis in the placenta1. Biol Reprod  2001; 64(4): 1033-40.
 [http://dx.doi.org/10.1095/biolreprod64.4.1033] [PMID:  11259247]

[83]
Anh ND, Thuong PH, Sim NT, Thao TTP, Anh LTL, Canh TTT. Maternal vascular endothelial growth factor receptor and interleukin levels in pregnant women with twin-twin transfusion syndrome. Int J Med Sci  2021; 18(14): 3206-13.
 [http://dx.doi.org/10.7150/ijms.61014]

[84]
Fox CE, Lash GE, Pretlove SJ, Chan BC, Holder R, Kilby MD. Maternal plasma and amniotic fluid angiogenic factors and their receptors in monochorionic twin pregnancies complicated by twin-to-twin transfusion syndrome. Ultrasound Obstet Gynecol  2010; 35: 695-701.
 [http://dx.doi.org/10.1002/uog.7515]

[85]
Yinon Y, Ben Meir E, Berezowsky A, et al. Circulating angiogenic factors in monochorionic twin pregnancies complicated by twin-to-twin transfusion syndrome and selective intrauterine growth restriction. Am J Obstet Gynecol  2014; 210(2): 141.e1-7.
 [http://dx.doi.org/10.1016/j.ajog.2013.09.022] [PMID:  24055584]

[86]
Mao Q, Chu S, Shapiro S, Yao H, De Paepe ME. Discordant placental oxygenation and autophagy in twin anemia-polycythemia sequence (TAPS). Placenta  2020; 90(90): 9-17.
 [http://dx.doi.org/10.1016/j.placenta.2019.11.003] [PMID:  32056557]

[87]
Tamanna S, Lumbers ER, Morosin SK, Delforce SJ, Pringle KG. ACE2: a key modulator of the renin-angiotensin system and pregnancy. Am J Physiol Regul Integr Comp Physiol  2021; 321(6): R833-43.
 [http://dx.doi.org/10.1152/ajpregu.00211.2021] [PMID:  34668428]

[88]
Mao Q, Chu S, Shapiro S, Bliss JM, De Paepe ME. Increased placental expression of angiotensin-converting enzyme 2, the receptor of SARS-CoV-2, associated with hypoxia in twin anemia-polycythemia sequence (TAPS). Placenta  2021; 105: 7-13.
 [http://dx.doi.org/10.1016/j.placenta.2021.01.008] [PMID:  33497931]

[89]
Fishel-Bartal M, Weisz B, Mazaki-Tovi S, et al. Can middle cerebral artery peak systolic velocity predict polycythemia in monochorionic-diamniotic twins? Evidence from a prospective cohort study. Ultrasound Obstet Gynecol  2016; 48(4): 470-5.
 [http://dx.doi.org/10.1002/uog.15838] [PMID:  26663574]

[90]
Slaghekke F, Tollenaar L, Middeldorp A, et al. 460: Additional value of delta MCA-PSV to predict TAPS. Am J Obstet Gynecol  2018; 218(1): S277-8.
 [http://dx.doi.org/10.1016/j.ajog.2017.10.396]

[91]
Moaddab A, Nassr AA, Espinoza J, et al. Twin anemia polycythemia sequence: a single center experience and literature review. Eur J Obstet Gynecol Reprod Biol  2016; 205: 158-64.
 [http://dx.doi.org/10.1016/j.ejogrb.2016.08.033] [PMID:  27597647]

[92]
Brock CO, Bergh EP, Johnson A, Lai D, Papanna R. 858 Secondary sonographic markers for diagnosis of twin anemia polycythemia sequence (TAPS). Am J Obstet Gynecol  2021; 224(2): S533.
 [http://dx.doi.org/10.1016/j.ajog.2020.12.881] [PMID:  32835718]

[93]
Nicholas L, Fischbein R, Ernst-Milner S, Wani R. Review of international clinical guidelines related to prenatal screening during monochorionic pregnancies. J Clin Med  2021; 10(5): 1128.
 [http://dx.doi.org/10.3390/jcm10051128] [PMID:  33800344]

[94]
Stritzke A, Thomas S, Somerset D. Placental dichotomy: a hint in twin anemia polycythemia sequence. J Obstet Gynaecol Can  2014; 36(12): 1097-100.
 [http://dx.doi.org/10.1016/S1701-2163(15)30388-1] [PMID:  25668046]

[95]
Bamberg C, Diemert A, Glosemeyer P, Hecher K. Quantified discordant placental echogenicity in twin anemia-polycythemia sequence (TAPS) and middle cerebral artery peak systolic velocity. Ultrasound Obs Gynecol  2018; 52: 373-7.

[96]
Soundararajan LP, Howe DT. Starry sky liver in twin anemia-polycythemia sequence. Ultrasound Obstet Gynecol  2014; 43(5): 597-9.
 [http://dx.doi.org/10.1002/uog.13276]

[97]
Nicolaides KH, Thilaganathan B, Mibashan RS. Cordocentesis in the investigation of fetal erythropoiesis. Am J Obstet Gynecol  1989; 161(5): 1197-200.
 [http://dx.doi.org/10.1016/0002-9378(89)90664-9] [PMID:  2589439]

[98]
Lopriore E, Slaghekke F, Oepkes D, Middeldorp JM, Vandenbussche FPHA, Walther FJ. Hematological characteristics in neonates with twin anemia-polycythemia sequence (TAPS). Prenat Diagn  2010; 30(3): 251-5.
 [http://dx.doi.org/10.1002/pd.2453] [PMID:  20087909]

[99]
Slaghekke F, Van Klink JMM, Koopman HM, Middeldorp JM, Oepkes D, Lopriore E. Neurodevelopmental outcome in twin anemia polycythemia sequence after laser surgery for twin twin transfusion syndrome. Ultrasound Obs Gynecol  2014; 44(3): 316-21.

[100]
Kondo S, Sugita Y, Suzuki S. Hematological characteristics in neonates with twin-twin blood transfusion. J Med Cases  2017; 8(9): 269-70.
 [http://dx.doi.org/10.14740/jmc2882w]

[101]
Chen K, Kuhlmann R, Bell A, et al. Twin anemia–polycythemia sequence in sex‐discordant monochorionic dizygotic twins. Ultrasound Obstet Gynecol  2020; 56(3): 461-2.
 [http://dx.doi.org/10.1002/uog.22073] [PMID:  32395871]

[102]
Visser GL, Tollenaar LSA, Bekker V, et al. Leukocyte counts and other hematological values in twin-twin transfusion syndrome and twin anemia-polycythemia sequence. Fetal Diagn Ther  2020; 47(2): 123-8.
 [http://dx.doi.org/10.1159/000500859] [PMID:  31261154]

[103]
Zhao D, Tollenaar LSA, Slaghekke F, Oepkes D, Duan T, Lopriore E. Evaluation of color difference in placenta with twin anemia polycythemia sequence. J Vis Exp  2020; e61312(160): 1-11.

[104]
Tollenaar LSA, Zhao DP, Middeldorp JM, Slaghekke F, Oepkes D, Lopriore E. Color difference in placentas with twin anemia-polycythemia sequence: an additional diagnostic criterion? Fetal Diagn Ther  2016; 40(2): 123-7.
 [http://dx.doi.org/10.1159/000442154] [PMID:  26788848]

[105]
Tollenaar LSA, Prins SA, Beuger S, Slaghekke F, Oepkes D, Lopriore E. Twin anemia polycythemia sequence in a dichorionic twin pregnancy leading to severe cerebral injury in the recipient. Fetal Diagn Ther  2021; 48(4): 321-6.
 [http://dx.doi.org/10.1159/000514408]

[106]
Herway C, Johnson A, Moise K, Moise KJ Jr. Fetal intraperitoneal transfusion for iatrogenic twin anemia-polycythemia sequence after laser therapy. Ultrasound Obstet Gynecol  2009; 33(5): 592-4.
 [http://dx.doi.org/10.1002/uog.6334] [PMID:  19402103]

[107]
Zilliox M, Koch A, Favre R, Sananes N. Unusual twin anemia-polycythemia sequence in a dichorionic diamniotic pregnancy. J Gynecol Obstet Hum Reprod  2019; 48(5): 359-61.
 [http://dx.doi.org/10.1016/j.jogoh.2019.02.005] [PMID:  30794958]

[108]
Parodi E, Romano F, Ramenghi U. How We Use reticulocyte parameters in workup and management of pediatric hematologic diseases. Front Pediatr  2020; 8: 588617.
 [http://dx.doi.org/10.3389/fped.2020.588617] [PMID:  33344383]

[109]
Christensen RD, Henry E, Bennett ST, Yaish HM. Reference intervals for reticulocyte parameters of infants during their first 90 days after birth. J Perinatol  2016; 36(1): 61-6.
 [http://dx.doi.org/10.1038/jp.2015.140] [PMID:  26513452]

[110]
Lopriore E, Hecher K, Vandenbussche FPHA, van den Wijngaard JPHM, Klumper FJ, Oepkes D. Fetoscopic laser treatment of twin-to-twin transfusion syndrome followed by severe twin anemia-polycythemia sequence with spontaneous resolution. Am J Obstet Gynecol  2008; 198(2): e4-7.
 [http://dx.doi.org/10.1016/j.ajog.2007.08.073] [PMID:  18226611]

[111]
Lopriore E, Slaghekke F, Kersbergen KJ, De Vries LS, Drogtrop AP, Middeldorp JM. Severe cerebral injury in a recipient with twin anemia-polycythemia sequence. Ultrasound Obs Gynecol  2013; 41(6): 702-6.
 [http://dx.doi.org/10.1002/uog.12337]

[112]
Lopriore E, Slaghekke F, Oepkes D, Middeldorp JM, Vandenbussche FP, Walther FJ. Clinical outcome in neonates with twin anemia-polycythemia sequence. Am J Obstet Gynecol  2010; 203(1): 54.e1-5.
 [http://dx.doi.org/10.1016/j.ajog.2010.02.032] [PMID:  20417489]

[113]
Lorenz L, Peter A, Arand J, Springer F, Poets CF, Franz AR. Reference ranges of reticulocyte haemoglobin content in preterm and term infants: A retrospective analysis. Neonatology  2017; 111(3): 189-94.
Cite As
Current Vascular Pharmacology

Twin Anemia-Polycythemia Sequence (TAPS): From Basic Research to Clinical Practice

Abstract

Graphical Abstract
