perinatal outcomes of twin anemia-polycythemia sequence: a systematic review

AUGUST JOGC AOÛT 2014 l 701

OBSTETRICS

Key Words: Monochorionic pregnancy, twins, anemia polycythemia sequence, twin transfusion syndromes

Competing Interests: None declared .

Received on November 2, 2013

Accepted on February 12, 2014

Perinatal Outcomes of Twin Anemia– Polycythemia Sequence: A Systematic ReviewA. Cristina Rossi, MD,1 Federico Prefumo, MD, PhD2

1 Department of Obstetrics and Gynecology, University of Bari, Bari, Italy2 Maternal-Fetal Medicine Unit, Department of Obstetrics and Gynecology, University of Brescia, Brescia, Italy

J Obstet Gynaecol Can 2014;36(8):701–707

Abstract

Objective: To analyze outcomes of monochorionic twins with twin anemia-polycythemia sequence (TAPS) .

Data Sources: PubMed, EMBASE, Medline, and reference list .

Study Selection: We included reports of TAPS defined prenatally with abnormal Doppler studies of middle cerebral artery and normal amniotic fluid volume which reported data as proportional rates.

Data Extraction: Abstracted outcomes were postnatal hemoglobin levels, postnatal procedures, and survival rates . Outcomes were analyzed for gestational age at diagnosis of TAPS (15 to 23 weeks, 24 to 29 weeks, > 29 weeks), in utero therapy, and nature of onset (isolated TAPS, or following twin-to-twin transfusion syndrome) . The review was performed using MOOSE guidelines . Differences were significant if P < 0 .05 .

Data Synthesis: We assessed data on 28 pregnancies with TAPS . Diagnosis at 15 to 23 weeks’ gestation and in utero therapy were associated with the highest mean levels of hemoglobin in anemic twins (P = 0 .021), the lowest levels in polycythemic twins (P = 0 .025), and the lowest frequency of postnatal procedures (P < 0 .001) . Survival rate was independent of gestational age at diagnosis and in utero therapy . In cases of TAPS following twin-to-twin transfusion, the mean hemoglobin level was higher in donors than in anemic twins with isolated TAPS (P = 0 .029) and similar between recipients and polycythemic twins with isolated TAPS (P = 0 .135) . Twins with TAPS following twin-to-twin transfusion received in utero therapy more frequently than isolated TAPS twins (P = 0 .030) and required a postnatal procedure less often (P < 0 .001) . Survival rates were similar in each group .

Conclusion: Diagnosis of TAPS at an early gestational age is associated with more favourable outcomes than later diagnosis . In utero therapy improves neonatal hemoglobin levels but does not change survival rates . Previous twin-to-twin transfusion syndrome does not worsen outcomes .

Résumé

Objectif : Analyser les issues que connaissent les jumeaux monozygotes qui présentent une séquence anémie-polyglobulie gémellaire (twin anemia-polycythemia sequence ou TAPS) .

Sources de données : PubMed, EMBASE, Medline et liste de références .

Sélection des études : Nous avons inclus les études ayant porté sur la TAPS établie avant la naissance (obtention de résultats anormaux aux études Doppler visant l’artère cérébrale moyenne et constatation d’un volume normal de liquide amniotique) qui signalaient leurs données sous forme de taux proportionnels .

Extraction des données : Les issues résumées ont été les suivantes : taux postnataux d’hémoglobine, interventions postnatales et taux de survie . Les issues ont été analysées en fonction de l’âge gestationnel au moment du diagnostic de TAPS (15-23 semaines, 24-29 semaines, > 29 semaines), de la présence d’un traitement in utero et de la nature de l’apparition de la TAPS (TAPS isolée ou apparaissant à la suite du syndrome transfuseur-transfusé) . L’analyse a été menée au moyen des lignes directrices MOOSE . Les différences ont été considérées significatives lorsque P < 0,05.

Synthèse des données : Nous avons évalué des données portant sur 28 grossesses présentant une TAPS . Le diagnostic à 15-23 semaines de gestation et le traitement in utero ont été associés aux taux moyens d’hémoglobine les plus élevés chez les jumeaux anémiques (P = 0,021), aux taux moyens d’hémoglobine les plus bas chez les jumeaux présentant une polyglobulie (P = 0,025) et à la fréquence d’interventions postnatales la plus basse (P < 0,001) . Le taux de survie ne dépendait ni de l’âge gestationnel au moment du diagnostic ni de la présence d’un traitement in utero . Dans les cas de TAPS suivant le syndrome transfuseur-transfusé, le taux moyen d’hémoglobine était plus élevé chez les transfuseurs (par comparaison avec la situation constatée chez les jumeaux anémiques dans les cas de TAPS isolée [P = 0,029]) et il était semblable chez les transfusés (par comparaison avec la situation constatée chez les jumeaux présentant une polyglobulie dans les cas de TAPS isolée [P = 0,135]) . Les jumeaux présentant une TAPS constatée à la suite du syndrome transfuseur-transfusé ont reçu un traitement in utero plus fréquemment (P = 0,030) et ont nécessité une intervention postnatale moins souvent (P < 0,001) que les jumeaux présentant une TAPS isolée . Les taux de survie étaient semblables d’un groupe à l’autre .

Conclusion : L’établissement d’un diagnostic de TAPS à un âge gestationnel précoce est associé à des issues plus favorables que l’établissement d’un diagnostic de TAPS à un âge gestationnel plus tardif . L’administration d’un traitement in utero améliore les taux néonataux d’hémoglobine, mais ne modifie en rien les taux de survie. La présence d’un syndrome transfuseur-transfusé au préalable n’aggrave en rien les issues .

702 l AUGUST JOGC AOÛT 2014

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INTRODUCTION

Twin anemia-polycythemia sequence is a specific complication of monochorionic twin pregnancy. It

has been classified as isolated TAPS or TAPS associated with twin-to-twin transfusion syndrome. Both TAPS and TTTS are typical features of monochorionic pregnancies. TTTS is characterized by polyhydramnios in the recipient sac and oligohydramnios in the donor sac, whereas TAPS is characterized by polycythemia in the recipient and anemia in the donor twin, but amniotic fluid volume is normal in both sacs. These characteristics are used to distinguish between the two conditions. TAPS can occur in isolation or may arise when laser therapy for TTTS is followed by the persistence of vascular anastomoses, leading again to anemia and polycythemia but with normal amniotic fluid volumes.1 TAPS is diagnosed prenatally by Doppler measurement of the peak systolic velocity of the middle cerebral artery in each twin. PSV in the MCA > 1.5 MoM in one twin and < 0.8 MoM in the other are generally used to identify the anemic and polycythemic twin, respectively.2,3 Prenatal diagnosis is confirmed at birth by measurement of each neonate’s hemoglobin concentration, and thresholds of < 110 g/L and > 200 g/L are applied for diagnosis of anemia and polycythemia, respectively.4 Postnatal TAPS can be classified according to the criteria proposed by Lopriore, which are based on differences in Hb levels between twins.5 The incidence of TAPS in monochorionic pregnancies is estimated at 3% to 5% for the isolated forms4 and at 2% to 13% after laser therapy for TTTS.3 Because of the relatively low incidence, the literature is limited to the description of small series or case reports of twins affected by TAPS. The aim of this review was to collect and pool published case reports of perinatal outcomes of TAPS identified prenatally, in order to obtain a larger sample size.

METHODS

We searched PubMed, Embase, Medline, Clinicaltrials.org, and reference lists to identify articles that described perinatal outcomes of TAPS, from the inception of these databases to November 2012. Key words used in the search were twins, monochorionic pregnancies, twin anemia-polycythemia sequence, twin-to-twin transfusion syndrome, placental anastomoses, recurrent TTTS, fetal anemia, and fetal polycythemia. Each author independently selected articles, and discordance was resolved by consensus. The MOOSE guidelines were followed. This meta-analysis was based on case reports with raw data described for each case; the data were collected and pooled as a single large study. Where data were missing, we attempted to contact the corresponding author to obtain unpublished data. When more than one article was published by the same authors, we selected the article with the largest sample size in order to avoid overlap of population. Overlap of population was assessed according to the authors and institution where the study was performed and the year of publication.

Inclusion criteria for study selection were:

1. prenatal diagnosis of TAPS based on MCA-PSV > 1.5 MoM in one twin and < 0.8 MoM in the second with normal amniotic fluid volumes, and

2. confirmation of the diagnosis at birth with Hb levels < 110 g/L for the anemic twin and > 200 g/L for the polycythemic twin. Monoamniotic twin pregnancies were excluded.

Outcomes of interest were Hb concentration and reticulocyte count at birth, postnatal procedures, neonatal morbidity, and overall survival rates. Postnatal procedures comprised blood exchange in the polycythemic twin and blood transfusion in the anemic twin. Overall survival rate was defined as the number of survivors at least 28 days after birth. Outcomes were stratified according to gestational age at diagnosis of TAPS, performance of intrauterine therapy, mode of onset, and presence of patent vascular anastomoses on placental histological examination. Gestational age at diagnosis was arbitrarily divided into three intervals: 15 to 23 weeks, 24 to 29 weeks, and > 29 weeks. Intrauterine therapy included laser therapy of placental vascular anastomoses, blood transfusion by cordocentesis, and umbilical cord occlusion. The mode of onset consisted of isolated TAPS or TAPS associated with previous laser therapy for TTTS.

We used the Mann-Whitney U, Kruskall-Wallis, and Fisher exact test, as appropriate, in GraphPad Prism (GraphPad Software Inc., La Jolla CA) for statistical analysis. Statistical

ABBREVIATIONSaTAPS TAPS following TTTS

Hb hemoglobin

iTAPS isolated TAPS

MCA middle cerebral artery

MoM multiple of the median

MVP maximum vertical pocket

PSV peak systolic velocity

TAPS twin anemia-polycythemia sequence

TTTS twin-to-twin transfusion syndrome


Perinatal Outcomes of Twin Anemia–Polycythemia Sequence: A Systematic Review

significance was reached with two-sided P values < 0.05. We addressed quality issues in the description of studies and in the discussion of findings.

RESULTS

The steps taken for study selection are shown in the Figure. Of 36 articles retrieved for detailed evaluation, 10 articles were selected for inclusion in the analysis; these described 28 monochorionic twin pregnancies affected by TAPS (56 fetuses).1,3,6–13 The characteristics of each study are described in Table 1. Median gestational age at diagnosis was 24 weeks (range 15 to 33 weeks). In 17 pregnancies (61%), TAPS was diagnosed after laser treatment of TTTS. Intrauterine therapy was performed in 20 pregnancies (71%); this consisted of laser treatment of placental vascular anastomoses (4 cases, 20%), blood transfusion in the anemic twin by cordocentesis (13 cases, 65%), and umbilical cord occlusion for impending intrauterine death (3 cases, 15%).

At birth, the mean (± SD) Hb levels were 108.9 ± 54.4 g/L and 203.7 ± 46.2 g/L in the anemic and polycythemic twins, respectively. Blood exchange was required in seven polycythemic twins (30%) and blood transfusion was

required in nine anemic twins (39%). The overall survival rate was 82% (46/56); of these survivors, 50% (23/46) were the anemic twin and 50% (23/46) were the polycythemic twin. For each twin set, there were no survivors in 3% of pregnancies (1/28), one survivor in 28% (8/28), and two survivors in 68% (19/28). Neonatal morbidity affected five newborns (9%) and was represented by thrombocytopenia, neurologic disease, skin necrosis, mild hypotonia, and respiratory distress. In two cases, neonatal morbidity was fatal. Placental examination was performed in 11 of 28 pregnancies (39%) and revealed patent vascular anastomoses in seven (64%); two of these had previously undergone laser therapy for TTTS.

Diagnosis at 15 to 23 weeks’ gestation was associated with more normal Hb levels. When TAPS was diagnosed at > 29 weeks, conservative management was more likely than with earlier diagnosis, but postnatal procedures were more frequently performed. The overall survival rates did not differ according to gestational age at diagnosis (Table 2).

Comparison between TAPS treated in utero and TAPS managed conservatively showed that the former significantly improved Hb levels at birth and reduced the

Observational studies with usableinformation included in the

meta-analysisn = 10

Potentially relevant observationalstudies concerning perinatal

outcomes of TAPSN = 1203

Observational studies excluded basedon title or abstract (case reports,

reviews, personal communications)n = 14

Observational studies retrieved formore detailed evaluation

n = 36

Observatinal studies excludedbecause were not published during

the study periodn = 407

Potentially appropriateobservational studies to be

included in the meta-analysisn = 22

Observational studies excluded because did not meet the

inclusion criterian = 12

Flow chart for study selection


OBSTETRICS

Table 1. Characteristics of the studies Author

Cases

Type of TAPS

GA at diagnosis of TAPS

In utero therapy

Residual anastomoses

Postnatal procedure

Survivors, n

Lopriore et al .12 Case 1 Isolated 15 No NA None 1

Groussolles et al .8 Case 1 Associated 18 II Laser Absent None 2

Herway et al .10 Case 1 Associated 20 Transfusion Present E/T 2

Weingertner et al .13 Case 1 Isolated 32 No Present E/T 2

Case 2 Isolated 32 No Present E/T 2

Case 3 Isolated 32 No Present E/T 2

Case 4 Isolated 23 Laser Absent E/T 2

Gucciardo et al .9 Case 1 Isolated 26 Transfusion NA T 2

Case 2 Isolated 24 UCO Transfusion

NA T 1

Case 3 Isolated 29 Laser Transfusion

Hemodilution

Absent None 2

Fratelli et al . 7 Case 1 Associated 27 No Present E/T 2

Lopriore et al .1 Case 1 Isolated 33 No Present T 2

Case 2 Isolated na No Present E/T 2

Robyr et al .3 Case 1 Associated 27 Transfusion NA None 2

Case 2 Associated 24 Transfusion NA None 2





Case 7 Associated 21 Transfusion NA NA 1

Case 8 Associated 25 UCO NA None 1






Lopriore et al .11 Case 1 Associated 20 No Absent None 2

Assaf et al . 6 Case 1 Isolated 19 Laser NA None 1UCO: umbilical cord occlusion; E: blood exchange in the polycythemic twin; T: blood transfusion in the anemic twin; NA: not available

Table 2. Outcomes according to gestational age at diagnosis of TAPSGestational age at diagnosis of TAPS

N

15 to 23 weeks13 pregnancies

(26 twins)

24 to 29 weeks10 pregnancies

(20 twins)

32 to 33 weeks 4 pregnancies

(8 twins)

P

Hb anemic twin, g/L, mean ± SD 146 ± 60 .1 98 .6 ± 35 .1 60 .7 ± 20 .7 0 .021

Hb polycythemic twin g/L, mean ± SD 171 ± 46 .7 227 ± 34 .1 216 .8 ± 9 .4 0 .025

In utero therapy, n (%) 10/13 (77) 9/10 (90) 0/4 (0) 0 .003

Overall survival, n (%) 18/26 (69) 18/20 (90) 8/8 (100) 0 .068

Postnatal procedures, n (%) 4/26 (15) 4/20 (20) 7/8 (87) < 0 .001



risk of postnatal procedures. Survival rates did not differ significantly, either in overall survival or according to the number of surviving twins (Table 3).

When compared with iTAPS, cases of aTAPS were treated in utero more often and required postnatal procedures less frequently. Gestational age at diagnosis of TAPS, Hb levels at birth, and survival rates did not differ between the two groups. We observed more normal Hb levels in neonates after aTAPS than after iTAPS In Table 4, this comparison is shown with twins classified as follows:

● Donor twin: donor twin with TAPS following TTTS treated with laser therapy

● Anemic twin: donor twin with TAPS without previous TTTS

● Recipient twin: recipient twin with TAPS following TTTS treated with laser therapy

● Polycythemic twin: recipient twin with TAPS without previous TTTS

Finally, the Hb levels were not influenced by the patency of vascular anastomoses (Table 5).

DISCUSSION

In this review we found that the overall survival rate in twins affected by TAPS was 82% and was similar for the anemic and the polycythemic twin. Neonatal morbidity occurred in 9% of cases, and in a very few it was severe enough to cause neonatal death. We also observed that more normal Hb levels at birth were related to early diagnosis (gestational age 15 to 23 weeks), probably because this allows specific management and intrauterine therapy. However, we noted that survival rates increased from 69% to 100% in association with increasing gestational age at diagnosis.

In addition, previous TTTS did not worsen neonatal outcomes. Indeed, TAPS after laser therapy for TTTS was associated with more normal Hb levels in both anemic and polycythemic twins than isolated TAPS. It may be speculated that laser therapy provides protection by reducing the severity of later TAPS.

It is generally believed that TAPS results from inter-twin blood transfusion through small vascular anastomoses.1 In the cases in our review, placental histological assessment (which should be mandatory in monochorionic twin pregnancies complicated by TAPS or TTTS) was performed in only 39%. Histological assessment did not reveal patent vascular anastomoses in 36% of the examined placentas. Because patent anastomoses are necessary for inter-twin transfusion, it is likely that thrombotic events, probably

secondary to polycythemia, closed small anastomoses. Therefore, failure to demonstrate patent vessels on placental examination is not a requirement for excluding the diagnosis of TAPS.

We found that neonatal anemia and polycythemia do not depend on the patency of vascular anastomoses. However, in anemic neonates with patent placental anastomoses detected by placental histological examination, the mean Hb was lower (85.1 g/L) than in anemic neonates without patent anastomoses (167.5 g/L). This difference might be clinically relevant, although it did not reach statistical significance (likely because of the small sample size).

The key limitation of our review was the paucity of information available in the literature. Although we observed better outcomes for twins with TAPS treated in utero, there are no standard criteria for selecting the initial treatment for TAPS. Doppler surveillance of the middle cerebral artery every four weeks has been suggested,3 but the threshold value for intervention has not been established. Intrauterine blood transfusion, laser ablation of placental anastomoses, umbilical cord occlusion, and expectant management have been described,1,3,6–13 but the numbers in case series have been too small to compare the different methods. Moreover, the limited number of cases in our dataset did not allow us to perform multivariable analyses.

Reticulocyte count is essential for the postnatal diagnosis of TAPS,5 but in the articles we reviewed there was no consensus about units or values. In fact, the reticulocyte count was reported as a percentage in some articles,10–12 as an absolute value in others,1,7–9,13 and was sometimes unreported,3,6 making it impossible to pool data in a single meta-analysis.

TAPS associated with TTTS might have a different natural history from isolated TAPS, although the definition is similar. Therefore, further studies are needed to clarify what management and treatment should be performed for these two entities.

In our opinion, the main limitation of assessing conditions associated with inter-twin transfusion is that it is still difficult to determine when inter-twin blood exchange becomes unequal. It is generally believed that blood transfusion becomes pathological (and unequal) when a twin oligo/polyhydramnios sequence develops. However, the definition of oligo/polyhydramnios (MVP < 2 cm for oligohydramnios and > 8 cm for polyhydramnios) is subjective,14 since to our knowledge there have been no studies comparing amniotic fluid volumes in normal and abnormal monochorionic twins. In addition, the definition


OBSTETRICS

Table 3. Outcomes according to prenatal management

In utero therapyConservative management

N

20 pregnancies (40 twins)


P

Hb anemic twin, g/L, mean ± SD 129 .1 ± 50 .0 71 .0 ± 43 .5 0 .011

Hb polycythemic twin, g/L, mean ± SD 190 .3 ± 50 .1 230 .5 ± 20 .1 0 .018

Overall survival, n (%) 31/40 (77) 15/24 (62) 0 .254

No survivors, n (%) 1/20 (20) 0/8 NS

1 survivor, n (%) 7/20 (35) 1/8 (12) 0 .053

2 survivors, n (%) 12/20 (60) 7/8 (87) 0 .502

Postnatal procedures, n (%) 6/40 (15) 12/24 (50) 0 .004NS: not significant

Table 4. Outcomes according to mode of onset aTAPS iTAPS

N



P

Hb donor vs . anemic twin, g/L, mean ± SD 130 .5 ± 53 .6 80 .8 ± 42 .9 0 .029

Hb recipient vs polycythemic twin, g/L, mean ± SD 192 .7 ± 53 .5 221 .9 ± 22 .9 0 .135

Hb donor vs polycythemic twin, g/L, mean ± SD 130 .5 ± 53 .6 221 .9 ± 22 .9 < 0 .001

Hb recipient vs anemic twin, g/L, mean ± SD 192 .7 ± 53 .5 80 .8 ± 42 .9 < 0 .001

GA at diagnosis of TAPS, weeks, mean ± SD 22 .65 ± 3 .23 26 .50 ± 6 .20 0 .07

In utero therapy, n (%) 15/17 (88) 5/11 (50) 0 .03

Overall survival, n (%) 27/34 (79) 19/22 (86) 0 .723

No survivors, n (%) 1/17 (16) 0/11 NS

1 survivor, n (%) 5/17 (29) 3/11 (27) NS

2 survivors 11/17 (65) 8/11 (73) NS

Postnatal procedures 3/34 (9) 14/22 (64) < 0 .001

Table 5. Hemoglobin levels according to patency of vascular anastomoses assessed by placental examination

Patent anastomoses

No patent anastomoses

N 7 placentas 4 placentas P

Hb anemic twin, g/L, mean ± SD 85 .1 ± 27 .0 167 .5 ± 26 .1 0 .072

Hb polycythemic twin, g/L, mean ± SD 209 .4 ± 53 .4 199 .0 ± 55 .1 0 .412



does not include gestational age. In a recent study reporting percentiles of amniotic fluid volume in normal monochorionic diamniotic twins, Dekoninck et al. found that from 15 to 37 gestational weeks, the MVP at the 2.5th centile ranges from 2.01 to 2.83 cm.15 Therefore, using a definition of oligohydramnios < 2 cm would miss cases from 15 to 37 weeks. Similarly, polyhydramnios (MVP at the 97.5th centile) was > 8 cm only from 23 to 31 weeks.15 Moreover, at any gestational age, out-of-range MVP was never < 2 cm and > 8 cm at the same time, as required to define pathological inter-twin transfusion.14 We believe that a better definition would be helpful to understand why some twins develop selective growth restriction, some the twin oligo/polyhydramnios sequence, and some TAPS, while most are normal.

In addition, it has been suggested that the pathophysiology of TAPS is the slow transfusion of blood through a few small vascular anastomoses1. If inter-twin blood exchange becomes unequal, anemia and polycythemia develop, manifested by abnormal Doppler velocimetry of the middle cerebral artery; however, amniotic fluid volume remains normal in both sacs, indicating blood flow depletion in the fetal brain but normal renal function. Nevertheless, because cerebral impairment is the late stage of fetal distress, it is unlikely that cerebral impairment would occur before impairment of renal function.

We suggest that these conditions may be considered as a single entity and probably occur in sequence:

● No inter-twin transfusion of blood: normal twins● Mild inter-twin transfusion: selective intrauterine

growth restriction● Moderate inter-twin transfusion: abnormal renal

function leading to amniotic fluid discordance (TTTS)● Severe inter-twin transfusion: abnormal cerebral

perfusion (TAPS).

Because of the relatively low incidence of monochorionic twin pregnancies and related complications, large multicentre studies are needed in order to investigate the natural history of monochorionic twins.

CONCLUSION

Improved hematological outcomes in both the anemic and polycythemic twins affected by TAPS are associated with early gestational age at diagnosis, intrauterine therapy, and previous laser therapy for TTTS. Due to the low incidence of TAPS, large multicentre studies would be useful to develop standards for the management of twins affected by TAPS.

REFERENCES

1. Lopriore E, Middeldorp JM, Oepkes D, Kanhai HH, Walther FJ, Vandenbussche FP. Twin anemia-polycythemia sequence in two monochorionic twin pairs without oligo-polyhydramnios sequence. Placenta 2007;28(1):47–51.

2. Klaritsch P, Deprest J, Van Mieghem T, Gucciardo L, Done E, Jani J, et al. Reference ranges for middle cerebral artery peak systolic velocity in monochorionic diamniotic twins: a longitudinal study. Ultrasound Obstet Gynecol 2009;34(2):149–54.

3. Robyr R, Lewi L, Salomon LJ, Yamamoto M, Bernard JP, Deprest J, 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.

4. Lewi L, Jani J, Blickstein I, Huber A, Gucciardo L, Van Mieghem T, 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.

5. Slaghekke F, Kist WJ, Oepkes D, Pasman SA, Middeldorp JM, Klumper FJ, et al. Twin anemia-polycythemia sequence: diagnostic criteria, classification, perinatal management and outcome. Fetal Diagn Ther 2010;27(4):181–90.

6. Assaf SA, Benirschke K, Chmait RH. Spontaneous twin anemia-polycythemia sequence complicated by recipient placental vascular thrombosis and hydrops fetalis. J Matern Fetal Neonatal Med 2011;24(3):549–52.

7. Fratelli N, Prefumo F, Zambolo C, Zanardini C, Fichera A, Frusca T. Conservative management in a case of iatrogenic twin anemia-polycythemia sequence. Ultrasound Obstet Gynecol 2012;39(5):597–8.

8. Groussolles M, Sartor A, Connan L, Vayssiere C. Evolution of middle cerebral artery peak systolic velocity after a successful laser procedure for iatrogenic twin anemia-polycythemia sequence. Ultrasound Obstet Gynecol 2012;39(3):354–6.

9. Gucciardo L, Lewi L, Vaast P, Debska M, De Catte L, Van Mieghem T, et al. Twin anemia polycythemia sequence from a prenatal perspective. Prenat Diagn 2010;30(5):438–42.

10. 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.

11. Lopriore E, Hecher K, Vandenbussche FP, van den Wijngaard JP, 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.

12. Lopriore E, Slaghekke F, Kersbergen KJ, de Vries LS, Drogtrop AP, Middeldorp JM, et al. Severe cerebral injury in a recipient with twin anemia-polycythemia sequence. Ultrasound Obstet Gynecol 2013;41(6):702–6.

13. Weingertner AS, Kohler A, Kohler M, Bouffet N, Hunsinger MC, Mager C, et al. Clinical and placental characteristics in four new cases of twin anemia-polycythemia sequence. Ultrasound Obstet Gynecol 2010;35(4):490–4.

14. Quintero RA, Morales WJ, Allen MH, Bornick PW, Johnson PK, Kruger M. Staging of twin-twin transfusion syndrome. J Perinatol 1999;19(8 Pt 1):550–5.

15. Dekoninck P, Deprest J, Lewi P, Richter J, Galjaard S, Van Keirsbilck J, et al. Gestational age-specific reference ranges for amniotic fluid assessment in monochorionic diamniotic twin pregnancies. Ultrasound Obstet Gynecol 2013;41(6):649–52.

perinatal outcomes of twin anemia-polycythemia sequence: a systematic review

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