Twin-twin transfusion syndrome (TTTS) is a severe complication in monochorionic (MC) twin pregnancies, for which fetoscopic laser surgery is the preferred treatment. TTTS occurs in approximately 10% of MC pregnancies.1 Without treatment this condition is lethal in 73% to 100% of cases.2 TTTS is characterized by a net transfer of blood between twins through vascular anastomoses on the shared placenta. As a result, one fetus, the recipient, presents with a polyhydramnios while the other fetus, the donor, is often “stuck” behind the intertwin membranes due to oligohydramnios. Fetoscopic laser surgery is the preferred treatment in TTTS and is associated with an increased survival rate and a reduced risk of cerebral injury compared to twins treated with amnioreduction.3–5
This improving survival rate and decrease in perinatal complications have led to a shift in attention towards the long-term outcome of survivors of TTTS, especially the impact on neurodevelopment later in life. Neurodevelopment is an important outcome measure as it has a great influence on overall quality of life and academic achievement of children, burden on the family and on society.
The improved outcome in TTTS is a result of growing expertise and improved techniques, including the use of a selective sequential method and the Solomon laser technique.6 Therefore, discussing studies from several decades ago gives an unreliable perspective on current outcome. This review focuses on the long-term neurodevelopmental outcome after fetoscopic laser surgery for TTTS reported by studies from the last decade, 2009 to 2019.
A systematic literature search was performed to obtain all relevant articles. We searched PubMed, Embase, Emcare, Web of Science, Cochrane library, and Academic Search Premier using the following search (mesh) terms: fetofetal transfusion, fetoscopy, laser therapy, lasers, neurodevelopmental disorders, human development, cognition, cognition disorders, motor skills, cerebral palsy (CP), patient health questionnaire, neuropsychological tests, and neurobehavioral manifestations. For the complete search strategy see Supplemental Digital Content 1 (https://links.lww.com/MFM/A5). Inclusion criteria were articles published between January 2009 and April 2019 about neurodevelopmental outcome in TTTS-survivors treated with fetoscopic laser surgery and assessed after the neonatal period using neurologic exams and cognitive developmental tests. Exclusion criteria were publications in other languages than English, reviews, case reports, guidelines, and letters. Reference lists of eligible studies were searched for relevant articles which were possibly missed by our search strategy. Eligibility and methodological quality of each study were assessed independently by two reviewers (P.K. and J.v.K.).
We searched eligible articles on neurodevelopmental primary and secondary outcomes, including CP, cognitive delay, blindness, and deafness. We registered lost to follow-up rates, reported risk factors and the tests used to determine cognitive delay and CP. Severe cognitive delay was defined as either a score below −2 standard deviations (SD) on a developmental test or was based on the description of severe cognitive delay by the authors when no validated test was used. CP was classified as Grade I-V on the Gross Motor Function Classification System (GMFCS) or was based on other tests and reports of CP by the authors when GMFCS was not used.7
The primary outcome for this study was severe neurodevelopmental impairment (NDI), a composite of CP, severe motor and/or cognitive delay (<−2 SD), bilateral blindness and/or bilateral deafness requiring amplification with hearing aids.
A secondary outcome was used to record adverse neurodevelopmental outcome as reported according to the various definitions in the included studies.
Data are reported as mean ± SD or median (interquartile range), as appropriate.
Our search yielded 178 articles, 125 published between January 2009 and April 2019 (Fig. 1). In total, 26 articles met our inclusion criteria. We excluded seven articles because the same cohort was more fully described in later, larger or more detailed series by the same authors.8–14 We included three articles written by the Leiden University Medical Center, which describe patients from three different cohorts (2000–2005, 2008–2012, and 2011–2014).15–17 We report the main findings in the following sections and discuss advantages and limitations.
Long-term neurodevelopmental outcome in TTTS treated with laser surgery
From 1999 to 2009 only five long-term follow-up studies were published, compared to nineteen follow-up studies in the last decade, 2009 to 2019. Table 1 summarizes the long-term neurodevelopmental outcome stated as the prevalence of CP and NDI reported by these follow-up studies.
The majority of studies (17/19) reported CP as a primary outcome or part of a composite outcome. The mean prevalence of CP was 5.1% (87/1700, 95% confidence interval (CI): 4.1–6.2). Several tests were used to determine CP, including Amiel-Tison neurodevelopmental examination and other standard neurologic examinations. The GMFCS was used to classify CP by 4/19 (21.1%) studies.7
To assess cognitive outcome, 6/18 (33.3%) studies used the ages stages questionnaire (ASQ), a developmental questionnaire for children aged 1 to 66 months and to be completed by parents.18–33 In all studies, which used the ASQ, scores below −2 SD ranged between 6.0% and 42.4%. Salomon et al. (2010) followed-up a cohort from 6 months to 6 years of age and used both the ASQ at 12, 24, 48, and 60 months and the Wechsler Intelligence Scale for Children-IV at 6 years to evaluate cognitive development.19 Mean ASQ-score at 60 months was (261 ± 53.7) and mean total IQ on the Wechsler Intelligence Scale for Children-IV was (90.6 ± 19.9). However, the proportion of children with scores below −2 SD was not reported. Korsakissok et al. (2018) and Schou et al. (2019) assessed 53.4% (31/58) and 68.0% of their cohorts with an ASQ.22,23 In the others outcome was based on recent hospital records, telephone interviews with parents or International classification of diseases-10 codes. Schou et al. (2019) reported a mean ASQ-score of (176.4 ± 51.5) at a median age of 27 months. In TTTS-survivors with a similar age (median 24 months), Lenclen et al. (2009) reported a mean ASQ-score of (216.3 ± 54).18
In 5/18 (27.7%) studies the Bayley scales second or third edition (Bayley II or III) was used to assess neurodevelopment.15–17,24,25 Scores below −2 SD ranged from 3.2% to 15.8%, though only 3/5 studies presented these data.15,16,24 Lopriore et al. (2009) conducted an international multicenter study in the Netherlands, Belgium, and Spain, the largest cohort in this review (n = 278).15 Campos et al. (2016) evaluated their TTTS-survivors twice, first at 1 to 6 months followed by a second assessment at 7 to 12 months of age.25 Because the Bayley screening test is not validated in Brazil, the authors included a comparison group of 22 “normal” children. Inappropriate performance at both evaluations, defined as “the child requires subsequent reviews or should be referred for diagnostic assessment,” for the TTTS group was 18% for the cognitive domain, 9% for receptive communication, 21% for expressive communication, 24% for fine motor and 24% for gross motor skills. In a cohort with a similar follow-up range (at age 12 months), Chang et al. (2012) reported cognitive impairment in 6.8% (4/59) using Bayley scales with a cut-off point of <70.24 For both studies, follow-up was too early (≤12 months) to assess “long-term” outcome in a reliable way, in particular CP.
In 4/18 studies several tests were used according to the age range of their TTTS cohort. Gray et al. (2011) used both Griffith Mental Development Scales (Griffiths’ scales) (71.7%) and Bayley II and III (13.3% and 15.0%) to assess neurodevelopment and detected scores below −2 SD in 13 (11.5%) TTTS-survivors.26 Graeve et al. (2012) used the Kaufman-Assessment Battery for Children and the German national screening examination to assess cognitive and motor development in TTTS-survivors at a median age of 6 years and 5 months.27 This cohort has the longest follow-up period of all studies included in this review. Normal test scores were achieved by 151 (79.5%) children. McIntosh et al. (2014) used the Wechsler Preschool and Primary Scale of Intelligence Third Edition in 41 children, in four (8.0%) children other tests were used, in five (10.0%) children neurodevelopment was considered normal based on parental reports.28 Scores below −2 SD were detected in one child (2.0%). Vanderbilt et al. (2014) used the Battelle Developmental Inventory scores in 2-year-old TTTS-survivors and detected cognitive scores below −2 SD in one child (1.0%).29
In four studies, no validated test was used to assess neurodevelopment. Information on long-term outcome was obtained from parents, patient records, questionnaires, check-ups or the child's pediatrician.30–33 Mullers et al. (2015) described “neurodevelopmental concerns” in 14.1% (15/106) based on pediatric review and correspondence with parents.31 These neurodevelopmental concerns were specified as speech and language delay in seven children, behavioral concerns in two children, mild motor delay in two children and CP in four children.
A wide variety of definitions was used to report neurodevelopmental outcome. The composite outcome “severe NDI” as defined in our Methods section was used in only 7/19 (36.8%) studies.15–17,22,23,26,29 These studies reported NDI in 4.0% to 18.0%, with a mean of 9.7% (106/1 092, 95% CI: 7.8–11.5).
The majority of other follow-up studies used a different definition for NDI. Three studies reported a composite outcome including CP and a score below −2 SD on a developmental test, though lacking deafness and blindness.24,27,28 Five studies did not define a composite outcome; two studies reported only a proportion of children with ASQ scores below −2 SD and four reported CP.20,21,25,32,33 Four studies reported a composite outcome without cognitive impairment based on validated developmental tests and used other definitions (see Table 1).18,19,30,31 The prevalence of the reported adverse neurodevelopmental outcome when combining these different definitions is 10.5% (194/1 853, 95% CI: 9.1–11.9). Seven studies also included minor impairment defined as “borderline” scores or scores below −1 SD on developmental tests, minor neurological impairments, or temporary and treatable impairments with no significant impact on daily life (Table 2). The prevalence of minor impairment ranges between 0% and 25.9% with a summarized mean of 13.7% (117/853, 95% CI: 11.4–16.0).16,17,19,22,27,28,30
Four studies compared neurodevelopmental outcome of TTTS-survivors with a control group of singletons, uncomplicated MC or dichorionic-twins. Campos et al. (2016) reported in both evaluations (1–6 and 7–12 months), more children in the TTTS group with an inadequate performance than in the control group of uncomplicated singletons.25 Schou et al. (2019) reported lower ASQ scores for TTTS survivors with a median age of 27 months (range 11–60) compared to a control group of uncomplicated MC-twins of 18 months (range 17–25) (–23.5 points; 95% CI: –44.8 to –2.2, P = 0.03).23 However, the prevalence of NDI was comparable between the TTTS-survivors and the uncomplicated MC-twins (3.1%, 3/98) when corrected for gestational age (GA) at birth, birthweight, and gender (P = 0.07). Lenclen et al. (2009) reported comparable ASQ scores in 85 TTTS-survivors born between 24 and 34 weeks of GA and assessed at the corrected age of 2 years and 184 DC-twin controls, (216.3 ± 54) versus (225.5 ± 54) respectively (P = not significant).18 Sommer et al. (2018) described the outcome in TTTS-survivors born <29 weeks of GA at a corrected age of eighteen months.32 Compared to a control group of DC twins matched for GA, no difference in prevalence of CP, vision impairment, hearing impairment (with or without hearing aid), and growth was found. Hearing impairment was 5.7% (4/70) in DC twins versus 23.1% (3/13) in TTTS-survivors (P = 0.07).
An important characteristic of long-term outcome studies is the possibility to assess (perinatal) risk factors for long-term impairment. All nineteen studies included for this review assessed risk factors for their primary outcome.
The severity of TTTS, defined as Quintero Stage I to V, is reported a risk factor for adverse outcome in 5/12 (41.6%) studies.17,19,21,26,29,34 Four studies found higher Quintero stage at laser surgery associated with adverse long-term neurodevelopmental outcome. In contrast, Sananès et al. (2016) reported an association between Quintero Stage I, indicating less severe disease, and abnormal ASQ scores (P = 0.021).21 However, 63.5% (40/63) Stage I cases were lost to follow-up in this study (P = 0.004), leading to possible selection bias, since lost to follow-up was 49.5% (54/109) in Stage II, 38.6% (27/70) in Stage III, and 37.5% (3/8) in Stage IV.
Prematurity and low birth weight, in particular fetal growth restriction or being small for GA, are well-known risk factors for adverse long-term outcome. Low GA at birth was reported a risk factor for adverse long-term neurodevelopmental outcome in 30.7% (4/13) studies.15,17,21,22 Additionally, Sommer et al. (2018) reported a high prevalence of CP (15.4%) in very premature infants (<29 weeks of GA) born after laser therapy for TTTS.32 In the study cohort of Kowitt et al. (2012), 90.9% (10/11) children with severe neurological morbidity (see definition in Table 1) were born before 32 weeks of gestation.30 Schou et al. (2019) reported CP or ASQ-scores below −2 SD in 23.1% of TTTS-survivors born before 34 weeks of gestation versus 6.6% in survivors born after a GA of 34 weeks.23
Low birth weight was reported as a risk factor for long-term impairment in 44.4% (4/9) studies.15,17,21,22 Spruijt et al. (2019) reported an independent association between cognitive scores and low birth weight (regression coefficient B: 0.3; 95% CI: 0.1–0.6, P = 0.004) and between cognitive scores and growth restriction below the tenth percentile (regression coefficient B: −4.3; 95% CI: −7.9 to −0.7, P = 0.021).17 Sananès et al. (2016) described an association between birth weight below the fifth percentile and adverse neurodevelopmental outcome (P = 0.036): 23.1% (9/39) children with a birth weight below the fifth percentile had an abnormal ASQ.21 Lopriore et al. (2009) found low birth weight associated with NDI (odds ratio: 1.2 for each 100-g decrease; 95% CI: 1.1–1.3; P < 0.001) though no association between NDI and growth restriction below the tenth percentile.15
Graeve et al. (2012) described significantly better Kaufman-Assessment Battery for Children mental processing scores in recipients compared to donors (median 106 (69–127) and 100 (70–124) respectively, P = 0.045), though no significant difference in overall scores.27 Campos et al. (2016) reported an association between donor status and difficulties with expressive communication (odds ratio: 6.8, 95% CI: 1.0–44.6).25 Altogether 11/12 (91.7%) studies did not report a difference in long-term impairment between donor and recipient twins.
In one study, cranial magnetic resonance imaging (MRI) was routinely performed in the whole study population. Chang et al. (2012) described impairment in one child with no cerebral injury on MRI and two children with cerebral injury on MRI and normal neurologic exams.24 Spruijt el al. (2019) reported an association between decreased Bayley motor scores and severe cerebral injury (regression coefficient B: −14.1; 95% CI: −25.0 to −3.2, P = 0.012), although 58.8% (10/17) of children with NDI had no severe cerebral injury on cranial ultrasound.17
Maternal education was associated with scores on the Battelle Developmental Inventory by Vanderbilt et al. (2014).29 Education level defined as high school or less was associated with lower scores. Lower maternal education level had a higher impact on NDI (β level 0.60, P < 0.001) than lower GA at birth (β level 0.3, P < 0.01) and advanced Quintero stage (β level −0.4, P < 0.01). In contrast, Campos et al. (2016) reported no association between impairment and maternal education, although they did find an association between impairment and economic class, defined according to the Brazilian Association of Research Companies, (each point decreased the risk of abnormality with 16%).25
In the past decade, fetal medicine centers all over the world increasingly reported on the long-term neurodevelopmental outcome after fetoscopic laser surgery for TTTS. Overall, in the last 10 years, 19 studies evaluated the long-term neurodevelopmental outcome. Severe NDI was reported in seven studies and the prevalence of severe NDI was 9.7% (range 4.0%–18.0%). The prevalence of adverse neurodevelopmental outcome (our secondary outcome) was 10.5% (Table 1) and the prevalence of CP was 5.1%. Minor impairment was reported in 13.7%.
Important risk factors for adverse long-term neurodevelopmental outcome include prematurity, low birth weight, and advanced Quintero stage. The association between Quintero stage and long-term impairment suggests that increasing disease severity may not only lead to increased perinatal mortality but also to increased long-term morbidity. Recipient or donor status of the fetus was not associated with adverse neurodevelopmental outcome in most studies, although two studies found lower scores on one domain. The prognostic value of severe antenatal or postnatal cerebral injury for long-term impairment remains a subject of debate. Conclusions on long-term neurodevelopmental outcome based on cerebral injury are difficult to make as cerebral injury does not directly correlate with long-term neurodevelopment. The prevalence of minor impairment implies that, even in children without obvious NDI, subtle problems may occur, including mild CP and neurocognitive impairments. These “subtle” problems can have a significant impact on the care and educational requirements of children throughout life.
The prevalence of NDI and CP in this review is equivalent to the prevalence described in a recent review by Hecher et al. (2018), reporting NDI in 6% to 18% and CP in 3% to 11% of TTTS-survivors.35 Previous reviews of Rossi et al. (2011) and van Klink et al. (2016) reported mean NDI in 11.1% and 9.8% and CP in 4.8% and 6.1%, respectively.36,37 In this review, though a broad range of studies was included, a similar mean prevalence was found. This indicates that since the introduction of laser therapy, severe NDI after laser surgery for TTTS has a relatively stable prevalence of about 9.7%.36,37 However, this mean prevalence must be interpreted with caution as the range of reported impairment and CP is broad and most studies did not use the composite outcome NDI. Low GA at birth and low birth weight are well-recognized risk factors for long-term impairment: severe NDI in children born preterm is very frequent and is inversely related with GA and birth weight.
In several studies bias may have occurred, the majority due to an unequal distribution of Quintero stages in the follow-up group, as no Quintero Stage I cases were included or a higher proportion of low or high Quintero stages were lost to follow-up.21,26,28,29 In addition, lost to follow-up was relatively high in several cohorts, included significantly more children with low birth weights and less or more severe neonatal morbidity or the study included only very premature children.21,22,29,32 Control groups were sometimes not accurately matched in age to the TTTS-survivors.23 Furthermore, in several studies not all children were examined by researchers and conclusions on neurological development were solely based on information from parents, treating physicians or pediatricians or medical records.
An important limitation for comparison between studies is the substantial difference in the timing of follow-up (age range from 1 month to 10 years), their definition of the primary outcome, inclusion criteria, and the methods and materials to assess outcome. The majority of studies performed their assessments at an adjusted age of 2 years. At this age, it is possible to discover severe developmental abnormalities that require and benefit from early intervention. However, developmental outcomes assessed during early childhood are only moderate predictors of long-term neurodevelopment, particularly for scores on cognitive tests and academic performance. Although some studies followed their cohort until a mean of five years of age, some developmental problems, including learning difficulties, speech and language deficits, and communication disorders, cannot be detected until later on, once the children start becoming more socially and academically challenged at school age. In addition, definitions of primary outcome ranged widely from CP to impaired cognitive function, sometimes including blindness and hearing impairment. The aforementioned composite outcome, NDI, was unfortunately used in less than half of the included studies. Therefore, the mean prevalence of NDI must be interpreted with caution as it is based on a minority of the reported impairment. In these studies, different neurodevelopmental tests were used, like Bayley II and III, ASQ, as well as nonvalidated questionnaires and neurologic exams. Results were either reported as mean scores per domain of the developmental test, the proportion of children with abnormal results per domain or only overall scores, which makes it difficult to compare results between studies.
Longer follow-up of TTTS-survivors is required to understand the clinical relevance of milder forms of impairments diagnosed in early childhood and to follow speech and language development, for instance at the age of 2, 5, and 8 years. Studies reporting on long-term neurodevelopment should use a uniform definition of NDI that is, scores on neurodevelopmental tests below −2 SD, CP GMFCS grade II or higher, bilateral blindness and/or severe hearing impairment. In this review, we had to include all grades of CP in the composite outcome NDI since most studies did not report or grade CP according to GMFCS. To reliably compare study results, it is important that diagnoses of individual cases are reported and in particular when there are comorbidities. Only TTTS-survivors treated with laser surgery should be included in follow-up along with an appropriate control group. When other groups are included in follow-up, presentation of separate results on primary and secondary outcomes are recommended. Validated neurodevelopmental test is of uttermost importance to assess neurodevelopment. Methods sections should contain a detailed description of the used definitions and methods. In the results section authors should report both mean scores, including SD, per domain and on the overall test, and the proportion of children with scores below −2 SD. Consensus on these terms is necessary to allow valid comparison of cohorts, which would improve the quality of research and lead to more accurate knowledge on TTTS. Accordingly, development of a core outcome set to allow comparison of study data would be beneficial in improving the quality of research.38,39
Moreover, large prospective multicenter studies with stringent neuroimaging and long-term follow-up protocols could provide more clarity around the association between cerebral injury and NDI.
In conclusion, TTTS-survivors are at increased risk for NDI and close fetal monitoring and long-term follow-up remains required. Continuing follow-up until at least school age is recommended. International collaboration in long-term follow-up of TTTS-survivors to form universal inclusion criteria, developmental tests, ages at assessment, and outcome measures are of great importance to improve knowledge on long-term neurodevelopmental outcome and allow adequate parental counseling.
The authors thank J.W. Schoones for assistance with the literature search strategy.
Conflicts of Interest
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