The use of obstetric ultrasound in the antenatal diagnosis of craniosynostosis: We need to do better

Abstract

Introduction

The cranial sutures allow for growth of the developing brain in both the pre‐ and post‐natal period but also play a crucial role in vaginal delivery. Birth problems are commonly reported by the mothers of children with craniosynostosis and, in particular, sagittal synostosis.

Methods

Patients presenting with all forms of craniosynostosis were identified through a search of computer records, and the antenatal imaging was obtained and examined. The fetal cranial measurements including biparietal diameter, occipitofrontal diameter and head circumference were recorded, and the cephalic index (CI) was calculated for each affected fetus. A birth history was also recorded.

Results

Scans in both the second and third trimesters were available for 28 fetuses who had sagittal synostosis. Eight fetuses (29%) had a significant reduction in CI (>3) between the morphology and growth scans. There was an increase in the number of emergency caesarean deliveries in women whose fetuses had sagittal synostosis when compared with the general population (22% vs. 17%).

Conclusion

The calculation of CI can be performed routinely at antenatal scanning. A value outside the normal range or a change in CI during the pregnancy should prompt detailed scanning of the fetal skull and cranial sutures. This will assist obstetricians with delivery planning.

Introduction

Craniosynostosis occurs in approximately 1 in 2500 live births.1 Most of these are isolated (non‐syndromic) sutural fusions with 15% occurring as part of a craniofacial syndrome.2 The antenatal diagnosis of severe conditions such as Pfeiffer, Crouzon and Apert syndromes is often made antenatally via morphology ultrasound scanning, whereas non‐syndromic sutural stenoses are uncommonly detected with ultrasound.3 Many do not see this as a significant issue as there is no antenatal treatment available for craniosynostosis. When the more severe syndromes are diagnosed antenatally, many parents elect to terminate the pregnancy.

The cranial sutures allow for growth of the developing brain in both the pre‐ and post‐natal period but also play a crucial role in vaginal delivery. The patent sutures allow moulding of the fetal skull to facilitate passage through the birth canal. There are only a handful of published reports that describe the delivery problems associated with craniosynostosis, in particular sagittal synostosis,3, 4, 5 and the morbidity to both mother and child as a result.

This article discusses the effects of craniosynostosis on vaginal delivery and the need for increased awareness of the condition at antenatal scanning, with particular emphasis on sagittal synostosis.

Methods

This retrospective study was approved by the Women's and Children's Health Network Human Research Ethics Committee, which waived consent.

The Australian Craniofacial Unit is Australia's leading surgical unit for the diagnosis and management of craniofacial disorders. It is based in Adelaide, South Australia (SA), and manages patients from all over Australia and South‐East Asia. The majority of the pre‐ and post‐surgical imaging for both paediatric and adult patients is performed at the Women's and Children's Hospital (WCH) in Adelaide.

Patients presenting to the WCH with all forms of craniosynostosis were identified through a search of computer records. The antenatal imaging for patients born between 1 January 2000 and 31 December 2014 was traced, and the ultrasound reports and images were obtained where possible. Imaging for some older patients was no longer available, and antenatal scans performed outside SA and Northern Territory (NT) were not traced. These patients were excluded from the audit. Pregnancies that did not result in the birth of a live child were also excluded from analysis.

The fetal cranial measurements including biparietal diameter (BPD), occipitofrontal diameter (OFD) and head circumference (HC) were recorded. These measurements were either recorded at the ultrasound scan or were measured on the computer images. Measurements were recorded from the morphology scan (performed between 17 and 23 weeks) and a third trimester growth scan. If several growth scans were performed in pregnancy, the scan performed closest to 32 weeks' gestation was selected. The gestation at delivery and the type of craniosynostosis were also noted.

The cephalic index (CI) was calculated for each affected fetus from measurements obtained at each scan using the formula (Jeanty et al.6):

$$\text{CI}=\text{BPD/OFD}\times 100$$

Any change in CI was noted between the morphology and growth scans. The CI was considered normal if between 75 and 85.6, 7 The available images were also reviewed for any visible signs of craniosynostosis.

The method of delivery of each child was recorded, including the reason for any interventional deliveries. Where the information was available, pelvic injuries to the mother as a result of the delivery were also recorded. Data were compared to the state‐wide data provided by the South Australian Pregnancy Outcome Unit (unpublished data).

Results

There were 229 children born in SA/NT during the 15‐year audit period who have been diagnosed with craniosynostosis.

One hundred and ninety five (85%) children have an isolated, single suture craniosynostosis. Only 9% of children have a diagnosis of a recognised craniofacial syndrome, including Muencke syndrome, (7 children), Saethre–Chotzen syndrome, (5 children), Crouzon syndrome (2 children), Pfeiffer syndrome (2 children), Antley–Bixler syndrome (1 child), Beare–Stevenson syndrome (1 child), Jacobsen syndrome (1 child) and Diamond–Blackfan Anaemia (1 child). Four children had no clear syndromic diagnosis, miscellaneous chromosomal anomalies or VACTERL sequence. Seven children were born severely premature, which was thought to contribute to the diagnosis (hypoxic‐ischaemic injury, shunting, etc.). The demographic data of the children are summarised in Table 1.

Table 1.

Demographic data of children diagnosed with craniosynostosis born in SA/NT 2000–2014

	Number of fetuses (%)	Isolated craniosynostosis	Multiple synostoses	Recognised craniofacial syndrome
Male	141 (62)	123	18	10
Female	88 (38)	72	16	11
Total	229 (100)	195	35	21

There are 118 children (52%) diagnosed with a sagittal synostosis. Eighty‐nine of these children had an isolated sagittal synostosis (75%). The demographic data of the children with sagittal synostosis are summarised in Table 2.

Table 2.

Demographic data of children diagnosed with sagittal synostosis born in SA/NT 2000–2014

	Number of fetuses (%)	Isolated sagittal synostosis	Multiple synostoses	Recognised craniofacial syndrome
Male	82 (69)	60	12	7
Female	36 (31)	29	7	2
Total	118 (100)	89	19	9

Data from at least one obstetric scan were obtained for 89 of the 118 pregnancies in which the child was diagnosed with a sagittal synostosis (75%), and data from two scans were obtained for 28 patients (24%). Morphology scans were available for 82 pregnancies (69%) and growth scans in 37 pregnancies (31%). The majority of pregnancies did not have any formal ultrasound scans after 20 weeks.

The CI was calculated from the morphology scan for 80 fetuses who developed sagittal synostosis (Figure 1). Twenty‐six fetuses (33%) had a CI below the normal range. The mean CI was 76 (67–85), standard deviation (SD) = 4. The CI was calculated in the third trimester for 36 fetuses who developed sagittal synostosis (Figure 2). Seventeen fetuses (47%) had a CI outside of the normal range. The mean CI was 75 (63–85), SD = 5.

Figure 1.

Distribution of the cephalic index (CI) of fetuses who developed sagittal synostosis. These measurements were obtained at the routine morphology scan performed between 17 and 22 weeks' gestation. The mean CI was 76.

Figure 2.

Distribution of the cephalic index (CI) of fetuses who developed sagittal synostosis. These measurements were obtained at third trimester growth scan performed after 26 weeks' gestation. The gestation for each fetus varied, as the scans were performed for a variety of clinical indications. The mean CI was 75.

Scans in both the second and third trimesters were available for 28 fetuses who developed sagittal synostosis. Eight fetuses (29%) had a significant reduction in CI (>3) between the morphology and growth scans. The mean change in CI was −1 (range −13 to 9).

The group of children with isolated sagittal synostosis were also examined (78 fetuses). The CI was below the normal range in 24 of 78 (31%) of available scans in the second trimester and in 15 of 28 (54%) of available scans in the third trimester. Twenty‐one fetuses had scans available from both second and third trimesters. The CI reduced significantly between second and third trimesters in eight (33%) fetuses. The mean change in CI was −2 (range −13 to 9).

A diagnosis of craniosynostosis was suspected antenatally in only 7 of the 168 cases with imaging available for review (4.8%). Five of these cases were syndromal with multiple sutural fusions confirmed postnatally. One case had metopic synostosis and polyhydramnios, and the other case had an isolated sagittal synostosis. In a further five cases (3%), a comment was made about an unusual fetal head shape in the ultrasound report, but this was dismissed or not followed up. One case of Crouzon syndrome was diagnosed via chromosome analysis (mother also affected), but the head shape was normal on ultrasound.

On retrospective review of the available antenatal imaging, the diagnosis of sagittal synostosis is strongly suggested in several cases. A progressive reduction in CI indicating progressive scaphocephaly in late pregnancy has been demonstrated in a number of cases. In all these cases, the CI in the late third trimester was below 75.

Case 1 (Figure 3)

Figure 3.

Scans performed during a pregnancy in a 30‐year‐old woman. (a) Axial cranial image and measurements at the morphology scan. (b) Axial cranial image and measurements at 27 weeks. (c) Graphic representation of the biparietal diameter (BPD) measurements, showing a drop in growth from the 50th to the 5th percentile. (d) Graphic representation of the head circumference (HC) measurements, showing appropriate head growth along the 50th percentile. The axial images show the fetal head becoming more dolichocephalic as the pregnancy progressed. This is confirmed by the stable growth of the HC, but dropping growth of the BPD.

Thirty‐year‐old woman: The morphology scan showed a normal fetus with both BPD and HC on the mean and a CI of 81. A growth scan at 26+ weeks showed the HC to being growing along the mean, but the BPD now on the 5th percentile. The head shape is clearly more scaphocephalic and the CI has reduced to 74. The child was delivered by emergency caesarean section due to breech presentation in labour.

Case 2 (Figure 4)

Figure 4.

Scans performed during a pregnancy in a 36‐year‐old woman. (a) Axial cranial image and measurements at the morphology scan. (b) Axial cranial image and measurements at 37 weeks. (c) Graphic representation of the biparietal diameter (BPD) measurements, showing a progressive drop in growth from the 50th to the 5th to below the 2nd percentile. (d) Graphic representation of the head circumference (HC) measurements, showing appropriate head growth along the 50th percentile. The axial images show the fetal head becoming more dolichocephalic as the pregnancy progressed. This is confirmed by the stable growth of the HC, but progressive drop in growth of the BPD.

Thirty‐six‐year‐old woman: The morphology scan showed a normal 22‐week fetus with a BPD and HC close to the mean. The CI was calculated at 78. A growth scan at 32 and again at 37 weeks shows progressive scaphocephaly, with the HC remaining on the mean and the BPD dropping below the 5th percentile. The CI at 37 weeks had reduced to 68. The child was delivered by emergency caesarean section for fetal distress due to prolonged labour without progression.

Case 3 (Figure 5)

Figure 5.

Scans performed during a pregnancy in a 21‐year‐old woman with Crouzon syndrome. (a) Axial cranial image and measurements at 29 weeks. (b) Axial cranial image and measurements at 31 weeks. (c) Axial cranial image and measurements at 35 weeks. (d) Graphic representation of the biparietal diameter (BPD) measurements, showing a gradual drop in growth from the 40th to the 10th percentile. (e) Graphic representation of the head circumference (HC) measurements, showing appropriate head growth along the 60th percentile. The axial images show the fetal head becoming more dolichocephalic as the pregnancy progressed. This is confirmed by the stable growth of the HC, but progressive drop in growth of the BPD. The diagnosis of Crouzon syndrome was confirmed post‐natally.

Twenty‐one‐year‐old woman with Crouzon syndrome: The morphology scan performed in a rural centre showed a normal fetus at 19 weeks. The head shape was mildly dolichocephalic, but well within the normal range. Serial growth scans were performed showing progressive scaphocephaly with a reduction in CI from 76 at 30 weeks, to a CI of 74 at 32 weeks and to a CI of 72 at 38 weeks. The child was delivered by emergency caesarean section due to cephalopelvic disproportion (CPD). The boy was diagnosed with Crouzon syndrome postnatally and had only a sagittal synostosis at birth.

The mode of delivery for those diagnosed with sagittal synostosis was also recorded. Infants born prematurely (earlier than 36 weeks' gestation) were excluded from analysis. A total of 112 pregnancies were included. The pattern of delivery is listed in Table 3. The data were compared with the total population data in SA over the same time period, provided by The Pregnancy Outcome (Statistics) Unit, SA Health (Table 4).

Table 3.

Method of delivery of term infants with sagittal synostosis in SA/NT 2000–2014

Delivery type	Number (n = 112)	Per cent
Vaginal	51	46
Elective section	31	28
Emergency section	25	22
Unknown	5	4

Table 4.

Delivery statistics for infants with sagittal synostosis compared with the population data in SA.^a

	Study group (%)	Population (%)
Emergency section	22	17
Failure to progress, CPD	61	50
Breech at term	6	12
3rd/4th tears	2	2

^aThe Pregnancy Outcome (Statistics) Unit, SA Health. Data from 1 January 2000 to 31 December 2014.

There was an increase in the number of emergency caesarean deliveries in women whose fetuses had sagittal synostosis when compared with the general population (21% vs. 17%). There were also a higher number of emergency caesarean sections performed for CPD and failure to progress in the study group compared with the general population.

There were 15 fetuses who had a CI of under 75 at the third trimester scan. Four of these fetuses (27%) were breech presentation at term. A further four fetuses (27%) were delivered by emergency caesarean section for CPD. Only two fetuses (13%) were born vaginally without grade 3 or 4 perineal or vaginal tears to the mother.

We have also been able to identify the cranial sutures with three‐dimensional (3D) ultrasound in the second and early third trimester. The open sutures and anterior fontanelle are clearly seen in this normal fetus (Figure 6a), while in this 20‐week fetus subsequently diagnosed with Pfeiffer syndrome, global craniosynostosis is obvious (Figure 6b).

Figure 6.

(a) 3D ultrasound image of a normal fetus at 20 weeks. The metopic, coronal and anterior sagittal sutures are clearly patent and well‐demonstrated. (b) 3D ultrasound image in a 20‐week fetus later diagnosed with Pfeiffer syndrome. The metopic and coronal sutures are fused in keeping with global craniosynostosis. This was confirmed at autopsy.

Discussion

Craniosynostosis is under diagnosed antenatally. The largest study to date found only 10.8% of affected children were diagnosed or even had mention of an abnormal skull shape on antenatal ultrasound.3 The numbers in our group were even lower (7.8%), and many of these had syndromic diagnoses where abnormalities of the face and limbs contributed to the diagnosis. There have been a small number of studies evaluating the cranial sutures on antenatal ultrasound, and these studies have universally found that the sutures are best seen on 3D ultrasound and the sagittal suture is the most difficult to identify.8, 9, 10, 11 It is only in the last 10 years that 3D ultrasound has become available, but this requires special ultrasound probes and highly skilled sonographers to obtain good images, which are still not available in many smaller centres due to the costs involved. 3D scanning is also time consuming in many cases, which prohibits its routine use in many centres.

The causes and timing of onset of craniosynostosis is still not clear. There have been suggestions made that fetal constraint may play a role in some cases,5, 12 and a number of genes have been identified as being involved, especially in syndromic cases. The cause is almost certainly multifactorial. The time of onset is also likely to be variable, which may explain our observation of a very large change in CI in some affected fetuses, and very little change in others. The data examining the stability of the CI antenatally is quite old and fairly sparse, and more research is needed in the area. Jeanty et al.,6 Hadlock et al.,7 and Mador et al.,13 found the cranial index remains stable in the second and third trimester, whereas Kurmanavicius et al.,14 and Gray et al.,15 found significant variation with gestational age. The latter two studies, however, were both cross‐sectional in design, whereas the Jeanty study6 was longitudinal in nature producing more reliable results.

The CI was outside the normal range in a significant number of our patients. In many cases, this was not recognised, as the CI is not routinely calculated at antenatal scanning. Our data suggest that a CI outside the normal range, especially in the third trimester, should prompt careful evaluation of the cranial sutures, and consideration should be given to a further antenatal scanning late in the third trimester to re‐examine the fetal skull and CI.

The article by Anderson et al.4 was one of the first to raise concerns over maternal well‐being from delivery of a child with craniosynostosis. Four cases were reported where fetal craniosynostosis caused obstruction to labour, resulting in a significant perineal injury to the mother, and/or emergency caesarean section. Both Graham et al.5 and Swanson et al.16 noted a high incidence of CPD in their series, leading to a high frequency of emergency sections or forcep deliveries. They did not comment on any maternal pelvic injuries. Weber et al.3 found the rate of perineal injuries was not significantly increased, but there was a significant increase in the number of vaginal tears compared with the general population. The rate of emergency section in this group was 17% higher than in the general population.

Weber et al.3 also found significant concerns with fetal well‐being in this group of infants as a result of these traumatic deliveries. Infants with craniosynostosis were four times more likely to need neonatal intensive care treatment than those not affected. Of great importance, they found those affected infants who were diagnosed antenatally and were delivered by caesarean section showed no major complications, whereas those delivered vaginally had cephalhaematomas in 16.7% of cases, dystocias occurred in 16.7% of cases and maternal perineal ruptures in one third of cases.

Cephalopelvic disproportion can be difficult to diagnose clinically by even the most experienced obstetrician.17 Half of the emergency sections performed in SA are because of CPD, with a further 12% due to malpresentation [The Pregnancy Outcome (Statistics) Unit, SA Health]. Higher rates of malpresentation, including breech presentation, have been reported in fetuses later diagnosed with craniosynostosis.3 A number of our group also had emergency sections for CPD and malpresentation, and a number were also delivered by planned section for breech presentation.

To our knowledge, the observation of a serial reduction in CI during pregnancy as detected by ultrasound scanning has not previously been reported. While this was not a feature seen in every case of sagittal synostosis, our cases resulted in emergency caesarean deliveries for malpresentation and/or obstructed labour. Recognition of this feature antenatally could prevent this situation by planning an elective caesarean section. The calculation of the CI is not routinely performed or reported in many Australian institutions. Most ultrasound machines can produce this calculation automatically at any obstetric scan with minimal programming.

Conclusion

Our data suggest that craniosynostosis could be diagnosed antenatally in a significant number of cases. The routine calculation of CI can be performed at antenatal scanning, and a value outside the normal range, or a change in CI during the pregnancy should prompt detailed scanning of the fetal skull and cranial sutures, including 3D scanning. An increase in antenatal diagnosis will enable better delivery planning for this group of patients, which should lead to a decrease in fetal and maternal morbidity as a result of obstructed labour.

Authorship

All three authors have contributed to the preparation of this article. The content, including images, has been agreed upon, and all authors have agreed on the final paper being submitted to the Australasian Journal of Ultrasound in Medicine.

Disclosure

No financial support was provided for this study. The authors do not have any conflicts of interest to declare.