Intracranial hemorrhage and additional anomalies detected on prenatal magnetic resonance imaging: a large, retrospective study in two tertiary medical institutions

doi:10.21203/rs.3.rs-3243838/v1

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Intracranial hemorrhage and additional anomalies detected on prenatal magnetic resonance imaging: a large, retrospective study in two tertiary medical institutions

https://doi.org/10.21203/rs.3.rs-3243838/v1

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Purpose

To clarify the prenatal magnetic resonance (MR) imaging characteristics of foetal intracranial haemorrhages (ICHs) in a large cohort and correlate them with birth outcomes.

Methods

We retrospectively reviewed MR images of foetuses with ICH on screening ultrasound (US) on picture archiving communication system (PACS) servers within a nearly five-year period from two medical tertiary centres. The indications, main abnormal findings and coexistent anomalies were recorded by two experienced radiologists with census readings.

Results

We recruited 81 cases (average gestational week, 28.0 ± 5.0 weeks) with prenatal MR imaging, including 71 singleton pregnancies and 10 monochromic twin pregnancies. Predominant coexistent anomalies were ventriculomegaly (35.8%), holoprosencephaly or porencephaly (13.6%) and enlarged posterior fossa/ or posterior fossa cyst (7%) in the lesion-based evaluation. The number of haemorrhagic lesions and the occurrence of the detected complications did not show a correlation with the size of the haematoma. The mass effect of ICH was more commonly observed in foetuses with a large for gestational age (GA) than in foetuses with a small for GA.

Conclusion

Prenatal MR imaging could better show ICH morphology and associated abnormal findings. As a complementary tool of US, MR imaging could help with prenatal counselling and treatment selection after birth.

Health sciences/Medical research/Outcomes research

Health sciences/Risk factors

Foetus

Magnetic resonance imaging

Intracranial hemorrhages

Foetal malformation

Intracranial haemorrhage (ICH) in the foetus is a rare condition with a prevalence of 1/100,000 to 1/1000 in the reported literature [1]. The exact aetiology of foetal brain haemorrhage is unknown. A pregnant woman will not experience any symptoms during an intracranial bleeding process in the foetal brain. It is difficult to detect ICH as early as possible, meaning that the prognoses of these foetuses may be dismal [2–3]. Ultrasonography (US) is the first-choice modality to screen out these suspected abnormal findings [4]. Some subtle lesions are occasionally missed due to either shielding by the calvaria or an uncooperative foetal head position [5]. As a reliable complimentary tool to US, magnetic resonance imaging (MRI) can depict intracranial anatomic structures well and show multiple system anomalies in one scanning plane [6–8]. Unlike MRI characteristics detected in infants or adults, imaging characteristics of foetal ICH vary depending on when and where the haemorrhagic components occur [9]. Coexistent malformations also complicate an accurate diagnosis and evaluation of these abnormal findings on prenatal MRI [10]. To date, reports in the literature on foetal ICH are alarmingly limited, especially in a relatively large cohort study [11, 12]. Knowledge of the MRI signs and abnormal findings will help clinicians perform prenatal counselling and treatment selection at term.

Therefore, our purpose in this research is threefold: (1) to describe the primary and secondary MRI characteristics of foetal ICH on prenatal MRI in a large cohort sample from two independent tertiary centres; (2) to summarize the clinical indications and complications for all foetuses with ICH and analyse whether the volume of a haematoma affects the occurrence of coexistent complications detected on MRI; and (3) to correlate these MRI findings with the postnatal outcomes of the foetuses and some follow-up infants.

Study population

Our institutional review board approved this retrospective study. The flow chart of the selected samples was as follows: first, we retrieved foetal head MR scans from picture archiving communication systems (PACS) in our institution from Jan. 2015 to Dec. 2019 and from another institution from Jan. 2014 to Dec. 2019. All of these foetuses underwent MR examination for suspected abnormal central nervous system findings on US or MR performed in a referring hospital. The exclusion criteria included normal findings and only ventriculomegaly reports on MR. Other anomalies (agenesis of the corpus callosum, intracranial tumours, lip/palate cleft, etc.) or developmental abnormal findings (arachnoid cyst, lymphangioma, vascular malformations, etc.) detected on MR were also excluded. Finally, 81 pregnancies were included in this retrospective study (45 pregnancies in our institution and 36 pregnancies in another institution, Fig. 1). The gestational age (GA) of all foetuses was verified by the date of the last menstrual period and the US findings in the early trimester. Among them, 10 were twin pregnancies, and the others were singleton pregnancies (Table 1).

Table 1

Imaging, demographic and perinatal characteristics (N = 81)
Maternal age in year ( mean ± SD, range)	29.3 ± 4.7 (21–43)
GA in week (mean ± SD, range)	28.0 ± 5.0 (21–40)
Sex (male/female, n %)	39 (48.1%)/42 (51.9%)
Mass effect (present/absent, n %)	13 (16.0%)/68 (83.9%)
Multiple/single lesions, n (%)	28/53, 52.8%
Bigeminal/ singleton pregnancy, n (%)	10/71, 14.1%
Clinical indications (n %)
Intracranial hemorrhage	15 (18.5%)
Ventriculomegaly	16 (19.8%)
Hydrocephalus	8 (9.9%)
Cerebellum/posterior fossa malformation	5 (6.2%)
Others (agenesis of corpus callosum, low spinal cord, tethered cord syndrome, TTTs, TAPs, etc.)	37 (45.7%)
Complications* (n %)
Ventriculomegaly	29 (35.8%)
Porencephaly or holoprosencephaly	11 (13.6%)
Enlarged posterior fossa/ or posterior fossa cyst	7 (8.6%)
Agenesis of corpus callosum	2 (2.5%)
Cerebellar dysplasia/hypoplasia	2 (2.5%)
Hydrocephalus	9 (11.1%)
Others (gyri malformation, hydrops fetalis , subependymal cyst, low spinal cord, hydrops fetalis)	11 (13.6%)
Outcomes
Termination of pregnancy or selective reduction	34 (42.0%)
Dead birth or fetal demise	3 (3.7%)
Live birth	21 (25.9%)
Loss to follow-up	23 (28.4%)
*Some fetuses had multiple complications

MRI acquisition and interpretation

In our hospital, all the examinations were performed without sedation. MRI was performed using a 1.5-T magnetic resonance imaging system with a phased array coil (Magnetom Avanto, Siemens). Conventional MRI protocols used for fetal evaluation included axial/sagittal/coronal half-Fourier acquisition of a single-shot turbo spin (HASTE), and axial/sagittal/coronal true-fast-imaging steady-state precession (True-FISP) sequences. Acquisition parameters for the HASTE sequence were as follows: repetition time (TR) = 1350 ms, echo time (TE) = 92 ms, field of view (FOV) = 400 mm, voxel size: 1.4 × 1.1 × 4.0 mm, flip angle = 170°, matrix = 384 × 256, slice thickness = 4 mm, gap = 0.8 mm, acquisition time = 20-25s. The parameters for the True-FISP sequence were as follows: TR = 3.87 ms, TE = 1.68 ms, FOV = 400 mm, voxel size: 1.7 ×1.6 × 4.0 mm, flip angle = 60°, matrix = 256 × 144, slice thickness = 4 mm, gap = 0.4 mm, and acquisition time = 10-20s. Diffusion-weighted imaging (DWI) was performed in the axial plane using a two-dimensional echo-planar imaging sequence and parallel acquisition technique, with b values of 0, 100, and 500 s/mm². For all MRI sequences, the specific absorption ratio value was controlled under 2.0 W/kg.

In another hospital, MR was performed using a 1.5-T MR system (Optima MR 360, GE) with an 8-channel phased-array cardiac coil using the breath-hold technique. The detailed parameters were as follows: fast imaging applying a steady-state acquisition (FIESTA) sequence, TR = 4.4 ms, TE = minimum, FOV = 380 × 380 mm, matrix = 224 × 224, slice thickness/interslice gap = 6/0 mm, bandwidth = 83.13 Hz/pixel; sagittal fast spin-echo (FSE) T2WI, TE = 61 ms; TR = 3000 ms; thickness = 7 mm; gap = 5 mm; FOV = 36 cm; matrix = 320 × 224; number of excitations (NEX) = 2; band = 41. 7 Hz/pixel. Axial T1WI, TE = 11 ms; TR = 830 ms; thickness = 7 mm; gap = 5 mm; FOV = 36 cm; matrix = 320 × 192; NEX = 2; band = 41. 7 Hz/pixel. DWI sequence, b values = 800 s/mm²,TE = 78 ms; TR = 4100 ms; thickness = 8 mm; gap = 6 mm; FOV = 36 cm; matrix = 96 × 128; NEX = 6.

All fetal MRI scans were independently assessed by two experienced radiologists (both with more than 10 years of experience in fetal MRI knowledge) at the PACS terminal server. Image quality was assessed in the following four grades: excellent (grade 4: excellent diagnostic image quality without fetal motion artifacts), good (grade 3: moderate artifacts but adequate diagnostic quality), poor (grade 2: moderate motion artifacts affecting the assessment of the brain), and unacceptable (grade 1: motion artifacts that severely affect image quality and diagnostic ability). On T1WI, the amniotic fluid, pelvic wall muscle, and subcutaneous fat signals were similar in hypo-, iso-, and hyper-intensity; on T2WI, the pelvic bone, pelvic wall muscle, and amniotic fluid signals were similar hypo-, iso-, and hyper-intensity; and on b = 800 s/mm² DWI images, the amniotic fluid and brain parenchyma signals were similar in hypo-, iso-intensity.

We confirmed that all methods were performed in accordance with the relevant guidelines and regulations by including a statement in the methods section to this effect. All conclusions required consensual agreement between the observers. The MRI images were assessed, including (1) the presence of ICH, (2) the location of ICH and the area of the lesion, and (3) the grade of the IVH. The location of the non-GM-IVH was defined as a haematoma or its debris occurring in the cerebellum, subdural space or corpus callosum. GM-IVH was graded according to the modified Papile classification[13]. The volume of intracranial haematoma was measured by one radiologist based on the reported methods in a previous study [14]. Other coexistent malformations, including ventriculomegaly, holoprosencephaly, hydrocephalus, cerebellar malformations, porencephaly, dilated posterior fossa, agenesis of corpus callosum, etc. were also recorded case-by-case (Table 1).

Postnatal follow-up

All newborns delivered were evaluated by a pediatrician and an obstetrician. Demographic characteristics and perinatal factors were recorded, including fetal sex, birth weight, mode of delivery, and Apgar score (1 to 10). The clinical course included motor (reduced or asymmetric muscle tone or strength), intellectual (mental retardation or cerebral palsy) and cognitive function (visual or auditory impairment).

Statistical analysis

Continuous variables are reported as median ± standard deviation and were compared by Student's t-test. Categorical variables are reported as percentages and were compared by chi-square and Fisher's exact tests. All analyses were performed using SPSS (version 23.0, IBM). Values of p < 0.05 were considered statistically significant.

General information

Eighty-one pregnant women with 71 singletons (average GA: 28.5 ± 5.0, 21–40 weeks) and 10 monochromic twin pregnancies (average GA: 24.3 ± 2.5, 21–30 weeks) were recruited in this study and underwent prenatal MR imaging. The mean GA for all included pregnancies was 28.0 ± 5.0 (21–40) weeks. Foetus sex differences were not seen in this selected sample (39 males versus 42 females). The main clinical indications for further MR evaluation included intracranial haemorrhage (18.5%), ventriculomegaly (19.8%) and hydrocephalus (9.9%) (Table 1).

MRI findings

On MR imaging, most ICH in foetuses appeared as a relatively high signal on T1WI (62/81, 76.5%), an intermediate signal on T2WI (46/81, 56.8%) and a high signal on DWI (65/81, 80.2%) in the foetus-based evaluation. The frequency of foetal ICH and their average sizes across gestation are shown in Fig. 1. In this study, GM-IVH (Fig. 2) was seen in 72 pregnancies (average GA: 28.0 ± 4.9 weeks), cerebellar haematoma in 6 pregnancies (average GA: 24.6 ± 1.14 weeks) and haematoma of the corpus callosum (average GA: 36.0 ± 1.0 weeks) in 3 pregnancies. The average volumes of the haematoma for the GM-IVH, cerebellum and corpus callosum were 3.62 ± 7.9, 0.30 ± 0.21 and 0.44 ± 0.26 mm³, respectively (Table 2). The volume of haemorrhagic components across the various anatomic sites did not differ at the statistical level (p = 0.705. There were 47 foetuses with ICH (average size: 1.43 ± 3.35 cm³) less than 28 GWs and 34 foetuses with ICH (average size: 6.10 ± 10.83 cm³) more than 28 GWs. The numbers of haemorrhagic lesions and the occurrence of detected complications did not show any dependence on the size of the haematoma (Table 3). However, for foetuses with a large GA, the mass effect of the haematoma could be more easily observed due to its relatively large volume (p = 0.031). Thirty-seven foetuses with ICH had one coexistent malformation or abnormal finding, 20 had multiple complications and 23 had no complications on MR imaging. Ventriculomegaly (35.8%, Fig. 3), holoprosencephaly or porencephaly (13.6%, Fig. 3) and enlarged posterior fossa/or posterior fossa cysts (7%) were the three most commonly detected abnormal findings in the lesion-based evaluation. There were 20 ICH fetuses with more than one malformation, including 4 fetuses with three coexistent malformations. There were 20 foetuses with ICH having more than one and 4 foetuses having three coexistent malformations. Brain infarction (Fig. 2) and edema (Fig. 4) were also encountered as rare complications related to foetal ICH in this study group.

Table 2

MR imaging characteristics of fetal intracranial parenchyma hemorrhage across various anatomic sites on fetus-based evaluation
	GM-IVH	Corpus callosum	Cerebellum	P value
Total	72	3	6
Average GA	28.0 ± 4.9	36.0 ± 1.0	24.6 ± 1.14	0.007
Average Size(cm³)*	3.62 ± 7.9	0.44 ± 0.26	0.30 ± 0.21	0.705
Grade	2.59 ± 1.1	-	-
Observed Mass effect	12	-	1^#	0.149
Coexistent malformation (Num. %)	56 (77.8%)	-	-	0.003
GM-IVH, germinal matrix intraventricular hemorrhage;* the lesion could not be outlined in six cases; ^#this case also had GM-IVH

Table 3

The detected complications associated with intracranial hemorrhage in fetuses on MR Imaging by various size and gestational weeks’ group.
	≤ 28 GW (N = 47)		> 28 GW (N = 34)		Total
	Average hemorrhagic area size (1.43 ± 3.35cm³)		Average hemorrhagic area size (6.10 ± 10.83 cm³)
	<=5	> 5	<=5	> 5
Complications (Num.)
Single	25	0	17	6
Multiple	19	2	4	2
p value					0.874
Mass effect (Num.)
Observed	4	0	4	4
Non-observed	38	2	16	2
p value					0.031
Outcomes (Num.)
Live	9	0	10	2
TOP/fetus reduction	21	2	10	1
Dead birth/fetal demise	1	0	1	1
p value					0.296

Outcomes and follow-up of liveborn foetuses

Overall, in the present study, 21 livebirths (Fig. 5), 34 TOP, 1 stillbirth and 2 foetal deaths were recorded. The other pregnancies’ final outcomes were lost. One live infant with ICH detected on prenatal MR imaging from a singleton pregnancy had definite neurological symptoms (Fig. 6). His chromosomal microarray analysis results revealed a de novo mutation of PLOD1, which is associated with Ehlers–Danlos syndrome. One case of hydrops fetalis with alloimmune haemolysis was also detected. The volume of haemorrhagic components did not show a correlation with the final outcome in the present study. All indications, MR findings, complications and outcomes for twin pregnancies are shown in Table 4. One pregnant woman with a twin anaemia-polycythemia sequence (Taps) delivered both healthy infants (Fig. 7). One pregnancy with twin-twin transfusion syndrome (TTTs) stage 4, reduction surgery performed for one foetus and expectation treatment for another with hydrops fetalis was applied. In one TTT stage 1 twin pregnancy, one foetus was in utero dead, and another foetus was a live birth with premature delivery (Fig. 8). After thoroughly evaluating the intrauterine conditions, the TOP procedure was performed in three twin pregnancies.

Table 4

Summaries of imaging findings and fetuses outcomes in the monochorionic twin pregnancies (N = 10) with ICH detected on MR.
	MRI findings				Outcomes
	Indication	Location	Size (cm³)	Complications
Case No.
1	sIUGR	GM-IVH	0.45	VM, porencephaly	Loss to follow-up
2	TAPs	GM-IVH	1.48	VM, ascites, hydrops fetalis	Both live births (Fig. 1)
3	TTTS stage4	GM-IVH	0.16	Hydrops fetalis	One small fetus with selective reduction; the other fetus having hydrops fetalis with expecting delivery
4	TTTS stage3	GM-IVH, Cerebellum	0.98	VM	TOP
5	TTTS stage1	GM-IVH	0.38	Hydrops fetalis	Fetal demise in one fetus; another one was live birth in premature delivery (Fig. 3)
6	TTTS stage4, sIUGR	GM-IVH	0.12	VM	TOP
7	TTTS stage3, sIUGR	GM-IVH	0.57	VM, porencephaly	Loss to follow-up
8	Selective fetus reduction	GM-IVH	0.18		TOP
9	IVF	GM-IVH	0.89	Hydropericardium, ascites, hydrops fetalis	Loss to follow-up
10	TTTs stage3, sIUGR	GM-IVH	0.47		Loss to follow-up
sIUGR, selective fetal in-utero growth restriction; TAPs, twin anemia-polycythemia sequence; TTTS, twin-twin transfusion syndrome; IVF, in vitro fertilization; GM-IVH, germinal matrix intraventricular haemorrhage; VM, ventriculomegaly; TOP, termination of pregnancy

We conducted a retrospective study reviewing MRI characteristics in foetuses with ICH and their co-occurrence abnormal findings in a large cohort sample from two tertiary centres. We found that foetal ICH could occur at any time across gestation and had various appearances depending on the onset time as observed on MR imaging. GM-IVH was the most common site of the intracranial bleeding. Ventriculomegaly (29 cases) was the most common coexistent abnormal finding on MRI, followed by porencephaly or holoprosencephaly (11 cases) and enlarged posterior fossa/or posterior fossa cysts (7 cases) in the present studied samples. We did not find a correlation between the haematoma volume and the final outcome.

It has been reported that ICH is more often detected in premature infants than in prenatal life [1]. However, even if detected, the prognoses for these foetuses are dismal. Foetal ICH can be identified with both in utero US and MR imaging. The advantages of MR include better soft tissue resolution and simultaneous evaluation of multisystem malformations in one scan [15]. On foetal MR, the characteristics of ICH show an atypical signal because ICH is occasionally detected or suspected on routine US screening of pregnancies. At this time, foetuses will exhibit no specific symptoms. In this study, most ICHs were magnified as relatively high signals on T1WI, intermediate signals on T2WI and high signals on DWI. The margin of the haematoma could be better outlined on DWI (Fig. 4–6.) than in the other two protocols. Furthermore, we also calculated the size of the haemorrhagic components in each case (similar results were not reported in the previously published literature) and found that the volume of the detected haematoma seemed larger in the late gestation than in the early gestation. However, the volume of the haematoma did not show a significant difference across either the gestation or the anatomic compartments at the statistical level. In one study, the authors reported that GM-IVH occurred more frequently and later in pregnancy than non-GM haemorrhage [16]. In our study, both GM-IVH and cerebellum [17] bleeding occurred in early pregnancy, and corpus callosum haemorrhage was only detected in later pregnancy. However, due to the limited number of included samples, this needs to be validated in a larger sample.

Many causes could be responsible for foetal ICH, including infectious disease, maternal drug exposure, alloimmune thrombocytopenia, maternal trauma, coagulation disorders, twin-to-twin transfusion syndrome (TTTs), etc. [18]. A genetic disorder should be taken into account as the potential cause for many indeterminate cases. In the present study, we only performed gene analysis in one case (Fig. 6). For all 10 twin pregnancies in the included samples, TTTs was the most common indication for foetal ICH evaluation [19]. In terms of coexistent complications, 42 (51.8%) cases had abnormal findings apart from ventriculomegaly on in utero MR. For singleton pregnancies, 3 foetuses with ICH had gyri malformations, 1 foetus had TCS, and 13 foetuses with porencephaly were observed in this study. For twin pregnancies, hydrops foetalis was the most commonly detected abnormal finding, although this complication may not be associated with foetal ICH itself. Furthermore, in this study, the number of haemorrhagic lesions did not show a correlation with the haematoma volume but had some correlations with the haematoma mass effect itself. In the present study, 58 pregnancies had the final outcome recorded by either correspondence with the involved patients or by searching the inpatient medical records through a stillhospital information system. Among them, 1 stillbirth and 2 foetal deaths (one in a singleton and one in a twin pregnancy) were recorded. Additionally, the volume of haemorrhagic components did not show a correlation with the final outcome in the present study [17]. Neurodevelopmental outcomes were not evaluated owing to the short follow-up period. Comparatively, twin pregnancies have more complicated complications and poor prognoses [20]. On the one hand, these pregnancies had predisposed disease (herein, TTTs are the underlying aetiology); on the other hand, some invasive reduction surgery was performed for foetuses with growth restriction. A large amount of haematoma was not observed in this cohort of twin pregnancies on prenatal MR.

Our study has some limitations. First, a relatively small number of infants were followed up after birth. A longer follow-up time will help better assess the neurodevelopmental outcome for foetuses with ICH in utero. A high rate of termination of pregnancy can underestimate the occurrence of adverse outcomes. Second, in this study, 1.5T MR equipment was applied. Although it has not yet been well evaluated for intrauterine examinations, 3.0T foetal MR with a high signal-to-noise ratio and fast scanning protocols may improve the image resolution [21]. Future studies will help to clarify the differences in imaging characteristics in foetal ICH between these two MR strengths.

Prenatal MR imaging could better show the ICH morphology and the associated abnormal findings. As a complementary tool of US, MR imaging could help with prenatal counselling and treatment selection after birth.

ICH Intracranial haemorrhage

GM-IVH Germinal matrix intraventricular haemorrhage

MRI Magnetic resonance imaging

HASTE Half-Fourier single-shot turbo spin echo

DWI Diffusion-weighted imaging

US Ultrasound

VM Ventriculomegaly

GA Gestational age

GW Gestational week

TOP Termination of pregnancy

FIESTA Fast imaging employing steady-state acquisition

sIUGR, Selective in-utero growth restriction

TAPs Twin anemia-polycythemia sequence

TTTS Twin-twin transfusion syndrome

IVF In vitro fertilization

Authors’ contributions

H. Zhang and G. Zhang designed of the whole study; X. Liu and Y. Lu performed the experiments and analyzed the raw data; T. Wang prepared US reports; H. Zhu collected clinical data; Y. Bai performed statistical analysis; X. Liu and Y. Lu wrote the first draft; H. Zhang and G. Zhang revised and wrote the manuscript finally.

Consent to participate

The requirement for the informed consent of all participants was waived (IRB No.2020-138). The signed consent for further MR scan was obtained from each pregnancy when have indeterminate anomalies on screening ultrasound. This consent will comprehensively tell each pregnancy that indications, contraindications, advantages, limitations and potential medical use on MR imaging.

Consent to publish

Verbal informed consent for publication was obtained from the pregnancies to usage these clinical and imaging data (Figure 2- 8).

Ethics approval

Obstetrics and Gynecological hospital, Medical College, Fudan University of institutional review board approved the study and the requirement for the informed consent of all participants was waived by Obstetrics and Gynecological hospital, Medical College, Fudan University institutional review board

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

The authors declare that all data supporting the findings of this study are available within the article.

Acknowledgements:

This project is supported by Shanghai Natural Science Funding Project (No. 19ZR1407200, Receptor: Dr. Guofu Zhang).

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No competing interests reported.

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Intracranial hemorrhage and additional anomalies detected on prenatal magnetic resonance imaging: a large, retrospective study in two tertiary medical institutions

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Abstract

Purpose

Methods

Results

Conclusion

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Introduction

Methods

Study population

MRI acquisition and interpretation

Postnatal follow-up

Statistical analysis

Results

General information

MRI findings

Outcomes and follow-up of liveborn foetuses

Discussion

Conclusion

Abbreviations

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References

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