Abstract
BACKGROUND:
A few studies have been reported on the influence of fetal hiccups on umbilical artery. The aim of this study is to clarify the influence of fetal hiccups on Doppler blood flow waveform (DBFW) of some fetal arteries, and to show the difference in these influences among fetal arteries.
OBJECTIVE:
DBFW of umbilical artery, descending aorta, and middle cerebral artery were recorded at hiccups in normal fetuses between 34th and 40th gestational weeks. The changes on DBFW were classified into three shapes by the direction and the size of the changes. Shape 1: sharp decrease but not to the baseline, Shape 2: sharp decrease to the baseline (absence), and Shape 3: reverse flow.
RESULTS:
At all hiccups, the changes on DBFW of these arteries were observed. These changes were classified into three shapes. Changes of umbilical artery were widely distributed in three shapes depending on when hiccup occurred during cardiac cycle. On the other hand, most changes of the descending aorta and middle cerebral artery were Shape 3 whenever the hiccup occurred during cardiac cycle.
CONCLUSION:
The changes on DBFW of fetal arteries were observed at all hiccups. Changes of umbilical artery were widely distributed in three shapes depending on when hiccup occurred during cardiac cycle. On the other hand, most changes of descending aorta and middle cerebral artery were Shape 3. This is the first study clarified the influence of fetal hiccups on DBFW of some fetal arteries, and showed the difference in these influences among fetal arteries.
Abbreviations
Doppler blood flow waveform
Introduction
Ultrasound B-mode examination is widely used in obstetric practice, and fetal hiccups can occasionally be recognized during examination. A few studies have been reported on the influence of fetal hiccups on Doppler blood flow waveform [DGFW] of fetal umbilical artery. Muller et al. reported decreased or reversed blood flow of fetal umbilical artery at hiccups in normal fetuses or complicated fetuses with intrauterine growth restriction (IUGR), malformation or anemia [1]. However, no study has been reported on the influence of fetal hiccups on DBFW of another arteries in normal fetuses.
The aim of this study is to clarify the influence of fetal hiccups on DBFW of the umbilical artery, descending aorta, and middle cerebral artery in normal fetuses and to show the difference in these influences among fetal arteries.
Materials and methods
DBFW of the umbilical artery, descending aorta, and middle cerebral artery were recorded when fetal hiccups were observed during ultrasound examination of pregnant women between 34th and 40th gestational weeks for six years from January, 2014 to December, 2019. Fetuses with complications such as IUGR, malformation, poly or oligohydramnios, multiple pregnancy or with poor outcomes were excluded. Ultrasound examination was performed using Volson730 Expert BT08 with probe RAB2-5L (1.0–4.0 MHz) and VolsonE10 BT15 with probe RM6C (1.0–7.0 MHz) (GE Healthcare UK Ltd, Amersham Place, Little Chalfont, Buckinghamshire HP7 9NA, England).
The study protocol was prepared according to the principles of the Declaration of Helsinki. The study was approved by the Institutional Ethics Committee, and was performed after obtaining informed consent from all pregnant women.
Classification of changes on DBFW at hiccups
The changes on DBFW of the umbilical artery, descending aorta, and middle cerebral artery were observed at all fetal hiccups (Figs. 1, 2). And the changes on DBFW were classified into three shapes by the direction and the size of the change (Fig. 3). Shape 1: Sharp decrease but not to the baseline. Shape 2: Sharp decrease to the baseline (absence). Shape 3: Reverse flow.
Doppler blood flow waveform (DBFW) of the umbilical artery at fetal hiccups. Changes on DBFW were observed at all hiccups (arrows). The shape of the change on DBFW at hiccup varied depending on when hiccup occurred during the cardiac cycle.
Changes on DBFW of the descending aorta (a) and middle cerebral artery (b) at fetal hiccups (arrows). Reverse flow on DBFW were observed at hiccups (arrows) in both arteries.
Three shapes of changes on DBFW at fetal hiccups (arrows). Shape 1: Sharp decrease on DBFW at hiccup but not to the baseline, Shape 2: Sharp decrease on DBFW at hiccup to the baseline (absence), and Shape 3: Reverse flow on DBFW at hiccup.
Peak-systolic (ps) blood flow velocity (BFV) and end-diastolic (ed) BFV were measured on DBFW at hiccups by caliper in the machine (Fig. 4). Furthermore, peak-systolic minus bottom (pmb) on Shape 1 DBFW, and reverse peak (rp) BFV on Shape 3 DBFW were measured (Fig. 4).
Measured parameters on DBFW. Peak-systolic (ps) blood flow velocity (BFV), and end-diastolic (ed) BFV were measured on DBFW at all hiccups. Peak-systolic (ps) BFV minus bottom BFV (pmb) on Shape 1 change on DBFW, and reverse peak (rp) BFV on Shape 3 change on DBFW were measured.
The study included 498 hiccups in 107 fetuses of 107 pregnant women. And the changes on DBFW of the umbilical artery, descending aorta, and middle cerebral artery were observed at all 498 fetal hiccups.
Classification of changes on DBFW at hiccups
The results of the classification of changes on DBFW of the umbilical artery, descending aorta, and middle cerebral artery are presented in (Table 1).
Changes on DBFW of the umbilical artery, descending aorta, and middle cerebral artery at fetal hiccups
Changes on DBFW of the umbilical artery, descending aorta, and middle cerebral artery at fetal hiccups
Changes on DBFW of umbilical artery were recorded at all the 406 hiccups in 82 fetuses. Shape 1 changes were recorded at 148(36.3%) hiccups, Shape 2 changes were at 114(28.1%) hiccups, and Shape 3 changes were recorded at 139(34.2%) hiccups. Five (1.2%) changes could not be classified. Thus, the changes on DBFW of fetal umbilical artery at hiccups were widely distributed in all three shapes depending on when hiccup occurred during cardiac cycle (Table 1).
Descending aorta and middle cerebral artery
The changes on DBFW of the descending aorta were recorded at all the 24 hiccups in 11 fetuses. Sharp 1 change was recorded at one (4.1%) hiccup, and Shape 3 was at 23 hiccups (95.8%). The changes on DBFW of middle cerebral artery were recorded at all the 68 hiccups in 14 fetuses. Shape 1 changes were recorded at two (2.9%) hiccups, Shape 2 changes were at two (2.9%) hiccups, and Shape 3 changes were at 64 (94.1%) hiccups. Thus, Shape 3 was extremely more frequent than other Shape in descending aorta or middle cerebral artery (p < 0.0001). Most changes on DBFW of descending aorta and middle cerebral artery were Shape 3 whenever hiccups occurred during cardiac cycle (Table 1).
Characteristics of changes on DBFW of umbilical artery at hiccups
The characteristics of changes on DBWF of umbilical artery was shown in Table 2. Changes on DBFW of umbilical artery were recorded at all the 406 hiccups in 82 fetuses. The gestational age of these fetuses was 36.0±5.5 (range, 34–40) weeks. The peak-systolic (ps) BFV was 45.1±11.6 (range, 12–80) cm/s, and the end-diastolic BFV was 18.7±5.9 (range, 8–35) cm/s.
Characteristics of DBFW of the umbilical artery
Characteristics of DBFW of the umbilical artery
n, number of category; BFV, blood flow velocity.
Peak-systolic minus bottom (pmb) of BFV was 36.2±10.3 (range, 4–64) cm/s in 148 Shape 1 hiccups, and reversed peak BFV was 14.3±7.1 (range, 4–48) cm/s in 139 Shape 3 hiccups. The shape of the change on DBFW at hiccup varied depending on when hiccup occurred during cardiac cycle. Therefore, the standard deviations of peak-systolic minus bottom (pmb) of BFV in Shape 1 change, and of reversed peak (rp) BFV in Shape 3 change were relatively large.
Ultrasound B-mode examination is widely used in obstetric practice, and fetal hiccups can occasionally be recognized during examination. Fetal hiccup is an unexplained phenomenon, and only a little is known about this phenomenon. Murchison presented the hypothesis that hiccups promote amniotic fluid influx to the primitive gut, allowing fluid to be transferred to the fetal and then maternal vasculature [2]. Pillai et al. described fetal hiccup are the most dominant form of early diaphragmatic activity, giving way later to rhythmic fetal breathing movement [3].
DBFW examination of umbilical artery and middle cerebral artery is widely used to estimate fetal condition. The decrease of end-diastolic blood flow until absent and then reverse flow in umbilical artery is reported in the cases of IUGR or oligohydramnios [4, 5]. And the increase of end-diastolic blood flow in the middle cerebral artery is associated with increased risk of adverse perinatal outcomes [6, 7].
A few studies were reported on the influence of fetal hiccups on DBFW of fetal umbilical artery. Muller et al. reported decreased or reversed blood flow of fetal umbilical artery at hiccups in normal fetuses or complicated fetuses with IUGR, malformation or anemia [1]. However, no study has been reported on the influence of fetal hiccups on DBFW of another arteries in normal fetuses.
The aim of this study is to clarify the influence of fetal hiccups on DBFW of some fetal arteries, and to show the difference in these influences among fetal arteries. In this study, the changes on DBFW of umbilical artery, descending aorta and middle cerebral artery were observed at all 496 hiccups in 107 normal fetuses. These changes were classified into three shapes: Shapes 1, Sharp decrease, 2, Absence, and 3, Reverse by the direction and size of the change.
Changes on DBFW of fetal umbilical artery at hiccups were widely distributed in all three shapes depending on when hiccup occurred during cardiac cycle. Therefore, the standard deviations of peak-systolic minus bottom (pmb) of BFV in Shape 1 change, and of reversed peak (rp) BFV in Shape 3 change were relatively large. On the other hand, most changes on DBFW of descending aorta and middle cerebral artery were Shape 3 whenever hiccup occurred during cardiac cycle. This may be because of the descending aorta and middle cerebral artery are nearer to the heart than the umbilical artery.
This is the first study classified and clarified the influence of fetal hiccups on DBFW of the umbilical artery, descending aorta and middle cerebral artery in normal fetuses, and showed the difference in these influences among fetal arteries.
We evaluated the mechanisms behind these changes on DBFW of the umbilical artery, descending aorta, and middle cerebral artery at fetal hiccups. Levi et al. studied the change on DBFW of the aortic and pulmonic valves at fetal hiccups and reported transient reduction of peak flow velocity at aortic and pulmonic valves in systolic cardiac cycle, and transient reversed flow at aorta and ductus arteriosus in diastolic cardiac cycle at fetal hiccups [8]. Mathew studied the relationship between hiccups and arterial pressure in intubated preterm infants. He showed that when hiccups occurred during early systole, the systolic pressure decreased, and when hiccups occurred during early diastole, the diastolic pressure decreased [9]. Owing to these results, the changes on DBFW of the umbilical artery, descending aorta and middle cerebral artery are supposed to be caused by decrease of the output from the aortic valve due to decrease of blood pressure in the aortic value.
What is the mechanism that the blood pressure in the aortic valve decrease during fetal hiccups? Hiccup has been recognized to be caused by involuntary spasmodic contractions of respiratory muscles such as diaphragm, external intercostal muscles, or superior posterior serratus muscles, with sudden closure of the glottis. These spastic contractions of the respiratory muscles suddenly decrease the intrathoracic pressure of the fetus. This sudden decrease of the intrathoracic pressure decreases the pressure in the aortic valve of the fetus. Mathew reported that systolic blood pressure decrease at hiccups in intubated preterm infants, and this results indicate that transient decreases in intrathoracic pressure at hiccups deduce systemic arterial pressure [9]. This should be the mechanism of the sharp decrease in DBFW of the umbilical artery, descending aorta, or middle cerebral artery at fetal hiccups.
Further studies are necessary to clarify the more details of fetal hiccup or its influence on fetal blood flow.
Conclusion
At all hiccups in normal fetuses, the changes on DBFW of umbilical artery, descending aorta and middle cerebral artery were observed. These changes were classified into three shapes: Sharp decrease, absence or reverse. The changes on umbilical artery were widely distributed in three shapes depending on when hiccup occurred during cardiac cycle. On the other hand, most changes of descending aorta and middle cerebral artery were reverse whenever the hiccup occurred during cardiac cycle.
This is the first study clarified the influence of fetal hiccups on DBFW of umbilical artery, descending aorta and middle cerebral artery, and showed the difference in these influences among fetal arteries.
Footnotes
Disclosure statements
The authors declare no conflict of interest.