We performed a prospective cohort study of 13 foetuses whose mothers, aged between 20 and 38 years and with no risk factors, consecutively sought prenatal care for a normal pregnancy starting at the eight postmenstrual week in the Department of Obstetrics and Gynaecology of our hospital in 2005. The project was approved by the ethics board of the hospital, and the mothers signed the informed consent form after being told that second-trimester monthly ultrasound explorations would be prolonged by 30min to analyse foetal movements and that this was a harmless procedure, adhering to the criteria of the International Society of Ultrasound in Obstetrics and Gynecology (ISUOG).14,15 Every foetus in the cohort (seven females and six males) was born to term in an eutocic delivery and had a normal weight, length, and head circumference and an Apgar test score ranging from 9 to 10 measured between the first and fifth minute after birth. On the third day after birth, the spontaneous behaviour of every newborn while awake and not crying included a type of general movement known as writhing movements,16,17 and the rest of the conventional neurological examination 18–21 was normal in all subjects. Regular paediatric follow-up visits until 5 years of age confirmed that all 13 subjects had normal psychomotor and language development and academic performance.

Transabdominal ultrasonography was performed with a Voluson 730 machine (G.E. Healthcare, Milwaukee, USA) with a 2-5MHz probe. The morphological examination was done using the 4D mode (movement on three planes), and the foetal wellbeing parameters and spontaneous movements were assessed using the 2D mode (movement on one plane) at weeks 12, 16, 20, and 24 of gestation. The machine scans 40 frames per second in 2D mode, which allowed the observation of foetal movements with no breaks in continuity. The safety indices used were a mechanical index of 0.9 and a thermal index of 0.1, as recommended by the ISUOG.14,15 All examinations were performed 3h following the last intake of food by the mother, at an environmental temperature between 23°C and 26°C and in the absence of extraneous noises or interferences. The analogue U-Matic recordings were digitised. A single obstetric ultrasonographer (JLA) acquired all the material, while two neuropaediatricians (CR and JN) performed the visual analysis of the recordings of foetal movements.

We defined the applicable observation time (OT) of foetal activity as the period of the 2D ultrasound during which the ultrasound image contained a full parasagittal plane of the foetal body without external stimulation (Table 1). We documented the heart rate of the foetus during periods of motor activity and periods of quiescence. Following an initial examination of the material, we decided to limit our analysis to the five movement patterns that were most prominent:

• –

  Startle (S): a sudden and isolated extension of the trunk in the cephalocaudal direction lasting between 1 and 3s and without active movement of the extremities.2,9

• –

  Axo-rhizomelic rhythmias (ARRs): excursions along the cervicodorsal axis that travel symmetrically along the proximal portions of the four extremities, occurring in rhythmic clusters.

• –

  Axial stretching (AS): tonic posture in axial extension held for two or more seconds; it may be restricted to the cervical region or extend to the rest of the body axis, with negligible movement of the limbs.4

• –

  General movements (GMs): complex movement patterns that combine flexions, extensions and rotations, with the asynchronous involvement of different parts of the trunk and extremities and of varying speed, amplitude, and direction.2,7,10 The morphology of GMs is fluid and unpredictable, and their complexity and variety increase during the second and third trimesters. MGs continue to appear in waves with increasing duration, complexity and variability through the second month post-term during quiet wakefulness and REM sleep.10,13,16–18

• –

  Diaphragmatic contractions (DC): series of contractions of the diaphragm, irregular in speed and rhythm, in clusters of 1–10 beats. Other published works refer to these as “hiccups” and “breathing movements”,2,5,6,9,10 but since they do not have those functions in the foetus, we have interpreted them phenomenologically as practising diaphragmatic movements.

Any observed occurrence of these five movement patterns at 12, 16, 20, and 24 weeks of gestation (total number of events) was recorded in the data sheet, and we calculated their incidence (mean number of events per 10min of observation) for the entire series for each point in time. We calculated the total time during which foetal movements were observed, as well as the time spent in each type of movement and on all the five target movements combined. We classified movements as isolated or clustered depending on their rhythm, and as short or long based on the amplitude of the displacement (Table 1).

We conducted a longitudinal study with repeated measures allowing for the description of foetal movement patterns through the four observation dates during the second trimester of gestation and the term neonatal period by means of a mixed linear model. We used the SPSS 10.0 software to calculate the descriptive statistics of quantitative variables for each movement pattern and did a repeated measures ANOVA to compare the patterns at different gestational ages. The nominal variables that characterise foetal movements were analysed using the Friedman test.

Foetal movement was observed on a mean 29.7% of the OT. Startles were the most frequent movements among the five target-patterns of our study, as they occurred in every foetus at a rate of 13.8 startles per 10min. They usually appeared clustered in arrhythmic clusters of 2–15 successive startles; sometimes a cluster of startles was followed by a GM. ARRs were observed in 11 foetuses and amounted to 4.17% of the total motor activity time. Isolated AS movements restricted to the cervical region were observed in three foetuses. GMs were clearly discernible in 10 foetuses, with a mean incidence of five events per 10min, amounting to 13.3% of the OT. The presence of DCs was only observed in three foetuses; they were short in amplitude and occurred in isolation or in clusters.

There was evidence of foetal movement for a mean 23.8% of the total OT. Motor behaviour was more organised, as movements were frequently combined, with one leading to another. The incidence and duration of AS, GMs, and DCs increased; the latter usually had a short amplitude and occurred in clusters. In contrast, the observed presence of the simpler and more abrupt movements, startles and ARRs, started to decline (Table 1). The most prevalent events were GMs, as they were observed in every foetus and amounted to 12.3% of the OT. The presence of ARRs decreased by half, with very few events per foetus.

Motor activity became slower and more complex, as simpler and more abrupt movements, like startles and ARRs, decreased dramatically in their presence and incidence, while the considerable presence of AS and GMs was sustained, with these patterns accounting for most of the foetuses’ motor activity, amounting to 19.7% of the OT. Both AS and GMs were observed in eight foetuses; AS was observed in three foetuses that did not have any GMs at this time point; conversely, GMs were observed in two foetuses in whom no AS was detected at this age; while it was only in one foetus that neither GMs nor AS was detected, although they were detected in the preceding and following examinations. Clusters of AS were clearly perceived in 12 foetuses.

The five target movements accounted for 80% of the total foetal motor activity at this age. The incidence of all patterns decreased compared to previous weeks, but the behaviour patterns increased in complexity and duration. Startles were disappearing and ARRs were only observed in three foetuses. Meanwhile, AS and DCs were observed in 12 foetuses and amounted to 1.9 and 4.6% of the OT, respectively. Compared to the preceding gestational weeks, the patterns with the highest incidence at this age were GMs and DCs, which accounted for 27.8% and 35% of the total foetal motor activity, with characteristics that were similar to those observed at earlier ages.

It is apparent from Fig. 2 and Tables 1 and 2 that the shortest and fastest foetal skeletal movements (S and ARRs) were observed very frequently in week 12 and then gradually decreased until they practically disappeared by week 24. In contrast, the presence of slow, prolonged and arrhythmic movement patterns involving the trunk increased gradually. Thus, AS was observed in an increasing number of foetuses throughout the second trimester of gestation. GMs were observed in most foetuses at 12, 20 and 24 weeks of postmenstrual age, and were seen in the entire sample at week 16 (Fig. 3).

Figure 2.

(a) Presence of startles and axo-rhizomelic rhythmias at the four observation times in the second trimester of gestation (12, 16, 20 and 24 weeks) and the term neonatal period (NB). (b) Presence of axial stretching, general movements and diaphragmatic contractions at the four observation times in the second trimester of gestation (weeks 12, 16, 20 and 24) and the term neonatal period (NB).

(0.13MB).

Figure 3.

(a) Incidence of startle events (in vertical axis) in the 13 foetuses at the four observation times in the second trimester of gestation (in horizontal axis: weeks 12, 16, 20 and 24). (b) Incidence of general movements (in vertical axis) in the 13 foetuses at the four observation times in the second trimester of gestation (in horizontal axis: weeks 12, 16, 20 and 24).

(0.09MB).

Consistent with the above, the percentage of time spent in startles and ARRs declined from week 12 throughout the second trimester of gestation, while the time spent in episodes of AS increased from week 20 in comparison to week 12. GMs occurred in most foetuses at the four observation times, but motor events had a shorter duration as gestational weeks passed. The mean incidence of motor events was lower at week 24 compared to preceding weeks.

Diaphragmatic contractions were observed rarely at week 12, but they were detected in 11 foetuses from week 16, and amounted to an increasingly longer portion of the observation time through the end of the second trimester. Diaphragmatic movements usually occurred in clusters of several arrhythmic excursions of short amplitude; they frequently appeared as diaphragmatic flutters or “hiccups”.