The earliest emergence of fetal motility was first described by three groups7, 8, 34. What all three studies had in common is that they described movement occurring at one or two poles of the fetus (head or rump) as small slow displacements, and with movement occurring between 7 and 8 weeks and disappearing thereafter.
For later emergence, the differentiation of the various movement patterns was divided initially into three categories, depending primarily on the gestational age at which the movements were observed25, 26, 28, 34. Birnholz et al.13, Ianniruberto and Tajani7 and de Vries et al.8 further differentiated movement into 16 patterns. These three groups of investigators differentiated increasingly the classification of the body part participating and how the movement is performed qualitatively. The classification system of de Vries et al.8 is the most reproducible since it is independent of gestational age and is derived from the nomenclature used for preterm and full-term infants. The emergence of SMPs is presented in Figure 2, using data derived from de Vries et al.8 and from the eye movements from 14 weeks onwards as reported by de Elejalde and Elejalde15. A further categorization into four eye movements was published by Birnholz14. Other facial activities, such as eyelid opening, appear from 26 weeks15. Activities such as grimacing, non-nutritive sucking and tongue protrusion, as seen near term, have not been examined for their emergence36.
The earliest physiological form of tactile stimulation was described by Piontelli et al.23, who examined the SMPs in twins as did de Vries et al.8 and demonstrated reactions after stimulation from the cotwin from 11 weeks onwards. They observed, however, no specific evoked response.
Besides specifying movement patterns, describing qualitatively how the movement is performed has also served its purpose for obtaining insight into the emergence of motor activity. The majority of SMPs are performed qualitatively, movements being performed fluently with varying amplitude, speed and participating body parts, waxing and waning during one burst, from the moment they emerge8. Qualitatively, all SMPs are performed strikingly similarly throughout gestation. Exceptions to this are startles, hiccups, isolated twitches, and cloni of the arm, leg or head (retroflexion). Startles and hiccups occur frequently during the first trimester, which led to descriptions such as those mentioned by Reinold25 (fluctuating movements at 8–12 weeks, strong and sudden movements at 13–16 weeks and low and inert movements in the body and extremities at 17–18 weeks). Looking at the overall impression of startles and hiccups, quick displacements of trunk, head and extremities are seen. However, checking carefully for where the movement is initiated shows that startles begin in the extremities and hiccups in the diaphragm. The other body parts can have large displacements, but are merely moved passively.
The fact that, qualitatively, the SMP remains recognizable throughout gestation facilitates quantification. All SMPs except non-nutritive sucking, grimacing and tongue protrusion36 have been studied with respect to their emergence; breathing and eye movements have been studied most (39 and 31 times, respectively).
Early asymmetrical development was first reported by Hepper et al.18, with more right thumb-sucking from 15 weeks17 and more frequent right arm movements from 10 weeks.
The relationship between meals eaten by the mother and increased fetal breathing in the 2nd hour after the meal was first found to occur from 30 weeks onwards21, but this was later noted as early as 20 weeks37.
Diurnal rhythm in breathing movements, general movements, and both together were found to begin as early as 20 weeks37.
Behavioral states were first reported to emerge at 38 weeks9. Thereafter evidence was found that they appear at 36 weeks, and the change of no coincidence of the state parameters to coincidences with short transition time develops gradually over the time period of 28 weeks until term for 1F to 2F11.
In summary, most notable from this review of developmental milestones in the emergence of motor activity, as found within the limitations of 2D sonography, are the early onset of SMPs, their similarity in quality of performance throughout gestation, and the start of coordinated behavioral state parameters at 36 weeks.
Quantitative data are available for all SMPs during both the first43 and second68 halves of gestation, and age-related development of each movement pattern has been described. All investigators have reported impressive inter- and intrafetal differences, resulting in a wide range of observed motor activity in uncomplicated pregnancies. Roodenburg et al.68 found a higher percentage of general movements at 20 weeks (24%; range, 5–47%) than did de Vries et al.16 (10%; range 5–21%). Ten Hof et al.73 made important progress in understanding these differences with their examination of the normative data on a burst of general movements, pointing out that the various authors applied different smoothing procedures to predefine interburst intervals (de Vries et al.16: 1 s; Roodenburg et al.68: 5 s). Unsmoothed assessment of general movements showed a 16% incidence at 24–26 weeks and a decrease to 8–10% near term.
Ranking of the quantity of SMPs, from most to least frequent, was found to be strictly age-related as examined during the first half of gestation between 16.00 and 18.00 h37. This ranking demonstrated high interfetal consistency, with general movements ranked first at every age. Second in rank were startles at 8–9 weeks, hiccups at 10–13 weeks, and breathing movements at 14–19 weeks. Observations at three other times of day at 13 weeks showed that hiccups remained high in rank, but could be replaced in second rank by retroflexion of the head at 08.00 h and breathing at 13.00 h. At 20–22 weeks, monitoring at 09.00–11.00, 13.00–15.00, and 22.00–24.00 h demonstrated that general movements remained first in rank and breathing second, each with one exception: general movements were replaced from their first place ranking once by breathing at 13.00–14.00 h and breathing was displaced once to third rank by jaw opening at 10.00–11.0016.
Conflicting reports were found with respect to sex differences. de Vries et al.16 found no sex-related differences in the various SMPs during the first half of gestation and also no differences in general movements in the second half of gestation. The latter was confirmed by Robles de Medina et al.67. Others found more mouth movements in females throughout gestation49.
Asymmetrical development of hand–head contacts could not be demonstrated by de Vries et al.44. Despite the fact that unimanual contact is preferred from 30 weeks onwards, no co-development with head preference to the ipsilateral side was found.
Qualitatively, Kozuma et al.51 described the performance of motility involved in all body parts, emphasizing a more detailed categorization than that for general movements. They described upper and lower extremity activities, as well as upper, lower and whole trunk activity. The latter was categorized according to flexion, stretch, rolling, startle, stepping and writhing.
Studies on temporal patterning have been performed on several SMPs. Startles, frequently seen early in gestation, have no regular duration of the interval between them either then or later in pregnancy. This is in contrast to hiccups, which are also found frequently early in gestation and which have the same interval between them throughout gestation (1–3 s)43. For breathing movements the most common interval at 12 weeks is 2–3 s, at 19 weeks it is 0–1 s43, and after 30 weeks it is 1–1.3 s74. The most frequently occurring SMP during the whole of pregnancy, general movements, also has age-related development. At their emergence, general movements are short-lasting and have short pauses. During the first half of gestation the duration of general movements and the pauses between bursts of general movements increase43. de Vries et al.43 also found rest periods not exceeding 13 min before 20 weeks. In the second half of gestation, Ten Hof et al.72 demonstrated a further increase in pauses, and a reduction in the number of bursts with unaltered duration. They explained the reduced percentage incidence as being due to age. From its introduction, the behavioral state variable gross movement has been analyzed through a 3-min moving window technique9. This technique tests every 30 s if the various state variables meet the 1–4F criteria throughout a 3-min window. This eliminates short-lasting motor activities. Subsequently this technique has been accepted widely for adequate behavioral state analysis. However, with the present knowledge available on long pauses between general movement bursts, this window is now known to interfere with an otherwise well-organized 2F. Also, short-lasting bursts of general movements can interfere with an otherwise stable 1F72. Every 90 min the four behavioral states occur. The median value of resting (1F) is 20 min9, and the longest is 45 min. Only 1% of cases exceed 45 min, with values recorded of up to 75 min62.
In summary, the most noteworthy findings with respect to milestones in the developmental aspects of motility are, on the one hand, the impressive variability in the quantity of the various SMPs and, on the other hand, the age-related longest pauses between the general movements and the ranking of SMPs. The first finding limits, while the second facilitates, their application for diagnostic purposes.
Qualitatively, all SMPs are similar before and after birth, although after birth the force of gravity can affect certain SMPs (for example, anteflexion of the head) and makes movements less fluent and elegant; a sudden relaxation of an elevated limb before birth results in a fluent downwards movement and does not produce a rapid drop as seen after birth.
Quantitatively, general movement rates at 38 and 40 weeks show continuity with 2 and 4 weeks postpartum83. From a study on development of various hand movements (seven categories) the fetal hand-to-head/face at 32 weeks best predicted the neonatal movements71. Right-handed thumb-sucking before birth showed continuity with right handedness after birth84.
The prevalence of behavioral states 1F, 2F and no coincidence of state parameters is the same before and after birth. However, fewer transitions occur before birth and the transitions are shorter after birth82.
In summary, the important progress in knowledge on continuity of motor activity is the continuity in SMPs and behavioral states observed. A drawback here is the limited number of relevant studies.
The agreement between sonographically examined movements and what the mother feels has been examined in six studies90, 104–108. When participating body parts were specified, the mother felt 82% of movements in the case of trunk and limbs, and only 56% in the case of limbs only104. As for the duration of sonographically examined movements, those lasting more than 3 s were felt in 83.9% of cases, those lasting 1–3 s were felt in 64.9% of cases and those lasting < 1 s were felt in 51.1% of cases108.
Various articles have reported on the relationship between SMP and FHRP, namely, accelerations in FHRP in relation to trunk with/without arm or leg movements (71%), arm/leg movements (18%), breathing or contractions (7%), and movements not recognized sonographically (4%)105. Van Woerden et al.113 also reported FHR increases during hiccupping and breathing movements and FHR oscillation induced by regular mouthing115. Basal FHR decreases and accelerations and increases in FHR variation from 20 to 38 weeks were reported by Swartjes et al.109
Nine articles have reported on relationship with behavioral states36, 87, 91, 97–100, 103, 113. For example, during 1F, there is mainly (74%) regular mouthing and little jaw opening, tongue protrusion, yawns and grimaces (5–16%), whereas during 2F there is always jaw opening, frequent tongue protrusions, yawning and grimaces36. Startles, hiccups and breathing are state-related103, 113. Breathing occurs more in 2F than it does in 1F, but is dependent on glucose intake. Behavioral states are not influenced by Braxton Hicks contractions or vice versa99.
Six studies have reported on the influence of motility on blood flow parameters92, 93, 101, 102, 110, 111: the pulsatility index (PI) of the umbilical artery, descending aorta, and internal carotid artery is higher in 1F than it is in 2F, and the pulse waveform of the aorta is higher in 1F than it is in 2F during and without breathing. The difference in the umbilical artery PI disappears when no breathing movements are present. Breathing increases the inferior vena cava flow. The PI of the renal artery is identical in 1F and 2F despite the fact that fetuses urinate during the transition from 1F to 2F.
In summary, with respect to milestones in the relationship between fetal motor activity and other parameters, it is important to realize how little the mother actually feels of fetal movement, while in contrast, how well even the smallest fetal motion, such as non-nutritive sucking, is represented by FHR variation. Another noteworthy development in our knowledge is the finding that blood flow velocity and motility are closely related and modulated in the healthy fetus.