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Keywords:

  • assessment procedures;
  • developmental milestones;
  • normal fetal motility;
  • sonography

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

After 35 years of real-time two-dimensional sonography, and now that 4D sonography is within our grasp, this article presents an overview of present-day knowledge of normal fetal motility. A literature search was carried out on articles from 1970, using the keywords: ‘fetal’, ‘movements’, ‘motility’, ‘movement patterns’, ‘ultrasound’ and ‘sonography’. Inclusion criteria were human studies and use of real-time sonography. Articles were screened for type of motor assessment procedure, in terms of whether they: specified movements for participating body parts (specific movement pattern, SMP), were qualitative (performance in terms of speed and amplitude), were quantitative, identified behavioral states, stated the duration of observation, and specified gestational age. We noted developmental milestones obtained for each study aim. One of four aims was identified for each article, depending on whether it focused on emergence, development, or continuity after birth of the movement patterns, or on the relationship of various motor aspects to other parameters that evaluate fetal condition, such as blood flow and fetal heart rate. A total of 109 relevant articles was identified, examining 9862 fetuses. Assessment was performed primarily with analysis of SMPs (89%); 52% also included non-SMPs (NSMPs), 78% included quantification, 24% assessment of quality, and 32% behavioral states. The duration of observation was 1 h or longer in 50% of the studies. The focus in 28 studies was on emergence, in 44 it was on development, in five it was on continuity and in 32 it was on relationship of the movements with other parameters of fetal well-being. A few milestones identified were determination of the strictly age-related emergence of SMPs and behavioral states, the highly reproducible quality of SMPs throughout gestation, the age-related trends in quantified SMPs, the continuity in quality and quantity after birth, and the close relationship between motility and heart-rate variability, flow parameters, and behavioral states. Periods of longest inactivity recorded before 20 weeks were 13 min; after 30 weeks they were 45 min. Much insight was obtained into the development of motility and its relationship to other parameters from those articles applying comparable assessment procedures. An assessment procedure with well-defined SMPs, qualitative and quantitative aspects of SMPs and NSMPs, and an observation period dependent on age are advocated for future research. Copyright © 2006 ISUOG. Published by John Wiley & Sons, Ltd.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The first scientific publication on human fetal motility, by the obstetrician Erbkam1, was in 1837. The first overview on this subject was published in 1885; Preyer2, a physiologist from the university of Jena (Germany), dedicated a whole chapter to human motility in his book entitled ‘Specielle Physiologie des Embryo’. In that period, specialists from various disciplines examined how and why the fetus moves, performing their investigations within the limitations of both their observational possibilities and their theoretical background. The observational procedures varied from indirect visualization—merely describing maternal wall excursions (Ahlfeld in 1888)3—to direct surveillance of fetuses after spontaneous miscarriage (Erbkam in 1837)1 or Cesarean section in early pregnancy (psychiatrist Minkowsky in 19284; anatomists Hooker in 19525 and Humphrey in 19786). Whereas the obstetrician Ahlfeld in 18883 considered movements visualized indirectly to be spontaneous breathing movements, this was not pursued since at that time physiologists and anatomists considered all movements to be evoked.

The possibility of observing the fetus in its own intrauterine environment was facilitated in the early 1970s by the introduction of two-dimensional (2D) sonography with a number of images per minute sufficient for real-time imaging. From that point on, investigations were performed mainly by obstetricians, with a few, such as Ianniruberto and Tajani7, de Vries et al.8 and Nijhuis et al.9, evaluating the onset of motility and behavioral states, in collaboration with developmental neurologists such as Milani-Comparetti10 and Prechtl8, 9.

After 35 years of real-time 2D sonography and now that 4D sonography (real-time three-dimensional (3D) ultrasound) is within our grasp, the time has come for reflection. What did 2D sonography reveal? Have we gained insight into developmental aspects such as the emergence and development of motor activity, its continuity after birth, and its mutual relationships or relationships with other parameters of fetal health? Has real-time 2D sonography enhanced our understanding of neuromuscular development? Moreover, are the insights gained by researchers in fetal development so convincing and the assessment procedures so reliable that they can be applied in daily practice by obstetric care providers? And finally, if this is the case, is motor assessment taught sufficiently and systematically to those caring for pregnant women?

The purpose of this article is to evaluate present knowledge of fetal motor activity in uncomplicated pregnancies as studied by 2D sonography. Articles obtained from a literature search were examined for the assessment procedure used and the knowledge obtained on milestones in the emergence and development of fetal motor activity, its continuity after birth and its mutual relationship with other parameters of fetal well-being. We discuss which assessment procedures helped determine and elucidate certain milestones in normal fetal motor development, with the ultimate goal of stimulating a focus on assessment procedures in future (4D) research.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

A Pubmed® and Medline® literature search was performed of all articles from 1970 onwards with the following terms: ‘fetal’, ‘movements’, ‘motility’, ‘movement patterns’, ‘ultrasound’, and ‘sonography’. Inclusion criteria were: studies on humans with real-time sonography. In addition, a manual search was performed on the basis of the references found in the articles retrieved. Each publication was then classified according to the assessment procedure that it used, and its aim.

Assessment procedures

Specific movement pattern (SMP)

This procedure involves specification of the movement pattern for that body part which actively participated in the movement, along with initiation and continuation of the movement (head, arm, leg, trunk, or combination of all (general movements))8. Examples of non-specific movement patterns (NSMPs) are total activity, activity, body activity, gross movements, and trunk movements. The latter three items are used frequently in the assessment of behavioral states. The original article by Nijhuis et al.9 stated explicitly that gross movements consist of various SMPs and NSMPs, classified into four distinct behavioral states (see below).

Articles using the biophysical profile as an assessment procedure were not included in this overview, despite the fact that three of the five parameters concern motor activities (one SMP (breathing), one NSMP (body movement) and one qualitative aspect (tone)) are scored 0, 1 or 2. This decision was made because the scores of the five items are summed and therefore hamper insights into, for example, emergence and development, for each motor item.

Quantitative assessment

Quantitative assessment is based on the availability of numerical data (figures or numbers) for each examined movement pattern (SMP and NSMP). Data limited to ‘activity was more or less’ and the like were excluded from the assessment.

Qualitative assessment

Qualitative assessment is based on the description of speed and amplitude of the movement. In the case of the SMPs, ‘general movements’, the participating body parts, the fluency of performance and increasing and decreasing activity levels (‘waxing and waning’) can also be described. The quality of the motility is normal when the various items vary (e.g. between low and high speeds, small and large amplitudes, few and all body parts participating).

Behavioral states

This is the coordination of state parameters as described by Nijhuis et al. in 19829 and consists of the SMP eye movement, the NSMP gross movement/body movement, and four classes of fetal heart rate patterns (FHRP A–D). It results in four fetal (F) behavioral states with varying motor activity levels: 1F, least active (brief gross movements, mostly startles); 2F, active (eye movements, frequent gross movements, mainly stretches and retroflexions and movements of extremities); 3F, more active than 1F (eye movements, no gross movements); 4F, very active (eye movements, vigorous, continual activity including many trunk rotations).

Duration of observation

Duration of observation was divided into four groups: ≤ 15 min, 16–59 min, ≥ 60 min, and unknown.

Gestational age

Age categories at which the studies were performed were divided into four groups: ≤ 20 weeks, > 20 weeks, longitudinally throughout gestation, and unknown.

Aims of the studies

Emergence

Studies on the start of aspects such as movement patterns, behavioral states, and diurnal rhythm.

Development

Studies on how various aspects progress with age.

Continuity

Studies examining whether there is consistency between aspects of fetal and neonatal motility.

Relationship

Studies examining mutual relationships between various motor aspects as well as relationships between motor aspects and other parameters to examine fetal well-being, such as blood flow and FHRP.

At the end of each section, we present the milestones in development in a concise summary for each aim. Raw data are presented per article and not per fetus.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The literature search identified 109 articles examining 9862 fetuses7–9, 11–116. The number of published articles in 5-year groups demonstrates a normal distribution with a peak of activity in motor research between 1980 and 1990 and a decline thereafter (Figure 1).

thumbnail image

Figure 1. Distribution of articles published on fetal motor activity since the introduction of real-time two-dimensional ultrasound.

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Assessment procedure

The various aspects which were examined in the assessment of motor activity are presented for all articles together as well as according to the aim of the investigation in Table 1. The majority of articles have investigated the development of motor activity, while very few have studied continuity of motor activity after birth.

Table 1. Distribution of studies performing motor assessment procedures with respect to aim (emergence, development, continuity after birth and relationship with other parameters)
 EmergenceDevelopmentContinuityRelationshipTotal
  1. (N)SMPs, (non-) specific movement patterns.

n2844532109
SMPs only11194640
NSMPs only560112
Both SMPs and NSMPs121912557
Quantity213842285
Quality1482226
Behavioral states6911935
Duration of observation 
 ≤ 15 min1031418
 16–59 min4110823
 ≥ 60 min92641554
 Unknown540514
Gestational age 
 ≤ 20 weeks1150117
 > 20 weeks173953091
 Unknown00011

In the SMP research, breathing movements have been studied most, followed by eye movements (78 and 62 times, respectively). Approximately the same SMPs have been examined for each aim.

Milestones of each aim

Emergence7–9, 11–35

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.

thumbnail image

Figure 2. Emergence of specific fetal movement patterns with time (data from de Vries et al.8 and de Elejalde and Elejalde15).

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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.

Development37–80

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.

Continuity81–85

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.

Relationship36, 86–116

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.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

This review of the literature has yielded a number of important results regarding fetal motor activity. We have summarized the developmental milestones in fetal motor activity. The SMPs, with their clear qualitative description, facilitate quantification and the quantified data reveal that a characteristic of normality seems to be the wide range of prevalence of the various SMPs, although rank orders from most to least frequently occurring movement are strictly age-related, and there is temporal patterning with age.

Although a few critical notes on the drawbacks in assessment procedure must be noted, a positive point should first be emphasized. Most publications state the duration of the study (this was lacking in only 14 articles) and thus in most articles prevalence could be examined for each observation period. Moreover, the duration of most investigations seemed to be adequate, since it is now known that the longest intervals between periods of activity before 20 weeks are 13 min and those near term are 45 min.

The comparability of the assessment procedures was influenced negatively by a number of aspects. Sixty-nine articles applied a classification of the motor activity which did not describe unequivocally which body parts participated (12 used NSMP only and 57 in combination with SMP) and as such these could not be compared with other studies. SMPs are reproducible by providing information as to which body part initiated the movement and was involved during the movement, often with qualitative aspects of speed and amplitude. Kozuma et al.51 supported an even more detailed categorization of thorax movements and considered the descriptions of general movements to be too limited. They did not apply, however, the important concept of de Vries et al.8 which enables the numerous complex movements to be distinguished well and which describes where a movement is initiated, which body parts participate actively and not merely passively, whether a movement is performed in isolation or with ongoing activity elsewhere, together with the quality of its performance in amplitude and speed. This concept can be used to describe general movements recognizably throughout gestation and the same holds true for the other SMPs. Thus the categorization facilitates quantification, and SMPs have been applied most in studies on emergence and development, although their application has been very limited in studies involving continuity and relationships to other parameters.

Quantification has not been performed identically in the various studies, despite their use of SMPs. For example, since a characteristic of general movements is the coming and going of activity, an interval needs to be determined to distinguish between two consecutive bursts. Ten Hof et al.73 explored the best interval between bursts of movement in great detail and advised 1–3 s as the interval needed to allow sufficient discrimination between short-lasting and long-lasting bursts of activity. An exception in the literature is the same approach of determining the four fetal behavioral states. Since its introduction in 19829, studies have tended to use the 3-min window system, in which the presence or absence of body activity, including startles, gross body movements and movements of the extremities, was scored.

In addition, many articles did not describe in their methods sections whether they performed their observations continuously on the examined body part or region of interest, or whether observations were made in relation to food intake or time of day. Both aspects may have a major influence on the prevalence of the examined activity.

The focus of interest of most (83%) studies was the second half of pregnancy. Far fewer studies dealt with the first half and very few with continuity after birth. A positive effect of the studies during the second half of pregnancy is the growing awareness of the influence of motor activity on FHRP, behavioral states, and flow parameters, or vice versa.

Of the various SMPs, there was obviously a preference for studying breathing movements and eye movements. Investigation into the rich variety of SMPs has rarely been the focus, despite the good reproducibility. Attention to general movements has been limited and more attention has been paid to NSMPs despite their lower precise reproducibility.

Neuromuscular development

Investigations have been performed primarily by fetal developmental researchers within obstetrics, although a few groups worked in collaboration with developmental neurologists. Whereas Milani-Comparetti and Gidoni10 proposed the description of evoked and intentional movement patterns, de Vries et al.8 stressed the spontaneous character of motility. Since observations of long duration, under constant environmental conditions, demonstrated the variability of motility, its spontaneous character has been well-documented and accepted8.

The sideways bending of the head and/or rump which emerges at 7 weeks and disappears a week later is an SMP that is performed identically with small amplitude and low speed every 2 min. This representation of the earliest spontaneous motility was observed in the mouse embryo by Suzue and Shinoda117 and can be found throughout the mammals as a highly reproducible spatiotemporal pattern. It is probably initiated via circuits of nerve activity at the spinal level, as supported by investigations on the earliest forms of motility in chick embryos118.

In contrast, the wealth of differentiation of SMPs that develop thereafter, within the period 8–14 weeks, is hypothesized to originate supraspinally. Sedlacek and Doskocil119 described supraspinal factors being indispensable for normal morphological development of the spinal chord motor apparatus in the chick embryo. The emergence of spontaneously generated human SMPs occurs for the first time at the same age at which they can be elicited in exteriorized fetuses120.

Normal quantitative output in fetuses of uncomplicated pregnancies is characterized by a wide range of occurrence of each specific movement pattern. On the other hand the ranking in the frequency of SMPs from most to least frequent is strongly age-related, exhibits less individual variance than does the raw quantified data and is energy-related (e.g. the first-place rank of general movements is taken over by breathing movements during the second hour after a maternal meal). Moreover, the strongly age-related gradual changes in temporal patterning of, for instance, general movements, breathing movements and clustering of movements (behavioral states), suggest influence of the central nervous system (CNS), on which are superimposed the smaller influences of hormones (e.g. diurnal rhythm in general movements inverse to maternal adrenal hormonal activity16) and the previously mentioned energy relationship. After birth, the transition periods of the behavioral state variables become shorter, supporting increasing CNS control82. Behavioral states seem not to be easily influenced by external stimuli with the exception of prolonged uterine contractions or vibroacoustic stimulation100.

The onset of asymmetrical motor activity has a long history of investigation into its origin. The prenatal onset of a few asymmetries in motor activity (e.g. right thumb-sucking and arm movement) suggests an influence of the CNS. Moreover, this is supported by the continuity of preference found after birth84. The restriction of the study on preference for right thumb-sucking, however, is that only one burst of thumb-sucking was examined in about 15 min17.

Sonographic motor assessment has not yet obtained a place in routine care. Nowadays it is merely limited to detecting the presence of any motility. However, presence of motility does not exclude anomalies. Analogous to the introduction of the examination of the four-chamber view of the heart into routine practice to enhance the chance of finding major heart anomalies, we advocate introduction of the examination of at least one SMP into routine care: the most frequently occurring, general movements. In cases where general movements are performed with participation of all body parts and with varying speed and amplitude, this does exclude many high-risk situations. An absence of general movements or of a normal quality of general movements will stimulate adequate referrals for detailed sonographic motor examination. Just as it took time to introduce the four-chamber view of the heart into routine scanning practice, it will also take a while before the idea of adding the assessment of general movements to routine scanning is accepted. The same holds true for the recommended detailed motor assessment during an advanced sonographic examination.

As a consequence of the insights obtained here with respect to normal motor development, the following procedure to evaluate normal motor milestones could be considered. As a part of routine care one should observe general movements including of the head, trunk and extremities, at varying speeds and amplitudes. In an advanced sonographic examination: one should focus continuously on the head, including eye and jaw, the trunk and at least one arm and one leg for a total duration of 15 min (at <20 weeks), 30 min (at 20–30 weeks) or 60 min (at >30 weeks). Also covered during the advanced sonographic examination should be scoring ranking of SMPs (at least the three highest at the examined age), concerning qualitative aspects of all SMPs involving variance in amplitude, speed and, in the case of general movements, variance in participating body parts, waxing and waning during one burst, quantification of these SMPs, at least in terms of the general movements (Table 2).

Table 2. Motor assessment scorings chart
 Differentiation: SMP present/absentQuantity (n)Quality: presence (+), absence (−) or reduced ( ± ) variation in:
SpeedAmplitude
  • Shading indicates when no parameter needs to be scored, since an absence of variation is the normal characteristic.

  • *

    The qualitative assessment is based on a minimum of three general movements for each observation period126 (the recommended observation duration is therefore 15 min at < 20 weeks, 30 min at 20–30 weeks and 60 min at > 30 weeks) and concerns participating body parts as well as speed and amplitude.

  • Normal values for each specific movement pattern vary with gestational age43, 68. GM, general movement.

Specific movement pattern (SMP)
 Sideways bending (< 9 weeks)equation imageequation image
 General movement*
 Participating body part:
 Startlesequation image 
 Breathing 
 Hiccupequation image 
 Isolated retroflexion, head
 Isolated rotation, head
 Isolated anteflexion, head
 Isolated arm, slow
 Isolated arm, single quick (twitch) equation image 
 Isolated leg, slow
 Isolated leg, single quick (twitch) equation image 
 Jaw opening
 Sucking and swallowing
 Non-nutritive sucking
 Yawnequation imageequation image
 Stretchequation imageequation image
 Eye movement 
 Hand–face contact 
Conclusions drawn
 Normal> 3 SMPs> 3 GMsSpeed, amplitude and body parts vary
 Abnormal≤ 3 SMPs≤ 3 GMsNone of the above vary
 Suspect Two of the above vary and one is abnormal or suspect

The decline in articles since 2000 described in this study is explained in part by the increase in 4D sonographic studies121–125. This overview shows what fetal motor studies using 2D sonography have revealed until now. Since the whole fetus cannot be visualized continuously, studies only report on fetal body areas of interest. When 4D sonography with real-time dynamics enables the study of qualitative motor performance and posture of the whole fetus, the tools will become available to overcome this omission.

Finally, this overview on assessment procedures and present knowledge of milestones in motor developmental aspects is limited by the fact that we chose to evaluate a limited number of assessment aspects and focus on one aim per article. We mean, however, to stimulate future research with reproducible methods.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We are very grateful for the support with the literature search of M.M.A. van der Zanden, student of the Faculty of Movement Sciences, Institute of Fundamental and Clinical Human Movement Sciences.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References