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Decreased expression of the righting reflex and locomotor movements in breech-presenting newborns in the first days of life
Early Human Development 85 (2009) 263–266
Contents lists available at ScienceDirect
Early Human Development j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / e a r l h u m d ev
Decreased expression of the righting reflex and locomotor movements in breech-presenting newborns in the first days of life Slobodan Sekulić a,⁎, Marija Žarkov a, Petar Slankamenac a, Ksenija Božić a, Tihomir Vejnović b, Aleksandra Novakov-Mikić b a b
Department of Neurology, University of Novi Sad, Clinical Center of Vojvodina, Serbia Department of Obstetrics and Gynecology, University of Novi Sad, Clinical Center of Vojvodina, Serbia
a r t i c l e
i n f o
Article history: Received 15 July 2008 Received in revised form 26 October 2008 Accepted 3 November 2008 Keywords: Breech presentation Newborn Neurological examination Pregnancy Cesarean section
a b s t r a c t Aim: To investigate differences between the infants born in occipital and breech presentation relative to the passive and active motility. Method: A prospective study was conducted in the period from 2006 to 2007 at the Department of Obstetrics and Gynecology in Novi Sad. Subjects were 50 breech-presenting and 87 occipital-presenting term newborns delivered by elective cesarean section following a regular course of pregnancy, without fetal, newborn, and the pregnant female disease. Outcome measures were popliteal angle; extension of the hip-joint; ventral flexion and dorsal extension in the axis; spontaneous displacement; crawling reflex; righting reaction in vertical and sitting positions; righting reaction in horizontal suspension, the automatic walking investigated on the second and fourth day of life. Results: Except for righting reaction in horizontal suspension, the newborns from breech presentation had a significantly lower score for all investigated parameters of active movements at the first and second examination. There was no difference between occipital and breech-group relative to the ventral flexion and dorsal extension in the axis. The popliteal angle was significantly increased, whereas the extension in the hip joint was significantly decreased in the breech group. Conclusions: Investigations showed a significantly decreased expression of active movements in the breech group, which cannot be explained only by postural deformities. © 2008 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Breech presentation at birth increases the risk of deviation from normal delivery mechanisms and causes incomplete engaging of the presenting part of the fetus in the isthmic part of the uterus. This could be followed by a delay in delivery and increased incidence of birth asphyxia and injuries to the newborn [1]. Additionally, the breech presentation at birth is followed by increased incidence of prematurity and congenital malformations of the fetus, which by their side also increases the incidence of morbidity and mortality [2–4]. Causes of breech presentation are either fetal diseases, which cause the absence of fetal movements, or the lack of adequate volume of intrauterine cavity necessary for fetal movements [5]. The ultrasound observation of the fetus shows that it turns from the breech to cephalic presentation by active whole body movements such as kicking [6]. These movements are generated by excitation of antigravity muscles, i.e., the extensor muscles of the trunk and legs. Recent studies investigating neurological findings in newborns from breech pre⁎ Corresponding author. Department of Neurology, Clinical Center of Vojvodina, Hajduk Veljkova 1-7, 21000 Novi Sad, Serbia. Tel.: +381 643886715; fax: +381 2126520. E-mail addresses: [email protected], [email protected] (S. Sekulić). 0378-3782/$ – see front matter © 2008 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.earlhumdev.2008.11.001
sentation registered aberrations of neurological findings relative to the excitation of antigravity muscles of the trunk and legs as well as of locomotor movements such as the following: either decrease or absence of spontaneous movements of lower extremities; incomplete response in the positive-support reflex [7,8]; or the absence of stepping reflex and the foot placing reflex [9]. Additionally, the infants showed limited extension of hip joints and increase of popliteal angle, which pointed to the restriction of the volume of the intrauterine cavity and the resulting decrease of physiologic amplitude of movements [7,10]. The characteristic of all these abnormalities of neurologic examination is that at the repeated examinations performed within several days or weeks, they showed to be either absent or in regression. Nevertheless, although the differences have been identified, either there were no statistical significances [8] or the data have not been analyzed to estimate the statistical significance [7,9]. The aim of this study is to investigate possible differences between the breech-presenting and occipital-presenting newborns in relation to the following: excitation of antigravity muscles, spontaneous and provoked locomotion of the newborns, and passive motility of the trunk and of lower extremities. The presumption was that the breechpresenting infants would have impaired motility in comparison to the occipital-presenting infants.
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2. Method A prospective investigation was performed in the period from January 2006 to September 2007 at the Department of Obstetrics and Gynecology at the Clinical Center of Vojvodina in Novi Sad. The research was approved by the Ethical Committee of the Department of Neurology at the Clinical Center of Vojvodina in Novi Sad. Each mother of the newborns gave written consent for neurological examination. Consecutive examinations led to the formation of two study groups: an experimental group of 50 cases and a control group of 87 cases. The recruiting criterion in the experimental group was breech presentation at birth versus occipital presentation in the control group. The recruiting criteria for both groups were as follows: singleton gestation; elective cesarean section delivery; general anesthesia; gestational age ≥37 weeks; 1st min. Apgar scores of 8, 9, 10 and 5th min. Apgar scores of 9 and 10; and newborn body weight within the 90th percentile. The excluding criteria for both groups were the following: multiple gestation; fetal presentation accomplished by either external or internal rotation; gestational age of less than 37 weeks; body weight of the fetus outside the 10th percentile; epidural anesthesia; emergency cesarean section; 1st min. Apgar score ≤7 and 5th min. Apgar score ≤8; fetal and newborn infant disease; oligohydramnion; polyhydramnion; placental calcifications; placenta praevia; intrauterine synechia; congenital malformations of the uterus; bone deformities in the pelvic region of pregnant female; the presence of either ovarian or uterine tumors; EPH gestoses; psychiatric diseases of the pregnant female; the use of hormonal agents during pregnancy; and use of any other drugs during gestation except antibiotics or vitamins. The newborns were examined on the 2nd and 4th days of life. Neurological examination was performed 1 to 2 h following breast feeding. Because there was no statistical significance recorded in a previous study [8], the existing tests were adjusted for the needs of this study during a pilot study. The observed parameters and their scoring are presented in Table 2. Neurological examination was done without knowledge about the type of presentation. Ventral flexion and dorsal extension in the axis are performed and scored as described by Amiel-Tisson: “Ventral flexion in the axis—with the child supine, the lower limbs are grasped and both legs and pelvis are pushed towards the head in order to achieve the maximum curvature of the spine. Dorsal extension in the axis—with the infant lying on his or her side, the flat of the palm of one hand is placed on the lumbar region and both legs pulled backwards with the other hand” [11]. Popliteal angle was examined with the newborn lying on his or her back. The examiner flexes the newborn's thighs laterally beside the abdomen and then extends the knee to its limit. The popliteal angle is then measured [11]. Passive limitation of the hip
joint movements is estimated by extension of the hip joint with the infant in supine position on the examination table. Thighs are passively extended to their limit. The angle between examination table and extended thigh is measured [10]. When assessing spontaneous displacement, the infant is in horizontal pronation being observed for 1 min in order to evaluate the displacement relative to the umbilical region. In crawling reflex, the contact with plantar region has been maintained until obtaining the two successive responses, but not longer than 1 min. Displacement is again estimated relative to the umbilical region. In righting reaction in the vertical position, the infant is placed in a standing position supported by both hands of the investigator across the axial region. Feet are in contact with the examination table. The degree of extension was observed over a maximum of 1 min. In a full response, legs are first extended, then trunk, and finally head [11]. In righting reaction in the sitting position, the infant is placed in a sitting position supported by the hand of the investigator across the chest region. The trunk is bent forward 10–15°. The degree of head and trunk extension is observed during a maximum of 1 min. When assessing automatic walking, the infant is placed in a standing position supported by both hands of the investigator across the axial region and then tilted forward slightly. The head is tilted up and backward with the examiner's fingers. Automatic walking is evaluated until three or more steps are obtained but not longer than 1 min. To elicit righting reaction in horizontal suspension, the newborn is lifted from the examination table and held prone across the chest region by the examiner. In a full response, the head is first extended, then trunk, and finally legs. The degree of extension is observed over a maximum of 1 min. In the case of spontaneous displacement, crawling reflex, righting reaction in sitting position, righting reaction in vertical position, automatic walking, and righting reaction in horizontal suspension, the examination is twice repeated in each session, and the higher score is taken into account. The Mann–Whitney U-test is used in evaluation of the Apgar score, whereas maternal age, pregnancy rate, parity, gestational weeks, body length, and body weight are processed by t-test. Neurological parameters are analyzed using the Mann–Whitney U-test. 3. Results Indications for elective cesarean section in the control group were as follows: previous cesarean section in 53 cases; dysproportio fetopelvina in 28 cases; myopia alta degenerativa in 5 cases; and condylomata acuminata perinei in 1 case. The incidence of breech presentation was as follows: frank breech presentation in 30 cases; complete breech presentation in 9; incomplete breech presentation in 5; and footling breech presentation in 6 cases. Table 1 shows general characteristics of the breech and occipital group with statistical
Table 1 General characteristics of the breech and occipital group Group Occipital presentation
Breech presentation
Characteristics
Mean value
Standard deviation
Mean value
Standard deviation
Statistical difference
Maternal age Pregnancy Parity Gender
29.60 years 2.31 1.87 Male Female 39.83 9.64 9.94 50.34 cm 3480.11 g 35.14 cm 63.82 cm 594.37 g
5.10 years 1.00 0.70 No 49 No 38 0.87 0.55 0.23 1.31 cm 257.44 g 1.05 cm 5.82 cm 67.09 g
29.04 years 1.88 1.50 Male Female 39.80 9.42 9.84 49.48 cm 3333.00 g 35.26 cm 64.74 cm 572.80 g
5.77 years 1.38 0.71 No 30 No 20 1.21 0.67 0.37 1.68 cm 324.30 g 1.35 cm 6.95 cm 65.19 g
F = 0.56 F = 4.41 F = 9.05 χ2 = 0.81
p = 0.56 p = 0.04 p = 0.00
NS p b 0.05 p b 0.05 NS
F = 0.02 Z = −1.98 Z = −1.96 F = 11.20 F = 8.55 F = 0.35 F = 0.69 F = 3.35
p = 0.88 p = 0.04 p = 0.05 p = 0.00 p = 0.00 p = 0.56 p = 0.40 p = 0.07
NS p b 0.05 NS p b 0.05 p b 0.05 NS NS NS
Gestational weeks Apgar score 1 min Apgar score 5 min Body length Body weight Head circumference Umbilical length Placental weight NS-not significant.
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Table 2 The observed neurological parameters during first and second examinations, their scoring, and statistical differences Item
Score
Popliteal angle
≈ 90° ≈ 135° ≈ 180° ≈ 0° ≈ 10–30° ≥ 40° Absent Minimal Moderate Extreme Absent Minimal Moderate Extreme Absent b 10 cm N 10 cm Absent b 10 cm N 10 cm Absent Head righting Head righting and turning on back Prompt extension of trunk and turning on back Absent Legs righting Legs and trunk righting Legs, trunk, and head righting Absent Head righting Head and trunk righting Head, trunk, and legs righting Absent 1–2 steps ≥ 3 steps
Extension of the hip joint
Ventral flexion in the axis
Dorsal extension in the axis
Spontaneous displacement
Crawling reflex
Righting reaction in sitting position
Righting reaction in vertical position
Righting reaction in horizontal suspension
Automatic walking
IO
II O
Statistical difference
IB
II B
% of cases 82.8% 5.7% 11.5% 90.8% 8% 1.1% 1.1% 21.8% 56.3% 20.7% 0% 42.5% 35.6% 21.8% 33.3% 52.2% 11.5% 8% 15% 77% 2.3% 4.6% 57.5%
% of cases
I O vs II O
% of cases
% of cases
I B vs II B
I O vs I B
II O vs II B
67.8% 17.2% 14.9% 91.3% 6.9% 0% 1.1% 19.5% 62.1% 17.2% 0% 34.5% 41.4% 24.1% 8% 56.4% 35.6% 3.4% 4.6% 92% 0% 0% 66.7%
Z = −2.63 p = 0.00 p b 0.05 Z = −1.13 p = 0.26 NS Z = −0.12 p = 0.90 NS
20% 14% 66% 68% 28% 4% 4% 28% 50% 18% 0% 38% 34% 28% 66% 32% 2% 36% 18% 46% 16% 18% 60%
18% 8% 74% 76% 22% 2% 2% 28% 48% 22% 0% 32% 46% 22% 16% 56% 28% 8% 12% 80% 2.2% 4.4% 68.6%
Z = −1.67 p = 0.09 NS Z = −2.23 p = 0.00 p b 0.05 Z = −0.87 p = 0.414 NS
Z = −7.27 p = 0.00 p b 0.05 Z = −3.36 p = 0.00 p b 0.05 Z = −1.04 p = 0.29 NS
Z = −6.57 p = 0.00 p b 0.05 Z = −2.86 p = 0.00 p b 0.05 Z = −0.44 p = 0.66 NS
Z = −0.24 p = 0.98 NS
Z = −0.74 p = 0.46 NS
Z = −0.05 p = 0.96 NS
Z = −5.03 p = 0.00 p b 0.05 Z = −3.92 p = 0.00 p b 0.05 Z = −2.56 p = 0.01 p b 0.05
Z = −3.82 p = 0.00 p b 0.05 Z = −4.04 p = 0.00 p b 0.05 Z = −4.98 p = 0.00 p b 0.05
Z = −1.33 p = 0.18 NS Z = −2.02 p = 0.04 p b 0.05 Z = −4.22 p = 0.00 p b 0.05
35.6%
33.3%
6%
24.8%
2.3% 2.3% 6.9% 88.5% 1.1% 12.7% 33.3% 52.9% 2.3% 18.4% 79.3%
1.1% 1.1% 5.8% 92% 1.1% 5.7% 40.3% 52.9% 0% 14.9% 85.1%
36% 16% 4% 44% 6% 10% 48% 36% 18% 48% 34%
10% 6% 20% 64% 0% 10% 46% 44% 4% 34% 62%
Z = −3.52 p = 0.00 p b 0.05
Z = −5.97 p = 0.00 p b 0.05
Z = −4.11 p = 0.00 p b 0.05
Z = −1.75 p = 0.08 NS
Z = −1.72 p = 0.08 NS
Z = −1.04 p = 0.29 NS
Z = −3.13 p = 0.00 p b 0.05
Z = −5.41 p = 0.00 p b 0.05
Z = −3.13 p = 0.00 p b 0.05
Z = −1.17 p = 0.24 NS Z = −5.68 p = 0.00 p b 0.05 Z = −2.75 p = 0.00 p b 0.05 Z = −0.75 p = 0.45 NS
Z = −0.89 p = 0.37 NS Z = −0.84 p = 0.40 NS Z = −1.46 p = 0.14 NS
Statistical difference
Statistical difference
Statistical difference
I—first examination, II—second examination, O—occipital presentation, B—breech presentation, NS—not significant.
difference. In the breech group, pregnancy and parity rate was significantly lower as well as Apgar score in the first minute, body length, and body weight. The difference between two groups is almost significant regarding Apgar score in the fifth minute and placental weight. Table 2 shows the results of the observed neurological parameters. Data showed statistically increased popliteal angle in the breech group compared to the occipital group at the first and the second examinations. Additionally, there was a statistically significant decrease in passive extension of the hip joint in the breech group compared to the occipital group during the first and second examinations. The occipital group showed statistically significant increased popliteal angle at the second examination relative to the first one. In the breech group, there was a statistically significant increase of passive extension in the hip joint at the second versus the first examination. The Mann–Whitney U-test confirmed the statistical significance of decreased spontaneous displacement in the breech group compared to the cephalic group at the first examination. The statistically significant decreased displacement in the breech group compared to the cephalic group was present for the crawling reflex both at the first and the second examinations. Furthermore, there were a lesser number of steps in the breech group compared to the cephalic group during automatic walking during the first and second examinations. The incidence of righting reaction in vertical position in the breech group compared to the cephalic group at the first and second examinations was significantly decreased. During the spontaneous displacement test, the occipital group showed a statistically
significant increase in spontaneous displacement at the second examination relative to the first, as well as in crawling reflex. In the breech group, there was a statistically significant higher score at the second examination compared to the first in spontaneous displacement, crawling reflex, automatic walking, righting reaction in a sitting position, and righting reaction in vertical position. The results showed a lower score for righting reactions in sitting position in the breech group relative to the occipital group at the first and second examinations. 4. Discussion This study, like some other investigations, recorded increased incidence of breech presentation in primiparas [3]. As far as breech presentation lowers the subsequent pregnancy rate, it is possible that previous breech presentation favors a woman's decision not to reproduce [12]. Body characteristics of the breech-presenting infants recorded in this study, such as a reduced body length and weight relative to the occipital group, had been present in other reports as well, even when data were adjusted for gestational age. This finding points to fetal distress and suboptimal intra-uterine development [3,8]. The impaired fetal growth does not predate breech presentation; it is a condition associated with the breech presentation [13]. Statistically, a decreased 1 min Apgar score in the breech group has also been present in other studies [4,8], suggesting that the stress resulting from the delivery is more expressed in this group of infants than in the occipital group.
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The study showed differences in neurological findings between the breech and occipital groups, which cannot be attributed to delivery trauma, identified fetal or maternal diseases. There was no statistically significant difference relative to the gestational age between the breech and occipital-presenting groups, which eliminated the bias that the younger group presented with a lower score. In the breech group, there was a significantly limited passive extension of the hip joint disabling active extension as well. Such a prenatal postural deformity can significantly affect the excitation of antigravity muscles. Previous studies showed that intra-uterine movement restriction of legs caused long-term alterations in the development of leg posture, reflexes, and posture while walking, mediated by alterations in proprioceptive feedback mechanisms [10,14]. The breech group obtained lower scores while assessing the reflexes-reactions including the hip-joint extension such as righting reaction in vertical position, automatic walking, crawling reflex, and spontaneous displacement. However, the excitation of antigravity muscles in righting reaction in a sitting position was also less expressed in the breech group at both the first and second examinations, although there was no statistically significant difference in passive movements of the trunk between the breech and occipital groups. On the other hand, there was no difference between the breech and occipital group while evaluating excitation of antigravity muscles of the neck, trunk, and lower extremities in righting reaction in horizontal suspension. Weaker excitation of extensor musculature in righting reaction and locomotor movements in the breech group, as well as the absence of difference in excitation of extensor muscles in righting reaction in horizontal suspension, suggest that this difference cannot be explained only by the limited hip-joint extension, increased popliteal angle, and alterations in proprioceptive feedback mechanisms. Decreased expression of postural reflexes caused by limited intra-uterine space can also be followed by absence of the development of central mechanisms of postural reflexes. Additionally, the intra-uterine fetal distress has to be taken into account, as well as the resulting muscle weakness of the newborn infant associated with lower scores [8]. Functional integration of righting reflexes and locomotor movements within the body posture occurs during the period from 24 to 36 gestational weeks [11]. The period from 24 to 36 gestational weeks is characterized by increased incidence of cephalic presentation and decreased incidence of breech, oblique, and transverse presentation [5]. During this period for fetuses in breech and cephalic presentation, occurs the probability to be in that very same presentation at delivery [15,16]. The decreased expression of righting reflexes and locomotor movements in the breech group suggest that during this critical period, from 24 to 36 gestational weeks, there was no complete development of these reflexes. As mentioned earlier, the fetuses change from cephalic to breech presentation and vice versa by active whole body movements such as kicking. The body rolling also has been reported as a possible movement of the fetus while changing presentation [1]. Other authors reported that the fetus changes from breech to cephalic presentation, and vice versa, by the movement of legs and feet [17]. This suggests that the fetuses change from breech to cephalic presentation, and vice versa, using all available repertoire of movements already present in the middle stage of gestation [18]. The decreased expression of righting reactions and locomotor movements in the breech group are in agreement with this. While comparing the first and second examination scores, the breech group has significantly higher scores in all reflexes and reactions relative to active motility at the second examination. The increased degree of passive hip-joint extension has also been
registered upon second examination. Obviously, the subsequent normalization of neurological findings has been reached following fetal displacement from an inadequate intra-uterine environment after the delivery. Increase in passive hip-joint extension and spontaneously generated movements of lower extremities, as well as the better characteristics of primitive reflexes during follow-ups, have also been registered in previously mentioned studies [7–9]. Our study cannot answer whether the primary cause of breech presentation in the investigated sample is of extrinsic origin – resulting from the absence of sufficient intra-uterine volume, or of intrinsic origin – resulting from fetal affection associated with temporary muscle weakness. The differences between the breech and occipital groups do not point to qualitatively different characteristics of neurological findings. They are presented by quantitative differences in expression of the righting reflexes and locomotion. The breech group does not exhibit any special characteristics of neurological findings occurring only in their group. The neurological findings present in this group have also been registered in the occipital group.
Acknowledgement This study was supported by the Serbian Ministry of Science and Environmental Protection Grant Number 143021/2006.
References [1] Collea JV. Malpresentation & cord prolapse. In: DeCheney AH, Pernoll ML, editors. Obstetrics & gynecologic diagnosis & treatment. Upper Saddle River, New Jersey: Prentice-Hall International Inc; 1994. p. 410–27. [2] Fawole AO, Adeyemi AS, Adewole IF, Omigbodun AO. A ten-year review of breech deliveries at Ibadan. Afr J Med Med Sci 2001;30:87–90. [3] Rayl J, Gibson PJ, Hickok DE. A population-based case-control study of risk factors for breech presentation. Am J Obstet Gynecol 1996;174:28–32. [4] Molkenboer JF, Vencken PM, Sonnemans LG, Roumen FJ, Smits F, Buitendijk SE, et al. Conservative management in breech deliveries leads to similar results compared with cephalic deliveries. J Matern Fetal Neonatal Med 2007;20:599–603. [5] Sekulić SR. Possible explanation of cephalic and noncephalic presentation during pregnancy: a theoretical approach. Med Hypothes 2000;55:429–34. [6] Suzuki S, Yamamuro T. Fetal movement and fetal presentation. Early Hum Dev 1985;11:255–63. [7] Бабкин ПС. The motor adaptation syndrome in the human fetus and its dynamics in newborns. Zh Nevropatol Psikhiatr Im S S Korsakova 1994;94:19–21. [8] Bartlett D, Piper M, Okun N, Byrne P, Watt J. Primitive reflexes and the determination of fetal presentation at birth. Early Hum Dev 1997;48:261–73. [9] Stojčević-Polovina M, Petković Z. Specific reactions of infants at risk in the first 3 days of life. Acta Med Iugosl 1986;40:189–99. [10] Sival DA, Prechtl HFR, Sonder GHA, Touwen BCL. The effect of intra-uterine breech position on postnatal motor functions of the lower limbs. Early Hum Dev 1993;32:161–76. [11] Amiel-Tison C. Clinical assessment of the infant nervous system. In: Levene MI, Lilford RJ, editors. Fetal and neonatal neurology and neurosurgery. Edinburgh: Churchill Livingstone; 1995. p. 83–104. [12] Albrechtsen S, Rasmussen S, Dalaker K, Irgens L. Reproductive career after breech presentation: subsequent pregnancy rates, interpregnancy interval, and recurrence. Obstet Gynecol 1998;92:345–50. [13] Zhang J, Schwingl PJ. Breech presentation and fetal growth retardation. J Reprod Med 1993;38:193–6. [14] Prechtl HFR, Knol AR. Effects of breech presentation on the plantar reflex in the newborn. Arch Psychiatr Nervenkr Z gesamte Neurol Psychiatr 1958;196:542–53. [15] Tadmor OP, Rabinowitz R, Alon L, Mostoslavky V, Aboulafia Y. Can breech presentation at birth be predicted from ultrasound examination during the second or third trimester? Int J Gynaecol Obstet 1994;46:11–4. [16] Boos R, Hendrik HJ, Schmidt W. Fetal position in the second half of pregnancy in births from breech and vertex presentation. Geburtshilfe Frauenheilkd 1987;47:341–5. [17] Liley AW. The foetus as a personality. By A.W. Liley, 1972. Fetal Ther 1986;1:8–17. [18] de Vries JI, Fong BF. Normal fetal motility: an overview. Ultrasound Obstet Gynecol 2006;27:701–11.
Contents lists available at ScienceDirect
Early Human Development j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / e a r l h u m d ev
Decreased expression of the righting reflex and locomotor movements in breech-presenting newborns in the first days of life Slobodan Sekulić a,⁎, Marija Žarkov a, Petar Slankamenac a, Ksenija Božić a, Tihomir Vejnović b, Aleksandra Novakov-Mikić b a b
Department of Neurology, University of Novi Sad, Clinical Center of Vojvodina, Serbia Department of Obstetrics and Gynecology, University of Novi Sad, Clinical Center of Vojvodina, Serbia
a r t i c l e
i n f o
Article history: Received 15 July 2008 Received in revised form 26 October 2008 Accepted 3 November 2008 Keywords: Breech presentation Newborn Neurological examination Pregnancy Cesarean section
a b s t r a c t Aim: To investigate differences between the infants born in occipital and breech presentation relative to the passive and active motility. Method: A prospective study was conducted in the period from 2006 to 2007 at the Department of Obstetrics and Gynecology in Novi Sad. Subjects were 50 breech-presenting and 87 occipital-presenting term newborns delivered by elective cesarean section following a regular course of pregnancy, without fetal, newborn, and the pregnant female disease. Outcome measures were popliteal angle; extension of the hip-joint; ventral flexion and dorsal extension in the axis; spontaneous displacement; crawling reflex; righting reaction in vertical and sitting positions; righting reaction in horizontal suspension, the automatic walking investigated on the second and fourth day of life. Results: Except for righting reaction in horizontal suspension, the newborns from breech presentation had a significantly lower score for all investigated parameters of active movements at the first and second examination. There was no difference between occipital and breech-group relative to the ventral flexion and dorsal extension in the axis. The popliteal angle was significantly increased, whereas the extension in the hip joint was significantly decreased in the breech group. Conclusions: Investigations showed a significantly decreased expression of active movements in the breech group, which cannot be explained only by postural deformities. © 2008 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Breech presentation at birth increases the risk of deviation from normal delivery mechanisms and causes incomplete engaging of the presenting part of the fetus in the isthmic part of the uterus. This could be followed by a delay in delivery and increased incidence of birth asphyxia and injuries to the newborn [1]. Additionally, the breech presentation at birth is followed by increased incidence of prematurity and congenital malformations of the fetus, which by their side also increases the incidence of morbidity and mortality [2–4]. Causes of breech presentation are either fetal diseases, which cause the absence of fetal movements, or the lack of adequate volume of intrauterine cavity necessary for fetal movements [5]. The ultrasound observation of the fetus shows that it turns from the breech to cephalic presentation by active whole body movements such as kicking [6]. These movements are generated by excitation of antigravity muscles, i.e., the extensor muscles of the trunk and legs. Recent studies investigating neurological findings in newborns from breech pre⁎ Corresponding author. Department of Neurology, Clinical Center of Vojvodina, Hajduk Veljkova 1-7, 21000 Novi Sad, Serbia. Tel.: +381 643886715; fax: +381 2126520. E-mail addresses: [email protected], [email protected] (S. Sekulić). 0378-3782/$ – see front matter © 2008 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.earlhumdev.2008.11.001
sentation registered aberrations of neurological findings relative to the excitation of antigravity muscles of the trunk and legs as well as of locomotor movements such as the following: either decrease or absence of spontaneous movements of lower extremities; incomplete response in the positive-support reflex [7,8]; or the absence of stepping reflex and the foot placing reflex [9]. Additionally, the infants showed limited extension of hip joints and increase of popliteal angle, which pointed to the restriction of the volume of the intrauterine cavity and the resulting decrease of physiologic amplitude of movements [7,10]. The characteristic of all these abnormalities of neurologic examination is that at the repeated examinations performed within several days or weeks, they showed to be either absent or in regression. Nevertheless, although the differences have been identified, either there were no statistical significances [8] or the data have not been analyzed to estimate the statistical significance [7,9]. The aim of this study is to investigate possible differences between the breech-presenting and occipital-presenting newborns in relation to the following: excitation of antigravity muscles, spontaneous and provoked locomotion of the newborns, and passive motility of the trunk and of lower extremities. The presumption was that the breechpresenting infants would have impaired motility in comparison to the occipital-presenting infants.
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2. Method A prospective investigation was performed in the period from January 2006 to September 2007 at the Department of Obstetrics and Gynecology at the Clinical Center of Vojvodina in Novi Sad. The research was approved by the Ethical Committee of the Department of Neurology at the Clinical Center of Vojvodina in Novi Sad. Each mother of the newborns gave written consent for neurological examination. Consecutive examinations led to the formation of two study groups: an experimental group of 50 cases and a control group of 87 cases. The recruiting criterion in the experimental group was breech presentation at birth versus occipital presentation in the control group. The recruiting criteria for both groups were as follows: singleton gestation; elective cesarean section delivery; general anesthesia; gestational age ≥37 weeks; 1st min. Apgar scores of 8, 9, 10 and 5th min. Apgar scores of 9 and 10; and newborn body weight within the 90th percentile. The excluding criteria for both groups were the following: multiple gestation; fetal presentation accomplished by either external or internal rotation; gestational age of less than 37 weeks; body weight of the fetus outside the 10th percentile; epidural anesthesia; emergency cesarean section; 1st min. Apgar score ≤7 and 5th min. Apgar score ≤8; fetal and newborn infant disease; oligohydramnion; polyhydramnion; placental calcifications; placenta praevia; intrauterine synechia; congenital malformations of the uterus; bone deformities in the pelvic region of pregnant female; the presence of either ovarian or uterine tumors; EPH gestoses; psychiatric diseases of the pregnant female; the use of hormonal agents during pregnancy; and use of any other drugs during gestation except antibiotics or vitamins. The newborns were examined on the 2nd and 4th days of life. Neurological examination was performed 1 to 2 h following breast feeding. Because there was no statistical significance recorded in a previous study [8], the existing tests were adjusted for the needs of this study during a pilot study. The observed parameters and their scoring are presented in Table 2. Neurological examination was done without knowledge about the type of presentation. Ventral flexion and dorsal extension in the axis are performed and scored as described by Amiel-Tisson: “Ventral flexion in the axis—with the child supine, the lower limbs are grasped and both legs and pelvis are pushed towards the head in order to achieve the maximum curvature of the spine. Dorsal extension in the axis—with the infant lying on his or her side, the flat of the palm of one hand is placed on the lumbar region and both legs pulled backwards with the other hand” [11]. Popliteal angle was examined with the newborn lying on his or her back. The examiner flexes the newborn's thighs laterally beside the abdomen and then extends the knee to its limit. The popliteal angle is then measured [11]. Passive limitation of the hip
joint movements is estimated by extension of the hip joint with the infant in supine position on the examination table. Thighs are passively extended to their limit. The angle between examination table and extended thigh is measured [10]. When assessing spontaneous displacement, the infant is in horizontal pronation being observed for 1 min in order to evaluate the displacement relative to the umbilical region. In crawling reflex, the contact with plantar region has been maintained until obtaining the two successive responses, but not longer than 1 min. Displacement is again estimated relative to the umbilical region. In righting reaction in the vertical position, the infant is placed in a standing position supported by both hands of the investigator across the axial region. Feet are in contact with the examination table. The degree of extension was observed over a maximum of 1 min. In a full response, legs are first extended, then trunk, and finally head [11]. In righting reaction in the sitting position, the infant is placed in a sitting position supported by the hand of the investigator across the chest region. The trunk is bent forward 10–15°. The degree of head and trunk extension is observed during a maximum of 1 min. When assessing automatic walking, the infant is placed in a standing position supported by both hands of the investigator across the axial region and then tilted forward slightly. The head is tilted up and backward with the examiner's fingers. Automatic walking is evaluated until three or more steps are obtained but not longer than 1 min. To elicit righting reaction in horizontal suspension, the newborn is lifted from the examination table and held prone across the chest region by the examiner. In a full response, the head is first extended, then trunk, and finally legs. The degree of extension is observed over a maximum of 1 min. In the case of spontaneous displacement, crawling reflex, righting reaction in sitting position, righting reaction in vertical position, automatic walking, and righting reaction in horizontal suspension, the examination is twice repeated in each session, and the higher score is taken into account. The Mann–Whitney U-test is used in evaluation of the Apgar score, whereas maternal age, pregnancy rate, parity, gestational weeks, body length, and body weight are processed by t-test. Neurological parameters are analyzed using the Mann–Whitney U-test. 3. Results Indications for elective cesarean section in the control group were as follows: previous cesarean section in 53 cases; dysproportio fetopelvina in 28 cases; myopia alta degenerativa in 5 cases; and condylomata acuminata perinei in 1 case. The incidence of breech presentation was as follows: frank breech presentation in 30 cases; complete breech presentation in 9; incomplete breech presentation in 5; and footling breech presentation in 6 cases. Table 1 shows general characteristics of the breech and occipital group with statistical
Table 1 General characteristics of the breech and occipital group Group Occipital presentation
Breech presentation
Characteristics
Mean value
Standard deviation
Mean value
Standard deviation
Statistical difference
Maternal age Pregnancy Parity Gender
29.60 years 2.31 1.87 Male Female 39.83 9.64 9.94 50.34 cm 3480.11 g 35.14 cm 63.82 cm 594.37 g
5.10 years 1.00 0.70 No 49 No 38 0.87 0.55 0.23 1.31 cm 257.44 g 1.05 cm 5.82 cm 67.09 g
29.04 years 1.88 1.50 Male Female 39.80 9.42 9.84 49.48 cm 3333.00 g 35.26 cm 64.74 cm 572.80 g
5.77 years 1.38 0.71 No 30 No 20 1.21 0.67 0.37 1.68 cm 324.30 g 1.35 cm 6.95 cm 65.19 g
F = 0.56 F = 4.41 F = 9.05 χ2 = 0.81
p = 0.56 p = 0.04 p = 0.00
NS p b 0.05 p b 0.05 NS
F = 0.02 Z = −1.98 Z = −1.96 F = 11.20 F = 8.55 F = 0.35 F = 0.69 F = 3.35
p = 0.88 p = 0.04 p = 0.05 p = 0.00 p = 0.00 p = 0.56 p = 0.40 p = 0.07
NS p b 0.05 NS p b 0.05 p b 0.05 NS NS NS
Gestational weeks Apgar score 1 min Apgar score 5 min Body length Body weight Head circumference Umbilical length Placental weight NS-not significant.
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Table 2 The observed neurological parameters during first and second examinations, their scoring, and statistical differences Item
Score
Popliteal angle
≈ 90° ≈ 135° ≈ 180° ≈ 0° ≈ 10–30° ≥ 40° Absent Minimal Moderate Extreme Absent Minimal Moderate Extreme Absent b 10 cm N 10 cm Absent b 10 cm N 10 cm Absent Head righting Head righting and turning on back Prompt extension of trunk and turning on back Absent Legs righting Legs and trunk righting Legs, trunk, and head righting Absent Head righting Head and trunk righting Head, trunk, and legs righting Absent 1–2 steps ≥ 3 steps
Extension of the hip joint
Ventral flexion in the axis
Dorsal extension in the axis
Spontaneous displacement
Crawling reflex
Righting reaction in sitting position
Righting reaction in vertical position
Righting reaction in horizontal suspension
Automatic walking
IO
II O
Statistical difference
IB
II B
% of cases 82.8% 5.7% 11.5% 90.8% 8% 1.1% 1.1% 21.8% 56.3% 20.7% 0% 42.5% 35.6% 21.8% 33.3% 52.2% 11.5% 8% 15% 77% 2.3% 4.6% 57.5%
% of cases
I O vs II O
% of cases
% of cases
I B vs II B
I O vs I B
II O vs II B
67.8% 17.2% 14.9% 91.3% 6.9% 0% 1.1% 19.5% 62.1% 17.2% 0% 34.5% 41.4% 24.1% 8% 56.4% 35.6% 3.4% 4.6% 92% 0% 0% 66.7%
Z = −2.63 p = 0.00 p b 0.05 Z = −1.13 p = 0.26 NS Z = −0.12 p = 0.90 NS
20% 14% 66% 68% 28% 4% 4% 28% 50% 18% 0% 38% 34% 28% 66% 32% 2% 36% 18% 46% 16% 18% 60%
18% 8% 74% 76% 22% 2% 2% 28% 48% 22% 0% 32% 46% 22% 16% 56% 28% 8% 12% 80% 2.2% 4.4% 68.6%
Z = −1.67 p = 0.09 NS Z = −2.23 p = 0.00 p b 0.05 Z = −0.87 p = 0.414 NS
Z = −7.27 p = 0.00 p b 0.05 Z = −3.36 p = 0.00 p b 0.05 Z = −1.04 p = 0.29 NS
Z = −6.57 p = 0.00 p b 0.05 Z = −2.86 p = 0.00 p b 0.05 Z = −0.44 p = 0.66 NS
Z = −0.24 p = 0.98 NS
Z = −0.74 p = 0.46 NS
Z = −0.05 p = 0.96 NS
Z = −5.03 p = 0.00 p b 0.05 Z = −3.92 p = 0.00 p b 0.05 Z = −2.56 p = 0.01 p b 0.05
Z = −3.82 p = 0.00 p b 0.05 Z = −4.04 p = 0.00 p b 0.05 Z = −4.98 p = 0.00 p b 0.05
Z = −1.33 p = 0.18 NS Z = −2.02 p = 0.04 p b 0.05 Z = −4.22 p = 0.00 p b 0.05
35.6%
33.3%
6%
24.8%
2.3% 2.3% 6.9% 88.5% 1.1% 12.7% 33.3% 52.9% 2.3% 18.4% 79.3%
1.1% 1.1% 5.8% 92% 1.1% 5.7% 40.3% 52.9% 0% 14.9% 85.1%
36% 16% 4% 44% 6% 10% 48% 36% 18% 48% 34%
10% 6% 20% 64% 0% 10% 46% 44% 4% 34% 62%
Z = −3.52 p = 0.00 p b 0.05
Z = −5.97 p = 0.00 p b 0.05
Z = −4.11 p = 0.00 p b 0.05
Z = −1.75 p = 0.08 NS
Z = −1.72 p = 0.08 NS
Z = −1.04 p = 0.29 NS
Z = −3.13 p = 0.00 p b 0.05
Z = −5.41 p = 0.00 p b 0.05
Z = −3.13 p = 0.00 p b 0.05
Z = −1.17 p = 0.24 NS Z = −5.68 p = 0.00 p b 0.05 Z = −2.75 p = 0.00 p b 0.05 Z = −0.75 p = 0.45 NS
Z = −0.89 p = 0.37 NS Z = −0.84 p = 0.40 NS Z = −1.46 p = 0.14 NS
Statistical difference
Statistical difference
Statistical difference
I—first examination, II—second examination, O—occipital presentation, B—breech presentation, NS—not significant.
difference. In the breech group, pregnancy and parity rate was significantly lower as well as Apgar score in the first minute, body length, and body weight. The difference between two groups is almost significant regarding Apgar score in the fifth minute and placental weight. Table 2 shows the results of the observed neurological parameters. Data showed statistically increased popliteal angle in the breech group compared to the occipital group at the first and the second examinations. Additionally, there was a statistically significant decrease in passive extension of the hip joint in the breech group compared to the occipital group during the first and second examinations. The occipital group showed statistically significant increased popliteal angle at the second examination relative to the first one. In the breech group, there was a statistically significant increase of passive extension in the hip joint at the second versus the first examination. The Mann–Whitney U-test confirmed the statistical significance of decreased spontaneous displacement in the breech group compared to the cephalic group at the first examination. The statistically significant decreased displacement in the breech group compared to the cephalic group was present for the crawling reflex both at the first and the second examinations. Furthermore, there were a lesser number of steps in the breech group compared to the cephalic group during automatic walking during the first and second examinations. The incidence of righting reaction in vertical position in the breech group compared to the cephalic group at the first and second examinations was significantly decreased. During the spontaneous displacement test, the occipital group showed a statistically
significant increase in spontaneous displacement at the second examination relative to the first, as well as in crawling reflex. In the breech group, there was a statistically significant higher score at the second examination compared to the first in spontaneous displacement, crawling reflex, automatic walking, righting reaction in a sitting position, and righting reaction in vertical position. The results showed a lower score for righting reactions in sitting position in the breech group relative to the occipital group at the first and second examinations. 4. Discussion This study, like some other investigations, recorded increased incidence of breech presentation in primiparas [3]. As far as breech presentation lowers the subsequent pregnancy rate, it is possible that previous breech presentation favors a woman's decision not to reproduce [12]. Body characteristics of the breech-presenting infants recorded in this study, such as a reduced body length and weight relative to the occipital group, had been present in other reports as well, even when data were adjusted for gestational age. This finding points to fetal distress and suboptimal intra-uterine development [3,8]. The impaired fetal growth does not predate breech presentation; it is a condition associated with the breech presentation [13]. Statistically, a decreased 1 min Apgar score in the breech group has also been present in other studies [4,8], suggesting that the stress resulting from the delivery is more expressed in this group of infants than in the occipital group.
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The study showed differences in neurological findings between the breech and occipital groups, which cannot be attributed to delivery trauma, identified fetal or maternal diseases. There was no statistically significant difference relative to the gestational age between the breech and occipital-presenting groups, which eliminated the bias that the younger group presented with a lower score. In the breech group, there was a significantly limited passive extension of the hip joint disabling active extension as well. Such a prenatal postural deformity can significantly affect the excitation of antigravity muscles. Previous studies showed that intra-uterine movement restriction of legs caused long-term alterations in the development of leg posture, reflexes, and posture while walking, mediated by alterations in proprioceptive feedback mechanisms [10,14]. The breech group obtained lower scores while assessing the reflexes-reactions including the hip-joint extension such as righting reaction in vertical position, automatic walking, crawling reflex, and spontaneous displacement. However, the excitation of antigravity muscles in righting reaction in a sitting position was also less expressed in the breech group at both the first and second examinations, although there was no statistically significant difference in passive movements of the trunk between the breech and occipital groups. On the other hand, there was no difference between the breech and occipital group while evaluating excitation of antigravity muscles of the neck, trunk, and lower extremities in righting reaction in horizontal suspension. Weaker excitation of extensor musculature in righting reaction and locomotor movements in the breech group, as well as the absence of difference in excitation of extensor muscles in righting reaction in horizontal suspension, suggest that this difference cannot be explained only by the limited hip-joint extension, increased popliteal angle, and alterations in proprioceptive feedback mechanisms. Decreased expression of postural reflexes caused by limited intra-uterine space can also be followed by absence of the development of central mechanisms of postural reflexes. Additionally, the intra-uterine fetal distress has to be taken into account, as well as the resulting muscle weakness of the newborn infant associated with lower scores [8]. Functional integration of righting reflexes and locomotor movements within the body posture occurs during the period from 24 to 36 gestational weeks [11]. The period from 24 to 36 gestational weeks is characterized by increased incidence of cephalic presentation and decreased incidence of breech, oblique, and transverse presentation [5]. During this period for fetuses in breech and cephalic presentation, occurs the probability to be in that very same presentation at delivery [15,16]. The decreased expression of righting reflexes and locomotor movements in the breech group suggest that during this critical period, from 24 to 36 gestational weeks, there was no complete development of these reflexes. As mentioned earlier, the fetuses change from cephalic to breech presentation and vice versa by active whole body movements such as kicking. The body rolling also has been reported as a possible movement of the fetus while changing presentation [1]. Other authors reported that the fetus changes from breech to cephalic presentation, and vice versa, by the movement of legs and feet [17]. This suggests that the fetuses change from breech to cephalic presentation, and vice versa, using all available repertoire of movements already present in the middle stage of gestation [18]. The decreased expression of righting reactions and locomotor movements in the breech group are in agreement with this. While comparing the first and second examination scores, the breech group has significantly higher scores in all reflexes and reactions relative to active motility at the second examination. The increased degree of passive hip-joint extension has also been
registered upon second examination. Obviously, the subsequent normalization of neurological findings has been reached following fetal displacement from an inadequate intra-uterine environment after the delivery. Increase in passive hip-joint extension and spontaneously generated movements of lower extremities, as well as the better characteristics of primitive reflexes during follow-ups, have also been registered in previously mentioned studies [7–9]. Our study cannot answer whether the primary cause of breech presentation in the investigated sample is of extrinsic origin – resulting from the absence of sufficient intra-uterine volume, or of intrinsic origin – resulting from fetal affection associated with temporary muscle weakness. The differences between the breech and occipital groups do not point to qualitatively different characteristics of neurological findings. They are presented by quantitative differences in expression of the righting reflexes and locomotion. The breech group does not exhibit any special characteristics of neurological findings occurring only in their group. The neurological findings present in this group have also been registered in the occipital group.
Acknowledgement This study was supported by the Serbian Ministry of Science and Environmental Protection Grant Number 143021/2006.
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