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Early Human Development
journal homepage:www.elsevier.com/locate/earlhumdev
Evaluation of Moro reflex with an objective method in late preterm and
term infants
Deniz Anuk Ince
a,⁎, Ayşe Ecevit
a, Metin Yıldız
b, Ali Ulas Tugcu
a, Burak Ceran
c,
Mustafa Agah Tekindal
d, Ozden Turan
a, Aylin Tarcan
aaDivision of Neonatology, Department of Pediatrics, Başkent University Faculty of Medicine, Ankara, Turkey bBaskent University Faculty of Engineering, Department of Biomedical Engineering, Ankara, Turkey
cDivision of Neonatology, Department of Pediatrics, Zekai Tahir Burak Maternity and Teaching Hospital, Ankara, Turkey dDepartment of Biostatistics, Selcuk University Faculty of Veterinary Medicine, Konya, Turkey
1. Introduction
Moro reflex is present as early as 28 weeks of gestation with hand opening, extension and abduction by 32 weeks and anterior flexion by 37 weeks of gestation [1]. Absence, depressed or exaggeration of the reflex may indicate central nervous system disorders and asymmetria of the Moro reflex may be related to obstetrical damage of plexus or nerve [1]. Persistence of the primitive reflexes beyond 6 months interferes with developmental and neurological impairment [2]. Preterm infants born between 25 and 34 weeks' gestation showed several differences on neurological examination at term when compared to newborn term infants [3]. Preterm born infants who evaluated at term were more hyperexcitable, have less flexor tone in the limbs and have less extensor tone in the neck [3]. Romeo et al. [4] assessed the range and frequency distribution of neonatal neurological scores in late preterm infants at term and compared with full-term newborns. Preterm infants born at 34 gestational weeks showed some differences compared to preterm in-fants born at 35 and 36 gestational weeks in visual orientation, tone and Moro reflex. However late preterm infants who was born at 35 weeks or after have a neurological scores similar to term born infants.
There are different methods for eliciting Moro response in infants [5,6]. Vestibular and proprioceptive stimulation is necessary for Moro response. The stimulation of the semicircular canals of vestibular appa-ratus and the movement of the neck that cause proprioceptive stimula-tion are very important for a strong Moro response [7]. The extension and abduction of the arms are primarily triggered by vestibular receptors after the head and trunk are tilted backwards. The flexion and adduction of the arms are triggered by proprioceptive receptors [6]. Moro response diminishes at 3 months of age and usually disappears at the end of the fourth month [8]. An absence of Moro response may be predictive for adverse developmental outcome including cerebral palsy in early infancy [9,10]. The persistence of Moro response beyond 4 months also indicates higher risk for poor developmental outcome [9].
An objective evaluation of the Moro reflex may be guide for the identification of diagnostic disorders in clinical evaluation and in determining the relationship between early and late morbidities in long-term follow-up. To date there have only been a few methods available for assessing Moro response objectively. The aim of the study was to evaluate Moro response in late preterm and term infants with a video monitorization and with three-axis accelerometer.
2. Material and methods
The study protocol was approved by the Institutional Review Board of Baskent University Faculty of Medicine, and informed consent was obtained from each infant's parents. Seventy-three infants enrolled to the study and three infants were excluded from the study due to in-tracranial hemorrhage and sepsis (Fig. 1). The subjects were 35 late preterm infants born between 34 and 36 weeks of gestation, and 35 healthy infants (the control group) born full term. All the babies were born at Baskent University Hospital between June 2015 and July 2016. The exclusion criteria were major congenital abnormalities, intracranial hemorrhage, culture-positive sepsis and respiratory distress syndrome. All infants are awake and satiated during assessment. The late preterm and term infants were assessed after 48 h of birth for physiological stabilization. The latency interval of Moro reflex was defined as the time between the stimulus was given and the onset of the lateral arm displacement. Total Moro response was defined as the time taken for a complete response.
2.1. Data collection
Moro reflex was elicited by pulling the infant from wrists and lowering the infant until there is only slight space between the neck and bed and allowing the infant to fall back suddenly [11].
https://doi.org/10.1016/j.earlhumdev.2019.01.009
Received 12 December 2018; Received in revised form 8 January 2019; Accepted 9 January 2019
⁎Corresponding author at: Department of Pediatrics, Division of Neonatology, Baskent University Hospital, Cocuk Saglıgı ve Hastalıkları Poliklinigi, Sehit Temel
Kuguoglu sok. No:24 Kat:4, 06490, Bahcelievler, Ankara, Turkey.
E-mail address:denizanuk@yahoo.com(D.A. Ince).
0378-3782/ © 2019 Elsevier B.V. All rights reserved.
The three-axis accelerometer (MMA7361L) placed on the baby's wrists which were used to monitor Moro reflex movements and a web camera (A4 Tech, Taiwan) was recorded Moro response simultaneously. The investigator analyzed the video recordings, we used MATLAB programme for the data collection and the control of the camera and accelerometers.
The accelerometers were operated in a mode capable of sensing a maximum of ± 1.5 g and the collected data were transferred to the computer by sampling with a data acquisition card (USB-1208Fs+, Measurement Computing, USA) at 1 kHz. For providing a wide field of view from the clinical practice, the video camera was programmed to capture images of 640 ∗ 480 pixels. The speed of the video recording was set up 25 frames per seconds.
Fig. 2shows the graphical user interface of the system that devel-oped for recording and measuring of Moro reflex at three-axis and with video monitorization. After the accelerometers are connected to the baby's wrists, the steerable camera is turned towards the baby. After the baby's name was entered, the video monitorization of the baby and the accelerations during the Moro reflex evaluation were recorded.
Our clinical evaluation was done in a quiet environment by the same investigator. All infants were awake during evaluation, the infants were placed in the center and head position was centered midline when the stimulus was applied. For the evaluation, first, the desired baby's data was selected and the recorded information was displayed in the windows in the user interface. When Moro reflex measurements were taken from the video images, two consecutive video images were dis-played in two windows in the interface. The investigator clicked the mouse to watch the Moro reflex images using the 2-second forward/ backward, 10-frame forward /backward, 1-frame forward/back but-tons. The first frame that the investigator leaved the baby's hand (ex-citation), the baby's reaction frame (start) and the reflex completion frames (finish) were labelled by clicking on their buttons. The latency of reflex and total Moro reflex duration were automatically calculated from the marked video frames, and the results are shown in the upper boxes in the screen.
When the data was selected for analysis, the acceleration data of two arms for three-axis were shown in the right and left windows in
Fig. 2. Firstly, the investigator selected the arm and axis to measure latency interval and duration of complete Moro response from the right panel. Meanwhile, a command holding data of the three mouse clicks were activated. We labelled three points including that the first point was labelled where the acceleration change on the x-axis started first, and second one was the maximum acceleration of the reflex response, and the last point was labelled as the complete of the response where the acceleration change returns to the initial point on the x-axis.
With video monitorization, the investigator labelled three points (first one is during the first stimulus, and second point was the reaction of the onset of the first sign of reflex response, and the last point was labelled as the complete response). From this data, Moro reflex mea-surements were performed automatically and shown as video latency interval and duration of complete Moro response in the upper text boxes in the screen.
For this study, it was also aimed to evaluate the symmetry of the movements of two arms by determining the correlation of accelerations on both sides. For each axis, the correlation between the acceleration change patterns in the two arms was calculated with reference to the shorter signal length (Eq.(1)) and was shown their boxes.
= n x x x x
n x x n x x
r 1 2 ( 1)( 2)
( 1 )2 ( 1)2 ( 2 )2 ( 2)2 (1)
In the Eq.(1), x1 and x2 show x, y, z axis acceleration data for both arms. The n showed used sample length. All results could be stored in a format that can be processed in excel when the click a button on the user interface.
In addition to video monitorization and accelerometer, we eval-uated the symmetry of the Moro reflex based on visual observation. We reported the Moro response as symmetric and asymmetric.
2.2. Statistical analysis
A power analysis, after evaluation of Biostatistics power of 80%, a significance level of α = 0.05 indicated a minimum of 35 infants. For discrete and continuous variables, descriptive statistics (mean, standard deviation, median, minimum value, maximum value, and percentile)
73 infants enrolled
Excluded (n= 3 )
Culture positive sepsis (n= 2)
Intracranial hemorrhage (n= 1)
35 late preterm group
35 term group
70 infants enrolled
35 term infants evaluated
35 late preterm infants evaluated
were given. In addition, the homogeneity of the variances, which is one of the prerequisites of parametric tests, was checked through Levene's test. The assumption of normality was tested via the Shapiro-Wilk test. To compare the differences between the two groups, the Student's t-test was used when the parametric test prerequisites were fulfilled, and the Mann Whitney U test was used when such prerequisites were not ful-filled. The data were evaluated via SPPS 20 (IBM Corp. Released 2011. IBM SPSS Statistics for Windows, Version 20.0. Armonk, NY: IBM Corp.). p < 0.05 and p < 0.01 were taken as significance levels. 3. Results
For the late preterm and term infants, mean gestational ages were 35.09 ± 0.9 weeks and 38.23 ± 0.9 weeks, respectively, and mean birth weights were 2282.43 ± 396 g and 3116.57 ± 506 g. The de-mographic and clinical features of the late preterm and term infants are presented inTable 1.
The mean latency interval for the late preterm infants (mean ± SD) was 0.48 ± 0.17 s and 0,49 ± 0,38 s for term group with video monitorization. There was significant difference for latency interval in the x- and z-axis of left arm between two groups (p-value: 0.01; p-value: 0.04) and there was significant difference at right arm complete Moro response on x- and y-axis with accelerometer between late preterm and term infants (p < 0.05) (Table 2).
The average correlation of x and z axis Moro response of right and left arm revealed no significant difference (late preterm and term, mean ± SD 0.29 ± 0.22, 0.32 ± 0.16 (p-value: 0.62), and 0.33 ± 0.23, 0.22 ± 0.25; p-value: 0.05); however, there was sig-nificant difference for y-axis Moro response of right and left arm
between late preterm and term infants (late preterm and term, mean ± SD 0.27 ± 0.1, 0.37 ± 0.23; p-value: 0.038) (Table 2).
Moro response for three-axis showed significant difference right-left arm y and z axis between two groups. It was observed that 72% of those who were symmetrical based on Moro reflex evaluation with accel-erometer were symmetrical with visually evaluation. However 65% of the results which were asymmetrical with accelerometer were observed to be symmetrical in the visually evaluation (p-value: 0.03) (Table 2). The late preterm and term infants' percentile results for latency interval and duration of complete Moro response of right and left arm for three-axis and video monitorization are given inTable 3.
4. Discussion
Moro reflex was evaluated with an objective method in our study. We used three-axis accelerometer for the analysis of Moro reflex and video monitorization was done simultaneously. Using this technique, we observed that there was significant difference for latency interval in the x- and z-axis of left arm between two groups with accelerometer however the latency interval of Moro reflex and total Moro reflex duration did not show difference between late preterm and term infants with video monitorization.
Late preterm infants showed different neurological profile according to term infants. Although term infants and the infants born at 35 and 36 weeks' gestational age have similar neurological profile in the tone (marked flexor tone), Moro reflex and head control; the infants born at 34 weeks gestational age had a more immature profile [4]. Moro reflex is usually evaluated as normal, asymmetric or absent. There are few studies evaluating Moro reflex qualitatively [6,11–13]. In our study, we observed that there was significant difference for latency interval of left arm in two axes between two groups with accelerometer however there was no difference between late preterm and term infants with video monitorization. The vestibular stimulus could be adequate for Moro response. The afferent input is responsible for the elicitation of response that the semicircular canals of the vestibular apparatus are important for strong Moro response [7]. Bijesh et al. [13] evaluated latency tervals of Moro reflex in newborns after 48 h of birth. The latency in-terval of Moro response was 0.41–0.49 s and latency inin-terval was Fig. 2. The graphical user interface for recording and measuring of Moro reflex at three-axis and with video monitorization.
Table 1
Demographic features of late preterm and term infants.
Late preterm (n = 35) Term (n = 35)
Gestational age (wks) M ± SD 35.09 ± 0.9 38.23 ± 0.9
Birth weight (g) M ± SD 2282.43 ± 396 3116.57 ± 506
Gender (female/male) (n) 22/13 15/20
classified as normal (0.41–0.49 s), short (< 0.41 s) and long (> 0.49 s) in that study. Short latency intervals may be related to long term be-havior problems such as mood instability, short concentration span and learning difficulty. Long latency intervals may be related to central nervous system pathology [14]. In our study the mean latency interval for preterm infants was 0.48 ± 0.17 s. and the mean latency interval for term infants was 0,49 ± 0,38 s that were both in normal range with video monitorization.
In our study, there was significant difference at right arm complete Moro response on x- and y-axis with accelerometer between late
preterm and term infants. Preterm infants have shorter duration of Moro response that they were more hyperexcitable, have less flexor tone in the limbs and have less extensor tone in the neck, this difference may related to shorter response of preterm infants [3].
Rönnqvist et al. [6] showed that asymmetric Moro response may be normal as revealed by the three-dimensional velocity and accel-erometer however the studies reported until today showed asymmetric Moro response were related to pathologic conditions. Asymmetric Moro reflex may be related to head position [12]. Rönnqvist et al. [6] ex-cluded asymmetry based on an asymmetrical position of the head, that if the head was turned one side during the administration of the sti-mulus this could be concluded with an asymmetric response. Rönnqvist indicated that at least one feature of Moro response was asymmetric in their study. To evaluate this response with naked eye is difficult. This response may be due to intrauterine lateralized position of the fetus during last trimester. The left otolithic development is dominant at this period [15]. The results of our study showed that Moro response may be mistaken in determining asymmetry based on visually evaluation. In our study 65% of the Moro response which were asymmetrical with accelerometer were observed to be symmetrical in the visually eva-luation. Hepper et al. [16] think that asymmetry may be related to early fetal hand preference which was seen with ultrasonographic evalua-tions by 15 weeks of gestational age with fetal thumb sucking. Our results were similar in preterm and term infants including video latency interval and duration of complete Moro response, there was significant difference at right arm complete Moro response on x- and y-axis with accelerometer between late preterm and term infants. Term infants have marked flexor tone that Moro response was significantly shorter in preterm group [4].
In our study the infants were placed in the center and head position was centered midline when the stimulus was applied. Also postnatal age is an important for symmetry between arms, Prechtl et al. [17] re-marked infants were physiologically unstable in the first two days of life. In a study evaluating Moro response in 15 term infants with a full-body drop method, they measured onset latency and time-to-peak ac-celeration of both arms. They found that infants who were at postnatal 1 or 2 days had a less marked asymmetry between two arms when compared with the infants 3–5 days old. In our study we evaluated Moro response in 70 late preterm and term infants at 48 h of birth, and there was no significant difference at x and z axes of Moro response of right and left arm between two groups.
Sohn et al. [18] assessed primitive reflexes in high risk newborns and showed that Apgar scores and length of hospitalization were sta-tistically associated with the sucking and Babinski reflexes but there was no relation with Moro reflex. These results may represent that Moro reflex is related to development according to pathologic situa-tions.
Hepper et al. [15] observed that fetal thumb sucking is pre-dominantly right handed from 15 weeks of gestational age which will appear before a lateralized fetal position. Rönnqvist et al. [6] in-vestigated symmetry and state relation of Moro response. The study included 52 newborn infants with gestational age 36–42 weeks. Moro response was evaluated on 1–5 day of life. The mean Moro response durations were 1.09–1.56 s and the latencies were significantly shorter in right arm. Our study showed, there was significant difference of total Moro response in x- and y-axis of right arm between preterm and term infants with accelerometer that the total Moro response durations were shorter in preterm infants. Rönnqvist et al. [6] showed that the as-sumption of head position is state dependent, head position preference begins during the infant is in state 3. Rönnqvist and Hopkins [19] showed that newborns who were born < 3000 g birth weight or who were small for gestational age maintain their head in the midline po-sition. The infants with a birth weight > 3000 g may have stronger neck muscles to turn the head lateralized position [19]. Future studies in-vestigating the relationship between the muscle properties of the pre-term and pre-term infant and the Moro response should be planned. Table 2
Comparisons of latency intervals and Moro response for the late preterm and term infants. Group p Preterm (n = 35) (Mean ± SD) (Median) (Min–max.) Term (n = 35) (Mean ± SD) (Median) (Min–max.) Video latency interval (s) 0.48 ± 0.17
0.46 (0.14–1.07) 0.49 ± 0.38 0.43 (0.13–1.89) 0.87 Video duration of complete
Moro response (s) 1.49 ± 0.51.33 (0.61–2.5) 1.54 ± 0.56 1.52 (0.74–2.7) 0.70 Left arm latency x-axis (s) 0,04 ± 0,03
0.02 (0.0–0.1) 0,08 ± 0,08 0.04 (0.01–0.35) 0,01⁎ Left arm Moro response
x-axis (s) 0,75 ± 0,620.67 (0.14–2.6) 0,94 ± 0,45 0.81 (0.43–2.3) 0,13 Left arm latency y-axis (s) 0,14 ± 0,42
0.04 (0.01–2.14) 0,08 ± 0,09 0.05 (0.01–0.54) 0,40 Left arm Moro y-axis (s) 0,79 ± 0,63
0.79 (0.1–2.2) 1,02 ± 0,49 0.95 (0.39–2.3) 0,09 Left arm latency z-axis (s) 0,06 ± 0,07
0.05 (0.01–0.36) 0,1 ± 0,09 0.08 (0.0–0.4) 0,04⁎ Left arm Moro z-axis (s) 0,7 ± 0,66
0.5 (0.08–3.2) 0,86 ± 0,6 0.85 (0.01–2.5) 0,31 Right arm latency x-axis 0,05 ± 0,05
0.03 (0.00–0.19) 0,06 ± 0,05 0.05 (0.01–0.2) 0,19 Right arm Moro response
x-axis (s) 0,67 ± 0,630.51 (0.06–3.3) 0,96 ± 0,43 0.81 (0.22–2.3) 0,03⁎ Right arm latency y-axis (s) 0,06 ± 0,07
0.04 (0.00–0.28) 0,06 ± 0,05 0.04 (0.01–0.2) 0,96 Right arm Moro response
y-axis (s) 0,72 ± 0,650.53 (0.07–3.3) 1 ± 0,5 0.82 (0.36–2.2) 0,05⁎ Right arm latency z-axis (s) 0,02 ± 0,05
0.0001 (0.00–0.2) 0,03 ± 0,05 0.0001 (0.00–0.2) 0,25 Right arm Moro response
z-axis (s) 0,73 ± 0,590.58 (0.09–3) 0,98 ± 0,54 0.81 (0.37–2.6) 0,07 Average correlation
right-left arm x-axis Moro response (s) 0,18 ± 0,29 0.14 (−0.45–0.68) 0,31 ± 0,36 0.29 (−0.59–0.91) 0,10 Average correlation
right-left arm y-axis Moro response (s) −0,12 ± 0,31 −0.10 (−0.80–0.56) 0,05 ± 0,4 0.04 (−0.88–0.77) 0,04⁎ Average correlation
right-left arm z-axis Moro response (s) 0,18 ± 0,37 0.22 (−0.82–0.92) −0,07 ± 0,34 −0.02 (−0.69–0.79) 0,004⁎
Abbreviations: SD, standard deviation; s, second.
Moro response and latency interval were measured by using a new application and also video monitorization was used for confirmation which were the strengths of the study. The asymmetry seen in two axes in preterm and term infants may be related to the more pronounced flexor tonus in term infants. We believe that the evaluation of Moro reflex with an objective method may be a guide for early diagnosis of neurodevelopmental disorders and also may help to prevent long term complications.
Statement of financial support
This research was supported by Turkish Neonatology Society (grant).
Funder role
The funders did not play a role in study design, collection, analysis and interpretation of data, writing of the report nor in the decision to submit this manuscript to Early Human Development.
Competing interests None.
Disclosure statement
None, all authors have approved the final article. Conflict of interest statement
None.
Contributors statement
Dr. Ince conceptualized and designed the study, and acquired the data and interpreted findings, and wrote the first draft of the manu-script, worked on methodology, reviewed and edited the manumanu-script, supervised and approved the final manuscript as submitted.
Dr. Ecevit conceptualized the study, interpreted the data, supervised and approved the final manuscript as submitted.
Dr. Yıldız contributed the design of the study, carried out data collection and provided interpretation of the data, developed software programme, worked on methodology, validated developed programme, drafted the initial paper and approved the final manuscript as sub-mitted.
Dr. Tugcu, Dr. Ceran, Dr. Turan supported the data collection,
supported edits and subsequent drafts of the manuscript, and approved the final manuscript as submitted.
Dr. Tekindal contributed the design of the study, interpreted and analyzed the data and drafted the manuscript, reviewed, edited the manuscript and approved the final manuscript as submitted.
Dr. Tarcan conceptualized the idea for this study, interpreted and analyzed the data, worked on methodology, reviewed and revised the manuscript and approved the final manuscript as submitted.
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Table 3
Percentile (p) results for latency intervals and Moro response for the late preterm and term infants.
Late preterm (n = 35) Term (n = 35)
25th pa 50th pa 75th pa 25th pa 50th pa 75th pa
Video latency interval (s) 0.34 0.46 0.58 0.21 0.43 0.64
Video duration of complete Moro response (s) 1.1 1.33 1.74 1.04 1.52 2.05
Left arm latency x-axis (s) 0.01 0.02 0.05 0.02 0.04 0.09
Left arm Moro response x-axis (s) 0.29 0.67 0.95 0.61 0.81 1.03
Left arm latency y-axis (s) 0.02 0.04 0.06 0.03 0.05 0.09
Left arm Moro y-axis (s) 0.26 0.79 0.92 0.65 0.95 1.20
Left arm latency z-axis (s) 0.03 0.05 0.07 0.04 0.08 0.13
Left arm Moro z-axis (s) 0.20 0.50 0.98 0.40 0.85 1.13
Right arm latency x-axis 0.02 0.03 0.06 0.03 0.05 0.09
Right arm Moro response x-axis (s) 0.22 0.51 0.89 0.67 0.81 1.18
Right arm latency y-axis (s) 0.01 0.04 0.07 0.02 0.04 0.09
Right arm Moro response y-axis (s) 0.24 0.53 1.01 0.58 0.82 1.33
Right arm latency z-axis (s) 0.0001 0.01 0.02 0.0001 0.01 0.10
Right arm Moro response z-axis (s) 0.32 0.58 0.97 0.66 0.81 1.13
