Heart rate variability in infants with central coordination disturbance

doi:10.1016/j.earlhumdev.2010.01.022

Early Human Development

Volume 86, Issue 2, February 2010, Pages 77-81

https://doi.org/10.1016/j.earlhumdev.2010.01.022 Get rights and content

Abstract

Despite a remarkable medical progress in the field of Developmental Medicine and Child Neurology, early identification of infants at risk for permanent motor disabilities still presents challenge for both clinicians and researchers.

As an indicator of cardiac autonomic control, it was shown that heart rate variability (HRV) might reflect not only sympathetic or parasympathetic activity but also functional integrity of the central nervous system (CNS). Furthermore a pattern of HRV was demonstrated to correlate with motor developmental outcome in high risk infants.

The purpose of this study was to analyze the clinical usefulness as well as predictive value of time-domain HRV parameters in infants with central coordination disturbance.

The study included 35 infants with central coordination disturbance and 37 healthy age and sex-matched controls. Time-domain HRV indices were analyzed from 24-h electrocardiography recordings.

We found significantly lower values of SDNN, SDANN and RMSSD parameters in infants with central coordination disturbance compared to controls. Additionally, logistic regression analyses demonstrated independent predictive value of parameters SDNN and SDANN in infants who subsequently developed cerebral palsy (CP). By performing receiver operating characteristic (ROC) analyses, the optimal cut-off value of SDNN <= 48 ms predicted CP with a sensitivity of 68.7% (95% CI 41.4–88.9) and specificity of 84.2% (95 CI 60.4–96.4) while the optimal cut-off value of SDANN <= 41 ms predicted CP with a sensitivity of 87.5% (95% CI 61.6–98.1) and specificity of 57.9% (95 CI 33.5–79.7).

We are in opinion that time domain HRV analysis could be helpful clinically as well as a prognostic tool in infants with central coordination disturbance.

Introduction

To date there are numerous instruments dealing with an early diagnosis of cerebral palsy [1]. Their reliability, sensitivity and validity vary greatly, and each one's predictive power increases with the age of the infant or the young child [2].

It was shown that evaluation of neural regulation of the heart provides useful information not only of sympathetic or parasympathetic activity but also on functional integrity of the central nervous system [3]. Additionally, it was shown that heart rate variability (HRV) analyses could give useful information regarding infant's regulatory abilities and their neurodevelopment outcome [4], [5], [6], [7].

However, the lack of standardized methods, cut-off values as well as reliable parameters has resulted in poor clinical usage of HRV analyses in pediatric population.

The purpose of the current study was to assess the clinical usefulness as well as predictive value of time-domain indices of HRV in infants with central coordination disturbance [8], [9], [10].

Section snippets

Method

From June 2005 to August 2008, 46 consecutive infants admitted at our institution and diagnosed to have central coordination disturbance were enrolled in the study.

After complete pediatric and neurologic examination, routine laboratory analysis (standard hematological, biochemical and urinary tests) and metabolic tests (in selected cases), 35 infants (22 males and 13 females) were finally included in study.

Three infants with anemia, two infants with dysmorphic facial features and one infant,

HRV analyses

24-h ECG-Holter monitoring (Cardiolight FMC.A, Medset, and Medizintechnik, Hamburg, Germany, distributed in Serbia by company HAPEL, Belgrade) without selection of epochs relevant to sleep, was performed the same day as an echocardiography examination on all healthy infant controls, and within one week after initial neurological examination on all examiners. To determine HRV parameters, appropriate Holter software was used. Before HRV analyses we have checked the precision of computer assisted

Statistics

Descriptive data were presented as a mean values with standard deviation (SD) and range. Student's two-sample t-test for independent groups was used to compare time domain parameters and average heart rate in both groups.

Logistic regression model and receiver operating characteristic (ROC) analyses were performed to identify possible parameters and cut-off values in predicting cerebral palsy. Nonparametric data in some groups were compared using Chi-quadrat test or two-tailed Fisher's exact

Results

There were 35 infants (22 males and 13 females) diagnosed to have central coordination disturbance, mean corrected age 4.6 ± 1.3 months (age range 2–6 months) and 37 control infants (21 males and 16 females) mean corrected age 3.5 ± 1.1 months (age range 2–6 months). There wasn't a statistically significant age and sex difference between groups (p > 0.05). Among the examiners, 16 infants had light/mild and 19 infants had severe central coordination disturbance.

After follow up period of 18 months, the

Discussion

The assumption that central nervous system functional competence impacts on the wide range of physiological system abnormalities has long been acknowledged [14]. However, many studies related on neurodevelopment pathology still focuses on particular central nervous morphologic abnormalities rather than assessing its functional state [15].

Up to date a wealth of evidences demonstrated HRV analysis as a helpful clinical tool giving useful information regarding autonomic and concomitantly central

Acknowledgement

This work was supported by grant No 145004 from the Ministry of Science and Technological Development of Serbia.

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Cited by (17)

Assessment of general movements and heart rate variability in prediction of neurodevelopmental outcome in preterm infants
2016, Early Human Development
Citation Excerpt :
In our previous study, we demonstrated that HRV could be helpful clinically as well as a prognostic tool in infants with developmental coordination disorders. This study was the first to report the relationship between 24 h HRV time-domain indices and the infant neurodevelopmental status as well as their neurodevelopmental outcome, favouring a hypothesis of enhanced sympathetic and low parasympathetic nervous system activity in infants with neurodevelopmental abnormalities [17,18]. The purpose of the current study was to demonstrate the extent to which GM assessment can predict neurological outcome in preterm infants in our clinical setting; and to assess the clinical usefulness of time-domain indices of HRV in improving the predictive value of PR GMs in the writhing period.
Adverse neurologic outcome in preterm infants could be associated with abnormal heart rate (HR) characteristics as well as with abnormal general movements (GMs) in the 1st month of life.
To demonstrate to what extent GMs assessment can predict neurological outcome in preterm infants in our clinical setting; and to assess the clinical usefulness of time-domain indices of heart rate variability (HRV) in improving predictive value of poor repertoire (PR) GMs in writhing period.
Qualitative assessment of GMs at 1 and 3 months corrected age; 24 h electrocardiography (ECG) recordings and analyzing HRV at 1 month corrected age.
Seventy nine premature infants at risk of neurodevelopmental impairments were included prospectively.
Neurodevelopmental outcome was assessed at the age of 2 years corrected. Children were classified as having normal neurodevelopmental status, minor neurologic dysfunction (MND), or cerebral palsy (CP).
We found that GMs in writhing period (1 month corrected age) predicted CP at 2 years with sensitivity of 100%, and specificity of 72.1%. Our results demonstrated the excellent predictive value of cramped synchronized (CS) GMs, but not of PR pattern. Analyzing separately a group of infants with PR GMs we found significantly lower values of HRV parameters in infants who later developed CP or MND vs. infants with PR GMs who had normal outcome.
The quality of GMs was predictive for neurodevelopmental outcome at 2 years. Prediction of PR GMs was significantly enhanced with analyzing HRV parameters.
Differences in autonomic functions as related to induced stress between children with and without cerebral palsy while performing a virtual meal-making task
2016, Research in Developmental Disabilities
Citation Excerpt :
Several studies used biological markers associated with emotion regulation (Graziano & Derefinko, 2013), employing measures that are sensitive to autonomic nervous system (ANS) functions (Fusar-Poli, Landi, & O’Connor, 2009; Hempel, Tulen, van Beveren, Mulder, & Hengeveld, 2007; Porges, 2009; Porges et al., 2007; Utendale et al., 2013). Only a few studies have measured differences in autonomic functions between children with and without CP, most focusing on differences in heart rate variability (HRV) as a biomarker of sympathovagal balance (Bjelakovic et al., 2010; Ferreira et al., 2011; Kholod, Jamil, & Katz-Leurer, 2013; Park, Park, Cho, Lee, & Kim, 2002; Yang et al., 2002; Zamuner et al., 2011). Overall, children with CP were found to have significantly higher sympathetic activity and lower parasympathetic activity compared to typically developing children (Bjelakovic et al., 2010; Ferreira et al., 2011).
Efforts to improve the participation and performance of children with cerebral palsy (CP) are often related to the adaptation of environmental conditions to meet their cognitive and motor abilities. However, the influence of affective stimuli within the environment on emotion and performance, and their ability to improve or impede the children's participation has not been investigated in any systematic way although the emerging evidence suggests that it affects the individuals in many levels.
(1) To measure autonomic responses to affective stimuli during a simulated Meal-Maker task in children with CP in comparison to children who are typically developing, and (2) to examine the interactions between autonomic functions, subjective reports of stress, and task performance among children with and without CP.
Fifteen children with CP and 19 typically developing peers (6 to 12 years) participated. After completing behavioral questionnaires (e.g., State and Trait Anxiety Inventories), children prepared meals within a camera tracking virtual Meal-Maker environment. Either a negative, positive, or neutral visual stimulus was displayed, selected from the International Affective Picture System. Children also passively viewed the same pictures while rating their valence and arousal levels. Heart rate (HR) and skin conductance were recorded synchronously with stimulus onset.
Significant differences in autonomic functions were found between groups, i.e., a higher “low frequency” to “high frequency” (LF:HF) ratio in the children with CP during the meals associated with a negative stimulus (p = 0.011). Only children with CP had significant positive correlations between trait anxiety and LF:HF ratio during virtual meal-making associated with positive (p = 0.049) and negative stimuli (p = 0.003) but not during neutral stimuli. For children with CP the amplitude of skin conductance response during passive picture viewing was significantly higher for negative than for positive stimuli (p = 0.017) but there were no significant changes in autonomic responses during virtual Meal-Maker task.
Significant correlations between trait anxiety, autonomic activity during the calm state and Meal-Maker performance outcomes were found only for children with CP.
In general, the Meal-Maker virtual environment was shown to be a feasible platform for the investigation of the effect of emotionally loaded stimuli on the balance of autonomic functions in children with and without CP. Anxiety level appears to play a significant role in children with CP and should be considered as a potentially important factor during clinical evaluation and intervention. Further studies are needed to develop additional measurements of emotional responses and to refine the types of affective interference.
Heart rate variability during sleep in children with multiple disabilities
2013, Archives de Pediatrie
Étudier la variabilité du rythme cardiaque de l’enfant polyhandicapé pendant le sommeil afin d’observer le comportement de son système nerveux autonome.
La variabilité de l’intervalle R-R d’enfants de 4 à 12 ans a été enregistrée avec un cardiofréquencemètre durant une nuit. La comparaison entre enfants polyhandicapés (G1) et enfants sains (G2) a été réalisée dans les domaines temporel, fréquentiel et non linéaire.
Diverses variables temporelles (p < 0,01), fréquentielles (p < 0,05) et non linéaires (p < 0,01) du G1 étaient inférieures à celles du G2.
L’analyse temporelle et fréquentielle a confirmé une prédominance du système nerveux sympathique pendant le sommeil du G1. Des variables non linéaires réduites peuvent expliquer un sommeil moins riche en informations (dimension de corrélation : 2,203 ± 1,239 versus 3,842 ± 0,378 ; p < 0,001), aux cycles du sommeil moins complexes (entropie approximée 1,153 ± 0,200 versus 1,365 ± 0,099 ; p < 0,01) et à la variabilité à court terme moins corrélée (SD1 : 42,37 ± 19,0 ms versus 73,44 ± 25,3 ; p < 0,01). La structure fractale des enregistrements n’était pas altérée (p > 0,05). Les pathologies rencontrées sont probablement à l’origine de ces constatations, mais la diversité des troubles et des traitements des enfants polyhandicapés nécessiterait l’étude d’un échantillon plus large et plus varié.
La prédominance sympathique durant le sommeil de l’enfant polyhandicapé est associée à une réduction des capacités d’adaptation de son système nerveux autonome.
To study heart rate variability during sleep in children with multiple disabilities in order to observe the behavior of the autonomic nervous system.
The R-R interval variability of 4 to 12 years old children was recorded with a heart rate monitor during one night. Children with multiple disabilities (G1) and healthy children (G2) were compared in time, frequency, and non-linear domains.
Temporal (P < 0.01), frequency (P < 0.05), and non-linear (P < 0.01) variables in the G1 were lower than in the G2 group.
The time and frequency analysis confirmed the predominance of the sympathetic nervous system during sleep in G1 children. Reduced non-linear variables can explain sleep with less informations (correlation dimension: 2.203 ± 1.239 versus 3.842 ± 0.378; P < 0.001), less complex cycles of sleep (approximate entropy: 1.153 ± 0.200 versus 1.365 ± 0.099; P < 0.01), and a reduced correlation in short-term variability (SD1: 42.37 ± 19.0 (ms) versus 73.44 ± 25.3; P < 0.01). The fractal structure of the recordings was not affected (P > 0.05). The diseases encountered are probably the reason for these findings, but the variety of disorders and medications of the children with multiple disabilities needs to be studied with a larger and more varied sample.
Sympathetic predominance during sleep in children with multiple disabilities is associated with a decrease in adaptive abilities of these children's autonomic nervous system.
Skin temperature responses to cold stress in patients with severe motor and intellectual disabilities
2013, Brain and Development
Patients with severe motor and intellectual disabilities (SMID) often suffer from autonomic nervous system disturbances. At the same time, the caregivers of patients with SMID face challenges to understand the patients’ chronic health problems effectively by simply observing them. Therefore, recognizing specific symptoms is important to improve support for SMID. We investigated the autonomic nervous function in patients with SMID with skin vasomotor responses to cold stimuli. The relationship of the results of cold stress and autonomic symptoms observed by the main caretakers was also examined. We analyzed 38 patients with SMID. Their hand skin temperature was measured before and after cold stimuli using infrared thermography. A ‘distal-dorsal difference’ (DDD) at baseline, and the recovery rate of the second fingertip and dorsum were calculated. All main caregivers filled out questionnaires evaluating autonomic symptoms. The recovery rate of the second fingertip and dorsum after cold stimuli was lower than 80% in 64% and 60% patients, respectively. The baseline DDD was greater than 1 °C in 84% of the patients. A DDD > 1 °C was associated with a reduced recovery rate. All caregivers recognized some autonomic-related symptoms. Patients with constipation or snoring demonstrated a reduced recovery rate. However, none of the observed symptoms can predict the presence of a reduced rate with cold stimuli in a statistically significant way. This study showed excessive sympathetic nerve activities in patients with SMID. The baseline DDD could be a valuable parameter accessing their microvascular circulation. To improve the life of a person with SMID, accessing autonomic function using a noninvasive method, such as thermography is warranted without directly observed symptoms.
Artificial neural networks based prediction of cerebral palsy in infants with central coordination disturbance
2012, Early Human Development
Citation Excerpt :
There were no statistically significant differences in neurological outcome between infants with severe vs. infants with light/mild central coordination disturbance. Additionally, using Chi-square test we did not find association between postural reactions and final neurological outcome (p > 0.05) [8]. Within the group of infants with CCD, we also found significantly lower values of SDNN and SDANN but not RMSSD values for infants who developed CP (p = 0.008, p = 0.018 and p = 0.39 respectively).
In a previous study we demonstrated that heart variability parameters (HRV) could be helpful clinically as well as a prognostic tool in infants with central coordination disturbance (CCD). In recent years, outcome predictions using artificial neural networks (ANN) have been developed in many areas of health care research, but there are no published studies considered ANN models for prediction of cerebral palsy (CP) development.
To compare the results of an ANN analysis with results of regression analysis, using the same data set and the same clinical and HRV parameters.
The study included 35 infants with CCD and 37 healthy age and sex-matched controls. Time-domain HRV indices were analyzed from 24 h electrocardiography recordings. Clinical parameters and selected time domain HRV parameters are used to predict CP by logistic regression, and then an ANN analysis was applied to the same data set. Input variables were age, gender, postural responses, heart rate parameters (minimum, maximum and average), and time domain parameters of HRV (SDNN, SDANN and RMSSD). For each of one the pairs of ANN and clinical predictors, the area under the receiver operating characteristic (ROC) curves with test accuracy parameters were calculated and compared.
In the observed dataset, ANN model overall correctly classified all infants, compared with 86.11% correct classification for the logistic regression model, and compared with 67.65% and 77.14% for SDANN and SDNN respectively.
ANN model, based on clinical and HRV data can predict development of CP in patients with CCD with accuracy greater than 90%. Our results strongly indicate that a well-validated ANN may have a role in the clinical prediction of CP in infants with CCD.
Heart rate variability in children and adolescents with cerebral palsy—a systematic literature review
2020, Journal of Clinical Medicine

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Heart rate variability in infants with central coordination disturbance

Abstract

Introduction

Section snippets

Method

HRV analyses

Statistics

Results

Discussion

Acknowledgement

Early Hum Dev

Early Hum Dev

Biol Psychol

Pediatr Neurol

Early Hum Dev

Intrauterine growth retardation, general movements, and neurodevelopmental outcome: a review

Dev Med Child Neurol

Agreement between scales for screening and diagnosis of motor development at 6 months

J Pediatr (Rio J)

Maturation of autonomic control in preterm infants

Dev Psychobiol

Porges S The relation between neonatal period patterns and development outcome

Child Dev

Vagal regulation of heart rate in the prediction of developmental outcome for very low birth weight preterm infants

Child Dev

Abnormal heart rate variability as manifestation of autonomic dysfunction in hemispheric brain infarction

Stroke

Non-invasive assessment of cardioregulatory autonomic functions in children with epilepsy

Acta Neurol Scand