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Original Articles
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ПОЧКИ KIDNEYS
UDK 616.613-002-036.4-053.2:612.172 DOI: 10.22141/2307-1257.8.2.2019.166664
L.I. Vakulenko
State Institution "Dnipropetrovsk Medical Academy of the Ministry of Health of Ukraine", Dnipro, Ukraine
Heart rate variability in children with chronic pyelonephritis and I-III stages of chronic kidney disease
For cite: Pocki. 2019;8(2):88-93. doi: 10.22141/2307-1257.8.2.2019.166664
Abstract. Background. Assessment of heart rate variability allows us to get an idea about the functional state of the autonomic nervous system and to identify changes in autonomic homeostasis in children. The purpose was to study the features of vegetative regulation in children with chronic pyelonephritis at the initial stages of chronic kidney disease by analyzing heart rate variability. Materials and methods. There were surveyed 94 children aged 6-17 years without exacerbation of chronic pyelonephritis with CKD stage I-III. There was conducted daily monitoring of ECG, followed by mathematical processing. Results. Analysis of the statistical characteristics of the Z-scores of the time analysis indicators revealed a significant decrease in the standard (root-mean-square) deviations of the RR interval in patients of all groups with a significant decrease in this indicator in children with CKD stage III. A significant decrease in RMSSD values was demonstrated in patients with CKD stage III, and patients with CKD stages I to III demonstrated pNN50 decline. In a spectral analysis, patients showed a significant increase in the total power of the spectrum of heart rate variability of TP and its domains (VLF, LF), sympathetic-parasympathetic ratio of LF to HF and decrease of HF. Conclusions. 76.6 % of children with chronic pyelonephritis and CKD stage I-III presented with the vegetative imbalance. With the progression of CKD, the autonomic imbalance exacerbated, as evidenced by the presence of correlations between the glomerular filtration rate and findings of time (SDNN, pNN50) and spectral (TP, LF, HF) analysis of heart rate variability. The revealed changes suggest the expected development of cardiovascular disorders even before the appearance of significant changes in the central hemodynamics.
Keywords: heart rate variability; children; chronic pyelonephritis; chronic kidney disease
Introduction
Cardiovascular pathology leads to the death in the majority cases both in adults and children with chronic kidney disease (CKD) [1, 2]. However, in children and adolescents with CKD, cardiovascular complications usually have subclinical course, starting developing already at the early stages [3, 4]. With the progression of CKD, the importance of the sympathetic nervous system increases, which activity is accompanied by the increase of cardiovascular risks [5]. Damage and disorder of the structures of the autonomic nervous system leads to morphological rearrangements of the cardiovascular system associated with the release of mediators, hormones, biologically active substances, which, in turn, enhance the autonomic imbalance and provoke the
© «Нирки» / «Почки» / «Kidneys» (Pocki), 2019
© Видавець Заславський О.Ю. / Издатель Заславский А.Ю. / Publisher Zaslavsky O.Yu., 2019
development of a number of biochemical and immune shifts in the body [6]. At present, the most informative non-invasive method for quantitative assessment of the autonomic regulation of heart rate is the study of heart rate variability (HRV), which gives an opportunity to get an idea of the functional state of the CNS and to identify changes in vegetative homeostasis in children. In scientific publications, information on the results of HRV study in adult patients with terminal stage of chronic renal failure [7—9], as well as the effect of hemodialysis on the parameters of the CNS in this cohort of patients [10, 11] were highlighted. There are no enough data on the state of functional reserves of autonomic regulation, neurohumoral regulation of the heart, the ratio between sympathetic and parasympathe-
Для кореспонденци: Вакуленко Людмила 1вашвна, кандидат медичних наук, доцент кафедри пед1атри 2, ДЗ «Днтропетровська медична академ1я МОЗ УкраТни», вул. Вернадського, 9, м. Днтро, 49044, УкраТна; e-mail: [email protected]; контактний тел.: +38 (097) 158-88-88.
For correspondence: Liudmyla Vakulenko, PhD, MD, Associate Professor at the Department of pediatrics 2, State Institution "Dnipropetrovsk Medical Academy of the Ministry of Health of Ukraine'; Vernadsky str., 9, Dnipro, 49044, Ukraine; e-mail: [email protected], phone: +38 (097) 158-88-88.
tic parts of the autonomic nervous system in children with CKD [12, 13].
Purpose: to study the peculiarities of autonomic regulation in children with chronic pyelonephritis at the initial stages of CKD by analyzing the heart rate variability.
Materials and methods
There were examined 94 children aged from 6 to 17 years (41 boys and 53 girls) with chronic pyelonephritis with CKD stage I—III. The control group consisted of 78 virtually healthy children of the corresponding age. The patients were divided into groups depending on the stage of chronic kidney disease: the first group included 47 children with CKD stage I (GFR > 90 ml/min), the second group — 30 patients with CKD stage II (GFR from 60 to 90 ml/min), the third group — 17 patients with CKD stage III (GFR from 30 to 59 ml/min).
The planned clinical trial was approved by the Bioethics Committee of Dnipropetrovsk Medical Academy of the Ministry of Health of Ukraine and conducted in accordance with the guidelines of the Helsinki Declaration (1975). All participants and/or their parents were fully informed about the methods and scope of the study and provided written informed consent to participate.
The criteria for inclusion of patients in the study were following: the presence of the voluntary informed consent of a child and his/her parents to participate in the clinical study; age of patients from 6 years to 17 years 11 months 29 days; presence of verified diagnosis of chronic pyelonephritis; the absence of clinical and laboratory signs of exacerbation of chronic pyelonephritis. The criteria for exclusion of patients from the study were: refusal of a child or his/her parents to participate in a clinical trial; the presence of congenital heart disease or other primary cardiac diseases, acute infections.
All patients and children of the control group underwent daily ECG monitoring using the software-hardware complex Cardiotechnika-04-AD-1 (Inkart, St. Petersburg, Russia). The dynamic series of cardiac intervals detected during cardiointervalographic study were processed using the mathematical analysis of HRV. The HRV assessment was conducted in time and spectral analysis regimes in accordance with the International Standards of Measurement, Physiological Interpretation and Clinical Use developed by the European Society of Cardiology and North American Society of Pacing and Electrophysiology.
For time analysis of HRV, the following parameters were used: SDNN (ms) — standard (square root) RR deviation, SDNN index (ms) — average 5 minute standard deviation throughout the recording, SDANN (ms) — RMS deviation calculated on the basis of RR intervals, which were averaged over every 5 minutes of the recording, RMSSD (ms) — mean square deviation of inter-interval differences (activity of parasympathetic influences), pNN50 (%) — share of adjacent RR intervals, inter-interval differences between which exceed 50 ms of spectral power (ms2). The decrease in the values of time parameters of heart rate variability was interpreted as an enhancement of sympathetic effects, the increase — as the activation of parasympathetic ones.
Spectral analysis was carried out by means of a fast Fourier transform with the calculation of the total power of the spectrum — TP (ms2) and its three components in the following frequency band: very low frequencies (VLF) (0.003— 0.04 Hz), which characterizes the degree of connection of autonomous segmentary levels of blood circulation regulation with suprasegmentary; the power of the low frequency (LF) spectrum (0.04—0.15 Hz), which mainly reflects the activity of the sympathetic part of the autonomic nervous system; the power of the high frequency (HF) spectrum (0.15—0.4 Hz), which characterizes the influence of the parasympathetic part; as well as the sympatho-parasympa-thetic index of the LF/HF — the index reflecting the balance of the sympathetic and parasympathetic parts.
The results were statistically processed using the Statis-tica 8.0 program. The verification of the distribution according to the Gauss's law was carried out using the Shapiro-Wilk test. Given that most of the samples did not conform to the Gauss's law, the results were presented as median (Me) and interquartile range (Q25; Q75). Due to the age and gender dependence of heart rate variability in children, Z-esti-mates were used in order to compare with the corresponding normative parameters. The Z-estimate was the degree of deviation from the arithmetic mean of the statutory indicator for this age group expressed in terms of the standard deviation of the same series, or by the formula: Z = (X — Xn) / Sx, where X — the value of the obtained indicator in the examined child, Xn — the arithmetic mean of the normative indicator in this age group, S — the standard deviation of the arithmetic mean of the statutory indicator. Mann-Whitney criterion was used to compare the groups. A correlation and one-factor dispersion analysis was performed to determine the relationship between the indicators. The difference between values was considered statistically verisimilar at the level of significance criterion — p < 0.05.
Results
In children with chronic pyelonephritis and CKD stage I—III, when compared with statutory indicators, the unidirectional nature of changes in the time indices (SDNN, RMSSD, pNN50) (Table 1) and spectral analysis (TP, LF, HF, LF/HF) of HRV was recorded (Table 2).
Analysis of the statistical characteristics of Z-estimates of time analysis indicators revealed a probable decrease in SDNN levels in patients in all groups with the most significant decrease in this indicator in children with CKD stage III. A sharp decline in SDNN (greater than 3 S) was observed in 4.26 % of patients with CKD stage I, 13.3 % of patients with CKD stage II and in 35.3 % of patients with CKD stage III. The levels of RMSSD and pNN50, which are indicators of activity of the parasympathetic chain of vegetative regulation, also tended to decrease. However, the probable decrease in comparison with the control group was demonstrated for RMSSD in patients with CKD stage III, and for pNN50 — in patients with CKD stage I and III.
Describing the general tendencies of changes in the parameters of the spectral analysis of HRV, it can be noted that for patients with CKD stages I—Ill as compared with the control group, there is a verisimilar gradual increase in the
total power of HRV spectrum and its domain LF At the same time, with the progression of CKD, a probable decrease in the power of the high-frequency spectrum was recorded. The degree of changes in the power of HRV spectrum had probable group differences both for the low-frequency component (H = 23.22; p = 0.0001) and for high-frequency component (H = 14.45; p = 0.0023).
A significant decrease in the power of the high-frequency component against the background of low-frequency levels has led to a statistically significant increase in the ratio of LF/HF in patients with CKD stages I—Ill, as compared to healthy subjects, without any intergroup differences (H = 1.67; p = 0.8725).
Additionally, Spearman correlation analysis revealed likely correlations between the levels of glomerular filtration rate and HRV indices, namely, GFR and SDNN (r = +0.564; p = 0.023), GFR and pNN50 (r = +0.492; p = 0.037), GFR and TP, LF, HF (r = -0.591, p = 0.030; r = -0.662, p = 0.012; r = +0.627, p = 0.018, respectively).
Discussion
In our study in children with chronic pyelonephritis and CKD stages I-III, reliable shifts in both total HRV and domains were determined, which according to the present data is a complication of CKD, and not the initial state [14].
Probable changes in the SDNN, TP, LF and HF indices in the examined patients during the day reflect the decrease in the total effect of autonomous blood circulation regulation, associated with the increase of sympathetic regulation, which inhibits the activity of the autonomous circuit. The indicated signs of autonomous dysregulation are intensified by the presence of a possible decrease in the parameters characterizing the activity of the parasympathetic chain of vegetative regulation, namely: RMSSD in patients with GFR below 60 ml/min and pNN50 in all groups of patients with CKD. Reduced power of the high frequency component resulted in a statistically significant increase in LF/HF ratio in children with CKD in all groups as compared with healthy subjects without group differences. The increase in this indicator is also a reflection of vegetative imbalance toward hypersympathicotonia. The indicated shifts in the regulation of the autonomous circuit have been confirmed by the studies performed both among the adult contingent [15] and in the pediatric population [12, 16].
The power of the very low-frequency component of HRV spectrum of VLF characterizes the activity of the sympathetic part of the autonomic nervous system [17, 18]. However, in this case we are talking about more complex influences of the supra-segmentary level of regulation, since the amplitude of this domain is closely related to the
Table 1. Z-estimate of time characteristics of heart rate variability in children with chronic pyelonephritis
and chronic kidney disease, Me (Lq; Uq)
Indicators Groups of examined patients P
1st (n = 47) 2nd (n = 30) 3rd (n = 17)
SDNN, ms 24 hours -1.37* (-2.08; -0.68) -1.42* (-2.36; -0.94) -2.68* (-3.24; -1.62) p12 = 0.4121 p1 3 = 0.0232 P2-3 = 0.062
Day -1.43* (-2.15; -0.77) -1.45* (-2.43; -0.97) -2.78* (-3.24; -1.62) p12 = 0.4651 p1 3 = 0.0273 p2-3 = 0.057
Night -1.22 (-1.78; -0.62) -1.39* (-2.29; -0.92) -2.44* (-2.86; -1.43) p12 = 0.5465 p1 3 = 0.0329 p2-3 = 0.075
RMSDD, ms 24 hours -0.97 (-1.54; -0.65) -0.49 (-1.07; -0.48) -1.40* (-1.76; -0.95) p12 = 0.0355 p1 3 = 0.3791 p2-3 = 0.0371
Day -0.69 (-1.27; -0.49) -0.42 (-0.92; -0.37) -1.22* (-1.56; -0.88) p12 = 0.0365 p1 3 = 0.4564 p2-3 = 0.0291
Night -1.09 (-1.69; -0.77) -0.57 (-1.23; -0.55) -1.49* (-1.77; -0.98) p12 = 0.0321 p1 3 = 0.4427 p2-3 = 0.0251
pNN50, % 24 hours -2.80* (-3.66; -1.14) -0.99 (-3.54; 0.11) -3.50* (-3.72; -2.63) p12 = 0.0730 p1 3 = 0.4123 p2-3 = 0.0348
Day -2.78* (-3.56; -1.11) -0.69 (-3.44; 0.56) -3.45* (-3.65; -2.68) p12 = 0.0643 p1 3 = 0.2734 p2-3 = 0.0345
Night -2.84* (-3.73; -1.17) -1.63* (-3.62; -0.41) -3.54* (-3.76; -2.59) p12 = 0.0881 p1 3 = 0.4536 p2 3 = 0.0443
Note: * — statistically significant difference with the indicators of the control group.
psycho-emotional stress and functional state of the cerebral cortex, and the power of VLF fluctuations is a sensitive indicator of metabolic process control. That is, VLF reflects the effect of higher autonomic centers on the cardiovascular subcortical center, the state of neurohumoral and metabolic regulation levels and can be used as a marker for the relationship between the segmentary levels of blood flow regulation with supra-segmentary ones [19—21]. The increase in
the level of VLF, which indicates high power compensatory mechanisms and can lead to disruption of the adaptive reserves of the organism was recorded in 21.3 % of patients with CKD stage I, in 20.0 % of children with CKD stage II and in 11.8 % of patients with CKD stage III. Reduction in the power of the VLF spectrum, which confirms the depletion of the energy reserves of the body, was recorded at night and was typical for 61.7 % of patients with CKD stage I,
Table 2. Z-estimate of spectral characteristics of heart rate variability in children with chronic pyelonephritis
and chronic kidney disease, Me (Lq; Uq)
Indicators Groups of examined patients P
1st (n = 47) 2nd (n = 30) 3rd (n = 17)
TP, ms2 24 hours 0.89 (-0.67; 1.47) 1.45 (0.22; 1.65) 3.46* (1.53; 5.07) p1 2 = 0.3426 p1 3 = 0.0478 p2-3 = 0.0345
Day 0.92 (-0.19; 1.65) 1.42 (-0.14; 2.09) 4.87* (2.72; 6.03) p12 = 0.5126 p1 3 = 0.0212 p2-3 = 0.0127
Night -0.11 (-0.31; 1.45) 1.22 (-0.25; 2.31) 7.56* (2.25; 11.29) p12 = 0.3159 p1 3 = 0.0006 p2-3 = 0.0031
VLF, ms2 24 hours 3.34* (2.37; 3.72) 2.77* (0.47; 4.27) 4.14* (2.61; 4.99) p12 = 0.0886 p1 3 = 0.0743 p2-3 = 0.0498
Day 3.98* (2.59; 4.56) 2.93* (0.88; 3.87) 4.54* (2.55; 4.86) p12 = 0.0182 p1 3 = 0.0053 p2-3 = 0.0533
Night 0.59 (0.26; 1.27) 2.61* (0.30; 3.54) 3.89* (2.02; 4.56) p12 = 0.0617 p1 3 = 0.5927 p2-3 = 0.0087
LF, ms2 24 hours 2.55* (1.79; 2.79) 1.91* (1.33; 3.51) 5.11* (3.67; 7.94) p1 2 = 0.0794 p1 3 = 0.0019 p2-3 = 0.0000
Day 1.88* (1.76; 2.41) 1.69* (1.43; 2.47) 6.46* (3.32; 7.29) p12 = 0.3311 p1 3 = 0.0012 p2-3 = 0.0000
Night 1.46 (-0.65; 1.59) 2.86* (1.77; 3.35) 4.21* (3.23; 6.17) p12 = 0.0145 p1 3 = 0.0009 p2-3 = 0.0002
HF, ms2 24 hours -0.60 (-1.21; -0.46) -3.20* (-9.61; 0.68) -12.72* (-14.41; -9.05) p1 2 = 0.0365 p1 3 = 0.0241 p2-3 = 0.0025
Day -9.64* (-10.98; -6.12) -6.36* (-9.46; 0.47) -12.69* (-13.79; -9.12) p12 = 0.0312 p1 3 = 0.0160 p2-3 = 0.0015
Night 1.23 (-1.21; 1.25) -6.12* (-9.61; 0.55) -12.81* (-14.56; -9.18) p12 = 0.0312 p1 3 = 0.0160 p2-3 = 0.0015
LF/HF 24 hours 1.34 (-0.7; 3.53) 1.80* (-0.47; 5.12) 2.62* (0.7; 10.10) p1 2 = 0.3625 p1 3 = 0.0042 p2-3 = 0.0635
Day 3.37* (2.01; 5.47) 1.86* (-0.45; 4.92) 2.66* (0.88; 10.16) p12 = 0.4133 p1 3 = 0.8332 p2-3 = 0.2345
Night 1.21 (0.85; 2.76) 1.69* (-0.50; 5.23) 2.60* (0.66; 9.97) p12 = 0.3112 p1 3 = 0.0720 p2 3 = 0.3052
Note: * — statistically significant difference with the indicators of the control group.
70.0 % of patients with CKD stage II, and 76.5 % of children with CKD stage III.
The results of our study suggest that in children with chronic pyelonephritis changes in total HRV occur gradually during CKD progression, rather in the decrease of renal function, which is confirmed by the presence of probable correlations between GFR and the main indicators of HRV. This assumption is also evidenced in studies conducted among adult patients with CKD of IV—V stages [15, 22], and in a cohort of pediatric patients [12, 16]. At the same time, it was found that by the levels of most indicators of both time and spectral analysis of HRV, there is no probable difference between patients with CKD stage I and II. This is likely to be due to the fact that the overwhelming majority of patients with GFR below 90 ml/min received angiotensin converting enzyme inhibitors as a component of renonoprotective therapy for a long time, which, according to modern ideas, contribute to the normalization of total HRV [23—25].
Conclusions
1. In 76.6 % of children with chronic pyelonephritis and CKD of I—III stages, vegetative imbalance is detected, which manifests in HRV (growth of TP, LF, LF/HF and reduced SDNN, RMSSD, pNN50, HF). These changes reflect the shift of vago-sympathetic balance toward weakening of the parasympathetic and domination of the tone of the sympathetic part of the nervous system.
2. Gradual loss of renal functions, which occurs during CKD progression, exacerbates autonomic imbalance, which is confirmed by the presence of probable correlations between the integral index of renal function (GFR) and findings of time (SDNN, pNN50) and spectral (TP, LF, HF) analysis of HRV.
3. The autonomic imbalance with the weakening of the parasympathetic and domination of the sympathetic tone of the nervous system obviously leads to the weakening of the overall adaptive capacities of the organism and demonstrates expected development of cardiovascular disorders even before the appearance of significant changes of central hemodynamics.
Conflicts of interests. Author declares the absence of any conflicts of interests that might be construed to influence the results or interpretation of their manuscript.
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Received 18.04.2019, Accepted for printing 22.04.2019 ■
Вакуленко Л.1.
ДЗ «Д^пропетровська медична академiя МОЗ Укра'ни», м. AHinpo, Укра'на
Варiабельнiсть серцевого ритму в дтей i3 хрошчним
Резюме. Актуальшсть. Ощнка варiабельностi серцевого ритму дае можливють отримати уявлення щодо функцюналь-ного стану вегетативно! нервово! системи та щентифшувати змши вегетативного гомеостазу в дитей. Мета роботи: ви-вчити особливосп вегетативно! регуляци в дией i3 хрошчним телонефритом на початкових стад1ях хротчно! хвороби ни-рок (ХХН) шляхом анатзу варiабельностi серцевого ритму. Матерiали та методи. Обстежено 94 дитини вшом вщ 6 до 17 роив поза загостренням хротчного телонефриту з ХХН I—III стади. Проводилось добове мониторування електрокар-дюграми з подальшою математичною обробкою. Результата. Аналiз статистичних характеристик Z-оцшок показниюв часового аналiзу виявив вiроriдне зниження значень стандартного (середньоквадратичного) вщхилення штервалу RR у хворих усгх груп iз суттевим зменшенням цього показника в дией iз ХХН III стади. Вiрогiдне зменшення показника ак-тивносп парасимпатичних впливiв RMSSD продемонстру-
шелонефритом i хронiчною хворобою нирок 1-111 стади
вали хворi з ХХН III стади, а показника pNN50 — пащенти з I та III стадiею ХХН. При спектральному аналiзi у хворих виявлено вiрогiIдне збшьшення загально! потужностi спектра варiабельностi серцевого ритму (ТР) i його доменгв (VLF, LF), симпато-парасимпатичного сшввщношення LF/HF та зниження потужностi високочастотного спектра (HF). Ви-сновки. У 76,6 % дитей iз хрошчним телонефритом та ХХН ИП стади вщзначаеться порушення вегетативного балансу. Ь прогресуванням ХХН вегетативний дисбаланс поглиблю-еться, що пщтверджуеться наявнiстю вiрогiдних кореляцiй м1ж швидкiстю клубочково! фшьтраци та показниками часового (SDNN, pNN50) i спектрального (ТР, LF, HF) аналiзу варiабельностi серцевого ритму. Виявлеш змши свщчать про очшуване формування кардiоваскулярних порушень ще до появи значущих змiн центрально! гемодинамжи. Ключовi слова: варiабельнiсть серцевого ритму; дии; хро-нiчний пiелонефрит; хротчна хвороба нирок
Вакуленко Л.И.
ГУ «Днепропетровская медицинская академия МЗ Украины», г. Днепр, Украина
Вариабельность сердечного ритма у детей с хроническим пиелонефритом и хронической болезнью почек 1-111 стадии
Резюме. Актуальность. Оценка вариабельности сердечного ритма дает возможность получить представление о функциональном состоянии вегетативной нервной системы и идентифицировать изменения вегетативного гомеостаза у детей. Цель работы: изучить особенности вегетативной регуляции у детей с хроническим пиелонефритом на начальных стадиях хронической болезни почек (ХБП) путем анализа вариабельности сердечного ритма. Материалы и методы. Обследовано 94 ребенка в возрасте от 6 до 17 лет вне обострения хронического пиелонефрита с ХБП I—III стадии. Проводилось суточное мониторирование электрокардиограммы с последующей математической обработкой. Результаты. Анализ статистических характеристик Z-оценок показателей временного анализа выявил достоверное снижение значений стандартного (среднеквадратического) отклонения интервала RR у больных всех групп с существенным уменьшением этого показателя у детей с ХБП III стадии. Достоверное уменьшение показателя RMSSD продемонстрировали больные с ХБП III
стадии, а показателя pNN50 — пациенты с I и III стадией ХБП. При спектральном анализе у больных выявлено достоверное увеличение общей мощности спектра вариабельности сердечного ритма (ТР) и его доменов (VLF, LF), симпато-па-расимпатического соотношения LF/HF и снижение мощности высокочастотного спектра (HF). Выводы. У 76,6 % детей с хроническим пиелонефритом и ХБП НИ стадии отмечается нарушение вегетативного баланса. С прогрессированием ХБП вегетативный дисбаланс усугубляется, что подтверждается наличием корреляций между скоростью клубочковой фильтрации и показателями временного (SDNN, pNN50) и спектрального (ТР, LF, HF) анализа вариабельности сердечного ритма. Выявленные изменения свидетельствуют об ожидаемом формировании кардиоваскулярных нарушений еще до появления значимых изменений центральной гемодинамики.
Ключевые слова: вариабельность сердечного ритма; дети; хронический пиелонефрит; хроническая болезнь почек
