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Characterisation of Breathing and Associated Central Autonomic Arch Dis Child 2001;85:29–37 29 Characterisation of breathing and associated Arch Dis Child: first published as 10.1136/adc.85.1.29 on 1 July 2001. Downloaded from central autonomic dysfunction in the Rett disorder P O O Julu, A M Kerr, F Apartopoulos, S Al-Rawas, I Witt Engerström, L Engerström, G A Jamal, S Hansen Abstract is associated with non-epileptic vacant spells.11 Aim—To investigate breathing rhythm Low resting cardiac vagal tone and weak vagal and brain stem autonomic control in response to hyperventilation and breath hold- patients with Rett disorder. ing suggest inadequate parasympathetic con- Setting—Two university teaching hospi- trol.12 tals in the United Kingdom and the Rett Our aim in this study was to characterise the Centre, Sweden. abnormalities of respiratory rhythm and inves- Patients—56 female patients with Rett tigate the central autonomic competence in disorder, aged 2–35 years; 11 controls aged Rett disorder. 5–28 years. Design—One hour recordings of breath- ing movement, blood pressure, ECG R-R Methods interval, heart rate, transcutaneous blood SUBJECTS Fifty six subjects were referred for diagnostic gases, cardiac vagal tone, and cardiac assessment. Control values came from 11 sensitivity to baroreflex measured on-line female volunteers and from previous with synchronous EEG and video. Breath- studies.12–14 Parents received written explana- ing rhythms were analysed in 47 cases. tions of procedures and results and provided Results—Respiratory rhythm was normal consent. The ethics committee at South during sleep and abnormal in the waking Glasgow University Hospitals NHS Trust state. Forced and apneustic breathing Peripheral Nerve and approved the study. Rett subjects had all the were prominent among 5–10 year olds, Autonomic Unit, classic criteria,15 except as follows: no decline in Department of and Valsalva breathing in the over 18 year occipitofrontal circumference (n = 6); stagna- Neurology, Imperial olds, who were also most likely to breathe College of Science, tion in development without regression normally. Inadequate breathing peaked (n = 4); and seizures before regression (n = 4). Technology and among 10–18 year olds. Inadequate and Medicine, Central http://adc.bmj.com/ Middlesex Hospital, exaggerated breathing was associated with vacant spells. Resting cardiac vagal tone PROCEDURES AND ANALYSES Acton Lane, London The subjects sat comfortably with carers while NW10 7NS, UK and cardiac sensitivity to baroreflex were P O O Julu reduced. information was obtained by clinical examina- S Al-Rawas Conclusions—Labile respiratory rhythms tion and from case records, health question- G A Jamal and poor integrative inhibition in Rett naires, and one hour continuous, synchronous, disorder suggest brain immaturity. Link- non-invasive autonomic and respiratory moni- Department of toring, time locked with video and EEG. ing this to an early monoaminergic defect on September 26, 2021 by guest. Protected copyright. Psychological A stretch sensitive resistance plethysmo- Medicine, University suggests possible targets for the MECP2 graph at xiphisternal level recorded the ampli- of Glasgow, Gartnavel gene in clinical intervention. Exaggerated tude of thoracic and abdominal breathing Royal Hospital, and inadequate autonomic responses may movements in arbitrary units. A TCM3 moni- Glasgow, UK contribute to sudden death. A M Kerr tor (Radiometer, Copenhagen, Denmark) re- (Arch Dis Child 2001;85:29–37) corded partial pressures of oxygen (PO ) and Departments of 2 carbon dioxide (PCO ) transcutaneously. A fin- Neurophysiology and Keywords: Rett disorder; autonomic system; brain 2 Clinical Physics, stem; dysautonomia ger photoplethysmograph (Finapres™, Ohm- Institute of eda, USA) recorded digital arterial blood pres- Neurological Sciences, sure in waveforms for calculation of beat by South Glasgow Rett disorder, causing profound intellectual beat systolic, mean, and diastolic blood pres- University Hospitals and physical disability, is caused by MECP2 sure. The central autonomic (brain stem) con- NHS Trust, Glasgow, mutations.12Of 56 classic British cases tested, trol of cardioinhibitory activity was monitored UK 47 (87%) are mutation positive. There is a wide by the NeuroScope™ (MediFit Diagnostics, F Apartopoulos 34 S Hansen range of clinical severity. The prevalence of London, UK), which calculates cardiac vagal the disorder in the United Kingdom exceeds tone from ECG R-R intervals.16 The cardiac Rett Centre, Frösö 1 in 10 000 of the female population.5 vagal tone is expressed in arbitrary units on a Strand, Östersund Autonomic manifestations include agitation, linear vagal scale.17 Hospital, Sweden flushing, pupillary dilatation, and cold extremi- Breathing movements, levels of blood gases, I Witt Engerström 6 L Engerström ties relieved by sympathectomy. Disrupted and blood pressure waveforms were transmit- sleep staging suggests an early monoamine ted through an interface—the MedullaLab Correspondence to: defect.7 Immaturity is suggested by an infantile (MediFit Diagnostics)—and joined the Neuro- Dr Julu distribution of the forebrain circulation89 and Scope data in a common microcomputer. The email: [email protected] raised serotonin receptor binding in brain stem VaguSoft software (MediFit Diagnostics) si- Accepted 15 January 2001 nuclei.10 Irregular breathing in the waking state multaneously recorded ECG, heart rate, car- www.archdischild.com 30 Julu, Kerr, Apartopoulos, et al Ramp inspiration Expiration Breath hold 3500 Arch Dis Child: first published as 10.1136/adc.85.1.29 on 1 July 2001. Downloaded from early late Amplitude Amplitude 0 3500 Regular breath holds 1 s Figure 1 Normal breathing. Ramp inspiration terminated immediately by double phased expiration. Rate below 35 breaths/min, depth average for the individual. Amplitude measured in arbitrary units. Amplitude diac vagal tone, systolic, mean, and diastolic blood pressure, blood gases, and cardiac sensi- 0 Protracted inspiration tivity to the spontaneous arterial baroreflex. 3500 The EEG was recorded on a 16 channel PL-EEG in the United Kingdom (Walter Graphtek UK, West Sussex, UK) and on an eight channel paper machine (Nihon Ohden, Tokyo Japan) in Sweden. Breath by breath analyses of 47 cases excluded all interruptions. Baseline functions are defined as autonomic Amplitude activity during normal breathing with normal levels of blood gases. Control subjects volun- tarily hyperventilated and held their breath in 0 accordance with our demonstrations. 5 s Figure 2 Apneustic breathing style. Top:breath hold—a single fast full inspiration followed by a delayed fast STATISTICS expiration. Middle: regular breath holds—episodes of breath Values are given as mean (SEM). Statistical holding. Bottom: protracted inspiration—a prolonged and diVerences were assessed using analysis of vari- continuous inspiration ended abruptly by full expiration http://adc.bmj.com/ (achieved fast, often forcefully), insuYcient to obstruct ance (ANOVA) with a two sided Student t test venous return. Amplitude measured in arbitrary units. for probability (p) values, using Minitab for Windows 11.21. VENTILATORY EFFICIENCY IN RETT DISORDER Blood gases were recorded transcutaneously in Results 27 subjects. Carbon dioxide fell during intense BREATHING RHYTHMS hyperventilation and rose during inadequate As previously observed,12–14 no control subject breathing as oxygen levels fell. Mean lowest on September 26, 2021 by guest. Protected copyright. showed spontaneous breathing dysrhythmias. and highest PCO2 values were 4.12 and 5.43 All Rett subjects had some normal rhythm kPa (31 and 41 mm Hg), respectively; in two of while awake but also showed 5–11 (mean 8) 27 feeble breathers (7%) PCO2 exceeded 7.98 types of abnormal rhythm (figs 1 to 6). Valsalva kPa (60 mm Hg). Repeated central apnoea or breathing occurred in 26 of the 47 subjects Valsalva breathing was always associated with a tested (59%), Biot’s breathing in two, and PO2 below 10.64 kPa (80 mm Hg). Valsalva Cheyne-Stokes respiration in 12 subjects with breathers did not have raised PCO2, while inadequate breathing. oxygen fell below 6.65 kPa (50 mm Hg) in 14 Breathing patterns changed with age (fig 7 of 27 Rett subjects (52%). and table 1). Most forceful and apneustic breathers were under 5 years old and most BASELINE AUTONOMIC FUNCTION normal and Valsalva type breathers were older. Baseline brain stem autonomic function was Combined percentages of breathing dysrhyth- analysed in 48 girls aged 2 to 35 years, mean mias in the 0–9 year age groups (table 1) were 13.2 years, and in 11 controls aged 5 to 28, higher than in the older age groups mean 10.2 (fig 8). There was no significant dif- (p < 0.005). The percentage of Valsalva ference in mean resting heart rate (mean breathing in the over 19 year age group was (SEM): Rett 101 (3.6) beats/min; control 92 higher than in the youngest group (p < 0.01) (2.5) beats/min) or mean arterial blood pres- or in the 6–9 year old group (p < 0.05). sure (Rett 79 (5.3) mm Hg; control 86 (7.1) Inadequate breathing was most common under mm Hg). Mean cardiac sensitivity to baroreflex 18 years of age, where Cheyne-Stokes breath- was lower in Rett cases than in controls (Rett ing was also seen. Repeat examination of six 3.4 (0.4) ms/mm Hg; control 6.2 (0.9) ms/mm Rett subjects studied in 198713 indicated the Hg; p < 0.01). Mean cardiac vagal tone was same pattern of change with age. also low in Rett cases: Rett 4.5 (0.4) units; www.archdischild.com Breathing dysfunction in Rett disorder 31 3500 Deep breathing Arch Dis Child: first published as 10.1136/adc.85.1.29 on 1 July 2001. Downloaded from 3500 Rapid shallow Amplitude Amplitude 0 3500 0 3500 Shallow Tachypnoea Amplitude Amplitude 0 Hyperventilation 0 3500 3500 Central apnoea Amplitude Amplitude 0 10 s 0 5 s Figure 3 Forceful breathing style. Top:deep breathing—episode of exaggerated inspirations followed Figure 4 Inadequate breathing style. Top:rapid shallow immediately by exaggerated expirations without causing breathing—episode of shallow inspiration followed central apnoea; rate below 35 breaths/min, depth must be immediately by equally shallow expiration; rate above 35 well above average for that person.
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