Skip to main content
Top
Published in: European Child & Adolescent Psychiatry 10/2017

Open Access 01-10-2017 | Original Contribution

The respiratory control of carbon dioxide in children and adolescents referred for treatment of psychogenic non-epileptic seizures

Authors: Kasia Kozlowska, Reena Rampersad, Catherine Cruz, Ubaid Shah, Catherine Chudleigh, Samantha Soe, Deepak Gill, Stephen Scher, Pascal Carrive

Published in: European Child & Adolescent Psychiatry | Issue 10/2017

Login to get access

Abstract

Psychogenic non-epileptic seizures (PNES) are a common problem in paediatric neurology and psychiatry that can best be understood as atypical responses to threat. Threats activate the body for action by mediating increases in arousal, respiration, and motor readiness. In previous studies, a range of cardiac, endocrine, brain-based, attention-bias, and behavioral measures have been used to demonstrate increases in arousal, vigilance, and motor readiness in patients with PNES. The current study uses respiratory measures to assess both the motor readiness of the respiratory system and the respiratory regulation of CO2. Baseline respiratory rates during clinical assessment and arterial CO2 levels during the hyperventilation component of routine video electroencephalogram were documented in 60 children and adolescents referred for treatment of PNES and in 50 controls. Patients showed elevated baseline respiratory rates [t(78) = 3.34, p = .001], with 36/52 (69%) of patients [vs. 11/28 (39%) controls] falling above the 75th percentile (χ 2 = 6.7343; df = 1; p = .009). Twenty-eight (47%) of patients [vs. 4/50 (8%) controls] showed a skewed hyperventilation-challenge profile—baseline PCO2 <36 mmHg, a trough PCO2 ≤ 20 mmHg, or a final PCO2 <36 mmHg after 15 min of recovery—signaling difficulties with CO2 regulation (χ 2 = 19.77; df = 1; p < .001). Children and adolescents with PNES present in a state of readiness-for-action characterized by high arousal coupled with activation of the respiratory motor system, increases in ventilation, and a hyperventilation-challenge profile shifted downward from homeostatic range. Breathing interventions that target arousal, decrease respiratory rate, and normalize ventilation and arterial CO2 may help patients shift brain–body state and avert PNES episodes.
Appendix
Available only for authorised users
Footnotes
1
In the earlier studies by Kozlowska et al., children/adolescents with PNES made up 51% (n = 29/57) of the samples [1012]. In the most recent study of cortical arousal, children/adolescents with PNES made up 56% (n = 32/57) of the sample [13].
 
Literature
1.
go back to reference AmericanPsychiatric A (2000) Diagnostic and statistical manual of mental disorders: DSM-IV-TR, 4th edn. American Psychiatric Association, Washington, DC AmericanPsychiatric A (2000) Diagnostic and statistical manual of mental disorders: DSM-IV-TR, 4th edn. American Psychiatric Association, Washington, DC
2.
go back to reference AmericanPsychiatric A (2013) Diagnostic and statistical manual of mental disorders: DSM-V, 4th edn. American Psychiatric Association, Washington, DCCrossRef AmericanPsychiatric A (2013) Diagnostic and statistical manual of mental disorders: DSM-V, 4th edn. American Psychiatric Association, Washington, DCCrossRef
5.
go back to reference Perez DL, Dworetzky BA, Dickerson BC, Leung L, Cohn R, Baslet G, Silbersweig DA (2015) An integrative neurocircuit perspective on psychogenic nonepileptic seizures and functional movement disorders: neural functional unawareness. Clin EEG Neurosci 46(1):4–15. doi:10.1177/1550059414555905 PubMedCrossRef Perez DL, Dworetzky BA, Dickerson BC, Leung L, Cohn R, Baslet G, Silbersweig DA (2015) An integrative neurocircuit perspective on psychogenic nonepileptic seizures and functional movement disorders: neural functional unawareness. Clin EEG Neurosci 46(1):4–15. doi:10.​1177/​1550059414555905​ PubMedCrossRef
12.
go back to reference Kozlowska K, Palmer DM, Brown KJ, Scher S, Chudleigh C, Davies F, Williams LM (2015) Conversion disorder in children and adolescents: a disorder of cognitive control. J Neuropsychol 9(1):87–108. doi:10.1111/jnp.12037 PubMedCrossRef Kozlowska K, Palmer DM, Brown KJ, Scher S, Chudleigh C, Davies F, Williams LM (2015) Conversion disorder in children and adolescents: a disorder of cognitive control. J Neuropsychol 9(1):87–108. doi:10.​1111/​jnp.​12037 PubMedCrossRef
18.
go back to reference Barzegaran E, Carmeli C, Rossetti AO, Frackowiak RS, Knyazeva MG (2016) Weakened functional connectivity in patients with psychogenic non-epileptic seizures (PNES) converges on basal ganglia. J Neurol Neurosurg Psychiatry 87(3):332–337. doi:10.1136/jnnp-2014-309483 PubMedCrossRef Barzegaran E, Carmeli C, Rossetti AO, Frackowiak RS, Knyazeva MG (2016) Weakened functional connectivity in patients with psychogenic non-epileptic seizures (PNES) converges on basal ganglia. J Neurol Neurosurg Psychiatry 87(3):332–337. doi:10.​1136/​jnnp-2014-309483 PubMedCrossRef
22.
go back to reference Carbon M, Wübbeler G, Trahms L, Curio G (2000) Hyperventilation-induced human cerebral magnetic fields noninvasively monitored by multichannel ‘direct current’ magnetoencephalography. Neurosci Lett 287:227–230PubMedCrossRef Carbon M, Wübbeler G, Trahms L, Curio G (2000) Hyperventilation-induced human cerebral magnetic fields noninvasively monitored by multichannel ‘direct current’ magnetoencephalography. Neurosci Lett 287:227–230PubMedCrossRef
23.
go back to reference Engel GL, Ferris EB, Logan M (1947) Hyperventilation: analysis of clinical symptomatology. Ann Intern Med 27:683–704PubMedCrossRef Engel GL, Ferris EB, Logan M (1947) Hyperventilation: analysis of clinical symptomatology. Ann Intern Med 27:683–704PubMedCrossRef
24.
go back to reference Hauge A, Thoresen M, Walloe L (1980) Changes in cerebral blood flow during hyperventilation and CO2 − breathing measured transcutaneously in humans by a bidirectional, pulsed, ultrasound Doppler blood velocitymeter. Acta Physiol Scand 110(2):167–173PubMedCrossRef Hauge A, Thoresen M, Walloe L (1980) Changes in cerebral blood flow during hyperventilation and CO2 breathing measured transcutaneously in humans by a bidirectional, pulsed, ultrasound Doppler blood velocitymeter. Acta Physiol Scand 110(2):167–173PubMedCrossRef
25.
go back to reference Yamatani M, Konishi T, Murakami M, Okuda T (1994) Hyperventilation activation on EEG recording in childhood. Epilepsia 35(6):1199–1203PubMedCrossRef Yamatani M, Konishi T, Murakami M, Okuda T (1994) Hyperventilation activation on EEG recording in childhood. Epilepsia 35(6):1199–1203PubMedCrossRef
26.
go back to reference Lum LC (1976) The syndrome of habitual chronic hyperventilation. In: Hill O (ed) Modern trends in psychosomatic medicine, vol 3. Butterworth, London, pp 196–230 Lum LC (1976) The syndrome of habitual chronic hyperventilation. In: Hill O (ed) Modern trends in psychosomatic medicine, vol 3. Butterworth, London, pp 196–230
27.
go back to reference Evans DW, Lum MB (1981) Hyperventilation as a cause of chest pain mimicking angina. Pract Cardiol 7(7):131–139 Evans DW, Lum MB (1981) Hyperventilation as a cause of chest pain mimicking angina. Pract Cardiol 7(7):131–139
28.
go back to reference Gibbs DM (1992) Hyperventilation-induced cerebral ischemia in panic disorder and effect of nimodipine. Am J Psychiatry 149(11):1589–1591PubMedCrossRef Gibbs DM (1992) Hyperventilation-induced cerebral ischemia in panic disorder and effect of nimodipine. Am J Psychiatry 149(11):1589–1591PubMedCrossRef
29.
go back to reference Ball S, Shekhar A (1997) Basilar artery response to hyperventilation in panic disorder. Am J Psychiatry 154(11):1603–1604PubMedCrossRef Ball S, Shekhar A (1997) Basilar artery response to hyperventilation in panic disorder. Am J Psychiatry 154(11):1603–1604PubMedCrossRef
30.
go back to reference Yamaguchi F, Meyer JS, Sakai F, Yamamoto M (1979) Normal human aging and cerebral vasoconstrictive responses to hypocapnia. J Neurol Sci 44(1):87–94PubMedCrossRef Yamaguchi F, Meyer JS, Sakai F, Yamamoto M (1979) Normal human aging and cerebral vasoconstrictive responses to hypocapnia. J Neurol Sci 44(1):87–94PubMedCrossRef
31.
32.
go back to reference Lafleur J, Reiher J (1977) Pseudoabsences. Electroencephalogr Clin 43:279–280 Lafleur J, Reiher J (1977) Pseudoabsences. Electroencephalogr Clin 43:279–280
33.
go back to reference Reiher J, Lafleur J (1977) Hyperventilation induced cyclic absences. Electroencephalogr Clin 42:717 Reiher J, Lafleur J (1977) Hyperventilation induced cyclic absences. Electroencephalogr Clin 42:717
34.
35.
go back to reference North KN, Ouvrier RA, Nugent M (1990) Pseudoseizures caused by hyperventilation resembling absence epilepsy. J Child Neurol 5(4):288–294PubMedCrossRef North KN, Ouvrier RA, Nugent M (1990) Pseudoseizures caused by hyperventilation resembling absence epilepsy. J Child Neurol 5(4):288–294PubMedCrossRef
36.
go back to reference Bruno-Golden B, Holmes GL (1993) Hyperventilation-induced seizures in mentally impaired children. Seizure J Br Epilepsy Assoc 2(3):229–233CrossRef Bruno-Golden B, Holmes GL (1993) Hyperventilation-induced seizures in mentally impaired children. Seizure J Br Epilepsy Assoc 2(3):229–233CrossRef
37.
go back to reference Chandra R, Srinivasan S, Chandrasekaran R, Mahadevan S (1993) The prevalence of mental disorders in school-age children attending a general paediatric department in southern India. Acta Psychiatr Scand 87(3):192–196PubMedCrossRef Chandra R, Srinivasan S, Chandrasekaran R, Mahadevan S (1993) The prevalence of mental disorders in school-age children attending a general paediatric department in southern India. Acta Psychiatr Scand 87(3):192–196PubMedCrossRef
38.
go back to reference Naschitz JE, Gaitini L, Mazov I, Eridzhanyan L, Keren D, Sabo E, Yeshurun D, Hardoff D, Jaffe M (1997) The capnography-tilt test for the diagnosis of hyperventilation syncope. QJM Mon J Assoc Physicians 90(2):139–145CrossRef Naschitz JE, Gaitini L, Mazov I, Eridzhanyan L, Keren D, Sabo E, Yeshurun D, Hardoff D, Jaffe M (1997) The capnography-tilt test for the diagnosis of hyperventilation syncope. QJM Mon J Assoc Physicians 90(2):139–145CrossRef
39.
go back to reference Naschitz JE, Hardoff D, Bystritzki I, Yeshurun D, Gaitini L, Tamir A, Jaffe M (1998) The role of the capnography head-up tilt test in the diagnosis of syncope in children and adolescents. Pediatrics 101(2):E6PubMedCrossRef Naschitz JE, Hardoff D, Bystritzki I, Yeshurun D, Gaitini L, Tamir A, Jaffe M (1998) The role of the capnography head-up tilt test in the diagnosis of syncope in children and adolescents. Pediatrics 101(2):E6PubMedCrossRef
40.
go back to reference Krishnakumar P, Sumesh P, Mathews L (2006) Temperamental traits associated with conversion disorder. Indian Pediatr 43(10):895–899PubMed Krishnakumar P, Sumesh P, Mathews L (2006) Temperamental traits associated with conversion disorder. Indian Pediatr 43(10):895–899PubMed
44.
go back to reference Kozlowska K, Chudleigh C, Elliott B, Landini A (2016) The body Comes to family therapy: Treatment of a school-aged boy with hyperventilation-induced non-epileptic seizures. Clin Child Psychol Psychiatry 21(4):669–685. doi:10.1177/1359104515621960 PubMedCrossRef Kozlowska K, Chudleigh C, Elliott B, Landini A (2016) The body Comes to family therapy: Treatment of a school-aged boy with hyperventilation-induced non-epileptic seizures. Clin Child Psychol Psychiatry 21(4):669–685. doi:10.​1177/​1359104515621960​ PubMedCrossRef
45.
go back to reference Chandra P, Kozlowska K, Cruz C, Baslet GC, Perez DL, Garralda ME (2017) Hyperventilation-induced non-epileptic seizures in an adolescent boy with pediatric medical traumatic stress. Harv Rev Psychiatry 25(4). doi:10.1097/HRP.0000000000000131 (in press) Chandra P, Kozlowska K, Cruz C, Baslet GC, Perez DL, Garralda ME (2017) Hyperventilation-induced non-epileptic seizures in an adolescent boy with pediatric medical traumatic stress. Harv Rev Psychiatry 25(4). doi:10.​1097/​HRP.​0000000000000131​ (in press)
47.
go back to reference Vein AM, Djukova GM, Vorobieva OV (1994) Is panic attack a mask of psychogenic seizures?–a comparative analysis of phenomenology of psychogenic seizures and panic attacks. Funct Neurol 9(3):153–159PubMed Vein AM, Djukova GM, Vorobieva OV (1994) Is panic attack a mask of psychogenic seizures?–a comparative analysis of phenomenology of psychogenic seizures and panic attacks. Funct Neurol 9(3):153–159PubMed
48.
49.
go back to reference Kozlowska K, English M, Savage B (2013) Connecting body and mind: the first interview with somatizing patients and their families. Clin Child Psychol Psychiatry 18(2):223–245CrossRef Kozlowska K, English M, Savage B (2013) Connecting body and mind: the first interview with somatizing patients and their families. Clin Child Psychol Psychiatry 18(2):223–245CrossRef
50.
go back to reference Fried R, Grimaldi J (1993) The psychology and physiology of breathing. Plnum Press, New YorkCrossRef Fried R, Grimaldi J (1993) The psychology and physiology of breathing. Plnum Press, New YorkCrossRef
51.
go back to reference Midgren B, Hansson L (1987) Changes in transcutaneous PCO2 with sleep in normal subjects and in patients with chronic respiratory diseases. Eur J Respir Dis 71(5):388–394PubMed Midgren B, Hansson L (1987) Changes in transcutaneous PCO2 with sleep in normal subjects and in patients with chronic respiratory diseases. Eur J Respir Dis 71(5):388–394PubMed
52.
go back to reference Rafferty GF, Saisch SG, Gardner WN (1992) Relation of hypocapnic symptoms to rate of fall of end-tidal PCO2 in normal subjects. Respir Med 86(4):335–340PubMedCrossRef Rafferty GF, Saisch SG, Gardner WN (1992) Relation of hypocapnic symptoms to rate of fall of end-tidal PCO2 in normal subjects. Respir Med 86(4):335–340PubMedCrossRef
53.
go back to reference Fleming S, Thompson M, Stevens R, Heneghan C, Plüddemann A, Maconochie I, Tarassenko L, Mant D (2011) Normal ranges of heart rate and respiratory rate in children from birth to 18 years of age: a systematic review of observational studies. Lancet 19(377):1011–1018. doi:10.1016/S0140-6736(10)62226-X CrossRef Fleming S, Thompson M, Stevens R, Heneghan C, Plüddemann A, Maconochie I, Tarassenko L, Mant D (2011) Normal ranges of heart rate and respiratory rate in children from birth to 18 years of age: a systematic review of observational studies. Lancet 19(377):1011–1018. doi:10.​1016/​S0140-6736(10)62226-X CrossRef
55.
go back to reference Chaitow L, Bradley D, Gilbert C (2002) Multidisciplinary approaches to breathing pattern disorders. Churchill Livingstone, London Chaitow L, Bradley D, Gilbert C (2002) Multidisciplinary approaches to breathing pattern disorders. Churchill Livingstone, London
59.
60.
go back to reference Hermans EJ, van Marle HJ, Ossewaarde L, Henckens MJ, Qin S, van Kesteren MT, Schoots VC, Cousijn H, Rijpkema M, Oostenveld R, Fernandez G (2011) Stress-related noradrenergic activity prompts large-scale neural network reconfiguration. Science 334(6059):1151–1153. doi:10.1126/science.1209603 PubMedCrossRef Hermans EJ, van Marle HJ, Ossewaarde L, Henckens MJ, Qin S, van Kesteren MT, Schoots VC, Cousijn H, Rijpkema M, Oostenveld R, Fernandez G (2011) Stress-related noradrenergic activity prompts large-scale neural network reconfiguration. Science 334(6059):1151–1153. doi:10.​1126/​science.​1209603 PubMedCrossRef
63.
go back to reference Gastaut H (1974) Syncopes: generalised anoxic cerebral seizures. In: Magnus O, Lorentz de Hoos AM (eds) The Epilepsies. Handbook of clinical neurology, vol 15. New Holland, Amsterdam, pp 815–835 Gastaut H (1974) Syncopes: generalised anoxic cerebral seizures. In: Magnus O, Lorentz de Hoos AM (eds) The Epilepsies. Handbook of clinical neurology, vol 15. New Holland, Amsterdam, pp 815–835
64.
66.
go back to reference Selye H (1956) The stress of life. McGraw-Hill, New York Selye H (1956) The stress of life. McGraw-Hill, New York
70.
go back to reference Shannon BJ, Dosenbach RA, Su Y, Vlassenko AG, Larson-Prior LJ, Nolan TS, Snyder AZ, Raichle ME (2013) Morning-evening variation in human brain metabolism and memory circuits. J Neurophysiol 109(5):1444–1456. doi:10.1152/jn.00651.2012 PubMedCrossRef Shannon BJ, Dosenbach RA, Su Y, Vlassenko AG, Larson-Prior LJ, Nolan TS, Snyder AZ, Raichle ME (2013) Morning-evening variation in human brain metabolism and memory circuits. J Neurophysiol 109(5):1444–1456. doi:10.​1152/​jn.​00651.​2012 PubMedCrossRef
71.
go back to reference Hoffmann U, Essfeld D, Stegemann J (1990) Comparison of arterial, end-tidal and transcutaneous PCO2 during moderate exercise and external CO2 loading in humans. Eur J Appl Physiol 61(1–2):1–4CrossRef Hoffmann U, Essfeld D, Stegemann J (1990) Comparison of arterial, end-tidal and transcutaneous PCO2 during moderate exercise and external CO2 loading in humans. Eur J Appl Physiol 61(1–2):1–4CrossRef
72.
go back to reference Vgontzas AN, Chrousos GP (2002) Sleep, the hypothalamic-pituitary-adrenal axis, and cytokines: multiple interactions and disturbances in sleep disorders. Endocrinol Metab Clin North Am 31(1):15–36PubMedCrossRef Vgontzas AN, Chrousos GP (2002) Sleep, the hypothalamic-pituitary-adrenal axis, and cytokines: multiple interactions and disturbances in sleep disorders. Endocrinol Metab Clin North Am 31(1):15–36PubMedCrossRef
Metadata
Title
The respiratory control of carbon dioxide in children and adolescents referred for treatment of psychogenic non-epileptic seizures
Authors
Kasia Kozlowska
Reena Rampersad
Catherine Cruz
Ubaid Shah
Catherine Chudleigh
Samantha Soe
Deepak Gill
Stephen Scher
Pascal Carrive
Publication date
01-10-2017
Publisher
Springer Berlin Heidelberg
Published in
European Child & Adolescent Psychiatry / Issue 10/2017
Print ISSN: 1018-8827
Electronic ISSN: 1435-165X
DOI
https://doi.org/10.1007/s00787-017-0976-0

Other articles of this Issue 10/2017

European Child & Adolescent Psychiatry 10/2017 Go to the issue