Laryngeal sensitivity in the neonatal period: From bench to bedside

Pediatric Pulmonology

Volumn 42, Issue 8, 2007, Pages 674-682

  Reix, Philippe ^a,b   St Hilaire, Marie ^b   Praud, Jean Paul ^b,c  

^a HÔPITAL DEBROUSSE   (France)

^b UNIVERSITÉ DE SHERBROOKE   (Canada)

^c UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Apnea of prematurity; Apparent life threatening event; Control of breathing; Laryngeal chemoreflexes (LCR); Sudden infant death syndrome (SIDS); Swallowing

Indexed keywords

BREATHING DISORDER; CHEMORECEPTOR REFLEX; CHEMOSENSITIVITY; HUMAN; LARYNX; NEWBORN; NEWBORN PERIOD; PRIORITY JOURNAL; REVIEW; SUDDEN INFANT DEATH SYNDROME;

EID: 34547747838     PISSN: 87556863     EISSN: 10990496     Source Type: Journal    
DOI: 10.1002/ppul.20645     Document Type: Review

References (95)

1. Bartlett D Jr. Comparative aspects of upper airway structure and function. In: Mathew OP, Sant'Ambrogio G, editors. Respiratory function of the upper airway. Lung biology in health and disease. Vol. 35, New York: Marcel Dekker; 1988. pp 31-45.
2. Widdicombe JG, Tatar M. Upper airway reflex control. Ann N Y Acad Sci 1988;533:252-261.
3. Sant'Ambrogio G, Sant'Ambrogio FB. Role of laryngeal afferents in cough. Pulm Pharmacol 1996;9:309-314.
4. Yoshida Y, Tanaka Y, Hirano M, Nakashima T. Sensory innervation of the pharynx and larynx. Am J Med 2000;108:51S-61S.
5. Sant'Ambrogio G, Tsubone H, Sant'Ambrogio FB. Sensory information from the upper airway: role in the control of breathing. Respir Physiol 1995;102:1-16.
6. Bradley RM. Sensory receptors of the larynx. Am J Med 2000; 108:47S-50S.
7. Sant'Ambrogio G, Mathew OP, Fisher JT, Sant'Ambrogio FB. Laryngeal receptors responding to transmural pressure, airflow and local muscle activity. Respir Physiol 1983;54:317-330.
8. Mortola JP, Fisher JT. Upper airway reflexes in newborns. In: Mathew OP, Sant'Ambrogio G, editors. Respiratory function of the upper airway. Lung biology in health and disease, Vol. 35, New York: Marcel Dekker; 1988. pp 303-357.
9. Widdicombe J. Airway receptors. Respir Physiol 2001;125:3-15.
10. Eichenwald EC, Howell RG 3rd, Kosch PC, Ungarelli RA, Lindsey J, Stark R. Developmental changes in sequential activation of laryngeal abductor muscle and diaphragm in infants. J Appl Physiol 1992;73:1425-1431.
11. Nielson DW, Ku PL, Egger M. Topical lidocaine exaggerates laryngomalacia during flexible bronchoscopy. Am J Respir Crit Care Med 2000;161:147-151.
12. Ertekin C, Aydogdu I. Neurophysiology of swallowing. Clin Neurophysiol 2003;114:2226-2244.
13. Bailey EF, Fregosi RF. Modulation of upper airway muscle activities by bronchopulmonary afferents. J Appl Physiol 2006; 101:609-617.
14. Diaz V, Dorion D, Kianicka I, Letourneau P, Praud J-P. Vagal afferents and active upper airway closure during pulmonary edema in lambs. J Appl Physiol 1999;86:1561-1569.
15. Nishino T. Physiological and pathophysiological implications of upper airway reflexes in humans. Jpn J Physiol 2000;50:3-14.
16. Taylor-Clark T, Umden BJ. Transduction mechanisms in airway sensory nerves. J Appl Physiol 2006;101:950-959.
17. Anderson JW, Sant'Ambrogio FB, Mathew OP, Sant'Ambrogio G. Water-responsive laryngeal receptors in the dog are not specialized endings. Respir Physiol 1990;79:33-43.
18. Hanamori T. Effects of various ion transport inhibitors on the water response in the superior laryngeal nerve in rats. Chem Senses 2001;26:897-903.
19. Forsberg K, Karlsson JA, Theodorsson E, Lundberg JM, Persson CG. Cough and bronchoconstriction mediated by capsaicin-sensitive sensory neurons in the guinea-pig. Pulm Pharmacol 1988;1:33-39.
20. Fox AJ. Mechanisms and modulation of capsaicin activity on airway afferent nerves. Pulm Pharmacol 1995;8:207-215.
21. Naida AM, Ghosh TK, Mathew OP. Airway protective reflexes elicited by laryngeal ammonia: role of C-fiber afferents. Respir Physiol 1996;103:11-17.
22. Mutoh T, Tsubone H, Nishimura R, Sasaki N. Effects of volatile anesthetics on vagal C-fiber activities and their reflexes in anesthetized dogs. Respir Physiol 1998;112:253-264.
23. Nishijima K, Atoji Y. Taste buds and nerve fibers in the rat larynx: an ultrastructural and immunohistochemical study. Arch Histol Cytol 2004;67:195-209.
24. Thach BT. Maturation and transformation of reflexes that protect the laryngeal airway from liquid aspiration from fetal to adult life. Am J Med 2001;111:69S-77S.
25. Martin RJ, Abu-Shaweesh JM. Control of breathing and neonatal apnea. Biol Neonate 2005;87:288-295.
26. Gauda E. Upper airway muscle control during development: Application to clinical disorders that occur in premature infants. In: Mathew OP, editor. Respiratory control and disorders in the newborn. Lung biology in health and disease. Vol. 173; New York: Marcel Dekker; 2003. pp 115-148.
27. Bland RD. Lung epithelial ion transport and fluid movement during the perinatal period. Am J Physiol 1990;259:L30-37.
28. Johnson P, Salisbury DM, Storey AT. Apnea induced by stimulation of sensory receptors in the larynx. In: Bosma JF, Showacre J, editors. Symposium on development of upper respiratory anatomy and function. Implications for sudden infant death syndrome. Washington, DC: US Department of Health, Education and Welfare; 1975. pp 160-185.
29. Harding R, Johnson P, McClelland ME. Liquid-sensitive laryngeal receptors in the developing sheep, cat and monkey. J Physiol 1978;277:409-422.
30. Downing SE, Lee JC. Laryngeal chemosensitivity: a possible mechanism for sudden infant death. Pediatrics 1975;55:640-649.
31. Lee JC, Stoll BJ, Downing SE. Properties of the laryngeal chemoreflex in neonatal piglets. Am J Physiol 1977;233:R30-36.
32. Boggs DF, Bartlett D Jr. Chemical specificity of a laryngeal apneic reflex in puppies. J Appl Physiol 1982;53:455-462.
33. Harned HS, Myracle J, Ferreiro J. Respiratory suppression and swallowing from introduction of fluids into the laryngeal region of the lamb. Pediatr Res 1978;12:1003-1009.
34. Kovar I, Selstam U, Catterton WZ, Stahlman MT, Sundell HW. Laryngeal chemoreflex in newborn lambs: respiratory and swallowing response to salts, acids, and sugars. Pediatr Res 1979;13:1144-1149.
35. Lanier B, Richardson MA, Cummings C. Effect of hypoxia on laryngeal reflex apnea - implications for sudden infant death. Otolaryngol Head Neck Surg 1983;91:597-604.
36. Lucier GE, Storey AT, Sessle BJ. Effects of upper respiratory tract stimuli on neonatal respiration: reflex and single neuron analyses in the kitten. Biol Neonate 1979;35:82-89.
37. Sladek M, Grogaard JB, Parker RA, Sundell HW. Prolonged hypoxemia enhances and acute hypoxemia attenuates laryngeal reflex apnea in young lambs. Pediatr Res 1993;34:813-820.
38. Storey AT, Johnson P. Laryngeal water receptors initiating apnea in the lamb. Exp Neurol 1975;47:42-55.
39. Marchal F, Corke BC, Sundell H. Reflex apnea from laryngeal chemo-stimulation in the sleeping premature newborn lamb. Pediatr Res 1982;16:621-627.
40. Marchal F, Crance JP, Arnould P. Ventilatory and waking responses to laryngeal stimulation in sleeping mature lambs. Respir Physiol 1986;63:31-41.
41. Sullivan CE, Murphy E, Kozar LF, Phillipson EA. Waking and ventilatory responses to laryngeal stimulation in sleeping dogs. J Appl Physiol 1978;45:681-689.
42. Page M, Jeffery HE, Marks V, Post EJ, Wood AK. Mechanisms of airway protection after pharyngeal fluid infusion in healthy sleeping piglets. J Appl Physiol 1995;78:1942-1949.
43. Page M, Jeffery H, Post EJ, Wood AK. Simulated pharyngeal reflux can lead to life-threatening apnea if swallowing and arousal are depressed. J Sudden Infant Death Syndrome Infant Mortality 1996;1:281-293.
44. Donnelly DF. Laryngeal reflexes. Integrated and cellular aspects. In: Haddad GG, Farber JP, editors. Developmental neurobiology of breathing. Lung biology in health and disease. Vol. 53; New York: Marcel Dekker; 1991. pp 271-288.
45. Davies AM, Koenig JS, Thach BT. Upper airway chemoreflex responses to saline and water in preterm infants. J Appl Physiol 1988;64:1412-1420.
46. Wennergren G, Hertzberg T, Milerad J, Bjure J, Lagercrantz H. Hypoxia reinforces laryngeal reflex bradycardia in infants. Acta Paediatr Scand 1989;78:11-17.
47. Lindgren C, Lin J, Graham BS, Gray ME, Parker RA, Sundell HW. Respiratory syncytial virus infection enhances the response to laryngeal chemostimulation and inhibits arousal from sleep in young lambs. Acta Paediatr 1996;85:789-797.
48. Jeffery HE, Megevand A, Page H. Why the prone position is a risk factor for sudden infant death syndrome. Pediatrics 1999;104: 263-269.
49. St-Hilaire M, Nsegbe E, Gagnon-Gervais K, Samson N, Moreau-Bussiere F, Fortier PH, Praud J-P. Laryngeal chemoreflexes induced by acid, water, and saline in nonsedated newborn lambs during quiet sleep. J Appl Physiol 2005;98: 2197-2203.
50. Hyman PE, Milla PJ, Benninga MA, Davidson GP, Fleisher DF, Taminiau J. Childhood functional gastrointestinal disorders: Neonate/Toddler. Gastroenterology 2006;130:1519-1526.
51. Beuchée A, Nsegbe E, St Hilaire M, Carrault G, Branger B, Pladys P, Praud J-P. Prolonged Dynamic Changes in Autonomic Heart Rate Modulation Induced by Acid Laryngeal Stimulation in Non-Sedated Lambs. Neonatology 2007;91:83-91.
52. St-Hilaire M, Samson N, Nsegbe E, Duvareille C, Moreau-Bussiere F, Micheau P, Leblond J, Praud JP. Postnatal maturation of laryngeal chemoreflexes in the preterm lamb. J Appl Physiol 2007;102:1429-1438.
53. Downs DH, Johnson K, Goding GS Jr. The effect of antihistamines on the laryngeal chemoreflex. Laryngoscope 1995;105: 857-861.
54. Heman-Ackah YD, Goding GS Jr. Effects of intralaryngeal carbon dioxide and acetazolamide on the laryngeal chemoreflex. Ann Otol Rhinol Laryngol 2000;109:921-928.
55. Grogaard J, Kreuger E, Lindstrom D, Sundell H. Effects of carotid body maturation and terbutaline on the laryngeal chemoreflex in newborn lambs. Pediatr Res 1986;20:724-729.
56. McCulloch TM, Flint PW, Richardson MA, Bishop MJ. Lidocaine effects on the laryngeal chemoreflex, mechanoreflex, and afferent electrical stimulation reflex. Ann Otol Rhinol Laryngol 1992;101:583-589.
57. Bauman NM, Wang D, Jaffe DA, Sandler AD, Luschei ED. Effect of intravenous calcitonin gene-related peptide antagonist on the laryngeal chemoreflex in piglets. Otolaryngol Head Neck Surg 1999;121:1-6.
58. McKelvey GM, Post EJ, Wood AKW, Jeffery HE. Airway protection following simulated gastro-esophageal reflux in sedated and sleeping neonatal piglets during active sleep. Clin Exp Pharmacol Physiol 2001;28:533-539.
59. Fagenholz SA, Lee JC, Downing SE. Association of anemia with reduced central respiratory drive in the piglet. Yale J Biol Med 1979;52:263-270.
60. Pickens DL, Schefft GL, Storch GA, Thach BT. Characterization of prolonged apneic episodes associated with respiratory syncytial virus infection. Pediatr Pulmonol 1989;6:195-201.
61. Lindgren C, Jing L, Graham B, Grogaard J, Sundell H. Respiratory syncytial virus infection reinforces reflex apnea in young lambs. Pediatr Res 1992;31:381-385.
62. Lindgren C, Grogaard J. Reflex apnoea response and inflammatory mediators in infants with respiratory tract infection. Acta Paediatr 1996;85:798-803.
63. Xia L, Damon TA, Leiter JC, Bartlett D. Focal warming in the nucleus of the solitary tract prolongs the laryngeal chemoreflex in decerebrate piglets. J Appl Physiol 2007;102:54-62.
64. Thach BT. Reflux associated apnea in infants: evidence for a laryngeal chemoreflex. Am J Med 1997;103:120S-124S.
65. Wetmore RF. Effects of acid on the larynx of the maturing rabbit and their possible significance to the sudden infant death syndrome. Laryngoscope 1993;103:1242-1254.
66. Thach BT. Sudden infant death syndrome: can gastroesophageal reflux cause sudden infant death? Am J Med 2000;108:144S-148S.
67. Page M, Jeffery H. The role of gastro-oesophageal reflux in the aetiology of SIDS. Early Hum Dev 2000;59:127-149.
68. Orenstein SR. Respiratory complications of reflux disease in infants. In: Stein MR, editor. Gastroesophageal Reflux Disease and Airway Disease. Lung biology in health and disease. Vol. 129, New York: Marcel Dekker; 1999. pp 269-284. 2003.
69. Herbst JJ, Book LS, Bray PF. Gastroesophageal reflux in the "near miss" sudden infant death syndrome. J Pediatr 1978; 92: 73-75.
70. Leape LL, Holder TM, Franklin JD, Amoury RA, Ashcraft KW. Respiratory arrest in infants secondary to gastroesophageal reflux. Pediatrics 1977;60:924-928.
71. Poets CF. Gastroesophageal reflux: a critical review of its role in preterm infants. Pediatrics 2004; e128-e132.
72. Bancalari E. Apnea is not prolonged by acid gastroesophageal reflux in preterm infants. Pediatrics 2005;116:1217-1218.
73. Molloy EJ, Di Fiore JM, Martin RJ. Does gastroesophageal reflux cause apnea in preterm infants? Biol Neonate 2005;87:254-261.
74. Peter CS, Sprodowski N, Bohnhorst B, Silny J, Poets CF. Gastroesophageal reflux and apnea of prematurity: no temporal relationship. Pediatrics 2002;109:8-11.
75. Di Fiore JM, Arko M, Whitehouse M, Kimball A, Martin RJ. Apnea is not prolonged by acid gastroesophageal reflux in preterm infants. Pediatrics 2005;116:1059-1063.
76. Wenzl TG, Schenke S, Peschgens T, Silny J, Heimann G, Skopnik H. Association of apnea and nonacid gastroesophageal reflux in infants: Investigations with the intraluminal impedance technique. Pediatr Pulmonol 2001;31:144-149.
77. Magista AM, Indrio F, Baldassarre M, Bucci N, Menolascina A, Mautone A, Francavilla R. Multichannel intraluminal impedance to detect relationship between gastroesophageal reflux and apnoea of prematurity. Dig Liver Dis 2007;39:216-221.
78. Finer NN, Higgins R, Kattwinkel J, Martin RJ. Summary proceedings from the apnea-of-prematurity group. Pediatrics 2006; 117:S47-51.
79. Filiano JJ, Kinney HC. A perspective on neuropathologic findings in victims of the sudden infant death syndrome: the triple-risk model. Biol Neonate 1994;65:194-197.
80. Thach BT. The role of respiratory control disorders in SIDS. Respir Physiol Neurobiol 2005;149:343-353.
81. Sutton D, Taylor EM, Lindeman RC. Prolonged apnea in infant monkeys resulting from stimulation of superior laryngeal nerve. Pediatrics 1978;61:519-527.
82. Curran AK, Xia L, Leiter JC, Bartlett D Jr. Elevated body temperature enhances the laryngeal chemoreflex in decerebrate piglets. J Appl Physiol 2005;98:780-786.
83. Sundell HW, Karmo H, Milerad J. Impaired cardiorespiratory recovery after laryngeal stimulation in nicotine-exposed young lambs. Pediatr Res 2003;53:104-112.
84. Hernandez E, Khoshoo V, Thoppil D, Edell D, Ross G. Aspiration: a factor in rapidly deteriorating bronchiolitis in previously healthy infants? Pediatr Pulmonol 2002;33:30-31.
85. Khoshoo V, Ross G, Kelly B, Edell D, Brown S. Benefits of thickened feeds in previously healthy infants with respiratory syncytial viral bronchiolitis. Pediatr Pulmonol 2001;31:301-302.
86. Rayyan M, Naulaers G, Daniels H, Allegaert K, Debeer A, Devlieger H. Characteristics of respiratory syncytial virus-related apnoea in three infants. Acta Paediatr 2004;93:847-849.
87. Kneyber MC, Brandenburg AH, de Groot R, Joosten KF, Rothbarth PH, Ott A, Moll HA. Risk factors for respiratory syncytial virus associated apnoea. Eur J Pediatr 1998;157:331-335.
88. Church NR, Anas NG, Hall CB, Brooks JG. Respiratory syncytial virus-related apnea in infants. Demographics and outcome. Am J Dis Child 1984;138:247-250.
89. Meert K, Heidemann S, Abella B, Sarnaik A. Does prematurity alter the course of respiratory syncytial virus infection? Crit Care Med 1990;18:1357-1359.
90. Sabogal C, Auais A, Napchan G, Mager E, Zhou BG, Suguihara C, Bancalari E, Piedimonte G. Effect of respiratory syncytial virus on apnea in weanling rats. Pediatr Res 2005;57:819-825.
91. Gleeson M, Clancy RL, Cox AJ, Gulliver SA, Hall ST, Cooper DM. Mucosa immune responses to infections in infants with acute life threatening events classified as "near-miss" sudden infant death syndrome. FEMS Immunol Med Microbiol 2004;42:105-118.
92. An SF, Gould S, Keeling JW, Fleming KA. Role of respiratory viral infection in SIDS: detection of viral nucleic acid by in situ hybridization. J Pathol 1993;171:271-278.
93. Bajanowski T, Rolf B, Jorch G, Brinkmann B. Detection of RNA viruses in sudden infant death (SID). Int J Legal Med 2003;117: 237-240.
94. Fernandez-Rodriguez A, Ballestros S, de Ory F, Echevarria JE, Alvarez-Lafuente R, Vallejo G, Gomez J. Virological analysis in the diagnosis of sudden children death: a medico-legal approach. Forensic Sci Int 2006;161:8-14.
95. Paterson DS, Trachtenberg FL, Thompson EG, Belliveau RA, Beggs AH, Darnall R, Chadwick AE, Krous HF, Kinney HC. Multiple serotonergic brainstem abnormalities in sudden infant death syndrome. JAMA 2006;296:2124-2132.