Brainstem mechanisms underlying the sudden infant death syndrome: Evidence from human pathologic studies

Developmental Psychobiology

Volumn 51, Issue 3, 2009, Pages 223-233

  Kinney, Hannah C ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Arcuate nucleus; Autonomic nervous system; Brainstem gliosis; Maternal cigarette smoking; Medulla oblongata; Prenatal alcohol exposure; Raph obscurus; Serotonin

Indexed keywords

ALCOHOL; BIOLOGICAL MARKER; NEUROTRANSMITTER; NICOTINE; SEROTONIN; SEROTONIN 1A RECEPTOR; SEROTONIN TRANSPORTER; TRYPTOPHAN HYDROXYLASE;

ALCOHOL CONSUMPTION; ALLELE; ARCUATE NUCLEUS; BODY POSTURE; BRAIN HYPOXIA; BRAIN ISCHEMIA; BRAIN STEM; BRAIN STEM GLIOSIS; CIGARETTE SMOKING; DISEASE MARKER; DISEASE PREDISPOSITION; EVIDENCE BASED MEDICINE; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENOTYPE; GLIOSIS; HUMAN; INFANT; MATERNAL SMOKING; PATHOPHYSIOLOGY; POSTNATAL DEVELOPMENT; PRENATAL EXPOSURE; PROTEIN BINDING; PROTEIN FUNCTION; REVIEW; RISK FACTOR; SUDDEN INFANT DEATH SYNDROME;

ALCOHOL DRINKING; ARCUATE NUCLEUS; AUTONOMIC NERVOUS SYSTEM; BRAIN STEM; FEMALE; GLIOSIS; HOMEOSTASIS; HUMANS; INFANT; INFANT, NEWBORN; MEDULLA OBLONGATA; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PRONE POSITION; RAPHE NUCLEI; RECEPTORS, SEROTONIN; RISK FACTORS; SEROTONIN; SUDDEN INFANT DEATH;

EID: 66149114863     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.20367     Document Type: Review

References (90)

1. Awtry, T. L., & Werling, L. L. (2003). Acute and chronic effects of nicotine on serotonin uptake in prefrontal cortex and hippocampus of rats. Synapse, 50(3), 206-211.
2. Barnes, N. M., & Sharp, T. (1999). A review of central 5-HT receptors and their function. Neuropharmacology, 38(8), 1083-1152.
3. Biondo, B., Lavezzi, A., Tosi, D., Turconi, P., & Matturri, L. (2003). Delayed neuronal maturation of the medullary arcuate nucleus in sudden infant death syndrome. Acta Neuropathologica (Berlin), 106(6), 545-551.
4. Blakely, R. D., & Bauman, A. L. (2000). Biogenic amine transporters: Regulation in flux. Current Opinion in Neurobiology, 10(3), 328-336.
5. Bou-Flores, C., Lajard, A. M., Monteau, R., De Maeyer, E., Seif, I., Lanoir, J, et al. (2000). Abnormal phrenic motoneuron activity and morphology in neonatal monoamine oxidase A-deficient transgenic mice: Possible role of a serotonin excess. Journal of Neuroscience, 20(12), 4646-4656.
6. Bradley, S. R., Pieribone, V. A., Wang, W., Severson, C. A., Jacobs, R. A., & Richerson, G. B. (2002). Chemosensitive serotonergic neurons are closely associated with large medullary arteries. Nature Neuroscience, 5(5), 401-402.
7. Brown, J. W., Sirlin, E. A., Benoit, A. M., Hoffman, J. M., & Darnall, R. A. (2007). Activation of 5-HT1A receptors in medullary raphe disrupts sleep and decreases shivering during cooling in the conscious piglet. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 294, R884-R894.
8. Chang, A. B., Wilson, S. J., Masters, I. B., Yuill, M., Williams, J., & Williams, G, (2003). Altered arousal response in infants exposed to cigarette smoke. Archives of Disease in Childhood, 88(1), 30-33.
9. Chong, A., Murphy, N., & Matthews, T. (2000). Effect of prone sleeping on circulatory control in infants. Archives of Disease in Childhood, 82(3), 253-256.
10. Curran, A. K., & Leiter, J. C. (2007). Baroreceptor-mediated inhibition of respiration after peripheral and central administration of a 5-HT1A receptor agonist in neonatal piglets. Experimental Physiology, 92(4), 757-767.
11. Darnall, R. A., Harris, M. B., Gill, W. H., Hoffman, J. M., Brown, J. W., & Niblock, M. M. (2005). Inhibition of serotonergic neurons in the nucleus paragigantocellularis lateralis fragments sleep and decreases rapid eye movement sleep in the piglet: Implications for sudden infant death syndrome. Journal of Neuroscience, 25(36), 8322-8332.
12. de Fiebre, N. C., & de Fiebre, C. M. (2005). alpha7 Nicotinic acetylcholine receptor knockout selectively enhances ethanol-, but not beta-amyloid-induced neurotoxicity. Neuroscience Letters, 373(1), 42-47.
13. Dohrman, D. P., & Reiter, C. K. (2003). Ethanol modulates nicotine-induced upregulation of nAChRs. Brain Research, 975(1-2), 90-98.
14. Druse, M. J., Kuo, A., & Tajuddin, N. (1991). Effects of in utero ethanol exposure on the developing serotonergic system. Alcoholism-Clinical and Experimental Research, 15(4), 678-684.
15. Druse, M. J., Tajuddin, N. F., Gillespie, R. A., & Le, P. (2006). The effects of ethanol and the serotonin(1A) agonist ipsapirone on the expression of the serotonin(1A) receptor and several antiapoptotic proteins in fetal rhombencephalic neurons. Brain Research, 1092(1), 79-86.
16. Duncan, J. R., Randall, L. L., Belliveau, R. A., Trachtenberg, F. L., Randall, B., Habbe, D, et al. (2008). The effect of maternal smoking and drinking during pregnancy upon (3)H-nicotine receptor brainstem binding in infants dying of the sudden infant death syndrome: Initial observations in a high risk population. Brain Pathology 18, 21-31.
17. Filiano, J. J., Choi, J. C., & Kinney, H. C. (1990). Candidate cell populations for respiratory chemosensitive fields in the human infant medulla. Journal of Comparative Neurology, 293(3), 448-465.
18. Filiano, J. J., & Kinney, H. C. (1992). Arcuate nucleus hypoplasia in the sudden infant death syndrome. Journal of Neuropathology and Experimental Neurology, 51(4), 394-403.
19. Filiano, J. J., & Kinney, H. C. (1994). A perspective on neuropathologic findings in victims of the sudden infant death syndrome: The triple-risk model. Biology of the Neonate, 65(3-4), 194-197.
20. Franco, P., Groswasser, J., Hassid, S., Lanquart, J. P., Scaillet, S., & Kahn, A. (1999). Prenatal exposure to cigarette smoking is associated with a decrease in arousal in infants. Journal of Pediatrics, 135(1), 34-38.
21. Franco, P., Lipshut, W., Valente, F., Adams, S., Groswasser, J., & Kahn, A. (2003). Cardiac autonomic characteristics in infants sleeping with their head covered by bedclothes. Journal of Sleep Research, 12(2), 125-132.
22. Franco, P., Lipshutz, W., Valente, F., Adams, S., Scaillet, S., & Kahn, A. (2002). Decreased arousals in infants who sleep with the face covered by bedclothes. Pediatrics, 109(6), 1112-1117.
23. Galland, B. C., Reeves, G., Taylor, B. J., & Bolton, D. P. (1998). Sleep position, autonomic function, and arousal. Archives of Disease in Childhood, Fetal and Neonatal Edition, 78(3), F189-F194.
24. Gao, K., & Mason, P. (2001). The discharge of a subset of serotonergic raphe magnus cells is influenced by baroreceptor input. Brain Research, 900(2), 306-313.
25. Greenberg, B. D., Tolliver, T. J., Huang, S. J., Li, Q., Bengel, D., & Murphy, D. L. (1999). Genetic variation in the serotonin transporter promoter region affects serotonin uptake in human blood platelets. American Journal of Medical Genetics, 88(1), 83-87.
26. Groswasser, J., Simon, T., Scaillet, S., Franco, P., & Kahn, A. (2001). Reduced arousals following obstructive apneas in infants sleeping prone. Pediatric Research, 49(3), 402-406.
27. Gunther, S., Maroteaux, L., & Schwarzacher, S. W. (2006). Endogenous 5-HT2B receptor activation regulates neonatal respiratory activity in vitro. Journal of Neurobiology, 66(9), 949-961.
28. Hauck, F. (2001). Changing epidemiology. In: R. W. Byard & H. F. Krous (Eds.), Sudden infant death syndrome: Problems, progress, and possibilities (pp. 31-57). London, New York: Arnold; Co-published by Oxford University Press.
29. Hilaire, G., Morin, D., Lajard, A. M., & Monteau, R. (1993). Changes in serotonin metabolism may elicit obstructive apnoea in the newborn rat. Journal of Physiology, 466, 367-381.
30. Hoffman, J. M., Brown, J. W., Sirlin, E. A., Benoit, A. M., Gill, W. H., Harris, M. B, et al. (2007). Activation of 5-HT1A receptors in the paragigantocellularis lateralis decreases shivering during cooling in the conscious piglet. American Journal of Physiology-Regulatory Integrative and Comparative Physiology, 293(1), R518-R527.
31. Horne, R. S., Ferens, D., Watts, A. M., Vitkovic, J., Lacey, B., Andrew, S, et al. (2001). The prone sleeping position impairs arousability in term infants. Journal of Pediatrics, 138(6), 811-816.
32. Iyasu, S., Randall, L. L., Welty, T. K., Hsia, J., Kinney, H. C., Mandell, F, et al. (2002). Risk factors for sudden infant death syndrome among northern plains Indians. Journal of the American Medical Association, 288(21), 2717-2723.
33. Jacobs, B. L., Wilkinson, L. O., & Fornal, C. A. (1990). The role of brain serotonin. A neurophysiologic perspective. Neuropsychopharmacology, 3(5-6), 473-479.
34. Kato, I., Franco, P., Groswasser, J., Scaillet, S., Kelmanson, I., Togari, H, et al. (2003). Incomplete arousal processes in infants who were victims of sudden death. American Journal of Respiratory and Critical Care Medicine, 168(11), 1298-1303.
35. Kelai, S., Aissi, F., Lesch, K. P., Cohen-Salmon, C., Hamon, M., & Lanfumey, L. (2003). Alcohol intake after serotonin transporter inactivation in mice. Alcohol and Alcoholism, 38(4), 386-389.
36. Kim, E. K., Lee, M. H., Kim, H., Sim,Y. J., Shin, M. S., Lee, S. J, et al. (2005). Maternal ethanol administration inhibits 5-hydroxytryptamine synthesis and tryptophan hydroxylase expression in the dorsal raphe of rat offspring. Brain and Development, 27(7), 472-476.
37. Kinney, H., & Paterson, D. S. (2004). The sudden infant death syndrome. Pathology and Genetics: Acquired and Inherited Diseases of the Developing Nervous System, 194-203.
38. Kinney, H. C. (2005). Abnormalities of the brainstem serotonergic system in the sudden infant death syndrome: A review. Pediatric and Developmental Pathology, 8(5), 507-524.
39. Kinney, H. C., & Armstrong, D. L. (1996). Perinatal neuropathology. In: D. I. Graham & P. L. Lantos (Eds.), Greenfield's neurology (Vol. 2, 6th edition, pp. 537-600). New York: Oxford University Press, Inc.
40. Kinney, H. C., Belliveau, R. A., Trachtenberg, F. L., Rava, L. A., & Paterson, D. S. (2007). The development of the medullary serotonergic system in early human life. Autonomic Neuroscience, 132(1-2), 81-102.
41. Kinney, H. C., Burger, P. C., Harrell, F. E., Jr., & Hudson, R. P. Jr., (1983). 'Reactive gliosis' in the medulla oblongata of victims of the sudden infant death syndrome. Pediatrics, 72(2), 181-187.
42. Kinney, H. C., Filiano, J. J., Sleeper, L. A., Mandell, F., Valdes-Dapena, M., & White, W. F. (1995). Decreased muscarinic receptor binding in the arcuate nucleus in sudden infant death syndrome. Science, 269(5229), 1446-1450.
43. Kinney, H. C., Filiano, J. J., & White, W. F. (2001). Medullary serotonergic network deficiency in the sudden infant death syndrome: Review of a 15-year study of a single dataset. Journal of Neuropathology and Experimental Neurology, 60(3), 228-247.
44. Kinney, H. C., McHugh, T., Miller, K., Belliveau, R. A., & Assmann, S. F. (2002). Subtle developmental abnormalities in the inferior olive: An indicator of prenatal brainstem injury in the sudden infant death syndrome. Journal of Neuropathology and Experimental Neurology, 61(5), 427-441.
45. Kinney, H. C., Myers, M. M., Belliveau, R. A., Randall, L. L., Trachtenberg, F. L., Fingers, S. T, et al. (2005). Subtle autonomic and respiratory dysfunction in sudden infant death syndrome associated with serotonergic brainstem abnormalities: A case report. Journal of Neuropathology and Experimental Neurology, 64(8), 689-694.
46. Kinney, H. C., Randall, L. L., Sleeper, L. A., Willinger, M., Belliveau, R. A., Zec, N, et al. (2003). Serotonergic brainstem abnormalities in Northern Plains Indians with the sudden infant death syndrome. Journal of Neuropathology and Experimental Neurology, 62(11), 1178-1191.
47. Lewis, K. W., & Bosque, E. M. (1995). Deficient hypoxia awakening response in infants of smoking mothers: Possible relationship to sudden infant death syndrome. Journal of Pediatrics, 127(5), 691-699.
48. Li, X., Rainnie, D. G., McCarley, R. W., & Greene, R. W. (1998). Presynaptic nicotinic receptors facilitate monoaminergic transmission. Journal of Neuroscience, 18(5), 1904-1912.
49. Lovick, T. (1997). The medullary raphe nuclei: A system for integration and gain control in autonomic and somatomotor responsiveness? Experimental Physiology, 82, 31-41.
50. Machaalani, R., Rodriguez, M., & Waters, K. A. (2007). Active caspase-3 in the sudden infant death syndrome (SIDS) brainstem. Acta Neuropathologica (Berlin), 113(5), 577-584.
51. Machaalani, R., & Waters, K. A. (2003). NMDA receptor 1 expression in the brainstem of human infants and its relevance to the sudden infant death syndrome (SIDS). Journal of Neuropathology and Experimental Neurology, 62(10), 1076-1085.
52. Machaalani, R., & Waters, K. A. (2008). Neuronal cell death in the Sudden Infant Death Syndrome brainstem and associations with risk factors. Brain, 131(Pt 1), 218-228.
53. Mansouri, J., Panigrahy, A., Filiano, J. J., Sleeper, L. A., St John, W. M., & Kinney, H. C. (2001). Alpha2 receptor binding in the medulla oblongata in the sudden infant death syndrome. Journal of Neuropathology and Experimental Neurology, 60(2), 141-146.
54. Mason, P. (2001). Contributions of the medullary raphe and ventromedial reticular region to pain modulation and other homeostatic functions. Annual Review of Neuroscience, 24, 737-777.
55. Mathews, T. J., & MacDorman, M. F. (2006). Infant mortality statistics from the 2003 period linked birth/infant death data set. National Vital Statistics Reports, 54(16), 1-29.
56. Matturri, L., Biondo, B., Mercurio, P., & Rossi, L. (2000). Severe hypoplasia of medullary arcuate nucleus: Quantitative analysis in sudden infant death syndrome. Acta Neuropathologica (Berlin), 99(4), 371-375.
57. McGinty, D., & Harper, R. M. (1976). Dorsal raphe neruons: Depression of firing during sleep in cats. Brain Research, 101, 569-575.
58. 2 response in newborn piglets. Journal of Applied Physiology, 96, 1909-1919.
59. Monteau, R., Morin, D., Hennequin, S., & Hilaire, G. (1990). Differential effects of serotonin on respiratory activity of hypoglossal and cervical motoneurons: An in vitro study on the newborn rat. Neuroscience Letters, 111(1-2), 127-132.
60. Morrison, S. F. (2001). Differential control of sympathetic outflow. American Journal of Physiology-Regulatory Integrative and Comparative Physiology, 281(3), R683-R698.
61. Mossner, R., Daniel, S., Albert, D., Heils, A., Okladnova, O., Schmitt, A, et al. (2000). Serotonin transporter function is modulated by brain-derived neurotrophic factor (BDNF) but not nerve growth factor (NGF). Neurochemistry International, 36(3), 197-202.
62. Nachmanoff, D. B., Panigrahy, A., Filiano, J. J., Mandell, F., Sleeper, L. A., Valdes-Dapena, M, et al. (1998). Brainstem 3H-nicotine receptor binding in the sudden infant death syndrome. Journal of Neuropathology and Experimental Neurology, 57(11), 1018-1025.
63. Naeye, R. L. (1976). Brain-stem and adrenal abnormalities in the sudden-infant-death syndrome. American Journal of Clinical Pathology, 66(3), 526-530.
64. Nagai, M. (1992). The role of serotonergic system in body temperature regulation. Physiological Research, 41(1), 65-69.
65. Narita, N., Narita, M., Takashima, S., Nakayama, M., Nagai, T., & Okado, N. (2001). Serotonin transporter gene variation is a risk factor for sudden infant death syndrome in the Japanese population. Pediatrics, 107(4), 690-692.
66. Nattie, E. E., Li, A., Richerson, G., & Lappi, D. A. (2004). Medullary serotonergic neurones and adjacent neurones that express neurokinin-1 receptors are both involved in chemoreception in vivo. Journal of Physiology, 556(Pt 1), 235-253.
67. Obonai, T., Takashima, S., Becker, L. E., Asanuma, M., Mizuta, R., Horie, H, et al. (1996). Relationship of substance P and gliosis in medulla oblongata in neonatal sudden infant death syndrome. Pediatric Neurology, 15(3), 189-192.
68. Ootsuka, Y., & Blessing, W. W. (2006). Activation of 5-HT1A receptors in rostral medullary raphe inhibits cutaneous vasoconstriction elicited by cold exposure in rabbits. Brain Research, 1073-1074, 252-261.
69. Ozawa, Y., & Okado, N. (2002). Alteration of serotonergic receptors in the brain stems of human patients with respiratory disorders. Neuropediatrics, 33(3), 142-149.
70. Panigrahy, A., Filiano, J., Sleeper, L. A., Mandell, F., Valdes-Dapena, M., Krous, H. F, et al. (2000). Decreased serotonergic receptor binding in rhombic lip-derived regions of the medulla oblongata in the sudden infant death syndrome. Journal of Neuropathology and Experimental Neurology, 59(5), 377-384.
71. Panigrahy, A., Filiano, J. J., Sleeper, L. A., Mandell, F., Valdes-Dapena, M., Krous, H. F, et al. (1997). Decreased kainate receptor binding in the arcuate nucleus of the sudden infant death syndrome. Journal of Neuropathology and Experimental Neurology, 56(11), 1253-1261.
72. Paterson, D. S., Trachtenberg, F. L., Thompson, E. G., Belliveau, R. A., Beggs, A. H., Darnall, R, et al. (2006). Multiple serotonergic brainstem abnormalities in sudden infant death syndrome. Journal of the American Medical Association, 296(17), 2124-2132.
73. Pelaez, N. M., Schreihofer, A. M., & Guyenet, P. G. (2002). Decompensated hemorrhage activates serotonergic neurons in the subependymal parapyramidal region of the rat medulla. American Journal of Physiology-Regulatory Integrative and Comparative Physiology, 283(3), R688-R697.
74. Pena, F., & Ramirez, J. M. (2002). Endogenous activation of serotonin-2A receptors is required for respiratory rhythm generation in vitro. Journal of Neuroscience, 22(24), 11055-11064.
75. Penatti, E. M., Berniker, A. V., Kereshi, B., Cafaro, C., Kelly, M. L., Niblock, M. M, et al. (2006). Ventilatory response to hypercapnia and hypoxia after extensive lesion of medullary serotonergic neurons in newborn conscious piglets. Journal of Applied Physiology, 101(4), 1177-1188.
76. Ponsonby, A. L., Dwyer, T., & Cochrane, J. (2002). Population trends in sudden infant death syndrome. Seminars in Perinatology, 26(4), 296-305.
77. Rubenstein, J. L. (1998). Development of serotonergic neurons and their projections. Biological Psychiatry, 44(3), 145-150.
78. Schechtman, V. L., Harper, R. M., Kluge, K. A., Wilson, A. J., Hoffman, H. J., & Southall, D. P. (1989). Heart rate variation in normal infants and victims of the sudden infant death syndrome. Early Human Development, 19(3), 167-181.
79. Schechtman, V. L., Lee, M. Y., Wilson, A. J., & Harper, R. M. (1996). Dynamics of respiratory patterning in normal infants and infants who subsequently died of the sudden infant death syndrome. Pediatric Research, 40(4), 571-577.
80. Takashima, S., Armstrong, D., Becker, L., & Bryan, C. (1978). Cerebral hypoperfusion in the sudden infant death syndrome? Brainstem gliosis and vasculature. Annals of Neurology, 4(3), 257-262.
81. Takashima, S., & Becker, L. E. (1991). Delayed dendritic development of catecholaminergic neurons in the ventrolateral medulla of children who died of sudden infant death syndrome. Neuropediatrics, 22(2), 97-99.
82. 2. Journal of Applied Physiology, 97(5), 1763-1773.
83. Trulson, M. E., & Jacobs, B. J. (1979). Raphe unit activity in freely moving cats: Correlation with the level of behavior arousal. Brain Research, 163, 135-150.
84. van Dyck, C. H., Malison, R. T., Staley, J. K., Jacobsen, L. K., Seibyl, J. P., Laruelle, M, et al. (2004). Central serotonin transporter availability measured with [123I]beta-CIT SPECT in relation to serotonin transporter genotype. American Journal of Psychiatry, 161(3), 525-531.
85. Wang, W., Tiwari, J. K., Bradley, S. R., Zaykin, R. V., & Richerson, G. B. (2001). Acidosis-stimulated neurons of the medullary raphe are serotonergic. Journal of Neurophysiology, 85(5), 2224-2235.
86. Weese-Mayer, D. E., Berry-Kravis, E. M., Maher, B. S., Silvestri, J. M., Curran, M. E., & Marazita, M. L. (2003). Sudden infant death syndrome: Association with a promoter polymorphism of the serotonin transporter gene. American Journal of Medical Genetics, 117(3), 268-274.
87. Weese-Mayer, D. E., Zhou, L., Berry-Kravis, E. M., Maher, B. S., Silvestri, J. M., & Marazita, M. L. (2003). Association of the serotonin transporter gene with sudden infant death syndrome: A haplotype analysis. American Journal of Medical Genetics, 122(3), 238-245.
88. Willinger, M., James, L. S., & Catz, C. (1991). Defining the sudden infant death syndrome (SIDS): Deliberations of an expert panel convened by the National Institute of Child Health and Human Development. Pediatric Pathology, 11(5), 677-684.
89. Xu, Z., Seidler, F. J., Ali, S. F., Slikker, W., Jr., & Slotkin, T. A. (2001). Fetal and adolescent nicotine administration: Effects on CNS serotonergic systems. Brain Research, 914(1-2), 166-178.
90. Zhou, F. C., Sari, Y., Zhang, J. K., Goodlett, C. R., & Li, T. (2001). Prenatal alcohol exposure retards the migration and development of serotonin neurons in fetal C57BL mice. Brain Research Developmental Brain Research, 126(2), 147-155.