Apnea of prematurity: Pathogenesis and management strategies

Journal of Perinatology

Volumn 31, Issue 5, 2011, Pages 302-310

  Mathew, O P ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

airway receptors; apnea; caffeine; chemoreceptors; prematurity

Indexed keywords

ADENOSINE A1 RECEPTOR; ADENOSINE A2 RECEPTOR; ADENOSINE A2A RECEPTOR; CAFFEINE; CARBON DIOXIDE; DOXAPRAM; METHYLXANTHINE DERIVATIVE; PLACEBO; THEOPHYLLINE;

ABDOMINAL DISTENSION; ABSENCE OF SIDE EFFECTS; ARTICLE; ARTIFICIAL VENTILATION; BRADYCARDIA; BRAIN STEM; BREATHING MECHANICS; CHEMORECEPTOR; CONTINUOUS INFUSION; DISEASE CLASSIFICATION; DISEASE PREDISPOSITION; DRUG ABSORPTION; DRUG EFFECT; DRUG EFFICACY; DRUG HALF LIFE; DRUG MECHANISM; DRUG TOLERABILITY; GASTROESOPHAGEAL REFLUX; HUMAN; HYPERCAPNIA; HYPERTENSION; HYPOXIA; INTERMITTENT POSITIVE PRESSURE VENTILATION; IRRITABILITY; LUNG DYSPLASIA; LUNG INNERVATION; MYELINATION; NERVE STIMULATION; NERVOUSNESS; NEWBORN APNEA; NONHUMAN; NUTRITIONAL INTOLERANCE; PATHOGENESIS; POSITIVE END EXPIRATORY PRESSURE; RECEPTOR BLOCKING; RESTLESSNESS; SENSORY NERVE; SIDE EFFECT; SLEEP; TACHYCARDIA; UNSPECIFIED SIDE EFFECT; VOMITING;

ANOXIA; APNEA; ARRHYTHMIAS, CARDIAC; BRAIN STEM; CAFFEINE; CENTRAL NERVOUS SYSTEM STIMULANTS; CONTINUOUS POSITIVE AIRWAY PRESSURE; FETAL ORGAN MATURITY; HUMANS; HYPERCAPNIA; INFANT, NEWBORN; INFANT, PREMATURE; INFANT, PREMATURE, DISEASES; PROGNOSIS; RECEPTORS, PURINERGIC P1; RESPIRATORY RATE; RESPIRATORY SYSTEM;

EID: 79955568048     PISSN: 07438346     EISSN: 14765543     Source Type: Journal    
DOI: 10.1038/jp.2010.126     Document Type: Article

References (104)

1. Bianchi AL, Gestreau C. The brainstem respiratory network: an overview of a half century of research. Respir Physiol Neurobiol 2009; 168: 4-12.
2. Noble LM, Carlo WA, Miller MJ, DiFiore JM, Martin RJ. Transient changes in expiratory time during hypercapnia in premature infants. J Appl Physiol 1987; 62: 1010-1013. (Pubitemid 17073896)
3. Eichenwald EC, Ungarelli RA, Stark AR. Hypercapnia increases expiratory braking in preterm infants. J Appl Physiol 1993; 75: 2665-2670. (Pubitemid 24008385)
4. Martin RJ, Carlo WA, Robertson SS, Day WR, Bruce EN. Biphasic response of respiratory frequency to hypercapnea in preterm infants. Pediatr Res 1985; 19: 791-796. (Pubitemid 15029778)
5. Corcoran AE, Hodges MR, Wu Y, Wang W, Wylie CJ, Deneris ES et al. Medullary serotonin neurons and central CO2 chemoreception. Respir Physiol Neurobiol 2009; 168: 49-58.
6. Frantz III ID, Adler SM, Thach BT, Taeusch Jr HW. Maturational effects on respiratory responses to carbon dioxide in premature infants. J Appl Physiol 1976; 41: 41-45.
7. Rigatto H, Brady JP, de la Torre Verduzco R. Chemoreceptor reflexes in preterm infants: II. The effect of gestational and postnatal age on the ventilatory response to inhaled carbon dioxide. Pediatrics 1975; 55: 614-620.
8. Gerhardt T, Bancalari E. Apnea of prematurity. 1. Lung function and regulation of breathing. Pediatrics 1984; 74: 58-62. (Pubitemid 14078838)
9. Khan A, Qurashi M, Kwiatkowski K, Cates D, Rigatto H. Measurement of the CO2 apneic threshold in newborn infants: possible relevance for periodic breathing and apnea. J Appl Physiol 2005; 98: 1171-1176. (Pubitemid 40396486)
10. Cross KW, Oppe TE. The effect of inhalation of high and low concentration of oxygen on the respiration of the premature infant. J Physiol 1952; 117: 38.
11. Rigatto H, Kalapesi Z, Leahy FN, Durand M, MacCallum M, Cates D. Ventilatory response to 100% and 15% O2 during wakefulness and sleep in preterm infants. Early Hum Dev 1982; 7: 1-10. (Pubitemid 12001617)
12. Ang RC, Hoop B, Kazemi H. Role of glutamate as the central neurotransmitter in the hypoxic ventilatory response. J Appl Physiol 1992; 72: 1480-1487.
13. Rigatto H, Brady JP, de la Torre Verduzco R. Chemoreceptor reflexes in preterm infants: I. The effect of gestational and postnatal age on the ventilatory response to inhalation of 100% and 15% oxygen. Pediatrics 1975; 55: 604-613.
14. Alvaro R, Alvarez J, Kwiatkowski K, Cates D, Rigatto H. Small preterm infants (less than or equal to 1500 g) have only a sustained decrease in ventilation in response to hypoxia. Pediatr Res 1992; 32: 403-406.
15. Martin RJ, DiFiore JM, Jana L, Davis RL, Miller MJ, Coles SK et al. Persistence of the biphasic ventilatory response to hypoxia in preterm infants. J Pediatr 1998; 132: 960-964. (Pubitemid 28280406)
16. Eden GJ, Hanson MA. Effects of chronic hypoxia from birth on the ventilatory response to acute hypoxia in the newborn rat. J Physiol 1987; 392: 11-19. (Pubitemid 18014294)
17. Ling L, Olson Jr EB, Vidruk EH, Mitchell GS. Attenuation of the hypoxic ventilatory response in adult rats following one month of perinatal hyperoxia. J Physiol 1996; 495: 561-571. (Pubitemid 26331836)
18. Katz-Salamon M, Jonsson B, Lagercrantz H. Blunted peripheral chemoreceptor response to hyperoxia in a group of infants with bronchopulmonary dysplasia. Pediatr Pulmonol 1995; 20: 101-106.
19. Cardot V, Chardon K, Tourneux P, Micallef S, Stéphan E, Léké A et al. Ventilatory response to a hyperoxic test is related to the frequency of short apneic episodes in late preterm neonates. Pediatr Res 2007; 62: 591-596. (Pubitemid 351338996)
20. Nock ML, Difiore JM, Arko MK, Martin RJ. Relationship of the ventilatory response to hypoxia with neonatal apnea in preterm infants. J Pediatr 2004; 144: 291-295. (Pubitemid 38333883)
21. Peng YJ, Rennison J, Prabhakar NR. Intermittent hypoxia augments carotid body and ventilatory response to hypoxia in neonatal rat pups. J Appl Physiol 2004; 97: 2020-2025. (Pubitemid 39426026)
22. Nault MA, Vincent SG, Fisher JT. Mechanisms of capsaicin- and lactic acid-induced bronchoconstriction in the newborn dog. J Physiol 1999; 515: 567-578. (Pubitemid 29129226)
23. Sant'Ambrogio G, Widdicombe J. Reflexes from airway rapidly adapting receptors. Respir Physiol 2001; 125: 33-45. (Pubitemid 32184645)
24. Fleming PJ, Bryan AC, Bryan MH. Functional immaturity of pulmonary irritant receptors and apnea in newborn preterm infants. Pediatrics 1978; 61: 515-518. (Pubitemid 8299732)
25. Widdicombe JG, Sant'Ambrogio G, Mathew OP. Nervous receptors of the upper airway. In: Mathew OP, Sant'Ambrogio G (eds). Respiratory Function of the Upper Airway. Marcel Dekker: New York, 1988; 193-232.
26. Sant'Ambrogio G, Mathew OP, Fisher JT, Sant'Ambrogio FB. Laryngeal mechanoreceptors responding to transmural pressure, airflow and local muscle activity. Respir Physiol 1983; 54: 317-330. (Pubitemid 14177492)
27. Sant'Ambrogio G, Mathew OP, Sant'Ambrogio FB, Fisher JT. Laryngeal cold receptors. Respir Physiol 1985; 59: 35-44. (Pubitemid 15198654)
28. Mathew OP, Sant'Ambrogio G, Fisher JT, Sant'Ambrogio FB. Laryngeal pressure receptors. Respir Physiol 1984; 57: 113-122. (Pubitemid 14061906)
29. Boggs DF, Bartlett Jr D. Chemical specificity of a laryngeal apneic reflex in puppies. J Appl Physiol 1982; 53: 455-462. (Pubitemid 12049636)
30. Mendelowitz D. Superior laryngeal neurons directly excite cardiac vagal neurons within the nucleus ambiguus. Brain Res Bull 2000; 51: 135-138. (Pubitemid 30069875)
31. Fisher JT, Mathew OP, Sant'Ambrogio FB, Sant'Ambrogio G. Reflex effects and receptor responses to upper airway pressure and flow stimuli in developing puppies. J Appl Physiol 1985; 58: 258-264. (Pubitemid 15054365)
32. Johnson P, Salisbury DM. Sucking and breathing during artificial feeding in the human neonate. In: Bosma JF, Showacre J (eds). Development of Upper Respiratory Anatomy and Function. NIH: Bethesda, MD, 1975; 206-211.
33. Perkett EA, Vaughan RL. Evidence for a laryngeal chemoreflex in some human preterm infants. Acta Paediatr Scand 1982; 71: 969-972. (Pubitemid 12006571)
34. Milner AD, Saunders RA, Hopkin IE. Apnoea induced by airflow obstruction. Arch Dis Child 1977; 52: 379-382. (Pubitemid 8101382)
35. Thach BT, Schefft GL, Pickens DL, Menon AP. Influence of upper airway negative pressure reflex on response to airway occlusion in sleeping infants. J Appl Physiol 1989; 67: 749-755. (Pubitemid 19218676)
36. Widdicombe J. Nasal and pharyngeal reflexes. In: Mathew OP, Sant'Ambrogio G (eds). Respiratory Function of the Upper Airway. Marcel Dekker: New York, 1988; 233-258.
37. Jacobs BL, Heym J, Trulson ME. Behavioral and physiological correlates of brain serotoninergic unit activity. J Physiol (Paris) 1981; 77: 431-436. (Pubitemid 11032702)
38. Cohen G, Henderson-Smart DJ. Upper airway stability and apnea during nasal occlusion in newborn infants. J Appl Physiol 1986; 60: 1511-1517. (Pubitemid 16088036)
39. Amiel J, Laudier B, Attie-Bitach T, Trang H, de Pontual L, Gener B et al. Polyalanine expansion and frameshift mutations of the paired-like homeobox gene PHOX2B in congenital central hypoventilation syndrome. Nat Genet 2003; 33: 459-461. (Pubitemid 36390004)
40. Amiel J, Dubreuil V, Ramanantsoa N, Fortin G, Gallego J, Brunet JF et al. PHOX2B in respiratory control: lessons from congenital central hypoventilation syndrome and its mouse models. Respir Physiol Neurobiol 2009; 168(1-2): 125-132.
41. Menuet C, Dutschmann M, Hilaire G. Early breathing defects after moderate hypoxia or hypercapnia in a mouse model of Rett syndrome. Respir Physiol Neurobiol 2009; 168: 109-118.
42. Zanella S, Tauber M, Muscatelli F. Breathing deficits of the Prader-Willi syndrome. Respir Physiol Neurobiol 2009; 168: 119-124.
43. American Academy of Pediatrics, Committee on Fetus and Newborn. Apnea, sudden infant death syndrome, and home monitoring. Pediatrics 2003; 111: 914-917.
44. Dransfield DA, Spitzer AR, Fox WW. Episodic airway obstruction in premature infants. Am J Dis Child 1983; 137: 441-443. (Pubitemid 13129937)
45. Mathew OP, Roberts JL, Thach BT. Pharyngeal airway obstruction in preterm infants during mixed and obstructive apnea. J Pediatr 1982; 100: 964-968. (Pubitemid 12123605)
46. Brouillette RT, Thach BT. A neuromuscular mechanism maintaining extrathoracic airway patency. J Appl Physiol 1979; 46: 772-779. (Pubitemid 9172227)
47. Mathew OP. Maintenance of upper airway patency. J Pediatr 1985; 106: 863-869.
48. Wilson SL, Thach BT, Brouillette RT, Abu-Osba YK. Upper airway patency in the human infant: influence of airway pressure and posture. J Appl Physiol 1980; 48: 500-504. (Pubitemid 10141905)
49. Safar P, Escarraga LA, Chang F. Upper airway obstruction in the unconscious patient. J Appl Physiol 1959; 14: 760-764.
50. Thach BT, Stark AR. Spontaneous neck flexion and airway obstruction during apneic spells in preterm infants. J Pediatr 1979; 94: 275-281. (Pubitemid 9072427)
51. Gabriel M, Albani M, Schulte FJ. Apneic spells and sleep states in preterm infants. Pediatrics 1976; 57: 142-147.
52. Milner AD, Boon AW, Saunders RA, Hopkin IE. Upper airways obstruction and apnoea in preterm babies. Arch Dis Child 1980; 55: 22-25. (Pubitemid 10133462)
53. Idiong N, Lemke RP, Lin YJ, Kwiatkowski K, Cates DB, Rigatto H. Airway closure during mixed apneas in preterm infants: is respiratory effort necessary? J Pediatr 1998; 133: 509-512. (Pubitemid 28465376)
54. Rigatto H. Periodic breathing. In: Mathew OP (ed). Respiratory Control and its Disorders in the Newborn. Marcel Dekker: New York, 2003, pp 237-272.
55. Al-Saif S, Alvaro R, Manfreda J, Kwiatkowski K, Cates D, Qurashi M et al. A randomized controlled trial of theophylline versus CO2 inhalation for treating apnea of prematurity. J Pediatr 2008; 153: 513-518.
56. Mathew OP. Apnea, bradycardia and desaturation: the clinical issues. In: Mathew OP (ed). Respiratory Control and its Disorders in the Newborn. Marcel Dekker: New York, 2003, pp 273-293.
57. Henderson-Smart DJ, Butcher-Puech MC, Edwards DA. Incidence and mechanism of bradycardia during apnoea in preterm infants. Arch Dis Child 1986; 61: 227-232. (Pubitemid 16108938)
58. Vyas H, Milner AD, Hopkin IE. Relationship between apnoea and bradycardia in preterm infants. Acta Paediatr Scand 1981; 70: 785-790. (Pubitemid 11027037)
59. Carbone T, Marrero LC, Weiss J, Hiatt M, Hegyi T. Heart rate and oxygen saturation correlates of infant apnea. J Perinatol 1999; 19: 44-47.
60. Mathew OP, Gamble YD, Zimowski K. Prevalence of bradyarrhythmias during transient episodes of bradycardia among preterm Infants. J Neonatal-Perinatal Medicine 2008; 1: 43-47.
61. Andriessen P, Koolen AM, Bastin FH, Lafeber HN, Meijler FL. Supraventricular escape rhythms during transient episodes of bradycardia in preterm infants. Cardiol Young 2001; 11: 626-631. (Pubitemid 33768608)
62. Peter CS, Sprodowski N, Bohnhorst B, Silny J, Poets CF. Gastro esophageal reflux and apnea of prematurity: no temporal relationship. Pediatrics 2002; 109: 8-11. (Pubitemid 34049421)
63. Omari TI. Apnea-associated reduction in lower esophageal sphincter tone in premature infants. J Pediatr 2009; 154: 374-378.
64. Wheatley E, Kennedy KA. Cross-over trial of treatment for bradycardia attributed to gastroesophageal reflux in preterm infants. J Pediatr 2009; 155: 516-521.
65. Thoppil CK, Belan MA, Cowen CP, Mathew OP. Behavioral arousal in newborn infants and its association with termination of apnea. J Appl Physiol 1991; 70: 2479-2484.
66. Wulbrand H, Von Zezschwitz G, Bentele KHP. Submental and diaphragmatic muscle activity during and at resolution of mixed and obstructive apneas and cardiorespiratory arousal in preterm infants. Pediatr Res 1995; 38: 298-305.
67. McNamara F, Issa FQ, Sullivan CE. Arousal pattern following central and obstructive breathing abnormalities in infants and children. J Appl Physiol 1996; 81: 2651-2657. (Pubitemid 27043384)
68. Lawson EE. Nonpharmacological management of idiopathic apnea of the premature infant. In: Mathew OP (ed). Respiratory Control and its Disorders in the Newborn. Marcel Dekker: New York, 2003; 335-354.
69. Graham A, Finer NN. Pharmacotherapy of apnea of prematurity. In: Mathew OP (ed). Respiratory Control and its Disorders in the Newborn. Marcel Dekker: New York, 2003; 317-333.
70. Curzi-Dascalova L, Aujard Y, Gaultier C, Rajguru M. Sleep organization is unaffected by caffeine in premature infants. J Pediatr 2002; 140: 766-771. (Pubitemid 34666699)
71. Bairam A, Boutroy MJ, Badonnel Y, Vert P. Theophylline versus caffeine: comparative effects in treatment of idiopathic apnea in the preterm infant. J Pediatr 1987; 110: 636-639. (Pubitemid 17049061)
72. Brouard C, Moriette G, Murat I, Flouvat B, Pajot N, Walti H et al. Comparative efficacy of theophylline and caffeine in the treatment of idiopathic apnea in premature infants. Am J Dis Child 1985; 139: 698-700. (Pubitemid 15006408)
73. Sims ME, Yau G, Rambhatla S, Cabal L, Wu PY. Limitations of theophylline in the treatment of apnea of prematurity. Am J Dis Child 1985; 139: 567-570. (Pubitemid 15094788)
74. Erenberg A, Leff RD, Haack DG, Mosdell KW, Hicks GM, Wynne BA. Caffeine citrate for the treatment of apnea of prematurity: a double-blind, placebo-controlled study. Pharmacotherapy 2000; 20: 644-652. (Pubitemid 30387680)
75. Thurston JH, Hauhard RE, Dirgo JA. Aminophylline increases cerebral metabolic rate and decreases anoxic survival in young mice. Science 1978; 201: 649-651. (Pubitemid 9017743)
76. McDonnell M, Ives NK, Hope PL. Intravenous aminophylline and cerebral blood flow in preterm infants. Arch Dis Child 1992; 67: 416-418.
77. Hoecker C, Nelle M, Poeschl J, Beedgen B, Linderkamp O. Caffeine impairs cerebral and intestinal blood flow velocity in preterm infants. Pediatrics 2002; 109: 784-787. (Pubitemid 34493343)
78. Chang J, Gray PH. Aminophylline therapy and cerebral blood flow velocity in preterm infants. J Paediatr Child Health 1994; 30: 123-125. (Pubitemid 24103111)
79. Schmidt B, Roberts RS, Davis P, Doyle LW, Barrington KJ, Ohlsson A, Caffeine for Apnea of Prematurity Trial Group et al. Long-term effects of caffeine therapy for apnea of prematurity. N Engl J Med 2007; 357: 1893-1902. (Pubitemid 350074685)
80. Schmidt B, Roberts RS, Davis P, Doyle LW, Barrington KJ, Ohlsson A, Caffeine for Apnea of Prematurity Trial Group et al. Caffeine therapy for apnea of prematurity. N Engl J Med 2006; 354: 2112-2121.
81. Back SA, Craig A, Luo NL, Ren J, Akundi RS, Ribeiro I et al. Protective effects of caffeine on chronic hypoxia-induced perinatal white matter injury. Ann Neurol 2006; 60: 696-705. (Pubitemid 46048487)
82. Boutilier RG. Mechanisms of cell survival in hypoxia and hypothermia. J Exp Biol 2001; 204: 3171-3181. (Pubitemid 34861359)
83. Dunwiddie TV, Masino SA. The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 2001; 24: 31-55. (Pubitemid 32695222)
84. Mayer CA, Haxhiu MA, Martin RJ, Wilson CG. Adenosine A2A receptors mediate GABAergic inhibition of respiration in immature rats. J Appl Physiol 2006; 100: 91-97. (Pubitemid 43671094)
85. Zaidi SI, Jafri A, Martin RJ, Haxhiu MA. Adenosine A2A receptors are expressed by GABAergic neurons of medulla oblongata in developing rat. Brain Res 2006; 1071: 42-53. (Pubitemid 43255474)
86. Barrington KJ, Finer NN, Peters KL, Barton J. Physiologic effects of doxapram in idiopathic apnea of prematurity. J Pediatr 1986; 108: 124-129. (Pubitemid 16126049)
87. Mitchell RA, Herbert DA. Potencies of doxapram and hypoxia in stimulating carotidbody chemoreceptors and ventilation in anesthetized cats. Anesthesiology 1975; 42: 559-566.
88. Brion LP, Vega-Rich C, Reinersman G, Roth P. Low-dose doxapram for apnea unresponsive to aminophylline in very low birthweight infants. J Perinatol 1991; 11: 359-364.
89. Peliowski A, Finer NN. A blinded, randomized, placebo-controlled trial to compare theophylline and doxapram for the treatment of apnea of prematurity. Pediatr 1990; 116: 648-653. (Pubitemid 20124167)
90. Kattwinkel J, Nearman HS, Fanaroff AA, Katona PG, Klaus MH. Apnea of prematurity. Comparative therapeutic effects of cutaneous stimulation and nasal continuous positive airway pressure. J Pediatr 1975; 86: 588-592.
91. Miller MJ, Carlo WA, Martin RF. Continuous positive airway pressure selectively reduces obstructive apnea in preterm infants. J Pediatr 1985; 106: 91-94. (Pubitemid 15189918)
92. Kosch PC, Stark AR. Dynamic maintenance of end-expiratory lung volume in full-term infants. J Appl Physiol 1984; 57: 1126-1133. (Pubitemid 15211203)
93. Stark AR, Cohlan BA, Waggener TB, Frantz III ID, Kosch PC. Regulation of end-expiratory lung volume during sleep in premature infants. J Appl Physiol 1987; 62: 1117-1123. (Pubitemid 17073911)
94. Mathew OP, Sant'Ambrogio G, Fisher JT, Sant'Ambrogio FB. Laryngeal pressure receptors. Respir Physiol 1984; 57: 113-122. (Pubitemid 14061906)
95. Kubicka ZJ, Limauro J, Darnall RA. Heated, humidified high-flow nasal cannula therapy: yet another way to deliver continuous positive airway pressure? Pediatrics 2008; 121: 82-88.
96. Sreenan C, Lemke RP, Hudson-Mason A, Osiovich H. High-flow nasal cannulae in the management of apnea of prematurity: a comparison with conventional nasal continuous positive airway pressure. Pediatrics 2001; 107: 1081-1083. (Pubitemid 32440615)
97. Marlier L, Gaugler C, Messer J. Olfactory stimulation prevents apnea in premature newborns. Pediatrics 2005; 115: 83-88. (Pubitemid 43050894)
98. Al-Saif S, Alvaro R, Manfreda J, Kwiatkowski K, Cates D, Qurashi M et al. A randomized controlled trial of theophylline versus CO2 inhalation for treating apnea of prematurity. J Pediatr 2008; 153: 513-518.
99. Bloch-Salisbury E, Indic P, Bednarek F, Paydarfar D. Stabilizing immature breathing patterns of preterm infants using stochastic mechanosensory stimulation. J Appl Physiol 2009; 107: 1017-1027.
100. Ramanathan R, Corwin MJ, Hunt CE, Lister G, Tinsley LR, Baird T, Collaborative Home Infant Monitoring Evaluation (CHIME) Study Group et al. Cardiorespiratory events recorded on home monitors: Comparison of healthy infants with those at increased risk for SIDS. JAMA 2001; 285: 2199-2207. (Pubitemid 32416765)
101. Henderson-Smart DJ, Pettigrew AG, Campbell DJ. Clinical apnea and brain-stem neural function in preterm infants. N Engl J Med 1983; 308: 353-357. (Pubitemid 13187216)
102. Eichenwald EC, Aina A, Stark AR. Apnea frequently persists beyond term gestation in infants delivered at 24 to 28 weeks. Pediatrics 1997; 100: 354-359.
103. Zacharia A, Zimine S, Lovblad KO, Warfield S, Thoeny H, Ozdoba C et al. Early assessment of brain maturation by MR imaging segmentation in neonates and premature infants. Am J Neuroradiol 2006; 27: 972-977. (Pubitemid 44897670)
104. Inder TE, Warfield SK, Wang H, Hüppi PS, Volpe JJ. Abnormal cerebral structure is present at term in premature infants. Pediatrics 2005; 115: 286-294. (Pubitemid 43193809)