Caffeine for apnea of prematurity: Effects on the developing brain

NeuroToxicology

Volumn 58, Issue , 2017, Pages 94-102

  Atik, Anzari ^a   Harding, Richard ^a   De Matteo, Robert ^a   Kondos Devcic, Delphi ^b   Cheong, Jeanie ^c   Doyle, Lex W ^c   Tolcos, Mary ^a,b,d  

^a MONASH UNIVERSITY   (Australia)

^b RMIT UNIVERSITY   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Adenosine; Apnea; Brain; Caffeine; Development; Prematurity

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ADENOSINE; ADENOSINE A2A RECEPTOR; ALPHA 1A ADRENERGIC RECEPTOR; CAFFEINE; CAFFEINE CITRATE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; METHYLXANTHINE; CENTRAL STIMULANT AGENT;

ADVERSE OUTCOME; BRAIN BLOOD FLOW; BRAIN DEVELOPMENT; CENTRAL NERVOUS SYSTEM; CHOLINERGIC TRANSMISSION; COFFEE; COGNITION; DRUG MECHANISM; DRUG SAFETY; DRUG STRUCTURE; FOOD INTAKE; GLUTAMATERGIC SYNAPSE; HUMAN; NERVE STIMULATION; NEUROPROTECTION; NEWBORN APNEA; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; REVIEW; SURVIVAL; SYNAPTIC TRANSMISSION; TREATMENT DURATION; ANIMAL; APNEA; BRAIN; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING;

ANIMALS; APNEA; BRAIN; CAFFEINE; CENTRAL NERVOUS SYSTEM STIMULANTS; HUMANS;

EID: 85002263310     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2016.11.012     Document Type: Review

References (101)

1. Abu-Shaweesh, J.M., Martin, R.J., Neonatal apnea: what's new?. Pediatr. Pulmonol. 43:10 (2008), 937–944.
2. Abu-Shaweesh, J.M., Dreshaj, I.A., Haxhiu, M.A., Martin, R.J., Central GABAergic mechanisms are involved in apnea induced by SLN stimulation in piglets. J. Appl. Physiol. 90:4 (2001), 1570–1576.
3. Abu-Shaweesh, J.M., Activation of central adenosine A(2A) receptors enhances superior laryngeal nerve stimulation-induced apnea in piglets via a GABAergic pathway. J. Appl. Physiol. 103:4 (2007), 1205–1211.
4. Alexander, M., Smith, A.L., Rosenkrantz, T.S., Fitch, R.H., Therapeutic effect of caffeine treatment immediately following neonatal hypoxic-ischemic injury on spatial memory in male rats. Brain Sci. 3:1 (2013), 177–190.
5. Aranda, J.V., Cook, C.E., Gorman, W., Collinge, J.M., Loughnan, P.M., Outerbridge, E.W., Aldridge, A., Neims, A.H., Pharmacokinetic profile of caffeine in the premature newborn infant with apnea. J. Pediatr. 94:4 (1979), 663–668.
6. Atik, A., Cheong, J., Harding, R., Rees, S., De Matteo, R., Tolcos, M., Impact of daily high-dose caffeine exposure on developing white matter of the immature ovine brain. Pediatr. Res. 76:1 (2014), 54–63.
7. Back, S.A., Craig, A., Luo, N.L., Ren, J., Akundi, R.S., Ribeiro, I., Rivkees, S.A., Protective effects of caffeine on chronic hypoxia-induced perinatal white matter injury. Ann. Neurol. 60:6 (2006), 696–705.
8. Barrington, K., Finer, N., The natural history of the appearance of apnea of prematurity. Pediatr. Res. 29:4 Pt 1 (1991), 372–375.
9. Bernstein, G.A., Carroll, M.E., Crosby, R.D., Perwien, A.R., Go, F.S., Benowitz, N.L., Caffeine effects on learning, performance, and anxiety in normal school-age children. J. Am. Acad. Child Adolesc. Psychiatry 33:3 (1994), 407–415.
10. Black, A.M., Pandya, S., Clark, D., Armstrong, E.A., Yager, J.Y., Effect of caffeine and morphine on the developing pre-mature brain. Brain Res. 1219 (2008), 136–142.
11. Bona, E., Aden, U., Fredholm, B.B., Hagberg, H., The effect of long term caffeine treatment on hypoxic-ischemic brain damage in the neonate. Pediatr. Res. 38:3 (1995), 312–318.
12. Bonati, M., Latini, R., Galletti, F., Young, J.F., Tognoni, G., Garattini, S., Caffeine disposition after oral doses. Clin. Pharmacol. Ther. 32:1 (1982), 98–106.
13. Charles, B.G., Townsend, S.R., Steer, P.A., Flenady, V.J., Gray, P.H., Shearman, A., Caffeine citrate treatment for extremely premature infants with apnea: population pharmacokinetics, absolute bioavailability, and implications for therapeutic drug monitoring. Ther. Drug Monit. 30:6 (2008), 709–716.
14. Chen, J.F., Sonsalla, P.K., Pedata, F., Melani, A., Domenici, M.R., Popoli, P., Geiger, J., Lopes, L.V., de Mendonca, A., Adenosine A2A receptors and brain injury: broad spectrum of neuroprotection, multifaceted actions and fine tuning modulation. Prog. Neurobiol. 83:5 (2007), 310–331.
15. Connolly, S., Kingsbury, T.J., Caffeine modulates CREB-dependent gene expression in developing cortical neurons. Biochem. Biophys. Res. Commun. 397:2 (2010), 152–156.
16. Cunha, C., Brambilla, R., Thomas, K.L., A simple role for BDNF in learning and memory?. Front. Mol. Neurosci. 3 (2010), 1–14.
17. Cunha, R.A., Neuroprotection by adenosine in the brain: from A(1) receptor activation to A (2A) receptor blockade. Purinergic Signal 1:2 (2005), 111–134.
18. Dani, C., Bertini, G., Reali, M.F., Tronchin, M., Wiechmann, L., Martelli, E., Rubaltelli, F.F., Brain hemodynamic changes in preterm infants after maintenance dose caffeine and aminophylline treatment. Biol. Neonate 78:1 (2000), 27–32.
19. Desfrere, L., Olivier, P., Schwendimann, L., Verney, C., Gressens, P., Transient inhibition of astrocytogenesis in developing mouse brain following postnatal caffeine exposure. Pediatr. Res. 62:5 (2007), 604–609.
20. Dews, P.B., Caffeine. Annu. Rev. Nutr. 2 (1982), 323–341.
21. Di Fiore, J.M., Martin, R.J., Gauda, E.B., Apnea of prematurity – perfect storm. Respir. Physiol. Neurobiol. 189 (2013), 213–222.
22. Dirnagl, U., Niwa, K., Lindauer, U., Villringer, A., Coupling of cerebral blood flow to neuronal activation: role of adenosine and nitric oxide. Am. J. Physiol. 267:1 Pt 2 (1994), H296–301.
23. Doyle, L.W., Cheong, J., Hunt, R.W., Lee, K.J., Thompson, D.K., Davis, P.G., Rees, S., Anderson, P.J., Inder, T.E., Caffeine and brain development in very preterm infants. Ann. Neurol. 68:5 (2010), 734–742.
24. Doyle, L.W., Roberts, G., Anderson, P.J., Stu, V.I.C., Outcomes at age 2 years of infants <28 weeks' gestational age born in Victoria in 2005. J. Pediatr. 156:1 (2010), 49–U84.
25. Dunwiddie, T.V., Masino, S.A., The role and regulation of adenosine in the central nervous system. Annu. Rev. Neurosci. 24 (2001), 31–55.
26. Dunwiddie, T.V., Worth, T., Sedative and anticonvulsant effects of adenosine analogs in mouse and rat. J. Pharmacol. Exp. Ther. 220:1 (1982), 70–76.
27. Elkins, R.N., Rapoport, J.L., Zahn, T.P., Buchsbaum, M.S., Weingartner, H., Kopin, I.J., Langer, D., Johnson, C., Acute effects of caffeine in normal prepubertal boys. Am. J. Psychiatry 138:2 (1981), 178–183.
28. Etzel, B.A., Guillet, R., Effects of neonatal exposure to caffeine on adenosine A1 receptor ontogeny using autoradiography. Brain Res. Dev. Brain Res. 82:1–2 (1994), 223–230.
29. Fanaroff, A.A., Stoll, B.J., Wright, L.L., Carlo, W.A., Ehrenkranz, R.A., Stark, A.R., Bauer, C.R., Donovan, E.F., Korones, S.B., Laptook, A.R., Lemons, J.A., Oh, W., Papile, L.A., Shankaran, S., Stevenson, D.K., Tyson, J.E., Poole, W.K., Trends in neonatal morbidity and mortality for very low birthweight infants. Am. J. Obstet. Gynecol. 196:2 (2007), e141–e148 147.
30. Fastbom, J., Pazos, A., Palacios, J.M., The distribution of adenosine A1 receptors and 5'-nucleotidase in the brain of some commonly used experimental animals. Neuroscience 22:3 (1987), 813–826.
31. Fink, J.S., Weaver, D.R., Rivkees, S.A., Peterfreund, R.A., Pollack, A.E., Adler, E.M., Reppert, S.M., Molecular cloning of the rat A2 adenosine receptor: selective co-expression with D2 dopamine receptors in rat striatum. Brain Res. Mol. Brain Res. 14:3 (1992), 186–195.
32. Fisone, G., Borgkvist, A., Usiello, A., Caffeine as a psychomotor stimulant: mechanism of action. Cell. Mol. Life Sci. 61:7–8 (2004), 857–872.
33. Fredholm, B.B., Battig, K., Holmen, J., Nehlig, A., Zvartau, E.E., Actions of caffeine in the brain with special reference to factors that contribute to its widespread use. Pharmacol. Rev. 51:1 (1999), 83–133.
34. Fredholm, B.B., Astra Award Lecture. Adenosine, adenosine receptors and the actions of caffeine. Pharmacol. Toxicol. 76:2 (1995), 93–101.
35. Fredholm, B.B., Methylxanthines. Hofmann, F.B., (eds.) Handbook of Experimental Pharmacology, 2011, Springer, Heidelberg, 1–559.
36. Fuller, G.N., Wiggins, R.C., A possible effect of the methylxanthines caffeine, theophylline and aminophylline on postnatal myelination of the rat brain. Brain Res. 213:2 (1981), 476–480.
37. Fuller, G.N., Divakaran, P., Wiggins, R.C., The effect of postnatal caffeine administration on brain myelination. Brain Res. 249:1 (1982), 189–191.
38. Gaytan, S.P., Pasaro, R., Neonatal caffeine treatment up-regulates adenosine receptors in brainstem and hypothalamic cardio-respiratory related nuclei of rat pups. Exp. Neurol. 237:2 (2012), 247–259.
39. Gomes, C., Ferreira, R., George, J., Sanches, R., Rodrigues, D.I., Goncalves, N., Cunha, R.A., Activation of microglial cells triggers a release of brain-derived neurotrophic factor (BDNF) inducing their proliferation in an adenosine A2A receptor-dependent manner: a2A receptor blockade prevents BDNF release and proliferation of microglia. J. Neuroinflammation 10 (2013), 1–13.
40. Goodman, R.R., Synder, S.H., Autoradiographic localization of adenosine receptors in rat brain using [3H]cyclohexyladenosine. J. Neurosci. 2:9 (1982), 1230–1241.
41. Gray, P.H., Flenady, V.J., Charles, B.G., Steer, P.A., Grp, C.C.S., Caffeine citrate for very preterm infants: effects on development, temperament and behaviour. J. Paediatr. Child Health 47:4 (2011), 167–172.
42. Guillet, R., Dunham, L., Neonatal caffeine exposure and seizure susceptibility in adult rats. Epilepsia 36:8 (1995), 743–749.
43. Guillet, R., Kellogg, C., Neonatal exposure to therapeutic caffeine alters the ontogeny of adenosine A1 receptors in brain of rats. Neuropharmacology 30:5 (1991), 489–496.
44. Harding, R., Function of the larynx in the fetus and newborn. Annu. Rev. Physiol. 46 (1984), 645–659.
45. Henderson-Smart, D.J., De Paoli, A.G., Methylxanthine treatment for apnoea in preterm infants. Cochrane Database Syst. Rev., 2010, CD000140.
46. Henderson-Smart, D.J., Steer, P.A., Caffeine versus theophylline for apnea in preterm infants. Cochrane Database Syst. Rev., 2010, CD000273.
47. Henderson-Smart, D.J., The effect of gestational age on the incidence and duration of recurrent apnoea in newborn babies. Aust. Paediatr. J. 17:4 (1981), 273–276.
48. Herlenius, E., Lagercrantz, H., Adenosinergic modulation of respiratory neurones in the neonatal rat brainstem in vitro. J. Physiol. 518:Pt (1) (1999), 159–172.
49. Herlenius, E., Aden, U., Tang, L.Q., Lagercrantz, H., Perinatal respiratory control and its modulation by adenosine and caffeine in the rat. Pediatr. Res. 51:1 (2002), 4–12.
50. Johansson, B., Ahlberg, S., van der Ploeg, I., Brene, S., Lindefors, N., Persson, H., Fredholm, B.B., Effect of long term caffeine treatment on A1 and A2 adenosine receptor binding and on mRNA levels in rat brain. Naunyn. Schmiedebergs Arch. Pharmacol. 347:4 (1993), 407–414.
51. Juarez-Mendez, S., Carretero, R., Martinez-Tellez, R., Silva-Gomez, A.B., Flores, G., Neonatal caffeine administration causes a permanent increase in the dendritic length of prefrontal cortical neurons of rats. Synapse 60:6 (2006), 450–455.
52. Kang, S.H., Lee, Y.A., Won, S.J., Rhee, K.H., Gwag, B.J., Caffeine-induced neuronal death in neonatal rat brain and cortical cell cultures. Neuroreport 13:15 (2002), 1945–1950.
53. Katheria, A.C., Sauberan, J.B., Akotia, D., Rich, W., Durham, J., Finer, N.N., A pilot randomized controlled trial of early versus routine caffeine in extremely premature infants. Am. J. Perinatol. 32:9 (2015), 879–886.
54. Ko, K.R., Ngai, A.C., Winn, H.R., Role of adenosine in regulation of regional cerebral blood flow in sensory cortex. Am. J. Physiol. 259:6 Pt 2 (1990), H1703–H1708.
55. Lachance, M.P., Marlowe, C., Waddell, W.J., Autoradiographic disposition of [1-methyl-14C]- and [2–14C]caffeine in mice. Toxicol. Appl. Pharmacol. 71:2 (1983), 237–241.
56. Larsen, P.B., Brendstrup, L., Skov, L., Flachs, H., Aminophylline versus caffeine citrate for apnea and bradycardia prophylaxis in premature neonates. Acta Paediatr. 84:4 (1995), 360–364.
57. Latini, S., Pedata, F., Adenosine in the central nervous system: release mechanisms and extracellular concentrations. J. Neurochem. 79:3 (2001), 463–484.
58. Lazarus, M., Shen, H.Y., Cherasse, Y., Qu, W.M., Huang, Z.L., Bass, C.E., Winsky-Sommerer, R., Semba, K., Fredholm, B.B., Boison, D., Hayaishi, O., Urade, Y., Chen, J.F., Arousal effect of caffeine depends on adenosine A2A receptors in the shell of the nucleus accumbens. J. Neurosci. 31:27 (2011), 10067–10075.
59. Marret, S., Delpech, B., Girard, N., Leroy, A., Maingonnat, C., Menard, J.F., Fessard, C., Caffeine decreases glial cell number and increases hyaluronan secretion in newborn rat brain cultures. Pediatr. Res. 34:6 (1993), 716–719.
60. Martin, R.J., Wilson, C.G., Apnea of prematurity. Comp. Physiol. 2:4 (2012), 2923–2931.
61. Martin, R.J., Abu-Shaweesh, J.M., Baird, T.M., Apnoea of prematurity. Paediatr. Respir. Rev. 5:Suppl. (A) (2004), S377–S382.
62. Mathew, O.P., Apnea of prematurity: pathogenesis and management strategies. J. Perinatol. 31:5 (2011), 302–310.
63. Mayer, C.A., Haxhiu, M.A., Martin, R.J., Wilson, C.G., Adenosine A2A receptors mediate GABAergic inhibition of respiration in immature rats. J. Appl. Physiol. (1985) 100:1 (2006), 91–97.
64. McPherson, C., Neil, J.J., Tjoeng, T.H., Pineda, R., Inder, T.E., A pilot randomized trial of high-dose caffeine therapy in preterm infants. Pediatr. Res. 78:2 (2015), 198–204.
65. Millar, D., Schmidt, B., Controversies surrounding xanthine therapy. Semin. Neonatol. 9:3 (2004), 239–244.
66. Miller, M.J., Martin, R.J., Pathophysiology of Apnea of Prematurity. 4th ed., 2011, Elsevier Saunders.
67. Milner, A.D., Boon, A.W., Saunders, R.A., Hopkin, I.E., Upper airways obstruction and apnoea in preterm babies. Arch. Dis. Child. 55:1 (1980), 22–25.
68. Morton, S.U., Smith, V.C., Treatment options for apnoea of prematurity. Arch. Dis. Child. Fetal. Neonatal. Ed. 101:4 (2016), F352–356.
69. Orr, A.G., Orr, A.L., Li, X.J., Gross, R.E., Traynelis, S.F., Adenosine A(2A) receptor mediates microglial process retraction. Nat. Neurosci. 12:7 (2009), 872–878.
70. Pan, H.Z., Chen, H.H., Hyperalgesia, low-anxiety, and impairment of avoidance learning in neonatal caffeine-treated rats. Psychopharmacology (Berl.) 191:1 (2007), 119–125.
71. Portas, C.M., Thakkar, M., Rainnie, D.G., Greene, R.W., McCarley, R.W., Role of adenosine in behavioral state modulation: a microdialysis study in the freely moving cat. Neuroscience 79:1 (1997), 225–235.
72. Prediger, R.D., Pamplona, F.A., Fernandes, D., Takahashi, R.N., Caffeine improves spatial learning deficits in an animal model of attention deficit hyperactivity disorder (ADHD) – the spontaneously hypertensive rat (SHR). Int. J. Neuropsychopharmacol. 8:4 (2005), 583–594.
73. Rainnie, D.G., Grunze, H.C., McCarley, R.W., Greene, R.W., Adenosine inhibition of mesopontine cholinergic neurons: implications for EEG arousal. Science 263:5147 (1994), 689–692.
74. Rapoport, J.L., Jensvold, M., Elkins, R., Buchsbaum, M.S., Weingartner, H., Ludlow, C., Zahn, T.P., Berg, C.J., Neims, A.H., Behavioral and cognitive effects of caffeine in boys and adult males. J. Nerv. Ment. Dis. 169:11 (1981), 726–732.
75. Rebola, N., Simoes, A.P., Canas, P.M., Tome, A.R., Andrade, G.M., Barry, C.E., Agostinho, P.M., Lynch, M.A., Cunha, R.A., Adenosine A2A receptors control neuroinflammation and consequent hippocampal neuronal dysfunction. J. Neurochem. 117:1 (2011), 100–111.
76. Reppert, S.M., Weaver, D.R., Stehle, J.H., Rivkees, S.A., Molecular cloning and characterization of a rat A1-adenosine receptor that is widely expressed in brain and spinal cord. Mol. Endocrinol. 5:8 (1991), 1037–1048.
77. Rivkees, S.A., Wendler, C.C., Adverse and protective influences of adenosine on the newborn and embryo: implications for preterm white matter injury and embryo protection. Pediatr. Res. 69:4 (2011), 271–278.
78. Rivkees, S.A., The ontogeny of cardiac and neural A1 adenosine receptor expression in rats. Brain Res. Dev. Brain Res. 89:2 (1995), 202–213.
79. Robertson, C.M., Watt, M.J., Dinu, I.A., Outcomes for the extremely premature infant: what is new? And where are we going?. Pediatr. Neurol. 40:3 (2009), 189–196.
80. Satoh, S., Matsumura, H., Koike, N., Tokunaga, Y., Maeda, T., Hayaishi, O., Region-dependent difference in the sleep-promoting potency of an adenosine A2A receptor agonist. Eur. J. Neurosci. 11:5 (1999), 1587–1597.
81. Scanlon, J.E., Chin, K.C., Morgan, M.E., Durbin, G.M., Hale, K.A., Brown, S.S., Caffeine or theophylline for neonatal apnoea?. Arch. Dis. Child. 67:Spec No (4) (1992), 425–428.
82. Schiffmann, S.N., Jacobs, O., Vanderhaeghen, J.J., Striatal restricted adenosine A2 receptor (RDC8) is expressed by enkephalin but not by substance P neurons: an in situ hybridization histochemistry study. J. Neurochem. 57:3 (1991), 1062–1067.
83. Schmidt, B., Roberts, R.S., Davis, P., Doyle, L.W., Barrington, K.J., Ohlsson, A., Solimano, A., Tin, W., Caffeine for Apnea of Prematurity Trial G, Caffeine therapy for apnea of prematurity. N. Engl. J. Med. 354:20 (2006), 2112–2121.
84. Schmidt, B., Roberts, R.S., Davis, P., Doyle, L.W., Barrington, K.J., Ohlsson, A., Solimano, A., Tin, W., Caffeine for Apnea of Prematurity Trial G, Long-term effects of caffeine therapy for apnea of prematurity. N. Engl. J. Med. 357:19 (2007), 1893–1902.
85. Schmidt, B., Anderson, P.J., Doyle, L.W., Dewey, D., Grunau, R.E., Asztalos, E.V., Davis, P.G., Tin, W., Moddemann, D., Solimano, A., Ohlsson, A., Barrington, K.J., Roberts, R.S., Tri, C.A.P.C., Survival without disability to age 5 years after neonatal caffeine therapy for apnea of prematurity. J. Am. Med. Assoc. 307:3 (2012), 275–282.
86. Schmidt, B., Davis, P.G., Roberts, R.S., Timing of caffeine therapy in very low birth weight infants. J. Pediatr. 164:5 (2014), 957–958.
87. Steer, P.A., Flenady, V.J., Shearman, A., Lee, T.C., Tudehope, D.I., Charles, B.G., Periextubation caffeine in preterm neonates: a randomized dose response trial. J. Paediatr. Child Health 39:7 (2003), 511–515.
88. Stevens, B., Porta, S., Haak, L.L., Gallo, V., Fields, R.D., Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36:5 (2002), 855–868.
89. Supcun, S., Kutz, P., Pielemeier, W., Roll, C., Caffeine increases cerebral cortical activity in preterm infants. J. Pediatr. 156:3 (2010), 490–491.
90. Swanson, T.H., Drazba, J.A., Rivkees, S.A., Adenosine A1 receptors are located predominantly on axons in the rat hippocampal formation. J. Comp. Neurol. 363:4 (1995), 517–531.
91. Tomimatsu, T., Lee, S.J., Pena, J.P., Ross, J.M., Lang, J.A., Longo, L.D., Maternal caffeine administration and cerebral oxygenation in near-term fetal sheep. Reprod. Sci. 14:6 (2007), 588–594.
92. Tracy, M.B., Klimek, J., Hinder, M., Ponnampalam, G., Tracy, S.K., Does caffeine impair cerebral oxygenation and blood flow velocity in preterm infants?. Acta Paediatr. (Oslo, Norway: 1992) 99:9 (2010), 1319–1323.
93. Turner, C.P., Pulciani, D., Rivkees, S.A., Reduction in intracellular calcium levels induces injury in developing neurons. Exp. Neurol. 178:1 (2002), 21–32.
94. Turner, C.P., Yan, H., Schwartz, M., Othman, T., Rivkees, S.A., A1 adenosine receptor activation induces ventriculomegaly and white matter loss. Neuroreport 13:9 (2002), 1199–1204.
95. Valdez, R.C., Ahlawat, R., Wills-Karp, M., Nathan, A., Ezell, T., Gauda, E.B., Correlation between serum caffeine levels and changes in cytokine profile in a cohort of preterm infants. J. Pediatr. 158:1 (2011), 57–64 (e51).
96. Wilson, C.G., Martin, R.J., Jaber, M., Abu-Shaweesh, J., Jafri, A., Haxhiu, M.A., Zaidi, S., Adenosine A2A receptors interact with GABAergic pathways to modulate respiration in neonatal piglets. Respir. Physiol. Neurobiol. 141:2 (2004), 201–211.
97. Yazdani, M., Hartman, A.D., Miller, H.I., Temples, T.E., Nakamoto, T., Chronic caffeine intake alters the composition of various parts of the brain in young growing rats. Dev. Pharmacol. Ther. 11:2 (1988), 102–108.
98. Yazdani, M., Ide, K., Asadifar, M., Gottschalk, S., Joseph, F. Jr., Nakamoto, T., Effects of caffeine on the saturated and monounsaturated Fatty acids of the newborn rat cerebellum. Ann. Nutr. Metab. 48:2 (2004), 79–83.
99. Zaidi, S.I., Jafri, A., Martin, R.J., Haxhiu, M.A., Adenosine A2A receptors are expressed by GABAergic neurons of medulla oblongata in developing rat. Brain Res. 1071:1 (2006), 42–53.
100. Zimmerberg, B., Carr, K.L., Scott, A., Lee, H.H., Weider, J.M., The effects of postnatal caffeine exposure on growth, activity and learning in rats. Pharmacol. Biochem. Behav. 39:4 (1991), 883–888.
101. da Silva, R.S., Richetti, S.K., da Silveira, V.G., Battastini, A.M., Bogo, M.R., Lara, D.R., Bonan, C.D., Maternal caffeine intake affects acetylcholinesterase in hippocampus of neonate rats. Int. J. Dev. Neurosci. 26:3–4 (2008), 339–343.