Short- and long-term behavioral effects of exposure to 21%, 40% and 100% oxygen after perinatal hypoxia-ischemia in the rat

International Journal of Developmental Neuroscience

Volumn 29, Issue 6, 2011, Pages 629-638

  Woodworth, K Nina ^a   Palmateer, Julie ^a   Swide, Joseph ^a   Grafe, Marjorie R ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Behavior; Oxygen; Perinatal hypoxia ischemia; Rat

Indexed keywords

OXYGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; FEMALE; HEAD MOVEMENT; HYPOXIC ISCHEMIC ENCEPHALOPATHY; LOCOMOTION; MALE; MOTOR DEVELOPMENT; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NONHUMAN; PERINATAL CARE; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; REFLEX; SENSORIMOTOR BEHAVIOR; SENSORIMOTOR INTEGRATION; SENSORY DYSFUNCTION; TACTILE STIMULATION; TASK PERFORMANCE; TREATMENT OUTCOME; WALKING;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN INJURIES; FEMALE; HUMANS; HYPOXIA-ISCHEMIA, BRAIN; MALE; MOTOR ACTIVITY; MOTOR SKILLS; NEUROPSYCHOLOGICAL TESTS; OXYGEN; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY;

ANIMALIA; RATTUS;

EID: 80052424922     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2011.05.001     Document Type: Article

References (58)

1. Altman J., Sudharshan K. Postnatal development of locomotion in the laboratory rat. Anim. Behav. 1975, 23:896-920.
2. Balduini W., De Angelis V., Mazzoni E., Cimino M. Long-lasting behavioral alterations following a hypoxic-ischemic brain injury in neonatal rats. Brain Res. 2000, 859:318-325.
3. Bhushan V., Paneth N., Kiely J.L. Impact of improved survival of very low birth weight infants on recent secular trends in the prevalence of cerebral palsy. Pediatrics 1993, 91:1094-1100.
4. Bockhorst K.H., Narayana P.A., Dulin J., Liu R., Rea H.C., Hahn K., Wosik J., Perez-Polo J.R. Normobaric hyperoximia increases hypoxia-induced cerebral injury: DTI study in rats. J. Neurosci. Res. 2010, 88:1146-1156.
5. Bona E., Johansson B.B., Hagberg H. Sensorimotor function and neuropathology five to six weeks after hypoxia-ischemia in seven-day-old rats. Pediatr. Res. 1997, 42:678-683.
6. Davis P.G., Tan A., O'donnell C.P.F., Schulze A. Resuscitation of newborn infants with 100% oxygen or air: a systematic review and meta-analysis [see comment]. Lancet 2004, 364:1329-1333.
7. Fabian R., Perez-Polo J.R., Kent T.A. Perivascular nitric oxide and superoxide in neonatal cerebral hypoxia-ischemia. Am. J. Physiol. Heart Circ. Physiol. 2008, 295:H1809-H1814.
8. Felderhoff-Mueser U., Bittigau P., Sifringer M., Jarosz B., Korobowicz E., Mahler L., Piening T., Moysich A., Grune T., Thor F., Heumann R., Buhrer C., Ikonomidou C. Oxygen causes cell death in the developing brain. Neurobiol. Dis. 2004, 17:273-282.
9. Felt B.T., Schallert T., Shao J., Liu Y., Li X., Barks J.D.E. Early appearance of functional deficits after neonatal excitotoxic and hypoxic-ischemin injury: fragile recovery after development and role of the NMDA receptor. Dev. Neurosci. 2002, 24:418-425.
10. Ferrari D.C., Nesic O.B., Perez-Polo J.R. Oxygen resuscitation does not ameliorate neonatal hypoxia/ischemia-induced cerebral edema. J. Neurosci. Res. 2010, 88:2056-2065.
11. Fiskum G., Danilove C.A., Mahrabian Z., Bambrink L.L., Kristian T., Mckenna M.C., Hopkins I., Richards E.M., Rosenthal R.E. Postischemic oxidative stress promotes mitochondrial metabolic failure in neurons and astrocytes. Ann. N.Y. Acad. Sci. 2008, 1147:129-138.
12. Gill M.B., Bockhorst K., Narayana P., Perez-Polo J.R. Bax shuttling after neonatal hypoxia-ischemic: hyperoxia effects. J. Neurosci. Res. 2008, 86:3584-3604.
13. Goplerud J.M., Kim S., Delivoria-Papadopoulos M. The effect of post-asphyxial reoxygenation with 21% vs. 100% oxygen on Na+,K(+)-ATPase activity in striatum of newborn piglets. Brain Res. 1995, 696:161-164.
14. Grafe M.R. Developmental changes in the sensitivity of the neonatal rat brain to hypoxic/ischemic injury. Brain Res. 1994, 653:161-166.
15. Grafe M.R., Woodworth K.N., Noppens K., Perez-Polo J.R. Long-term histological outcome after post-hypoxic treatment with 100% or 40% oxygen in a model of perinatal hypoxic-ischemic brain injury. Int. J. Dev. Neurosci. 2008, 26:119-124.
16. Grow J.L., Liu Y.Q., Barks J.D.E. Can lateralizing sensorimotor deficits be identified after neonatal cerebral hypoxia-ischemia in rats?. Dev. Neurosci. 2003, 25:394-402.
17. Gustavsson M., Anderson M.F., Mallard C., Hagberg H. Hypoxic preconditioning confers long-term reduction of brain injury and improvement of neurological ability in immature rats. Pediatr. Res. 2005, 57:305-309.
18. Himpens E., Van Den Broeck C., Oostra A., Calders P., Vanhaesebrouck P. Prevalence, type, distribution, and severity of cerebral palsy in relation to gestational age: a meta-analytic review. Dev. Med. Child Neurol. 2008, 50:334-340.
19. Hurn P.D., Vannucci S.J., Hagberg H. Adult or perinatal brain injury: does sex matter?. Stroke 2005, 36:193-195.
20. ILCOR The International Liaison Committee on Resuscitation (ILCOR) consensus on science with treatment recommendations for pediatric and neonatal patients: neonatal resuscitation. Pediatrics 2006, 117:e978-e988.
21. Ivacko J., Sun P., Silverstein F.S. Hypoxic-ischemic brain injury induces an acute microglial reaction in perinatal rats. Pediatr. Res. 1996, 39:39-47.
22. Jansen E.M., Low W.C. Long-term effects of neonatal ischemic-hypoxic brain injury on sensorimotor and locomotor tasks in rats. Behav. Brain Res. 1996, 78:189-194.
23. Jantzie L.L., Cheung P.-Y., Obaid L., Emara M., Johnson S.T., Bigam D.L., Todd K.G. Persistent neurochemical changes in neonatal piglets after hypoxia-ischemia and resuscitation with 100%, 21% or 18% oxygen. Resuscitation 2008, 77:111-120.
24. Kattwinkel J., Perlman J.M., Aziz K., Colby C., Fairchild K., Gallagher J., Hazinski M.F., Halamek L.P., Kumar P., Little G., Mcgowan J.E., Nightengale B., Ramirez M.M., Ringer S., Simon W.M., Weiner G.M., Wyckoff M., Zaichen J. Part 15: neonatal resuscitation: 2010 American Heart Association Guidelines for cardiopulmonary resuscitation and emergency cardiovascular care. Circulation 2010, 122:S909-S919.
25. Koch J.D., Miles D.K., Gilley J.A., Yang C.-P., Kernie S.G. Brief exposure to hyperoxia depletes the glial progenitor pool and impairs fundtional recovery after hypoxic-ischemic brain injury. J. Cereb. Blood Flow Metab. 2008, 28:1294-1306.
26. Kuban K.C.K., Leviton A. Cerebral palsy. New Engl. J. Med. 1994, 330:188-195.
27. Lang J.T., Mccullough L.D. Pathways to ischemic neuronal cell death: are sex differences relevant?. J. Transl. Med. 2008, 6:33.
28. Lubics A., Reglodi D., Tamas A., Kiss P., Szalai M., Szalontay L., Lengvari I. Neurological reflexes and early motor behavior in rats subjected to neonatal hypoxic-ischemic injury. Behav. Brain Res. 2005, 157:157-165.
29. Markus T., Hansson S., Amer-Wahlin I., Hellstrom-Westas L., Saugstad O.D., Ley D. Cerebral inflammatory response after fetal asphyxia and hyperoxic resuscitation in newborn sheep. Pediatr. Res. 2007, 62:71-77.
30. Martin S.S., Perez-Polo J.R., Noppens K.M., Grafe M.R. Biphasic changes in the levels of poly(ADP-ribose) polymerase and caspase 3 in the immature brain following hypoxia-ischemia. Int. J. Dev. Neurosci. 2005, 23:673-686.
31. Mcauliffe J.J., Miles L., Vorhees C.V. Adult neurological funciton following neonatal hypoxia-ishcemia in a mouse model of the term neonate: water maze performance is dependent on separable cognitive and motor components. Brain Res. 2006, 1118:208-221.
32. Mouton P.R. Principles and Practices of Unbiased Stereology, An Introduction for Bioscientists 2002, The Johns Hopkins Press, Baltimore.
33. Munkeby B.H., Borke W.B., Bjornland K., Sikkeland L.I.B., Borge G.I.A., Halvorsen B., Saugstad O.D. Resuscitation with 100% O2 increases cerebral injury in hypoxemic piglets. Pediatr. Res. 2004, 56:783-790.
34. Oakden E., Chiswick M., Rothwell N., Loddick S. The influence of litter size on brain damage caused by hypoxic-ischemic injury in the neonatal rat. Pediatr. Res. 2002, 52:692-696.
35. Pazaiti A., Soubasi V., Spandou E., Karkavelas G., Georgiou T., Karalis P., Guiba-Tziampiri O. Evaluation of long-lasting sensorimotor consequences following neonatal hypoxic-ischemic brain injury in rats: the neuroprotective role of MgSO4. Neonatology 2009, 95:33-40.
36. Piecuch R.E., Leonard C.H., Cooper B.A., Kilpatrick S.J., Schlueter M.A., Sola A. Outcome of infants born at 24-26 weeks gestation: II Neurodevelopmental outcome. Obstet. Gynecol. 1997, 90:809-814.
37. Presti A.L., Kishkurno S.V., Slinko S.K., Randis T.M., Ratner V.I., Polin R.A., Ten V.S. Reoxygenation with 100% oxygen versus room air: late neuroanatomical and neurofunctional outcome in neonatal mice with hypoxic-ischemic brai injury. Pediatr. Res. 2006, 60:55-59.
38. Puka-Sundvall M., Gajkowska B., Cholewinski M., Blomgren K., Lazarewicz J.W., Hagberg H. Subcellular distribution of calcium and ultrastructural changes after cerebral hypoxia-ischemia in immature rats. Dev. Brain Res. 2000, 125:31-41.
39. Rice J.E., Vannucci R.C., Brierley J.B. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 1981, 9:131-141.
40. Saugstad O.D. Why are we still using oxygen to resuscitate term infants?. J. Perinatol. 2010, 30:S46-S50.
41. Schallert T., Wishaw I. Neonatal hemidecortication and bilateral cutaneous stimulation in rats. Dev. Psychobiol. 1985, 18:501-514.
42. Schallert T., Woodlee M.T. Orienting and placing. The Behavior of the Laboratory Rat: A Handbook with Tests 2005, 129-140. Oxford University Press, Oxford. I. Wishaw, B. Kolb (Eds.).
43. Schallert T., Woodlee M.T., Fleming S.M. Disentangling multiple types of recovery from brain injury. Pharmacology of Cerebral Ischemic 2002, 201-216. Medpharm Scientific Publishers, Stuttgart. J. Krieglstein, S. Klumpp (Eds.).
44. Shimabuku R., Ota A., Pereyra S., Véliz B., Paz E., Nakachi G., More M., Oliveros M. Hyperoxia with 100% oxygen following hypoxia-ischemic increases brain damage in newborn rats. Biol. Neonate 2005, 88:168-171.
45. Smith K.E., Keeney S., Zhang L., Perez-Polo R., Rassin D.K. The association of early blood oxygenation with child development in preterm infants with acute respiratory disorders. Int. J. Dev. Neurosci. 2008, 26:125-131.
46. Solås A.-B., Kalous P., Saugstad O.D. Reoxygenation with 100 or 21% oxygen after cerebral hypoxemia-ischemia-hypercapnia in newborn piglets. Biol. Neonate 2004, 85:105-111.
47. Stanley F. Survival and cerebral palsy in low birthweight infants: implications for perinatal care. Paediatr. Perinat. Edpidemiol. 1992, 6:298-310.
48. Sweet D.G., Carnielli V., Greisne G., Hallman M., Ozek E., Plavka R., Saugstad O.D., Simeoni U., Speer C.P., Halliday H.L. European consensus guidelines on the managment of neonatal respiratory distress syndrome in preterm infants-2010 update. Neonatology 2010, 97:402-417.
49. Temesvari P., Karg E., Bodi I., Nemeth I., Pinter S., Lazics K., Domoki F., Bari F. Impaired early neurologic outcome in newborn piglets reoxygenated with 100% oxygen compared with room air after pneumothorax-induced asphyxia. Pediatr. Res. 2001, 49:812-819.
50. Ten V.S., Bradley-Moore M., Gingrich J.A., Stark R., Pinsky D.J. Brain injury and neurofunctional deficit in neonatal mice with hypoxic-ischemic encephalopathy. Behav. Brain Res. 2003, 145:209-219.
51. Ten V.S., Wu E.X., Tang H., Bradley-Moore M., Fedarau M.V., Ratner V.I., Stark R.I., Gingrich J.A., Pinsky D.J. Late measures of brain injury after neonatal hypoxia-ischemia in mice. Stroke 2004, 35:2183-2188.
52. Tyree M.M., Dalgard C., O'Neill J.T. Impact of room air resuscitation on early growth response gene-1 in a neonatal piglet model of cerebral hypoxia ischemia. Pediatr. Res. 2006, 59:423-427.
53. Van Den Dungen F.A.M., Van Veenendaal M.B., Mulder A.L.M. Clinical practice: neonatal resuscitation. A Dutch consensus. Eur. J. Pediatr. 2010, 169:521-527.
54. Van Der Kooij M.A., Ohl F., Arndt S.S., Kavelaars A., Van Bel F., Heijnen C.J. Mild neonatal hypoxia-ischemia induces long-term motor- and cognitive impairments in mice. Brain Behav. Immun. 2010, 24:850-856.
55. Vannucci R.C., Connor J.R., Mauger D.T., Palner C., Smith M.B., Towfighi J., Vannucci S. Rat model of perinatal hypoxic-ischemic brain damage. J. Neurosci. Res. 1999, 55:158-163.
56. Vento M., Saugstad O.D. Resuscitation of the term and preterm infant. Semin. Fetal Neonatal Med. 2010, 15:216-222.
57. Wagner B.P., Nedelcu J., Martin E. Delayed postischemic hypothermia improves long-term behavioral outcome after cerebral hypoxia-ischemia in neonatal rats. Pediatr. Res. 2002, 51:354-360.
58. Young R.S.K., Kolonich J., Woods C.L., Yagel S.K. Behavioral performance of rats following neonatal cerebral ischemia. Stroke 1986, 17:1313-1316.