Skip to main content
Top
Published in: Pediatric Radiology 8/2014

01-08-2014 | Original Article

Diffusion tensor imaging in extremely low birth weight infants managed with hypercapnic vs. normocapnic ventilation

Authors: Xiawei Ou, Charles M. Glasier, Raghu H. Ramakrishnaiah, Teresita L. Angtuaco, Sarah B. Mulkey, Zhaohua Ding, Jeffrey R. Kaiser

Published in: Pediatric Radiology | Issue 8/2014

Login to get access

Abstract

Background

Permissive hypercapnia is a ventilatory strategy used to prevent lung injury in ventilated extremely low birth weight (ELBW, birth weight ≤1,000 g) infants. However, there is retrospective evidence showing that high CO2 is associated with brain injury.

Objective

The objective of this study was to compare brain white matter development at term-equivalent age in ELBW infants randomized to hypercapnic vs. normocapnic ventilation during the first week of life and in healthy non-ventilated term newborns.

Materials and methods

Twenty-two ELBW infants from a randomized controlled trial were included in this study; 11 received hypercapnic (transcutaneous PCO2 [tcPCO2] 50–60 mmHg) ventilation and 11 normocapnic (tcPCO2 35–45 mmHg) ventilation during the first week of life while still intubated. In addition, ten term healthy newborns served as controls. Magnetic resonance imaging (MRI) with diffusion tensor imaging (DTI) was performed at term-equivalent age for the ELBW infants and at approximately 2 weeks of age for the control infants. White matter injury on conventional MRI was graded in the ELBW and control infants using a scoring system adopted from literature. Tract-based spatial statistics (TBSS) was used to evaluate for differences in DTI measured fractional anisotropy (FA, spatially normalized to a customized template) among the ELBW and term control infants.

Results

Conventional MRI white matter scores were not different (7.3 ± 1.7 vs. 6.9 ± 1.4, P = 0.65) between the hypercapnic and normocapnic ELBW infants. TBSS analysis did not show significant differences (P < 0.05, corrected) between the two ELBW infant groups, although before multiple comparisons correction, hypercapnic infants had many regions with lower FA and no regions with higher FA (P < 0.05, uncorrected) compared to normocapnic infants. When compared to the control infants, normocapnic ELBW infants had a few small regions with significantly lower FA, while hypercapnic ELBW infants had more widespread regions with significantly lower FA (P < 0.05, fully corrected for multiple comparisons).

Conclusions

Normocapnic ventilation vs. permissive hypercapnia may be associated with improved white matter development at term-equivalent age in ELBW infants. This effect, however, was small and was not apparent on conventional MRI. Further research is needed using larger sample sizes to assess if permissive hypercapnic ventilation in ELBW infants is associated with worse white matter development.
Literature
1.
go back to reference Martin JA, Hamilton BE, Ventura SJ et al (2012) Births: final data for 2010. Natl Vital Stat Rep 61:1–71 Martin JA, Hamilton BE, Ventura SJ et al (2012) Births: final data for 2010. Natl Vital Stat Rep 61:1–71
2.
go back to reference Thome UH, Ambalavanan N (2009) Permissive hypercapnia to decrease lung injury in ventilated preterm neonates. Semin Fetal Neonatal Med 14:21–27PubMedCrossRef Thome UH, Ambalavanan N (2009) Permissive hypercapnia to decrease lung injury in ventilated preterm neonates. Semin Fetal Neonatal Med 14:21–27PubMedCrossRef
4.
go back to reference Mariani G, Cifuentes J, Carlo WA (1999) Randomized trial of permissive hypercapnia in preterm infants. Pediatrics 104:1082–1088PubMedCrossRef Mariani G, Cifuentes J, Carlo WA (1999) Randomized trial of permissive hypercapnia in preterm infants. Pediatrics 104:1082–1088PubMedCrossRef
5.
go back to reference Carlo WA, Stark AR, Wright LL et al (2002) Minimal ventilation to prevent bronchopulmonary dysplasia in extremely-low-birth-weight infants. J Pediatr 141:370–374PubMedCrossRef Carlo WA, Stark AR, Wright LL et al (2002) Minimal ventilation to prevent bronchopulmonary dysplasia in extremely-low-birth-weight infants. J Pediatr 141:370–374PubMedCrossRef
6.
go back to reference Thome UH, Carroll W, Wu TJ et al (2006) Outcome of extremely preterm infants randomized at birth to different PaCO2 targets during the first seven days of life. Biol Neonate 90:218–225PubMedCrossRef Thome UH, Carroll W, Wu TJ et al (2006) Outcome of extremely preterm infants randomized at birth to different PaCO2 targets during the first seven days of life. Biol Neonate 90:218–225PubMedCrossRef
7.
8.
go back to reference Fujimoto S, Togari H, Yamaguchi N et al (1994) Hypocapnia and cystic periventricular leukomalacia in premature-infants. Arch Dis Child 71:F107–F110PubMedCrossRef Fujimoto S, Togari H, Yamaguchi N et al (1994) Hypocapnia and cystic periventricular leukomalacia in premature-infants. Arch Dis Child 71:F107–F110PubMedCrossRef
9.
go back to reference Okumura A, Hayakawa F, Kato T et al (2001) Hypocarbia in preterm infants with periventricular leukomalacia: the relation between hypocarbia and mechanical ventilation. Pediatrics 107:469–475PubMedCrossRef Okumura A, Hayakawa F, Kato T et al (2001) Hypocarbia in preterm infants with periventricular leukomalacia: the relation between hypocarbia and mechanical ventilation. Pediatrics 107:469–475PubMedCrossRef
10.
go back to reference Wiswell TE, Graziani LJ, Kornhauser MS et al (1996) Effects of hypocarbia on the development of cystic periventricular leukomalacia in premature infants treated with high-frequency jet ventilation. Pediatrics 98:918–924PubMed Wiswell TE, Graziani LJ, Kornhauser MS et al (1996) Effects of hypocarbia on the development of cystic periventricular leukomalacia in premature infants treated with high-frequency jet ventilation. Pediatrics 98:918–924PubMed
11.
go back to reference Kaiser JR, Gauss CH, Pont MM et al (2006) Hypercapnia during the first 3 days of life is associated with severe intraventricular hemorrhage in very low birth weight infants. J Perinatol 26:279–285PubMedCrossRef Kaiser JR, Gauss CH, Pont MM et al (2006) Hypercapnia during the first 3 days of life is associated with severe intraventricular hemorrhage in very low birth weight infants. J Perinatol 26:279–285PubMedCrossRef
12.
go back to reference Fabres J, Carlo WA, Phillips V et al (2007) Both extremes of arterial carbon dioxide pressure and the magnitude of fluctuations in arterial carbon dioxide pressure are associated with severe intraventricular hemorrhage in preterm infants. Pediatrics 119:299–305PubMedCrossRef Fabres J, Carlo WA, Phillips V et al (2007) Both extremes of arterial carbon dioxide pressure and the magnitude of fluctuations in arterial carbon dioxide pressure are associated with severe intraventricular hemorrhage in preterm infants. Pediatrics 119:299–305PubMedCrossRef
13.
go back to reference Perlman JM (1998) White matter injury in the preterm infant: an important determination of abnormal neurodevelopment outcome. Early Hum Dev 53:99–120PubMedCrossRef Perlman JM (1998) White matter injury in the preterm infant: an important determination of abnormal neurodevelopment outcome. Early Hum Dev 53:99–120PubMedCrossRef
14.
go back to reference Volpe JJ (2001) Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res 50:553–562PubMedCrossRef Volpe JJ (2001) Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res 50:553–562PubMedCrossRef
15.
go back to reference Volpe JJ (2001) Neurology of the newborn, 4th edn. W.B. Saunders Co., Philadelphia Volpe JJ (2001) Neurology of the newborn, 4th edn. W.B. Saunders Co., Philadelphia
16.
go back to reference Childs AM, Cornette L, Ramenghi LA et al (2001) Magnetic resonance and cranial ultrasound characteristics of periventricular white matter abnormalities in newborn infants. Clin Radiol 56:647–655PubMedCrossRef Childs AM, Cornette L, Ramenghi LA et al (2001) Magnetic resonance and cranial ultrasound characteristics of periventricular white matter abnormalities in newborn infants. Clin Radiol 56:647–655PubMedCrossRef
17.
go back to reference Debillon T, N’Guyen S, Muet A et al (2003) Limitations of ultrasonography for diagnosing white matter damage in preterm infants. Arch Dis Child Fetal Neonatal Ed 88:F275–F279PubMedCentralPubMedCrossRef Debillon T, N’Guyen S, Muet A et al (2003) Limitations of ultrasonography for diagnosing white matter damage in preterm infants. Arch Dis Child Fetal Neonatal Ed 88:F275–F279PubMedCentralPubMedCrossRef
18.
go back to reference Inder TE, Anderson NJ, Spencer C et al (2003) White matter injury in the premature infant: a comparison between serial cranial sonographic and MR findings at term. AJNR Am J Neuroradiol 24:805–809PubMed Inder TE, Anderson NJ, Spencer C et al (2003) White matter injury in the premature infant: a comparison between serial cranial sonographic and MR findings at term. AJNR Am J Neuroradiol 24:805–809PubMed
19.
go back to reference Miller SP, Cozzio CC, Goldstein RB et al (2003) Comparing the diagnosis of white matter injury in premature newborns with serial MR imaging and transfontanel ultrasonography findings. AJNR Am J Neuroradiol 24:1661–1669PubMed Miller SP, Cozzio CC, Goldstein RB et al (2003) Comparing the diagnosis of white matter injury in premature newborns with serial MR imaging and transfontanel ultrasonography findings. AJNR Am J Neuroradiol 24:1661–1669PubMed
21.
go back to reference Inder T, Huppi PS, Zientara GP et al (1999) Early detection of periventricular leukomalacia by diffusion-weighted magnetic resonance imaging techniques. J Pediatr 134:631–634PubMedCrossRef Inder T, Huppi PS, Zientara GP et al (1999) Early detection of periventricular leukomalacia by diffusion-weighted magnetic resonance imaging techniques. J Pediatr 134:631–634PubMedCrossRef
22.
go back to reference Nakayama N, Okumura A, Shinoda J et al (2006) Evidence for white matter disruption in traumatic brain injury without macroscopic lesions. J Neurol Neurosurg Psychiatry 77:850–855PubMedCentralPubMedCrossRef Nakayama N, Okumura A, Shinoda J et al (2006) Evidence for white matter disruption in traumatic brain injury without macroscopic lesions. J Neurol Neurosurg Psychiatry 77:850–855PubMedCentralPubMedCrossRef
23.
go back to reference Arzoumanian Y, Mirmiran M, Barnes PD et al (2003) Diffusion tensor brain imaging findings at term-equivalent age may predict neurologic abnormalities in low birth weight preterm infants. AJNR Am J Neuroradiol 24:1646–1653PubMed Arzoumanian Y, Mirmiran M, Barnes PD et al (2003) Diffusion tensor brain imaging findings at term-equivalent age may predict neurologic abnormalities in low birth weight preterm infants. AJNR Am J Neuroradiol 24:1646–1653PubMed
24.
go back to reference Dudink J, Lequin M, van Pul C et al (2007) Fractional anisotropy in white matter tracts of very-low-birth-weight infants. Pediatr Radiol 37:1216–1223PubMedCentralPubMedCrossRef Dudink J, Lequin M, van Pul C et al (2007) Fractional anisotropy in white matter tracts of very-low-birth-weight infants. Pediatr Radiol 37:1216–1223PubMedCentralPubMedCrossRef
25.
go back to reference Huppi PS, Murphy B, Maier SE et al (2001) Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics 107:455–460PubMedCrossRef Huppi PS, Murphy B, Maier SE et al (2001) Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics 107:455–460PubMedCrossRef
26.
go back to reference Partridge SC, Mukherjee P, Henry RG et al (2004) Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. Neuroimage 22:1302–1314PubMedCrossRef Partridge SC, Mukherjee P, Henry RG et al (2004) Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. Neuroimage 22:1302–1314PubMedCrossRef
27.
go back to reference Anjari M, Srinivasan L, Allsop JM et al (2007) Diffusion tensor imaging with tract-based spatial statistics reveals local white matter abnormalities in preterm infants. Neuroimage 35:1021–1027PubMedCrossRef Anjari M, Srinivasan L, Allsop JM et al (2007) Diffusion tensor imaging with tract-based spatial statistics reveals local white matter abnormalities in preterm infants. Neuroimage 35:1021–1027PubMedCrossRef
28.
go back to reference Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505PubMedCrossRef Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505PubMedCrossRef
29.
go back to reference Woodward LJ, Anderson PJ, Austin NC et al (2006) Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. N Engl J Med 355:685–694PubMedCrossRef Woodward LJ, Anderson PJ, Austin NC et al (2006) Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. N Engl J Med 355:685–694PubMedCrossRef
30.
go back to reference Skranes J, Vangberg TR, Kulseng S et al (2007) Clinical findings and white matter abnormalities seen on diffusion tensor imaging in adolescents with very low birth weight. Brain 130:654–666PubMedCrossRef Skranes J, Vangberg TR, Kulseng S et al (2007) Clinical findings and white matter abnormalities seen on diffusion tensor imaging in adolescents with very low birth weight. Brain 130:654–666PubMedCrossRef
31.
go back to reference Rose J, Butler EE, Lamont LE et al (2009) Neonatal brain structure on MRI and diffusion tensor imaging, sex, and neurodevelopment in very-low-birthweight preterm children. Dev Med Child Neurol 51:526–535PubMedCrossRef Rose J, Butler EE, Lamont LE et al (2009) Neonatal brain structure on MRI and diffusion tensor imaging, sex, and neurodevelopment in very-low-birthweight preterm children. Dev Med Child Neurol 51:526–535PubMedCrossRef
32.
go back to reference van Kooij BJM, de Vries LS, Ball G et al (2012) Neonatal tract-based spatial statistics findings and outcome in preterm infants. AJNR Am J Neuroradiol 33:188–194PubMedCrossRef van Kooij BJM, de Vries LS, Ball G et al (2012) Neonatal tract-based spatial statistics findings and outcome in preterm infants. AJNR Am J Neuroradiol 33:188–194PubMedCrossRef
33.
go back to reference Deoni SCL, Mercure E, Blasi A et al (2011) Mapping infant brain myelination with magnetic resonance imaging. J Neurosci 31:784–791PubMedCrossRef Deoni SCL, Mercure E, Blasi A et al (2011) Mapping infant brain myelination with magnetic resonance imaging. J Neurosci 31:784–791PubMedCrossRef
34.
go back to reference Kaiser JR, Gauss CH, Williams DK (2004) Surfactant administration acutely affects cerebral and systemic hemodynamics and gas exchange in very-low-birth-weight infants. J Pediatr 144:809–814PubMed Kaiser JR, Gauss CH, Williams DK (2004) Surfactant administration acutely affects cerebral and systemic hemodynamics and gas exchange in very-low-birth-weight infants. J Pediatr 144:809–814PubMed
Metadata
Title
Diffusion tensor imaging in extremely low birth weight infants managed with hypercapnic vs. normocapnic ventilation
Authors
Xiawei Ou
Charles M. Glasier
Raghu H. Ramakrishnaiah
Teresita L. Angtuaco
Sarah B. Mulkey
Zhaohua Ding
Jeffrey R. Kaiser
Publication date
01-08-2014
Publisher
Springer Berlin Heidelberg
Published in
Pediatric Radiology / Issue 8/2014
Print ISSN: 0301-0449
Electronic ISSN: 1432-1998
DOI
https://doi.org/10.1007/s00247-014-2946-8

Other articles of this Issue 8/2014

Pediatric Radiology 8/2014 Go to the issue