Trends in Outcomes of Major Intracerebral Haemorrhage in a National Cohort of Very Preterm Born Infants in Switzerland
Abstract
:1. Introduction
2. Methods
2.1. Study Design and Population
2.2. Cranial Ultrasound
2.3. Neonatal and Sociodemographic Baseline
2.4. Neurodevelopmental Outcome
2.5. Outcome Definition
2.6. Statistical Analysis
3. Results
3.1. Study Population
3.2. Trends in Outcomes of G3-IVH and PVHI
3.3. Association between Major Brain Lesions and the Outcomes of Death and NDI
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
G3-IVH | grade 3 intraventricular haemorrhage |
PVHI | periventricular haemorrhagic infarction |
NDI | neurodevelopmental impairment |
GA | gestational age |
cUS | cranial ultrasound |
SES | socioeconomic status |
BSID-II | Bayley Scales of Infant Development, 2nd edition |
Bayley-III | Bayley Scales of Infant and Toddler Development, 3rd edition |
GMDS | Griffiths Mental Development Scales-Revised |
SD | standard deviation |
GMFCS | Gross Motor Function Classification System |
OR | odds ratio |
95% CI | 95% confidence interval |
m | mean |
M | median |
Appendix A
References
- Bolisetty, S.; Dhawan, A.; Abdel-Latif, M.; Bajuk, B.; Stack, J.; Oei, J.L.; Lui, K.; New South Wales and Australian Capital Territory Neonatal Intensive Care Units’ Data Collection. Intraventricular hemorrhage and neurodevelopmental outcomes in extreme pre-term infants. Pediatrics 2014, 133, 55–62. [Google Scholar] [CrossRef] [PubMed]
- Davis, A.S.; Hintz, S.R.; Goldstein, R.F.; Ambalavanan, N.; Bann, C.M.; Stoll, B.J.; Bell, E.F.; Shankaran, S.; Laptook, A.R.; Walsh, M.C.; et al. Outcomes of extremely preterm infants following severe intracranial hemorrhage. J. Perinatol. 2014, 34, 203–208. [Google Scholar] [CrossRef] [PubMed]
- Maitre, N.L.; Marshall, D.D.; Price, W.A.; Slaughter, J.C.; O’Shea, T.M.; Maxfield, C.; Goldstein, R.F. Neurodevelopmental outcome of infants with unilateral or bilateral periventricular hemorrhagic infarction. Pediatrics 2009, 124, e1153–e1160. [Google Scholar] [CrossRef] [PubMed]
- Roze, E.; Van Braeckel, K.N.J.A.; van der Veere, C.N.; Maathuis, C.G.B.; Martijn, A.; Bos, A.F. Functional outcome at school age of preterm infants with periventricular hemorrhagic infarction. Pediatrics 2009, 123, 1493–1500. [Google Scholar] [CrossRef]
- Takashima, S.; Mito, T.; Ando, Y. Pathogenesis of periventricular white matter hemorrhages in preterm infants. Brain Dev. 1986, 8, 25–30. [Google Scholar] [CrossRef]
- Volpe, J.J. Brain injury in the premature infant—current concepts of pathogenesis and prevention. Neonatology 1992, 62, 231–242. [Google Scholar] [CrossRef] [PubMed]
- Volpe, J.; Inder, T.; Darras, B.; de Vries, L.; Plessis, A.; Neil, J.; Perlman, J. Neurology of the Newborn; Elsevier: Amsterdam, The Netherlands, 2017. [Google Scholar]
- Maalouf, E.F.; Duggan, P.J.; Counsell, S.J.; Rutherford, M.A.; Cowan, F.; Azzopardi, D.; Edwards, A.D. Comparison of findings on cranial ultrasound and magnetic resonance imaging in preterm infants. Pediatrics 2001, 107, 719–727. [Google Scholar] [CrossRef]
- Parodi, A.; eurUS.brain group; Govaert, P.; Horsch, S.; Bravo, M.C.; Ramenghi, L.A. Cranial ultrasound findings in preterm germinal matrix haemorrhage, sequelae and outcome. Pediatr. Res. 2020, 87, 13–24. [Google Scholar] [CrossRef]
- Bassler, D.; Stoll, B.J.; Schmidt, B.; Asztalos, E.V.; Roberts, R.S.; Robertson, C.M.T.; Sauve, R.S.; Trial of indomethacin prophylaxis in preterms investigators. Using a count of neonatal morbidities to predict poor outcome in extremely low birth weight infants: Added role of neonatal infection. Pediatrics 2009, 123, 313–318. [Google Scholar] [CrossRef]
- Schlapbach, L.J.; Adams, M.; Proietti, E.; Aebischer, M.; Grunt, S.; Borradori-Tolsa, C.; Bickle-Graz, M.; Bucher, H.U.; Latal, B.; Natalucci, G.; et al. Outcome at two years of age in a Swiss national cohort of extremely preterm infants born between 2000 and 2008. BMC Pediatr. 2012, 12, 198. [Google Scholar] [CrossRef]
- Roze, E.; Kerstjens, J.M.; Maathuis, C.G.; ter Horst, H.J.; Bos, A.F. Risk Factors for adverse outcome in preterm infants with periventricular hemorrhagic infarction. Pediatrics 2008, 122, e46–e52. [Google Scholar] [CrossRef] [PubMed]
- Bassan, H.; Feldman, H.A.; Limperopoulos, C.; Benson, C.B.; Ringer, S.A.; Veracruz, E.; Soul, J.S.; Volpe, J.J.; Plessis, A.J. Periventricular hemorrhagic infarction: Risk factors and neonatal outcome. Pediatr. Neurol. 2006, 35, 85–92. [Google Scholar] [CrossRef] [PubMed]
- Richardson, D.K.; Gray, J.E.; Gortmaker, S.L.; Goldmann, D.A.; Pursley, D.M.; McCormick, M.C. Declining severity adjusted mortality: Evidence of improving neonatal intensive care. Pediatrics 1998, 102, 893–899. [Google Scholar] [CrossRef] [PubMed]
- Yeo, K.T.; Thomas, R.; Chow, S.S.; Bolisetty, S.; Haslam, R.; Tarnow-Mordi, W.; Lui, K. Improving incidence trends of severe intraventricular haemorrhages in preterm infants <32 weeks gestation: A cohort study. Arch. Dis. Child. Fetal Neonatal Ed. 2020, 105, 145–150. [Google Scholar] [CrossRef] [PubMed]
- Berger, T.M.; Bernet, V.; El Alama, S.; Fauchère, J.C.; Hösli, I.; Irion, O.; Kind, C.; Latal, B.; Nelle, M.; Pfister, R.E.; et al. Perinatal care at the limit of viability between 22 and 26 completed weeks of gestation in Switzerland. 2011 revision of the Swiss recommendations. Swiss Med. Wkly. 2011, 141, w13280. [Google Scholar]
- Adams, M.; the Swiss Neonatal Network & Follow-up Group; Natalucci, G.; Bassler, D. A narrative review of the Swiss Neonatal Network & Follow-up Group (SwissNeoNet). Pediatr. Med. 2021. Epub ahead of print. [Google Scholar]
- Papile, L.-A.; Burstein, J.; Burstein, R.; Koffler, H. Incidence and evolution of subependymal and intraventricular hemorrhage: A study of infants with birth weights less than 1500 gm. J. Pediatr. 1978, 92, 529–534. [Google Scholar] [CrossRef]
- Larg, R.H.; Graf, S.; Kundu, S.; Hunziker, U.; Molinari, L. Predicting developmental outcome at school age from infant tests of normal, at-risk and retarded infants. Dev. Med. Child Neurol. 1990, 32, 30–45. [Google Scholar] [CrossRef]
- Bayley, N. Bayley Scales of Infant Development, 2nd ed.; The Psychological Corporation: San Antonio, TX, USA, 1993. [Google Scholar]
- Bayley, N. Bayley Scales of Infant and Toddler Development, 3rd ed.; Administration Manual; Harcourt Assessment: San Antonio, TX, USA, 2006. [Google Scholar]
- Griffiths, R.; Huntley, M. The Griffiths Mental Development Scales: From Birth to Two Years. APA PsycTests 1996. [Google Scholar] [CrossRef]
- Rosenbaum, P.; Paneth, N.; Leviton, A.; Goldstein, M.; Bax, M.; Damiano, D.; Dan, B.; Jacobsson, B. A report: The definition and classification of cerebral palsy April 2006. Dev. Med. Child Neurol. Suppl. 2007, 109, 8–14. [Google Scholar]
- Palisano, R.; Rosenbaum, P.; Walter, S.; Russell, D.; Wood, E.; Galuppi, B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev. Med. Child Neurol. 1997, 39, 214–223. [Google Scholar] [CrossRef]
- Johnson, S.; Moore, T.; Marlow, N. Using the Bayley-III to assess neurodevelopmental delay: Which cut-off should be used? Pe-Diatric Res. 2014, 75, 670–674. [Google Scholar] [CrossRef] [PubMed]
- Bassan, H.; Benson, C.B.; Limperopoulos, C.; Feldman, H.A.; Ringer, S.A.; Veracruz, E.; Stewart, J.E.; Soul, J.S.; DiSalvo, D.N.; Volpe, J.J.; et al. Ultrasonographic features and severity scoring of periventricular hemorrhagic infarction in relation to risk factors and outcome. Pediatrics 2006, 117, 2111–2118. [Google Scholar] [CrossRef] [PubMed]
- Radic, J.A.; Vincer, M.; McNeely, P.D. Outcomes of intraventricular hemorrhage and posthemorrhagic hydrocephalus in a popu-lation-based cohort of very preterm infants born to residents of Nova Scotia from 1993 to 2010. J. Neurosurg. Pediatr. 2015, 15, 580–588. [Google Scholar] [CrossRef]
- Dudink, J.; Lequin, M.; Weisglas-Kuperus, N.; Conneman, N.; van Goudoever, J.B.; Govaert, P. Venous subtypes of preterm periventricular haemorrhagic infarction. Arch. Dis. Child. Fetal Neonatal Ed. 2008, 93, F201–F206. [Google Scholar] [CrossRef] [PubMed]
- Volpe, J.J. Volpe’s Neurology of the Newborn, 6th ed.; Elsevier: Philadelphia, PA, USA, 2018. [Google Scholar]
- Johnson, S.; Fawke, J.; Hennessy, E.; Rowell, V.; Thomas, S.; Wolke, D.; Marlow, N. Neurodevelopmental disability through 11 years of age in children born before 26 weeks of gestation. Pediatrics 2009, 124, e249–e257. [Google Scholar] [CrossRef] [PubMed]
Mean (SD), N (%) | G3-IVH N = 172 | Comparison with Normal cUS OR (95% CI) | PVHI N = 290 | Comparison with Normal cUS OR (95% CI) | Normal cUS N = 3296 (Reference) |
---|---|---|---|---|---|
Male sex | 103 (60%) | 1.37 (1.00 to 1.87) * | 184 (63%) | 1.59 (1.24 to 2.04) *** | 1719 (52%) |
Gestational age (weeks) | 26.9 (1.5) | −0.7 (−0.9 to −0.4) *** | 26.5 (1.6) | −1.1 (−1.3 to −0.9) *** | 27.6 (1.7) |
Multiple status | 47 (27%) | 0.84 (0.59 to 1.18) | 85 (29%) | 0.92 (0.71 to 1.20) | 1021 (31%) |
Birth weight (grams) | 940 (259) | −45 (−89 to −2) * | 913 (256) | −72 (−106 to −38) *** | 985 (285) |
z-score | −0.01 (0.84) | 0.13 (−0.00 to 0.26) | 0.04 (0.81) | 0.19 (0.08 to 0.29) *** | −0.14 (0.90) |
Small for gestational age | 12 (7%) | 0.66 (0.36 to 1.19) | 20 (7%) | 0.65 (0.41 to 1.03) | 338 (10%) |
Completed antenatal steroids course | 108/170 (63%) | 0.78 (0.57 to 1.08) | 138/283 (49%) | 0.43 (0.33 to 0.54) *** | 2173 (66%) |
Chorioamnionitis | 15/171 (9%) | 0.97 (0.56 to 1.66) | 32/289 (11%) | 1.25 (0.85 to 1.84) | 297/3285 (9%) |
Caesarean section | 130/171 (76%) | 0.80 (0.56 to 1.15) | 184/289 (64%) | 0.45 (0.35 to 0.57) *** | 2582/3237 (80%) |
Arterial cord pH | 7.28 (0.18) | −0.02 (−0.04 to 0.00) | 7.28 (0.15) | −0.02 (−0.04 to −0.01) ** | 7.30 (0.12) |
10’ Apgar score | 7.1 (1.9) | −0.6 (−0.9 to −0.3) *** | 7.3 (1.8) | −0.4 (−0.7 to −0.2) ** | 7.8 (2.1) |
NEC n (%) | 10 (6%) | 2.69 (1.36 to 5.30) ** | 14 (5%) | 2.21 (1.23 to 3.96) ** | 74 (2%) |
Sepsis n (%) | 41 (24%) | 2.00 (1.39 to 2.88) *** | 39 (13%) | 0.99 (0.70 to 1.41) | 446 (13%) |
Oxygen after 36 Weeks PMA n (%) | 31 (18%) | 1.48 (0.99 to 2.21) | 22 (8%) | 0.55 (0.35 to 0.86) ** | 414 (12%) |
ROP n (%) | 3 (1.7%) | 0.77 (0.24 to 2.48) | 4 (1%) | 0.61 (0.22 to 1.68) | 74 (2%) |
Patent arterial duct | 91 (53%) | 2.53 (1.86 to 3.44) *** | 136 (47%) | 1.99 (1.56 to 2.53) *** | 1014 (31%) |
Length of hospital stay (days) | 56.8 (41.6) | 2.4 (−3.2 to 8.0) | 35.1 (39.7) | −19.3 (−23.7 to −14.9) *** | 54.5 (35.9) |
Family socioeconomic status | 6.2 (2.6) | 0.1 (−0.4 to 0.5) | 6.2 (2.7) | 0.1 (−0.3 to 0.5) | 6.1 (2.6) |
N (%) | G3-IVH | OR (95% CI) 1 | Adjusted † OR (95% CI) 1 | PVHI | OR (95% CI) 2 | Adjusted † OR (95% CI) 2 | Normal cUS (Reference) |
---|---|---|---|---|---|---|---|
Total live births | 172 | N.A. | N.A. | 290 | N.A. | N.A. | 3296 |
Death | 56 (33%) | 2.75 (1.97 to 3.83) *** | 3.29 (1.94 to 5.57) *** | 175 (60%) | 8.65 (6.71 to 11.15) *** | 9.47 (6.06 to 14.81) *** | 493 (15%) |
Follow-up among survivors | 104/116 | N.A. | N.A. | 92/115 | N.A. | N.A. | 1776/2803 |
Neurodevelopmental impairment | 35/104 (34% of tested) | 2.96 (1.93 to 4.53) *** | 2.46 (1.50 to 4.03) *** | 49/92 (53% of tested) | 6.50 (4.24 to 9.97) *** | 6.68 (4.08 to 10.92) *** | 259/1776 (15% of tested) |
Cognitive development < - 2 SD | 25/104 (24% of tested) | 3.46 (2.14 to 5.59) *** | 2.76 (1.56 to 4.89) *** | 31/92 (34% of tested) | 5.46 (3.44 to 8.68) *** | 4.85 (2.81 to 8.36) *** | 149/1776 (8% of tested) |
Motor development < - 2 SD | 20/104 (19% of tested) | 2.42 (1.45 to 4.05) ** | 1.74 (0.94 to 3.25) | 37/92 (40% of tested) | 6.72 (4.30 to 10.50) *** | 7.52 (4.50 to 12.55) *** | 159/1776 (9% of tested) |
Cerebral palsy | 21/104 (20% of tested) | 7.49 (4.34 to 12.92) *** | 6.25 (3.31 to 11.80) *** | 47/92 (51% of tested) | 30.92 (19.03 to 50.24) *** | 33.13 (18.82 to 58.32) *** | 58/1776 (3% of tested) |
GMFCS > 1 | 9/104 (5% of tested) | 10.43 (4.49 to 24.21) *** | 6.47 (2.29 to 18.29) *** | 15/92 (16% of tested) | 21.27 (10.10 to 44.36) *** | 19.27 (7.94 to 46.77) *** | 16/1776 (0.5% of tested) |
Severe visual problems | 0/104 | - | - | 3/92 (3% of tested) | 11.81 (2.78 to 50.21) *** | 20.15 (3.67 to 110.71) ** | 5/1776 (0.3% of tested) |
Severe hearing problems | 2/104 (2% of tested) | 6.95 (1.33 to 36.25) ** | 3.39 (0.52 to 22.11) | 3/92 (3% of tested) | 11.81 (2.78 to 50.21) *** | 15.01 (2.88 to 78.21) ** | 5/1776 (0.3% of tested) |
Ongoing therapy | 21/104 (20% of tested) | 2.83 (1.70 to 4.70) *** | 3.12 (1.79 to 5.44) *** | 30/92 (33% of tested) | 5.32 (3.34 to 8.48) *** | 7.37 (4.36 to 12.47) *** | 146/1777 (8% of tested) |
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Thwaites, P.; Hagmann, C.; Schneider, J.; Schulzke, S.M.; Grunt, S.; Nguyen, T.D.; Bassler, D.; Natalucci, G., on behalf of the Swiss Neonatal Network and Follow-up Group. Trends in Outcomes of Major Intracerebral Haemorrhage in a National Cohort of Very Preterm Born Infants in Switzerland. Children 2023, 10, 1412. https://doi.org/10.3390/children10081412
Thwaites P, Hagmann C, Schneider J, Schulzke SM, Grunt S, Nguyen TD, Bassler D, Natalucci G on behalf of the Swiss Neonatal Network and Follow-up Group. Trends in Outcomes of Major Intracerebral Haemorrhage in a National Cohort of Very Preterm Born Infants in Switzerland. Children. 2023; 10(8):1412. https://doi.org/10.3390/children10081412
Chicago/Turabian StyleThwaites, Philip, Cornelia Hagmann, Juliane Schneider, Sven M. Schulzke, Sebastian Grunt, Thi Dao Nguyen, Dirk Bassler, and Giancarlo Natalucci on behalf of the Swiss Neonatal Network and Follow-up Group. 2023. "Trends in Outcomes of Major Intracerebral Haemorrhage in a National Cohort of Very Preterm Born Infants in Switzerland" Children 10, no. 8: 1412. https://doi.org/10.3390/children10081412