Surgical necrotizing enterocolitis but not spontaneous intestinal perforation is associated with adverse neurological outcome at school age.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
11 02 2020
11 02 2020
Historique:
received:
09
09
2019
accepted:
30
12
2019
entrez:
13
2
2020
pubmed:
13
2
2020
medline:
11
11
2020
Statut:
epublish
Résumé
Gastrointestinal complications during the neonatal period, i.e. necrotizing enterocolitis (NEC) and spontaneous intestinal perforation (SIP), are associated with adverse short-term outcome in very-low-birthweight infants (VLBWI, <1500 g birth weight). However, little is known about the neurological outcome of survivors at school age. We analysed data of 2241 infants followed-up at the age of 6 years. To determine the effect of NEC and SIP on cognitive outcome in consideration of other important confounding factors, we used multivariable logistic regression models. In addition, infants with surgical diagnosis of NEC (n = 43) or SIP (n = 41) were compared to NEC (n = 43) or SIP (n = 41) negative controls using Mahalanobis distance matching. Infants with a history for NEC had a three times increased risk (RR 3.0 [1.8-4.2], p < 0.001) to develop IQ scores <85 while history of surgical SIP did not increase the relative risk for lower IQs at school age (RR 1.0 [0.4-2.1], p = 1.000). In a matched-cohort analysis, we confirmed that infants with surgical NEC had lower mean IQ results than unaffected controls (±SD) (85±17 vs. 94±14, p = 0.023) while no differences were found for history of SIP. Our results reflect that the different aetiology and inflammatory extent of NEC and SIP may lead to disparate neurodevelopment trajectories. Hence, our data suggest a potential role of early gut-brain axis distortion in infants with NEC which needs to be further explored.
Identifiants
pubmed: 32047169
doi: 10.1038/s41598-020-58761-6
pii: 10.1038/s41598-020-58761-6
pmc: PMC7012917
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2373Investigateurs
Christian Wieg
(C)
Angela Kribs
(A)
Axel von der Wense
(A)
Ursula Weller
(U)
Thomas Höhn
(T)
Dirk M Olbertz
(DM)
Ursula Felderhoff-Müser
(U)
Rainer Rossi
(R)
Norbert Teig
(N)
Friedhelm Heitmann
(F)
Susanne Schmidtke
(S)
Bettina Bohnhorst
(B)
Matthias Vochem
(M)
Holger Michel
(H)
Jens Möller
(J)
Joachim G Eichhorn
(JG)
Jürgen Wintgens
(J)
Ralf Böttger
(R)
Mechthild Hubert
(M)
Michael Dördelmann
(M)
Georg Hillebrand
(G)
Claudia Roll
(C)
Reinhard Jensen
(R)
Mario Rüdiger
(M)
Julia Sandkötter
(J)
Stefan Schäfer
(S)
Thomas Schaible
(T)
Axel Franz
(A)
Malik Aydin
(M)
Silke Ehlers
(S)
Claudius Werner
(C)
Thorsten Orlikowsky
(T)
Hubert Gerleve
(H)
Katja Schneider
(K)
Claudius Werner
(C)
Kai Böckenholt
(K)
Knud Linnemann
(K)
Dirk Müller
(D)
Corinna Gebauer
(C)
Florian Guthmann
(F)
Jochen Reese
(J)
Roland Haase
(R)
Stephan Seeliger
(S)
Helmut Küster
(H)
Roland Hentschel
(R)
Thorsten Körner
(T)
Thomas Brune
(T)
Andreas Müller
(A)
Thomas Frank
(T)
Martin Andree Berghäuser
(MA)
Kristin Dawczynski
(K)
Références
Battersby, C., Santhalingam, T., Costeloe, K. & Modi, N. Incidence of neonatal necrotising enterocolitis in high-income countries: a systematic review. Arch. Dis. Child. - Fetal Neonatal Ed. 103, F182–F189 (2018).
doi: 10.1136/archdischild-2017-313880
Martin, C. R. et al. Neurodevelopment of Extremely Preterm Infants who had Necrotizing Enterocolitis with or without Late Bacteremia. J. Pediatr. 157, 751–756.e1 (2010).
doi: 10.1016/j.jpeds.2010.05.042
Härtel, C. et al. Less invasive surfactant administration and complications of preterm birth. Sci. Rep. 8, 8333 (2018).
doi: 10.1038/s41598-018-26437-x
Berry, M. J., Port, L. J., Gately, C. & Stringer, M. D. Outcomes of infants born at 23 and 24 weeks’ gestation with gut perforation. J. Pediatr. Surg. 54, 2092–2098 (2019).
doi: 10.1016/j.jpedsurg.2019.03.017
Yee, W. H. et al. Incidence and timing of presentation of necrotizing enterocolitis in preterm infants. Pediatrics 129, e298–304 (2012).
doi: 10.1542/peds.2011-2022
Moschopoulos, C. et al. The Neurodevelopmental Perspective of Surgical Necrotizing Enterocolitis: The Role of the Gut-Brain Axis. Mediators Inflamm. 2018, 1–8 (2018).
doi: 10.1155/2018/7456857
Warner, B. B. et al. Gut bacteria dysbiosis and necrotising enterocolitis in very low birthweight infants: a prospective case-control study. Lancet 387, 1928–36 (2016).
doi: 10.1016/S0140-6736(16)00081-7
Houben, C. et al. Spontaneous Intestinal Perforation: The Long-Term Outcome. Eur. J. Pediatr. Surg. 27, 346–351 (2017).
doi: 10.1055/s-0036-1593990
Wadhawan, R. et al. Spontaneous intestinal perforation in extremely low birth weight infants: association with indometacin therapy and effects on neurodevelopmental outcomes at 18–22 months corrected age. Arch. Dis. Child. - Fetal Neonatal Ed. 98, F127–F132 (2013).
doi: 10.1136/archdischild-2011-300659
Koshinaga, T. et al. Spontaneous localized intestinal perforation and intestinal dilatation in very-low-birthweight infants. Acta Paediatr. 95, 1381–1388 (2006).
doi: 10.1080/08035250600617123
Roze, E. et al. Functional Impairments at School Age of Children With Necrotizing Enterocolitis or Spontaneous Intestinal Perforation. Pediatr. Res. 70, 619–625 (2011).
doi: 10.1203/PDR.0b013e31823279b1
Mihi, B. & Good, M. Impact of Toll-Like Receptor 4 Signaling in Necrotizing Enterocolitis. Clin. Perinatol. 46, 145–157 (2019).
doi: 10.1016/j.clp.2018.09.007
Niño, D. F. et al. Cognitive impairments induced by necrotizing enterocolitis can be prevented by inhibiting microglial activation in mouse brain. Sci. Transl. Med. 10, eaan0237 (2018).
doi: 10.1126/scitranslmed.aan0237
O’Shea, T. M. et al. Inflammation-initiating illnesses, inflammation-related proteins, and cognitive impairment in extremely preterm infants. Brain. Behav. Immun. 29, 104–12 (2013).
doi: 10.1016/j.bbi.2012.12.012
Chan, K. Y. Y. et al. Immunoregulatory protein profiles of necrotizing enterocolitis versus spontaneous intestinal perforation in preterm infants. PLoS One 7, e36977 (2012).
doi: 10.1371/journal.pone.0036977
Zhang, J. & Yu, K. F. What’s the Relative Risk? JAMA 280, 1690 (1998).
doi: 10.1001/jama.280.19.1690
Wadhawan, R. et al. Neurodevelopmental outcomes of extremely low birth weight infants with spontaneous intestinal perforation or surgical necrotizing enterocolitis. J. Perinatol. 34, 64–70 (2014).
doi: 10.1038/jp.2013.128
Arnold, M., Moore, S. W., Sidler, D. & Kirsten, G. F. Long-term outcome of surgically managed necrotizing enterocolitis in a developing country. Pediatr. Surg. Int. 26, 355–360 (2010).
doi: 10.1007/s00383-010-2583-8
Salhab, W. A., Perlman, J. M., Silver, L. & Sue Broyles, R. Necrotizing enterocolitis and neurodevelopmental outcome in extremely low birth weight infants. J. Perinatol. 24, 534–40 (2004).
doi: 10.1038/sj.jp.7211165
Härtel, C. et al. Lactobacillus acidophilus/Bifidobacterium infantis probiotics are associated with increased growth of VLBWI among those exposed to antibiotics. Sci. Rep. 7, 5633 (2017).
doi: 10.1038/s41598-017-06161-8
Härtel, C. et al. NOD2 Loss-of-Function Mutations and Risks of Necrotizing Enterocolitis or Focal Intestinal Perforation in Very Low-birth-weight Infants. Inflamm. Bowel Dis. 22, 249–256 (2016).
doi: 10.1097/MIB.0000000000000658
Härtel, C. et al. Prophylactic Use of Lactobacillus acidophilus/Bifidobacterium infantis Probiotics and Outcome in Very Low Birth Weight Infants. J. Pediatr. 165, 285–289.e1 (2014).
doi: 10.1016/j.jpeds.2014.04.029
Kubota, A. et al. Focal intestinal perforation in extremely-low-birth-weight neonates: etiological consideration from histological findings. Pediatr. Surg. Int. 23, 997–1000 (2007).
doi: 10.1007/s00383-007-1984-9
Mizrahi, A., Barlow, O., Berdon, W., Blanc, W. A. & Silverman, W. A. Necrotizing enterocolitis in premature infants. J. Pediatr. 66, 697–705 (1965).
doi: 10.1016/S0022-3476(65)80003-8
Kuppala, V. S., Meinzen-Derr, J., Morrow, A. L. & Schibler, K. R. Prolonged initial empirical antibiotic treatment is associated with adverse outcomes in premature infants. J. Pediatr. 159, 720–5 (2011).
doi: 10.1016/j.jpeds.2011.05.033
Hintz, S. R. Neurodevelopmental and Growth Outcomes of Extremely Low Birth Weight Infants After Necrotizing Enterocolitis. Pediatrics 115, 696–703 (2005).
doi: 10.1542/peds.2004-0569
Kidokoro, H. et al. Brain injury and altered brain growth in preterm infants: predictors and prognosis. Pediatrics 134, e444–53 (2014).
doi: 10.1542/peds.2013-2336
Shin, S. H. et al. Surgical Necrotizing Enterocolitis versus Spontaneous Intestinal Perforation in White Matter Injury on Brain Magnetic Resonance Imaging. Neonatology 110, 148–54 (2016).
doi: 10.1159/000444387
Bouyssi-Kobar, M. et al. Third Trimester Brain Growth in Preterm Infants Compared With In Utero Healthy Fetuses. Pediatrics 138, e20161640 (2016).
doi: 10.1542/peds.2016-1640
Desai, R. J. et al. Extension of Disease Risk Score-Based Confounding Adjustments for Multiple Outcomes of Interest: An Empirical Evaluation. Am. J. Epidemiol. 187, 2439–2448 (2018).
pubmed: 29947726
Marißen, J. et al. Efficacy of Bifidobacterium longum, B. infantis and Lactobacillus acidophilus probiotics to prevent gut dysbiosis in preterm infants of 28+0–32+6 weeks of gestation: a randomised, placebo-controlled, double-blind, multicentre trial: the PRIMAL Clinical Study protocol. BMJ Open 9, e032617 (2019).
doi: 10.1136/bmjopen-2019-032617
Humberg, A. et al. Active perinatal care of preterm infants in the German Neonatal Network. Arch. Dis. Child. - Fetal Neonatal Ed., fetalneonatal-2018-316770, https://doi.org/10.1136/archdischild-2018-316770 (2019).
Bell, M. J. et al. Neonatal necrotizing enterocolitis. Therapeutic decisions based upon clinical staging. Ann. Surg. 187, 1–7 (1978).
doi: 10.1097/00000658-197801000-00001
Voigt, M. et al. New percentile values for the anthropometric dimensions of twin neonates: analysis of perinatal survey data of 2007-2011 from all 16 states of Germany. Z. Geburtshilfe Neonatol. 218, 254–260 (2014).
doi: 10.1055/s-0034-1385858
Reid, S. M., Carlin, J. B. & Reddihough, D. S. Using the Gross Motor Function Classification System to describe patterns of motor severity in cerebral palsy. Dev. Med. Child Neurol. 53, 1007–1012 (2011).
doi: 10.1111/j.1469-8749.2011.04044.x
Elvrum, A.-K. G. et al. Bimanual Fine Motor Function (BFMF) Classification in Children with Cerebral Palsy: Aspects of Construct and Content Validity. Phys. Occup. Ther. Pediatr. 36, 1–16 (2016).
doi: 10.3109/01942638.2014.975314
Fortmann, I. et al. Antifungal Treatment and Outcome in Very Low Birth Weight Infants. Pediatr. Infect. Dis. J. 37, 1165–1171 (2018).
doi: 10.1097/INF.0000000000002001
Diamond, A. & Sekhon, J. S. Genetic Matching for Estimating Causal Effects: A General Multivariate Matching Method for Achieving Balance in Observational. Studies. Rev. Econ. Stat. 95, 932–945 (2013).
doi: 10.1162/REST_a_00318