Download PDF
Am J Perinatol 2024; 41(S 01): e630-e640
DOI: 10.1055/a-1925-1797
Original Article

Bedside Ultrasound for Early Diagnosis of Necrotizing Enterocolitis: A Pilot Study

Ignacio Oulego-Erroz 
1   Pediatric Intensive Care Unit, Complejo Asistencial Universitario de León, León, Spain
,
Javier Rodríguez-Fanjul 
2   Pediatric Intensive Care Unit, Hospital Germans Trias i Pujol, Badalona, Spain
,
Sandra Terroba-Seara
1   Pediatric Intensive Care Unit, Complejo Asistencial Universitario de León, León, Spain
,
Clara Sorribes-Orti
2   Pediatric Intensive Care Unit, Hospital Germans Trias i Pujol, Badalona, Spain
,
David Fernandez-Fernández
3   Department of Pediatrics, Complejo Asistencial Universitario de León, León, Spain
,
Silvia Fuentes-Martínez
3   Department of Pediatrics, Complejo Asistencial Universitario de León, León, Spain
,
Álvaro Pou-Blázquez
3   Department of Pediatrics, Complejo Asistencial Universitario de León, León, Spain
› Author Affiliations Funding None.
› Further Information
Also available at
    Permissions and Reprints

Abstract

Objective This study aimed to assess whether bedside ultrasound (BUS) as the first imaging modality allows an earlier diagnosis of necrotizing enterocolitis (NEC) compared with abdominal radiography.

Study Design A before–after controlled study in preterm infants with suspected NEC. The intervention group (October 2019–October 2021) received BUS as the first imaging modality and was managed accordingly to BUS findings. The control group (October 2015–September 2019) received radiography as the first imaging modality. The main outcome was NEC confirmation at the time of initial imaging. Secondary outcomes included time to diagnosis, laboratory data, and treatment requirements.

Results Thirty-five episodes of suspected NEC with 14 (40%) confirmed NEC cases and 49 episodes of suspected NEC with 22 (44.9%) confirmed NEC cases were included in the intervention and control groups, respectively. In the intervention group, 11 of 14 (78.6%) NEC cases were confirmed at initial evaluation compared with 5 of 22 (22.7%) in the control group (p = 0.001). Infants in the intervention group developed thrombocytopenia and coagulopathy less frequently, were exposed to less radiation, and required less days of parenteral nutrition compared with the control group (p < 0.05).

Conclusion The use of BUS as the first imaging modality allowed an earlier diagnosis and timely treatment of NEC compared with abdominal radiography.

Key Points

  • This is the first study that has assessed the role of BUS as the first imaging modality in NEC.

  • BUS improves early diagnosis of NEC compared with abdominal radiography.

  • BUS shortens time to NEC confirmation and treatment initiation which may reduce clinical severity of the NEC episode.

Keywords

bedside ultrasound - preterm - necrotizing enterocolitis - biomarker - early diagnosis

Note

The authors declare that the current manuscript contains original material, has not been previously published nor it is has been submitted, or is being considered for publication elsewhere.


Ethics and Consent Statement

The protocol was reviewed and approved by the institutional review boards (IRBs) of both participating centers (CEIC provincial de León; codes PI-20–329 and CIEC Hospital German Trias I Pujol Badalona; code: PI 20–173). Parents or legal guardians of the study participants gave their informed consent for collection and use of clinical and BUS data during the intervention period. As a change in practice, study consent was waived by the IRB for the preintervention period.


Authors' Contributions

All the authors contributed to the study conception and design. Material preparation and data collection and analysis were performed by Ignacio Oulego-Erroz, Javier Rodríguez-Fanjul, Sandra Terroba Seara, Clara Sorribes Ortí, David Fernandez-Fernández, Silvia Fuentes-Martínez, and Álvaro Pou-Blázquez. The first draft of the manuscript was written by Ignacio Oulego-Erroz and all the authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.


Availability of Data and Material

Raw database is available from authors upon request.


Supplementary Material



Publication History

Received: 05 June 2022

Accepted: 01 August 2022

Accepted Manuscript online:
16 August 2022

Article published online:
19 October 2022

© 2022. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Frost BL, Modi BP, Jaksic T, Caplan MS. New medical and surgical insights into neonatal necrotizing enterocolitis: a review. JAMA Pediatr 2017; 171 (01) 83-88
    CrossrefPubMedGoogle Scholar
  • 2 Bell EF, Hintz SR, Hansen NI. et al; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network. Mortality, in-hospital morbidity, care practices, and 2-year outcomes for extremely preterm infants in the US, 2013-2018. JAMA 2022; 327 (03) 248-263
    CrossrefPubMedGoogle Scholar
  • 3 Jones IH, Hall NJ. Contemporary outcomes for infants with necrotizing enterocolitis-a systematic review. J Pediatr 2020; 220: 86.e3-92.e3
    CrossrefPubMedGoogle Scholar
  • 4 Bazacliu C, Neu J. Necrotizing enterocolitis: long term complications. Curr Pediatr Rev 2019; 15 (02) 115-124
    CrossrefPubMedGoogle Scholar
  • 5 Mondal A, Misra D, Al-Jabir A, Hubail D, Ward T, Patel B. Necrotizing enterocolitis in neonates: has the brain taken a hit 10 years later?. J Pediatr Neurosci 2021; 16 (01) 30-34
    CrossrefPubMedGoogle Scholar
  • 6 Zozaya C, Shah J, Pierro A. et al; Canadian Neonatal Network (CNN) and the Canadian Neonatal Follow-Up Network (CNFUN) Investigators. Neurodevelopmental and growth outcomes of extremely preterm infants with necrotizing enterocolitis or spontaneous intestinal perforation. J Pediatr Surg 2021; 56 (02) 309-316
    CrossrefPubMedGoogle Scholar
  • 7 Hickey M, Georgieff M, Ramel S. Neurodevelopmental outcomes following necrotizing enterocolitis. Semin Fetal Neonatal Med 2018; 23 (06) 426-432
    CrossrefPubMedGoogle Scholar
  • 8 Ahle M, Ringertz HG, Rubesova E. The role of imaging in the management of necrotising enterocolitis: a multispecialist survey and a review of the literature. Eur Radiol 2018; 28 (09) 3621-3631
    CrossrefPubMedGoogle Scholar
  • 9 Walsh MC, Kliegman RM. Necrotizing enterocolitis: treatment based on staging criteria. Pediatr Clin North Am 1986; 33 (01) 179-201
    CrossrefPubMedGoogle Scholar
  • 10 Soni R, Katana A, Curry JI, Humphries PD, Huertas-Ceballos A. How to use abdominal X-rays in preterm infants suspected of developing necrotising enterocolitis. Arch Dis Child Educ Pract Ed 2020; 105 (01) 50-57
    CrossrefPubMedGoogle Scholar
  • 11 Markiet K, Szymanska-Dubowik A, Janczewska I, Domazalska-Popadiuk I, Zawadzka-Kepczynska A, Bianek-Bodzak A. Agreement and reproducibility of radiological signs in NEC using the Duke Abdominal Assessment Scale (DAAS). Pediatr Surg Int 2017; 33 (03) 335-340
    CrossrefPubMedGoogle Scholar
  • 12 Baird R, Tessier R, Guilbault MP, Puligandla P, Saint-Martin C. Imaging, radiation exposure, and attributable cancer risk for neonates with necrotizing enterocolitis. J Pediatr Surg 2013; 48 (05) 1000-1005
    CrossrefPubMedGoogle Scholar
  • 13 Aliev MM, Dekhqonboev AA, Yuldashev RZ. Advantages of abdominal ultrasound in the management of infants with necrotizing enterocolitis. Pediatr Surg Int 2017; 33 (02) 213-216
    CrossrefPubMedGoogle Scholar
  • 14 McBride WJ, Roy S, Brudnicki A, Stringel G. Correlation of complex ascites with intestinal gangrene and perforation in neonates with necrotizing enterocolitis. J Pediatr Surg 2010; 45 (05) 887-889
    CrossrefPubMedGoogle Scholar
  • 15 Cuna AC, Reddy N, Robinson AL, Chan SS. Bowel ultrasound for predicting surgical management of necrotizing enterocolitis: a systematic review and meta-analysis. Pediatr Radiol 2018; 48 (05) 658-666
    CrossrefPubMedGoogle Scholar
  • 16 Valpacos M, Arni D, Keir A. et al. Diagnosis and management of necrotizing enterocolitis: an international survey of neonatologists and pediatric surgeons. Neonatology 2018; 113 (02) 170-176
    CrossrefPubMedGoogle Scholar
  • 17 Alexander KM, Chan SS, Opfer E. et al. Implementation of bowel ultrasound practice for the diagnosis and management of necrotising enterocolitis. Arch Dis Child Fetal Neonatal Ed 2021; 106 (01) 96-103
    CrossrefPubMedGoogle Scholar
  • 18 De Martino L, Yousef N, Ben-Ammar R, Raimondi F, Shankar-Aguilera S, De Luca D. Lung ultrasound score predicts surfactant need in extremely preterm neonates. Pediatrics 2018; 142 (03) e20180463
    CrossrefPubMedGoogle Scholar
  • 19 Rozé JC, Cambonie G, Marchand-Martin L. et al; Hemodynamic EPIPAGE 2 Study Group. Association between early screening for patent ductus arteriosus and in-hospital mortality among extremely preterm infants. JAMA 2015; 313 (24) 2441-2448
    CrossrefPubMedGoogle Scholar
  • 20 Faingold R. Technical aspects of abdominal ultrasound and color Doppler assessment of bowel viability in necrotizing enterocolitis. Pediatr Radiol 2018; 48 (05) 617-619
    CrossrefPubMedGoogle Scholar
  • 21 Epelman M, Daneman A, Navarro OM. et al. Necrotizing enterocolitis: review of state-of-the-art imaging findings with pathologic correlation. Radiographics 2007; 27 (02) 285-305
    CrossrefPubMedGoogle Scholar
  • 22 Faingold R, Daneman A, Tomlinson G. et al. Necrotizing enterocolitis: assessment of bowel viability with color doppler US. Radiology 2005; 235 (02) 587-594
    CrossrefPubMedGoogle Scholar
  • 23 García P, San Feliciano L, Benito F. et al; hospitales pertenecientes a SEN1500. Outcome at two years corrected age of a cohort of very low birth weight infants from hospitals within the neonatal SEN1500 network [in Spanish]. An Pediatr (Barc) 2013; 79 (05) 279-287
    PubMedGoogle Scholar
  • 24 Vermont Oxford Network. Manual of Operations: Part 2 Data Definitions & Infant Data Forms V. 2018. Accessed August 30, 2022 at: https://vtoxford.zendesk.com/hc/en-us/articles/360013115393-2019-Manual-of-Operations-Part-2-Release-23-2-PDF
    PubMedGoogle Scholar
  • 25 Gordon PV, Swanson JR, MacQueen BC, Christensen RD. A critical question for NEC researchers: can we create a consensus definition of NEC that facilitates research progress?. Semin Perinatol 2017; 41 (01) 7-14
    CrossrefPubMedGoogle Scholar
  • 26 Gephart SM, Gordon PV, Penn AH. et al. Changing the paradigm of defining, detecting, and diagnosing NEC: perspectives on Bell's stages and biomarkers for NEC. Semin Pediatr Surg 2018; 27 (01) 3-10
    CrossrefPubMedGoogle Scholar
  • 27 Gephart SM, Hanson C, Wetzel CM. et al. NEC-zero recommendations from scoping review of evidence to prevent and foster timely recognition of necrotizing enterocolitis. Matern Health Neonatol Perinatol 2017; 3: 23
    CrossrefPubMedGoogle Scholar
  • 28 Patel RM, Ferguson J, McElroy SJ, Khashu M, Caplan MS. Defining necrotizing enterocolitis: current difficulties and future opportunities. Pediatr Res 2020; 88 (Suppl. 01) 10-15
    CrossrefPubMedGoogle Scholar
  • 29 Agakidou E, Agakidis C, Gika H, Sarafidis K. Emerging biomarkers for prediction and early diagnosis of necrotizing enterocolitis in the era of metabolomics and proteomics. Front Pediatr 2020; 8: 602255
    CrossrefPubMedGoogle Scholar
  • 30 Tracy SA, Lazow SP, Castro-Aragon IM. et al. Is abdominal sonography a useful adjunct to abdominal radiography in evaluating neonates with suspected necrotizing enterocolitis?. J Am Coll Surg 2020; 230 (06) 903.e2-911.e2
    CrossrefPubMedGoogle Scholar
  • 31 Chen S, Hu Y, Liu Q, Li X, Wang H, Wang K. Comparison of abdominal radiographs and sonography in prognostic prediction of infants with necrotizing enterocolitis. Pediatr Surg Int 2018; 34 (05) 535-541
    CrossrefPubMedGoogle Scholar
  • 32 Biomarkers Definitions Working Group.. Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin Pharmacol Ther 2001; 69 (03) 89-95
    CrossrefPubMedGoogle Scholar
  • 33 Califf RM. Biomarker definitions and their applications. Exp Biol Med (Maywood) 2018; 243 (03) 213-221
    CrossrefPubMedGoogle Scholar
  • 34 Bobillo-Perez S, Rodríguez-Fanjul J, Jordan Garcia I. Is procalcitonin useful in pediatric critical care patients?. Biomark Insights 2018; 13: 1177271918792244
    CrossrefPubMedGoogle Scholar
  • 35 Syed MK, Al Faqeeh AA, Saeed N. et al. Surgical versus medical management of necrotizing enterocolitis with and without intestinal perforation: a retrospective chart review. Cureus 2021; 13 (06) e15722
    PubMedGoogle Scholar
  • 36 Bethell GS, Knight M, Hall NJ. BAPS-CASS NEC Investigator Group on behalf of BAPS-CASS. Surgical necrotizing enterocolitis: association between surgical indication, timing, and outcomes. J Pediatr Surg 2021; 56 (10) 1785-1790
    CrossrefPubMedGoogle Scholar
  • 37 Chen SC, Yen ZS, Wang HP, Lin FY, Hsu CY, Chen WJ. Ultrasonography is superior to plain radiography in the diagnosis of pneumoperitoneum. Br J Surg 2002; 89 (03) 351-354
    CrossrefPubMedGoogle Scholar
  • 38 Asrani A. Sonographic diagnosis of pneumoperitoneum using the ‘enhancement of the peritoneal stripe sign.’ A prospective study. Emerg Radiol 2007; 14 (01) 29-39
    CrossrefPubMedGoogle Scholar
  • 39 Sedgwick P. Before and after study designs. BMJ 2014; 349: g5074
    CrossrefPubMedGoogle Scholar