Research Article
No access
Published Online: 12 September 2023

Assessing the Response of Biomarkers to Anti-Inflammatory Medications in PIMS-TS by Longitudinal Multilevel Modeling: Real-World Data from a UK Tertiary Center

Publication: Pediatric Allergy, Immunology, and Pulmonology
Volume 36, Issue Number 3

Abstract

Background: Pediatric inflammatory multisystem syndrome temporarily associated with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection (PIMS-TS) is an acute complication of previous SARS-CoV-2 exposure. The relationship between inflammatory markers and anti-inflammatory medication in PIMS-TS is unknown. We retrospectively investigated the relationship between demographics, biomarkers, treatment, and length of stay (LOS) in this novel disease.
Methods: We reviewed the case notes and blood tests of all patients who met the Royal College of Paediatrics and Child Health diagnostic criteria for PIMS-TS at a large tertiary center in the United Kingdom. Biomarker trajectories were modeled using log linear mixed effects, and factors affecting LOS in hospital were evaluated using multiple regression.
Results: Between March 2020 and May 2022, a total of 56 patients attended Sheffield Children's Hospital with PIMS-TS, 70% male. Mean age was 7.4 ± 3.7 years and mean LOS 8.7 ± 4.5 days with 50% requiring intensive care and 20% requiring inotropes. Older males had shorter LOS than younger males (P = 0.04), not seen in females. Treatment included intravenous glucocorticoids in 93%, intravenous immunoglobulins (IVIG) in 77%, Anakinra in 11%, and infliximab in 1.8%. Biomarkers correlated poorly with trajectories that peaked at different times. C-reactive protein peaked first after median 1.3 days postadmission; while LFT's and neutrophils peaked after 3 days. Age had a large effect on some biomarkers, with older children having larger troponin and ferritin, and lower lymphocytes and platelets. Cumulative dose of glucocorticoids and IVIG had a statistically significant effect on some biomarkers, but effect size was small.
Conclusions: The heterogenous nature of PIMS-TS highlights the importance of a multidisciplinary approach. Worse inflammatory markers in older children within our cohort may be an indication of a different disease process occurring at different ages. Future work to investigate the association between age and troponin and ferritin in hyperinflammatory states is warranted.

Get full access to this article

View all available purchase options and get full access to this article.

Patient and Public Involvement

Neither patients nor the public were involved in the design, conduct, reporting, or dissemination of this research.

References

1. Verdoni L, Mazza A, Gervasoni A, et al. An outbreak of severe Kawasaki-like disease at the Italian epicentre of the SARS-CoV-2 epidemic: An observational cohort study. Lancet 2020;395(10239):1771–1778;
2. Wei M, Yuan J, Liu Y, et al. Novel coronavirus infection in hospitalized infants under 1 year of age in China. JAMA 2020;323(13):1313–1314;
3. Riphagen S, Gomez X, Gonzalez-Martinez C, et al. Hyperinflammatory shock in children during COVID-19 pandemic. Lancet 2020;395(10237):1607–1608;
4. González-Dambrauskas S, Vásquez-Hoyos P, Camporesi A, et al. Pediatric critical care and COVID-19. Pediatrics 2020;146(3):e20201766;
5. Venkataraman A, Kumar NP, Hanna LE, et al. Plasma biomarker profiling of PIMS-TS, COVID-19 and SARS-CoV2 seropositive children—A cross-sectional observational study from Southern India. EBioMedicine 2021;66:103317;
6. Anonymous. Guidance: Paediatric multisystem inflammatory syndrome temporally associated with COVID-19. R Coll Paediatr Child Health 2020;57(9):868.
7. Mansourian M, Ghandi Y, Habibi D, et al. COVID-19 infection in children: A systematic review and meta-analysis of clinical features and laboratory findings. Arch Pediatr 2021;28(3):242–248;
8. McArdle AJ, Vito O, Patel H, et al. Treatment of multisystem inflammatory syndrome in children. N Engl J Med 2021;385(1):11–22;
9. Bourne K, Gonzalez C, Daniel Hawley CK, et al. Sheffield Children's Hospital NHS Foundation Trust Guideline CG2015v2 PIMS-TS: Treatment and Management. Sheffield Children's Hospital: Sheffield, UK; 2021;1–16.
10. Ankola AA, Bradford VR, Newburger JW, et al. Coagulation profiles and viscoelastic testing in multisystem inflammatory syndrome in children. Pediatr Blood Cancer 2021;68(12):e29355;
11. Al-Ghafry M, Vagrecha A, Malik M, et al. Multisystem inflammatory syndrome in children (MIS-C) and the prothrombotic state: Coagulation profiles and rotational thromboelastometry in a MIS-C cohort. J Thromb Haemost 2021;19(7):1764–1770;
12. Lam HPJ, Alamelu J, Brighouse J, et al. Thrombosis and risk management in paediatric inflammatory multisystem syndrome—Temporally Associated with Sars-CoV2 (PIMS-TS). Blood 2020;136(Supplement 1):32;
13. Schlapbach LJ, Andre MC, Grazioli S, et al. Best practice recommendations for the diagnosis and management of children with Pediatric Inflammatory Multisystem Syndrome Temporally Associated With SARS-CoV-2 (PIMS-TS; Multisystem Inflammatory Syndrome in Children, MIS-C) in Switzerland. Front Pediatr 2021;9:396;
14. De Onis M, Onyango AW, Borghi E, et al. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ 2007;85(9):660;
15. Anonymous. Glucocorticoid Therapy | Treatment Summaries | BNF | NICE. n.d. Available from: https://bnf.nice.org.uk/treatment-summaries/glucocorticoid-therapy [Last accessed: October 8, 2022].
16. Piel FB, Parkes BL, Daby H, et al. The challenge of opt-outs from NHS data: a small-area perspective. J Public Health (Oxf) 2018;40(4):e594;
17. Penner J, Abdel-Mannan O, Grant K, et al. 6-month multidisciplinary follow-up and outcomes of patients with paediatric inflammatory multisystem syndrome (PIMS-TS) at a UK tertiary paediatric hospital: A retrospective cohort study. Lancet Child Adolesc Heal 2021;5(7):473–482;
18. Dufort EM, Koumans EH, Chow EJ, et al. Multisystem inflammatory syndrome in children in New York State. N Engl J Med 2020;383(4):347–358;
19. Rhedin S, Lundholm C, Horne AC, et al. Risk factors for multisystem inflammatory syndrome in children—A population-based cohort study of over 2 million children. Lancet Reg Health Eur 2022;19:100443;
20. Ramcharan T, Nolan O, Lai CY, et al. Paediatric Inflammatory Multisystem Syndrome: Temporally Associated with SARS-CoV-2 (PIMS-TS): Cardiac Features, management and short-term outcomes at a UK Tertiary Paediatric Hospital. Pediatr Cardiol 2020;41(7):1391;
21. Whittaker E, Bamford A, Kenny J, et al. Clinical characteristics of 58 children with a pediatric inflammatory multisystem syndrome temporally associated with SARS-CoV-2. JAMA 2020;324(3):259–269;
22. Feldstein LR, Rose EB, Horwitz SM, et al. Multisystem inflammatory syndrome in U.S. children and adolescents. N Engl J Med 2020;383(4):334–346;
23. Kiess A, Green J, Willenberg A, et al. Age-dependent reference values for hs-Troponin T and NT-proBNP and determining factors in a cohort of healthy children (The LIFE Child Study). Pediatr Cardiol 2022;43(5):1071;
24. Sorg AL, Hufnagel M, Doenhardt M, et al. Risk for severe outcomes of COVID-19 and PIMS-TS in children with SARS-CoV-2 infection in Germany. Eur J Pediatr 2022;181(10):3635–3643;
25. Vecchio A Lo, Garazzino S, Smarrazzo A, et al. Factors associated with severe gastrointestinal diagnoses in children with SARS-CoV-2 infection or multisystem inflammatory syndrome. JAMA Netw Open 2021;4(12):e2139974–e2139974;
26. Cohen JM, Carter MJ, Cheung CR, et al. Lower risk of multisystem inflammatory syndrome in children (MIS-C) with the delta and omicron variants of SARS-CoV-2. Clin Infect Dis 2023;76(3):e518–e521;
27. Escobedo RA, Kaushal D, Singh DK. Insights into the changing landscape of coronavirus disease 2019. Front Cell Infect Microbiol 2022;11:1305;
28. Huang FL. Alternatives to multilevel modeling for the analysis of clustered data. J Exp Educ 2014;84(1):175–196;

Information & Authors

Information

Published In

cover image Pediatric Allergy, Immunology, and Pulmonology
Pediatric Allergy, Immunology, and Pulmonology
Volume 36Issue Number 3September 2023
Pages: 94 - 103
PubMed: 37433192

History

Published online: 12 September 2023
Published in print: September 2023
Published ahead of print: 11 July 2023
Accepted: 19 May 2023
Received: 13 February 2023

Permissions

Request permissions for this article.

Data Sharing

Requests for anonymous patient data will be considered by written request to the corresponding author following publication of the article.

Authors

Affiliations

Joseph J. Tonge
Academic Unit of Medical Education, University of Sheffield, Sheffield, United Kingdom.
Olivia Stevens
Academic Unit of Medical Education, University of Sheffield, Sheffield, United Kingdom.
Jeremy Dawson
School of Health and Related Research (ScHARR), University of Sheffield, Sheffield, United Kingdom.
Management School, University of Sheffield, Sheffield, United Kingdom.
Daniel Hawley
Sheffield Children's Hospital NHS Foundation Trust, Sheffield, United Kingdom.
Caroline Kerrison
Sheffield Children's Hospital NHS Foundation Trust, Sheffield, United Kingdom.
Nils Krone
Sheffield Children's Hospital NHS Foundation Trust, Sheffield, United Kingdom.
Department of Oncology and Metabolism, University of Sheffield, Sheffield, United Kingdom.
Sarah L. Maltby
Sheffield Children's Hospital NHS Foundation Trust, Sheffield, United Kingdom.
Anne-Marie McMahon
Sheffield Children's Hospital NHS Foundation Trust, Sheffield, United Kingdom.
Fiona Shackley
Sheffield Children's Hospital NHS Foundation Trust, Sheffield, United Kingdom.
Rupa Talekar
Sheffield Children's Hospital NHS Foundation Trust, Sheffield, United Kingdom.
PIMS-TS Working Group
Sheffield Children's Hospital NHS Foundation Trust, Sheffield, United Kingdom.
Carmen Gonzalez-Martinez
Sheffield Children's Hospital NHS Foundation Trust, Sheffield, United Kingdom.
Sheffield Children's Hospital NHS Foundation Trust, Sheffield, United Kingdom.
Department of Oncology and Metabolism, University of Sheffield, Sheffield, United Kingdom.

Notes

Address correspondence to: Neil Lawrence, MBChB, Department of Oncology and Metabolism, University of Sheffield, Sheffield S10 2RX, United Kingdom [email protected]

Authors' Contributions

All authors take responsibility for data collection, analysis and interpretation, the conduct of the research, and submission of the article. N.L. and J.J.T. conceptualized the study. J.J.T. and O.S. extracted data from patient records. N.L. completed the statistical analysis and modeling. All authors were involved in editing the article before submission. All authors take full responsibility for the decision to submit the article for publication. All authors have seen and approved the final article.

Author Disclosure Statement

We declare no competing interests which could influence the undertaking, analysis, or interpretation of the results showed in this article.

Funding Information

No funding was received for this study.

Metrics & Citations

Metrics

Citations

Export citation

Select the format you want to export the citations of this publication.

View Options

Get Access

Access content

To read the fulltext, please use one of the options below to sign in or purchase access.

Society Access

If you are a member of a society that has access to this content please log in via your society website and then return to this publication.

Restore your content access

Enter your email address to restore your content access:

Note: This functionality works only for purchases done as a guest. If you already have an account, log in to access the content to which you are entitled.

View options

PDF/EPUB

View PDF/ePub

Full Text

View Full Text

Media

Figures

Other

Tables

Share

Share

Copy the content Link

Share on social media

Back to Top