Skip to main content
SpringerLink
Log in

Microcirculatory Changes in Pediatric Patients During Congenital Heart Defect Corrective Surgery

  • Original Article
  • Published:
Journal of Cardiovascular Translational Research Aims and scope Submit manuscript

Abstract

A prospective, observational single-center study was carried out. Pediatric patients undergoing congenital heart defect surgery were evaluated before, during, and after surgery. At each time point, sublingual microcirculation and clinical parameters were assessed, along with analytical variables. Twenty-four patients were included. All microcirculatory parameters worsened during cardiopulmonary bypass and returned to baseline values after surgery (p ≤ 0.001). In the intraoperative evaluation, body temperature correlated with perfused small vessel density (p = 0.014), proportion of perfused small vessels (p < 0.001), small vessel microvascular flow index (p = 0.003), and small vessel heterogeneity index (p < 0.002). Patients with cyanotic disease exhibited higher small vessel density (p < 0.008) and higher density of perfused small vessels (p < 0.022) at baseline, and a lower microvascular flow index (p = 0.022) and higher heterogeneity (p = 0.026) in the intraoperative phase. Children with congenital heart disease exhibited decreased vascular density and microvascular blood flow and increased heterogeneity during cardiopulmonary bypass. All these parameters returned to baseline values after surgery.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

CHD:

Congenital heart defects

CI95%:

95% confidence interval

DB:

De Backer score

FiO2 :

Fraction of inspired oxygen

HI:

Heterogeneity index

IQR:

Interquartile range

MFI:

Microcirculatory flow index

NIRS:

Near infrared photospectrometry

PEEP:

Positive end expiratory pressure

PICU:

Pediatric intensive care unit

PIP:

Peak inspiratory pressure

PPV:

Proportion of perfused vessels

PVD:

Perfused vessel density

SDF:

Sidestream dark-field imaging

SV:

Small vessels

TVD:

Total vessel density

VIS:

Vasoactive inotropic score

References

  1. Vellinga, N. A. R., Boerma, E. C., Koopmans, M., Donati, A., Dubin, A., Shapiro, N. I., et al. (2017). Mildly elevated lactate levels are associated with microcirculatory flow abnormalities and increased mortality: A microSOAP post hoc analysis. Critical Care, 21(1), 255. https://doi.org/10.1186/s13054-017-1842-7.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Trzeciak, S., Dellinger, R. P., Parrillo, J. E., Guglielmi, M., Bajaj, J., Abate, N. L., et al. (2007). Early microcirculatory perfusion derangements in patients with severe sepsis and septic shock: Relationship to hemodynamics, oxygen transport, and survival. Annals of Emergency Medicine, 49(1), 88–98.e2. https://doi.org/10.1016/j.annemergmed.2006.08.021.

    Article  PubMed  Google Scholar 

  3. De Backer, D., Donadello, K., Sakr, Y., Ospina-Tascon, G., Salgado, D., Scolletta, S., & Vincent, J.-L. (2013). Microcirculatory alterations in patients with severe sepsis: Impact of time of assessment and relationship with outcome. Critical Care Medicine, 41(3), 791–799. https://doi.org/10.1097/CCM.0b013e3182742e8b.

    Article  CAS  PubMed  Google Scholar 

  4. Bauer, A., Kofler, S., Thiel, M., Eifert, S., & Christ, F. (2007). Monitoring of the sublingual microcirculation in cardiac surgery using orthogonal polarization spectral imaging: preliminary results. Anesthesiology, 107(6), 939–945. https://doi.org/10.1097/01.anes.0000291442.69337.c9.

    Article  PubMed  Google Scholar 

  5. Maier, S., Hasibeder, W. R., Hengl, C., Pajk, W., Schwarz, B., Margreiter, J., et al. (2009). Effects of phenylephrine on the sublingual microcirculation during cardiopulmonary bypass. British Journal of Anaesthesia, 102(4), 485–491. https://doi.org/10.1093/bja/aep018.

    Article  CAS  PubMed  Google Scholar 

  6. De Backer, D., Dubois, M.-J., Schmartz, D., Koch, M., Ducart, A., Barvais, L., & Vincent, J.-L. (2009). Microcirculatory alterations in cardiac surgery: Effects of cardiopulmonary bypass and anesthesia. The Annals of Thoracic Surgery, 88(5), 1396–1403. https://doi.org/10.1016/j.athoracsur.2009.07.002.

    Article  PubMed  Google Scholar 

  7. Elbers, P. W. G., Wijbenga, J., Solinger, F., Yilmaz, A., van Iterson, M., van Dongen, E. P. A., & Ince, C. (2011). Direct observation of the human microcirculation during cardiopulmonary bypass: Effects of pulsatile perfusion. Journal of Cardiothoracic and Vascular Anesthesia, 25(2), 250–255. https://doi.org/10.1053/j.jvca.2010.06.014.

    Article  PubMed  Google Scholar 

  8. Yuruk, K., Almac, E., Bezemer, R., Goedhart, P., de Mol, B., & Ince, C. (2011). Blood transfusions recruit the microcirculation during cardiac surgery. Transfusion, 51(5), 961–967. https://doi.org/10.1111/j.1537-2995.2010.02971.x.

    Article  PubMed  Google Scholar 

  9. O’Neil, M. P., Alie, R., Guo, L. R., Myers, M.-L., Murkin, J. M., & Ellis, C. G. (2018). Microvascular responsiveness to pulsatile and nonpulsatile flow during cardiopulmonary bypass. The Annals of Thoracic Surgery, 105(6), 1745–1753. https://doi.org/10.1016/j.athoracsur.2018.01.007.

    Article  PubMed  Google Scholar 

  10. Koning, N. J., Vonk, A. B. A., Vink, H., & Boer, C. (2016). Side-by-side alterations in glycocalyx thickness and perfused microvascular density during acute microcirculatory alterations in cardiac surgery. Microcirculation, 23(1), 69–74. https://doi.org/10.1111/micc.12260.

    Article  PubMed  Google Scholar 

  11. Dekker, N. A. M., Veerhoek, D., Koning, N. J., van Leeuwen, A. L. I., Elbers, P. W. G., van den Brom, C. E., et al. (2019). Postoperative microcirculatory perfusion and endothelial glycocalyx shedding following cardiac surgery with cardiopulmonary bypass. Anaesthesia, 74(5), 609–618. https://doi.org/10.1111/anae.14577.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. den Uil, C. A., Lagrand, W. K., Spronk, P. E., van Domburg, R. T., Hofland, J., Lüthen, C., et al. (2008). Impaired sublingual microvascular perfusion during surgery with cardiopulmonary bypass: A pilot study. The Journal of Thoracic and Cardiovascular Surgery, 136(1), 129–134. https://doi.org/10.1016/j.jtcvs.2007.10.046.

    Article  Google Scholar 

  13. Nussbaum, C., Haberer, A., Tiefenthaller, A., Januszewska, K., Chappell, D., Brettner, F., et al. (2015). Perturbation of the microvascular glycocalyx and perfusion in infants after cardiopulmonary bypass. The Journal of Thoracic and Cardiovascular Surgery, 150(6), 1474–1481.e1. https://doi.org/10.1016/j.jtcvs.2015.08.050.

    Article  PubMed  Google Scholar 

  14. Scolletta, S., Marianello, D., Isgrò, G., Dapoto, A., Terranova, V., Franchi, F., et al. (2016). Microcirculatory changes in children undergoing cardiac surgery: A prospective observational study. British Journal of Anaesthesia, 117(2), 206–213. https://doi.org/10.1093/bja/aew187.

    Article  CAS  PubMed  Google Scholar 

  15. Ugenti, V., Romano, A. C., & Tibirica, E. (2018). Microvascular endothelial dysfunction during cardiopulmonary bypass in surgery for correction of cyanotic and acyanotic congenital heart disease. Microvascular Research, 120, 55–58. https://doi.org/10.1016/j.mvr.2018.06.004.

    Article  PubMed  Google Scholar 

  16. De Backer, D., Hollenberg, S., Boerma, C., Goedhart, P., Büchele, G., Ospina-Tascon, G., et al. (2007). How to evaluate the microcirculation: Report of a round table conference. Critical Care, 11(5), R101. https://doi.org/10.1186/cc6118.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Ince, C., Boerma, E. C., Cecconi, M., De Backer, D., Shapiro, N. I., Duranteau, J., et al. (2018). Second consensus on the assessment of sublingual microcirculation in critically ill patients: Results from a task force of the European Society of Intensive Care Medicine. Intensive Care Medicine, 44(3), 281–299. https://doi.org/10.1007/s00134-018-5070-7.

    Article  PubMed  Google Scholar 

  18. Gaies, M. G., Gurney, J. G., Yen, A. H., Napoli, M. L., Gajarski, R. J., Ohye, R. G., et al. (2010). Vasoactive-inotropic score as a predictor of morbidity and mortality in infants after cardiopulmonary bypass. Pediatric Critical Care Medicine, 11(2), 234–238. https://doi.org/10.1097/PCC.0b013e3181b806fc.

    Article  PubMed  Google Scholar 

  19. Vellinga, N. A. R., Boerma, E. C., Koopmans, M., Donati, A., Dubin, A., Shapiro, N. I., et al. (2015). International study on microcirculatory shock occurrence in acutely ill patients. Critical Care Medicine, 43(1), 48–56. https://doi.org/10.1097/CCM.0000000000000553.

    Article  PubMed  Google Scholar 

  20. den Os, M. M., van den Brom, C. E., van Leeuwen, A. L. I., & Dekker, N. A. M. (2020). Microcirculatory perfusion disturbances following cardiopulmonary bypass: A systematic review. Critical Care, 24(1), 218. https://doi.org/10.1186/s13054-020-02948-w.

    Article  Google Scholar 

  21. De Blasi, R. A., Palmisani, S., Boezi, M., Arcioni, R., Collini, S., Troisi, F., & Pinto, G. (2008). Effects of remifentanil-based general anaesthesia with propofol or sevoflurane on muscle microcirculation as assessed by near-infrared spectroscopy. British Journal of Anaesthesia, 101(2), 171–177. https://doi.org/10.1093/bja/aen136.

    Article  CAS  PubMed  Google Scholar 

  22. Koch, M., De Backer, D., Vincent, J. L., Barvais, L., Hennart, D., & Schmartz, D. (2008). Effects of propofol on human microcirculation. British Journal of Anaesthesia, 101(4), 473–478. https://doi.org/10.1093/bja/aen210.

    Article  CAS  PubMed  Google Scholar 

  23. Liu, X., Zhang, K., Wang, W., Xie, G., Cheng, B., Wang, Y., et al. (2016). Dexmedetomidine versus propofol sedation improves sublingual microcirculation after cardiac surgery: A randomized controlled trial. Journal of Cardiothoracic and Vascular Anesthesia, 30(6), 1509–1515. https://doi.org/10.1053/j.jvca.2016.05.038.

    Article  CAS  PubMed  Google Scholar 

  24. Riedijk, M. A., & Milstein, D. M. J. (2018). Imaging sublingual microcirculatory perfusion in pediatric patients receiving procedural sedation with propofol: A pilot study. Microcirculation, e12484. https://doi.org/10.1111/micc.12484

  25. Özarslan, N. G., Ayhan, B., Kanbak, M., Çelebioğlu, B., Demircin, M., Ince, C., & Aypar, Ü. (2012). Comparison of the effects of sevoflurane, isoflurane, and desflurane on microcirculation in coronary artery bypass graft surgery. Journal of Cardiothoracic and Vascular Anesthesia, 26(5), 791–798. https://doi.org/10.1053/j.jvca.2012.03.019.

    Article  CAS  PubMed  Google Scholar 

  26. Maar, S. P. (2008). Searching for the Holy Grail: A review of markers of tissue perfusion in pediatric critical care. Pediatric Emergency Care, 24(12), 883–887. https://doi.org/10.1097/PEC.0b013e31819112b7.

    Article  PubMed  Google Scholar 

  27. Englehart, M. S., & Schreiber, M. A. (2006). Measurement of acid-base resuscitation endpoints: Lactate, base deficit, bicarbonate or what? Current Opinion in Critical Care, 12(6), 569–574. https://doi.org/10.1097/MCC.0b013e328010ba4f.

    Article  PubMed  Google Scholar 

  28. Holley, A., Lukin, W., Paratz, J., Hawkins, T., Boots, R., & Lipman, J. (2012). Review article: Part two: Goal-directed resuscitation--Which goals? Perfusion targets. Emergency Medicine Australasia, 24(2), 127–135. https://doi.org/10.1111/j.1742-6723.2011.01515.x.

    Article  PubMed  Google Scholar 

  29. González, R., Urbano, J., Solana, M. J., Hervías, M., Pita, A., Pérez, R., et al. (2019). Microcirculatory differences in children with congenital heart disease according to cyanosis and age. Frontiers in Pediatrics, 7, 264. https://doi.org/10.3389/fped.2019.00264.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Boerma, E. C., & Ince, C. (2010). The role of vasoactive agents in the resuscitation of microvascular perfusion and tissue oxygenation in critically ill patients. Intensive Care Medicine, 36(12), 2004–2018. https://doi.org/10.1007/s00134-010-1970-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Buijs, E. A. B., Verboom, E. M., Top, A. P. C., Andrinopoulou, E.-R., Buysse, C. M. P., Ince, C., & Tibboel, D. (2014). Early microcirculatory impairment during therapeutic hypothermia is associated with poor outcome in post-cardiac arrest children: A prospective observational cohort study. Resuscitation, 85(3), 397–404. https://doi.org/10.1016/j.resuscitation.2013.10.024.

    Article  PubMed  Google Scholar 

  32. Ergenekon, E., Hirfanoğlu, I., Beken, S., Turan, O., Kulali, F., Koç, E., & Gücüyener, K. (2013). Peripheral microcirculation is affected during therapeutic hypothermia in newborns. Archives of Disease in Childhood. Fetal and Neonatal Edition, 98(2), F155–F157. https://doi.org/10.1136/archdischild-2012-301647.

    Article  PubMed  Google Scholar 

  33. González, R., Urbano, J., López, J., Solana, M. J., Botrán, M., García, A., et al. (2016). Microcirculatory alterations during haemorrhagic shock and after resuscitation in a paediatric animal model. Injury, 47(2), 335–341. https://doi.org/10.1016/j.injury.2015.10.075.

    Article  PubMed  Google Scholar 

  34. González, R., López, J., Urbano, J., Solana, M. J., Fernández, S. N., Santiago, M. J., & López-Herce, J. (2017). Evaluation of sublingual microcirculation in a paediatric intensive care unit: Prospective observational study about its feasibility and utility. BMC Pediatrics, 17(1), 75. https://doi.org/10.1186/s12887-017-0837-5.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the contribution to the study of all members of the infant heart area of Gregorio Marañón General University Hospital. The authors would like to specially acknowledge the patients and their families who decided to collaborate with our study.

Funding

This study was partially funded by the Mutua Madrileña Foundation (grant FMM 14/02), by the Spanish Society of Paediatric Intensive Care (Francisco Ruza’s grant 2017), and by the Carlos III Health Institute Subdirectorate General for Research Assessment and Promotion, and the European Regional Development Fund (ERDF) (grant PI17/01319).

Author information

Authors and Affiliations

  1. Paediatric Intensive Care Unit, Gregorio Marañón General University Hospital, Calle Dr. Castelo 47, 28007, Madrid, Spain

    Rafael González Cortés, Javier Urbano Villaescusa, María J. Solana García, Jorge López González, Sarah N. Fernández Lafever & Jesús López-Herce Cid

  2. Mother and Child Health and Development Network (REDSAMID), ISCIII Subdirectorate General for Research Assessment and Promotion and the ERDF (RD16/0022), Madrid, Spain

    Rafael González Cortés, Javier Urbano Villaescusa, María J. Solana García, Jorge López González, Sarah N. Fernández Lafever & Jesús López-Herce Cid

  3. Paediatric Hemoperfusionist, Gregorio Marañón General University Hospital, Madrid, Spain

    Blanca Ramírez Gómez

  4. Paediatric Anesthesia, Gregorio Marañón General University Hospital, Madrid, Spain

    José R. Fuentes Moran, Irene Hidalgo García & Ana Peleteiro Pensado

  5. Paediatric Cardiac Surgery, Gregorio Marañón General University Hospital, Madrid, Spain

    Ramón Pérez-Caballero Martínez & Carlos A. Pardo Prado

  6. Paediatric Cardiology, Gregorio Marañón General University Hospital, Madrid, Spain

    Alejandro Rodríguez Ogando & María López Blazquez

  7. Department of Paediatrics, School of Medicine, Complutense University of Madrid, Madrid, Spain

    Jesús López-Herce Cid

Authors
  1. Rafael González Cortés
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Javier Urbano Villaescusa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. María J. Solana García
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jorge López González
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sarah N. Fernández Lafever
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Blanca Ramírez Gómez
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. José R. Fuentes Moran
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Irene Hidalgo García
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ana Peleteiro Pensado
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ramón Pérez-Caballero Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Carlos A. Pardo Prado
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Alejandro Rodríguez Ogando
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. María López Blazquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Jesús López-Herce Cid
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rafael González Cortés.

Ethics declarations

Human Subjects/Informed Consent Statement

The study was approved by Gregorio Marañón General University Hospital Institutional Review Board. All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation and with the Helsinki Declaration of 1975, as revised in 2000. Informed consent was obtained from all patients or their legal representatives for being included in the study

Conflict of Interest

The authors declare no competing interests.

Additional information

Associate Editor Junjie Xiao oversaw the review of this article

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González Cortés, R., Urbano Villaescusa, J., Solana García, M.J. et al. Microcirculatory Changes in Pediatric Patients During Congenital Heart Defect Corrective Surgery. J. of Cardiovasc. Trans. Res. 14, 1173–1185 (2021). https://doi.org/10.1007/s12265-021-10132-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12265-021-10132-w

Keywords

Search

Navigation