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The effect of red blood cell transfusion on the microcirculation of anemic children

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Abstract

Red blood cell transfusion can improve but also might temporarily reduce the microcirculation. The buccal microcirculation was visualized and total vessel density (TVD) determined with sidestream dark field imaging in 19 pediatric anemic (Hb 7.2 g/dL, 95 % CI 6.5–7.9) oncology or hematology patients receiving red blood cell transfusions (Tx) and in 18 age-matched healthy non-anemic controls. After transfusion, Hb (8.0 g/dL, 95 % CI 7.3–8.6) and TVD increased (14.7 ± 1.7 versus 16.6 ± 2.0 mm/mm2) significantly with a concomitant decrease in RBC velocity in medium-sized vessels (pre-Tx 711 ± 199 versus post-Tx 627 ± 163 μm/s). Compared to the controls, pre-Tx TVD (17.5 ± 1.3 mm/mm2) was lower and RBC velocity (476 ± 77 μm/s) was significantly higher. After transfusion, TVD and RBC velocity remained significantly lower and higher, respectively. In a subgroup, analysis of the transfused children with infection of TVD at baseline was lower with a larger increase after transfusion compared to anemic children without infection (ΔTVD 3.4 ± 2.6 versus ΔTVD 1.3 ± 1.5 mm/mm2).

Conclusion: With the rise of hemoglobin after transfusion, significant improvements of tissue perfusion were demonstrated but differences to non-anemic controls persisted. In particular, the microcirculation of anemic oncology patients with infection improved after transfusion.

What is Known:

• Transfusions can improve but also temporarily reduce the microcirculation.

• In neonates, transfusion significantly increases total vessel density.

What is New:

• Pretransfusion, the microcirculation of the anemic children differed significantly from the controls.

• After transfusion, the microcirculation improved but still differed from the controls.

• These changes were most profound in anemic patients with concurrent infection, therefore transfusion threshholds might need to be higher.

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Abbreviations

CG:

Control group

InfGroup:

Anemic group with infections

nInfGroup:

Anemic group without infections

LED:

Light-emitting diode

pre-Tx:

Before transfusion

pTx1:

After transfusion

pTx2:

48–72 h after transfusion

TVD:

Total vessel density

RBC Tx:

Red blood cell transfusion

SDF:

Sidestream dark field

Tx G:

Transfusion group

References

  1. Basran S, Frumento RJ, Cohen A, Lee S, Du Y, Nishanian E, Kaplan HS, Stafford-Smith M, Bennett-Guerrero E (2006) The association between duration of storage of transfused red blood cells and morbidity and mortality after reoperative cardiac surgery. Anesth Analg 103:15–20, table of contents

    Article  PubMed  Google Scholar 

  2. Bosman GJCGM, Werre JM, Willekens FLA, Novotný VMJ (2008) Erythrocyte ageing in vivo and in vitro: structural aspects and implications for transfusion. Transfus Med 18:335–347

    Article  CAS  PubMed  Google Scholar 

  3. Creteur J, Neves AP, Vincent J-L (2009) Near-infrared spectroscopy technique to evaluate the effects of red blood cell transfusion on tissue oxygenation. Crit Care 13(Suppl 5):S11. doi:10.1186/cc8009

    Article  PubMed  PubMed Central  Google Scholar 

  4. De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL (2002) Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med 166:98–104

    Article  PubMed  Google Scholar 

  5. De Backer D, Hollenberg S, Boerma C, Goedhart P, Buchele G, Ospina-Tascon G, Dobbe I, Ince C (2007) How to evaluate the microcirculation? Report of a round table conference. Crit Care 11:R101–R101

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ellis CG, Jagger J, Sharpe M (2005) The microcirculation as a functional system. Crit Care 9(Suppl 4):S3–S8

    Article  PubMed  PubMed Central  Google Scholar 

  7. Friedlander MH, Simon R, Machiedo GW (1998) The relationship of packed cell transfusion to red blood cell deformability in systemic inflammatory response syndrome patients. Shock 9:84–88

    Article  CAS  PubMed  Google Scholar 

  8. Gauvin F, Spinella PC, Lacroix J, Choker G, Ducruet T, Karam O, Hébert PC, Hutchison JS, Hume HA, Tucci M et al (2010) Association between length of storage of transfused red blood cells and multiple organ dysfunction syndrome in pediatric intensive care patients. Transfusion 50:1902–1913. doi:10.1111/j.1537-2995.2010.02661.x

    Article  PubMed  Google Scholar 

  9. Glas V, Genzel-Borovicz O, Christ F (2004) Elective transfusion leads to an increase in functional capillary density in the skin of preterm neonates. Pediatr Res 54:599–599

    Google Scholar 

  10. Goedhart PT, Khalilzada M, Bezemer R, Merza J, Ince C (2007) Sidestream dark field (SDF) imaging: a novel stroboscopic LED ring-based imaging modality for clinical assessment of the microcirculation. Opt Express 15:15101–15114

    Article  CAS  PubMed  Google Scholar 

  11. Gould S, Cimino MJ, Gerber DR (2007) Packed red blood cell transfusion in the intensive care unit: limitations and consequences. Am J Crit Care 16:39–48, quiz 49

    PubMed  Google Scholar 

  12. Harris AG, Sinitsina I, Messmer K (2002) Validation of OPS imaging for microvascular measurements during isovolumic hemodilution and low hematocrits. Am J Physiol Heart Circ Physiol 282:H1502–H1509

    Article  CAS  PubMed  Google Scholar 

  13. Kerger H, Saltzman DJ, Menger MD, Messmer K, Intaglietta M (1996) Systemic and subcutaneous microvascular Po2 dissociation during 4-h hemorrhagic shock in conscious hamsters. Am J Physiol 270:H827–H836

    CAS  PubMed  Google Scholar 

  14. Kneyber MCJ, Gazendam RP, Markhorst DG, Plötz FB (2009) Length of storage of red blood cells does not affect outcome in critically ill children. Intensive Care Med 35:179–180

    Article  PubMed  Google Scholar 

  15. Marik PE, Sibbald WJ (1993) Effect of stored-blood transfusion on oxygen delivery in patients with sepsis. JAMA 269:3024–3029

    Article  CAS  PubMed  Google Scholar 

  16. Nolte D, Zeintl H, Steinbauer M, Pickelmann S, Messmer K (1995) Functional capillary density: an indicator of tissue perfusion? Int J Microcirc Clin Exp 15:244–249, Sponsored by the European Society for Microcirculation

    Article  CAS  PubMed  Google Scholar 

  17. Roseff SD, Luban NLC, Manno CS (2002) Guidelines for assessing appropriateness of pediatric transfusion. Transfusion 42:1398–1413

    Article  PubMed  Google Scholar 

  18. Sadaka F, Aggu-Sher R, Krause K, O'Brien J, Armbrecht ES, Taylor RW (2011) The effect of red blood cell transfusion on tissue oxygenation and microcirculation in severe septic patients. Ann Intensive Care 1:46. doi:10.1186/2110-5820-1-46

    Article  PubMed  PubMed Central  Google Scholar 

  19. Sakr Y (2004) Persistent microcirculatory alterations are associated with organ failure and death in patients with septic shock. Crit Care Med 32:1825–1831

    Article  PubMed  Google Scholar 

  20. Sakr Y, Chierego M, Piagnerelli M, Verdant C, Dubois MJ, Koch M, Creteur J, Gullo A, Vincent JL, De Backer D (2007) Microvascular response to red blood cell transfusion in patients with severe sepsis. Crit Care Med 35:1639–1644. doi:10.1097/01.CCM.0000269936.73788.3

    Article  PubMed  Google Scholar 

  21. Salazar Vázquez BY, Martini J, Chávez Negrete A, Cabrales P, Tsai AG, Intaglietta M (2009) Microvascular benefits of increasing plasma viscosity and maintaining blood viscosity: counterintuitive experimental findings. Biorheology 46:167–179

    PubMed  Google Scholar 

  22. Saldivar E, Cabrales P, Tsai AG, Intaglietta M (2003) Microcirculatory changes during chronic adaptation to hypoxia. Am J Physiol Heart Circ Physiol 285:H2064–H2071

    Article  CAS  PubMed  Google Scholar 

  23. Seidl T, Genzel-Boroviczeny O, Abicht JM, Christ F (2004) Does red blood cell transfusion change the near infra red photoplethysmography signal in infants? Intensive Care Med 30:1602–1606

    Article  PubMed  Google Scholar 

  24. Stapley R, Owusu BY, Brandon A, Cusick M, Rodriguez C, Marques MB, Kerby JD, Barnum SR, Weinberg JA, Lancaster JR Jr et al (2012) Erythrocyte storage increases rates of NO and nitrite scavenging: implications for transfusion-related toxicity. Biochem J 446:499–508. doi:10.1042/bj20120675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Tinmouth A, Chin-Yee I (2001) The clinical consequences of the red cell storage lesion. Transfus Med Rev 15:91–107

    Article  CAS  PubMed  Google Scholar 

  26. Top AP, van Dijk M, van Velzen JE, Ince C, Tibboel D (2011) Functional capillary density decreases after the first week of life in term neonates. Neonatology 99:73–77

    Article  CAS  PubMed  Google Scholar 

  27. Tsai AG, Friesenecker B, McCarthy M, Sakai H, Intaglietta M (1998) Plasma viscosity regulates capillary perfusion during extreme hemodilution in hamster skinfold model. Am J Physiol Heart Circ Physiol 275:H2170–H2180

    CAS  Google Scholar 

  28. Walsh TS, Saleh E-E-D (2006) Anaemia during critical illness. Br J Anaesth 97:278–291

    Article  CAS  PubMed  Google Scholar 

  29. Weinberg JR, Boyle P, Thomas K, Murphy K, Tooke JE, Guz A (1991) Capillary blood cell velocity is reduced in fever without hypotension. Int J Microcirc Clin Exp 10:13–19

    CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  31. Yürük K, Milstein DMJ, Bezemer R, Bartels SA, Biemond BJ, Ince C (2013) Transfusion of banked red blood cells and the effects on hemorheology and microvascular hemodynamics in anemic hematology outpatients. Transfusion 53:1346–1352. doi:10.1111/j.1537-2995.2012.03905.x

    Article  PubMed  Google Scholar 

  32. Zimrin AB, Hess JR (2009) Current issues relating to the transfusion of stored red blood cells. Vox Sang 96:93–103

    Article  CAS  PubMed  Google Scholar 

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Contributions

C. M. Schinagl recruited the patients, obtained the images, collected and analyzed the data, and wrote the first draft.

Z. H. Mormanova and I. Schmid were involved in planning the study; in addition, Z.M was very important in adapting the method to children.

A. Puchwein-Schwepcke was integral in writing the manuscript and establishing the method.

O. Genzel-Boroviczény planned the study and wrote the final manuscript.

Author information

Authors and Affiliations

  1. Division of Neonatology, Dr. von Hauner Children’s Hospital Medical Center University Munich, 80337, Munich, Germany

    Carina M. Schinagl, Zuzana H. Mormanova, Alexandra Puchwein-Schwepcke & Orsolya Genzel-Boroviczény

  2. Division of Hematology and Oncology, Dr. von Hauner Children’s Hospital Medical Center University Munich, 80337, Munich, Germany

    Irene Schmid

Authors
  1. Carina M. Schinagl
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  2. Zuzana H. Mormanova
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  3. Alexandra Puchwein-Schwepcke
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  4. Irene Schmid
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  5. Orsolya Genzel-Boroviczény
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Corresponding author

Correspondence to Orsolya Genzel-Boroviczény.

Ethics declarations

Human and animal rights and informed consent

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments. All parents of the patients gave informed consent.

Conflict of interest

No financial assistance was received in support of this study; no conflict of interest to report from any of the authors; and no honorarium, grant, or other payment was given to anybody to produce the manuscript.

C. Schinagl declares no conflict of interest. Z. Mormanova declares no conflict of interest. A. Puchwein-Schwepcke declares no conflict of interest. I. Schmid declares no conflict of interest. O. Genzel-Boroviczeny declares no conflict of interest.

Additional information

Communicated by David Nadal

Revisions received: 11 November 2015; 2 January 2016 (2)

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Schinagl, C.M., Mormanova, Z.H., Puchwein-Schwepcke, A. et al. The effect of red blood cell transfusion on the microcirculation of anemic children. Eur J Pediatr 175, 793–798 (2016). https://doi.org/10.1007/s00431-016-2704-z

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  • DOI: https://doi.org/10.1007/s00431-016-2704-z

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