Skip to main content
SpringerLink
Log in

Microvascular ultrastructure in non-freezing cold injuries

  • Published:
Research in Experimental Medicine

Summary

The effects of repeated local exposure to cold on the integrity of the subcutaneous microcirculation were studied in a model using a transparent tissue chamber implanted into a dorsal skin fold of Syrian hamsters. A detailed study of the vascular ultrastructure within the chamber revealed the following features: Endothelial damage was prominent in true capillaries and venous vessels, while arterioles remained unaffected. The endothelial lining appeared extremely attenuated around the entire vascular perimeter causing the development of “gaps”, some of which contained leukocytes or platelets. Smaller vessels were often completely filled with blood cells with leukocytes integrated into the endothelial wall. Fibrin was never observed within these occluded vessels. Finally, only veil-like remnants of the endothelium persisted, and compressed erythrocytes were still mimicking the original vascular outline. It is concluded that the ultrastructural changes observed after a repeated non-freezing cold injury closely resemble those observed during ischemia/reperfusion injury.

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

Similar content being viewed by others

References

  1. Albrektsson B (1972) Late microvascular changes after slow and rapid thawing of frozen tissue. Adv Microcirc 4:161–176

    Google Scholar 

  2. Albrektsson B, Brånemark RI (1969) Early microvascular reactions to slow and rapid thawing of frozen tissue. Adv Microcirc 2:37–68

    Google Scholar 

  3. Arturson G (1966) Capillary permeability in experimental rapid freezing with rapid and slow rewarming. Acta Chir Scand 131:402–407

    PubMed  CAS  Google Scholar 

  4. Aschoff J (1944) Über die Kältedilatation der Extremität des Menschen in Eiswasser. Pflügers Arch 248:183–196

    Article  Google Scholar 

  5. Bagge U, Amundson B, Lauritsen C (1980) White blood cell deformability and plugging of skeletal muscle capillaries in hemorrhagic shock. Acta Physiol Scand 108:159–163

    Article  PubMed  CAS  Google Scholar 

  6. Barker JH, Bartlett R, Funk W, Hammersen F, Meßmer K (1987) The effect of superoxide dismutase on the skin microcirculation after ischemia and reperfusion, Prog Appl Microcirc 12:276–281

    Google Scholar 

  7. Bowers WD Jr, Hubbard RW, Daum RC, Ashbaugh P, Nilson E (1973) Ultrastructural studies of muscle cells and vascular endothelium immediately after freeze-thaw injury. Cryobiology 10:9–21

    Article  PubMed  Google Scholar 

  8. Brown E, Landis EM (1947) Effect of local cooling on fluid movement, effective osmotic pressure and capillary permeability in the frog's mesentery. Am J Physiol 149:302–315

    Google Scholar 

  9. Clark ER, Clark EL, Rex RD (1936) Observations on polymorphonuclear leukocytes in living animal. Am J Anat 59:123–173

    Article  Google Scholar 

  10. Endrich B, Meßmer K (1984) Quantitative analysis of the microcirculation in the awake animal. In: Olszewski ML (ed) Handbook of microsurgery, vol 1. CRC Press, Boca Raton, pp 79–105

    Google Scholar 

  11. Endrich B, Asaishi K, Goetz A, Meßmer K (1980) Technical report. A new chamber technique for microvascular studies in unanesthetized hamsters. Res Exp Med 177:125–134

    Article  CAS  Google Scholar 

  12. Endrich B, Laprell-Moschner C, Brendel W, Meßmer K (1982) Effects of prolonged cold injury on the subcutaneous microcirculation of the hamster: I. Technique, morphology and tissue oxygenation. Res Exp Med 181:49–61

    Article  CAS  Google Scholar 

  13. Funk W, Endrich B, Meßmer K, Intaglietta M (1983) Spontaneous arteriolar vasomotion as a determinant of peripheral vascular resistance. Int J Microcirc Clin Exp 2:11–25

    PubMed  CAS  Google Scholar 

  14. Faustmann PM, Dermietzel R (1985) Extravasation of polymorphonuclear leukocytes from the cerebral microvasculature. Inflammatory response induced by alpha-bungarotoxin. Cell Tissue Res 242:399–407

    Article  PubMed  CAS  Google Scholar 

  15. Gaehtgens P (1987) Pathway and interactions of white cells in the microcirculation. Prog Appl Microcirc 12:51–66

    Google Scholar 

  16. Grant L (1973) The sticking and emigration of white blood cells in inflammation. In: Zweifach BW, Grant L, McCluskey RT (eds) The inflammatory process. Academic Press, New York London, pp 205–249

    Google Scholar 

  17. Hammersen F, Hammersen E (1987) The ultrastructure of endothelial gap-formation and leukocyte emigration. Prog Appl Microcirc 12:1–34

    Google Scholar 

  18. Hammersen F, Endrich B, Meßmer K (1985) The fine structure of tumor blood vessels: I. Participation of non-endothelial cells in tumor angiogenesis. Int J Microcirc Clin Exp 4:31–43

    PubMed  CAS  Google Scholar 

  19. Höflin FG, Rahn BA, Perren SM, Ziegler WJ (1977) Rasches oder langsames Wiedererwärmen? Ärztl Praxis 21:1035–1041

    Google Scholar 

  20. Lewis RE, Granger HJ (1988) Diapedesis and the permeability of venous microvessels to protein macromolecules: the impact of leukotriene B4(LTB4). Microvasc Res 35:27–47

    Article  PubMed  Google Scholar 

  21. Lewis RB, Gerstner HB (1954) Blood flow as indicated by temperature changes in rabbit legs before and after exposure to local cold. Am J Physiol 117:501–503

    Google Scholar 

  22. Meßmer K, Funk W, Endrich B, Zeintl H (1984) The perspectives of new methods in microcirculation research. Prog Appl Microcirc 6:77–90

    Google Scholar 

  23. Metzger HP, Brüggemann H, Plewnia A (1987) The use of fluorescent-protein conjugates for staining brain capillaries in hypo-and hyperthermia (26–42°C). Microvasc Res 34:311–317

    Article  PubMed  CAS  Google Scholar 

  24. Movat HZ (1985) The inflammatory reaction. Elsevier Science Biomed Division, Amsterdam New York Oxford

    Google Scholar 

  25. Rabb JM, Renaud ML, Brandt PA, Witt CW (1974) Effect of freezing and thawing on the microcirculation and capillary endothelium of the hamster cheek pouch. Cryobiology 11: 508–518

    Article  PubMed  CAS  Google Scholar 

  26. Sack FU, Funk W, Hammersen F, Meßmer K (1987) Microvascular injury of skeletal muscle and skin after different periods of pressure induced ischemia. Prog Appl Microcirc 12: 282–288

    Google Scholar 

  27. Schindelmeiser J, Bergmann M, Lehmenkühler A, Kersting U (1987) Tracer permeability of rat cortical blood vessels during regional hypothermia. Acta Neuropathol (Berl) 73: 349–356

    Article  CAS  Google Scholar 

  28. Schmid-Schoenbein GW (1987) Mechanisms of granulocyte-capillary-plugging. Prog Appl Microcirc 12:223–230

    Google Scholar 

  29. Schmid-Schoenbein GW, Engler RL (1986) Granulocytes as active participants in acute myocardial ischemia and infarction. Am J Cardiovasc Pathol 1:15–30

    Google Scholar 

  30. Suval WD, Duran WN, Boric MP, Hobson RW, Berendsen PB, Ritter AB (1987) Microvascular transport and endothelial cell alterations preceding skeletal muscle damage in ischemia and reperfusion injury. Am J Surg 154:211–218

    Article  PubMed  CAS  Google Scholar 

  31. Svanes K, Zweifach BW, Intaglietta M (1970) Effect of hypothermia on transcapillary fluid exchange. Am J Physiol 218:981–989

    PubMed  CAS  Google Scholar 

  32. Trusal LR, Guzman AW, Baker CJ (1984) Characterization of freeze-thaw induced ultrastructural damage to endothelial cells in vitro. In Vitro 20:353–364

    PubMed  CAS  Google Scholar 

  33. Tuma RF (1985) White cell adherence in microvessels. Prog Appl Microcirc 7:31–42

    CAS  Google Scholar 

  34. Unterberg A, Wahl M, Hammersen F, Baethmann A (1987) Permeability, and vasomotor response of cerebral vessels during exposure to arachidonic acid. Acta Neuropathol (Berl) 73:209–219

    Article  CAS  Google Scholar 

  35. Vanhoutte PM, Janssens WJ (1978) Local control of venous function. Microvasc Res 16: 196–214

    Article  PubMed  CAS  Google Scholar 

  36. Wiedeman MP, Brigham MP (1971) The effects of cooling on the microvasculature after thermal injury. Microvasc Res 3:154–161

    Article  PubMed  CAS  Google Scholar 

  37. Zarins CK, Skinner DB (1975) Hemodynamics and blood flow distribution following prolonged circulation at 5°C. Am J Physiol 229:275–278

    PubMed  CAS  Google Scholar 

  38. Zweifach BW (1973) Microvascular aspects of tissue injury. In: Zweifach BW, Grant L, McCluskey RT (eds) The inflammatory process. Academic Press, New York London, pp 3–46

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Experimental Surgery, University of Heidelberg, Heidelberg, Federal Republic of Germany

    B. Endrich, F. Hammersen & K. Meßmer

  2. Institute of Anatomy, Technical University of Munich, Munich, Federal Republic of Germany

    B. Endrich, F. Hammersen & K. Meßmer

Authors
  1. B. Endrich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Hammersen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Meßmer
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Endrich, B., Hammersen, F. & Meßmer, K. Microvascular ultrastructure in non-freezing cold injuries. Res. Exp. Med. 190, 365–379 (1990). https://doi.org/10.1007/BF00000043

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00000043

Key words

Search

Navigation