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[Cancer Research 48, 2641-2658, May 15, 1988]
© 1988 American Association for Cancer Research
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Determinants of Tumor Blood Flow: A Review1

Rakesh K. Jain

Department of Chemical Engineering, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213-3890

Blood flow rate in a vascular network is proportional to the pressure difference between the arterial and venous sides and inversely proportional to the viscous and geometric resistances. Despite rapid progress in recent years, there is a paucity of quantitative data on these three determinants of blood flow in tumors and several questions remain unanswered. This paper reviews our current knowledge of these three parameters for normal and neoplastic tissues, the methods of their measurements, and the implications of the results in the growth and metastasis formation as well as in the detection and treatment of tumors.

Microvascular pressures in the arterial side are nearly equal in tumor and nontumorous vessels. Pressures in venular vessels, which are numerically dominant in tumors, are significantly lower in a tumor than those in a nontumorous tissue. Decreased intravascular pressure and increased interstitial pressure in tumors are partly responsible for the vessel collapse as well as the flow stasis and reversal in tumors.

The apparent viscosity (viscous resistance) of blood is governed by the viscosity of plasma and the number, size, and rigidity of blood cells. Plasma viscosity can be increased by adding certain solutes. The concentration of cells can be increased by adding cells to blood or by reducing plasma volume. The rigidity of RBC, which are numerically dominant in blood, can be increased by lowering pH, elevating temperature, increasing extracellular glucose concentration, or making the suspending medium hypo- or hypertonic. Effective size of blood cells can be increased by forming RBC aggregates (also referred to as rouleaux). RBC aggregation can be facilitated by lowering the shear rate (i.e., decreasing velocity gradients) or by adding macromolecules (e.g., fibrinogen, globulins, dextrans). Since cancer cells and WBC are significantly more rigid than RBC, their presence in a vessel may also increase blood viscosity and may even cause transient stasis. Finally, due to the relatively large diameters of tumor microvessels the Fahraeus effect (i.e., reduction in hematocrit in small vessels) and the Fahraeus-Lindqvist effect (i.e., reduction in blood viscosity in small vessels) may be less pronounced in tumors than in normal tissues.

Geometric resistance for a network of vessels is a complex function of the vascular morphology, i.e., the number of vessels of various types, their branching pattern, and their length and diameter. Geometric resistance to flow in a single vessel is proportional to the vessel length and inversely proportional to vessel diameter to the fourth power. Hence, vessel diameter is the dominant parameter in flow regulation. In normal tissues, changes in vessel diameter are mediated primarily via smooth muscle cells. A tumor has two types of vessels: those recruited from the preexisting network of the host vasculature; and those resulting from the angiogenic response to cancer cells. Since a tumor rarely invades the arteries and arterioles of the host vasculature, the smooth muscle cells, with their contractile and nervous apparatus, surrounding these vessels may respond to physical or chemical stimuli. Since the newly formed vessels lack smooth muscle cells, they may not respond to these stimuli. As a result, the overall response of tumors will depend on the ratio of host vessels to newly formed vessels. This ratio would vary from one location to another and from one day to the next in the same tumor and from one tumor to another.

Recent studies suggest that endothelial cells and pericytes also possess contractile elements capable of causing changes in vessel diameter. The extent to which these cells control blood flow is not known. Other factors which may contribute to changes in effective diameter of tumor vessels include: swelling or destruction of endothelial cells; adhesion of platelets, WBC, or cancer cells to the vascular endothelium; and partial or total collapse of a vessel due to increased interstitial and decreased microvascular pressures. Due to micro- and macroscopic heterogeneities in the tumor microcirculation, care must be exercised in extrapolating from one tumor to another.

1 This article is based on research supported by grants from the National Cancer Institute, the National Science Foundation, and the Richard K. Mellon Foundation; by a NIH Research Career Development Award; and by a Guggenheim Fellowship.

Received 8/31/87. Revised 2/ 1/88. Accepted 2/23/88.




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