Location and size of carotid body-like organs (paraganglia) revealed in rats by the permeability of blood vessels to Evans blue dye

Abstract

Summary We determined the number, distribution, size, and morphology of paraganglia near the glossopharyngeal, vagus, and sympathetic nerves of rats. The location of paraganglia was revealed by a method that takes advantage of the comparatively high permeability of their blood vessels to Evans blue dye. Rats were fixed by vascular perfusion of glutaraldehyde 2 min after receiving an intravenous injection of Evans blue dye. Paraganglia appeared as circumscribed, intensely blue structures that were readily distinguished from unstained nerves associated with them. Similarly, some groups of small intensely fluorescent (SIF) cells in autonomic and sensory ganglia were surrounded by Evans blue at a time that other portions of the ganglia contained little detectable dye. An average of 92.5 (range 41–134) paraganglia and 41 (range 17–68) blue spots in ganglia were found in the neck, thorax and abdomen of each of 10 rats. Carotid bodies had a mean length of 601 ± 123 μm, width of 275 ± 65 μm, and volume of 25.1 ± 11.2,μm³ × 10⁶. Other paraganglia had an average length of 168 ± 108μm, width of 77 ± 41 μm, and volume of 0.87 ± 1.55 μm³ × 10⁶. The total volume of paraganglion tissue averaged 128 μm³ × 10⁶ (range 62–215 μm³ × 10⁶), 59% of which was due to paraganglia other than the carotid bodies. By using fluorescence microscopy, we verified that small catecholamine-containing cells, visible because of their yellow-green fluorescence induced by formaldehyde gas, were located in regions along nerves and within ganglia that contained extravascular dye, visible because of its red fluorescence. Electron-microscopic studies confirmed that blue-stained organs (presumptive paraganglia) associated with the superior laryngeal nerve and other branches of the vagus nerve contained cells morphologically similar to glomus cells of the carotid body. Celiac ganglia contained, in addition, some cells similar to chromaffin cells of the adrenal medulla. Paraganglia (but not SIF cells in ganglia) were encapsulated by layers of perineurium, which may constitute a barrier to diffusion. Tortuous thin-walled blood vessels, some with a fenestrated endothelium, were present in all paraganglia examined and were near most groups of SIF cells in ganglia. Neural connections of the small catecholamine-containing cells varied. Most nerve terminals on cells in paraganglia resembled sensory nerve endings on glomus cells of the carotid body, although some were morphologically similar to preganglionic nerves on chromaffin cells of the adrenal medulla.