Photoactivation of rose bengal leads to the generation of reactive oxygen intermediates (predominantly singlet oxygen with some superoxide anion) which are potentially injurious to biological systems. Isolated rat hearts were perfused aerobically at 37 degrees C with bicarbonate buffer for 10 min without rose bengal and for 10 min with rose bengal (500 nM). During the last 5 min of perfusion with rose bengal, hearts were globally illuminated (5500 lux) with light (530 to 590 nm) and electrocardiographic changes were detected within 2.7 +/- 0.3 s (approximately 15 beats) of the onset of illumination. All hearts developed ventricular premature beats, ventricular tachycardia and complete atrioventricular block after 20.2 +/- 6.6, 68.0 +/- 29.7 and 184.3 +/- 20.9 s, respectively. Photoactivation by rose bengal also resulted in severe ultrastructural damage including intracellular clarifications, swelling of mitochondria with disruption and clumping of cristae and the development of contraction band necrosis. Extensive degranulation of mast cells was also observed. These changes were most evident in myocytes adjacent to large epicardial blood vessels. Cytochemical studies demonstrated that there was a loss of the calcium which is normally localized at the inner sarcolemmal surface, and the appearance of intramitochondrial calcium precipitates. In control hearts (no illumination and/or no rose bengal), arrhythmias did not develop and tissue morphology and calcium distribution remained normal. In additional studies, rose bengal-perfused hearts were illuminated regionally for 10 min over an area (approximately 6 mm2) of the left ventricle. Extensive tissue injury and calcium overload developed in the area of maximum illumination.(ABSTRACT TRUNCATED AT 250 WORDS)