Previous studies have suggested that greater arterial concentrations of undegraded low density lipoprotein (LDL) and/or greater arterial rates of LDL degradation may play role(s) in determining regional differences in arterial susceptibility to atherosclerosis in rabbits (Schwenke and Carew, Arteriosclerosis 1989;9:895-918). The White Carneau (WC) pigeon is also useful for investigating potential mechanism(s) that might account for regional variation in arterial susceptibility to atherosclerosis because atherosclerosis develops predictably in the aorta at the level of the celiac bifurcation (atherosclerosis-susceptible celiac site). In this study we sought to determine whether the 125I-tyramine cellobiose (125I-TC) content 1 day after injecting 125I-TC-LDL ("125I-TC-LDL accumulation") would be greater in the celiac site in arteries of WC pigeons and whether 125I-TC-LDL accumulation would be exaggerated by cholesterol feeding. Because 125I-TC remains trapped in cells after cellular degradation, arterial sites that either degrade LDL at higher rates or contain higher concentrations of undegraded LDL or both will demonstrate greater 125I-TC-LDL accumulation. Young WC pigeons were studied while consuming a cholesterol-free diet and after consuming a cholesterol-containing diet for 1, 2, 4, and 8 weeks. In pigeons fed a cholesterol-free diet, 125I-TC-LDL accumulation in the celiac site was equivalent to 0.24 +/- 0.02 micrograms LDL cholesterol/cm2 aortic surface/day compared with only 0.14 +/- 0.02 micrograms LDL cholesterol/cm2/day for the adjacent aorta, which is resistant to atherosclerosis (atherosclerosis-resistant site) (p less than 0.025). In atherosclerotic lesions excised from the celiac site, 125I-TC-LDL accumulation was equivalent to 21 +/- 10 micrograms LDL cholesterol/cm2 aortic surface/day compared with 0.66 +/- 0.17 micrograms LDL cholesterol/cm2/day for the adjacent atherosclerosis-resistant site (p less than 0.001). During cholesterol feeding, 125I-TC-LDL cholesterol accumulation in the celiac site as a whole increased 30-fold compared with a fivefold increase in plasma LDL cholesterol. In comparison, 125I-TC-LDL cholesterol accumulation in the adjacent atherosclerosis-resistant arterial site increased at the same rate as the plasma LDL cholesterol, while 125I-TC-LDL cholesterol accumulation in two other relatively atherosclerosis-resistant arterial sites that we studied increased relatively little during cholesterol feeding. The results of this study suggest that differences in arterial 125I-TC-LDL accumulation, both those present in normal animals and those induced by cholesterol feeding, may contribute to the characteristic regional variation in arterial susceptibility to atherosclerosis in WC pigeons.(ABSTRACT TRUNCATED AT 400 WORDS)