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The Transport and Localization of Benzo(¿/)Pyrenã©-Hematiteand Hematite-210Po in the Hamster Lung Following Intratracheal Instillation1

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The Transport and Localization of Benzo(¿/)Pyrenã©-Hematiteand Hematite-210Po in the Hamster Lung Following Intratracheal Instillation1 [CANCER RESEARCH 34, 1344^1352, June 1974] The Transport and Localization of Benzo(¿/)pyrené-Hematiteand Hematite-210Po in the Hamster Lung following Intratracheal Instillation1 Ann R. Kennedy and John B. Little Department of Physiology, Harvard School of Public Health, Boston, Massachusetts 02115 SUMMARY soot in the urban atmosphere (2). Intratracheal instillations of 210Poadsorbed onto hematite carrier particles to mimic When administered intratracheally adsorbed onto hema adsorption to soot produced combined epidermoid and tite carrier particles, 210Poand benzo(a)pyrene (BP) induce adenocarcinomas in the peripheral lung of hamsters, while lung tumors of different histologies and apparent sites of BP-hematite produced mainly epidermoid carcinomas in origin. Hematite-210Po produces combined epidermoid and the major bronchi and trachea (10, 16). This difference in adenocarcinomas in the peripheral lung, while BP-hematite the histology and apparent sites of origin of the induced produces mainly epidermoid carcinomas of the major tumors suggests either that the cells in the lung are bronchi and trachea. To determine whether cells in the lung differentially sensitive to these 2 types of carcinogen or that are differentially sensitive to the two types of carcinogen or the carcinogens are reaching and acting at different sites in whether the carcinogens are reaching and acting at different the lung despite the fact that they were administered in the sites, we have studied their transport and localization same manner. To investigate this question, we have studied following intratracheal administration on carrier particles: the transport and localization of these carcinogens in the 210Polocalization by freeze-dry autoradiography and BP by lung. ultraviolet light fluorescence microscopy of frozen sections. Conventional histológica! techniques were inappropriate The results show that 210Po represents a firmly bound in these localization experiments since tissue processing insoluble carcinogen which delivers its primary dose to the involved liquid steps which might lead to translocation of peripheral lung from the particles that are retained in the the carcinogen; techniques not requiring liquid preparation alveolar duct region. BP, on the other hand, is a loosely steps were therefore sought. Freeze-dry autoradiography, a bound soluble carcinogen which leaves the carrier particles technique originally developed by Stumpf and Roth (23) and enters upper airway epithelial cells during clearance of and modified for use with the delicate, inflated lung (6) was the particles on the mucous ciliary escalator. We thus used for the study of 210Po localization. Since BP is conclude that BP induces central tumors because a signifi autofluorescent, it can be identified directly on histological cant amount of the carcinogen reaches the upper airway sections by UV fluorescence microscopy (16). Frozen epithelial cells, while 210Po induces peripheral tumors sections seemed to be the most appropriate histological because the major radiation dose is delivered to the alveolar medium for the study of BP localization by autofluores- region. cence since frozen sections would most closely preserve the i/i vivo localization of the carcinogen. The localization of 210Poand BP following intratracheal INTRODUCTION administration adsorbed onto hematite carrier particles is 210Po,a naturally occurring «-emittingradionuclide, and described in this report, and the significance of their BP,2 a chemical carcinogen, are potent lung carcinogens in deposition and localization in the lung in relation to the tumors induced by either agent is discussed. Syrian golden hamsters following intratracheal administra tion on hematite carrier particles (10, 16, 17). Thea-radia- tion emitted by 210Po is very densely ionizing; for each a MATERIALS AND METHODS disintegration, 5.3 MeV of energy is deposited in a track length of only 37 jtm in tissue. 210Po has been found in Male Syrian golden hamsters, 100 to 125 g, obtained cigarette smoke (15) and cigarette smokers' lungs (15). BP, from Dennen Animal Industries, Inc., Gloucester, Mass., were given intratracheal instillations of either 0.2 fid 210Po also found in cigarette smoke (1), is commonly adsorbed to or 3 mg BP, both bound to 3 mg hematite particles suspended in 0.2 ml 0.9% NaCl solution as described by 'This research was supported by Contract NOI CP 33273 from the Little et al. (10). Instillations were given to hamsters in an National Cancer Institute and Grant ES-00002 from the National Institutes of Environmental Health Sciences. upright position on a slanted board as described by Saffiotti 2The abbreviation used is: BP, benzo(a)pyrene. el al. (16). Animals were killed by Brevital sodium (Eli Lilly Received December 12, 1973: accepted March 4, 1974. and Co., Indianapolis, Ind.) overdose and exsanguination 1344 CANCER RESEARCH VOL. 34 Downloaded from cancerres.aacrjournals.org on October 1, 2021. © 1974 American Association for Cancer Research. Localization of Ini rat rächeally Administered Carcinogens from a renal artery. The trachea was clamped before Single Instillation opening the thoracic cavity to prevent lung collapse. Lungs were removed en bloc and frozen rapidly by placing them Zero to 1 Hr. Hematite-210Po was present overlying the for 1 min in methyl butane cooled to the viscous stage by epithelium throughout the airways in the lung, although in a liquid nitrogen. patchy distribution. In some branches, airway epithelium To study the localization of hematite-210Po, freeze-dried from the major bronchi to the bronchioles, including the frozen lung sections (2 to 4 /urnthick) were prepared for dry respiratory bronchioles and alveolar duct regions, was mourit autoradiography; stains used in this study were coated with hematite-210Po (Fig. 1). Occasional single celestine blue-Van Gieson's and hematoxylin-eosin. This tracks were seen in peripheral alveolar areas. These may technique has been described in detail (6) and involves no represent ionic 2l°Po(not particle associated) or 210Po liquid steps during processing and autoradiography. To associated with minute dispersed particles. These single study the localization of BP-hematite, frozen sections (2 to 4 tracks declined rapidly in number during the 1st week, then ¿¿mthick)were cut, stained with thionin or hematoxylin- gradually disappeared. No cells (macrophages) containing eosin, and immediately examined by UV fluorescence hematite-210Po were seen in the bronchioles or bronchi. microscopy. The white-yellow fluorescence of the BP could One to 4 Hr. Same as 0 to 1 hr, except that clumps of be easily distinguished using this technique (Figs. 4 to 7). hematite-210Po appeared on or overlying the ciliated epithe Animals used for the hematite-210Po localization study were lium of the trachea. sacrificed immediately after a single instillation and hourly Four to 6 Hr. The epithelium from the trachea to the for the 1st 8 hr, daily for the 1st week, weekly for the 1st 2 bronchioles still contained overlying hematite-210Po, but it months, and at 4 and 8 months; after the 2nd, 4th, and 6th was more patchy in nature. A few cells (macrophages) instillations sacrifices were made at 3 and 7 days; and at 10, containing hematite-210Po have now appeared in the bron 14, and 21 days after the 7th instillation. Animals used for chioles. the BP-hematite localization study were sacrificed after a Six to 12 Hr. Some airways still contained patches of single instillation at the same times as for the hematite- hematite-210Po. More macrophages containing hematite- 210Postudy up to 1 month after instillation. 210Po were found within the airways than at 4 to 6 hr. Sixteen to 48 Hr. Very few patches of hematite-2l°Po were left in the airway lumina. Many macrophages contain RESULTS ing hematite-210Po were found within the airways (Fig. 2). Many such cells containing hematite-210Po were present in Hematite-210Po the esophagus. Two to 5 Days. The peak numbers of cells containing Throughout the study, 210Po activity remained closely hematite-210Po were found in the airway lumina (Fig. 2). associated with the visible hematite particles in the lung. As Patches of extracellular hematite-210Po remained in the the a particle emitted by 210Po travels only 37 /¿min tis alveolar duct regions but not in the larger airways. Much of sue, the distribution of radiation dose was closely related the hematite-210Po in the alveolar region appeared to be to the distribution of hematite particles and aggregates. The hematite-2 IOPo was present in a distinctly nonhomo- engulfed by macrophages. This finding was confirmed in geneous distribution in the lung. In general, within a histo- separate serial sacrifice studies (A. R. Kennedy and J. B. Little, unpublished data) utilizing glycol methacrylate (plas- logical section of a given lobe, apical regions contained less hematite-210Po than basal regions, probably an effect of tic)-embedded lung tissue; the thin l-^m sections allowed high resolution in the identification of individual cells types. gravity on the flow of hematite during instillation in the Six to 7 Days. Rapid decline in the number of macro upright position. At any given time after instillation, there phages containing hematite-210Po in the airways; patches of was a great variation in the amount of hematite-2l°Po hematite-210Po remained in alveolar duct regions. appearing in different lobes of the same lung; some lobes Two to 8 Weeks. Very little macrophage associated were completely free of hematite-210Po while others had hematite-210Po remained in airways; patches of hematite- large amounts of activity, although the hematite did become 210Po in alveolar duct regions were somewhat reduced in more evenly distributed among the lobes following multiple intensity. instillations. Even within a single histological section, the Four to 8 Months. Airways were free of hematite-210Po. initial deposition of hematite was much greater in some Although the alveolar distribution was variable, all remain branches of the respiratory tree than others. At all times ing hematite-210Po was in the alveolar duct regions. studied, the hematite-210Po was patchy in nature.
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