Go AKAGI, AKIKO AKAGI, Masuo KIMURA, and Hisashi OTSUKA (2nd Department of Pathology, School of Medicine, Tokushima University*2) Synopsis

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1 [GANN, 64, ; August, 1973] UDC [616.62] COMPARISON OF BLADDER TUMORS INDUCED IN RATS AND MICE WITH N-BUTYL-N-(4-HYDROXYBUTYL)- NITROSOAMINE*1 (Plates LIII-LV) Go AKAGI, AKIKO AKAGI, Masuo KIMURA, and Hisashi OTSUKA (2nd Department of Pathology, School of Medicine, Tokushima University*2) Synopsis Male Wistar rats and male BALB/c mice received 0.05% N-butyl-N-(4-hydroxybutyl)nitrosoamine (BBN) solution as drinking water. After more than 10 weeks, 8 hyperplasias of the epithelium, 5 papillomas, and 36 carcinomas developed selectively in the bladder were found in 49 of the rats, while 4 hyperplasias, 3 papillomas, and 36 carcinomas of the bladder were found in 43 of the mice, After more than 25 weeks, all the rats and mice examined had developed tumors including 3 papillomas in the bladder. The mean induction time of carcinomas was 55.1 weeks in rats and 30.7 weeks in mice, All carcinomas induced in rats were papillary, and histologically they were transitional cell (83.3%) or squamous cell (16.7%) type. About 2/3 of the tumors showed no invasion into the bladder wall. Carcinomas of mice were squamous cell (52.8%), transitional cell (38.9%), or anaplastic (8.3%) type, and all were more or less invasive. No metastatic foci were found in rats or mice. From Druckrey's comprehensive studies on induction of tumors by alkyl- and acylnitrosoamines, N-nitroso compounds are known to be strong carcinogens and their organotropic effects vary with their chemical structure.7) Among these N-nitroso compounds, dibutylnitrosoamine (DBN) and N-butyl-N-(4-hydroxybutyl)nitrosoamine (BBN) are unique in inducing bladder tumors.6) DBN also induces tumors of other organs in rats,5) mice,2,14) hamsters,1) and guinea pigs,11) while BBN selectively induces only bladder tumors in rats.6,9) Description of its effect on mice is rare.3) This paper reports experiments on the induction of bladder tumors in both rats and mice by BBN and comparative studies on the tumors in these two species. MATERIALS AND METHODS Sixty male Wistar rats and 46 BALB/c male mice of 7-10 weeks old were used. These animals were housed 3 to a wirenetting cage in rats and 5 to a metal cage in mice. They were given MF pellets (Oriental Yeast Co., Tokyo) and a solution of 0.05% BBN (synthesized by Mr. S. Hashimoto, Taiho Pharmaceutical Co. Ltd., Naruto) as drinking water freely. The drinking solution was changed daily and the volume drunk was recorded. The total carcinogenic dose per animal was calculated assuming that all the animals in a cage drunk the same amount. All the animals were autopsied, including *1 This study was supported in part by a Grant-in-Aid for Scientific Research from the Ministry of Education. 64(4)

2 G. AKAGI, ET AL. those which died during the experiment. Tissues were fixed in 10% Formalin and stained with Hematoxylin and Eosin for histological examination. RESULTS Rats Changes in the urinary bladder of rats that received carcinogen for more than 10 weeks are shown in Table I. In the eleven rats that died within 10 weeks, varying degrees of diffuse hyperplasia of the transitional epithelium of the bladder were seen. Table I. Epithelial Changes in the Urinary Bladder Induced by BBN in Rats and Mice a) Renal carcinoma b) Lung adenoma Among 49 rats treated with BBN for more than 10 weeks, hyperplaia of the mucosa, consisting of 8-15 cell layers, was observed in 8 rats (Photo 1), papilloma in 5 rats, and carcinoma of the bladder in 36 rats. Multiple hyperplastic lesions developed in a relatively short period of less than 25 weeks of treatment. Papillomas showing transitional epithelial proliferation with vascular stroma, slight cellular atypism, and occasionally mitotic figures, were found in 5 rats that received carcinogen for weeks (Photo 2). Some of the papillomas were multifocal in origin. Carcinomas of the urinary bladder were found in 36 rats treated with BBN for weeks (Photo 3). The mean induction time of carcinomas in 36 rats, including 10 animals that were killed, was 55.1 weeks (386 days) and the mean total dose of carcinogen was 5.55g per rat, namely, about 15.85g/kg, taking the mean body weight as 350g. Most carcinomas showed papillomatous growth, filling the entire lumen of the bladder, and no predilection site was found. Two carcinomas invaded adjacent organs, but no metastatic foci were found in animals with bladder carcinoma. Histological findings on the carcinomas are shown in Table II. Most carcinomas showed a well-differentiated papillary pattern with a fine vascular core (Photo 4). They were usually composed of tumor cells with a transitional character and of squamous cell areas showing cornification, and occasionally of anaplastic areas with high cellularity. Tumor cells showed little pleomorphism but mitotic figures were seen frequently. Necrosis, hemorrhage, and inflammatory changes in the stroma were also observed. Histologically, the carcinomas were classified into two cell types; transitional (Photo 5) and squa- 332 GANN

3 BLADDER CARCINOMA OF RATS AND MICE BY BBN Table II. Comparison of Bladder Carcinomas Induced by BBN in Rats and Mice *These 13 mice also had cancerous invasion to the serosal tissues. mous cell carcinomas. The transitional cell type predominated (30/36) and the squamous cell type was less frequent (6/36). No carcinomas were found consisting mainly of anaplastic tumor cells. The depth of cancerous invasion of the bladder walls varied, with invasion of the submucosa in 2 animals, muscular layer in 4, and serosal tissue in 3 animals (Photo 6). Invasion of the prostate and peritoneum was seen in 2 animals. In the other 25 rats no cancerous infiltration into the bladder wall was observed microscopically. Mice Changes of the urinary bladder in 43 mice that received BBN for more than 10 weeks are shown in Table I. In 4 mice killed after 14 to 21 weeks, multiple hyperplastic foci of the bladder mucosa were found microscopically. Papillomas, which were papillary proliferations of well-differentiated transitional epithelium without cellular irregularity, developed in 2 mice killed after 24 weeks and one mouse which died at 26th week of the experiment. A carcinoma, invading the submucosa of the bladder, was first found in a mouse killed at 14th week (98 days). Carcinomas were later found in 35 mice treated with BBN for 43 weeks (304 days) or less. The mean induction time of carcinomas in these 36 mice, including 6 mice which were killed, was 30.7 weeks (215 days) and the mean total dose of BBN was 451mg/mouse, namely 18.04g/kg, taking the mean body weight as 25g. One mouse with bladder carcinoma also had an adenoma of the lung, while another had carcinoma of the renal pelvis. Apart from these, no carcinomas were observed in organs other than the urinary bladder and kidney. Carcinomas of the bladder frequently developed in the base of the organ. Extensive infiltrative growth of the tumor into the wall of the bladder was found in 25 mice, while tumors showing papillary exstructive growth were seen only in 5 mice, and 6 other mice had solid tumors filling the entire lumen of the bladder (Table II). Many of the carcinomas adhered to surrounding tissues 64(4)

4 G. AKAGI, ET AL. or organs, such as the prostates and seminal vesicles, and were often accompanied with uni- or bilateral hydronephrosis (Photo 7). Microscopically most bladder carcinomas of mice were of a poorly differentiated type, showing marked cellular and structural atypia, and they invaded deeper layers of the bladder wall (Photo 8), unlike the bladder carcinomas in rats. Classified according to their predominant histological types, these carcinomas consisted of 19 (58.2%) squamous cell carcinomas with cornification (Photo 9), 14 (38.9%) transitional cell carcinomas (Photo 10), and 3 (8.3%) anaplastic carcinomas (Photo 11). Tumor cell invasion of serosal tissue was seen in 31 carcinomas. Six of these 31 tumors showed penetration of the prostates (Photo 12) and 7 invaded the sphincter muscles of the urinary bladder. A comparison of the histological types, growth patterns, and invasions of the carcinomas in rats and mice induced by BBN is listed in Table II. DISCUSSION The present results clearly showed that BBN selectively induces a high incidence of bladder tumors in mice as well as in rats. Druckrey et al.6) first reported that all BD II rats treated with BBN for 180 days or more developed bladder tumors, and Ito et al.9) confirmed the selective induction of bladder carcinomas by BBN in Wistar rats. In the present experiments also no tumors developed in rats other than in the urinary system, but in mice one adenoma of the lung and one renal pelvic carcinoma were observed besides bladder tumors. The adenoma of the lung was probably a spontaneous tumor.13) The pelvic carcinoma was a transitional cell type, and associated with hydronephrosis, suggesting that the tumor was induced by retention of urine containing the nitroso compound, as shown in Ito's experiments with rats.10) The time required to induce bladder carcinomas in mice is shorter than that in rats (Table I). All the mice with bladder carcinomas died within 45 weeks, while 14 of 36 rats with malignancy survived for over 50 weeks. This may be due to the differences in the dose of carcinogen and behavior of the tumors in the two animal species. The mean daily dosage of BBN calculated from total dose of the carcinogen was 83.9mg/kg for mice and 41.0mg/kg for rats. Druckrey et al.6) reported that bladder tumors developed more quickly in rats given a high dose of BBN than those receiving a low dose. The bladder carcinomas induced in mice seem to be more aggressive than those in rats (Table II). By applying the criteria of histological grading of malignancy used clinicopathologically for human tumors4,8) to these experimental tumors, most of the carcinomas in mice corresponded to high grade infiltrating malignancy, while those in rats corresponded to a low grade papillary type. Thus, mice seem to be suitable as experimental models of human bladder carcinoma with an invasive character, while rats can be used as models of rather slowly growing papillary carcinoma. It is also noteworthy that about half of bladder tumors in mice were squamous cell carcinomas which show a more malignant behavior than transitional cell tumors. On the other hand, most of the metaplastic lesions in rat tumors showed complete stratification and cornification. Similar differences in histological figures have been observed among bladder tumors in different species induced by DBN.1,2,11,12) The significant difference in the histological appearance of bladder tumors in the two species observed in our experiments seems to depend on a difference in the histogenesis 334 GANN

5 BLADDER CARCINOMA OF RATS AND MICE BY BBN of these tumors in mice and rats. Only a few papillomatous lesions were seen in the bladder of mice, either at an early, non-malignant stage or after appearance of malignancy, while many papillomatous hyperplastic lesions were seen besides carcinomas in rats. Therefore, it is suggested that bladder carcinomas in mice may develop directly from hyperplastic or metaplastic areas, as indicated by the work of Bertram and Craig,3) while in rats malignant bladder tumors may arise mainly from precancerous papillomas.9) The authors express their thanks to Mr. Sadao Hashimoto, Research Laboratory, Taiho Pharmaceutical Company Ltd., for kindly synthesizing N-butyl-N-(4-hydroxybuty)nitrosoamine, to Mr. Toshio Yamaguchi and Mr. Koichiro Amo for their technical assistance, and to Miss Junko Abe for typing the manuscript. (Received March 1, 1973) REFERENCES 1) Althoff, J., Kruger, F. W., Mohr, U., Schmahl, D., Proc. Soc. Exp. Biol. Med., 136, 168 (1971). 2) Bertram, J. S., Craig, A. W., Brit, J. Cancer, 24, 352 (1970). 3) Bertram, J. S., Craig, A. W., Eur. J. Cancer, 8, 587 (1972). 4) Dean, A. L., Stofi, F. K. M., Thomson, R. V., Clark, M. L., J. Urol., 71, 571 (1954). 5) Druckrey, H., Preussmann, R., Schmahl, D., Muller, M., Naturwiss., 49, 19 (1962). 6) Druckrey, H., Preussmann, R., Ivankovic, S., Schmidt, C. H., Mennel, H. D., Stahl, K. W., Z. Krebsforsch., 66, 280 (1964). 7) Druckrey, H., Preussmann, R., Ivankovic, S., Schmahl, D., Z. Krebsforsch., 69, 103 (1967). 8) Ferguson, R. S., J. Urol., 36, 651 (1936). 9) Ito, N., Hiasa, Y., Tamai, A., Okajima, E., Kitamura, H., GANN, 60, 401 (1969). 10) Ito, N., Makiura, N., Yokota, Y., Kamamoto, Y., Hiasa, Y., Sugihara, S., GANN, 62, 359 (1971). 11) Ivankovic, S., Bucheler, U., Z. Krebsforsch., 71, 183 (1968). 12) Kunze, E., Schauer, A., Z. Krebsforsch., 75, 146 (1971). 13) Stauts, J., Cancer Res., 24, 147 (1964). 14) Takayama, S., Imaizumi, T., GANN, 60, 353 (1969). EXPLANATION OF PLATES LIII-LV Photo 1. Hyperplastic lesion of the bladder epithelium in a rat treated with BBN for 18 weeks. Photo 3. Bladder tumor of a rat after 36 weeks of BBN administration. Photo 4. Low-power view of a papillary carcinoma filling the entire lumen of the bladder of a Photo 5. Well-differentiated transitional cell carcinoma of a rat treated with BBN for 47 weeks. Photo 6. Poorly differentiated squamous cell carcinoma invading the muscular layer and subserosa Photo 7. Carcinoma of mouse bladder induced by BBN administration for 26 weeks. The tumor invades the ureters and surrounding organs. Hydronephrosis is evident. Photo 8. Squamous cell carcinoma of mouse bladder invading submucosal tissue. The mucosal Photo 9. Well-differentiated squamous cell carcinoma with cornification induced in a mouse 64(4)

6 G. AKAGI, ET AL. Photo 10. Papillary transitional cell carcinoma induced in the bladder of a mouse after 44 weeks Photo 11. Anaplastic carcinoma infiltrating the muscular layer of a mouse bladder after 27 weeks Photo 12. Poorly differentiated squamous cell carcinoma of a mouse bladder invading the pros- H-E=Hematoxylin and Eosin stain 336 GANN

7 GANN, Vol. 64 PLATE LIII

8 GANN, Vol. 64 PLATE LIV

9 GANN, Vol. 64 PLATE LV

EFFECT OF VARIOUS FACTORS ON INDUCTION OF URINARY BLADDER TUMORS IN ANIMALS BY N-BUTYL-N-(4-HYDROXYBUTYL) NITROSOAMINE

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