THE EFFECT OF FLUORINE UPON THE PHOSPHATASE CONTENT OF PLASMA, BONES, AND TEETH OF ALBINO RATS

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1 THE EFFECT OF FLUORINE UPON THE PHOSPHATASE CONTENT OF PLASMA, BONES, AND TEETH OF ALBINO RATS BY MARGARET CAMMACK SMITH AND EDITH M. LANTZ (From the Department oj Nutrition, Agricultural Experiment Station, the University of Arkona, Twson) (Received for publication, August 19, 1935) In 1923 Robinson (1) demonstrated the presence in ossifying bone of a phosphoric acid ester-splitting ensyme which he believed to play an important role in bone calcification. Kay (2) and Bodansky and Jaffe (3) have since made extensive studies of plasma and serum phosphatase under various conditions. In general it appears from their work that plasma phosphatase is changed from the normal in many conditions in which calcium metabolism is disturbed. Kay reports that the phosphatase value of plasma in many cases of generalized bone disease rises to more than 20 times the normal value, the degree of increase being correlated with the severity of the disease. Work in this laboratory has shown that fluorine interferes with the normal development of teeth and bones. In 1932 (4) fluorine in drinking water was shown to be the cause of a dental disease in humans known as mottled enamel, and this dental damage was produced experimentally (5) in rats, dogs, and guinea pigs by fluorine feeding or injections. The extensive investigation of the effect of chronic fluorine poisoning upon the metabolism of calcium and phosphorus which followed showed that growing fluorine-fed rats (6) and dogs (7) retained less of these mineral elements than do their non-fluorine-fed litter mate controls and the path of excretion was altered. The evidence indicated that fluorine decreased the absorption of calcium. The possibility of a change in plasma phosphatase values accompanying fluorine toxicosis was suggested by Phillips (8). He briefly reported that the plasma phosphatase of dairy cows fed a 303

2 304 Effect of Fluorine on Phosphatase high concentration of fluorine in their ration was practically double that of the control animals. His statement that the plasma phosphatase in fluorosis forms a sensitive test for the toxic effects of chronic fluorine poisoning was of great interest to us from the standpoint of a possible application and use in detecting fluorosis in human beings drinking fluorine-containing water and in establishment of the toxic level for fluorine intake. Our preliminary analyses of the plasma phosphatase in rats suffering from chronic fluorosis did not, however, reveal a higher content than in the control animals. Accordingly, a more thorough investigation of plasma phosphatase of rats in different stages and degrees of fluorine poisoning was conducted. It has been our observation that a relatively low intake of fluorine by rats (6) and humans (9) results in no measurable interference with calcium metabolism as determined by balance experiments and yet causes a devastating effect upon the enamel of the teeth when no other symptoms of fluorosis are present. Histological examinations (10) of the teet.h suggest that fluorine exerts a direct local action on the enamel-forming cells. In order to discover a possible effect of fluorine upon the phosphatase enzymes present at the site of tooth and bone calcification our studies were extended to include phosphatase values of both teeth and bone in fluorine poisoning. EXPERIMENTAL In the first series of experiments, a study is made of the effect of chronic fluorine intoxication produced by feeding harmful amounts of sodium fluoride upon the phosphatase content of plasma, teeth, and bones of growing rats of different ages. In the second series of experiments, an acute fluorine poisoning is produced by the subcutaneous injection of a solution of sodium fluoride in adult animals and determination of their plasma phosphatase. Series I-Litter mate albino rats were divided at weaning (28 days of age) into two groups. One group was given Sherman s B composed of 3 whole wheat, 5 whole milk powder, and salt equal to 2 per cent of the weight of the wheat ( 13) and was used as a control group. The second group was given the same ration to which 0.1 per cent sodium fluoride had been added. This

3 M. C. Smith and E. M. Lantz ration ( 214) has been used in much of the experimental work in this laboratory. It produces severe stunting in growth of the experimental animals, gross changes in tooth and bone structure, and diminished retention of calcium and phosphorus (5, 6, 11). In a few cases, a third group was given the control ration to which per cent sodium fluoride had been added. This ration ( 216) produces visible changes in the incisor teeth of rats but has little effect on the growth or general health of the animals. Only male rats were used, so as to avoid possible sex differences in phosphatase values. At 2 week intervals, litter mate rats were taken from each group and the phosphatase content of the plasma and, in most cases, of the bones and teeth was determined. A fasting blood sample for analysis was taken directly from the heart of the animals which were first anesthetized with chloroform. The animals were deprived of food overnight, because it had been found that extremely variable and much higher results were obtained when a fasting sample was not taken. Phosphatase was determined at first by the method of Kay (12). This methodwas discarded in favor of the clinical method of Jenner and Kay (13), which can be carried out with smaller blood samples and in a shorter time. The method consists essentially of incubation of the plasma with the substrate, sodium P-glycerophosphate, highly buffered with a glycine-nacl-naoh mixture, for 3 hours at 38. After precipitation of the proteins with trichloroacetic acid the degree of hydrolysis of the glycerophosphate is estimated by determination of the phosphorus calorimetrically, with stannous chloride as the reducing agent. The results are compared with the results of the nonincubated aliquots and the phosphatase content of the plasmas expressed in terms of the number of mg. of phosphorus which were liberated by 100 cc. of the plasma under the conditions described. While the blood samples were in the water bath, the incisor teeth and leg bones (tibia) were removed, freed from flesh, and quickly weighed. They were then ground with sand in a mortar and extracted overnight with distilled water to which a few drops of chloroform had been added. The amount of water used was based on the weight of material to be extracted and was 50 times the weight of the bone and 100 times the weight of the teeth.

4 306 Effect of Fluorine on Phosphatase After extraction the mixture was filtered and 0.5 cc. aliquots were taken for analysis by the same method used for blood. The results are expressed as mg. of phosphorus liberated per gm. of fresh tooth or bone material. To exclude the possibility of litter variation or changes in temperature conditions during the determination of phosphatase, comparisons were always made of analyses which were made at the same time on litter mates. TABLE I Eflect of Sodium Fluoride on Phosphatase Content oj Plasma, Bones, and Teeth of Growing Rats !s%t m diet Age of after rats weaning -- wks. wks * Average of six rats. t Average of two rats. Planma. mg. P liberated per 100 cc. plasma zt (0.1 (0.025 (COIk Per Per hol) cent cent NaF) NaF) Average phosphatase content -.-, - 7 Bones, mg. k&h, mg. P liberated P liberated per gm. per gm. fresh incisor fresh bone tooth con- I x01) (0.l, Zt (0%5 per ten NaF.) NaF) --- cc!&- trol) -,O.?fl cent NaF) : , (0.025,er cent NaF) * 9.5t The results of these determinations are summarized in Table I. It may be seen at a glance that the blood plasma phosphate of young growing rats was not increased in chronic fluorine poisoning induced by feeding a ration containing 0.1 per cent sodium fluoride. In comparing the plasma phosphatase value of the normal control animals with those of the fluorine-fed animals it is interesting to note first, the decrease in plasma phosphatase with age in the control animals, and second, the somewhat lower values in the

5 M. C. Smith and E. M. Lantz fluorine-fed animals of the same age up to 70 days and the somewhat higher values thereafter. The decrease in plasma phosphatase with age in the normal animals parallels the rate of growth and skeletal development. Hammett (14) noted an abrupt decline in bone growth in young rats when from 65 to 75 days of age. In a series of calcium and phosphorus balance experiments in the authors laboratory (6) a striking decline in the retention of calcium and phosphorus was noted at approximately 70 days of age. In the present investigation, an abrupt decline in plasma phosphatase content may also be noted after the rats have reached the age of 70 days. The plasma phosphatase of the fluorine-fed animals is lower at first than that of the controls but also decreases with age, although the decrease is more gradual. The drop at 70 days of age is less marked than that of the control animals and higher phosphatase values are thereafter noted in the fluorine-fed animals. Here again, the results parallel our previous findings that animals fed 0.1 per cent sodium fluoride in their ration are stunted in growth and bone development and retain less calcium and phosphorus than do the control animals up to the age of 70 days but the retention of these elements is higher thereafter. This difference is probably due to the slower rate of development and calcification of the stunted fluorine-fed animals which was extended over a longer period of time. The phosphatase content of the bones of the two groups of animals shows no measurable difference until the age of 70 days, at which time the bone phosphatase values of the fluorine-fed animals are greater, again probably indicative of more active calcification as compared with the controls which have passed the period of most active bone growth and, therefore, show lower bone phosphatase content. The incisor teeth of the fluorine-fed animals after 2 weeks on a ration containing 0.1 per cent sodium fluoride show no difference in phosphatase content. However, when the animals are continued on this diet, a very positive decrease of the content of the glycerophosphate-splitting enzyme was observed and the incisors of fluorine-fed animals showed a lower content of this enzyme than did the teeth of the control litter mate rats. The rate of eruption of the incisor teeth of rats on these diets has been previously

6 308 Effect of Fluorine on Phosphatase measured (15) and it was found that the incisors of rats on the fluorine 214 grew at a rate of 16.8 mm. in a 10 week period after weaning as compared with a 31.7 mm. growth of the incisors of the control animals in the same period of time. Growth of the incisors was practically normal during the first 2 weeks but markedly retarded thereafter, with almost cessation of growth after 8 weeks on the fluorine ration. Thus it appears that the phosphatase content of the incisor teeth is dependent upon the activity of their growth and calcification. The lower phosphatase values of plasma, bones, and teeth of the fluorine-fed animals during the period of most active growth of the normal animals seemed to be best explained secondary to the growth and calcification stunting effect of fluorine instead of any specific effect of fluorine upon the phosphatase enzyme itself. Further corroborating evidence may be seen in the phosphatase values of the plasma, bones, and teeth of rats receiving sufficient fluorine in their ration (0.025 per cent sodium fluoride) to mottle the teeth but not a high enough concentration to interfere with the rate of growth of the animals or give any evidence of abnormality of skeletal development. As may be seen in Table I rats on 216 had phosphatase values practically the same as those of the control non-fluorine-fed rats of the same age, litter, and sex. Series II-In order to test further the effect of fluorine upon the phosphatase enzyme, an acute fluorine poisoning was produced in rats by the subcutaneous injection of a solution of sodium fluoride. Schour and Smith (10) have shown that the single injection of 0.3 cc. of a 2.5 per cent solution of sodium fluoride produced marked gross and histologic changes in the incisor teeth. Accordingly, male albino rats taken from the stock colony (basal 13) were given subcutaneous injections of 0.3 cc. of 2.5 per cent sodium fluoride solution. The animals were then fasted overnight, at which time (18 hours after injection) the blood was sampled and glasma phosphatase determined in the usual manner. The period of active growth and sex differences was avoided by using only male rats 14 weeks of age or older. As before, comparisons are made between the plasma samples of litter mate rats analyzed at the same time. Most of these analyses were made in the summer months, which may explain the slightly higher values found for the few animals of the same age as compared with those reported in Series I.

7 M. C. Smith and E. M. Lantz The results of this study appear in Table II. While in a few cases the injected animals had a slightly higher plasma phosphatase content than the control animals, in other cases the reverse was true and in most cases no difference could be noted. In no cases were the differences of the striking order reported by Phillips as occurring in fluorosis in dairy cows. The average plasma phosphatase values for nineteen injected rats of different adult ages was 18.9 units as compared with 18.7 units for nineteen of their non-injected litter mate controls. Thus it may be concluded that the concentration in the plasma of the enzyme probably involved in tooth and bone calcification was not TABLE Effect of Injection of Sodium Fluoride upon Plasma Phosphatase of Albino Rats No. of rat pairs _- - Age wks II Avera e phosphatase content, mg. P likated per 100 cc. plasma Control rats Average of 19 adult rats _- I Injected increased in acute fluorine poisoning 18 hours after the injection of a solution of sodium fluoride rats SUMMARY A study has been made of the effect of sodium fluoride upon the phosphatase content of the plasma, bone, and incisor teeth of albino rats. Comparisons were drawn between analyses made at the same time on fluorine-fed and non-fluorine-fed rats of the same age, sex, and litter. The plasma pbosphatase values of the normal control rats decreased with age, a rather precipitous dip occurring at about 70 days of age, with little change thereafter. The plasma phosphatase value of the animals whose ration con-

8 310 Effect of Fluorine on Phosphatase tained 0.1 per cent sodium fluoride also decreased with age, but more slowly. They are lower than those of the control rats until the age of approximately 70 days, after which they are slightly higher. It is believed that the lower values noted are an indication of less active bone growth and delayed maturity rather than a specific fluorine effect. Animals receiving per cent sodium fluoride in their ration, a concentration sufficient to mottle the teeth but not to stunt bone development or produce other signs of fluorosis, show phosphatase values of the same order as the control rats. The phosphatase content of the incisor teeth of the animals on the high fluorine diet is less than that of the controls. Previous work has shown that their rate of eruption is inhibited by fluorine feeding. Little difference was seen in bone phosphatase values of the controls and their fluorine-fed litter mates until about 70 days of age, after which time they were slightly higher in the fluorine-fed rats. The plasma phosphatase values in adult rats, determined approximately 18 hours after the injection of 0.3 cc. of a 2.5 per cent sodium fluoride solution, were not significantly different from those of the controls. It is concluded that fluorine does not exert its characteristic damage to the teeth of rats through its effect upon the enzyme involved in tooth and bone calcification, nor can an increase in plasma phosphatase content be considered a sensitive indication of fluorosis in rats as reported by Phillips (8) for dairy cows. BIBLIOGRAPHY 1. Robinson, R., Biochem. J., 17, 286 (1923). 2. Kay, H. D., J. Biol. Chem., 89, 249 (1930); Physiol. Rev., 12, 384 (1932). 3. Bodansky, A., and Jaffe, H. L., Arch. Int. Med., 64,88 (1934). 4. Smith, M. C., Lantz, E. M., and Smith, H. V., Arizona Agric. Exp. Stat., Tech. Bull. $2, (1931); J. Dent. Research, 12,149 (1932). 5. Smith, M. C., and Lantz, E. LM., Arizona Agric. Exp. Stat., Tech. Bull. 45, 327 (1933). 6. Lantz, E. -M., and Smith, X C., Am. J. Physiol., 109,645 (1934). 7. Smith, M. C., J. Am. Dent. Assn., 22,817 (1935). 8. Phillips, P. H., Science, 76,239(1932). 9. Lantz, E. M., and Smith, M. C., J. Home Econ., 27,236 (1935).

9 M. C. Smith and E. M. Lantz Schour, I., and Smith, M. C., Arizona Agric. Exp. Stat., Tech. Bull. 68, 69 (1934); J. Am. Dent. Assn., 22, 796 (1935). 11. Smith, M. C., and Leverton, R. M., Ind. and Eng. Chem., 26,791 (1934). 12. Kay, H. D., J. Biol. Chem., 89,235 (1930). 13. Jenner, H. D., and Kay, H. D., Brit. J. Exp. Path., 13,22 (1932). 14. Hammett, F. S., J. Biol. Chem., 64,409 (1925). 15. Smith, M. C., J. Dent. Research, 14,139 (1934).

10 THE EFFECT OF FLUORINE UPON THE PHOSPHATASE CONTENT OF PLASMA, BONES, AND TEETH OF ALBINO RATS Margaret Cammack Smith and Edith M. Lantz J. Biol. Chem. 1935, 112: Access the most updated version of this article at Alerts: When this article is cited When a correction for this article is posted Click here to choose from all of JBC's alerts This article cites 0 references, 0 of which can be accessed free at tml#ref-list-1

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