DIETARY CHLORIDE DEFICIENCY AND ALKALOSIS IN THE RAT. (Received for publication, June 29, 1942)

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1 DIETARY CHLORIDE DEFICIENCY AND ALKALOSIS IN THE RAT BY DAVID M. GREENBERG AND ELIZABETH M. CUTHBERTSON (From the Division of Biochemistry, University of California Medical School, Berkeley) (Received for publication, June 29, 1942) Signal advances in the knowledge of the biochemical functions of the different mineral elements have been made in recent years through studies of the effects of diets deficient only in a single element upon the animal organism. With certain of the mineral elements normally present in great abundance in the diet, notably potassium (l-3) and sodium (d-6), the degree of dietary deficiency must be very severe to bring out the characteristic effects of their deprivation. Few experiments have been carried out on the effect of chloride deficiency and these have heretofore yielded little indication of a striking need for chloride by the animal organism. In experiments by Osborne and Mendel (7) and by St. John (8) there was no decrease in the growth of rats when the chloride content of the diet was reduced to and 0.05 per cent respectively. Orent-Keiles, Robinson, and McCollum (5) noted retardation of growth on a low chloride diet of unknown chloride content and Marquis (9) on a diet of 0.01 per cent chloride. In a paper which appeared when the present work was nearly completed, Voris and Thacker (10) found that a diet containing 0.02 per cent chloride caused a depression of appetite, increased consumption of water, increased heat production, and diminished body gain of nitrogen and energy as well as retarded growth. The present study was prompted by the knowledge that recent advances in scientific knowledge and technology of the nutritionally essential factors allow the preparation from purified constituents of diets drastically low in chloride, or any other desired component, but apparently adequate otherwise for the biological needs of the rat. One reason for undertaking the investigation was that from the well known reciprocal relationship between the chloride and bicarbonate concentrations in the blood (11) it can be predicted that a continuous chloride deficiency should produce a chronic state of alkalosis in the animal. Virtually all of the available information on alkalosis has been gained from acute experimental conditions and the study of chronic alkalosis may be expected to yield interesting information on the adaptation of the animal organism to this and its associated state, tetany. This paper contains the report of the effects of a diet containing per 179

2 180 CHLORIDE DEFICIENCY AND ALKALOSIS cent chloride or less on the gain in body weight, food and water consumption, and susceptibility to tetany of the rat. Chemical d.ata reported are the changes induced by the deficiency on the chloride, bicarbonate, and ph of the blood and on the excretion of chloride in the urine. Aside from a few chemical analyses of blood and tissue chlorides by Marquis (9) no published data exist on the chemical changes produced in the body by chloride deficiency. Composition of Basal Diet and Salt Mixtures Basal diet Casein Fat Sucrose Liver extract.. O.li Cod liver oil Supplements per kilo diet11?%. Thiamine hydro- I chloride Riboflavin. Pyridoxine. Inositol. Calcium nate. pantothe I 16 Ca,(POn)s... CaC NaCl NaN NaHC03... KC1... KzHPOd.... MgSOd.7HzO.... MgC12.6H Fe(NH&(S0&~6H,O... KI Totals... Salt mixtures* Diet Controls I - pz. per 100 gm. food Diet II Chloride-low With bicarmlate m.. per 00 gm. food diet With nitrate :m. per 100 gm. food * Mn, Cu, Zn, and Co were added to each diet in trace amounts. t Crisco. $ A 50 per cent alcoholic extract of Lilly s liver preparation. $ Fortified to contain 5000 units of vitamin A per ml. 11 The synthetic water-soluble vitamins were generously supplied by Merck and Company, Inc Composition of Diets and tixperimental Methods The composition of the basal diet and salt mixtures used in the experimental work is given in Table I. The salt mixtures of the chief diets, control Diet I and the bicarbonate-containing chloride-low diet, were devised so as to yield the same contents of all the mineral constituents except chloride. The approximate percentages in the two diets were calcium 0.6,

3 D. M. GREENBERG AND E. M. CUTHBERTSON 181 phosphorus 0.55, sodium 0.4, potassium 0.9, and magnesium The control diet contained 1.4 per cent chloride and the deficient diet not over per cent. Control Diet II and the nitrate-containing chloride-low diets were employed to demonstrate that the bicarbonate and carbonate contents were not responsible for the changes and increases in blood carbon dioxide observed in the chloride-deficient animals. Blood chloride values were determined on tungstate filtrates of whole blood by the mercuric nitrate titration method of Schales and Schales (12). Urinary chlorides were determined by the same method with the modification that solid benzoic acid was added to maintain the solution automatically at a slightly acid ph. A slightly acid reaction is necessary in order to obtain accurate titrations. The control urines were titrated with a solution of mercuric nitrate about 5 times as concentrated as that specified for blood filtrates, while that of rats on the chloride-low diets was titrated with a solution of the strength specified for blood filtrates. Urine samples for analysis were obtained from groups of three or four rats kept in a wire metabolism cage placed over a large glass funnel. The feces were separated from the urine by a perforated paraffin plate. At each collection the funnel and plate were washed and the wash water added to the urine. Carbon dioxide was determined on 1 ml. samples of whole blood collected under oil by the manometric method of Van Slyke and Neil1 (13). The ph of the blood was determined with a Beckman ph meter, with the special air-tight cell of 0.5 ml. capacity for blood supplied by the Beckman Company. All blood samples for analysis were obtained by heart puncture on rats anesthetized with amytal. Oxalate was used as anticoagulant in all cases except for blood intended for ph estimation, which was maintained fluid with heparin. No restriction was put on the consumption of food or water (distilled). In one series, the young rats were placed on the experimental diets at the age of 3 weeks; with another series the mothers were first put on these diets 2 days after the young were born. In the latter series, there was no significant difference at 3 weeks of age between the body weights of the young on the control and chloride-low diets. Apparently the weight and general condition of the young rats at weaning depended more on the previous history of the mother than on whether they were fed the control or chloride- deficient diet. For that reason, the results of both series of experiments have been considered together. 1 Chloride in the chloride-deficient diet was determined by digesting about 100 gm. portions with nitric acid in the presence of AgNOa and determining the silver chloride gravimetrically.

4 182 CHLORIDE DEFICIENCY AND ALKALOSIS RESULTS AND DISCUSSION Growth and Food and Water Consumption-The statistics for the gain in body weight and the food and water consumption of three groups of rats are given in Table II. The rats on the chloride-low diets to all outward appearances were normal and on autopsy revealed no apparent deviations from the normal in gross structure. In appearance and behavior they could not be distinguished from the controls. There was no noticeable effect on longevity in the period under observation; namely, 150 days. All the rats on the chloridelow diets survived until they were sacrificed. They gave no evidence of irritability or sluggishness. However, in each group of rats the chloride-de- TABLE Gain in Body Weights and Food and Water Intakes of Rats Maintained on Control and Chloride-Low Diets Initial Final age... age... Average initial weight.. I final weight.. I gain in weight.. I I perday... food intake per day. Food intake per gm. gain. Average water intake per day. Water intake per gm. gain in weight. - c II Group I, 0 hloride low, 7 rats dgys gm I ( :ontro1, 6 rats days gm Group II, c? - (:ontro1, 2 rats C Group III, 0 ( :ontro1, 2 rats days &ZYS days dllys m. gm. m. w ficient animals gained less weight over a given period of time than did their controls. Though the lower weight was not great enough to be significant in any one group, it was consistent in all groups; so that it may rightly be considered a significant fact from the data of all groups. Another method used to show the retardation of growth by chloride deficiency was to maintain a group of rats on the chloride-low diet for a time and later change half of the group of rats to the control diet. The results of such an experiment in which seven male rats were maintained on the chloride-low ration for 42 days and then four of the rats were changed to the control diet are plotted in Fig. 1. The change to the control diet caused a striking acceleration in the growth rate of the animals.

5 D. M. GREENBERG AND E. M. CUTHBERTSON 183 The animals on the low chloride diet consumed more food per gm. of gain in body weight than did their controls (Table II). In contrast to the results of Voris and Thacker (lo), there was no consistent evidence of a depression of appetite on the part of the chloride-deficient rats. The data of Table II show that the food consumption of the control and deficient animals was not significantly different. The water consumption per gm. of gain in body weight was the same in the females. The apparently higher water consumption observed for the chloride-deficient males is not conclusive because of the few animals in this group. Chemical Changes-The electrolyte pattern of the blood is altered in severe chloride deficiency by a decrease in the chloride and an increase in FIG. 1. The acceleration in the growth curve of rats when changed from the chloride-low to the control diet. The time of change is indicated by the arrow. Curve 1, average growth curve of four male rats that were changed to the control diet after 42 days on the chloride-deficient diet. Curve 2, average growth curve of three male rats maintained on the chloride-low diet. the total carbon dioxide content. The data are summarized in Table III. The blood chloride values were obtained on rats ranging from 55 to 119 days in age, that were on the experimental diets from 32 to 100 days. The body weights ranged from 115 to 300 gm. There was no apparent variation in the chloride values with age, length of time on the diet, or with body weight. The difference between the mean chloride values for the deficient (252 f 18 mg. per 100 ml.) and the control (295 X!Z 15 mg. per 100 ml.) animals is definitely significant considering the rather large number of rats tested. The probability of the occurrence of such a difference between the means by chance is less than one in twenty. The increase in the total carbon dioxide of the blood of the chloridedeficient animals is highly significant, statistically. The probability of the occurrence of the difference in the means between deficient (72.3 f 4.5

6 184 CHLORIDE DEFICIENCY AND ALKALOSIS volumes per cent) and control (57.8 f 4.1) groups is less than one in a hundred. The greater amount of bicarbonate and carbonate in the diet of the chloride-deficient animals is not responsible for the increase in the carbon dioxide content of the blood. This is demonstrated by the fact that a similar increase in carbon dioxide resulted when the rats were fed the nitrate-containing low chloride ration. No carbonate or bicarbonate whatsoever was present in this diet mixture. The alkalosis of the chloride-deficient rats is virtually compensated. The difference between the mean ph values of the controls and chloridedeficient rats, 0.06, is statistically insignificant, though there appears to be a tendency toward a higher blood ph in the chloride-deficient animals. The blood chloride in volumes per cent. / Bicarbonate Nitrate TABLE Effect of Chloride Deficiency on Electrolyte Pattern of Blood Blood Cl co2 PH Cl co2 III figures are measured in mg. of Cl per 100 ml. of blood; the COz Control I Chloride-deficient Range Mean I I S.D..~ The increase in the carbon dioxide content of the blood does not keep pace with the reduction in chloride concentration. On the basis of the mean values, the increase in mm of carbon dioxide per liter of blood is only one-fourth the decrease that occurs in the chloride concentration. To study the urinary excretion of chloride, it was found best to determine the change in the rate of excretion of the chloride when rats on the chloride-low diet were changed to the control diet and vice versa. Groups of three or four rats were employed to obtain sufficient urine for titration over short time intervals (as low as 1 hour). The chloride-deficient rats excreted 0.02 to 0.05 mg. of halide2 per hour per rat, or from 0.5 to 1.2 mg. of halide per day per rat. 5 to 8 hours after they were transferred to the control diet, the excretion of the chloride-deficient animals began to rise and continued to do so for several hours, finally surpassing the usual rate of 2 Calculated as chloride.

7 D. M. GREENBERG AND E. M. CUTHBERTSON 185 excretion of the control rats. The excretion dropped back to the normal control level within 24 hours. The control rats excreted 4.5 to 7.0 mg. of chloride per hour per rat, or 110 to 170 mg. per rat per day. When these rats were changed to the chloride-low ration, the urinary excretion of chloride decreased quickly and within 4 to 11 hours reached the rate of excretion of the rats that had been on the chloride-low diet for a long time. The curves showing the average rates of excretion of chloride by the rats after the change of dietary regimens are plotted in Fig. 2. The ability of the rat to reduce the excretion of chloride enormously within a few hours explains its ability to withstand a severe deficiency of FIG. 2. Excretion of chloride in the urine of rats changed from the chloride-rich to the chloride-low diet (curve on left) and from the chloride-deficient diet to the control diet (curve on right). this element. There is about a 500-fold difference in the excretion of chloride in the urine between chloride-deficient and control animals. The lowest rate of excretion observed, about 0.5 mg. per rat per day, represents about half the daily chloride intake on the present chloride-low diet. The iodide in the diet could account for 0.6 mg. of halide excretion per day calculated as chloride. Some chloride also must be lost through other excretory channels; e.g., perspiration. It is apparent, however, that the rats are able to retain and accumulate some chloride on a deficient diet which provides an intake of only 1 mg. per day. A rough calculation from the blood chloride values shows that an adult rat on the chloride-low diet has made a gain of approximately 60 mg. of chloride. Consequently, the degree of chloride deficiency and its accom-

8 186 CHLORIDE DEFICIENCY AND ALKALOSIS panying chemical and physical changes are due to the increase in the mass of the tissues of the body and not to an actual deficit of body chloride by the animal as a result of excretory loss. The ability to reduce the urinary excretion to a very low level is also true for sodium (3) and potassium (6). This explains why the intake of these ions and of chloride has to be drastically reduced to produce an actual deficiency. Tetuny-The chloride-deficient rats exhibited no signs of neuromuscular hyperirritability observable by mere inspection, probably because of the nearly completely compensated state of the existing alkalosis. Tests for the existence of tetany have been carried out with the hissing sound of an air blast and a mild galvanic current (see (14)), on a large number of deficient and control rats, usually after they were maintained for 3 to 4 weeks on the experimental rations. A very few of the deficient and none of the control rats went into tetany from the sound of the air blast. A few of the deficient rats exhibited prolonged convulsions of the same tonic epileptiform nature that have been observed in rats with tetany due to thyroparathyroidectomy and to magnesium deficiency (14), when subjected to the galvanic current. However, in the great majority of the cases the galvanic current only caused a fleeting convulsion after prolonged stimulation lasting only for the duration of the current, which could also be produced by the electrical stimulation in similar young control and stock rats. SUMMARY Rats were maintained on a chloride-low diet for periods of up to 15 weeks. In spite of the extreme chloride deficiency (0.012 per cent Cl or less in the diet) the rats showed no striking outward signs of deficiency. They gained less weight and ate more food per gm. of gain in body weight than did their controls. The whole blood chloride values in the chloride-deficient rats were significantly lower than in the controls; the mean for the rats on the chloridelow diet was 252 mg. per 100 ml. and for the controls 295 mg. per 100 ml. The total carbon dioxide content of the blood was significantly higher, the mean being 72.3 volumes per cent as compared to 57.8 volumes per cent for the controls. No significant difference was found in the ph values for whole blood. The animals were able to conserve their chloride by reducing their urinary output within a few hours after being given the deficient diet. They then excreted 0.5 to 1.2 mg. of Cl per day per rat as compared to a control excretion of 110 to 170 mg. per day per rat.

9 D. M. GREENBERG AND E. M. CUTHBERTSON 187 BIBLIOGRAPHY 1. Heppel, L. A., and Schmidt, C. L. A., Univ. California Pub. Physiol., 14, 189 (1938). 2. Grijns, G., Z. physiol. Chem., 261, 97 (1938). 3. Orent-Keiles, E., and McCollum, E. V., J. Biol. Chem., 140, 337 (1941). 4. St. John, J. L., J. Biol. Chem., 77, 27 (1928). 5. Orent-Keiles, E., Robinson, A., and McCollum, E. V., Am. J. Physiol., 119, 651 (1937). 6. Orent-Keiles, E., and McCollum, E. V., J. Biol. Chem., 133, 75 (1940). 7. Osborne, T. B., and Mendel, L. B., J. Biol. Chem., 34, 131 (1918). 8. St. John, J. L., J. Agric. Research, 37, 55 (1928). 9. Marquis, M., Compt. rend. Sot. biol., 128, 449 (1938). 10. Voris, L., and Thacker, E. J., J. Nutrition, 23, 365 (1942). 11. Peters, J. P., and Van Slyke, D. D., Quantitative clinical chemistry, Interpretations, Baltimore, 1043 (1931). 12. Schales, O., and Schales, S. S., J. Biol. Chem., 149, 879 (1941). 13. Van Slyke, D. D., and Neill, J. M., J. Biol. Chem., 61, 523 (1924). 14. Greenberg, D. M., Boelter, M. D. D., and Knopf, B. W., Am. J. Physiol., in press.

10 DIETARY CHLORIDE DEFICIENCY AND ALKALOSIS IN THE RAT David M. Greenberg and Elizabeth M. Cuthbertson J. Biol. Chem. 1942, 145: 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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