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1 : /18 SOME OBSERVATIONS ON THE COMPARATIVE EFFECTS OF COLD AND BURNS ON PROTEIN METABOLISM IN RATS. By G. H. LATHE 1 and R. A. PETERS. From the Department of Biochemistry, Oxford. (Received for publication 18th February 1949.) IN recent years considerable attention has been devoted to the metabolic disturbances which are set up by various types of trauma. Cuthbertson [1932] especially has shown that an increased excretion of nitrogen is one of the most striking expressions of this altered metabolism. In studies of protein metabolism in burned rats in 1945, it was noted by Peters in a previously unpublished experiment (experiment 1 of the series now reported) that when the environmental temperature fell during a period of cold weather, the nitrogen excretion of the burned animals was not additionally increased, suggesting some initial common path. In contrast, control animals excreted nitrogen in amounts which approached the increased excretion in the burned animals. This observation has led us to perform some experiments upon the relation between environmental temperature, burns and nitrogen excretion. Since cold is frequently considered to stimulate the thyroid, this has also been investigated in parallel researches [Gribble and Peters, 1949]. Since also the stimulus to some of this work has been the observations by Croft and Peters [1945] upon the effect of methionine, the influence of this upon the increases in nitrogen excretion under cool conditions has also been examined. Though not complete, it has seemed advisable to report our experiments for the benefit of others working in the field, as we are unable to continue them. EXPERIMENTAL METHODS. The methods used in experiment 1 (1945) were adapted from those previously reported from this laboratory by Croft and Peters [1945]. Some changes were made in experiments 2, 3 and 4, in which albino rats were maintained in individual cages placed over glass bowls containing a perforated zinc plate for the separation of faeces from the urine, which passed through into 50 ml. of 0 1 N H2SO4. Urine was 1 I.C.I. Fellow. Present address: Maternity Hospital, London. Research Laboratories, Queen Charlotte' 55

2 56 Lathe and Peters removed at intervals, as stated in the individual experiments, made up to a fixed volume, and the ammonia and urea nitrogen determined as previously described. Throughout this paper nitrogen excretion refers to ammonia and urea nitrogen only. It has been assumed that the frecal N remains practically constant as was found by Croft and Peters [ Feeding.-Experiment 1 was made by the previous technique, with the addition of paired feeding to control the lowered food intake through failure of appetite after burning. In the experiments of 1946 (2, 3 and 4 of the present paper), in order to circumvent the difficulties and disadvantages of the paired feeding technique, all animals were tube-fed with a diet of the following composition: Percentage by weight of calorie components. Percentage of calories. Casein (Glaxo A.E.).. 33 g Arachis oil 42.2 ml Cod-liver oil ml Wheat starch g Salt mixture g. Agar g. Vitamin supplement.. 6 ml. Water ml. Total volume ml. This diet was modified from the 14 per cent. protein diet previously used in this laboratory. These modifications consisted of (1) replacement of casein and yeast by casein alone, (2) substitution of a portion of the carbohydrate by arachis oil, and (3) the use of purified vitamin preparations. It was thought that in these short experiments the animals would not run out of other unknown B factors. The diet was homogenized in a Waring blender, ice-cold water being used to prevent the starch from swelling. The diet was administered by tube twice daily, at nine in the morning and five in the afternoon, a No. 3 hard rubber catheter attached to a 10-ml. metal-glass syringe being used [Lathe, 1948]. The animals were held over the cages during feeding in order to prevent urine loss, and weighed immediately thereafter, allowance being made for the weight of food administered. All the animals were fasted for 16 hours before the initial tube feeding. Water was available to the animals at all times. Fifteen ml. of the diet provided 18 cals. per 100 g. for a 240-g. rat. It contained 235 mg. of nitrogen. The vitamin supplement

3 Effects of Cold and Burns on Protein Metabolism in Rats 57 consisted of: aneurin, 10 mg.; riboflavin, 10 mg.; choline chloride, 6 g.; Ca d-pantothenate, 30 mg.; nicotinic acid amide, 20 mg.; p-aminobenzoic acid, 30 mg.; pyridoxine hydrochloride, 7 mg.; inositol, 2 g.; 10 per cent. ethanol, to 60 ml. When a methionine supplement was given, it consisted of 100 mg. of DL-methionine incorporated in the diet Ėxcept where otherwise stated, the animals were kept in a constant temperature room at 22 C. Where lower temperatures were desired, these were obtained by exposing the animals in an open room during the autumn of the year. Under these circumstances the temperature depended on the weather. A recording thermometer was used in each such experiment to indicate the degree of cold to which the animals had been subjected. Even a drop of 20 C. is sufficient to change the metabolism of rats on a constant diet. Burning was carried out as previously described [Croft and Peters, 1945] at 730 C. for 30 seconds. Ether was used to anaesthetize burned and control rats. All the experiments consisted of a preliminary basal period during which the nitrogen excretion on the diet was estimated. Then followed an experimental period of several days, which was begun by burning the animals, or placing them in the cold. Comparisons are made of the average daily nitrogen excretion during the basal and the experimental periods, and between the nitrogen excretion of different groups of animals. RESULTS. In experiment 1, which was made in 1945 with the technical assistance of R. W. Wakelin and which led to the further work, the N excretion of 12 adult rats was studied; these were divided into two groups of 6. They were fed on the basal diet of Croft and Peters [1945], supplemented with choline hydrochloride (10 mg. per 100 g.); after the preliminary period upon this diet 6 of the animals were anaesthetized and burned and the remainder anaesthetized and used as controls. It happened that during the latter course of the experiment, the simultaneous presence of a cold spell and of a failure in the heating of the animal house led to a fall in environmental temperature to which the animals were exposed. The average excretions per rat per diem are given in Table I for the basal period and for the 7 days following burning (excluding the first day). The increase in the excretion of the burned animals fell within that to be expected in this series ( mg. for 9 days); on the other hand, the control animals showed an increased excretion little different and falling within that previously observed for burning (+420 mg. for 9 days). This suggested that the N excretion due to cold was not additive to that of the burn.

4 58 Lathe and Peters TABLE I.-CHANGE IN EXCRETION OF N (MG. PER DIEM PER RAT) OF CONTROLS, DUE TO COLD ENVIRONMENT, IN A BURNING EXPERIMENT (EXP. 1). Mean excretion of N (mg./diem/rat). Before burning After buring (5 days). (7 days). _Difference between means. Control i 6X82 Burned ±12.23 In all tables the figures following i are the standard error of the mean, or difference between means, as calculated from individual figures. Effect8 of Cold and of Methionine. In the 1946 experiments in which 51 rats were used, it was important at the outset to obtain some quantitative estimate of the effect of cold on nitrogen excretion, as well as any possible influence of methionine. In experiment 2, 19 rats were kept in the constant temperature room for a basal period of 2 days, during which the nitrogen excretion was estimated daily. They were then divided into four groups and treated as follows: group 1 remained under identical conditions, group 2 received a daily supplement of 100 mg. of DL-methionine in the food, group 3 was transferred to the cold room where the temperature varied from 100 to 160 C., and group 4 was transferred to the cold room and received the methionine supplement. The experimental period lasted 7 days. The initial weight of the animals varied from 208 to 307 g., averaging 256 g. Each animal received 16 ml. of diet per day (equivalent to 18 calories per 100 g. of body-weight for a rat of 256 g.). The summarized effect of cold, both with and without methionine, is indicated in Table II. The individual nitrogen excretion and weight changes are given in Appendix Table V. Experiment 2 shows that, as would be expected on a constant diet, cold increases the daily nitrogen excretion, and that a methionine supplement has little if any effect upon this. Examination of the detailed results (Appendix Table V) indicates that the cold stimulus in 3/5 animals caused a rise in N excretion on the first day, in 4/5 upon the second day, and in all animals by the third day. Effects of Cold and of Burning. Experiment 3 was designed to determine whether the effects of cold and of burning were additive. Thirteen rats were divided into three groups, which were maintained during a four-day basal period in the

5 Effects of Cold and Burns on Protein Metabolism in Rats 59 TABLE II.-COMPARISON OF N EXCRETION OF GROUPS OF RATS MAINTAINED UNDER WARM AND COLD (150 C.) ENVIRONMENTAL CONDITIONS WITH AND WITHOUT ADDITION OF METHIONINE (ExP. 2). Average daily nitrogen excretion (mg.). Average weight change (g.). Number prliminary Experi - Preliminary Experiof periodm. mental period. mental animals. period. period. In warm ,,,,+meth In cold ,,+meth Change in average daily N excretion (mg.). Warm. Cold. Effect of cold. Standard diet ± ± Methionine supplement ± constant temperature room. Initial animal weights varied from 246 to 266 g., and averaged 257 g. At the conclusion of the basal period two groups, 1 and 2, were burned (day 5), all animals were ansesthetized, and the following day groups 1 and 3 were placed in the cold room, where the temperature varied between 15 and 200 C. The experiment concluded on day 11. There was a slight difference between groups 1 and 2 and group 3. The latter served as a control for another experiment and was fed a slightly higher diet. Groups 1 and 2 received 17 calories per 100 g. of body-weight, and group 3 received 18 calories per 100 g. The changes in mean daily nitrogen excretion and in weight, between basal and experimental periods for the three groups, are given in Table III. Nitrogen excretion of individuals is given in Appendix Table VI. In experiment 3 the mean daily change in the cold was of the same order as in experiment 1 (+ 48). The burned animals kept in the warm excreted + 89 mg. extra N; those in the cold + 78 mg. This is so much less than the combined figure of 137 mg. that it confirms the impression given in experiment 1 that the stimuli for the burn and for cold in this

6 60 Lathe and Peters TABLE III.-COMPARISON OF N EXCRETION FOR ANIMALS BURNED AND KEPT UNDER WARM AND COOL (170 C.) ENVIRONMENTAL CONDITIONS (ExP. 3). Mean daily excretion Number (mg./rat/diem). Difference Group. of Treatment. due to animals. Basal Experimental treatment. period. period. 1 4 Cold after burning Warm after burning Not burned. In cold ±18 1 Weight changes: Group 1, -24 g.; 2, - 14 g.; 3, - 12 g. experiment drew upon some source of N by a common path; 3/4 animals showed the increased excretion in the cold by the first day and 4/5 by the second day. Effects of Cold, Burning and Methionine. In experiment 4, cold, burning and methionine were compared simultaneously. Nineteen animals, averaging 276 g., were maintained for a basal period of 5 days at 220 C. They received 19 calories per 100 g. The diet was of the same composition as previously, except that the inositol in the vitamin supplement was reduced to 4 of the previous level. During the experimental period the animals were divided into four groups as follows: group 1 was handled as during the basal period, group 2 was burned, group 3 was given a daily supplement of 100 mg. of DL-methionine in the diet, and group 4 was burned and received the methionine supplement. All animals were anaesthetized. On the second day of the experimental period all animals were transferred to the cold room, where the temperature fluctuated from 6 to 160 C. The differences between the mean daily nitrogen excretion during basal and experimental periods is given in Table IV. It will be seen that in experiment 4 the cold induced somewhat of the same change as before. However, the combined effect of cold and burning showed an additional increase which was statistically significant. It is a pity that, owing to technical difficulties, an extra control group in the warm could not be included; but the values for burning and keeping in the warm do not often much exceed + 80 mg., and for a 9-day period are usually lower. In experiment 4 the experimental temperature was lower than in the other experiments. Methionine had no appreciable influence.

7 Effects of Cold and Burns on Protein Metabolism in Rats 61 TABLE IV.-COMPARISON OF EFFECTS OF COLD ( 11 C.), BURNING AND METHIONINE UPON N EXCRETION (ExP. 4). Mean N excretion (mg./diem/rat). Number Group. of Basal Experimental Change. animals. Treatment for period. period experimental period. (5 days). (6 days). 1 5 Cold ± 7* Cold+burn ± Cold +methionine ± Cold+burn+meth ±16 ionine. DIsCUSSION. That under certain conditions cold [Lusk, 1929] and burns individually will increase nitrogen excretion in animals is now well established [Clark, Peters and Rossiter, 1945]. In any comparison of their effects two questions would seem to be of paramount importance: (1) Are the effects on N excretion of approximately the same order, and are they additive? (2) Does the time from stimulus to response vary from one type of stimulus to another? (1) In experiments 1, 3 and 4 the average excess nitrogen excreted as a result of burning is seen to be somewhat greater than that from cold. The effect of the cold alone varied from 48 to 65 mg., while that of burning and cold was 59 mg. in experiment 1, 78 mg. in experiment 3 and 126 mg. in experiment 4. Hence in regard to the question whether the effects of cold and of burning are additive, an unequivocal answer has not been obtained. In experiment 3 the combined effect of cold and of burning was slightly less than that of burning alone. This is consistent with experiment 1, and shows that there may be no additive effect. However, in experiment 4, burning plus cold showed an apparent increase over and above the effect of the cold; this may be due to the greater degree of cold, but it shows that the matter is not quite straightforward. Nevertheless, there is a suggestion that a common path is partly involved. (2) The speed of response to the stimulus of cold or of burning is important in relation to possible thyroid effects. In our experiments 1 and 2 the effect of cold on the N excretion was often present in 24 hours and usually marked in 48 hours. The excess N excretion as a result of burns may appear within 24 hours [Croft and Peters, 1945, confirmed

8 62 Lathe and Peters experiment 2] and reach a peak in 3-7 days. A similar time element is found in the N excretion following fractures in the rat [Cuthbertson, 1939] and following skeletal trauma in the human [Cuthbertson, 1932]. In the absence of a control of the degree of cold, it is impossible to say whether this is a qualitative or quantitative difference. In regard to the effects of methionine, if account is taken of the extra 11 mg. N added in the diet in the methionine supplement, experiment 2 or 4 shows that this addition neither prevented the N loss due to cold, nor that due to cold and burning. Gribble et al. [1949] have discussed the problems of methionine and burns. The effects of excess of calories given as sugar in burning are discussed in a separate paper [Lathe and Peters, 1949], as also the possible influence of thyroid factors [Gribble and Peters, 1949]. It is evident that, even under ideal conditions, a constant nitrogen excretion in experiments involving a constant calorie intake can only be obtained when the temperature is rigidly controlled. Failing this, the increased excretion of controls under cool conditions might lead to the erroneous conclusion that cold reduces the N loss. The difficulties of experiments in this field are well illustrated by Appendix Tables V and VI, giving the detailed results of experiments 2 and 3. Even when constant amounts of nitrogen are introduced into the animal each day, the daily variations in excretion of individual rats are considerable. To reduce these to statistical order much larger numbers of animals would be required. SUMMARY. 1. The comparative effects on nitrogen excretion of cold and burns have been investigated in preliminary experiments by a study of nitrogen excretion in rats receiving a constant calorie and protein intake on a high fat diet administered by tube. 2. Under these conditions, as is to be expected, cold and burns produce an increase in nitrogen excretion within 24 or 48 hours. 3. In two experiments the effects of cold and of burning on nitrogen excretion were not additive; in one at a colder temperature N loss was increased by burning. 4. A methionine supplement does not reduce the excess nitrogen excretion due to cold, or the excess nitrogen excretion due to burning in the cold. We are grateful to R. W. Wakelin and Miss J. Jenkins for technical assistance in experiment 1, and to Miss C. Stayte for assistance in experiments 2, 3 and 4, and to T. F. Clarke for help with animals. We are also grateful for financial help from the Medical Research Council, and to the Ministry of Supply for methionine.

9 Effects of Cold and Burns on Protein Metabolism in Rats 63 APPENDIX TABLE V.-INDIVIDUAL VALUES FOR EXPERIMENT 2. Nitrogen excretion (mg.). Days In warm * 197* Mean In warm + methionine Mean In cold Mean In cold + methionine Mean * Urines for days 6 and 7 were pooled for analysis.

10 64 Effects of Cold and Burns on Protein Metabolism in Rats APPENDIX TABLE VI.-INDIVIDUAL VALUES FOR EXPERIMENT 3. Nitrogen excretion (mg.). Days Group 1 Burned in Cold * 193* * 274* Mean Group 2 Burned in warm Mean Group 3 Not burned in cold Mean * Urines for days 3 and 4 and 10 and 11 were pooled for analysis. REFERENCES. CLARK, E. J., PETERS, R. A., and RoSSITER, R. J. (1945). Quart. J. exp. Physiol. 33, 113. CROFT, P. B., and PETERS, R. A. (1945). Lancet (March 3), 266. CUTHBERTSON, D. P. (1932). Quart. J. Med. 25, 233. CUTHBERTSON, D. P. (1939). Quart. J. exp. Physiol. 29, 13. GRIBBLE, M. DE G., PETERS, R. A., and WAKELrN, R. W. (1947). J. Physiol. 106, 36 P. GRIBBLE, M. DE G., and PETERS, R. A. (1949). As yet unpublished. LATHE, G. H. (1949). J. Physiol. 108 P. In press. LATHE, G. H., and PETERS, R. A. (1949). Quart. J. exp. Physiol. In Press. LuSK, G. (1929). Elements of Science of Nutrition. 4th Edition. Philadelphia and London.

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