O F TIlE commonly eaten foodstuffs, sea

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1 Nature and Availability of Iodine in Fish % ICIIAEL T. HARRISON, M.D., * SHEENA MCFARLANE, B.SC., t RONALD McG. HARDEN, M.B.CH.B. AND EDWARD WAYNE M.D.,F.R.C.P. O F TIlE commonly eaten foodstuffs, sea fish has the highest iodine content. Iodine deficiency is rare in maritime communities, and in areas in which iodine-deficiency goiter is efl(lefiflc the scarcity of fish is thought to be a contributing factor to an inadequate intake of iodine. In a community in which iodine-deficiency goiter is uncommon, we have found that the majority of patients with the condition, especially men, rarely eat fish. It is not known, however, whether all the iodine present in fish is available, or whether the calculated intake of iodine based on the chemical analysis of uncooked fish indicates the amount of iodine actually eaten, absorbed and available to the thyroid gland. Therefore, studies were carried out to determine the cheniical nature of iodine in fish, the extent of iodine losses during cooking and the efficiency of intestinal absorption of iodine from fish. METHOD Adult female plaice (Pleuronectes pkzlessa) were given lot.) c. I s by injection into the coelomic cavity. The fish were killed two days later, the total radioactivity counted with a directional scmtillation counter and the fillets removed. Nature of Iodine in Fish Portions of fillet of plaice or haddock (Gadus aegiefinus), 1)0th uncooked and fried, were homogenized in a \\ aring blender. The homogenate was centrifuged, and the precipitate separated from the supernatant and washed with deionized water. The content of 1131 and stable iodine (11V) was determined in supernatant and precipitate. Stable iodine was measured after chloric acid digestion by From the University Department of Medicine, Gardiner Institute, Western Infirmary, Glasgow, Scotland. * Lecturer iii Medicine; t Research Assistant; Registrar in Medicine; Professor of Medicine. the method of Farrell and Richmond.2 The supernatant was then studied in the following ways: (1) Excess trichloroacetic acid (TCA) was added to separate free from protein-bound iodine, and the amount of radioactive and stable iodine was determined in the supernatant and precipitate. (2) After TCA precipitation, the supernatant was subjected to chromatography on Dowex 1 resin, and tests for the presence of radioactive and stable iodine were carried out on the fraction eluted at ph 1.4. This is the fraction in which thyroid hormones (thyroxine and triiodothyronine) appear. (3) The original supernatant was extracted with acid butanol, and radioactive and stable iodine content measured before and after washing with 4 N sodium hydroxide. A 10 ml. portion of the original homogenate was exhaustively dialyzed in a cellophane bag against deionized water, and the iodine remaining in the homogenate measured. The total iodine concentration was measured in serum pooled from twelve haddock. The pooled serum, diluted twenty times, was then passed through an Amberlite IRA-400 resin in the chloride form, to remove inorganic iodine, and the iodine content of the eluate determined. Effect of Cooking on Iodine Content of Fish Weighed portions of fillets of plaice and of haddock were cooked by boiling in iodine-free water, grilling or frying. To determine the iodine content of the raw and cooked fillets, a desiccated pellet containing about I gm. of homogenized fillet was ignited in a Gallenkamp bomb calorimeter at 23 atmospheres of oxygen, and the liberated iodine was absorbed in normal solution of sodium hydroxide inside the bomb 3b Also measured was the iodine content of the water used for boiling, after chloric acid digestion. Absorption of Iodine s from two or three radioactive-labeled plaice were blended in a Turmix homogenizer, made into cakes with a little mashed potato, coated with egg and breadcrumbs and fried. The fish American Journal of Clinical Nutrition 73 Vol. 17, August 1965

74 Harrison, McFarlane, Harden and Wayne FIG. 1. Autoradiogram of plaice two days after injection of I 131 into coelornic cavity showing generalized distribution of radioactivity.

2 74 Harrison, McFarlane, Harden and Wayne FIG. 1. Autoradiogram of plaice two days after injection of I 131 into coelornic cavity showing generalized distribution of radioactivity. cakes were weighed after cooking, and one was used as a standard. The others were fed to volunteer subjects, who then collected all feces and urine separatelv for five days. I s uptake by the thyroid gland was prevented by the administration of carbimazole in a dose of 15 mg. given every 6 hours during the I)eriod of collection. Radioactivity in feces, urine and in the homogenized standard fish cake was counted in a well-type scintillation counter. RESULTS Radioiodiiie was absorbed from the coelomic cavity and within 48 hours of injection was distributed throughout the body of the fish (Fig. 1), confirming the findings of Hickman.4 Fish Iodii,e Content of s of Plaice Before and After Cooking Uncooked Iodine Co!,tent* (/.Lg. per gin, wet fish) Boiled * Figures in parentheses represent per cent loss. I Water Used for Boiling Grilled (35) 0.36 (33) 0.98 (9) (29) 0.026(29) 0.054(40) (50) 0.03 (14) (62) 0.30 (49)... Nature of Iodine in Fish After separation of the supernatant and precipitate of the homogenized fish, the entire iodine content, both radioactive and stable, was found to be present in the supernatant, the washed precipitate being free from iodine. On further study of the supernatant fraction, it was found that (1) after precipitation of proteins by TCA, the entire radioactivity remained in the supernatant fraction, none was present in the washed precipitate ; (2) after TCA precipitation, resin chromatography of the supernatant on Dowex 1 resin showed that no radioactive or stable iodine was eluted at ph 1.4, the ph at which thyroid hormone vould have appeared in the eluate ; and (3) the extraction of radioactive and stable iodine from the supernatant by acid butanol was PH) per cent. After washing with alkali, no radioactivity or stable iodine remained in the butanol phase. After dialysis of fish homogenate, no iodine could be detected in the homogenate indicating that all the iodine present was diffusible. The total iodine concentration of the pooled haddock serum was 1,480 gig. per 100 ml. After passage through the Amberlite resin no iodine was detected in the eluate, indicating that virtually all the serum iodine was present in inorganic form. These results indicate that all the iodine present in the fillet, both radioactive and stable, was present in inorganic form, and no thyroxme-like compounds or iodoproteins were detected either before or after cooking. Effect of Cooking on Iodine Content of Fish Losses of iodine resulting from cooking fillets of plaice and haddock are shown in Tables I and ii. There was marked variation in the iodine content of the different fish, varying from 0.09 to 1.07 gig. per gm. wet eight in uncooked plaice and from 1.22 to 1.69 jig. per gm. wet weight in haddock. The iodine losses in plaice varied from 29 to 62 per cent on boiling. In two cases, the losses were completely accounted for by the iodine content of the water used for boiling. Two plaice fillets were grilled, and the iodine losses were

3 Nature and Availability of Iodine in Fish 75 Iodine Content of s of Haddock Before and After Cooking II Iodine Content* (big. per gm. wet fish) F Is II Uncooked Boiled Water Used Grilled for Boiling Fried (70) 0.82(67) 0.97(21) 1.04(15) (59) (31) 1.01(20) (63) 0.82(63) 0.96(27) 1.02(22) (82) 0.69(52) 1.13(15) 1.24 (6) (50) 0.66(49) 1.04(23) 1.16(14) (76) 0.64(38) 1.30(21) 0.98(42) * Figures iii parentheses represent per cent loss. 9 and 41) per cent. The boiling of haddock resulted in iodine losses varying from 50 to SO per cent ; in three cases the iodine content of the water used for boiling accounted for the loss. After some of the fillets were boiled, a sediment was noted in the water, due to fragmentation of small parts of the fish. When haddock was grilled the iodine varied from 15 to 31 p cent, when fried from 6 to 42 per cent. Absorption of Iodine Ten Patients with no evidence of gastrointestinal disorder were studied. The results of ingestion of radioactive plaice are shown in Table III. Iii all the patients fecal excretion of was less than 1 per cent of ingested radioactivity, and in four patients no I s was detectable. In the six patients in whom urinary collections were complete, more than 81) per cent of the ingested J131 appeared in the urine over the period of collection. COMMENTS These studies indicate that all the iodine measured in the fish fillets and in the serum was present in inorganic form. While it is known that the thyroid glands of fish can synthesize thyroxine from inorganic iodine,5 the thyroid is rarely eaten by man as it is situated in the head of the fish below the floor of the mouth. It is probable that small amounts of thyroid hormone circulate in the fish and are present in the edible portion, but we were unable to detect either radioactive or stable organicallybound iodine. It is not known by what mechanism fish are able to maintain a high gradient of inorganic iodine between their flesh and body fluids and sea water. It is likely that their intake of iodine is high but, in addition, that a concentrating mechanism is probably required to keep the level of inorganic iodine in the blood higher than that of sea water. In the case of the haddock, this concentration gradient is approximately 3() : 1 which is similar to that maintained by the thyroid gland and other iodine-concentrating organs.6 There is some evidence that the gills may possess such an iodide-concentrating mechanism7 but little is known about its properties. Excretion of J131 in Feces and Urine After Ingestion of Fish Sex % % and Age Diagnosis 1131 in J131 (yr.) Feces Urine F, 42 Obesity 0... F, 43 Rheumatic heart disease M, 49 Ischemic heart disease M, 50 Ischemic heart disease, 0 96 F, 60 Nontoxic goiter M, 63 Treated hypothyroidism I M, 64 Ischemic heart disease 0 95 F, 65 Ischemic heart disease 0 86 M, 65 Bronchitis F, 66 Rheumatic heart disease III

4 76 Harrison, McFarlane, Harden and Wayne When fish is cooked, significant losses of iodine occur. These losses were greatest after boiling, when an average of 58 per cent of the iodine disappeared from the fish ; in about half the cases the loss could be accounted for completely by the amount of iodine found in the water used for boiling. In the rest some iodine was probably lost in the sediment at the bottom of the container. When fish was grilled, the average loss of iodine was 23 per cent ; when fried, 20 per cent. Such losses in cooking are clearly of importance when iodine intake is studied, since fish is an important source of dietary iodine. If iodine intake is calculated from dietary surveys and tables listing the iodine content of uncooked foods considerable errors will arise. Suspicion of such errors in calculating iodine intakes has arisen8 as a result of the discrepancy observed between the urinary excretion of iodine in normal subjects (44 to 171 g. per day) and the mean calculated iodine intake in the same subjects (290 j.g. per day). Iodine losses during cooking are not the sole cause of inaccurate calculated dietary intakes ; errors also result from the use of tables9 in which the iodine content of different samples of the same foodstuffs may vary. This is illustrated in the present study by the variation in the iodine content of individual plaice obtained from different sources. Also shown in the present studies is the fact that, in the case of fish at least, losses due to cooking are equally important and that a sample diet must be analyzed after it has been cooked in order to determine its true iodine content. Our studies demonstrate that in persons without evidence of any disorder of the alimentary tract, virtually all the available iodine in fillets of plaice is absorbed after ingestion. Whether iodine absorption in patients with malabsorption is as efficient is not known, but Harden and Adams #{176}have found evidence of iodine deficiency after total gastrectomy, probably a result of poor iodine absorption since the diets of the patients studied contained fish. In man, inorganic iodine is completely absorbed from the alimentary tract after ingestion, at least in the fasting state, but the iodine in thyroxine is not (after ingestion of radioactive thyroxine, up to 40 per cent of the activity appears in the feces. 12) The complete absorption of iodine from fish, therefore, is consistent with our finding that its iodine content in the edible fillet is entirely in inorganic form. SUMMARY In fillets of plaice (Pleuronecles platessa) and haddock (Gadus aeglefinus) the entire content of iodine was found to be present in inorganic form ; no thyroid hormone could be detected. Significant losses of iodine occurred when fillets were cooked. An average of 58 per cent of iodine was lost from the fish on boiling, mainly by diffusion of iodine into the water, but some by fragmentation of small portions of fish. The corresponding losses after grilling and frying were 23 per cent and 21) per cent, respectively. Absorption of iodine from I 31-labeled plaice was determined in ten subjects vith normal intestinal function. Iodine absorption in all was virtually complete with less than I per cent of the ingested I being recovered from the feces. ACKNOWLEDGMENT \Ve are most grateful to Mr. T. B. Bagenal aiul Mr. F. Latham for help in the preparation of radioactive plaice at the Marine Biology Research Station, Millport, Great Cumbrae. REFERENCES I. HARDEN, R. McG., ALExANDER, W. D. aiid HARRI- SON, M. T. Non-toxic goitre in males. Brit. M. J., 1: 1419, FARRELL, L. P. and RICHMOND, M. H. A rapid method for the estimation of serum l)roteinbound iodine. Clin. chim. acta, 6: 620, (a) PILEGGI, V. J., LEE, N. D., GoLuB, 0. J. and HENRY, R. J. I)etermination of iodine compounds in serum. I. Serum thyroxine in the presence of some iodine contaminants. J. C lin. Endorinol., 21: 1272, (b) MITCHELL, \V. I). In preparation. 4. HICKMAN, C. P., JR. The osmoregulatory role of the thyroid gland in tile starry flounder, Platichthys stellatus. anad. J. Zool., 37: 997, HICKMAN, C. P., JR. The conversion ratio as a discriminatory test for thyroid activity in fish, Nature, 189: 1012, 1961.

$Iodine metabolism in lower vertebrates. Ann. New York Acad. Sc., 86:316, 1960. 8. \\ AVNE, E. J., KOUTRAS, D. A. and ALEXANDER, \\. D. Clinical Aspects of Iodine Metabolism Oxford, 1964.$

5 Nature and Availability of Iodine in Fish BROWN-GRANT, K. Extrathyroidal iodide concentrating mechanisms. Physiol. Rev., 41: 189, LELOUP,.1. and FONTAINE, M. Iodine metabolism in lower vertebrates. Ann. New York Acad. Sc., 86:316, \\ AVNE, E. J., KOUTRAS, D. A. and ALEXANDER, \\. D. Clinical Aspects of Iodine Metabolism Oxford, Blackwell Scientific Publications. 9. \oug,it, R. L. amid LONDON, \V. T. Dietary sources of iodine. Am. J. Qin. Nutrition, 14: 186, HARDEN, R. McG. and ADAMS, J. F. Iodine de. ficiency following total gastrectomy. Metabolism, 13:843, ALBERT, A., RALL, J. B., KEATING, F. R., POWER, M. H. and WILLIAMS, M. M. D. The behaviour of labelled thyroglobulin and labelled thyroxine in patients with myxoedema. J. Clin. Endocrinol., 9: 1392, VAN MIDDLESWORTH, L. Re-evaluation of certain aspects of iodine metabolism. Recent Progr. Hormone Res., 16: 405, 1960.

Hypothyroidism. Causes. Diagnosis. Christopher Theberge

Hypothyroidism. Causes. Diagnosis. Christopher Theberge Hypothyroidism Pronunciations: (Hypothyroidism) Hypothyroidism (under active thyroid) is a condition where the thyroid gland fails to secrete enough of the thyroid hormones thyroxine (T4) and triiodothyronine