Transfer of orally administrated iodine-131 into chicken eggs

Applied Radiation and Isotopes 58 (2003) 299–307

Transfer of orally administrated iodine-131 into chicken eggs . . Turan Unak*, Yeliz Yildirim, U&gur Avcibas-i, Berkan C . Unak , etinkaya, Gulcan Division of Nuclear Chemistry, Department of Chemistry, Faculty of Science, Ege University, Bornova, Izmir 35100, Turkey Received 6 January 2002; received in revised form 25 November 2002; accepted 3 December 2002

Abstract Radioactive iodine-131 as both as free iodide (Na131I) and covalently bound to aniline (aniline-131I) was added to the drinking water of two Leghorn laying hens as a single dose and also as a cumulative dose over 1 week. The radioactivity of the principal parts of the eggs, i.e. shell, white, and yolk, was measured, and the radioactivity levels per gram material, and percent of the total radioactivity were calculated. The radioactivity measurements were continued for 1 month following the administration of 131I. In the case of the single dose administration, the results obtained showed that about 15% of the total radioactivity administered as Na131I was transported into the egg structure; compared to only about 1% for aniline-131I. After cumulative administration, about 15% of the total administered radioactivity was transported into the egg structure with both forms of 131I. This was probably because of metabolic cleavage of iodine bonds in the labeled aniline molecules during the longer period of exposure. These results also showed considerable accumulation of 131I in the egg yolks. In the case of the single dose administration, 131I can be detected in eggs up to about 20 days after administration, and up to about 30 days, in the case of the cumulative administration over 1 week. r 2003 Elsevier Science Ltd. All rights reserved. Keywords: Iodine-131; Chicken egg; Radioiodinated aniline

1. Introduction Iodine is a very important trace element in foods consumed by humans as well as by animals; poultry eggs are one of the essential foods consumed by humans. The high cholesterol level in eggs seriously limits their safe consumption especially by people having high cholesterol problems. On the other hand, in recent years it has been reported that iodine has an important role in the decreasing of human cholesterol level (Rys et al., 1995). These interesting relations among iodine, egg, and cholesterol, have led to the production of iodineenriched eggs being considered to eliminate the negative action of egg on human cholesterol levels, and consequently to augment the safe consumption of eggs (Michella and Slaugh, 2000; Garber et al., 1993). In

*Corresponding author. Tel/fax: +90-232-388-8264. . E-mail address: [email protected] (T. Unak).

addition to this, 131I is one of the most important fission fragments, produced in the fuel core of nuclear power plants, and during nuclear tests and accidents. For this reason, the global atmosphere and consequently human foods are always have a risk of being contaminated seriously by 131I. The Chernobyl nuclear plant accident that occurred in the Ukraine in 1986 was a dramatic example of environmental contamination by this radionuclide (Cosma et al., 1996). All these phenomenon show clearly the importance of studying the transfer of orally administrated 131I into chicken eggs. A number of studies of iodine distribution in eggs have been reported (Bogdanov et al., 1996; Travnicek et al., 2000; Stibilj et al., 1997; Hou et al., 1997; Daugeras-Bernard and Lachiver, 1980), but few of used 131I as a tracer of small amounts of iodine administered to chickens (Kirshin et al., 1970; Shibata and Ikeda, 1970). For this reason, in this study we measured the radioactivity distribution of orally administered 131I in chicken eggs.

0969-8043/03/$ - see front matter r 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0969-8043(02)00350-0

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2. Experimental 2.1. Preparation of a special poultry-house A special poultry-house for two separated chickens was designed to control the radioactive contamination of the working area, and to facilitate the radioactivity measurements of eggs. A small glove box of about 2 m3, of the type used for general radioactivity manipulations, was used for these studies. The glow-box was connected to an aspiration system, and was equipped with some additional systems for the daily removal of feces, collection of eggs, and regularly charging with water, food, and 131I. Two Leghorn chickens were brought from the chicken farm of the Faculty of Agriculture, and were kept in this special poultry-house from 2 weeks before the work started to ensure their adaptation to the new surrounding, and their regular schedule of laying eggs. 2.2. Administration of iodine-131 Iodine-131 was administered to each chicken in two different chemical forms, which were added to their drinking water: either as aqueous solutions of free iodide (Na131I) or as radioiodinated aniline (aniline-131I). The administration of 131I was carried out in two different ways. In the first, about 1.85  106 Bq/0.5 ml (50 mCi/ 0.5 ml) of either Na131I or aniline-131I were added separately to the drinking water of each chicken. In the second method, the aqueous solutions of Na131I were added gradually everyday to the drinking water during 1 week. The total 131I administrated was about 1.63  107 Bq/1.4 ml (440 mCi/1.4 ml); about 2.33  106 Bq/0.200 ml (65 mCi/0.200 ml) on the first day, and then 0.2 ml everyday at the same time during one week. By the last day, the 131I had decayed to about 1.54  106 Bq/0.2 ml (43 mCi/0.2 ml). In the case of aniline-131I, the total administered 131I was about 9.99  106 Bq/1.05 ml (270 mCi/1.05 ml). The radioactivity added to the drinking water of the second chicken on the first day was about 1.40  106 Bq/0.15 ml (38 mCi/ 0.15 ml); on the last day this was about 8.88  105 Bq/ 0.15 ml (24 mCi/0.15 ml). Each day at the same time about 250 ml of water corresponding to the daily water needs of each chicken was added simultaneously to their water bowls. In addition, about 125 g commercial poultry food corresponding to the daily need of a chicken was added everyday to their mangers, and lighting was provided for 17 h per day. 2.3. Radioiodination of aniline with iodine-131 . The procedure described earlier (Unak et al., 2001) was used for the preparation of aniline-131I. According to this procedure, 50 ml of freshly distilled aniline was

dissolved in 50 ml of water, and 1 ml of this solution (about 1 mg aniline/ml) was added to a glass tube coated with solid iodogen (1,3,4,6-tetrachloro-3a-6a-diphenylglucoluril) and containing broken glass pieces. About 15 min waiting time was sufficient for a >95% radioiodination yield. 2.4. Radioactivity measurements of eggs Leghorn chicken laid eggs approximately everyday, and these were collected daily, and processed immediately for radioactivity measurements. Up to about 30 eggs from each chicken were processed. Each egg was first washed well using light detergent to eliminate any external radioactivity contamination, and then weighed. Gently broken eggs were carefully and as far as possible completely separated into their principal parts, shell, white, and yolk, and each of these was weighed. Radioactivity measurements were carried out under approximately the same geometrical conditions using a counting system having a 4  4 in NaI(Tl) scintillation detector. Before the counting, the shells were slightly pressed to prevent their volumes from swelling.

3. Results and discussion As mentioned above, two different ways were pursued to study the accumulation of 131I in chicken eggs. In the first, 131I was given to a chicken as a single dose; in the second, the 131I was administered gradually over a time period of 1 week. The results obtained with each form of administration are discussed below. 3.1. Administration as a single dose The 131I in the principal parts of the eggs, expressed as per gram of material and as per cent of the total egg radioactivity, are summarized in Tables 1 and 2 for Na131I and aniline-131I, respectively. The total radioactivity variations in the yolk, white, and shell of each egg as a function of time are shown in Figs. 1 and 2, for both cases. Fig. 3 shows the variation in the externally measured total radioactivity in the eggs as a function of time for the same cases. Fig. 3 shows that the total radioactivity of the eggs gradually increases to reach a maximum value in the fourth egg after both forms of 131 I administration. The radioactivity then decreased drastically, reaching background levels in about two weeks in both cases. The data given in Tables 1 and 2, and Figs. 1 and 2 also clearly show that in general the 131 I accumulated principally in the yolk of the egg, however, in the first eggs laid the radioactivity levels of the white parts were considerably higher than those of the yolks. This probably results from the earlier development of the yolks in the chicken egg production

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Table 1 Dataa obtained of Na131I administration as a single dose Eggs order

Date (2001)

Yolk (counts)

White (counts)

Shell (counts)

Yolk (counts/g)

White (counts/g)

Shell (counts/g)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

9 April 10 April 11 April 12 April 14 April 15 April 16 April 17 April 20 April 21 April 22 April 23 April 25 April 26 April 27 April 28 April 29 April 30 April 2 May 3 May

1140 85,092 216,672 265,242 195,522 95,994 34,386 5166 1289 1002 685 641 585 449 511 438 341 297 209 286

54,354 7038 3102 2586 300 114 222 78 63 59 13 0 66 20 14 48 5 24 28 34

7440 1500 534 402 78 66 18 0 15 23 0 28 14 0 14 0 0 16 14 10

67 4600 12,452 16,894 14,377 4923 1859 325 71 54 40 41 34 27 27 24 20 19 13 15

1288 183 73 60 8 3 5 2 1 2 0 0 2 1 0 1 0 1 1 1

647 130 48 41 9 6 1 0 1 2 0 2 2 0 1 0 0 2 2 1

Total of eggs: 985,097 cpm (E3.28  105 Bq). a All radioactivity data are given as cpm, and 1 cpmE0.33 Bq. Counting errors were about 71% for counts higher than 10,000, about 72% for counts between 10,000 and 1000, about 710% for counts between 1000 and 100, and about 750% for counts less than 100.

Table 2 Dataa obtained of aniline-131I administration as a single dose Eggs order

Date (2001)

Yolk (counts)

White (counts)

Shell (counts)

Yolk (counts/g)

White (counts/g)

Shell (counts/g)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

9 April 10 April 12 April 13 April 14 April 15 April 16 April 18 April 19 April 20 April 21 April 22 April 24 April 25 April 26 April 27 April 28 April 29 April 30 April 1 May

6 6648 14,118 17,454 13,896 5832 2472 613 507 322 353 496 653 585 440 321 302 319 219 138

515 594 282 0 0 60 108 34 83 24 84 23 47 66 22 0 28 2 80 19

286 102 66 48 48 0 18 0 50 29 18 0 0 14 0 4 0 0 26 8

0 223 856 904 764 322 133 34 25 17 19 26 37 33 25 16 16 18 16 8

14 17 7 0 0 2 3 1 2 1 2 1 1 2 1 0 1 0 2 1

30 10 6 5 4 0 2 0 5 3 2 0 0 2 0 0 0 0 3 1

Total of eggs: 69,522 cpm (E2.32  104 Bq). a All radioactivity data are given as cpm, and 1 cpmE0.33 Bq. Counting errors were about 71% for counts higher than 10,000, about 72% for counts between 10,000 and 1000, about 710% for counts between 1000 and 100, and about 750% for counts less than 100.

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302

100 90 80 Radioactivity (%)

70 60 50 40 30 20 10 0 1

2

3

4

5

6

7

8

9

10 11 12 13 14 15 16 17 18 19 20

Order of eggs Yolk

White

Shell

Fig. 1. Radioactivity variations in yolk, white, and shell as percent of the total radioactivity of eggs for aniline-131I administered as a single dose.

100 90

Radioactivity (%)

80 70 60 50 40 30 20 10 0 1

2

3

4

5

6

7

8

9

10 11 12 13 14 15 16 17 18 19 20

Order of eggs Yolk

White

Shell

Fig. 2. Radioactivity variations in yolk, white, and shell as percent of the total radioactivity of eggs for Na131I administered as a single dose.

mechanism. The 131I content of the shell was rather low. This indicates that 131I is transported into the structure of eggs so as to be bound eventually to the proteins or protein-like molecules. It is also interesting to note that

the externally measured radioactivity of eggs 2 or 3 times lover than that of their yolks. This was surely due to selfabsorption of some portion of the radiation emitted from the yolk, which lies at the center of the egg, by the

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303

140

Total radioactivity (×103 cpm)

120

Covalently bound iodine-131 (aniline-l-131) Free iodine-131 (NaI-131)

100 80 60 40 20 0

1 2

3

4

5

6

7

8

9 10 11 12 13 14 15 16 17 18 19 20 Order of eggs

Fig. 3. Externally measured radioactivity variations of eggs after administration of a single dose of Na131I or aniline-131I. Table 3 Dataa obtained of Na131I administration as a cumulative dose over 1 week Eggs order

Date (2001)

Yolk (counts)

White (counts)

Shell (counts)

Yolk (counts/g)

White (counts/g)

Shell (counts/g)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30

8 February 9 February 11 February 15 February 16 February 18 February 19 February 20 February 21 February 22 February 23 February 25 February 26 February 27 February 28 February 1 March 2 March 3 March 5 March 6 March 7 March 9 March 10 March 11 March 12 March 13 March 14 March 15 March 17 March 18 March

7008 110,916 626,022 1,516,230 1,201,242 919,068 821,208 654,120 359,970 216,384 62,304 24,084 15,084 9666 5898 8322 6990 5004 4284 4007 3441 2171 1679 1967 1989 2460 1843 1448 1000 606

98,700 221,754 139,290 105,012 35,034 8022 4332 1632 744 696 390 174 420 840 396 384 258 42 230 104 152 139 267 87 42 118 5 0 0 37

22,986 31,362 22,596 18,300 5106 1746 606 210 114 54 18 0 0 162 0 216 0 0 78 21 83 0 116 129 0 0 0 0 0 48

387 5807 30,538 85,663 58,884 51,925 45,878 34,980 17,560 11,571 3461 1361 833 537 288 457 402 284 230 219 188 117 95 112 112 142 98 78 56 35

2577 5790 3500 2431 905 209 116 38 19 17 10 4 11 21 12 11 7 1 6 3 3 3 7 2 1 3 0 0 0 1

3193 3779 2568 1906 516 180 63 21 9 5 2 0 0 17 0 22 0 0 8 2 8 0 12 15 0 0 0 0 0 5

Total of eggs: 7,311,345 cpm (E2.44  106 Bq). a All radioactivity data are given as cpm, and 1 cpmE0.33 Bq. Counting errors were about 71% for counts higher than 10,000, about 72% for counts between 10,000 and 1000, about 710% for counts between 1000 and 100, and about 750% for counts less than 100.

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Table 4 Dataa obtained of aniline-131I administration as a cumulative dose over 1 week Eggs order

Date (2001)

Yolk (counts)

White (counts)

Shell (counts)

Yolk (counts/g)

White (counts/g)

Shell (counts/g)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30

9 February 10 February 11 February 12 February 13 February 14 February 15 February 17 February 18 February 19 February 20 February 21 February 22 February 23 February 25 February 26 February 27 February 28 February 1 March 2 March 3 March 5 March 6 March 7 March 9 March 10 March 11 March 12 March 13 March 14 March

1554 20,640 146,382 414,960 644,406 708,324 695,778 522,498 401,622 365,034 173,748 89,646 48,558 19,956 12,846 8694 5196 5310 5940 6060 5556 5660 5275 4542 3166 1759 1015 1416 602 507

21,144 30,522 37,818 38,514 39,282 35,760 26,982 6402 1184 1062 978 432 534 100 114 306 366 174 246 270 144 204 102 128 90 0 9 0 0 0

5028 4644 6354 9072 6282 5706 5274 534 264 120 168 36 138 48 0 0 84 0 108 78 72 158 166 54 68 0 0 0 0 0

81 1042 7393 21,171 34,645 40,246 39,987 29,354 20,182 19,314 9547 4694 2583 1045 680 488 315 178 325 322 302 308 249 227 150 94 49 36 30 26

470 757 918 949 982 892 694 161 43 25 24 11 12 0 3 8 8 4 6 6 4 5 2 3 2 0 0 0 0 0

513 430 594 848 604 571 549 58 26 13 6 3 13 5 0 0 8 0 11 8 7 18 15 6 8 0 0 0 0 0

Total of eggs: 4,614,573 cpm (E1.54  106 Bq). a All radioactivity data are given as cpm, and 1 cpmE0.33 Bq. Counting errors were about 71% for counts higher than 10,000, about 72% for counts between 10,000 and 1000, about 710% for counts between 1000 and 100, and about 750% for counts less than 100.

solid structure of the shell and the egg white. The radioactivity concentrations in the shell, white, and yolk, per gram of material, are also given in Tables 1 and 2. Figs. 1 and 2 show the percent radioactivity distribution between yolk, white, and shell. In the case of Na131I, the radioactivity of the white and yolk were 86.4% and 1.8%, respectively; but the radioactivity of the yolk reached 99.5% at the end of 1 week. In the case of aniline-131I, the radioactivity of white and yolk were about 63.8% and 0.7%, and similar radioactivity variations in shell, white, and yolk were observed. It is very interesting to note that the total egg radioactivity, as well as the 131I accumulation in the principal parts of eggs, was considerably lower in the case of aniline-131I than in that of Na131I. These results indicate clearly the importance of the chemical form of iodine-131 for transport into the egg structure during the egg production in chickens.

3.2. Cumulative administration of iodine-131 as gradually increased doses The data obtained from the study involving the cumulative administration of 131I are summarized in Tables 3 and 4, and their variations as a function of time are shown in Figs. 4–6. As is seen clearly from these tables and figures, the total externally measured radioactivity values of the eggs gradually increased, and reached a maximum value in the fifth egg in the case of Na131I, and in the sixth egg in the case of aniline-131I, within the period of about 1 week, and then drastically decreased. It is clearly seen that about 15% of the total administrated 131I was equally transported into the egg structure for both Na131I and aniline-131I, this result is different from the case of single dose administration. This was probably due to the metabolic cleavage of iodine bonds during the longer residence of aniline-131I

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305

100 90 80 Radioactivity (%)

70 60 50 40 30 20 10 0 1

3

5

7

9

11

13

15

17

19

21

23

25

27

29

Order of eggs Yolk

White

Shell

Fig. 4. Radioactivity variations in yolk, white, and shell as percent of the total radioactivity of eggs after Na131I administration as a cumulative dose over 1 week.

100 90 80

Radioactivity (%)

70 60 50 40 30 20 10 0 1

3

5

7

9

3

15

1

21

23

25

27

29

Order of eggs Yolk

White

Shell

Fig. 5. Radioactivity variations in yolk, white, and shell as percent of the total radioactivity of eggs after aniline-131I administration as cumulative dose over 1 week.

molecules in the chicken. The radioactivity levels of the eggs decreased to about background levels within about 1 month for Na131I, and about 20 days for aniline-131I. The variations of the 131I concentrations in shell, white, and yolk per gram material are, for both forms of 131I,

similar to the case of a single dose administration, but it should be also noted, Fig. 6, that the decrease of total radioactivity in the case of aniline-131I was considerably slower than with Na131I. This was probably because of the binding of aniline-131I to proteins or protein-like

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306

800

Total radioactivity (×103 cpm)

700 Covalently bound iodine-131 (aniline-l-131) Free iodine-131 (NaI-131)

600 500 400 300 200 100 0 1

3

5

7

9

11

13

15

17

19

21

23

25

27

29

Order of eggs Fig. 6. Externally measured radioactivity variations of eggs after administration of Na131I or aniline-131I as a cumulative dose in 1 week.

molecules were more difficult. Thus, 131I transfer into the egg structure, i.e. into the yolk, becomes much slower for the same time period, as compared to Na131I.

4. Conclusions The conclusions of this study can be summarized as follows: 1. The results obtained have shown clearly that orally administrated iodine either as free iodide (Na131I) or as covalently bound to an organic molecule (aniline-131I) can be accumulated in chicken eggs, especially in the yolk, but free iodide can accumulate to a greater extent than its covalently bound form. 2. In the case of a single administration, the radioactivity measurements have indicated that about 15% of total 131I administered as Na131I was transported into the egg structure; but only about 1% for aniline-131I. In the case of cumulative dose administration, the 131I transportation ratios into the egg structure were similar, at about 15%, for both Na131I and aniline-131I forms. This was probably due to the metabolic cleavage of iodine bonds during the longer residence of aniline-131I molecules in the chicken. 3. Iodine-131 radioactivity administered as a single dose was detected in eggs for up to 20 days after its administration, but for cumulative administration over 1 week, this was longer, up to 30 days. This means that, in the case of the environmental contamination with 131I including the natural or

commercial foods of chickens, the eggs should not be eaten for at least 1 month following the disappearance of the contamination; then, they can be safely eaten in respect of 131I. 4. It would also be interesting to examine 131I transportation into chicken meat, and the rate of excretion in the feces. 5. Similar studies with other radionuclides such as 90Sr and 137Cs, which are the potential radionuclides for environmental contamination during a nuclear accident, would be helpful to determine the health regulations for consumption of eggs by the public. 6. These results also indicate that iodine metabolism in relation to chicken eggs and poultry meat consumption by the public could be studied using 131I to obtain much more easily than with cold iodine measurements.

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