- Email: [email protected]
Accessory Thyroid Tissue in the Goat
Br. vet. ]. ( I g67),
123 1
I 62
ACCESSORY THYROID TISSUE IN THE GOAT By }3. F.
SANSOM
Agricultural R esearch Council, Institute for R esearch on Animal Diseases, Compton, Nr. Newbury, Berks.
SUMMARY
Accessory thyroid tissue was present either a t the base of the neck or between the rami of the jaws in four of r 7 normal adult goats. Six-and-a-half months after three of these four goats had been thyroidectomized the accessory tissues had disappeared in two and their 131 1-concentrating capacity had diminished greatly in the other. Residual or accessory thyroid tissue was found at the site of the original thyroid gland or in other sites 12 to 14 months after operation in I3 of r6 goats thyraparathyroidectomized as immature animals. Mature surgically thyroidectomized goats often do not show the symptoms commonly associated with hypothyroidism. Myxoedema does not always occur; if the animals are young the growth rate is severely affected, although to a smaller extent than after thyra-parathyroidectomy (Payne & Chamings, 1964). Similar observations have been reported on merino sheep, but even in lambs thyroidectomy produced variable effects, some showing practically no depression in basal metabolic rate or growth rate (Marston & Peirce, 1932). The failure to show symptoms after thyroidectomy has been attributed to the presence of accessory thyroid tissue. Indeed the occurrence of accessory thyroid tissues has been described in cattle, pigs, goats, horses, dogs and cats (see Ellenberger & Baum, 1943), and recently by inference from 131 1 uptake studies in goats (Ekman, 1965). The present work was designed to assess how commonly accessory thyroid tissue occurs in the goat and to show how such tissue reacts to the removal of the main thyroid gland lobes.
MATERIALS AND METHODS
Animals
Castrated male or non-lactating non-pregnant female goats in a state of anoestrus were used. They were thyroidectomized or thyra-parathyroidectomized as d escribed by Payne & Chamings (1964).
Isotope Gelatine capsules containing 50-roo f-lC 131 1, Code IBS 51P (as issued by the Radiochemical Centre, Amersham), were given orally to the goats with the aid of a balling gun.
ACCESSORY THYROID TISSUE IN THE GOAT
Monitoring of thyroid tissue An Ekco Type W559E scintillation head with a Type 556A Nai (Tl) crystal, fitted with a simple cylindrical lead collimator, was used. The collimator, which had a central hole I8 mm. in diameter, was held in contact with the skin of the animal. The first measurements were made 24 hours after dosing and consisted of a rapid scan of the whole surface of the animal. The skin over the thyroid gland was between five and 50 times more active than that over surrounding tissues, and localized areas with activities only twice that of the immediately surrounding tissues could also be distinguished. These and any areas of greater relative activity were considered to be possible sites of accessory thyroid tissue and they were monitored daily. Radioactivity in the thyroid gland or other tissue was taken as the count rate over the gland less the background count rate over an adjacent area of relatively uniform low activity. Counting methods Approximately 5 g. of fresh tissue or 5 ml. of a solution of thyroid gland in N-NaOH were counted in an Ekco Type N 550A scintillation head with a Nai (Tl) well-type crystal. Standards were prepared by dissolving one of the standard 131 I gelatine capsules (see above) in water. The results were expressed as a percentage of the dose. The in vivo monitoring technique was calibrated when possible by comparing the radioactivity of the gland, as measured by in vivo monitoring immediately before slaughter, with the radioactivity of the gland removed from the body after death. The maximum uptake of 131 I by the thyroid could thus be expressed as a percentage of the dose given. The maximum uptake of 131 I by accessory thyroid tissue as measured by in vivo monitoring is expressed as a percentage of the maximum uptake of 13 1J by the main thyroid gland measured in the same way. Thyroxine Sodium L-thyroxine (Glaxo Laboratories Ltd.) was injected intramuscularly in doses of 4 or 20 f-Lg. /kg. per day. Plan of Experiment I Three mature male goats were dosed with IOO ftC 131 I, monitored and slaughtered three days later. Tissues were taken and analysed for 131 I (see Table I). Plan of Experiment 2 Eight mature female goats were dosed with 13 1!, monitored, and a month later surgically thyroidectomized. Six weeks after operation they were given a second dose ofl 31 I and again monitored. Finally, after a further five months they were given a third dose of 131 I, monitored and slaughtered (see Table II). Plan of Experiment 3 Sixteen male goats which had all been surgically thyra-parathyroidectomized I 2 to I4 months previously at ages between six and I 2 months, and six male
BRITISH VETERINARY JOURNAL, 123, 4
goats with intact thyroid and parathyroid glands, were given 131 1 and monitored. They were slaughtered two days later and their thyroids and any accessory thyroid tissues removed and analysed for 131 1. For I6 weeks before the administration of 131 1, six of these thyra-parathyroidectomized goats received 4 JLg. sodium L-thyroxinefkg. per day and six received 20 flg. /kg. per day (see T able III ). RESUL TS
Experiment I At necropsy three d ays after a single oral dose the concentration of 131 I in the thyroid glands, I ·03 per cent of the dose given/g. tissue, was approximately I ,ooo times that in any other tissue except for a small piece dissected from near the root of the tongue of one animal. This had a concentration of 0·43 per cent of the dose of 1 31Jfg. Histological examination proved this to be thyroid tissue similar in structure and colloid content to the main thyroid gland lobes of this goat. Table I shows the mean concentration of 131 1 in various organs and tissues three days after dosing. Only the thyroid glands concentrated 1311, so their uptake of this isotope appears to be a reliable diagnostic test for thyroid tissue. It is of interest that in vivo monitoring revealed no accessory thyroid tissue. Presumably that found at the time of necropsy near the root of the tongue was not d etected earlier because it was close to the main thyroid gland.
TABLE I THE
MEAN CONCENTRATION OF 131 1 I N TH E THYROID GLAND AND OTHE R T I SSUES OF THREE MALE GOATS THREE DAYS AFTE R DOSING
Tissue
Thyroid Tissue near root of tongue (one goat) Whole blood Blood plasma Skin Bone Voluntary muscle Fat Reticulum Omasum Duodenum Abomasum Bladder Heart Aorta
Mean
% dosefg.
131J
X Io•
1034 426 o·82 o·88 0'79 0' 19 0' 14 o·o5 o·84 o·69 1'1 3 1·8o 0'59 0'27 0'42
Tissue
Lung Diaphragm Kidney Liver Spleen Pa ncreas Trachea Thymus Adrenal Tongue Oesophagus Thyroid cartilage Parotid Pharynx Lymph node
Mean
% dose fg.
131/
X 103
o·68 0•26 0'75 o·61 0'55 0'37 1'0 1 0'45 0'36 1'36 1'34 0'51 0 '55 2'13 0'48
Experiment 2 Only one of the eight female goats (F4I I ) possessed an 131 1-concentrating region in addition to the main thyroid gland mass. It was situated at the base
TABLE II THE RES ULTS OF EXTERNAL MONITORING OF EIGHT GOATS WHICH HAD RECEIVED I 00 j.lC 131 I, BEFORE AND 6 WEEKS AND 6t MONTHS AFTER SURGICAL THYROIDECTOMY Before surgery Goat
F411 F4I1
Age when first dosed (years and months )
3"9
Maximum 131/ uptake (% dose)
44 4
-
F4II
F372 F372
3"8
F377 F377
3"8
Ws3 G4o G3I9 E202 G88
7"I I 3"0 2·8 4"9 2"I I
28
-
Site
Thyroid Base of neck -
Thyroid
-
Weigh (g. )
6 weeks after surgery Biological Maximum 131 / half-life uptake relative to days ) thyroid (%)
Site
0 0
6! months after surgery
Biological Maximum 131I half-life uptake relative to (days) thyroid (%)
Site
II > tr:l
Biological half-life (days )
IJJ IJJ
0
:::0
>< >-l
11 "5 ?
29 6
0 IO
-
-
IO
7"2
-
30 -
Thyroid Base of neck Rami of jaw
0 2 2
0 0 I
Thyroid Base of neck Rami of jaw
0 0 2
:r: ><
:::0
0...... 0
>-l ......
0 I
Thyroid Base of neck
0 5
0 0
Thyroid Base of neck
0 5
Thyroid Rami of jaw
0 2
0 0
Thyroid Rami of jaw
0 0
0 0 0 0 0
Thyroid Thyroid Thyroid Thyroid Thyroid
0 0 0 0 0
0 0 0 0 0
Thyroid Thyroid Thyroid Thyroid Thyroid
0 0 0 0 0
0 0
II ~
......
26
-
3I 23 39
44 37
Thyroid
Thyroid Thyroid Thyroid Thyroid Thyroid
8·5 -
I6·o I7•8 5"7 9"4 ll·8
2"2 -
2"2 2"0 5"3 5"3 29
II ~
II ~ O"l
(.;1
166
BRITISH VETERINARY JOURNAL, 123, 4
of the neck near the thoracic inlet and its 131 I-concentrating capacity was approximately ro per cent of that of the thyroid gland. Six weeks after thyroidectomy, when a second dose of 131 I was administered, the same accessory 131 I-concentrating area in goat F4I I could still be demonstrated. However, although it had approximately the same 1 31 I-concentrating ability, it did not retain the isotope for so long, i.e. it h ad a shorter biological half-life for 131 !. In addition another area of similar 131 I-concentrating capacity and biological half-life had appeared between the rami of the jaw. Two other animals in the group now also possessed 1 31 I-concentrating regions. In one (F372) this was situated towards the b ase of the n eck and had approximately I per cent of the 1 31 I -concentrating capacity of its original thyroid, and in the other (F377 ) a region at the back of its jaw had an 131 I -concentrating capacity of approximately 5 per cent of its thyroid gland. When a third dose of 131 I was administered five months later monitoring showed that only F4I I retained a site with 131 I-concentrating capacity. This was b etween the rami of its jaw, but the 131 I-concentrating capacity was only I per cent of that of its original thyroid gland. These findings are summarized in Table II. After death two small pieces of radioactive tissue were dissected from near the root of the tongue of F 4 I I. On histological examination these proved to be thyroid tissue.
Experiment 3 Table III shows 'that none of the six normal goats possessed accessory thyroid tissue, either on in vivo monitoring or at dissection after death. Three out of the four thyra-parathyroidectomized goats which had not received any supplementary thyroxine showed evidence, from monitoring and from post-mortem examination, of fragments of the original thyroid isthmus, presumably left at the time of surgery. One of these animals (J 326) also possessed a large nearly spherical lobe of thyroid tissue at the base of its neck, ventral to the trachea (Fig. I ) . The concentration of 131 I in this tissue was more than ten times greater than that in the thyroid glands of the normal goats. Five out of six goats which had received 4 f-lg. sodium L-thyroxinefkg. per day for the I6 weeks before administration of 131 I showed the presence of 131 Iconcentrating regions either at the site of the original thyroid or in other situations. Aft~r slaughter one goat (J 396) was found to possess three distinct masses of thyroid tissue spaced at equal intervals down the mid-line of the n eck from 5 em. to 6 em. below the position of the original thyroid gland to the thoracic inlet (Fig. 2). The concentration ofl 3 ll in these pieces of tissue and in those isolated from the other goats was again higher than that in the thyroid glands of the normal goats. Only one of the six goats receiving 20 p,g. sodium L-thyroxinefkg. per day showed the presence of accessory thyroid tissue by external monitoring. This animal possessed one piece of 131!-concentrating tissue at the site of the original thyroid and two small pieces in the region of the la rynx. All three tissues concentrated 13 1 I, but weakly compared with the thyroid glands of the normal goats. At necropsy four other goats in this group showed the presence of
ACCESSORY THYROID TISSUE I
THE GOAT
tissue resembling thyroid in the position of the original gland. Histological examination confirmed that these and all the other tissues described were thyroid gland. TABLE Ill 131 1
FOUND IN THE THYROID GLANDS AND ACCESSORY THYROID THE CONCENTRATION OF TISSUES OF 6 NORMAL GOATS AND I 6 THYRO-PARATHYROIDE CTOMIZED GOATS 48 HO URS AFTER ADMINISTRATION OF A SINGLE ORAL DOSE
Goat
Tissue
Thyroid Thyroid Thyroid Thyroid Thyroid Thyroid
Site NORMAL GOATS Thyroid Thyroid Thyroid Thyroid Thyroid Thyroid
THYRO-PARATHYROIDECTOMIZED GOATS At site of thyroid Residual thyroid isthmus Base of nec k (see fig. 1) Accessory thyroid Thyroid isthmus At si te of thyroid Thyroid isthmus At site of thyroid
131
1 Content (% dose fg. )
Weight (g. )
0'25 0'39 0'30 0'45 0'43 0•38
2'46 5'34 o·86 I·I8
I 3 '0 I 2·8 6·I 4'6 7'0 8·I
0'35 I'50 2•I 0'40
THYRO-PARATHYROIDECT6MIZED GOATS RECEIVING 4 j.!G. SODIUM L-THYROXINE/ KG. PER DAY Thyroid isthmus At site of thyroid o ·85 I '92 Accessory thyroid Near larynx 0'70 2'34 Accessory thyroid Near larynx 0'40 I '75 Thyroid isthmus At site of thyroid 2·6I 0'3I Accessory thyroid Near larynx 4'26 0'70 2•I Accessory thyroid In a chain lying in the 0'49 mid-line of the neck o·6 I'20 o·8I (see fig. 2 ) I' 30 Thyroid isthmus At site of thyroid 0'7 3'89 At site of thyroid Thyroid isthmus 5'80 0'4I Accessory thyroid Base of neck 7•88 0'4
J 328 J 328 ] 328
J I 77
ji84 ]I34 J 170
THYRO-PARATHYROIDECTOMIZED GOATS RECEIVING 20 j.!G . SODIUM L-THYROXINE/ KG. PER Thyroid isthmus Original thyroid o·I6 Accessory thyroid Near larynx o·2o Near larynx o·2o Accessory thyroid Thyroid isthmus Original thyroid Very low Thyroid isthmus Original thyroid Very low Thyroid isthmus Original thyroid Very low Thyroid isthmus Original thyroid Very low
DAY 0·38 o· I o·2 o· I 5 o·I o·2 o·2
DIS CUSSION
Accessory thyroid tissue was d etected either by in vivo monitoring or at necropsy in four of I7 normal adult goats. A remarkable property of this accessory tissu e was that it tended to regress and even disappear after thyroidectomy. This phenomenon occurred in three goats in which the accessory tissue detected either before or six weeks after operation disappeared completely or diminished substantially in 131 !-concentrating ability by six-and-a-half months after operation.
!68
BRITISH VETERINARY JOURNAL, 123, 4
This finding is difficult to explain. Thyroidectomy would be expected to increase the pituitary secretion of thyroid-stimulating hormone (TSH), which would in turn cause hypertrophy of any residual thyroid tissue. However, Wissig (I g64) suggested, on the basis of electron microscope examination of thyroid tissue, that there is a difference between the effects of mild and severe stimulation by TSH. During mild stimulation the Golgi apparatus appears to be more active in the formation of colloid droplets, whereas protracted severe stimulation disperses the Golgi apparatus and causes it to cease forming colloid droplets. Wissig suggests that the latter situation may be a manifestation of exhaustion resulting from over-activity and this may account for the atrophy of these glands in the present experiment. In contrast to the above findings in mature goats, residual and accessory thyroid tissue has been commonly found in goats thyra-parathyroidectomized between the ages of six and I 2 months. Of I 6 goats I 3 showed either residual thyroid tissue at the original site (I 2 animals) and/or quite distinct pieces of thyroid tissue at various other sites (five animals) I2 to I4 months after operation. Residual thyroid tissue in such a large number of animals is probably due to the fact that they were operated upon to remove parathyroid glands for another experiment and only sufficient thyroidectomy was carried out to ensure removal of the internal parathyroid glands. The 131 I-concentrating capacity of both the residual and accessory thyroid tissues in these animals was inversely related to the supplementary dose of sodium L-thyroxine which the animals had been receiving for the I 6 weeks before administration of 131I. Those receiving no sodium L-thyroxine or only 4 f.lg. Jkg. per day possessed hyperactive accessory thyroid tissues, while those receiving 20 f.lg. Jkg. per day had hypoactive thyroid tissues with respect to their 131 I-concentrating capacity in comparison with the thyroid glands of a group of normal controls. This may be accounted for by the direct inhibitory action of exogenous thyroid hormone on the secretion of TSH, and in this respect the accessory thyroid tissues behave like normal thyroid tissue. It seems· unlikely that in this group of animals which were operated upon while immature the absence of parathyroid glands would have had any influence on the presence or absence, or the hypertrophy or atrophy of the accessory thyroid tissues, subsequent to the operation. The accessory thyroid tissues of young animals are possibly less likely to atrophy on prolonged stimulation by TSH than those of adults. In view of the above results it appears that thyroidectomy of immature goats is followed by the retention or even the hypertrophy of residual or accessory thyroid tissue, whereas in adult goats the operation, although it may initially be incomplete, eventually results in complete thyroidectomy by the subsequent atrophy of any accessory thyroid tissue. The results of physiological experiments on "thyroidectomized" animals may be influenced by the above findings unless care is taken to ensure the removal of all thyroid tissue, or unless mature animals are used and an interval of at least six months is allowed to intervene between the date of operation and their use in experiments.
PLATE I
Fig.
1.
Accessory th yroid tissue a t base of neck of goat ] 326.
San om, B r. vet. ] ., I2J, 4
PLATE II
Fig . 2 . Th e po sit ion of the thr ee pieces of accessory thy roi d tiss ue lyi ng in the mi d-l ine of the nec k of go a t ] 396 .
Sa nso :n, Br. "'et. ]. , xz3, 4
ACCESSORY THYROID TISSUE IN THE GOAT
r6g
ACKNOWLEDGEMENTS
I thank Mr. R. J.
Colwil~
and Mr. M. Burrows for technical assistance. REFERENCES
EKMAN, L. ( 1965). Acta physiol. scand., 65, 331. ELLENBERGER, W. & BAuM, H. (I943). Handbuch der vergleichenden Anatomie der Haustiere, pp. 598-6oo. Berlin: Springer-Verlag. MARSTON, H. R. & PEIRCE, A. W. (I932). Aust. ]. exp. Bioi. med. Sci., 10, 203. PAYNE, ]. M. & CHAMINGS,j. (I964).]. Endocr., 29, I9. WISSIG, S. L. (I964). In The Thyroid Gland, Chapter 3, p . 52, ed. PITT-RIVERs, R. & TROTTER, W.R. London: Butterworths. (Accepted for publication 2 3rd January I 967)
La glande thyroide access oire chez Ia chevre (Sanso:rn) Resunte. Du tissu thyroide accessoire etait present a la base du col ou entre les branches montantes du maxillaire inferieur chez 4 sur I 7 chevres adultes normales. La thyroidectomie fut pratiquee sur trois d'entre ces quatre chevres et, apres six mois et demi le tissu accessoire avait disparu chez deux et le pouvoir de concentrer l'iode-I3I avait diminui considerablement chez la troisieme. Du tissu residue! ou accessoire etait present au site de Ia glande thyroide originaire ou en autres sites chez I3 sur I6 chevres I2-I4 mois apres thyro-parathyroidectomie a l'age impubere. Ober akzess orisches Schilddriisenge webe bei der Zi ege (Sanso:rn) Zusa:nunenfassung. Der Verfasser hat akzessorisches Schilddri.isengewebe bei vier von siebzehn gesunden erwachsenen Ziegen entweder vor dem Brusteingang oder im Kehlgang gefunden. Bei drei dieser vier Ziegen wurde die Schilddri.ise entfernt. Nach 6! Mona ten konnte 13 eine schwere Abnahme des 11-Konzentrationsvermogens und in zwei Fallen das Verschwinden des akzessorischen Gewebes festgestellt werden. Zwolfbis vierzehn Monate nach Entfernung der Schild- und Nebenschilddri.isen bei sechzehn unreifen Ziegen wurde bei dreizehn Tieren zuriickgebliebenes oder akzessorisches Schilddri.isengewebe an der ehemaligen Stelle der Schilddri.ise oder an anderen Stellen gefunden. La glandula tiroides acces orio en Ia cabra (Sans om) Resunten. Tejido accesorio era presente al nivel de la base del cuello o entre las ramas de Ia mandibula en 4 sobre I 7 cabras adultas normales. La tiroidectomia fue practicada sobre tres de estas cuatro cabras y seis meses y medio mas tarde en dos de elias el tejido accesorio haboa desaparecido y en Ia tercera el poder de concentrar el yodo- I 3 I habia disrninuido considerablemente. Tejido residual o accesorio era presente en el sitio de la glandula tiroides original o en otros sitios en 13 de I6 cabras I2-I4 meses despues de Ia tiro-paratiroidectornia en edad impubera.
123 1
I 62
ACCESSORY THYROID TISSUE IN THE GOAT By }3. F.
SANSOM
Agricultural R esearch Council, Institute for R esearch on Animal Diseases, Compton, Nr. Newbury, Berks.
SUMMARY
Accessory thyroid tissue was present either a t the base of the neck or between the rami of the jaws in four of r 7 normal adult goats. Six-and-a-half months after three of these four goats had been thyroidectomized the accessory tissues had disappeared in two and their 131 1-concentrating capacity had diminished greatly in the other. Residual or accessory thyroid tissue was found at the site of the original thyroid gland or in other sites 12 to 14 months after operation in I3 of r6 goats thyraparathyroidectomized as immature animals. Mature surgically thyroidectomized goats often do not show the symptoms commonly associated with hypothyroidism. Myxoedema does not always occur; if the animals are young the growth rate is severely affected, although to a smaller extent than after thyra-parathyroidectomy (Payne & Chamings, 1964). Similar observations have been reported on merino sheep, but even in lambs thyroidectomy produced variable effects, some showing practically no depression in basal metabolic rate or growth rate (Marston & Peirce, 1932). The failure to show symptoms after thyroidectomy has been attributed to the presence of accessory thyroid tissue. Indeed the occurrence of accessory thyroid tissues has been described in cattle, pigs, goats, horses, dogs and cats (see Ellenberger & Baum, 1943), and recently by inference from 131 1 uptake studies in goats (Ekman, 1965). The present work was designed to assess how commonly accessory thyroid tissue occurs in the goat and to show how such tissue reacts to the removal of the main thyroid gland lobes.
MATERIALS AND METHODS
Animals
Castrated male or non-lactating non-pregnant female goats in a state of anoestrus were used. They were thyroidectomized or thyra-parathyroidectomized as d escribed by Payne & Chamings (1964).
Isotope Gelatine capsules containing 50-roo f-lC 131 1, Code IBS 51P (as issued by the Radiochemical Centre, Amersham), were given orally to the goats with the aid of a balling gun.
ACCESSORY THYROID TISSUE IN THE GOAT
Monitoring of thyroid tissue An Ekco Type W559E scintillation head with a Type 556A Nai (Tl) crystal, fitted with a simple cylindrical lead collimator, was used. The collimator, which had a central hole I8 mm. in diameter, was held in contact with the skin of the animal. The first measurements were made 24 hours after dosing and consisted of a rapid scan of the whole surface of the animal. The skin over the thyroid gland was between five and 50 times more active than that over surrounding tissues, and localized areas with activities only twice that of the immediately surrounding tissues could also be distinguished. These and any areas of greater relative activity were considered to be possible sites of accessory thyroid tissue and they were monitored daily. Radioactivity in the thyroid gland or other tissue was taken as the count rate over the gland less the background count rate over an adjacent area of relatively uniform low activity. Counting methods Approximately 5 g. of fresh tissue or 5 ml. of a solution of thyroid gland in N-NaOH were counted in an Ekco Type N 550A scintillation head with a Nai (Tl) well-type crystal. Standards were prepared by dissolving one of the standard 131 I gelatine capsules (see above) in water. The results were expressed as a percentage of the dose. The in vivo monitoring technique was calibrated when possible by comparing the radioactivity of the gland, as measured by in vivo monitoring immediately before slaughter, with the radioactivity of the gland removed from the body after death. The maximum uptake of 131 I by the thyroid could thus be expressed as a percentage of the dose given. The maximum uptake of 131 I by accessory thyroid tissue as measured by in vivo monitoring is expressed as a percentage of the maximum uptake of 13 1J by the main thyroid gland measured in the same way. Thyroxine Sodium L-thyroxine (Glaxo Laboratories Ltd.) was injected intramuscularly in doses of 4 or 20 f-Lg. /kg. per day. Plan of Experiment I Three mature male goats were dosed with IOO ftC 131 I, monitored and slaughtered three days later. Tissues were taken and analysed for 131 I (see Table I). Plan of Experiment 2 Eight mature female goats were dosed with 13 1!, monitored, and a month later surgically thyroidectomized. Six weeks after operation they were given a second dose ofl 31 I and again monitored. Finally, after a further five months they were given a third dose of 131 I, monitored and slaughtered (see Table II). Plan of Experiment 3 Sixteen male goats which had all been surgically thyra-parathyroidectomized I 2 to I4 months previously at ages between six and I 2 months, and six male
BRITISH VETERINARY JOURNAL, 123, 4
goats with intact thyroid and parathyroid glands, were given 131 1 and monitored. They were slaughtered two days later and their thyroids and any accessory thyroid tissues removed and analysed for 131 1. For I6 weeks before the administration of 131 1, six of these thyra-parathyroidectomized goats received 4 JLg. sodium L-thyroxinefkg. per day and six received 20 flg. /kg. per day (see T able III ). RESUL TS
Experiment I At necropsy three d ays after a single oral dose the concentration of 131 I in the thyroid glands, I ·03 per cent of the dose given/g. tissue, was approximately I ,ooo times that in any other tissue except for a small piece dissected from near the root of the tongue of one animal. This had a concentration of 0·43 per cent of the dose of 1 31Jfg. Histological examination proved this to be thyroid tissue similar in structure and colloid content to the main thyroid gland lobes of this goat. Table I shows the mean concentration of 131 1 in various organs and tissues three days after dosing. Only the thyroid glands concentrated 1311, so their uptake of this isotope appears to be a reliable diagnostic test for thyroid tissue. It is of interest that in vivo monitoring revealed no accessory thyroid tissue. Presumably that found at the time of necropsy near the root of the tongue was not d etected earlier because it was close to the main thyroid gland.
TABLE I THE
MEAN CONCENTRATION OF 131 1 I N TH E THYROID GLAND AND OTHE R T I SSUES OF THREE MALE GOATS THREE DAYS AFTE R DOSING
Tissue
Thyroid Tissue near root of tongue (one goat) Whole blood Blood plasma Skin Bone Voluntary muscle Fat Reticulum Omasum Duodenum Abomasum Bladder Heart Aorta
Mean
% dosefg.
131J
X Io•
1034 426 o·82 o·88 0'79 0' 19 0' 14 o·o5 o·84 o·69 1'1 3 1·8o 0'59 0'27 0'42
Tissue
Lung Diaphragm Kidney Liver Spleen Pa ncreas Trachea Thymus Adrenal Tongue Oesophagus Thyroid cartilage Parotid Pharynx Lymph node
Mean
% dose fg.
131/
X 103
o·68 0•26 0'75 o·61 0'55 0'37 1'0 1 0'45 0'36 1'36 1'34 0'51 0 '55 2'13 0'48
Experiment 2 Only one of the eight female goats (F4I I ) possessed an 131 1-concentrating region in addition to the main thyroid gland mass. It was situated at the base
TABLE II THE RES ULTS OF EXTERNAL MONITORING OF EIGHT GOATS WHICH HAD RECEIVED I 00 j.lC 131 I, BEFORE AND 6 WEEKS AND 6t MONTHS AFTER SURGICAL THYROIDECTOMY Before surgery Goat
F411 F4I1
Age when first dosed (years and months )
3"9
Maximum 131/ uptake (% dose)
44 4
-
F4II
F372 F372
3"8
F377 F377
3"8
Ws3 G4o G3I9 E202 G88
7"I I 3"0 2·8 4"9 2"I I
28
-
Site
Thyroid Base of neck -
Thyroid
-
Weigh (g. )
6 weeks after surgery Biological Maximum 131 / half-life uptake relative to days ) thyroid (%)
Site
0 0
6! months after surgery
Biological Maximum 131I half-life uptake relative to (days) thyroid (%)
Site
II > tr:l
Biological half-life (days )
IJJ IJJ
0
:::0
>< >-l
11 "5 ?
29 6
0 IO
-
-
IO
7"2
-
30 -
Thyroid Base of neck Rami of jaw
0 2 2
0 0 I
Thyroid Base of neck Rami of jaw
0 0 2
:r: ><
:::0
0...... 0
>-l ......
0 I
Thyroid Base of neck
0 5
0 0
Thyroid Base of neck
0 5
Thyroid Rami of jaw
0 2
0 0
Thyroid Rami of jaw
0 0
0 0 0 0 0
Thyroid Thyroid Thyroid Thyroid Thyroid
0 0 0 0 0
0 0 0 0 0
Thyroid Thyroid Thyroid Thyroid Thyroid
0 0 0 0 0
0 0
II ~
......
26
-
3I 23 39
44 37
Thyroid
Thyroid Thyroid Thyroid Thyroid Thyroid
8·5 -
I6·o I7•8 5"7 9"4 ll·8
2"2 -
2"2 2"0 5"3 5"3 29
II ~
II ~ O"l
(.;1
166
BRITISH VETERINARY JOURNAL, 123, 4
of the neck near the thoracic inlet and its 131 I-concentrating capacity was approximately ro per cent of that of the thyroid gland. Six weeks after thyroidectomy, when a second dose of 131 I was administered, the same accessory 131 I-concentrating area in goat F4I I could still be demonstrated. However, although it had approximately the same 1 31 I-concentrating ability, it did not retain the isotope for so long, i.e. it h ad a shorter biological half-life for 131 !. In addition another area of similar 131 I-concentrating capacity and biological half-life had appeared between the rami of the jaw. Two other animals in the group now also possessed 1 31 I-concentrating regions. In one (F372) this was situated towards the b ase of the n eck and had approximately I per cent of the 1 31 I -concentrating capacity of its original thyroid, and in the other (F377 ) a region at the back of its jaw had an 131 I -concentrating capacity of approximately 5 per cent of its thyroid gland. When a third dose of 131 I was administered five months later monitoring showed that only F4I I retained a site with 131 I-concentrating capacity. This was b etween the rami of its jaw, but the 131 I-concentrating capacity was only I per cent of that of its original thyroid gland. These findings are summarized in Table II. After death two small pieces of radioactive tissue were dissected from near the root of the tongue of F 4 I I. On histological examination these proved to be thyroid tissue.
Experiment 3 Table III shows 'that none of the six normal goats possessed accessory thyroid tissue, either on in vivo monitoring or at dissection after death. Three out of the four thyra-parathyroidectomized goats which had not received any supplementary thyroxine showed evidence, from monitoring and from post-mortem examination, of fragments of the original thyroid isthmus, presumably left at the time of surgery. One of these animals (J 326) also possessed a large nearly spherical lobe of thyroid tissue at the base of its neck, ventral to the trachea (Fig. I ) . The concentration of 131 I in this tissue was more than ten times greater than that in the thyroid glands of the normal goats. Five out of six goats which had received 4 f-lg. sodium L-thyroxinefkg. per day for the I6 weeks before administration of 131 I showed the presence of 131 Iconcentrating regions either at the site of the original thyroid or in other situations. Aft~r slaughter one goat (J 396) was found to possess three distinct masses of thyroid tissue spaced at equal intervals down the mid-line of the n eck from 5 em. to 6 em. below the position of the original thyroid gland to the thoracic inlet (Fig. 2). The concentration ofl 3 ll in these pieces of tissue and in those isolated from the other goats was again higher than that in the thyroid glands of the normal goats. Only one of the six goats receiving 20 p,g. sodium L-thyroxinefkg. per day showed the presence of accessory thyroid tissue by external monitoring. This animal possessed one piece of 131!-concentrating tissue at the site of the original thyroid and two small pieces in the region of the la rynx. All three tissues concentrated 13 1 I, but weakly compared with the thyroid glands of the normal goats. At necropsy four other goats in this group showed the presence of
ACCESSORY THYROID TISSUE I
THE GOAT
tissue resembling thyroid in the position of the original gland. Histological examination confirmed that these and all the other tissues described were thyroid gland. TABLE Ill 131 1
FOUND IN THE THYROID GLANDS AND ACCESSORY THYROID THE CONCENTRATION OF TISSUES OF 6 NORMAL GOATS AND I 6 THYRO-PARATHYROIDE CTOMIZED GOATS 48 HO URS AFTER ADMINISTRATION OF A SINGLE ORAL DOSE
Goat
Tissue
Thyroid Thyroid Thyroid Thyroid Thyroid Thyroid
Site NORMAL GOATS Thyroid Thyroid Thyroid Thyroid Thyroid Thyroid
THYRO-PARATHYROIDECTOMIZED GOATS At site of thyroid Residual thyroid isthmus Base of nec k (see fig. 1) Accessory thyroid Thyroid isthmus At si te of thyroid Thyroid isthmus At site of thyroid
131
1 Content (% dose fg. )
Weight (g. )
0'25 0'39 0'30 0'45 0'43 0•38
2'46 5'34 o·86 I·I8
I 3 '0 I 2·8 6·I 4'6 7'0 8·I
0'35 I'50 2•I 0'40
THYRO-PARATHYROIDECT6MIZED GOATS RECEIVING 4 j.!G. SODIUM L-THYROXINE/ KG. PER DAY Thyroid isthmus At site of thyroid o ·85 I '92 Accessory thyroid Near larynx 0'70 2'34 Accessory thyroid Near larynx 0'40 I '75 Thyroid isthmus At site of thyroid 2·6I 0'3I Accessory thyroid Near larynx 4'26 0'70 2•I Accessory thyroid In a chain lying in the 0'49 mid-line of the neck o·6 I'20 o·8I (see fig. 2 ) I' 30 Thyroid isthmus At site of thyroid 0'7 3'89 At site of thyroid Thyroid isthmus 5'80 0'4I Accessory thyroid Base of neck 7•88 0'4
J 328 J 328 ] 328
J I 77
ji84 ]I34 J 170
THYRO-PARATHYROIDECTOMIZED GOATS RECEIVING 20 j.!G . SODIUM L-THYROXINE/ KG. PER Thyroid isthmus Original thyroid o·I6 Accessory thyroid Near larynx o·2o Near larynx o·2o Accessory thyroid Thyroid isthmus Original thyroid Very low Thyroid isthmus Original thyroid Very low Thyroid isthmus Original thyroid Very low Thyroid isthmus Original thyroid Very low
DAY 0·38 o· I o·2 o· I 5 o·I o·2 o·2
DIS CUSSION
Accessory thyroid tissue was d etected either by in vivo monitoring or at necropsy in four of I7 normal adult goats. A remarkable property of this accessory tissu e was that it tended to regress and even disappear after thyroidectomy. This phenomenon occurred in three goats in which the accessory tissue detected either before or six weeks after operation disappeared completely or diminished substantially in 131 !-concentrating ability by six-and-a-half months after operation.
!68
BRITISH VETERINARY JOURNAL, 123, 4
This finding is difficult to explain. Thyroidectomy would be expected to increase the pituitary secretion of thyroid-stimulating hormone (TSH), which would in turn cause hypertrophy of any residual thyroid tissue. However, Wissig (I g64) suggested, on the basis of electron microscope examination of thyroid tissue, that there is a difference between the effects of mild and severe stimulation by TSH. During mild stimulation the Golgi apparatus appears to be more active in the formation of colloid droplets, whereas protracted severe stimulation disperses the Golgi apparatus and causes it to cease forming colloid droplets. Wissig suggests that the latter situation may be a manifestation of exhaustion resulting from over-activity and this may account for the atrophy of these glands in the present experiment. In contrast to the above findings in mature goats, residual and accessory thyroid tissue has been commonly found in goats thyra-parathyroidectomized between the ages of six and I 2 months. Of I 6 goats I 3 showed either residual thyroid tissue at the original site (I 2 animals) and/or quite distinct pieces of thyroid tissue at various other sites (five animals) I2 to I4 months after operation. Residual thyroid tissue in such a large number of animals is probably due to the fact that they were operated upon to remove parathyroid glands for another experiment and only sufficient thyroidectomy was carried out to ensure removal of the internal parathyroid glands. The 131 I-concentrating capacity of both the residual and accessory thyroid tissues in these animals was inversely related to the supplementary dose of sodium L-thyroxine which the animals had been receiving for the I 6 weeks before administration of 131I. Those receiving no sodium L-thyroxine or only 4 f.lg. Jkg. per day possessed hyperactive accessory thyroid tissues, while those receiving 20 f.lg. Jkg. per day had hypoactive thyroid tissues with respect to their 131 I-concentrating capacity in comparison with the thyroid glands of a group of normal controls. This may be accounted for by the direct inhibitory action of exogenous thyroid hormone on the secretion of TSH, and in this respect the accessory thyroid tissues behave like normal thyroid tissue. It seems· unlikely that in this group of animals which were operated upon while immature the absence of parathyroid glands would have had any influence on the presence or absence, or the hypertrophy or atrophy of the accessory thyroid tissues, subsequent to the operation. The accessory thyroid tissues of young animals are possibly less likely to atrophy on prolonged stimulation by TSH than those of adults. In view of the above results it appears that thyroidectomy of immature goats is followed by the retention or even the hypertrophy of residual or accessory thyroid tissue, whereas in adult goats the operation, although it may initially be incomplete, eventually results in complete thyroidectomy by the subsequent atrophy of any accessory thyroid tissue. The results of physiological experiments on "thyroidectomized" animals may be influenced by the above findings unless care is taken to ensure the removal of all thyroid tissue, or unless mature animals are used and an interval of at least six months is allowed to intervene between the date of operation and their use in experiments.
PLATE I
Fig.
1.
Accessory th yroid tissue a t base of neck of goat ] 326.
San om, B r. vet. ] ., I2J, 4
PLATE II
Fig . 2 . Th e po sit ion of the thr ee pieces of accessory thy roi d tiss ue lyi ng in the mi d-l ine of the nec k of go a t ] 396 .
Sa nso :n, Br. "'et. ]. , xz3, 4
ACCESSORY THYROID TISSUE IN THE GOAT
r6g
ACKNOWLEDGEMENTS
I thank Mr. R. J.
Colwil~
and Mr. M. Burrows for technical assistance. REFERENCES
EKMAN, L. ( 1965). Acta physiol. scand., 65, 331. ELLENBERGER, W. & BAuM, H. (I943). Handbuch der vergleichenden Anatomie der Haustiere, pp. 598-6oo. Berlin: Springer-Verlag. MARSTON, H. R. & PEIRCE, A. W. (I932). Aust. ]. exp. Bioi. med. Sci., 10, 203. PAYNE, ]. M. & CHAMINGS,j. (I964).]. Endocr., 29, I9. WISSIG, S. L. (I964). In The Thyroid Gland, Chapter 3, p . 52, ed. PITT-RIVERs, R. & TROTTER, W.R. London: Butterworths. (Accepted for publication 2 3rd January I 967)
La glande thyroide access oire chez Ia chevre (Sanso:rn) Resunte. Du tissu thyroide accessoire etait present a la base du col ou entre les branches montantes du maxillaire inferieur chez 4 sur I 7 chevres adultes normales. La thyroidectomie fut pratiquee sur trois d'entre ces quatre chevres et, apres six mois et demi le tissu accessoire avait disparu chez deux et le pouvoir de concentrer l'iode-I3I avait diminui considerablement chez la troisieme. Du tissu residue! ou accessoire etait present au site de Ia glande thyroide originaire ou en autres sites chez I3 sur I6 chevres I2-I4 mois apres thyro-parathyroidectomie a l'age impubere. Ober akzess orisches Schilddriisenge webe bei der Zi ege (Sanso:rn) Zusa:nunenfassung. Der Verfasser hat akzessorisches Schilddri.isengewebe bei vier von siebzehn gesunden erwachsenen Ziegen entweder vor dem Brusteingang oder im Kehlgang gefunden. Bei drei dieser vier Ziegen wurde die Schilddri.ise entfernt. Nach 6! Mona ten konnte 13 eine schwere Abnahme des 11-Konzentrationsvermogens und in zwei Fallen das Verschwinden des akzessorischen Gewebes festgestellt werden. Zwolfbis vierzehn Monate nach Entfernung der Schild- und Nebenschilddri.isen bei sechzehn unreifen Ziegen wurde bei dreizehn Tieren zuriickgebliebenes oder akzessorisches Schilddri.isengewebe an der ehemaligen Stelle der Schilddri.ise oder an anderen Stellen gefunden. La glandula tiroides acces orio en Ia cabra (Sans om) Resunten. Tejido accesorio era presente al nivel de la base del cuello o entre las ramas de Ia mandibula en 4 sobre I 7 cabras adultas normales. La tiroidectomia fue practicada sobre tres de estas cuatro cabras y seis meses y medio mas tarde en dos de elias el tejido accesorio haboa desaparecido y en Ia tercera el poder de concentrar el yodo- I 3 I habia disrninuido considerablemente. Tejido residual o accesorio era presente en el sitio de la glandula tiroides original o en otros sitios en 13 de I6 cabras I2-I4 meses despues de Ia tiro-paratiroidectornia en edad impubera.