To identify the thyroid histological and hormonal changes in response to ambient temperature variations, thyroid glands and blood samples were randomly collected from 800 indigenous corss-breed cattle of both sex and different age groups from municipal Tabriz slaughter house. The extent of fluctuations in triiodothyronine (T3), thyroxin (T4), T3 uptake and thyroid histopathological lesions were scrutinized in 2 months in year 2007, viz., February (the coldest month) and August (the hottest month). A marked decline was discernable in T3, T4 and T3 uptake in August compared to February. Out of 800 pairs of thyroid glands, 120 (15%) had lesions in which histopathological changes were categorized as follicular atrophy (2.5%), Paranchymal cyst (1.38%), colloid goiter (3.39%), follicular cell hyperplasia (0.27%), thyroid fibrosis(0.635%), focal hyperplastic goiter (0.88%), diffuse hyperplastic goiter additional paranchymal cyst (0.63%). Mean of thyroidal parameters for T4, T3 and T3 uptake was lower in lesioned group (p<0.01). The frequency of lesioned thyroid was higher in summer than winter (p<0.001). The result of this study showed that high ambient temperature has profound effect on thyroid function, secretion and pathological changes in cattle.
PDF Abstract XML References Citation
How to cite this article
Thyroid function of domestic animals is known to be altered by many environmental factors including environmental factors. Special attention has been given to the effect of ambient temperature (Hoersch et al., 1961; Thompson et al., 1963; Valtorta et al., 1982; Prawl et al., 1998; Webster et al., 1991; Starling et al., 2005) and feed intake (Yousef and Johnson, 1960; Singh et al., 1971; Pereira et al., 2008) on thyroid activity. The effects of exposure to high environmental temperature on blood thyroid hormone concentration in ruminants have been the subjects of numerous review articles. It has been shown that exposure to high environmental temperatures depresses thyroid activity whereas exposure to cool environments increase thyroid activity (Yousef and Johnson, 1960; Thompson, 1973; Johnson and Vanjonak, 1976; Young, 1981; Pratt and Wettemann, 1986; Hocquette, 1992; Doubek et al., 2003). In another study in cattle, a decreased feed intake caused by exposure to a high environmental temperature correlated with decrease in T4 (Yousef and Jhonson, 1960). In experiments carried out on sheep, it was shown that blood thyroid hormone (T4) concentration decreased gradually between the 40th and 80th day of exposure to 32 °C (Sanchez and Evans, 1972).
In researchers study in cattle, it has been found that a decreased feed intake caused by exposure to a high environmental temperature is correlated with a decrease in T4 (Yousef and Johnson, 1960). It has been reported that increase in ambient temperature depresses feed intake in sheep and results in decrease in plasma T4 concentration, but temperature per se appears to provide an additional depression in the reduction of plasma T4 levels (Valtorta et al., 1982). Recent study in a very hot place in the south of Iran revealed the existence of high percentage of histopathological changes in the thyroid glands of sheep in that area (Nouri et al., 2006). We have also recently noticed that ovine fetuses in summer have significantly histologic changes in their thyroids in comparison with the fetuses in winter months (unpublished data). The present study was undertaken to determine the relationship between ambient temperature and histological and hormonal changes in the thyroid glands of cows in an area in the north east of Iran with a low ambient temperature in winter and mild temperature in summer.
MATERIALS AND METHODS
The research was carried out in Tabriz, capital of East Azarbaijan province, a city in East of Iran, 600 km to Tehran, the capital, with very low temperature in winter and a mild climate in summer and its temperature in winter reaches -10 °C and some days even low than -15 °C.
In this study blood samples and thyroid glands were collected randomly from 800 cows slaughtered at Tabriz Municipal Abattoir. The cows in the area were kept indoors throughout year. The age of the animals ranged from below 8 months to above 60 months. The entire period of study was classified into two months in year 2007 with very different temperatures; February with minimum and maximum temperatures below 15 and above 1 °C, respectively and relative humidity 76% and August with minimum and maximum temperatures 22 and 34 °C, respectively and relative humidity 60% were the months we collected our samples. In each month 400 blood and thyroid samples were collected. After collection, the blood samples were allowed to stand for 20-30 minutes and then they were centrifuged at 2000 to 3000 rpm. The serum was separated and stored at -22 °C till assayed. Serum T3, T4 and T3 uptake were determined by the standard ELISA method according to the protocol described in the commercial kits of Pishtazteb Inc, Tehran, Iran.
After macroscopical examination, all thyroid glands were fixed 10% formaldehyde for 24-48 h, dehydrated in an ethyl alcohol series (70, 80, 90, 100, 100-I, 100-II%) and embedded in paraffin wax. Sections were cut and stained with Hematoxylin and Eosin, periodic Acid Schiff-Hematoxylin by Gallegos method (McManus and Mowry, 1968).
Quantitative data were analysed by one way ANOVA followed by Post Hoc Tukey methods and levels below 5% were considered statistically significant.
Analysis on blood samples showed significant differences of total T3, T4 and T3 uptake between February and August (Table 1). Total T3, T4 and T3 uptake decreased in August compared to February (p<0.01).
Among 800 thyroid glands divided equally in two groups of 400, 120 revealed some pathological changes under light microscopy which equals 15% of all samples (Table 2). Among all pathological changes, 34.16 and 65.84% were in February and August, respectively; In other words, 5.065% of thyroid samples in February and 9.935% of samples in August had some pathological changes, which was significantly different (p<0.01). Furthermore in Table 3, the incidences of specific types of pathological changes are demonstrated.
|Table 1:||Thyroidal indices in cow slaughtered in Tabriz abattoir|
On the other hand, evaluation of the effect of these pathological lesions on thyroid function showed significant decrease in thyroid function in the presence of pathology (Table 4). For more information, each pathologic lesion is shown in brief in Fig. 1.
|Table 2:||Number and incidence of pathological lesions in cow in February and August|
|Table 3:||Incidence of pathological lesions in thyroid glands in February and August|
|Table 4:||Thyroidal indices based on the presence of pathological lesions|
|Fig. 1:||Light microscopy sections demonstrate wide variety of pathological changes in thyroid glands: Follicular atrophy showing small follicles contained small quantity of colloid (a), Paranchymal cysts where some are too distended and ruptured (b), colloid goiter with large follicles contained eosinophilic colloid (c), Para follicular cell hyperplasia seen in some follicles (d), Thyroid fibrosis with fibrous connective tissue (e), thyroid necrosis (f), multi nodular goiter (g), hyperplastic goiter (h). (H and E, Ax66; Bx66; Cx660; Dx66; Ex66; Fx660; Gx66; Hx1650)|
It is well known that among environmental factors, two factors more importantly affect the blood level of thyroid hormones: Ambient temperature and feed intake (Grossie and Turner, 1962; Sutherland and Irvine, 1974; Evans and Ingram, 1977; Webster et al., 1991; Todini, 2007). High temperature and decreased feed intake have been shown to decline thyroid hormone via various mechanisms (Portnay et al., 1974; Panda and Turner, 1967; Szabo and Frohman, 1977; Hefco et al., 1975; Vagenakis et al., 1977; Suda et al., 1978). Notably, it has been proposed that temperature plays a dual role in between: Its direct effect on TRH and subsequently plasma T4 (Valtorta et al., 1982) and indirect effect on decreasing appetite which on its own can decrease thyroid hormone blood level. T3 directly stimulates feed intake at the hypothalamic level (Kong et al., 2004) while on the other hand, the quantity and quality of food eaten is a major factor determining plasma concentrations of TH (Dauncey, 1990). So, whether high temperature independently suppresses thyroid hormone may raise controversy. To shed some light on it, Yousef and Johnson (1960) proclaimed that even the force-fed cattle showed a significant decrease in thyroid activity when subjected to the heat treatment. For reconfirmation, Valtorta et al. (1982) ran a study contained a heat- stressed group compared with control and feed-restricted groups which showed temperature effect was additional to the feed effect and the heat-stressed group displayed a significantly greater decline in plasma T4. Based on these studies, we come to the point that although feed restriction has a great impact on plasma levels of thyroid hormone, we can not ignore the dramatic independent effect of ambient temperature. One aim in this study was to compare the effect of temperature, a hot month versus a cold month, on the thyroid hormones and as it could be prognosticated, our experience revealed significant decreased blood levels of T4, T3 and T3 uptake in August compared to February (Table 1). Since the animals were fed ad libitum, it is not claimed that the intake effect as a confounding factor has been eliminated, but according to the evidence given above, it could be concluded that differences observed in our study, were mostly due to the high temperature effect not decreased food intake.
More interestingly, not mentioned previously in literatures, samples collected in August were affected more frequently than those obtained in February (Table 2), which is in line with the findings of Nouri et al. (2006), who showed a high range of thyroids pathological changes in sheep in August in comparison with February. A wide spectrum of pathological changes were observed in these lesions depicted in Table 3 among which colloid goiter and diffuse hyperplastic goiter, which compose 7.75% of all lesions, worth being more addressed. These pathologic changes can be attributed to the increased TSH level in August, which may lead to pathologic lesions, due to decreased T4 and T3 level (Thomson, 1988).
Last thing which attracted our attention was the high incidence of pathologic changes in thyroid glands in both seasons and the low levels of T3, T4 secretion and T3 uptake in lesioned thyroid in comparison to other reports around the world (Sutherland and Irvine, 1974; Valtorta et al., 1982; Guerrini and Bertchinger, 1983; Mixner et al., 1962).
The results of this research revealed that thyroid lesions are very high among cattle in the area and deeply affect the function of the gland. The consequences of this malfunction have not been evaluated yet and a case control study to estimate the related economical losses is recommended.
- Suda, A.K., C.S. Pittman, T. Shimizu and J.B. Chambers, 1978. The production and metabolism of 3,5,3-triiodothyronine and 3,3',5'-triiodothyronine in normal and fasting subjects. J. Clin. Endocrinol. Metab., 47: 1311-1319.
- Johnson, H.D. and W.J. Vanjonack, 1976. Effects of environmental and other stressors on blood hormone patterns in lactating animals. J. Dairy Sci., 59: 1603-1617.
- Evans, S.E. and D.L. Ingram, 1977. The effect of ambient temperature upon the secretion of thyroxine in the young pig. J. Physiol., 264: 511-521.
- Sutherland, R.L. and C.H.G. Irvine, 1974. Effect of season and pregnancy on total plasma thyroxine concentration in sheep. Am. J. Vet. Res., 35: 311-312.
- Szabo, M. and L.A. Frohman, 1977. Suppression of cold-stimulated thyrotropin secretion by antiserum to thyrotropin-releasing hormone. Endocrinology, 101: 1023-1033.
- Grossie, J. and C.W. Turner, 1962. Thyroxine secretion rates during food deprivation in rats. Proc. Soc. Exp. Boil. Med., 110: 631-633.
- Mixner, J.P., D.H. Kramer and K.T. Szabo, 1962. Effects of breed, stage of lactation, and season of year on thyroid secretion rate of dairy cows as determined by the chemical thyroxin turnover method. J. Dairy Sci., 45: 999-1002.
- Guerrini, V.H. and H. Bertchinger, 1983. Effect of exposure to a hot-humid and a hot-dry environment on thyroid hormone values in sheep. Br. Vet. J., 139: 119-128.
- Nouri, M., K.H. Mirzadeh and B. Mohamadian, 2006. The effect of ambient temperature on thyroid hormones concentration and histopathological changes of thyroid gland in sheep. Pak. J. Biol. Sci., 9: 2308-2312.
- Thompson, R.D., J.E. Johnston, C.P. Breidenstein, M.R. Baberjee and W.T. Burnett, 1963. Effect of hot conditions on adrenal-cortical, thyroidal and other metabolic responses of dairy heifers. J. Dairy Sci., 46: 227-231.
- Hefco, E., L. Krulich, P. Illner and P.R. Larsen, 1975. Effect of acute exposure to cold on the activity of the hypothalamic-pituitary-thyroid system. Endocrinology, 97: 1185-1195.
- Panda, J.N. and C.W. Turner, 1967. Effect of thyroidectomy and low environmental temperature (4.4 ) upon plasma and pituitary thyrotrophin in the rat. Acta Endocrinol., 54: 485-493.
- Hoersch, T.M., E.P. Reineke and H.A. Henneman, 1961. Effect of artificial light and ambient temperature on the thyroid secretion rate and other metabolic measures in sheep. J. Anim. Sci., 20: 358-362.
- Vagenakis, A.G., G.I. Portany and J.T. O'Brian, 1977. Effect of starvation on the production and metabolism of thyroxine and triiodothyronine in euthyroid obese patients. J. Clin. Endocrinol. Metab., 45: 1305-1309.
- Portnay, G.I., J.T. O'Brian and J. Bush, 1974. The effect of starvation on the concentration and binding of thyroxine and triiodothyronine in serum and on the response to TRH. J. Clin. Endocrinol. Metab., 39: 191-194.
- Valtorta, S., L. Hahn and H.D. Johnson, 1982. Effect of high ambient temperature (35) and feed intake on plasma T4 levels in sheep. Proc. Soc. Exp. Biol. Med., 169: 260-265.
- Pratt, B.R. and R.P. Wettermann, 1986. The effect of environmental temperature on concentrations of thyroxine and triidothyronine after thyrotropin relasing hormone in steers. J. Anim. Sci., 62: 1346-1352.
- Young, B.A., 1981. Cold stress as it affects animal production. Am. Soc. Anim. Sci., 54: 154-163.
- Yousef, M.K. and H.D. Johnson, 1960. Blood thyroxine degradation rate of cattle as influenced by temperature and feed intake. Life Sci., 5: 1349-1349.
- Pereira, A.M.F., F. Baccari Junior, E.A.L. Titto and J.A.A. Almeida, 2008. Effect of thermal stress on physiological parameters, feed intake and plasma thyroid hormones concentration in Alentejana, Mertolenga, Frisian and Limousine cattle breeds. Int. J. Biochem., 52: 199-208.
- Silanikove, N., 2000. Effects of heat stress on the welfare of extensively managed domestic ruminants. Livestock Prod. Sci., 67: 1-18.
- Starling, J.M.C., R.G. Da Sila, J.A. Negrao, A.S.C. Maia and A.R. Bueno, 2005. Seasonal variation of thyroid hormones and cortisol of sheep in tropical environment. Rivista Brasileira de Zootecnia, 34: 2064-2073.
- Todini, L., 2007. Thyroid hormones in small ruminants: Effects of endogenous, environmental and nutritional factors. Animal, 1: 997-1008.
- Webster, J.R., S.M. Moenter, C.J.I. Woodfill and F.J. Karsh, 1991. Role of the thyroid gland in seasonal reproduction. II. Thyroxin allows a season-specific-suppresssion of gonadotropin secretion in sheep. Endocrinology, 129: 176-183.
- Dauncey, M.J., 1990. Thyroid hormones and thermogenesis. Proc. Nutr. Soc., 49: 203-215.
- Doubek, J., S. Slosarkova, P. Fleischer, G. Mala and M. Skrivanek, 2003. Metabolic and hormonal profiles of potentiated cold stress in lambs during early postnatal period. Czech J. Anim. Sci., 48: 403-411.
- Sanchez, O. and J.W. Evans, 1972. Isotope studies on the physiology of domestic animals. Proceedings of the International Atomic Energy Agency, Molecular Nutrition and Food Research, Volume 309, (IAEA'72), Vienna, pp: 473-474.
- Singh, D.V., R.R. Anderson and C.W. Turner, 1971. Effect of decreased dietary protein on the rate of thyroid hormone secretion and food consumption of rats. J. Endocrinol., 50: 445-450.