Postnatal changes in circulating concentrations of growth hormone, somatomedin C and thyroid hormones in pigs

DOMESTIC ANIMAL ENDOCRINOLOGY

Vol. 4(4):253-257, 1987

POSTNATAL CHANGES IN CIRCULATING CONCENTRATIONS OF GROWTH HORMONE, SOMATOMEDIN C AND THYROID HORMONES IN PIGS 1 Colin G. Scanes, Douglas Lazarus, Samuel Bowen, Frances C. Buonomo* and Rex L. Gilbreath Department of Animal Sciences, Rutgers - The State University New Brunswick, NJ 08903 *Monsanto Company, Chesterfield, MO 63038 Received April 3, 1987

ABSTRACT Plasma concentrations of growth hormone (GI-I), somatomedin (SmC), thyroxine (T~) and triiodothyronine (T3) were determined from birth to post weaning in pigs (Yorkshires). Plasma samples were obtained from the smallest, median and largest piglet from 11 litters. No differences in the circulating concentrations of any of the hormones were observed between piglets of different sizes. However, there were changes in circulating concentrations of hormones during postnatal development. Plasma concentrations of GH decreased between 2 and 8 to 10 days of age. A progressive increase in the circulating concentrations of SmC was observed with concentrations rising (3.83fold between 2 days and 40 days of age). Plasma concentrations of T~ and T3 were maximal at 23 and 16 days of age, respectively. INTRODUCTION Animal growth and metabolism are affected by a spectrum of homeostatic and homeorhetic hormones (1-4). Growth hormone (GH) appears to be the principal pituitary hormone affecting growth. In pigs, post-natal growth requires the presence of the pituitary gland (5). Not only does GH stimulate growth in hypophysectomized pigs (6,7) but also in intact pigs (8,9). It is likely that GH exerts its effect on growth by stimulating somatomedin production. Indeed circulating somatomedin C (SmC) concentrations were elevated in pigs receiving injections of GH (8). The present communication describes changes in circulating concentrations of GI-I and SmC together with the thyroid hormones (thyroxine, T4 and triiodothyronine, T3) in piglets during postnatal growth until weaning. There is already information on circulating concentrations of GI-I in fetal pigs (10) and during postnatal growth (10-12). However, the period between birth and weaning has not been considered in detail. Furthermore, there are no studies on changes in circulating concentrations of SmC, T4 and T 3 during early postnatal growth in pigs. A second objective of the present study was to compare circulating concentrations of GH, SmC, T4 and T 3 in the smallest, median and largest male piglets of 11 litters during preweaning growth. Previously, differences in circulating concentrations of GH have been observed in genetic lines of pigs with varying quantities of adipose tissue (12,13). It should be noted however, that there are few studies in farm animals where circulating concentrations of GH or other growth promoting hormones are correlated to growth.

Copyright© 1987by DOMENDO, INC.

253

0739-7240/87/$3.00

254

SCANES, LAZARUS, BOWEN, BUONOMO AND GILBREATH MATERIALS AND METHODS

A n i m a l E x p e r i m e n t s . The plasma concentrations of hormones, body weight and length were determined during postnatal growth in pre-weaning piglets. Three piglets from each of 11 litters were used in the study. The piglets, were, respectively the heaviest, median and lightest male member of the litter at 2 days of age. If one of these three piglets died, no further blood samples were taken from any piglet in that litter, and a replacement group of three piglets was sampled. Blood samples were taken by heart puncture at approximately weekly intervals from piglets beginning at 2 days of age. Plasma was stored at --20C prior to assay after centrifugation of the heparinized blood. At the time of blood sampling, two indices of growth were determined; these being weight and length (the distance from the external occipital proturberance to the caudal portion of the sacrum) using a flexible metric tape measure. Pigs. Batch-farrowing was employed in the present study. Gestating sows (Yorkshires) were placed in farrowing crates on day 110 of pregnancy to allow the sow to be c om e accustomed to the environment. Piglets were separated from the dams at birth and were segregated under heat lamps until farrowing was complete. At this time, piglets were permitted to nurse and remained with sows. At birth, the navels of the piglets were clipped and treated with iodine. On day 1 post-farrowing, piglets were weighed, ear notched for identification and the needle teeth were clipped. Piglets were maintained with heat lamps available and free access to the sows. The sows had free access to water and were fed twice daily with a standard corn-soy diet (15% crude protein and fortified to NRC recom m ended levels of minerals and vitamins). The piglets received an i m iron dextran injection at 5 days of age, and at 21 days a pre-starter diet was made available. Piglets remained with the dams until 35 days old when weaning occurred. Male piglets used in the study were not castrated to exclude confounding effects of stress. H o r m o n e Assays. Plasma concentrations of GH were determined by heterologous radioimmunoassay previously validated for porcine plasma (14). Circulating concentrations of somatomedin C were estimated by a heterologous radioimmunoassay (15,16), which has previously been validated for pig plasma samples (17) [sensitivity 0.79 ng/ml; interassay variance 9.8%; intrassay variance 3.0%]. In order to dissociate somatomedin C from binding protein, plasma samples were incubated for 24 hr at 37C with 1 M glycine-glycine HCI (pH 3.5) (16). The antiserum to somatomedin C was obtained from the National Pituitary Agency while radiolabelled somatomedin C was provided by Dr. Underwood (Chapel Hill, North Carolina) [sensitivity 0.16 ng/ml (0.78 mU/ ml) interassay variance 9.2%, intrassay variance 5.4%]. The standard was obtained from the Nichols Institute. The thyroid hormones were similarly assayed by radioimmunoassays using antibodies obtained by Antibodies Incorporated (Davis, California) IT3 assay: -- sensitivity 0.17 ng/ml, interassay variance 5.0%, intrassay variance 2.3%; T4 assay: -- sensitivity 0.32 ng/ml, interassay variance 4.4%, intrassay variance 2.9%]. S tatis tical Analysis. Statistical analyses were performed using the general linear model of the Statistical Analysis System. Means were separated using Duncan's multiple range test.

PORCINE

GH AND SmC

255 RESULTS

AND

DISCUSSION

The circulating concentrations of hormones, body weight and back length of male piglets during pre-weaning growth is shown in Table 1. Piglets have been placed in three groups on the basis of being the heaviest, median or lightest of the litter at 1 day. On this basis, it is not surprising that at 2 days of age, the heavy group had significantly (P<.05) higher body weights than those of the median group which in turn were heavier (P<.O5) than the light group. These weight differences were maintained at 8 to 10 days. Thereafter the median and heavy groups did not differ from each other but continued to be heavier than the group of piglets which were selected on the basis of being lightest at day 1. Data on piglet length were completely consistent with those on body weight. For instance, those piglets which were heaviest at day 1 were also longest (at day 2 and day 8 to 10), while those which were lightest at day 1 were shortest. This difference between length of the heavy and light groups was maintained throughout the study. The present data on the continuation of weight difference from birth to weaning is similar to that reported previously. Powell and Aberle (1980) observed that low birth weight pigs grew slower to 90 kg live weight than either high or median birth weight pigs. It should be noted that the piglets in the light group (Table 1) weighed 51% (range 38.5 to 63.0%) that of the heaviest piglets in the litter. On this basis, all the piglets in the light group might be classified as runts; runts weighing less than 65% of the heaviest litter mate (18). Similarly, the low birth weight piglets in the study of Powell and Aberle (19) were considered runts. It is possible that the reduced prenatal growth in runt piglets is either carried forward posmatally, or reflects a metabolic disfunction that influences both pre- and postnatal growth. In the present study no differences in the

TABLE 1. EFFECT OF BZRTH WEIGHT ON SUBSEQUENT GROWTH AND CIRCULATING CONCENTRATIONS OF GROWTH-RELATED HORMONES ( G R O W ~ HORMONE, SOMATOMEDIN C, T4 AND T3) IN MALE PIGLETS.

,~e, dap Class

2

8-10

15-17

22.24

29.31

36-40

B0dyWeigbt (ke)o~ Heavy Middle Light

1. 7 ± 1. 3 ± O. 9 ±

.05(7)b .05(7) c .05(8) d

3. 2 ± 2. 6 ± 1. 7 ±

Heavy

26. 2 ± 24. 3 ± 21.6 ±

. 5(7) b

30. 8 ±

4(7) ~ . 8(8) d

Middle Light

Growth Hormt~(ngml)(.) Heavy 1.98 ± .39(7) b Middle Light

2.43 ± .47(7) b 5.12 ± 1.60(3)b

SomaomedioC~/ml).~ HoW

2.90 ± 1.02(6)b

Middle Light

5. 1 ± !.39(6) ~ 10. 3 ± 4.18(6) ~

TbpoxJ~('l"4 (nedml)(') Heavy 52. 8 ± Middle 42. 3 ± Light 45.4 ± Tfii0d0thF0nine (T0 Heavy 3. 0 ± Middle 2. 6 ±

Light

2. 2 ±

b'c~a(a) M e a n

6. 3(7) b 14. 4(7)b 8. 6(7) b (ng/ml)O) . 4(7) b 4(7) b

. 2(7)~

1(8)b 1(10)" 2(8) d

4. 8 ± 4. 5 ± 2. 5 ±

1(8)b 2(6) b 4(7) c

28. 1 ±

8(8)b 36. 3 ± 8(10)~ 36. 0 ±

25. 3 ±

9(8) d

28. 6 ±

9(8) b 9(6) b 1(7)c

0.89 ± 1.61 ± 2.22 ±

.28(5)b .73(5) b .86(7) b

0.96 ± 0.98 ± 1.20±

.48(4)b .01(2)b .31(6)b

6.8± 5.9± 4.2±

.4(8) b .5(7) b .5(6) ~

40.4~ .9(8) b 37. 7 ± 1. 1(7) b 34. 2 2 2. 8(6) ~ 1.37 ± 0.96 ± 0.72 ±

9.5± 8.0± 5.6±

.5(5) b .3(8) ~ 5(6) d

4 5 . 7 ± 1.7(5) b 44. 5 ± 1. 1(8)b 39. 3± 1. 1(6)'

.60(5)b .12(5)b .21(5)b

1.04 ± .14(4)b~ 0.78 ± .16(7) b 1.21 ± .30(4)'

11.3± 9.8± 7.5±

. 5(8) b 6(7) b 1.2(4) c

4 8 . 9 ± 1. 2(8) b 46. I ± 1. 4(7) b 43.8± 3. 2(4) b 0.90 ± 0.81 ± 0.97 ±

.17(6)b .15(5)' .12(4) b

10. 8 ± 2.21(7) b 7. 0 ± 1.84(7)b 10. 1 ± 2.51(7) b

11. 1 ± 3.06(7) b 11. 4 ± 4.18(5) b 10. 2 ± 2.51(6) b

17. 8 ± 2.41(8) b 10. 9 ~ 2.41(5) b 16. 2 ± 5.10(6) b

16. 6 ± 5.00(4) b 21. 4 ± 4.25(7) b 16. 6 ± 5.27(5) b

26. 0 ± 5.00(8) b 24. 8 ± 4.90(7) b 12. 5 ± 4.08(3) b

43.7± 40.4± 39.7±

3.6(8) b 4.4(10) b 6.4(8) b

45.7± 49.6± 38.9±

4.7(8) b 3. 2(6) b 5. 1(6)b

58. 2± 6. 4(6) b 3 6 . 7 ± 5.9(5) b 55.4±10.0(5) b

52.0± 48.6± 52.9±

5.0(4) b 4. 5(7) b 6.5(4) b

47.0± 37.8± 33.9±

4.9(7) ~ 6. 0(7) ~ 7. 7(3) b

3.4± 2.8± 2. 7 ±

.4(8) b .3(10) b . 7(8) b

3.9± 4. 1± 3. 5 ±

,6(8) b 4(6) b 6(7) b

3.3± 2.6± 2. 5 ±

.7(5) b .5(8) b . 7(5) b

1,6± 1.4± 1. 2±

.2(8) b .7(7) b 4(4) b

_+ S.E.M. ( N = )

Means within

3.5± 3.0± 3. 4 ±

.4(8) b .4(7) b . 6(6) b

each age with different superscripts

differ (P<.O5).

256

SCANES, LAZARUS, BOWEN, BUONOMO AND GILBREATH

TABLE 2. PLASMACONCENTRATIONSMF.AN _+ SE OF GROWTH HORMONE (GH) SOMATOMEDIN C (SMC), THYROXINE (T4) AND TRIIODOTHYRONINE(T~) DURING POSTNATALGROW*I~ IN PIGS. Age, d 2 8-10 15-17 22-24 29-31 36-40

GH, n g / m l 2.7 1.6 1.2 1.0 0.9 0.9

-+ _+ + _+ -+ -+

.4(17) b .4(17) c .2(12) c .2(14) c .1(15)" .1(14)"

SmC, U / m l 6.1 9.3 11.9 15.6 18.4 23.3

_+ +_+ _+ _+ -+

1.46(21) 1.22(21) 1.80(18) 2.11(18) 2.65(16) 3.13(18)

T4, n g / m l b ~ c ca dc c

46.8 41.2 44.8 56.9 50.7 40.9

_+ _+ _+ _+ _+ _+

3.8(21) 2.72(6) 2.7(20) 4.1(16) 2.8(15) 3.6(17)

T~, n g / m l ~ b ~ d bd ~

2.6 3.0 3.8 3.3 2.8 1.4

± -+ ± -+ _+ _+

2(21) b .3(26) b .3(21)" .3(21) b' .3(18) h .1(19) a

b,c,d Means that have different superscripts differ ( P < . 0 5 ) . * N u m b e r s in parenthesis represent n u m b e r of animals.

circulating c o n c e n t r a t i o n s of GH, s o m a t o m e d i n C, T4 or T3, w e r e observed b e t w e e n the different birth w e i g h t piglets at any o f the ages examined. Thus it w o u l d a p p e a r that runt piglets do not differ from normal littermates in terms of circulating c o n c e n t r a t i o n s of these hormones. This provides e v i d e n c e for the lack of i n v o l v e m e n t of GH, s o m a t o m e d i n C, T4 or T 3 in the r e d u c e d growth in runts. Table 2 summarizes data on changes in circulating c o n c e n t r a t i o n s of h o r m o n e s during postnatal pre-weaning growth in piglets. Plasma concentrations of GH decreased b e t w e e n 2 and 8 to 10 days of age in piglets but thereafter remained relatively constant. Plasma concentrations of GH have previously b e e n f o u n d to be very high in the fetus (10) and low and further declining in post-weaning growing pigs ( 1 0 , 1 1 ) . It w o u l d t h e r e f o r e a p p e a r that in pigs, plasma concentrations of GH are high in the fetus, decline rapidly perinatally and then gradually decrease. These changes may reflect maturation of the hypothalamopituitary axis. Plasma c o n c e n t r a t i o n s of s o m a t o m e d i n C rose steadily t h r o u g h pre-weaning growth; the level at 36-40 days being 3.83-fold that observed at 2 days. The plasma c o n c e n t r a t i o n s of s o m a t o m e d i n C observed at the end of the present study are s o m e w h a t l o w e r than those r e p o r t e d in older pigs (8). Thus plasma c o n c e n t r a t i o n s o f s o m a t o m e d i n C p r o b a b l y c o n t i n u e to rise during growth. This pattern of increasing circulating concentrations of s o m a t o m e d i n C during post-natal growth is similar to that observed in o t h e r species (e.g., human 15, rats 20, chickens 21). It is interesting to note that plasma concentrations of s o m a t o m e d i n C are increasing w h i l e those of GH are decreasing. In view of the d e m o n s t r a t i o n that GH can elevate circulating s o m a t o m e d i n C concentrations in pigs (8), it is likely that this age-related increase in s o m a t o m e d i n C c o n c e n t r a t i o n s reflects increasing sensitivity to GH or perhaps to greater quantities of s o m a t o m e d i n - p r o d u c i n g tissues. Plasma c o n c e n t r a t i o n s of b o t h T4 and T 3 rose posmatally and t h e n decreased. There is no ready e x p l a n a t i o n for these changes. It is possible that both the rise and fall reflect o n t o g e n y and maturation of the hyhpothalamo-pituitarythyroid axis. Alternatively the post-natal increase in circulating concentrations of T4 and T 3 may reflect r e q u i r e m e n t s for t e m p e r a t u r e maintenance. The decrease in plasma c o n c e n t r a t i o n s of T4 and T 3 may be related to diet, with thryoid h o r m o n e s e c r e t i o n being r e d u c e d following solid food being made available and f u r t h e r r e d u c e d following weaning. ACKNOWLEDGEMENTS Paper of the Journal Series, New Jersey Agricultural Experiment Station; Supported by State and Hatch Act Funds (Project 19140).

PORCINE GH AND SmC

257 REFERENCES

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