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ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION |
Department of Animal Science, Cornell University, Ithaca, NY 14853-4801
Abstract
This study investigated effects of birth weight and postnatal nutrition on organ growth in neonatal lambs. Suffolk x (Finnsheep x Dorset) low- (mean ± SD 2.29 ± 0.34 kg, n = 28) and high- (4.84 ± 0.45 kg, n = 20) birth-weight male lambs were studied. Lambs within each birth weight category were allocated to be individually grown rapidly (ad libitum fed, ADG 337 g, n = 20) or slowly (ADG 150 g, n = 20) on a liquid diet to live weights up to approximately 20 kg. All organs weighed less at birth in small than in large newborns (P < 0.001), except the adrenals (P = 0.10). At birth, as a percentage of empty body weight (EBW), small newborns had larger testes (0.14 vs. 0.10%, P = 0.023) and smaller thymus (0.17 vs. 0.37%, P = 0.009), and tended to have a larger heart (0.85 vs. 0.75%, P = 0.060) and a smaller spleen (0.10 vs. 0.14%, P = 0.054) than large newborns. During the first 2 to 3 wk postpartum, small newborns had greater fractional growth rates of organs than large newborns, most notably spleen, thymus, and liver. Postnatal growth of organs was more closely associated with EBW than age, except for lungs, testes, and stomach. At completion of rearing to 20 kg of live weight, small newborns had a spleen approximately 30% heavier than large newborns (P < 0.001). Testes weights were 37% and 24% greater in small newborns reared slowly and rapidly, respectively, compared with their high-birth-weight counterparts (P = 0.034). It was also evident that postnatal nutrition altered the mass of individual organs at the conclusion of the rearing period without affecting the combined weight of dissected organs. Slowly reared lambs had a larger pancreas (+27%, P = 0.002), stomach complex (+83%, P < 0.001), large intestine (+39%, P < 0.001), entire gastrointestinal tract (+18%, P = 0.002), and testes (+54%, P = 0.016) and tended to have a larger heart (+6%, P = 0.068) than their rapidly reared counterparts at 20 kg of live weight. Rapidly reared lambs had a larger thymus (+61%, P = 0.003), liver (+34%, P < 0.001), kidneys (+33%, P < 0.001), and small intestine (+17%, P < 0.001) and tended to have a larger thyroid (+13%, P = 0.054) at 20 kg of live weight than slowly reared lambs. The functional significance of the smaller thymus at birth and increase in spleen and testes weights at 20 kg of live weight in low- compared with high-birth-weight lambs warrants further investigation. It also remains to be established whether these differences at 20 kg of live weight persist.
Key Words: Birth Weight • Growth • Lambs • Nutrition • Organs
Introduction
Little information exists on postnatal consequences of intrauterine growth retardation on organ growth in sheep. Effects of severely reduced birth weight, achieved using various experimental models, on organ growth have been described in newborn lambs (Alexander, 1974
). In these studies in which birth weights ranged from 1 to 5 kg, low-birth-weight lambs had body weight-specific increases in heart, kidneys, and esophagus and stomach complex, but weight-specific reductions in liver, spleen, thyroid, and, most especially, thymus. Conversely, the growth of brain, other head parts, and adrenals was relatively unimpaired in small newborns. These data are also generally consistent with those of others who have examined effects of maternal undernutrition (Wallace, 1948; Everitt, 1965, 1968), carunclectomy (Harding et al., 1985), placental embolization (Creasy et al., 1972), and overfeeding of adolescent ewes (Wallace et al., 2000). However, at 70 d postpartum, BW-specific differences in organ weights were not evident between singleton and twin lambs weighing 4.6 and 3.5 kg at birth, respectively (Gabbedy, 1974).
We have previously reported postnatal consequences of intrauterine growth retardation in lambs of very low birth weight (average 2.3 kg) compared with those studied by Gabbedy (1974). Postnatal differences in growth and chemical composition of the body (Greenwood et al., 1998), muscle development (Greenwood et al., 2000a), and aspects of energy metabolism and its regulation (Greenwood et al., 1998, 2002) were evident during growth to 20 kg of live weight (LW). However, some of these effects were ameliorated or exacerbated by postnatal nutrition.
The objective of this study, therefore, was to test the hypotheses that prenatal and postnatal nutrition affect organ growth of neonatal lambs, using our previously described model of fetal growth retardation (Greenwood et al., 1998, 1999, 2000b).
Materials and Methods
Experimental Design
The experimental animals and experimental design (2 x 2 factorial arrangement; see Tables 1 and 2), rearing system, growth characteristics, and killing procedures were described in detail by Greenwood et al. (1998). All experimental animals were male Suffolk x (Finnsheep x Dorset) lambs removed from ewes at birth. Forty-eight lambs were selected on the basis of their low- (mean ± SD 2.29 ± 0.34 kg, n = 28) or high- (4.84 ± 0.45 kg, n = 20) birth weights. Lambs were obtained from 42 ewes, with 2 lambs obtained from a ewe on six occasions. On five of these occasions, the lambs were of the same birth weight category, in which case they were allocated to postnatal nutritional groups and slaughter weights to minimize bias due to any effect of individual dam.
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All procedures were performed with the approval of the Cornell University Institutional Animal Care and Use Committee.
Tissue Dissections
Adrenal glands, heart, kidneys, liver, lungs (including trachea), pancreas, spleen, testes, thymus, thyroid glands, stomach complex (including esophagus), and small intestine and large intestine (including rectum) were dissected from each lamb and weighed. Stomach, small intestine, and large intestine were subsequently weighed following removal of contents.
Calculations
The empty body weight (EBW) was calculated as described by Greenwood et al. (1998). Predicted weights of organs at completion of the rearing period (17.5 kg EBW) were determined by regressing the data for each organ on EBW (linear and, when significant, quadratic terms) separately for each treatment group (slowly and rapidly reared low-birth-weight lambs, n = 16 per group; slowly and rapidly reared high-birth weight lambs, n = 12 per group) to enhance the precision of estimates. Data for baseline animals were included in the regression analyses for each birth weight/nutrition group.
Statistical Analyses
Comparisons at birth between small and large newborns were made using Student’s t-test (Lyman-Ott, 1993). Contrasts among groups at high-birth weight equivalence were performed using Fisher’s protected LSD procedure (Lyman-Ott, 1993). Statistical analyses to establish effects of birth weight and nutrition categories and their interaction during rearing to 20 kg LW were performed using analyses of covariance (Genstat 5, Release 4.2, Lawes Agricultural Trust, Rothamstead, England), with age or EBW at slaughter (including quadratic terms when significant) as the covariate, and animal as the experimental unit. The F-ratios used to determine the significance of birth weight and nutrition categories on organ mass were adjusted to account for duplication of data for the baseline groups. This duplication was accounted for by increasing the error sum of squares, and by reducing the error degrees of freedom by 3 degrees for low-birth-weight and by 3 degrees for high-birth-weight baseline lambs. Probability values and least squares means for birth weight and nutrition categories are reported following removal from the models of nonsignificant (P > 0.10) quadratic terms for the covariate and nonsignificant interactions between birth weight and nutrition categories. Statistical significance was accepted at the 5% level of alpha and tendency toward significance at the 10% level.
Results
Organ Weights at Birth
All dissected organs (Table 3) weighed less (P < 0.001) in low- than in high-birth-weight lambs at birth, except for the adrenals, which tended to weigh less in the low-birth-weight lambs (P = 0.010). As a proportion of EBW, the thymus was smaller (P = 0.009) and the testes larger (P = 0.023), and there was a tendency for the spleen to be smaller (P = 0.054) and the heart larger (P = 0.060) in small compared with large newborns.
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) were heavier (P < 0.05) than those of the high-birth-weight baseline lambs at equivalent BW (approximately 5 kg LW). At this BW, liver and lung weights were greater (P < 0.05) in the low-birth-weight/high-nutrition lambs than in the low-birth-weight/low-nutrition and high-birth-weight baseline lambs. Stomach, large intestine, and total dissected organs were heavier (P < 0.05) in the low-birth-weight/low-nutrition lambs than in the low-birth-weight/high-nutrition lambs, whereas these organs were also heavier in the low-birth-weight/high-nutrition lambs than in the high-birth-weight baseline animals. The thyroid gland was smaller (P < 0.05) in the low-birth-weight/low-nutrition lambs than in the high-birth-weight baseline or low-birth-weight/high-nutrition lambs. Differences between the groups in weight of adrenals, heart, thymus, and small intestines were not apparent.
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) during rearing (all P < 0.020), apart from the adrenals, which tended to be smaller (P = 0.055) and the spleen (P = 0.551), testes (P = 0.437), and thymus (P = 0.584). All dissected organs were heavier at any given age in the rapidly compared with the slowly reared lambs (all P < 0.041).
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and 7). Rapidly reared lambs had larger kidneys (P < 0.001), liver (P < 0.001), small intestine (P = 0.020), and thymus (P = 0.003) and smaller pancreas (P = 0.002), testes (P = 0.016), stomach (P < 0.001), large intestine (P < 0.001), and entire gastrointestinal tract (P = 0.002) than slowly reared lambs at any given EBW. Slowly reared lambs tended to have a larger heart (P = 0.068) and smaller thyroid (P = 0.054).
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This study shows that intrauterine growth retardation resulting in severely reduced birth weight influences the size of neonatal organs during the rearing of lambs to approximately 20 kg LW. In particular, low-birth-weight lambs had a larger spleen and testes and greater combined weight of dissected organs during rearing than their high-birth-weight counterparts.
At birth, when assessed relative to body weight, the only organs significantly influenced by birth weight were the thymus, which was smaller, and the testes, which were larger in the small newborns. The heart tended to be larger and the spleen tended to be smaller in the low-birth-weight lambs. These findings, and shifts due to intrauterine growth retardation in the average weight-specific mass of the other organs, appear generally consistent with those of Wallace (1948), Everitt (1965), and Alexander (1974). An exception is the thyroid gland, which was disproportionately small in the low-birth-weight lambs studied by Alexander (1974) but unaffected by intrauterine growth retardation on a BW-specific basis in the newborn lambs of this study and in the undernourished, late-gestation fetuses studied by Everitt (1965).
Specific nutritional effects on organ growth among the small newborns during the early postpartum period were also evident. The liver and lungs were larger in the small newborns reared rapidly to 5 kg LW than those reared slowly and probably reflect greater nutrient intake and metabolic rate among the rapidly reared lambs. Conversely, the weights of the stomach, large intestine, and total dissected organs were greater in the small newborns reared more slowly to 5 kg, suggesting age-related influences on the development of these organs during this period.
During the early postpartum period, the relative rates of gain of organs in the low-birth-weight lambs were greater, overall, than in the high-birth-weight lambs. However, only the spleen and the testes remained heavier in the low-birth-weight lambs during subsequent rearing to 20 kg LW. The organs exhibiting the greatest fractional rates of increase in mass during the early postpartum period were the lymphoreticular tissues (thymus and spleen), which were relatively small at birth in the low-birth-weight lambs. The extent to which the striking postpartum increase in the size of the spleen of the low-birth-weight lambs contributed to the 30% greater mass of this organ at 20 kg LW compared with the equivalent high-birth-weight lambs warrants further investigation.
The lymphoreticular tissues exhibited a high degree of plasticity during early postpartum growth of the low-birth-weight newborns. This is emphasized by an estimated increase in spleen mass of almost 800% in the slowly reared small newborn lambs, and an increase in mass of over 600% in their rapidly reared counterparts, during body growth from 2.3 to 5 kg LW. As a result, spleen weights were over three times greater among low-birth-weight lambs than in the high-birth-weight newborn lambs at the same LW (5 kg). During similar postpartum LW gain (approximately 2.5 kg), the spleens of the slowly and rapidly reared large newborns were estimated to have increased by about 300 and 200%, respectively, or about 40% of the relative increase of the small newborns. Although the functional consequences of this more rapid postnatal growth of spleen in the low-birth-weight lamb remains to be investigated, it would be beneficial to determine the extent to which it reflects increased tissue mass relative to blood volume. Similarly, the thymus increased in mass by an estimated 500 to 600% during the early postpartum period in the low-birth-weight lambs compared with 140 to 150% in the high-birth-weight lambs during the equivalent period. The functional significance of this finding, and of the reduced relative weight of thymus at birth in the small newborns, also warrant further investigation, particularly in relation to long-term consequences for immunocompetence and health in later life. In this regard, associations between prenatal and postnatal growth and thymus function during later life have been demonstrated (McDade et al., 2001). Other organs exhibiting greater plasticity in the small compared with the large newborns during the early postnatal period were the liver, lungs, kidneys, pancreas, testes, and the gastrointestinal tract.
Postnatal nutrition altered the mass of specific organs without significantly altering the combined weight of the dissected organs during rearing to 20 kg LW. Kidneys, liver, thymus, and small intestine were larger, whereas pancreas, testes, stomach, large intestine, and the entire gastrointestinal tract were smaller in the rapidly compared with the slowly reared lambs during rearing. As with older lambs (Ferrell, 1988), the different postnatal nutritional regimens that changed the weights of specific organs—most notably the liver, kidneys, and the components of the gastrointestinal tract—are likely to have resulted in altered energy expenditure between the two groups. Hence, it is also likely that subsequent partitioning and utilization of nutrients would have differed between the lambs reared rapidly or slowly to weaning, due to changes in the mass and energy expenditure of specific organs.
The postnatal growth of most organs was more closely associated with EBW than with age, except for the lungs, testes, and stomach. In previous studies on postnatal organ growth (Palsson and Verges, 1952a,b; Palsson, 1955), when animals were compared at equal age but at different weights, the brain, which was not measured in the present study, and the rumen, reticulum, and omasum were more closely associated with age than BW or nutrition. In contrast, the weight of thymus, liver, spleen, kidneys, and small intestine were more closely associated with preslaughter nutrition than with either age or carcass weight. When organ weights were compared at equivalent ages in the present study, all were significantly influenced by postnatal nutrition and all apart from the adrenals, lungs, and combined weight of dissected organs were influenced by postnatal nutrition when compared at equivalent EBW.
Functional consequences of the greater testes weight in low-birth weight lambs at any given EBW remains to be investigated but, clearly, age-related effects contributed to this increase. We speculate that greater testes mass at any given EBW may have a longer-term role in supporting skeletal development and the anabolism of muscle in low-birth weight lambs.
The only significant interaction between birth weight and postnatal nutritional categories when organ weights of lambs were compared at equivalent EBW was for the large intestine, such that the high-birth weight lambs reared slowly had the highest and those reared rapidly the lowest large intestinal weights. Again, the functional significance of this finding remains to be determined.
In conclusion, lambs with severely reduced birth weight had increased spleen and testes weights and combined weight of dissected organs at 20 kg LW compared with their high-birth-weight counterparts in the present study. The functional significance of these findings and the longer-term persistence of these changes in organ mass warrant further investigation. Finally, it was also evident that postnatal nutritional regimen altered the mass of individual organs without affecting the combined weight of dissected organs at the conclusion of the rearing period.
Implications
Small size at birth and rapid postnatal hypertrophy of the lymphoreticular tissues of small compared with large newborns may influence immune function of lambs. The functional significance of persistently increased spleen weight during the rearing of neonates also warrants further investigation. Nutritional regimens resulting in slow or rapid postnatal growth may alter the mass of individual organs without influencing their combined weight at equivalent body weights. Hence, subsequent partitioning and utilization of nutrients by young animals reared to the same live weight at substantially different rates of growth may differ. Greater relative mass of the testes among small compared with large newborn lambs at birth and during rearing may enhance the capacity of male animals to overcome effects of severe, chronic intrauterine growth retardation resulting from placental insufficiency.
Footnotes
1 Supported in part by Cornell Univ. Agric. Exp. Stn., Meat Research Corporation (Australia), and NSW Agriculture (Australia). 
2 The authors also wish to thank M. Ashdown, manager of the Cornell University Mt. Pleasant Sheep Farm, who provided lambs to specification, and J. Schuck, who assisted with lamb rearing. The assistance provided by W. English, manager of the Large Animal Research and Teaching Unit, and D. Shaw, manager of the Department of Animal Science Slaughter Facility, is also gratefully acknowledged. Throughout this study, D. Hogue provided support.
3 Recipient of Junior Research Fellowship from Meat Research Corporation (Australia).
4 Present Address: NSW Agriculture Beef Industry Centre, University of New England, Armidale NSW 2351, Australia.
5 Present Address: Nutritional Services, Fort Worth Zoo, Fort Worth, TX 76110.
6 Correspondence—phone: 607-255-2862; fax 607-255-9829; e-mail: awb6{at}cornell.edu.
Received for publication July 29, 2003. Accepted for publication October 8, 2003.
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