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The physical state and metabolic status of lambs of different birth rank soon after birth
Livestock Science 111 (2007) 10 – 15 www.elsevier.com/locate/livsci
The physical state and metabolic status of lambs of different birth rank soon after birth K.J. Stafford ⁎, P.R. Kenyon, S.T. Morris, D.M. West Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11222, Palmerston North, New Zealand Received 15 August 2006; received in revised form 18 October 2006; accepted 23 October 2006
Abstract This study investigated the physical state and metabolic status of lambs of different birth ranks soon after birth. The aim was to identify the factors that result in poorer survival rates in triplet than single or twin lambs. Six hundred and twenty one Romney ewes were mated over a 4-day period and 46 of them were observed continually from day 143 of pregnancy until they finished lambing. Blood samples, taken from all lambs within 5 min of birth, were placed on ice, centrifuged and the plasma harvested and subsequently analysed for glucose, fructose, lactate, thyroxine (T4) and gamma-glutamyl transferase (GGT). The rectal temperature of each lamb was recorded at birth and at 1, 2, 3 and 6 h of life. Lambs were weighed and measured at 3 h of age. At birth, triplet lambs were significantly lighter (P < 0.05) and had lower (P < 0.05) plasma fructose and thyroxine than twin and single lambs, higher (P < 0.05) lactate concentrations and a lower rectal temperature (P < 0.05) than twin lambs. These observations suggest that they are subject to placental insufficiency. The packed cell volume was significantly (P < 0.001) higher in twin than triplet lambs. The order at birth of twin or triplet lambs had no effect on birthweight or plasma metabolite concentrations. The smallest triplet was significantly lighter (P < 0.05) and had higher plasma lactate (P < 0.05) concentration than the largest triplet. These physiological limitations found in smaller triplet lambs at birth leave them prone to perinatal mortality. Management techniques, to increase triplet lamb birthweight and thereby improve their survival outcome need further investigation. © 2007 Elsevier B.V. All rights reserved. Keywords: Triplet; Quadruplets; Twin; Lambs; Rectal temperature; Glucose; Fructose; Lactate; Thyroxine; Birthweight
1. Introduction The survival of lambs in the hours following birth is influenced by many factors including ewe nutrition during pregnancy (Dwyer et al., 2003; Everett-Hincks Abbreviations: CIDR, Controlled internal drug release; GGT, Gamma-glutamyl transferase; PCV, Packed cell volume; PMSG, Pregnant mare serum gonadotropin; SE, Standard error; T4, Thyroxine. ⁎ Corresponding author. Tel.: +64 6 3505548; fax: +64 6 3505699. E-mail address: [email protected] (K.J. Stafford). 1871-1413/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.livsci.2006.10.018
et al., 2005a), the process of birth (Barlow et al., 1987), the behaviour of the ewe (Everett-Hincks et al., 2005b) and lamb (Dwyer et al., 2004), and the physical environment the lamb is born into (Mellor and Stafford, 2004). There were no significant anatomical differences between twin and triplet fetuses at 139 days of gestation to explain the difference in survival rates of triplet and twin lambs (Kenyon et al., in press). However, the physical state of the lamb at birth will influence its behaviour (Dwyer et al., 2004) and subsequent survival. Triplet-born lambs are smaller
K.J. Stafford et al. / Livestock Science 111 (2007) 10–15
and lighter than twin lambs (Morris and Kenyon, 2004) and have poorer survival rates than twin lambs under outdoor lambing conditions (Dalton et al., 1980; Morris and Kenyon, 2004; Thomson et al., 2004). Smaller lambs have a greater surface area to body mass ratio and display greater heat loss (Alexander, 1979; McCutcheon et al., 1981) which may explain in part some of the difference in survival rates between single, twin and triplet lambs. However other physical characteristics of the newborn lamb may influence survival. This study was undertaken to examine the relationship between birth rank and physical characteristics of the newborn lambs soon after birth to identify factors that might influence the difference in mortality rates between lambs of different litter sizes. 2. Materials and methods 2.1. Experimental design Multiparous Romney ewes, 3 to 5 years of age, were used in this trial. Oestrus was synchronised in 621 ewes with a progesterone releasing device (Eazi-Breed CIDR, Pfizer, New Zealand) inserted for 12 days. When the device was removed ewes were injected intramuscularly with 400 I.U. PMSG (Folligon™, Intervet, New Zealand) and 50 Romney rams with crayon mating harnesses were introduced for a 4-day breeding period. Ewes with crayon marks were pregnancy scanned 59 days after the mid-point of the breeding period. Ten singleton-, 18 twin-, 13 triplet- and 5 quadrupletbearing ewes respectively became available for the present study but this does not represent the distribution of litter sizes amongst the flock. During breeding and until day 141 of pregnancy the selected ewes were managed as one flock under commercial grazing conditions. At day 141, the ewes were weighed and moved indoors into individual pens (1.5 by 1.5 m) and offered grass silage ad libitum and water. The ewes were weighed on day 143 and then observed continually until the end of the lambing period. Rectal temperatures of the lambs were taken within 5 min of birth and at 1, 2, 3 and 6 h of life. Three hours after birth each lamb (dead or alive) was identified to its dam, tagged, weighed, its sex and birth rank determined, and crown rump length (CRL) and girth measured. If a lamb died or its rectal temperature fell below 36 °C during the 6 hour measurement period it was removed from the study but its data were still used for any previously recorded measurements. At the end of the sampling period ewes and their lambs were returned to pasture.
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2.2. Lamb blood samples Within 5 min of birth, two 5 mL blood samples were collected from each live lamb by jugular venepuncture into a Lithium Heparin and a Sodium Fluoride– Potassium Oxalate vacutainer (Becton Dickinson Vacutainer Systems, USA). Blood samples were immediately placed on ice until centrifuged at 3500 rpm for 15 min. The plasma was harvested and then frozen at − 20 °C until analysis was carried out. Samples were analysed for glucose using a hexokinase assay (Roche Diagnostics Ltd, Switzerland), fructose using an enzymatic assay (R Biopharm, Darmstadt, Germany), lactate using a lactate oxidase/peroxidase kit (Roche Diagnostics Ltd, New Zealand), thyroxine (T4) using a radioimmunoassay diagnostic kit (Coat-A-Count, Diagnostic Products Corporation, CA, USA) and gamma-glutamyl transferase (GGT) (Roche Diagnostics Ltd, Switzerland). The packed cell volume (PCV) of each blood sample was determined before it was placed on ice. This study was conducted at the Massey University Keeble Farm, Palmerston North, New Zealand, in September 2004, with approval from the Massey University Animal Ethics Committee. 2.3. Statistical analysis All measurements for both ewes and their lambs were subjected to analysis of variance using the Generalised Linear Model procedure of the statistical package Minitab 12.1 (Minitab, 2002). In the model used to partition variation in ewe liveweight pregnancy rank was used as a fixed effect. In the models used to partition variation in lamb birthweight, girth and CRL measurements and rectal temperatures, sex of the lamb and birth rank were used as fixed effects and date of birth as a covariate. The models used to partition variation in rectal temperature post-birth and at 1 h were analysed both with and without lamb birthweight as a covariate. To achieve a normal distribution glucose, fructose, lactate and thyroxine concentrations were subjected to a square root transformation and GGT to log10 transformation. Birth rank was used as a fixed effect in the models used to partition variation of lamb metabolite and hormone concentrations and date of birth was a covariate. To determine variation in metabolite and T4 concentrations within twin and triplet sets of lambs, data from full sets were ranked within set, on both birth order (i.e. first, second and/or third) and birth size (i.e. small, big and/or middle). In these models, day of birth was used as a covariate and birth order or birth size was
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Table 1 The effect of pregnancy rank on ewe liveweight (kg) at day 141 of pregnancy and lamb birthweight (kg), girth (cm) and crown rump length (CRL, cm) (mean ± SE)
Birth rank Singleton Twin Triplet Quadruplet
Ewe
Lamb
Liveweight
Birthweight
Girth
CRL
n
Mean
SE
n
Mean
SE
Mean
SE
Mean
SE
10 18 13 5
63.65x 72.42y 69.89xy 74.20y
2.05 1.53 2.16 2.90
10 36 39 20
4.77x 4.16x 2.80y 2.55y
0.22 0.11 0.10 0.17
37.76x 36.92x 32.22y 31.28y
1.06 0.52 0.49 0.83
51.91x 51.58x 46.77y 43.89y
1.66 0.82 0.77 1.30
Means within columns with differing superscripts are significantly (P < 0.05) different.
the rectal temperature of quadruplet-born lambs was significantly (P < 0.05) less than that of singleton-born lambs. Quadruplet-born lambs had significantly (P < 0.01) lower rectal temperatures than all other lambs at 2, 3 and 6 h. At 6 h triplet-born lambs tended (P = 0.05) to have lower rectal temperatures than twinborn lambs. When the rectal temperatures soon after birth and at 1 h were analysed using data only from those lambs still present in the study at 6 h, quadruplet-born lambs still had significantly lower rectal temperatures than both singletons and twins soon after birth (P = 0.05 and P < 0.001 respectively) and all birth ranks at 1 h (P < 0.001). In contrast the rectal temperatures of triplet-born lambs were no longer different from that of twins. Rectal temperatures of lambs after birth and at 1 h did not differ between the birth ranks when birthweight was used as a covariate.
used as appropriate as fixed effects. Variation with quadruplet lambs was not evaluated due to the small number of quadruplet lambs. 3. Results 3.1. Ewe and lamb size Singleton-bearing ewes were significantly lighter at day 141 of gestation than both twin- (P < 0.01) and quadruplet-bearing (P = 0.03) ewes (Table 1). Singletonborn lambs were significantly (P < 0.001) heavier than both triplet- and quadruplet-born lambs and tended to be heavier than twin-born lambs (P = 0.07). Twin-born lambs were significantly (P < 0.001) heavier than both triplet- and quadruplet-born lambs. Singleton- and twinborn lambs had significantly (P < 0.05) greater girth and CRL measurements than both triplet- and quadrupletborn lambs.
3.3. Lamb metabolite concentrations 3.2. Rectal temperature of lambs Quadruplet lambs had significantly (P = 0.01) lower square root of glucose concentration than triplet-born lambs (Table 3). Birth rank affected square root of fructose concentrations such that triplet-born lambs had significantly (P < 0.01) lower concentrations than both
The rectal temperatures of triplet- and quadrupletborn lambs were significantly lower than that of twinborn lambs soon after birth (P < 0.01) and at 1 h (P = 0.02 and P < 0.01 respectively) (Table 2). In addition, at 1 h
Table 2 The effect of birth rank on lamb rectal temperature (°C) within 5 min of birth and at 1, 2 and 6 h after birth (mean ± SE) Lamb rectal temperatures Birth
Birth rank Singleton Twin Triplet Quadruplet
1h
2h
3h
6h
n
Mean
SE
n
Mean
SE
n
Mean
SE
n
Mean
SE
n
Mean
SE
10 34 33 15
39.16xy 39.29y 38.19x 37.98x
0.45 0.23 0.23 0.36
10 33 32 14
39.59yz 39.76z 38.38xy 37.44x
0.63 0.32 0.32 0.50
10 33 30 13
39.68y 39.68y 39.09y 37.83x
0.41 0.21 0.22 0.34
10 32 29 13
39.63y 39.48y 39.16y 37.95x
0.35 0.18 0.19 0.29
9 32 25 13
39.60y 39.52y 39.06y 38.24x
0.25 0.12 0.13 0.19
At 6 h triplets and twins differ at P = 0.05. Means within columns with differing superscripts are significantly (P < 0.05) different.
K.J. Stafford et al. / Livestock Science 111 (2007) 10–15
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Table 3 The effect of birth rank on the square root of glucose (mmol/L), fructose (mmol/L), lactate (mmol/L) and thyroxine (mmol/L) and the log10 of gammaglutamyl transferase (GGT, U/L) concentrations (mean ± SE) Glucose
Birth rank Singleton Twin Triplet Quadruplet
Fructose
Lactate
Thyroxine
GGT
n
Mean
SE
Mean
SE
Mean
SE
Mean
SE
Mean
SE
10 29 31 11
1.48xy 1.34xy 1.49y 1.18x
0.09 (2.26) a 0.05 (1.88) 0.05 (2.31) 0.09 (1.45)
1.37yz 1.34z 1.13x 1.16xy
0.06 (1.90) 0.04 (1.83) 0.03 (1.29) 0.06 (1.37)
2.17xy 2.15x 2.51y 2.22xy
0.16 (4.85) 0.09 (4.87) 0.09 (6.53) 0.14 (5.06)
10.80x 10.24x 8.36y 7.42y
0.63 (119.94) 0.35 (108.02) 0.34 (74.24) 0.57 (56.13)
1.72 1.73 1.74 1.77
0.04 (58.61) 0.03 (55.49) 0.03 (57.31) 0.04 (63.78)
Means within columns with differing superscripts are significantly different (P < 0.05). a Values in parentheses are the nontransformed means. The statistical analysis was carried out on transformed data.
twin- and singleton-born lambs and quadruplet-born lambs had lower concentrations than twin-born lambs. Triplet-born lambs had significantly (P = 0.03) higher square root of lactate concentrations than their twin-born counterparts. The square root of thyroxine concentrations of both triplet- and quadruplet-born lambs were significantly (P < 0.01) lower than that of both singletonand twin-born lambs. 3.4. Effect of birth order Birth order had no effect on the birthweight of twinor triplet-born lambs (Table 4). There was no effect of birth order in twins on any of the metabolic or hormone concentrations measured. Within triplet lambs, the lamb that was born first had significantly lower square root of fructose concentrations than both the second-born (P = 0.03) and last-born lamb (P = 0.01). 3.5. Effect of size within litter Within twin-born lambs, birth size had no effect on any of the metabolite or hormone concentrations
measured (Table 5). The heaviest triplet lamb had significantly (P = 0.03) lower square root of glucose concentrations than the middle liveweight lamb although, it did not differ significantly with its lightest counterpart. The heaviest triplet lamb had significantly lower square root of lactate (P = 0.04) concentrations compared to its lightest counterpart. The heaviest triplet lamb had significantly (P < 0.01) higher square root of T4 concentrations compared to its lightest counterpart and in triplets but not twins T4 concentrations were correlated (P = 0.06) with birthweight. In addition, the lightest triplet lambs had significantly (P < 0.01) higher log10 GGT concentrations than both its middle and heaviest counterparts. 3.6 PCV The mean PCV was significantly (P < 0.001) higher in twin lambs (46.63, SE 0.84) compared to both triplet- (41.31, SE 0.86) and quadruplet- (40.83, SE 1.23) born lambs. Singleton-born lambs did not differ from any of the other birth ranks (43.61, SE 1.80). Within full sets of twin- and triplet-born lambs
Table 4 The effect of birth order within each pregnancy rank on the birthweight (kg) and square root of glucose (mmol/L), fructose (mmol/L), lactate (mmol/L) and thyroxine (mmol/L) and the log10 of gamma-glutamyl transferase (GGT, U/L) concentrations (mean ± SE)
Twin First Second Triplet First Second Third
Birthweight
Glucose
Fructose
Lactate
n
Mean
SE
Mean
12 12
4.02 4.16
0.15 0.16
8 8 8
2.93 2.94 3.12
0.19 0.19 0.19
Thyroxine
GGT
SE
Mean
SE
Mean
SE
Mean
SE
Mean
SE
1.46 1.28
0.09 (2.23) a 0.09 (1.72)
1.41 1.26
0.06 (2.07) 0.07 (1.63)
2.31 2.10
0.15 (5.69) 0.16 (4.54)
10.76 10.16
0.47 (119.67) 0.52 (104.67)
1.75 1.70
0.03 (57.70) 0.04 (53.44)
1.50 1.44 1.45
0.08 (2.32) 0.08 (2.11) 0.08 (2.13)
1.01x 1.18y 1.22y
0.05 (1.01) 0.05 (1.41) 0.05 (1.51)
2.20 2.60 2.54
0.18 (4.94) 0.18 (7.10) 0.18 (6.75)
8.33 9.04 8.47
0.77 (74.63) 0.77 (85.88) 0.77 (74.50)
1.76 1.70 1.68
0.04 (61.88) 0.04 (52.75) 0.04 (60.63)
Means within columns in birth ranks with differing superscripts are significantly different (P < 0.05). a Values in parentheses are the nontransformed means. Statistical analysis was carried out on transformed data.
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K.J. Stafford et al. / Livestock Science 111 (2007) 10–15
Table 5 The effect of birth size within each pregnancy rank on the birthweight (kg) and square root of glucose (mmol/L), fructose (mmol/L), lactate (mmol/L) and thyroxine (mmol/L) and the log10 of gamma-glutamyl transferase (GGT, U/L) concentrations (mean ± SE)
Twin Big Small Triplet Small Middle Big
Birthweight
Glucose
Fructose
Lactate
n
Mean
SE
Mean
12 12
4.31y 3.86x
0.14 0.14
8 8 8
2.56x 2.96x 3.48y
0.14 0.14 0.14
Thyroxine
GGT
SE
Mean
SE
Mean
SE
Mean
SE
Mean
SE
1.31 1.44
0.09 (1.80) a 0.09 (2.18)
1.34 1.35
0.07 (1.85) 0.07 (1.88)
2.19 2.24
0.16 (5.03) 0.16 (5.29)
10.91 10.07
0.49 (103.42) 0.49 (122.17)
1.73 1.73
0.04 (55.75) 0.04 (55.75)
1.40xy 1.63y 1.35x
0.07 (2.03) 0.07 (2.66) 0.07 (1.87)
1.10 1.11 1.20
0.06 (1.23) 0.06 (1.25) 0.06 (1.46)
2.75y 2.48xy 2.12x
0.17 (7.92) 0.17 (6.26) 0.17 (7.93)
7.24x 8.38xy 10.23y
0.61 (54.25) 0.61 (72.25) 0.61 (108.50)
1.86y 1.64x 1.68x
0.03 (75.88) 0.03 (50.62) 0.03 (48.75)
Means within columns in birth ranks with differing superscripts are significantly different (P < 0.05). a Values in parentheses are the nontransformed means. Statistical analysis was carried out on transformed data.
PCV did not differ based on either birth size or birth order. 4. Discussion The triplet- and quadruplet-born lambs were significantly lighter, had lower rectal temperature at birth and 1 h later and lower fructose and thyroxine levels and higher lactate than twin or single lambs. These physical characteristics suggest that triplets experience placental insufficiency (see Barlow et al., 1987) which makes them susceptible to perinatal mortality. At 6 h triplet lambs had temperatures similar to those to twins which suggests that either their temperature had risen or those with low temperatures had died or been removed from the study allowing the mean temperature to rise. This suggestion is supported by the observation that when the rectal temperature at birth and 1 h of only those lambs which remained in the study at 6 h, are analysed there is no difference between twin and triplet lambs although the rectal temperature of quadruplet lambs was still lower. Quadruplets remained with a low mean temperature at 6 h. The difference in rectal temperature was due to size, as indicated by a lack of difference in temperature after correction for liveweight and not due to birth rank itself. Smaller lambs had lower temperatures as found by Dwyer and Morgan (2006). Light lambs are more likely to suffer hypothermia than heavier lambs (Moore et al., 1986). Light lambs have a greater surface area to body mass ratio which results in an increase body heat loss to the environment (Alexander, 1979) plus reduced body reserves, and probably poorer thermogenic capacity of brown adipose tissue (Budge et al., 2000). Plasma fructose levels are elevated in lambs immediately after birth (Daniels et al., 1974) and it is an important source of energy for the newborn but it is
quickly utilised forcing the lamb to use alternatives. Triplet lamb foetuses had lower fructose levels than twin foetuses in late gestation (Kenyon et al., in press) and in this study triplet lambs were born with low fructose levels, and thus less energy with which to survive until they ingest colostrum. However, it is well established that triplet lambs ingest less colostrum than single- and twin-born lambs and that there is a wide variation in intake in triplet lambs (Kenyon et al., 2005). Quadruplet-born lambs also had low fructose and glucose levels. Adequate glucose and fructose is also important in allowing lambs to increase their birth temperature. The low T4 levels seen in triplet and quadruplet lambs may result in a poorer ability to generate heat (Dwyer and Morgan, 2006) and further influence rectal temperature changes. Biochemical and physical characteristics did not differ according to birth order in twin or triplet lambs. Thus first- or last-born lambs did not appear to be stressed more at birth than each other or the middleborn lamb in triplets. There was little difference between the physical state of the larger and smaller twin-born lambs. However the largest triplet was significantly larger than the other two, had lower lactate levels than the smallest lamb, higher T4 levels and higher but not significantly higher fructose levels. Moreover, the results suggest that the larger triplet lambs had the physical characteristics at birth to promote survival whilst the smaller triplets and quadruplet lambs had physical characteristics which give them a much poorer chance of survival than larger triplets, twins or singleton-born lambs. These results suggest that increasing birthweight and/or providing conditions which limit heat loss in triplet-born lambs should improve survival rates. Pasture grazing conditions, and supplementation with concentrate feeds in late pregnancy have been shown
K.J. Stafford et al. / Livestock Science 111 (2007) 10–15
to improve the liveweight and metabolic status of ewes pregnant with triplets and the birthweight of triplet lambs (Morris and Kenyon, 2004). In addition mid-pregnancy shearing has been shown to increase birthweight and survival of triplet lambs (Kenyon et al., 2001). The provision of shelter for ewes with singleton and twin lambs also improved lamb survival rates to weaning (Egan et al., 1972). Therefore practical means of increasing triplet lamb birthweight and the provision of shelter require further investigation. 5. Conclusions Triplet, especially the smaller triplets, and quadruplet lambs born to Romney ewes in this trial were constitutionally less capable of surviving than twins or single-born lambs. The management techniques which would improve their survival by increasing birthweight and providing a more sheltered environment at birth require further investigation. Acknowledgements The authors wish to acknowledge the funding provided by Massey University and Meat and Wool New Zealand and support from the National Centre for Growth and Development. References Alexander, G., 1979. Cold thermogenesis. International Review of Physiology: Environmental Physiology 20, 43–155. Barlow, R.M., Gardiner, A.C., Angus, K.W., Gilmour, J.S., Mellor, D.J., Cuthbertson, J.C., Newlands, G., Thompson, R., 1987. Clinical, biochemical and pathological study of perinatal lambs in a commercial flock. The Veterinary Record 120, 357–362. Budge, H., Bispham, J., Dandrea, J., Evans, E., Heasman, L., Ingleton, P.M., Sullivan, C., Wilson, V., Stephenson, T., Symonds, M.E., 2000. Effect of maternal nutrition on brown adipose tissue and its prolactin receptor status in the fetal lamb. Pediatric Research 47, 781–786. Dalton, D.C., Knight, T.W., Johnson, D.L., 1980. Lamb survival in sheep breeds on New Zealand hill country. New Zealand Journal of Agricultural Research 23, 167–173. Daniels, L.B., Perkins, J.L., Krieder, D., Tugwell, D., Carpenter, D., 1974. Blood glucose and fructose in the newborn ruminant. Journal of Dairy Science 57, 1196–1200.
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Dwyer, C.M., Morgan, C.A., 2006. Maintenance of body temperature in the neonatal lamb: effects of breed, birth weight and litter size. Journal of Animal Science 84, 1093–1101. Dwyer, C.M., Lawrence, A.B., Bishop, S.C., Lewis, M., 2003. Ewe– lamb behaviours at birth are affected by maternal undernutrition in pregnancy. British Journal of Nutrition 89, 123–136. Dwyer, C.M., Calvert, S.K., Farish, M., Donbavand, J., Pickup, H.E., 2004. Breed, litter and parity effects on placental weight and placentome number, and consequences for the neonatal behaviour of the lamb. Theriogenology 63, 1092–1110. Egan, J.K., McLaughlin, J.W., Thompson, R.L., McIntyre, J.S., 1972. The importance of shelter in reducing neonatal lamb deaths. Australian Journal of Experimental Agriculture and Animal Husbandry 12, 470–472. Everett-Hincks, J.M., Blair, H.T., Stafford, K.J., Lopez-Villalobos, N., Kenyon, P.R., Morris, S.T., 2005a. The effect of pasture allowance fed to twin- and triplet-bearing ewes in late pregnancy on ewe and lamb behaviour and performance to weaning. Livestock Production Science 97, 253–266. Everett-Hincks, J.M., Lopez-Villalobos, N., Blair, H.T., Stafford, K.J., 2005b. The effect of ewe maternal behaviour score on lamb and litter survival. Livestock Production Science 93, 51–61. Kenyon, P.R., Revell, D.K., Morris, S.T., 2001. Mid-pregnancy shearing can increase birthweight and survival to weaning of multiple-born lambs under commercial conditions. Australian Journal of Experimental Agriculture 46, 821–825. Kenyon, P.R., Stafford, K.J., Morel, P.C.H., Morris, S.T., 2005. Does sward height grazed by ewes in mid- to late-pregnancy affect indices of colostrum intake by twin and triplet lambs? New Zealand Veterinary Journal 53, 336–339. Kenyon, P.R., Stafford, K.J., Jenkinson, C.M.C., Morris, S.T., West, D.M., in press. The body composition and metabolic status of twin- and triplet-bearing ewes and their fetuses in late pregnancy. Livestock Science. McCutcheon, S.N., Holmes, C.W., McDonald, M.F., 1981. The starvation-exposure syndrome and neonatal lamb mortality: a review. Proceedings of the New Zealand Society of Animal Production 41, 209–233. Mellor, D.J., Stafford, K.J., 2004. Animal welfare implications of neonatal mortality and morbidity in farm animals. The Veterinary Journal 168, 118–133. Minitab, 2002. Minitab version 12.1. Minitab Inc., State College, PA, USA. Moore, R.W., Millar, C.M., Lynch, P.R., 1986. The effects of pre-natal nutrition and type of birth and rearing of lambs on vigour, temperature and weight at birth and weight and survival at weaning. Proceedings of the New Zealand Society of Animal Production 46, 259–262. Morris, S.T., Kenyon, P.R., 2004. The effect of litter size and sward height on ewe and lamb performance. New Zealand Journal of Agricultural Research 47, 275–286. Thomson, B.C., Muir, P.D., Smith, N.B., 2004. Litter size, lamb survival, birth and twelve week weight in lambs born to cross-bred ewes. Proceedings of the New Zealand Grassland Association 66, 233–238.
The physical state and metabolic status of lambs of different birth rank soon after birth K.J. Stafford ⁎, P.R. Kenyon, S.T. Morris, D.M. West Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Private Bag 11222, Palmerston North, New Zealand Received 15 August 2006; received in revised form 18 October 2006; accepted 23 October 2006
Abstract This study investigated the physical state and metabolic status of lambs of different birth ranks soon after birth. The aim was to identify the factors that result in poorer survival rates in triplet than single or twin lambs. Six hundred and twenty one Romney ewes were mated over a 4-day period and 46 of them were observed continually from day 143 of pregnancy until they finished lambing. Blood samples, taken from all lambs within 5 min of birth, were placed on ice, centrifuged and the plasma harvested and subsequently analysed for glucose, fructose, lactate, thyroxine (T4) and gamma-glutamyl transferase (GGT). The rectal temperature of each lamb was recorded at birth and at 1, 2, 3 and 6 h of life. Lambs were weighed and measured at 3 h of age. At birth, triplet lambs were significantly lighter (P < 0.05) and had lower (P < 0.05) plasma fructose and thyroxine than twin and single lambs, higher (P < 0.05) lactate concentrations and a lower rectal temperature (P < 0.05) than twin lambs. These observations suggest that they are subject to placental insufficiency. The packed cell volume was significantly (P < 0.001) higher in twin than triplet lambs. The order at birth of twin or triplet lambs had no effect on birthweight or plasma metabolite concentrations. The smallest triplet was significantly lighter (P < 0.05) and had higher plasma lactate (P < 0.05) concentration than the largest triplet. These physiological limitations found in smaller triplet lambs at birth leave them prone to perinatal mortality. Management techniques, to increase triplet lamb birthweight and thereby improve their survival outcome need further investigation. © 2007 Elsevier B.V. All rights reserved. Keywords: Triplet; Quadruplets; Twin; Lambs; Rectal temperature; Glucose; Fructose; Lactate; Thyroxine; Birthweight
1. Introduction The survival of lambs in the hours following birth is influenced by many factors including ewe nutrition during pregnancy (Dwyer et al., 2003; Everett-Hincks Abbreviations: CIDR, Controlled internal drug release; GGT, Gamma-glutamyl transferase; PCV, Packed cell volume; PMSG, Pregnant mare serum gonadotropin; SE, Standard error; T4, Thyroxine. ⁎ Corresponding author. Tel.: +64 6 3505548; fax: +64 6 3505699. E-mail address: [email protected] (K.J. Stafford). 1871-1413/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.livsci.2006.10.018
et al., 2005a), the process of birth (Barlow et al., 1987), the behaviour of the ewe (Everett-Hincks et al., 2005b) and lamb (Dwyer et al., 2004), and the physical environment the lamb is born into (Mellor and Stafford, 2004). There were no significant anatomical differences between twin and triplet fetuses at 139 days of gestation to explain the difference in survival rates of triplet and twin lambs (Kenyon et al., in press). However, the physical state of the lamb at birth will influence its behaviour (Dwyer et al., 2004) and subsequent survival. Triplet-born lambs are smaller
K.J. Stafford et al. / Livestock Science 111 (2007) 10–15
and lighter than twin lambs (Morris and Kenyon, 2004) and have poorer survival rates than twin lambs under outdoor lambing conditions (Dalton et al., 1980; Morris and Kenyon, 2004; Thomson et al., 2004). Smaller lambs have a greater surface area to body mass ratio and display greater heat loss (Alexander, 1979; McCutcheon et al., 1981) which may explain in part some of the difference in survival rates between single, twin and triplet lambs. However other physical characteristics of the newborn lamb may influence survival. This study was undertaken to examine the relationship between birth rank and physical characteristics of the newborn lambs soon after birth to identify factors that might influence the difference in mortality rates between lambs of different litter sizes. 2. Materials and methods 2.1. Experimental design Multiparous Romney ewes, 3 to 5 years of age, were used in this trial. Oestrus was synchronised in 621 ewes with a progesterone releasing device (Eazi-Breed CIDR, Pfizer, New Zealand) inserted for 12 days. When the device was removed ewes were injected intramuscularly with 400 I.U. PMSG (Folligon™, Intervet, New Zealand) and 50 Romney rams with crayon mating harnesses were introduced for a 4-day breeding period. Ewes with crayon marks were pregnancy scanned 59 days after the mid-point of the breeding period. Ten singleton-, 18 twin-, 13 triplet- and 5 quadrupletbearing ewes respectively became available for the present study but this does not represent the distribution of litter sizes amongst the flock. During breeding and until day 141 of pregnancy the selected ewes were managed as one flock under commercial grazing conditions. At day 141, the ewes were weighed and moved indoors into individual pens (1.5 by 1.5 m) and offered grass silage ad libitum and water. The ewes were weighed on day 143 and then observed continually until the end of the lambing period. Rectal temperatures of the lambs were taken within 5 min of birth and at 1, 2, 3 and 6 h of life. Three hours after birth each lamb (dead or alive) was identified to its dam, tagged, weighed, its sex and birth rank determined, and crown rump length (CRL) and girth measured. If a lamb died or its rectal temperature fell below 36 °C during the 6 hour measurement period it was removed from the study but its data were still used for any previously recorded measurements. At the end of the sampling period ewes and their lambs were returned to pasture.
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2.2. Lamb blood samples Within 5 min of birth, two 5 mL blood samples were collected from each live lamb by jugular venepuncture into a Lithium Heparin and a Sodium Fluoride– Potassium Oxalate vacutainer (Becton Dickinson Vacutainer Systems, USA). Blood samples were immediately placed on ice until centrifuged at 3500 rpm for 15 min. The plasma was harvested and then frozen at − 20 °C until analysis was carried out. Samples were analysed for glucose using a hexokinase assay (Roche Diagnostics Ltd, Switzerland), fructose using an enzymatic assay (R Biopharm, Darmstadt, Germany), lactate using a lactate oxidase/peroxidase kit (Roche Diagnostics Ltd, New Zealand), thyroxine (T4) using a radioimmunoassay diagnostic kit (Coat-A-Count, Diagnostic Products Corporation, CA, USA) and gamma-glutamyl transferase (GGT) (Roche Diagnostics Ltd, Switzerland). The packed cell volume (PCV) of each blood sample was determined before it was placed on ice. This study was conducted at the Massey University Keeble Farm, Palmerston North, New Zealand, in September 2004, with approval from the Massey University Animal Ethics Committee. 2.3. Statistical analysis All measurements for both ewes and their lambs were subjected to analysis of variance using the Generalised Linear Model procedure of the statistical package Minitab 12.1 (Minitab, 2002). In the model used to partition variation in ewe liveweight pregnancy rank was used as a fixed effect. In the models used to partition variation in lamb birthweight, girth and CRL measurements and rectal temperatures, sex of the lamb and birth rank were used as fixed effects and date of birth as a covariate. The models used to partition variation in rectal temperature post-birth and at 1 h were analysed both with and without lamb birthweight as a covariate. To achieve a normal distribution glucose, fructose, lactate and thyroxine concentrations were subjected to a square root transformation and GGT to log10 transformation. Birth rank was used as a fixed effect in the models used to partition variation of lamb metabolite and hormone concentrations and date of birth was a covariate. To determine variation in metabolite and T4 concentrations within twin and triplet sets of lambs, data from full sets were ranked within set, on both birth order (i.e. first, second and/or third) and birth size (i.e. small, big and/or middle). In these models, day of birth was used as a covariate and birth order or birth size was
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K.J. Stafford et al. / Livestock Science 111 (2007) 10–15
Table 1 The effect of pregnancy rank on ewe liveweight (kg) at day 141 of pregnancy and lamb birthweight (kg), girth (cm) and crown rump length (CRL, cm) (mean ± SE)
Birth rank Singleton Twin Triplet Quadruplet
Ewe
Lamb
Liveweight
Birthweight
Girth
CRL
n
Mean
SE
n
Mean
SE
Mean
SE
Mean
SE
10 18 13 5
63.65x 72.42y 69.89xy 74.20y
2.05 1.53 2.16 2.90
10 36 39 20
4.77x 4.16x 2.80y 2.55y
0.22 0.11 0.10 0.17
37.76x 36.92x 32.22y 31.28y
1.06 0.52 0.49 0.83
51.91x 51.58x 46.77y 43.89y
1.66 0.82 0.77 1.30
Means within columns with differing superscripts are significantly (P < 0.05) different.
the rectal temperature of quadruplet-born lambs was significantly (P < 0.05) less than that of singleton-born lambs. Quadruplet-born lambs had significantly (P < 0.01) lower rectal temperatures than all other lambs at 2, 3 and 6 h. At 6 h triplet-born lambs tended (P = 0.05) to have lower rectal temperatures than twinborn lambs. When the rectal temperatures soon after birth and at 1 h were analysed using data only from those lambs still present in the study at 6 h, quadruplet-born lambs still had significantly lower rectal temperatures than both singletons and twins soon after birth (P = 0.05 and P < 0.001 respectively) and all birth ranks at 1 h (P < 0.001). In contrast the rectal temperatures of triplet-born lambs were no longer different from that of twins. Rectal temperatures of lambs after birth and at 1 h did not differ between the birth ranks when birthweight was used as a covariate.
used as appropriate as fixed effects. Variation with quadruplet lambs was not evaluated due to the small number of quadruplet lambs. 3. Results 3.1. Ewe and lamb size Singleton-bearing ewes were significantly lighter at day 141 of gestation than both twin- (P < 0.01) and quadruplet-bearing (P = 0.03) ewes (Table 1). Singletonborn lambs were significantly (P < 0.001) heavier than both triplet- and quadruplet-born lambs and tended to be heavier than twin-born lambs (P = 0.07). Twin-born lambs were significantly (P < 0.001) heavier than both triplet- and quadruplet-born lambs. Singleton- and twinborn lambs had significantly (P < 0.05) greater girth and CRL measurements than both triplet- and quadrupletborn lambs.
3.3. Lamb metabolite concentrations 3.2. Rectal temperature of lambs Quadruplet lambs had significantly (P = 0.01) lower square root of glucose concentration than triplet-born lambs (Table 3). Birth rank affected square root of fructose concentrations such that triplet-born lambs had significantly (P < 0.01) lower concentrations than both
The rectal temperatures of triplet- and quadrupletborn lambs were significantly lower than that of twinborn lambs soon after birth (P < 0.01) and at 1 h (P = 0.02 and P < 0.01 respectively) (Table 2). In addition, at 1 h
Table 2 The effect of birth rank on lamb rectal temperature (°C) within 5 min of birth and at 1, 2 and 6 h after birth (mean ± SE) Lamb rectal temperatures Birth
Birth rank Singleton Twin Triplet Quadruplet
1h
2h
3h
6h
n
Mean
SE
n
Mean
SE
n
Mean
SE
n
Mean
SE
n
Mean
SE
10 34 33 15
39.16xy 39.29y 38.19x 37.98x
0.45 0.23 0.23 0.36
10 33 32 14
39.59yz 39.76z 38.38xy 37.44x
0.63 0.32 0.32 0.50
10 33 30 13
39.68y 39.68y 39.09y 37.83x
0.41 0.21 0.22 0.34
10 32 29 13
39.63y 39.48y 39.16y 37.95x
0.35 0.18 0.19 0.29
9 32 25 13
39.60y 39.52y 39.06y 38.24x
0.25 0.12 0.13 0.19
At 6 h triplets and twins differ at P = 0.05. Means within columns with differing superscripts are significantly (P < 0.05) different.
K.J. Stafford et al. / Livestock Science 111 (2007) 10–15
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Table 3 The effect of birth rank on the square root of glucose (mmol/L), fructose (mmol/L), lactate (mmol/L) and thyroxine (mmol/L) and the log10 of gammaglutamyl transferase (GGT, U/L) concentrations (mean ± SE) Glucose
Birth rank Singleton Twin Triplet Quadruplet
Fructose
Lactate
Thyroxine
GGT
n
Mean
SE
Mean
SE
Mean
SE
Mean
SE
Mean
SE
10 29 31 11
1.48xy 1.34xy 1.49y 1.18x
0.09 (2.26) a 0.05 (1.88) 0.05 (2.31) 0.09 (1.45)
1.37yz 1.34z 1.13x 1.16xy
0.06 (1.90) 0.04 (1.83) 0.03 (1.29) 0.06 (1.37)
2.17xy 2.15x 2.51y 2.22xy
0.16 (4.85) 0.09 (4.87) 0.09 (6.53) 0.14 (5.06)
10.80x 10.24x 8.36y 7.42y
0.63 (119.94) 0.35 (108.02) 0.34 (74.24) 0.57 (56.13)
1.72 1.73 1.74 1.77
0.04 (58.61) 0.03 (55.49) 0.03 (57.31) 0.04 (63.78)
Means within columns with differing superscripts are significantly different (P < 0.05). a Values in parentheses are the nontransformed means. The statistical analysis was carried out on transformed data.
twin- and singleton-born lambs and quadruplet-born lambs had lower concentrations than twin-born lambs. Triplet-born lambs had significantly (P = 0.03) higher square root of lactate concentrations than their twin-born counterparts. The square root of thyroxine concentrations of both triplet- and quadruplet-born lambs were significantly (P < 0.01) lower than that of both singletonand twin-born lambs. 3.4. Effect of birth order Birth order had no effect on the birthweight of twinor triplet-born lambs (Table 4). There was no effect of birth order in twins on any of the metabolic or hormone concentrations measured. Within triplet lambs, the lamb that was born first had significantly lower square root of fructose concentrations than both the second-born (P = 0.03) and last-born lamb (P = 0.01). 3.5. Effect of size within litter Within twin-born lambs, birth size had no effect on any of the metabolite or hormone concentrations
measured (Table 5). The heaviest triplet lamb had significantly (P = 0.03) lower square root of glucose concentrations than the middle liveweight lamb although, it did not differ significantly with its lightest counterpart. The heaviest triplet lamb had significantly lower square root of lactate (P = 0.04) concentrations compared to its lightest counterpart. The heaviest triplet lamb had significantly (P < 0.01) higher square root of T4 concentrations compared to its lightest counterpart and in triplets but not twins T4 concentrations were correlated (P = 0.06) with birthweight. In addition, the lightest triplet lambs had significantly (P < 0.01) higher log10 GGT concentrations than both its middle and heaviest counterparts. 3.6 PCV The mean PCV was significantly (P < 0.001) higher in twin lambs (46.63, SE 0.84) compared to both triplet- (41.31, SE 0.86) and quadruplet- (40.83, SE 1.23) born lambs. Singleton-born lambs did not differ from any of the other birth ranks (43.61, SE 1.80). Within full sets of twin- and triplet-born lambs
Table 4 The effect of birth order within each pregnancy rank on the birthweight (kg) and square root of glucose (mmol/L), fructose (mmol/L), lactate (mmol/L) and thyroxine (mmol/L) and the log10 of gamma-glutamyl transferase (GGT, U/L) concentrations (mean ± SE)
Twin First Second Triplet First Second Third
Birthweight
Glucose
Fructose
Lactate
n
Mean
SE
Mean
12 12
4.02 4.16
0.15 0.16
8 8 8
2.93 2.94 3.12
0.19 0.19 0.19
Thyroxine
GGT
SE
Mean
SE
Mean
SE
Mean
SE
Mean
SE
1.46 1.28
0.09 (2.23) a 0.09 (1.72)
1.41 1.26
0.06 (2.07) 0.07 (1.63)
2.31 2.10
0.15 (5.69) 0.16 (4.54)
10.76 10.16
0.47 (119.67) 0.52 (104.67)
1.75 1.70
0.03 (57.70) 0.04 (53.44)
1.50 1.44 1.45
0.08 (2.32) 0.08 (2.11) 0.08 (2.13)
1.01x 1.18y 1.22y
0.05 (1.01) 0.05 (1.41) 0.05 (1.51)
2.20 2.60 2.54
0.18 (4.94) 0.18 (7.10) 0.18 (6.75)
8.33 9.04 8.47
0.77 (74.63) 0.77 (85.88) 0.77 (74.50)
1.76 1.70 1.68
0.04 (61.88) 0.04 (52.75) 0.04 (60.63)
Means within columns in birth ranks with differing superscripts are significantly different (P < 0.05). a Values in parentheses are the nontransformed means. Statistical analysis was carried out on transformed data.
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K.J. Stafford et al. / Livestock Science 111 (2007) 10–15
Table 5 The effect of birth size within each pregnancy rank on the birthweight (kg) and square root of glucose (mmol/L), fructose (mmol/L), lactate (mmol/L) and thyroxine (mmol/L) and the log10 of gamma-glutamyl transferase (GGT, U/L) concentrations (mean ± SE)
Twin Big Small Triplet Small Middle Big
Birthweight
Glucose
Fructose
Lactate
n
Mean
SE
Mean
12 12
4.31y 3.86x
0.14 0.14
8 8 8
2.56x 2.96x 3.48y
0.14 0.14 0.14
Thyroxine
GGT
SE
Mean
SE
Mean
SE
Mean
SE
Mean
SE
1.31 1.44
0.09 (1.80) a 0.09 (2.18)
1.34 1.35
0.07 (1.85) 0.07 (1.88)
2.19 2.24
0.16 (5.03) 0.16 (5.29)
10.91 10.07
0.49 (103.42) 0.49 (122.17)
1.73 1.73
0.04 (55.75) 0.04 (55.75)
1.40xy 1.63y 1.35x
0.07 (2.03) 0.07 (2.66) 0.07 (1.87)
1.10 1.11 1.20
0.06 (1.23) 0.06 (1.25) 0.06 (1.46)
2.75y 2.48xy 2.12x
0.17 (7.92) 0.17 (6.26) 0.17 (7.93)
7.24x 8.38xy 10.23y
0.61 (54.25) 0.61 (72.25) 0.61 (108.50)
1.86y 1.64x 1.68x
0.03 (75.88) 0.03 (50.62) 0.03 (48.75)
Means within columns in birth ranks with differing superscripts are significantly different (P < 0.05). a Values in parentheses are the nontransformed means. Statistical analysis was carried out on transformed data.
PCV did not differ based on either birth size or birth order. 4. Discussion The triplet- and quadruplet-born lambs were significantly lighter, had lower rectal temperature at birth and 1 h later and lower fructose and thyroxine levels and higher lactate than twin or single lambs. These physical characteristics suggest that triplets experience placental insufficiency (see Barlow et al., 1987) which makes them susceptible to perinatal mortality. At 6 h triplet lambs had temperatures similar to those to twins which suggests that either their temperature had risen or those with low temperatures had died or been removed from the study allowing the mean temperature to rise. This suggestion is supported by the observation that when the rectal temperature at birth and 1 h of only those lambs which remained in the study at 6 h, are analysed there is no difference between twin and triplet lambs although the rectal temperature of quadruplet lambs was still lower. Quadruplets remained with a low mean temperature at 6 h. The difference in rectal temperature was due to size, as indicated by a lack of difference in temperature after correction for liveweight and not due to birth rank itself. Smaller lambs had lower temperatures as found by Dwyer and Morgan (2006). Light lambs are more likely to suffer hypothermia than heavier lambs (Moore et al., 1986). Light lambs have a greater surface area to body mass ratio which results in an increase body heat loss to the environment (Alexander, 1979) plus reduced body reserves, and probably poorer thermogenic capacity of brown adipose tissue (Budge et al., 2000). Plasma fructose levels are elevated in lambs immediately after birth (Daniels et al., 1974) and it is an important source of energy for the newborn but it is
quickly utilised forcing the lamb to use alternatives. Triplet lamb foetuses had lower fructose levels than twin foetuses in late gestation (Kenyon et al., in press) and in this study triplet lambs were born with low fructose levels, and thus less energy with which to survive until they ingest colostrum. However, it is well established that triplet lambs ingest less colostrum than single- and twin-born lambs and that there is a wide variation in intake in triplet lambs (Kenyon et al., 2005). Quadruplet-born lambs also had low fructose and glucose levels. Adequate glucose and fructose is also important in allowing lambs to increase their birth temperature. The low T4 levels seen in triplet and quadruplet lambs may result in a poorer ability to generate heat (Dwyer and Morgan, 2006) and further influence rectal temperature changes. Biochemical and physical characteristics did not differ according to birth order in twin or triplet lambs. Thus first- or last-born lambs did not appear to be stressed more at birth than each other or the middleborn lamb in triplets. There was little difference between the physical state of the larger and smaller twin-born lambs. However the largest triplet was significantly larger than the other two, had lower lactate levels than the smallest lamb, higher T4 levels and higher but not significantly higher fructose levels. Moreover, the results suggest that the larger triplet lambs had the physical characteristics at birth to promote survival whilst the smaller triplets and quadruplet lambs had physical characteristics which give them a much poorer chance of survival than larger triplets, twins or singleton-born lambs. These results suggest that increasing birthweight and/or providing conditions which limit heat loss in triplet-born lambs should improve survival rates. Pasture grazing conditions, and supplementation with concentrate feeds in late pregnancy have been shown
K.J. Stafford et al. / Livestock Science 111 (2007) 10–15
to improve the liveweight and metabolic status of ewes pregnant with triplets and the birthweight of triplet lambs (Morris and Kenyon, 2004). In addition mid-pregnancy shearing has been shown to increase birthweight and survival of triplet lambs (Kenyon et al., 2001). The provision of shelter for ewes with singleton and twin lambs also improved lamb survival rates to weaning (Egan et al., 1972). Therefore practical means of increasing triplet lamb birthweight and the provision of shelter require further investigation. 5. Conclusions Triplet, especially the smaller triplets, and quadruplet lambs born to Romney ewes in this trial were constitutionally less capable of surviving than twins or single-born lambs. The management techniques which would improve their survival by increasing birthweight and providing a more sheltered environment at birth require further investigation. Acknowledgements The authors wish to acknowledge the funding provided by Massey University and Meat and Wool New Zealand and support from the National Centre for Growth and Development. References Alexander, G., 1979. Cold thermogenesis. International Review of Physiology: Environmental Physiology 20, 43–155. Barlow, R.M., Gardiner, A.C., Angus, K.W., Gilmour, J.S., Mellor, D.J., Cuthbertson, J.C., Newlands, G., Thompson, R., 1987. Clinical, biochemical and pathological study of perinatal lambs in a commercial flock. The Veterinary Record 120, 357–362. Budge, H., Bispham, J., Dandrea, J., Evans, E., Heasman, L., Ingleton, P.M., Sullivan, C., Wilson, V., Stephenson, T., Symonds, M.E., 2000. Effect of maternal nutrition on brown adipose tissue and its prolactin receptor status in the fetal lamb. Pediatric Research 47, 781–786. Dalton, D.C., Knight, T.W., Johnson, D.L., 1980. Lamb survival in sheep breeds on New Zealand hill country. New Zealand Journal of Agricultural Research 23, 167–173. Daniels, L.B., Perkins, J.L., Krieder, D., Tugwell, D., Carpenter, D., 1974. Blood glucose and fructose in the newborn ruminant. Journal of Dairy Science 57, 1196–1200.
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