Supplementation of Merino ewes with cholecalciferol in late pregnancy improves the vitamin D status of ewes and lambs at birth but is not correlated with an improvement in immune function in lambs
A. Lockwood A D , A. Currie A , S. Hancock A , S. Broomfield A , S. Liu B , V. Scanlan A , G. A. Kearney C and A. N. Thompson AA School of Veterinary and Life Sciences, Murdoch University, Murdoch, WA 6150, Australia.
B School of Animal Biology, University of Western Australia, Crawley, WA 6009, Australia.
C 36 Payne Road, Hamilton, Vic. 3300, Australia.
D Corresponding author. Email: A.Lockwood@murdoch.edu.au
Animal Production Science 56(4) 757-766 https://doi.org/10.1071/AN15085
Submitted: 12 February 2015 Accepted: 22 October 2015 Published: 18 February 2016
Abstract
Functional deficiencies of the immune system are known to predispose human and animal neonates to death. Thus, immune competency may be a significant factor influencing the mortality of lambs. Vitamin D has been recognised to improve immune function and is transferred across the placenta. This study tested the hypotheses that (1) supplementation of Merino ewes with cholecalciferol during late pregnancy will increase the concentrations of vitamin D in the ewe and lamb at birth and (2) supplementation of Merino ewes with cholecalciferol during late pregnancy is correlated with an increase in innate phagocytic and adaptive antibody immune responses in the lamb. Merino ewes (n = 53) were injected intramuscularly with 1 × 106 IU cholecalciferol at Days 113 and 141 of pregnancy. A control group (n = 58) consisted of ewes receiving no additional nutritional treatments. The vitamin D status of ewes and lambs was assessed up until 1 month post-lambing. Lamb immune function was assessed by analysing the functional capacity of phagocytes, and the plasma IgG and anti-tetanus-toxoid antibody concentrations between birth and weaning. Maternal supplementation with cholecalciferol increased the plasma 25(OH)D concentrations of both ewes (137 vs 79 nmol/L; P < 0.001) and lambs (49 vs 24 nmol/L; P < 0.001) at birth compared with the controls. Supplementation with cholecalciferol had no significant effect on the phagocytic capacity of monocytes or polymorphonuclear leukocytes, the concentration of IgG in the colostrum or plasma of lambs, or the vaccine-specific antibody response against tetanus toxoid. Overall, the results support our first hypothesis, but suggest that maternal supplementation with 1 × 106 IU cholecalciferol does not improve innate, passive or adaptive immune function in lambs.
Additional keywords: lamb survival, immunity.
References
Abu-Amer Y, Bar-Shavit Z (1993) Impaired bone barrow-derived macrophage differentiation in vitamin D deficiency. Cellular Immunology 151, 356–368.| Impaired bone barrow-derived macrophage differentiation in vitamin D deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXmt1Cqurk%3D&md5=018491ff1fda9a41e1cf6b4f9c676134CAS | 8402942PubMed |
Adams DB, Anderson BH, Lynch JJ, Munro RK (1997) The effect of dexamethasone on immunological memory to tetanus toxoid in sheep. Veterinary Immunology and Immunopathology 60, 89–95.
| The effect of dexamethasone on immunological memory to tetanus toxoid in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvFGqu7k%3D&md5=1e41193397fa9194b9008f1797b35432CAS | 9533269PubMed |
Al-Sabbagh TA, Swanson LV, Thompson JM (1995) The effect of ewe body condition at lambing on colostral immunoglobulin G concentration and lamb performance. Journal of Animal Science 73, 2860–2864.
Bernadina WE, van Leeuwen MAW, Hendrikx WML, Ruitenberg EJ (1991) Serum opsonic activity and neutrophil phagocytic capacity of newborn lambs before and 24–36 h after colostrum uptake. Veterinary Immunology and Immunopathology 29, 127–138.
| Serum opsonic activity and neutrophil phagocytic capacity of newborn lambs before and 24–36 h after colostrum uptake.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38%2Fls1CktQ%3D%3D&md5=e175276cbd6359842f17d716f64fe2e2CAS | 1949575PubMed |
Borel P, Caillaud D, Cano NJ (2015) Vitamin D bioavailability: state of the art. Critical Reviews in Food Science and Nutrition 55, 1193–1205.
| Vitamin D bioavailability: state of the art.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFKjurbE&md5=a5acaa3c7bf0d603de42f9e11950748fCAS | 24915331PubMed |
Cashman KD, Seamans KM, Lucey AJ, Stöcklin E, Weber P, Kiely M, Hill TR (2012) Relative effectiveness of oral 25-hydroxyvitamin D3 and vitamin D3 in raising wintertime serum 25-hydroxyvitamin D in older adults. The American Journal of Clinical Nutrition 95, 1350–1356.
| Relative effectiveness of oral 25-hydroxyvitamin D3 and vitamin D3 in raising wintertime serum 25-hydroxyvitamin D in older adults.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnslWkurk%3D&md5=3297767153fafa2c335600293c362e8fCAS | 22552038PubMed |
Chniter M, Hammadi M, Khorchani T, Sassi MB (2013) Aspects of neonatal physiology have an influence on lambs’ early growth and survival in prolific D’man sheep. Small Ruminant Research 111, 162–170.
| Aspects of neonatal physiology have an influence on lambs’ early growth and survival in prolific D’man sheep.Crossref | GoogleScholarGoogle Scholar |
Dennis SM (1974) Perinatal lamb mortality in Western Australia 4. Neonatal infections. Australian Veterinary Journal 50, 511–514.
| Perinatal lamb mortality in Western Australia 4. Neonatal infections.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2M%2FptVSmtQ%3D%3D&md5=18dbdc9b682f44ed3b1229ed6a2dd949CAS | 4447537PubMed |
Dwyer CM (2008) The welfare of the neonatal lamb. Small Ruminant Research 76, 31–41.
| The welfare of the neonatal lamb.Crossref | GoogleScholarGoogle Scholar |
Firth MA, Shewen PE, Hodgins DC (2005) Passive and active components of neonatal innate immune defenses. Animal Health Research Reviews 6, 143–158.
| Passive and active components of neonatal innate immune defenses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktFWhsr4%3D&md5=df6fdcf915e60d8658a105e8da245d5eCAS | 16583779PubMed |
Fowler DG, Wilkins JF (1984) Diagnosis of pregnancy and number of foetuses in sheep by real-time ultrasonic imaging. I. Effects of number of foetuses, stage of gestation, operator and breed of ewe on accuracy of diagnosis. Livestock Production Science 11, 437–450.
| Diagnosis of pregnancy and number of foetuses in sheep by real-time ultrasonic imaging. I. Effects of number of foetuses, stage of gestation, operator and breed of ewe on accuracy of diagnosis.Crossref | GoogleScholarGoogle Scholar |
Freer M, Moore AD, Donnelly JR (1997) GRAZPLAN: decision support systems for Australian grazing enterprises: II. The animal biology model for feed intake, production and reproduction and the GrazFeed DSS. Agricultural Systems 54, 77–126.
| GRAZPLAN: decision support systems for Australian grazing enterprises: II. The animal biology model for feed intake, production and reproduction and the GrazFeed DSS.Crossref | GoogleScholarGoogle Scholar |
Futata EA, Fusaro AE, de Brito CA, Sato MN (2012) The neonatal immune system: immunomodulation of infections in early life. Expert Review of Anti-Infective Therapy 10, 289–298.
| The neonatal immune system: immunomodulation of infections in early life.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjs1Cmu7o%3D&md5=fe1d9d32eeee2953de15bfa40cfe5f5eCAS | 22397563PubMed |
Garvy BA (2004) Host defense against pulmonary infection in neonates. Clinical and Applied Immunology Reviews 4, 205–223.
| Host defense against pulmonary infection in neonates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhslSksbc%3D&md5=6703d37e047ddcd99d261028731c5dd3CAS |
Gezmish O, Black M (2013) Vitamin D deficiency in early life and the potential programming of cardiovascular disease in adulthood. Journal of Cardiovascular Translational Research 6, 588–603.
| Vitamin D deficiency in early life and the potential programming of cardiovascular disease in adulthood.Crossref | GoogleScholarGoogle Scholar | 23719723PubMed |
Gilbert RP, Gaskins CT, Hillers JK, Parker CF, McGuire TC (1988) Genetic and environmental factors affecting immunoglobulin G1 concentrations in ewe colostrum and lamb serum. Journal of Animal Science 66, 855–863.
Gokce E, Erdogan HM (2009) An epidemiological study on neonatal lamb health. Veteriner fakultesi dergisi 15, 225–236.
Gokce E, Atakisi O, Kirmizigul AH, Unver A (2014) Passive immunity in lambs: serum lactoferrin concentrations as a predictor of IgG concentration and its relation to health status from birth to 12 weeks of life. Small Ruminant Research 116, 219–228.
| Passive immunity in lambs: serum lactoferrin concentrations as a predictor of IgG concentration and its relation to health status from birth to 12 weeks of life.Crossref | GoogleScholarGoogle Scholar |
Grayson R, Hewison M (2011) Vitamin D and human pregnancy. Fetal and Maternal Medicine Review 22, 67–90.
| Vitamin D and human pregnancy.Crossref | GoogleScholarGoogle Scholar |
Hallwirth U, Pomberger G, Zaknun D, Szepfalusi Z, Horcher E, Pollak A, Roth E, Spittler A (2002) Monocyte phagocytosis as a reliable parameter for predicting early-onset sepsis in very low birthweight infants. Early Human Development 67, 1–9.
| Monocyte phagocytosis as a reliable parameter for predicting early-onset sepsis in very low birthweight infants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVWmsLg%3D&md5=da51ae66ec2389ce2ce6a882c053f7d6CAS | 11893430PubMed |
Hashemi M, Hashemi M, Zamiri MJ, Safdarian M (2008) Effects of nutritional level during late pregnancy on colostral production and blood immunoglobulin levels of Karakul ewes and their lambs. Small Ruminant Research 75, 204–209.
| Effects of nutritional level during late pregnancy on colostral production and blood immunoglobulin levels of Karakul ewes and their lambs.Crossref | GoogleScholarGoogle Scholar |
Hawken PAR, Williman M, Milton J, Kelly R, Nowak R, Blache D (2012) Nutritional supplementation during the last week of gestation increased the volume and reduced the viscosity of colostrum produced by twin bearing ewes selected for nervous temperament. Small Ruminant Research 105, 308–314.
| Nutritional supplementation during the last week of gestation increased the volume and reduced the viscosity of colostrum produced by twin bearing ewes selected for nervous temperament.Crossref | GoogleScholarGoogle Scholar |
Hinch GN, Brien F (2014) Lamb survival in Australian flocks: a review. Animal Production Science 54, 656–666.
| Lamb survival in Australian flocks: a review.Crossref | GoogleScholarGoogle Scholar |
Holick MF (2009) Vitamin D status: measurement, interpretation, and clinical application. Annals of Epidemiology 19, 73–78.
| Vitamin D status: measurement, interpretation, and clinical application.Crossref | GoogleScholarGoogle Scholar | 18329892PubMed |
Hollis BW, Roos BA, Draper HH, Lambert PW (1981) Vitamin D and its metabolites in human and bovine milk. The Journal of Nutrition 111, 1240–1248.
Hughes KL, Haughey KG, Hartley WJ (1971) Perinatal lamb mortality: infections occurring among lambs dying after parturition. Australian Veterinary Journal 47, 472–476.
| Perinatal lamb mortality: infections occurring among lambs dying after parturition.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE38%2Fls1SksA%3D%3D&md5=1826e57e63c3d4d12a098c4e271399c7CAS | 5001538PubMed |
Jefferies B (1961) Body condition scoring and its use in management. Tasmanian Journal of Agriculture 32, 19–21.
Jones G (2008) Pharmacokinetics of vitamin D toxicity. The American Journal of Clinical Nutrition 88, 582S–586S.
Konowalchuk JD, Rieger AM, Kiemele MD, Ayres DC (2013) Modulation of weanling pig cellular immunity in response to diet supplementation with 25-hydroxyvitamin D(3). Veterinary Immunology and Immunopathology 155, 57–66.
| Modulation of weanling pig cellular immunity in response to diet supplementation with 25-hydroxyvitamin D(3).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVKqs7nJ&md5=fcc70303aa954b211d3ed6e8cf8a93bcCAS | 23810417PubMed |
Kovacs CS (2013) Maternal vitamin D deficiency: fetal and neonatal implications. Seminars in Fetal & Neonatal Medicine 18, 129–135.
| Maternal vitamin D deficiency: fetal and neonatal implications.Crossref | GoogleScholarGoogle Scholar |
Lang PO, Samaras N, Samaras D, Aspinall R (2013) How important is vitamin D in preventing infections? Osteoporosis International 24, 1537–1553.
| How important is vitamin D in preventing infections?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtlWgsbY%3D&md5=27089d5587d8528496a6747c45977455CAS | 23160915PubMed |
Lapillonne A (2010) Vitamin D deficiency during pregnancy may impair maternal and fetal outcomes. Medical Hypotheses 74, 71–75.
| Vitamin D deficiency during pregnancy may impair maternal and fetal outcomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFSgsr7O&md5=ff2dcfe54e3b9feb802a9bb3e0971d54CAS | 19692182PubMed |
Loste A, Ramos JJ, Fernández A, Ferrer LM, Lacasta D, Verde MT, Marca MC, Ortín A (2008) Effect of colostrum treated by heat on immunological parameters in newborn lambs. Livestock Science 117, 176–183.
| Effect of colostrum treated by heat on immunological parameters in newborn lambs.Crossref | GoogleScholarGoogle Scholar |
Mellor DJ, Stafford KJ (2004) Animal welfare implications of neonatal mortality and morbidity in farm animals. The Veterinary Journal (1997) 168, 118–133.
Menge C, Neufeld B, Hirt W, Schmeer N, Bauerfeind R, Baljer G, Wieler LH (1998) Compensation of preliminary blood phagocyte immaturity in the newborn calf. Veterinary Immunology and Immunopathology 62, 309–321.
| Compensation of preliminary blood phagocyte immaturity in the newborn calf.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtVKqsb4%3D&md5=1b7dd94c753c4899e0d5edb99ec8b796CAS | 9646436PubMed |
Miller DR, Blache D, Jackson RB, Downie EF, Roche JR (2010) Metabolic maturity at birth and neonate lamb survival: association among maternal factors, litter size, lamb birth weight, and plasma metabolic and endocrine factors on survival and behavior. Journal of Animal Science 88, 581–593.
| Metabolic maturity at birth and neonate lamb survival: association among maternal factors, litter size, lamb birth weight, and plasma metabolic and endocrine factors on survival and behavior.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktVOqt7o%3D&md5=724c6e32fca956edd5eda697463f0085CAS | 19897628PubMed |
Oldham CM, Thompson AN, Ferguson MB, Gordon DJ, Kearney GA, Paganoni BL (2011) The birthweight and survival of Merino lambs can be predicted from the profile of liveweight change of their mothers during pregnancy. Animal Production Science 51, 776–783.
| The birthweight and survival of Merino lambs can be predicted from the profile of liveweight change of their mothers during pregnancy.Crossref | GoogleScholarGoogle Scholar |
Paganoni BL, Ferguson MB, Kearney GA, Thompson AN (2014) Increasing weight gain during pregnancy results in similar increases in lamb birthweights and weaning weights in Merino and non-Merino ewes regardless of sire type. Animal Production Science 54, 727–735.
| Increasing weight gain during pregnancy results in similar increases in lamb birthweights and weaning weights in Merino and non-Merino ewes regardless of sire type.Crossref | GoogleScholarGoogle Scholar |
Parkin J, Cohen B (2001) An overview of the immune system. Lancet 357, 1777–1789.
| An overview of the immune system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1Khsrc%3D&md5=a2d9d59a01e8c7a495aa1c7b16f03f31CAS | 11403834PubMed |
Prosser A, Hibbert J, Strunk T, Kok CH, Simmer K, Richmond P, Burgner D, Currie A (2013) Phagocytosis of neonatal pathogens by peripheral blood neutrophils and monocytes from newborn preterm and term infants. Pediatric Research 74, 503–510.
| Phagocytosis of neonatal pathogens by peripheral blood neutrophils and monocytes from newborn preterm and term infants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslGnt77N&md5=a41fb2b66cfa1be2d4e1e1f3a96b02d0CAS | 23999070PubMed |
Rad M, Movassaghi AR, Sharifi K, Naseri Z, Seifi HA (2011) Two outbreaks of Pasteurella multocida septicemia in neonatal lambs. Comparative Clinical Pathology 20, 57–59.
| Two outbreaks of Pasteurella multocida septicemia in neonatal lambs.Crossref | GoogleScholarGoogle Scholar |
Rosales Nieto CA, Ferguson MB, Macleay CA, Briegel JR, Martin GB, Thompson AN (2013) Selection for superior growth advances the onset of puberty and increases reproductive performance in ewe lambs. Animal 7, 990–997.
| Selection for superior growth advances the onset of puberty and increases reproductive performance in ewe lambs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntFWmtLc%3D&md5=ff23f8f83a74b3127bfa6ee4c1bb10b1CAS | 23394163PubMed |
Roth DE (2011) Vitamin D supplementation during pregnancy: safety considerations in the design and interpretation of clinical trials. Journal of Perinatology 31, 449–459.
| Vitamin D supplementation during pregnancy: safety considerations in the design and interpretation of clinical trials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotlektr4%3D&md5=29ad6d48ecdc6d67b12e3889f3dfe209CAS | 21252966PubMed |
Smith BS, Wright H, Brown KG (1987) Effect of vitamin D supplementation during pregnancy on the vitamin D status of ewes and their lambs. The Veterinary Record 120, 199–201.
| Effect of vitamin D supplementation during pregnancy on the vitamin D status of ewes and their lambs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhvFGisLs%3D&md5=8c128e65d408f324d285c9dba31acb0dCAS | 3033871PubMed |
Stafford KJ, Kenyon PR, Morris ST, West DM (2007) The physical state and metabolic status of lambs of different birth rank soon after birth. Livestock Science 111, 10–15.
| The physical state and metabolic status of lambs of different birth rank soon after birth.Crossref | GoogleScholarGoogle Scholar |
Swanson TJ, Hammer CJ, Luther JS, Carlson DB, Taylor JB, Redmer DA, Neville TL, Reed JJ, Reynolds LP, Caton JS, Vonnahme KA (2008) Effects of gestational plane of nutrition and selenium supplementation on mammary development and colostrum quality in pregnant ewe lambs. Journal of Animal Science 86, 2415–2423.
| Effects of gestational plane of nutrition and selenium supplementation on mammary development and colostrum quality in pregnant ewe lambs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFansbvN&md5=8c873637f57b6f050f73e53cc25dcbe0CAS | 18441080PubMed |
Thorne-Lyman A, Fawzi WW (2012) Vitamin D during pregnancy and maternal, neonatal and infant health outcomes: a systematic review and meta-analysis. Paediatric and Perinatal Epidemiology 26, 75–90.
| Vitamin D during pregnancy and maternal, neonatal and infant health outcomes: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 22742603PubMed |
Tosi MF (2005) Innate immune responses to infection. The Journal of Allergy and Clinical Immunology 116, 241–249.
| Innate immune responses to infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntVCru74%3D&md5=aaa4f4c3a4b8b60c2e2728824dfcec51CAS | 16083775PubMed |
Vieth R (1999) Vitamin D supplementation, 25-hydroxyvitamin D concentrations, and safety. The American Journal of Clinical Nutrition 69, 842–856.
Whyte MP, Haddad JG, Walters DD, Stamp TCB (1979) Vitamin D bioavailability: serum 25-hydroxyvitamin D levels in man after oral, subcutaneous, intramuscular, and intravenous vitamin D administration. The Journal of Clinical Endocrinology and Metabolism 48, 906–911.
| Vitamin D bioavailability: serum 25-hydroxyvitamin D levels in man after oral, subcutaneous, intramuscular, and intravenous vitamin D administration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXks1alt7s%3D&md5=a473410c0936fc07446c606528a17e25CAS | 447796PubMed |
Yılmaz ÖT, Kaşıkçı G, Gündüz MC (2011) Benefits of pregnant sheep immunostimulation with Corynebacterium cutis on post-partum and early newborn’s life IgG levels, stillbirth rate and lamb’s weight. Small Ruminant Research 97, 146–151.
| Benefits of pregnant sheep immunostimulation with Corynebacterium cutis on post-partum and early newborn’s life IgG levels, stillbirth rate and lamb’s weight.Crossref | GoogleScholarGoogle Scholar |