- Email: [email protected]
Biological control of lactation length
ELSEVIER
Livestock Production
Science 50 (1997) l-3
Biological control of lactation length C.H. Knight
*
Hannah Research Institute, Ayr kX6 SHL, UK
Keywords:
Extended lactation;
Bovine; Mammary
development;
Mammary
1. Introduction The first session of the Workshop deals with the concept of Extended Lactation. In this introduction, I shall briefly consider the merits and demerits of extended lactation as an alternative to intensive production before summarising some aspects of the biological control of lactation length. Why contemplate extended lactation? To answer this question, it is pertinent to consider the origins of the present-day intensive system. From a UK perspective the first driving force was the need for increased home production brought about by the two World Wars; very considerable effort was expended in the 1930s and 1940s to increase milk production. The second factor was the advent, in the early 1950s of artificial insemination and associated selective breeding programmes. By the time of Wood’s classic paper on mathematical modelling of yield curves (Wood, 1969) the intensive concept of maximising peak daily output and minimising calving interval was totally accepted. It had evolved from the 1930s onward to meet the immediate priority of food scarcity and the associated long term goal of genetic improvement. A better question might be, is the intensive sys-
* Tel.: +44 1292 476013; fax: [email protected]
+44
1292 678797; e-mail:
involution
tern still the most appropriate? One priority has certainly changed; for the developed world, food scarcity is not an issue, so it is the efficiency of production coupled with the consumer’s demand for improved welfare that drives current thinking. Genetic improvement continues to be a major goal, but the advent of multiple ovulation embryo transfer technology and the promise of selected sex offspring provides an opportunity for divorcing milk production from generation of replacement stock (assuming a new, specialist, industry could emerge to attend to the latter). In fact, what were once advantages are now handicaps. In Europe, we have learnt to deal with surplus milk, but are now faced with the additional problem of surplus calves. Both are products of intensive dairying. The goal of genetic improvement has undoubtedly been achieved, but may have introduced further problems. The typical UK dairy cow of the 1930s was producing little more than 2000 l/yr (Holmes, 1981), whereas the modem well-fed Holstein can yield five times this amount. Very high daily yields cause general (and widespread) concern about metabolic diseases, and lead to the specific problem of drying off late lactation cows which might still be yielding 20 l/d or more. Perhaps the most serious indictment of current practice, however, is the fact that so many cows are discarded after just one or two lactations. Lifetime productivity has been almost totally disregarded because of the usefulness and popularity of 305 d yield statistics.
0301-6226/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved. PIf SO301-6226(97)00067-5
2
C.H. Knight/Liuestock
Production Science 50 (1997) 1-3
So, the time is right to consider other strategies. What would happen if lactation could be maintained, without rebreeding, for the whole adult lifetime of the cow? Mathematical modelling has shown that this entirely hypothetical scenario, which we have called persistent lactation, would have a very favourable economic outcome (Knight and Mainland, 1995). Extremely long lactations (adult lifetime was approximately 6 years in this model) are not yet a realistic option, but very many cows are quite capable of lactating for longer than 10 months. So, the first two papers in this session will consider the practicalities and economics of extended lactation cycles of 15 to 18 months duration, firstly under European conditions (Bertilsson et al., 1997) and secondly in the USA where diets are more energy dense and recombinant growth hormone (bST) is used to increase daily yield. The American study (Van Amburgh et al., 1997) also includes animals managed for persistent lactation as just described.
2. Discussion Lactation length can be increased in two main ways, either by shifting the whole curve upwards (enhanced yield), or by changing the shape of the curve to reduce the rate of decline in yield after peak lactation (enhanced persistency). The effect of generations of selective breeding and the main effect of bST treatment has been to increase yield, not persistency. Unfortunately, little is known about biological controls on lactation persistency, particularly in ruminants. In rats and mice, the simple expedient of litter swopping to maintain a strong suckling stimulus can extend lactation long beyond its normal duration, an effect that appears to be mediated by prolactin (Flint et al., 1984). Prolactin is much less influential in ruminant lactation (Plaut et al., 19871, although a role in lactation persistency has never been totally ruled out. Oxytocin treatment has been shown to increase lactation persistency slightly in cows (Nostrand et al., 19911, but the mechanism is not known. However, enhanced milk removal will reduce the effect of the feedback inhibitor of lactation (FIL; Wilde et al., 1995), a locally-active autocrine inhibitory protein present in milk. This protein is responsible for fine-tuning milk secretion in
response to changing demand, elicited by more or less frequent suckling or milking. If oxytocin is acting through FIL, then similar effects would be expected from milking thrice daily rather than twice daily throughout lactation. Data presented in this volume (Bertilsson et al., 1997) suggest that this is not so. Studies of mammary involution during declining lactation in ruminants have shown that yield reduction is associated with loss of cells, rather than dedifferentiation (Knight and Peaker, 1984). Changes in cell population size are a function of cell proliferation (low in lactating tissue) and cell death or apoptosis. The latter is an area of intense investigation currently, as reviewed in the third main paper of this session (Wilde et al., 1997). Factors which regulate apoptosis are only just beginning to be identified, but one of the insulin-like growth factor binding proteins (IGFBP-5) has been implicated in several tissues, including mammary gland. A recent hypothesis (Flint and Knight, 1997; Guenette, 1997) proposes coordinated control by the hormones prolactin and GH, acting through IGF-I and IGFBP-5. GH stimulates IGF-I release, which maintains cell integrity and function. Prolactin suppresses IGFBP-5 production, thus enabling the action of IGF-I. In the absence of GH, IGF-I falls and apoptosis occurs. In the absence of prolactin, IGFBP-5 is increased and prevents the action of IGF-I so, once again, apoptosis results. Maintenance of lactation thus requires the combined presence of both prolactin and GH. In ruminants, lactational involution can be at least partially reversed by bST administration (Baldi et al., 1997; Knight et al., 1990; Politis et al., 1990). Given alone, bST has a small but positive effect on lactation persistency (Van Amburgh et al., 1997). In one study in goats, bST given in combination with more frequent milking produced a dramatic increase, such that yield was totally maintained at its peak value until the experiment terminated in week 40 of lactation (Knight et al., 1990). A similar experiment has been conducted recently in cows (Speicher et al., 1994). Persistency was not specifically analysed, but examination of the data suggests a small positive effect of bST irrespective of milking frequency. The most striking feature was the greater persistency of heifers compared to mature cows. This is a well known but poorly understood phenomenon.
C.H. Knight/
Liresfock
Production
3. Conclusion Writing with the benefits of hindsight, having listened to the workshop speakers, I am struck by increasing divergence between European and US scenarios. There is little doubt in my mind that American dairymen will gradually switch to longer lactations over the next decade or so, largely as a result of the introduction of bST. They will do so primarily for economic reasons, but their cows will enjoy welfare benefits as a result. In Europe the future is less clear. It is unlikely that bST will be used, at least in the foreseeable future, because of supposed adverse welfare implications for the cow. If in 5 or 10 years time it becomes apparent that bST has contributed positively to the welfare of US dairy cows through extension of calving intervals, will Europe then be able to catch up?
References Baldi, A., Chiofalo, V., Savoini, G., Greco, R., Polidori, F., Politis, I., 1997. Changes in plasmin, plasminogen and plasminogen activator activities in milk of late lactating ewes: effects of bovine somatotrophin (bST) treatment. Livest. Prod. Sci., in press (this volume). Bertilsson, J., Svennersten-Sjaunja, K., Wiktorsson, H., Berglund, B., Ratnayake, G., 1997. Optimising lactation cycles for the existing high-yielding dairy cow. A European perspective. Livest. Prod. Sci., in press (this volume). Flint, D.J., Knight, C.H., 1997. Interactions of prolactin and growth hormone (GH) in the regulation of mammary gland function and epithelial cell survival. J. Mammary Gland Biol. Neoplasia 2, in press. Flint, D.J., Clegg, R.A., Knight, C.H., 1984. Effects of prolactin, progesterone and ovariectomy on metabolic activities and insulin receptors in the mammary gland and adipose tissue during extended lactation in the rat. J. Endocrinol. 102, 231236.
Science 50 (19971 1-3
3
Guenette, S., 1997. The role of growth
factors and proteases in mammary gland involution. In: Wilde, C.J., Peaker, M. (Eds.), Hannah Symposium. Biological Signalling and the Mammary Gland. Hannah Research Institute, Ayr, in press. Holmes, W., 1981. Animal husbandry, 1931-1980. In: Cooke, G.W. (Ed.), Agricultural Research, 1931-1981. Agricultural Research Council. London, pp. 289-309. Knight, C.H., Mainland, D., 1995. Physiology of milk production: how can it be manipulated. Cattle Practice 3, 169- 173. Knight. C.H.. Peaker, M., 1984. Mammary development and regression during lactation in goats in relation to milk secretion. Quart. J. Exp. Physiol. 69, 331-338. Knight, C.H., Fowler, P.A., Wilde, C.J., 1990. Galactopoietic and mammogenic effects of long-term treatment with bovine growth hormone and thrice daily milking in goats. J. Endocrinol. 127. 129- 138. Nostrand, S.D.. Galton, D.M., Erb, H.N., Bauman, DE., 1991. Effects of daily exogenous oxytocin on lactation milk yield and composition. J. Dairy Sci. 74, 21 19-2127. Plaut, K., Bauman, D.E., Agergaard, N.. Akers. R.M., 1987. Effect of exogenous prolactin administration on lactational performance of dairy cows. Domest. Anim. Endocrinol. 4, 279-290. Politis, I.. Block, E., Turner, J.D.. 1990. Effect of somatotropin on the plasminogen and plasmin system in the mammary gland: proposed mechanism of action for somatotropin on the mammary gland. J. Dairy Sci. 73, 1494-1499. Speicher, J.A., Tucker, H.A., Ashley. R.W.. Stanisiewski, E.P., Boucher, J.F.. Sniffen, C.J., 1994. Production responses of cows to recombinantly derived bovine somatotropin and to frequency of milking. J. Dairy Sci. 77, 2509-2517. Van Amburgh, M., Galton, D., Bauman, D., Everett, R.W.. 1997. Management and economics of extended calving intervals with use of bST. Livest. Prod. Sci., in press (this volume). Wilde. C.J., Addey. C.V.P., Boddy, L.M., Peaker, M.. 1995. Autocrine regulation of milk secretion by a protein in milk. Biochem. J. 305, 51-58. Wilde. C.J., Quarrie. L.H., Blatchford, D.R.. Tonner, E., Flint, D.J., 1997. Mammary apoptosis. Livest. Prod. Sci,, in press (this volume). Wood. P.D.P., 1969. Factors affecting the shape of the lactation curve in cattle. Anim. Prod. 11. 307-316.
Livestock Production
Science 50 (1997) l-3
Biological control of lactation length C.H. Knight
*
Hannah Research Institute, Ayr kX6 SHL, UK
Keywords:
Extended lactation;
Bovine; Mammary
development;
Mammary
1. Introduction The first session of the Workshop deals with the concept of Extended Lactation. In this introduction, I shall briefly consider the merits and demerits of extended lactation as an alternative to intensive production before summarising some aspects of the biological control of lactation length. Why contemplate extended lactation? To answer this question, it is pertinent to consider the origins of the present-day intensive system. From a UK perspective the first driving force was the need for increased home production brought about by the two World Wars; very considerable effort was expended in the 1930s and 1940s to increase milk production. The second factor was the advent, in the early 1950s of artificial insemination and associated selective breeding programmes. By the time of Wood’s classic paper on mathematical modelling of yield curves (Wood, 1969) the intensive concept of maximising peak daily output and minimising calving interval was totally accepted. It had evolved from the 1930s onward to meet the immediate priority of food scarcity and the associated long term goal of genetic improvement. A better question might be, is the intensive sys-
* Tel.: +44 1292 476013; fax: [email protected]
+44
1292 678797; e-mail:
involution
tern still the most appropriate? One priority has certainly changed; for the developed world, food scarcity is not an issue, so it is the efficiency of production coupled with the consumer’s demand for improved welfare that drives current thinking. Genetic improvement continues to be a major goal, but the advent of multiple ovulation embryo transfer technology and the promise of selected sex offspring provides an opportunity for divorcing milk production from generation of replacement stock (assuming a new, specialist, industry could emerge to attend to the latter). In fact, what were once advantages are now handicaps. In Europe, we have learnt to deal with surplus milk, but are now faced with the additional problem of surplus calves. Both are products of intensive dairying. The goal of genetic improvement has undoubtedly been achieved, but may have introduced further problems. The typical UK dairy cow of the 1930s was producing little more than 2000 l/yr (Holmes, 1981), whereas the modem well-fed Holstein can yield five times this amount. Very high daily yields cause general (and widespread) concern about metabolic diseases, and lead to the specific problem of drying off late lactation cows which might still be yielding 20 l/d or more. Perhaps the most serious indictment of current practice, however, is the fact that so many cows are discarded after just one or two lactations. Lifetime productivity has been almost totally disregarded because of the usefulness and popularity of 305 d yield statistics.
0301-6226/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved. PIf SO301-6226(97)00067-5
2
C.H. Knight/Liuestock
Production Science 50 (1997) 1-3
So, the time is right to consider other strategies. What would happen if lactation could be maintained, without rebreeding, for the whole adult lifetime of the cow? Mathematical modelling has shown that this entirely hypothetical scenario, which we have called persistent lactation, would have a very favourable economic outcome (Knight and Mainland, 1995). Extremely long lactations (adult lifetime was approximately 6 years in this model) are not yet a realistic option, but very many cows are quite capable of lactating for longer than 10 months. So, the first two papers in this session will consider the practicalities and economics of extended lactation cycles of 15 to 18 months duration, firstly under European conditions (Bertilsson et al., 1997) and secondly in the USA where diets are more energy dense and recombinant growth hormone (bST) is used to increase daily yield. The American study (Van Amburgh et al., 1997) also includes animals managed for persistent lactation as just described.
2. Discussion Lactation length can be increased in two main ways, either by shifting the whole curve upwards (enhanced yield), or by changing the shape of the curve to reduce the rate of decline in yield after peak lactation (enhanced persistency). The effect of generations of selective breeding and the main effect of bST treatment has been to increase yield, not persistency. Unfortunately, little is known about biological controls on lactation persistency, particularly in ruminants. In rats and mice, the simple expedient of litter swopping to maintain a strong suckling stimulus can extend lactation long beyond its normal duration, an effect that appears to be mediated by prolactin (Flint et al., 1984). Prolactin is much less influential in ruminant lactation (Plaut et al., 19871, although a role in lactation persistency has never been totally ruled out. Oxytocin treatment has been shown to increase lactation persistency slightly in cows (Nostrand et al., 19911, but the mechanism is not known. However, enhanced milk removal will reduce the effect of the feedback inhibitor of lactation (FIL; Wilde et al., 1995), a locally-active autocrine inhibitory protein present in milk. This protein is responsible for fine-tuning milk secretion in
response to changing demand, elicited by more or less frequent suckling or milking. If oxytocin is acting through FIL, then similar effects would be expected from milking thrice daily rather than twice daily throughout lactation. Data presented in this volume (Bertilsson et al., 1997) suggest that this is not so. Studies of mammary involution during declining lactation in ruminants have shown that yield reduction is associated with loss of cells, rather than dedifferentiation (Knight and Peaker, 1984). Changes in cell population size are a function of cell proliferation (low in lactating tissue) and cell death or apoptosis. The latter is an area of intense investigation currently, as reviewed in the third main paper of this session (Wilde et al., 1997). Factors which regulate apoptosis are only just beginning to be identified, but one of the insulin-like growth factor binding proteins (IGFBP-5) has been implicated in several tissues, including mammary gland. A recent hypothesis (Flint and Knight, 1997; Guenette, 1997) proposes coordinated control by the hormones prolactin and GH, acting through IGF-I and IGFBP-5. GH stimulates IGF-I release, which maintains cell integrity and function. Prolactin suppresses IGFBP-5 production, thus enabling the action of IGF-I. In the absence of GH, IGF-I falls and apoptosis occurs. In the absence of prolactin, IGFBP-5 is increased and prevents the action of IGF-I so, once again, apoptosis results. Maintenance of lactation thus requires the combined presence of both prolactin and GH. In ruminants, lactational involution can be at least partially reversed by bST administration (Baldi et al., 1997; Knight et al., 1990; Politis et al., 1990). Given alone, bST has a small but positive effect on lactation persistency (Van Amburgh et al., 1997). In one study in goats, bST given in combination with more frequent milking produced a dramatic increase, such that yield was totally maintained at its peak value until the experiment terminated in week 40 of lactation (Knight et al., 1990). A similar experiment has been conducted recently in cows (Speicher et al., 1994). Persistency was not specifically analysed, but examination of the data suggests a small positive effect of bST irrespective of milking frequency. The most striking feature was the greater persistency of heifers compared to mature cows. This is a well known but poorly understood phenomenon.
C.H. Knight/
Liresfock
Production
3. Conclusion Writing with the benefits of hindsight, having listened to the workshop speakers, I am struck by increasing divergence between European and US scenarios. There is little doubt in my mind that American dairymen will gradually switch to longer lactations over the next decade or so, largely as a result of the introduction of bST. They will do so primarily for economic reasons, but their cows will enjoy welfare benefits as a result. In Europe the future is less clear. It is unlikely that bST will be used, at least in the foreseeable future, because of supposed adverse welfare implications for the cow. If in 5 or 10 years time it becomes apparent that bST has contributed positively to the welfare of US dairy cows through extension of calving intervals, will Europe then be able to catch up?
References Baldi, A., Chiofalo, V., Savoini, G., Greco, R., Polidori, F., Politis, I., 1997. Changes in plasmin, plasminogen and plasminogen activator activities in milk of late lactating ewes: effects of bovine somatotrophin (bST) treatment. Livest. Prod. Sci., in press (this volume). Bertilsson, J., Svennersten-Sjaunja, K., Wiktorsson, H., Berglund, B., Ratnayake, G., 1997. Optimising lactation cycles for the existing high-yielding dairy cow. A European perspective. Livest. Prod. Sci., in press (this volume). Flint, D.J., Knight, C.H., 1997. Interactions of prolactin and growth hormone (GH) in the regulation of mammary gland function and epithelial cell survival. J. Mammary Gland Biol. Neoplasia 2, in press. Flint, D.J., Clegg, R.A., Knight, C.H., 1984. Effects of prolactin, progesterone and ovariectomy on metabolic activities and insulin receptors in the mammary gland and adipose tissue during extended lactation in the rat. J. Endocrinol. 102, 231236.
Science 50 (19971 1-3
3
Guenette, S., 1997. The role of growth
factors and proteases in mammary gland involution. In: Wilde, C.J., Peaker, M. (Eds.), Hannah Symposium. Biological Signalling and the Mammary Gland. Hannah Research Institute, Ayr, in press. Holmes, W., 1981. Animal husbandry, 1931-1980. In: Cooke, G.W. (Ed.), Agricultural Research, 1931-1981. Agricultural Research Council. London, pp. 289-309. Knight, C.H., Mainland, D., 1995. Physiology of milk production: how can it be manipulated. Cattle Practice 3, 169- 173. Knight. C.H.. Peaker, M., 1984. Mammary development and regression during lactation in goats in relation to milk secretion. Quart. J. Exp. Physiol. 69, 331-338. Knight, C.H., Fowler, P.A., Wilde, C.J., 1990. Galactopoietic and mammogenic effects of long-term treatment with bovine growth hormone and thrice daily milking in goats. J. Endocrinol. 127. 129- 138. Nostrand, S.D.. Galton, D.M., Erb, H.N., Bauman, DE., 1991. Effects of daily exogenous oxytocin on lactation milk yield and composition. J. Dairy Sci. 74, 21 19-2127. Plaut, K., Bauman, D.E., Agergaard, N.. Akers. R.M., 1987. Effect of exogenous prolactin administration on lactational performance of dairy cows. Domest. Anim. Endocrinol. 4, 279-290. Politis, I.. Block, E., Turner, J.D.. 1990. Effect of somatotropin on the plasminogen and plasmin system in the mammary gland: proposed mechanism of action for somatotropin on the mammary gland. J. Dairy Sci. 73, 1494-1499. Speicher, J.A., Tucker, H.A., Ashley. R.W.. Stanisiewski, E.P., Boucher, J.F.. Sniffen, C.J., 1994. Production responses of cows to recombinantly derived bovine somatotropin and to frequency of milking. J. Dairy Sci. 77, 2509-2517. Van Amburgh, M., Galton, D., Bauman, D., Everett, R.W.. 1997. Management and economics of extended calving intervals with use of bST. Livest. Prod. Sci., in press (this volume). Wilde. C.J., Addey. C.V.P., Boddy, L.M., Peaker, M.. 1995. Autocrine regulation of milk secretion by a protein in milk. Biochem. J. 305, 51-58. Wilde. C.J., Quarrie. L.H., Blatchford, D.R.. Tonner, E., Flint, D.J., 1997. Mammary apoptosis. Livest. Prod. Sci,, in press (this volume). Wood. P.D.P., 1969. Factors affecting the shape of the lactation curve in cattle. Anim. Prod. 11. 307-316.