Livestock Production Science 66 2000 121–131 www.elsevier.com locate livprodsci
Regulation of development by nutrition and by the somatotrophic and thyroid axes in the neonatal pig
a , b
a
I. Louveau , M.J. Dauncey , J. Le Dividich
a
´ INRA
, Unite Mixte de Recherches sur le Veau et le Porc, 35590 Saint Gilles, France
b
The Babraham Institute , Cambridge CB2 4AT, UK
Abstract
The neonatal period is a particularly critical stage during which the long-term development of the individual can be affected. The rapid somatic growth is accompanied by tremendous anatomical, physiological and chemical composition
changes. This period is also associated with dramatic changes in the endocrine system which plays a central role in the control of metabolism and growth. The review focuses primarily on the somatotrophic and thyroid axes. Changes in hormone
and binding protein concentrations in plasma, as well as receptor expression in target tissues, are considered. After birth, the ability of the neonate to express its growth potential is related to milk intake and milk quality. There are interactions between
nutrition, endocrine parameters and development. In addition to nutrients, colostrum and milk contain a large group of biologically active components such as enzymes, hormones, growth factors and immunological agents that may be involved
in the neonatal development. The possible role of milk-borne insulin-like growth factor-I IGF-I on body growth, the gastrointestinal tract and protein synthesis in neonates has been the subject of considerable investigation in the past ten years.
There is increasing evidence that milk-borne IGF-I significantly affects gastrointestinal growth and development. The effects of this factor on development of other tissues and organs are not so clear.
2000 Elsevier Science B.V. All rights
reserved.
Keywords : Nutrition; Hormone; Development; Pig; Neonate
1. Introduction hormonal regulation of growth and development in
the neonatal pig. The review concentrates on the Development of the neonate involves complex
roles played by the growth hormone GH–insulin- interactions between genetics, environment, nutrition
like growth factor IGF axis and thyroid hormones and hormone status. The aim of the present paper is
THs. The influence of nutrition on growth and to review the data concerning the nutritional and
development will also be considered. There is con- siderable interest in the function of milk-borne
growth factors, and it has often been hypothesised that they affect neonatal growth and development.
Attention is therefore focused on the potential sig-
Corresponding author. Tel.: 1 33-2-2348-5046; fax: 1 33-2-
nificance of milk-borne IGF-I in the growth and
2348-5080. E-mail address
: louveaust-gilles.rennes.inra.fr I. Louveau.
functional development of the neonatal pig.
0301-6226 00 – see front matter
2000 Elsevier Science B.V. All rights reserved. P I I : S 0 3 0 1 - 6 2 2 6 0 0 0 0 2 1 9 - 0
122 I
. Louveau et al. Livestock Production Science 66 2000 121 –131
2. Nutrition of the suckling piglet 3. Growth and development during suckling
Once suckling is established in the newborn, During the 2- to 4-week suckling period, piglets
nutrition and therefore growth are almost entirely from modern genotypes grow at the rate of about
dependent on colostrum and milk availability. This is 250–270 g day King et al., 1999. The precise rate is
2
attested by the strong relationship R 5 0.87–0.90 very variable and is dependent mainly on the availa-
between preweaning growth of piglets and sow’s bility of milk, with growth rate increasing by 0.33 g
milk output Noblet and Etienne, 1987. A complete for each additional gram increase in milk intake
description of sow’s colostrum and milk is provided Marion and Le Dividich, 1999, unpublished data.
in a recent review by Darragh and Moughan 1998. The rapid increase in body weight is associated
Briefly, compared with milk, colostrum has higher with marked changes in organ growth and body
crude protein and lower fat and lactose contents. The composition. Widdowson et al. 1976 first reported
level of protein is high 14–16 in the first that colostrum elicits dramatic growth of the gas-
colostrum, decreases to 6–7 24 h later and remains trointestinal tract, and especially of the small intes-
constant 5–6 thereafter. This decrease is related tine. Feeding the piglet ad libitum with colostrum
to the fall in immunoglobulins mainly IgG which during the first 36 h postnatally induces an 80
account for 80 of total protein in the first colos- increase in small intestinal weight Schober et al.,
trum, decreasing to 35 and 14 after 1 and 21 days 1990; Le Dividich et al., 1997b; this is caused by
of lactation, respectively Klobasa et al., 1987. Fat both a transient retention of colostral macromole-
accounts for 35–45 and 55–65 of the energy cules and an enhanced protein synthesis Burrin et
provided by colostrum and mature milk, respectively, al., 1992. The specific effects of colostrum on
depending on the fat composition of the sow’s diet. protein synthesis have been studied in gastrointesti-
In contrast, milk protein and lactose are only margi- nal and peripheral tissues. Tissue protein synthesis is
nally dependent on the composition of the sow’s higher in 7- than in 26-day-old piglets Davis et al.,
diet, and the amino acid composition of colostrum 1996. Marion et al. 1999 reported that feeding
and milk is remarkably constant. In addition, colos- stimulates whole-body protein synthesis: for exam-
trum and to a lesser extent milk contains a variety ple, in 7-day-old piglets, whole body protein syn-
of polypeptide growth factors including insulin, IGF thesis increased linearly with the level of metabolis-
and epidermal growth factor Grosvernor et al., able milk energy intake. The stimulatory effect of
1992. Concentrations of most of these factors are colostrum ingestion on protein synthesis is attributed
higher in colostrum than in milk Table 1. Both largely to the supply of macronutrients and to
colostrum and milk are extremely well utilised by the colostral growth factors Kelly, 1994. However,
piglet, with the apparent digestibility of energy and whereas it is clear that colostrum has an immediate
nitrogen both averaging 98.5 Marion and Le effect on growth of the small intestine, its mid-term
Dividich, 1999. and long-term effects are unclear.
Table 1 Concentrations mean6S.D. of insulin and insulin-like growth factors IGFs in sow’s colostrum and milk
Days following parturition 1
2 3
7–21
a
Insulin mUI ml 4116214
2636190 1336113
28617 59650
b
IGF-I ng ml 136623
72611 31617
2769.3 1162
b
IGF-II ng ml 291665
165618 77650
50614 1763
a
¨ Westrom et al. 1987.
b
Donovan et al. 1994.
I . Louveau et al. Livestock Production Science 66 2000 121 –131
123 Table 2
1991. The GHR was first purified, sequenced and
Proximate composition of suckled piglets from birth to 21 days of
cloned from rabbit liver Leung et al., 1987. Sub-
age
sequently, the cDNA for the GHR has been cloned in
Age days
several other species including pigs Cioffi et al.,
a a
b c
Birth 1
7 21
1990. GHR is a transmembrane protein encoded by nine exons. Receptors are highly expressed in liver
Moisture, 80.5
79.2 74.6
68.2
but are also found in many other tissues Louveau
Crude protein N 3 6.25, 10.7
12.4 15.9
14.9 Fat,
1.7 2.3
4.6 11.3
and Etherton, 1992; S¢rensen et al., 1992; Lee et al.,
Gross energy kcal g 0.84
0.93 1.36
2.06
1993. The GHR is able to associate with and
a
Le Dividich et al. 1997a.
activate the tyrosine kinase JAK2 that in turn
b
Marion and Le Dividich unpublished data.
activates a number of intracellular pathways Wojcik
c
Noblet and Etienne 1987.
and Postel-Vinay, 1999. In addition to the membrane-bound GHR, a
GHBP, which essentially corresponds to the extracel- Major body composition changes begin early in
lular domain of the GHR Leung et al., 1987, has the neonatal period Table 2. At 24 h postpartum,
been identified in the serum of many species includ- fat and protein percentages have both increased
ing pigs Davis et al., 1992. GHBP is derived from significantly, with the increase in body fat being
the same gene as GHR and is generated by mecha- especially marked. Fat percentage continues to in-
nisms that differ between species Bauman, 1995. crease throughout the first 3 weeks whereas protein
Little is known about the physiological role of this content remains nearly constant after 2 weeks of age.
GHBP. It has been shown to enhance the growth- Body fat is derived primarily from dietary fat and
promoting effects of GH in vivo probably by increas- hence accretion of both fat and protein are highly
ing the half-life of GH in the circulation. dependent on the intake of milk fat and protein.
Between birth and 7 days of age, the regression 4.1.2. IGF, IGF receptors IGFRs and IGF
equations relating accreted protein aP and fat aF binding proteins
IGFBPs to protein Pi and fat intake Fi are as follows: aP
IGF-I and IGF-II are M | 7500 single-chain poly-
r 2
g day 5 0.96Pi g day 2 0.48 R 5 0.99; and aF peptides that retain 70 amino acid homology with
2
g day 5 0.58Fi g day 2 6.8 R 5 0.93 Marion each other and 50 homology with proinsulin. The
and Le Dividich, 1999, unpublished data. During the IGF amino acid sequence is highly conserved across
3-week suckling period, Noblet and Etienne 1987 species, showing 100 identity between human,
found that 88 and 54 of milk protein and fat intake, porcine and bovine IGF-I Tavakkol et al., 1988.
respectively, was retained in the body. While the growth-promoting properties of IGF-I are
well established, the biological significance of IGF-II postnatally is less clear. However, primary cultures
4. Hormonal control of neonatal growth of skeletal muscle satellite cells, the postnatal
