Increased capability for milk production has been associated with a decline in fertility of lactating cows. Nutritional requirements increase rapidly with milk production after calving and
Ž .
result in negative energy balance NEBAL . NEBAL delays the time of first ovulation through inhibition of LH pulse frequency and low levels of blood glucose, insulin and insulin-like growth
Ž .
factor-I IGF-I that collectively restrain estrogen production by dominant follicles. Up-regulation of LH pulses and peripheral IGF-I in association with the NEBAL nadir facilitates ovulation. NEBAL reduces serum progesterone concentrations and fertility. Diets high in crude protein support high milk yield, but are also associated with lower reproductive performance. High protein can result in elevated plasma urea concentrations that affect the uterine environment and fertility. Nutritional interactions resulting in poor fertility of high producing dairy cows include the antecedent effects of NEBAL and effects of high dietary protein.q2000 Elsevier Science B.V.
All rights reserved.
Keywords: Dairy cattle; Nutrition; Reproduction
1. Introduction
Increased genetic capability for milk production coupled with changes in nutritional management and larger herd size have been associated with a decline in fertility of
Ž .
lactating cows Fig. 1; Butler, 1998; Darwash et al., 1999 . Nutritional requirements shift abruptly at parturition as milk production rapidly increases and cows enter negative
Ž .
energy balance NEBAL . The severity and duration of NEBAL is primarily related to dry matter intake which, in turn, is related to body condition at calving. NEBAL during
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Ž .
E-mail address: [email protected] W.R. Butler .
0378-4320r00r$ - see front matterq2000 Elsevier Science B.V. All rights reserved.
Ž .
Ž .
Fig. 1. The inverse relationship between conception rate CR and annual milk production of Holstein dairy
Ž Ž . .
cows in New York Butler, 1998, by permission of J. Dairy Sci. 81 1998 2533–2539 .
the first 3–4 weeks postpartum is highly correlated with the days to first ovulation. Because a shorter delay to first ovulation is positively associated with conception rate later during the breeding period, the length of the postpartum interval to first ovulation represents an important interaction of energy status on reproductive performance.
High milk yield in cows is dependent on high levels of dietary protein as well as energy. Depending upon protein quantity and composition, serum concentrations of progesterone may be lowered, the uterine environment altered, and fertility decreased ŽButler, 1998 . Since metabolism and utilization of dietary protein depends on energy. availability, the effects of feeding high dietary protein superimposed on the preceding effects of NEBAL represents another important interaction of nutrition on reproductive performance in dairy cows. A comprehensive review of nutritional effects on ovulation
Ž .
and fertility in ruminants is recently available O’Callaghan and Boland, 1999 .
2. Nutrition and first ovulation in lactating dairy cows
Parturition results in an abrupt shift in the metabolic demands from nutrient accrual Žbody reserves and fetal mass to rapid mobilization of lipid and protein stores in.
Ž .
support of the sudden onset of high milk production Bauman and Currie, 1980 . In dairy cows the rapid increase in energy requirements at the onset of lactation results in NEBAL that begins a few days before calving and usually reaches its most negative
Ž . Ž .
level nadir about 2 weeks later Butler and Smith, 1989; Bell, 1995 . The timing of the Ž
NEBAL nadir has been implicated in the timing of first ovulation Beam and Butler,
. Ž
1999; Butler, 2000 that occurs about 30 days postpartum range of 17–42 days; Butler .
follicular wave and formation of a large dominant follicle during NEBAL does not appear to be a limitation for first ovulation. However, three outcomes of follicular
Ž . Ž .
development have been described Beam and Butler, 1997 : 1 Ovulation of the first
Ž . Ž .
dominant follicle 16–20 days postpartum ; 2 Non-ovulation of the first dominant Ž .
follicle followed by turnover and a new follicular wave. 3 The dominant follicle fails to ovulate and becomes cystic. The development of non-ovulatory dominant or cystic follicles prolongs the interval for first ovulation to 40 or 50 days postpartum.
Ovulation of a dominant follicle during early lactation is dependent on the re-estab-lishment of pulsatile LH secretion conducive to preovulatory follicular growth and
Ž .
estradiol production Butler, 2000 . The NEBAL that develops spontaneously in dairy cows represents a physiological state of undernutrition which impairs LH secretion and
Ž .
deters ovulation as detailed in a previous review Jolly et al., 1995 . From another recent
Ž .
review Beam and Butler, 1999 , the frequency of LH pulses was significantly lower during the first follicular wave postpartum in cows that developed a non-ovulatory dominant follicle as compared to those in which the dominant follicle continued development to ovulation. This is consistent with the observation that follicles emerging after the NEBAL nadir, rather than before, exhibited greater growth and diameter,
Ž
enhanced estradiol production, and were more likely to ovulate Beam and Butler, .
1997 .
Low energy availability during NEBAL not only suppresses pulsatile LH secretion,
Ž .
but also reduces ovarian responsiveness to LH stimulation Butler, 2000 . Both plasma Ž
glucose and insulin are decreased in NEBAL cows Beam and Butler, 1999; Butler,
. Ž
2000 and insulin is known to stimulate bovine follicular cells in vitro Spicer et al.,
. Ž .
1993 and in vivo Simpson et al., 1994 . In addition, plasma levels of insulin-like Ž .
growth factor-I IGF-I are directly related to energy status and IGF-I is critical to
Ž .
ovarian follicular development Beam and Butler, 1999 . In postpartum dairy cows the levels of IGF-I were 40–50% higher during the first 2 weeks in cows in which the dominant follicle would ovulate as compared to levels in cows with non-ovulatory
Ž .
follicles Beam and Butler, 1997; 1998 . Furthermore, plasma estradiol concentrations
Ž .
develop-Ž .
Fig. 2. A schematic model describing dominant follicle development circles and function in relation to
Ž .
changing metabolic and reproductive hormones, and energy balance EB , during the first follicular wave
Ž).
postpartum in dairy cows. The first-wave follicle either ovulates or undergoes atresia. LH pulse frequency is modulated by the day of the EB nadir and, to a lesser extent, the level of EB. The large upward arrows
Ž .
indicate increased insulin-like growth factor-I IGF-I and insulin leading to improved responsiveness to LH
Ž . Ž
and greater estradiol E2 production by the dominant follicle Beam and Butler, 1999, by permission of J.
Ž . .
Reprod. Fertil., Suppl. 54 1999 411–424 .
Ž .
ment in heifers Cohick et al.,1996; Perks et al., 1999 . During the early NEBAL period, the ability of follicles to produce sufficient estradiol for ovulation seems to depend on the availability of insulin and IGF-I in serum and the changing energy balance profile. A model for control of follicular development in postpartum cows is presented in Fig. 2 ŽBeam and Butler, 1999 ..
Since the extent of NEBAL depends upon dietary energy intake relative to require-ments, nutritional strategies to minimize NEBAL are of great interest. Increasing dietary energy intake by feeding more concentrates has limitations due to problems with digestion, milk composition and health. Alternatively, increasing dietary energy density by increasing the lipid content could ameliorate the limitation of intake and better meet the energetic demands of lactation. The effects of supplemental fat in the diet of lactating cows on postpartum ovarian activity and reproductive performance have been
Ž .
mixed Staples et al., 1998 . Fat supplementation increases follicle diameter, but does not consistently advance first ovulation. However, most studies with supplemental fat reported some improvement in conception or pregnancy rates.
3. Relationship of NEBAL to fertility
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tion is well documented Butler, 2000 . Minimizing the interval to first ovulation provides ample time for completion of multiple ovarian cycles prior to insemination,
Ž .
which in turn improves conception rate Butler and Smith, 1989 .
Another important link between NEBAL and fertility may be the carryover effects on blood progesterone concentrations. Progesterone in the peripheral circulation increases
Ž
during the first two or three postpartum ovulatory cycles Villa-Godoy et al., 1988; .
Spicer et al., 1990; Staples et al., 1990 and the rate of the increase in progesterone Ž
levels is reduced or moderated by NEBAL early postpartum Villa-Godoy et al., 1988; .
Spicer et al., 1990 . Cows with the most negative energy status during the first 9 days postpartum still had decreased serum progesterone levels during their third estrus cycles ŽVilla-Godoy et al., 1988 corresponding to the start of the breeding period. The ability. to produce and maintain optimum progesterone concentrations is important for fertility
Ž .
due to the effects of progesterone from one cycle to the next Folman et al., 1990 and Ž
since plasma progesterone was higher in pregnant than in non-pregnant cows Butler et .
al., 1996 .
The ‘‘memory’’ by which NEBAL early in the postpartum period translates into Ž . reduced progesterone production two months later has not been established. Britt 1992 hypothesized that ovarian follicles are detrimentally affected by exposure to NEBAL during their early growth and development and that ovulation of affected follicles would lead to lower progesterone secretion. This hypothesis may well explain the pattern of serum progesterone concentrations in lactating cows, however, the effects of dietary intake on progesterone clearance must also be considered. In sheep, high dietary energy
Ž
intake increases metabolic clearance of progesterone from blood by the liver Parr et al., .
1993 . Plasma progesterone concentrations were about 25% lower in heifers fed a high-energy diet as compared to those fed a low-energy diet, presumably as a result of
Ž .
increased clearance Nolan et al., 1998 . In lactating cows high dietary protein may also
Ž .
increase metabolic clearance rate of progesterone Westwood et al., 1998 . During early lactation total dietary intake in dairy cows increases two-fold by the beginning of the
Ž .
breeding period Bauman and Currie, 1980 . During the breeding period any increase in
Ž .
4. Dietary protein intake and reproductive performance
Dietary strategies for meeting the nutritional requirements of high producing dairy cows have been adjusted in response to genetic gains in milk yield. Diets high in crude
Ž .
protein 17% to 19% are typically fed during early lactation to both stimulate and support high milk production, however, high protein diets have been associated with
Ž .
reduced reproductive performance Butler, 1998; Westwood et al., 1998 . From previous
Ž .
reviews Butler, 1998; Westwood et al., 1998 , feeding high dietary protein does not appear to have a strong impact on the re-initiation of ovulatory activity in postpartum cows. In contrast, evidence has accumulated suggesting that reduced concentrations of plasma progesterone during the early breeding period may be a consequence of the
Ž
metabolic demands of high milk yield NEBAL and high dietary protein intake .
combined .
Successful embryo development depends upon the nature of the uterine environment. The uterine luminal milieu is dynamic and exhibits marked differences between the stages of the estrous cycle as a consequence of ovarian steroidal regulation of endome-trial secretion. Intake of high protein diets by lactating cows has been shown to alter the pH and the concentrations of other ions in uterine secretions, but only during the luteal phase and not at estrus. Uterine pH was also affected in heifers fed excess rumen
Ž .
degradable protein and was associated with reduced fertility Butler, 1998 .
The intake of high dietary protein can result in elevated blood concentrations of ammonia, urea, or both, depending upon the balance of protein fractions present in the rumen and the availability of fermentable carbohydrates. Increased plasma or milk urea
Ž nitrogen concentrations are highly correlated with decreased fertility in cows Butler,
.
1998; Westwood et al., 1998; Wittwer et al., 1999 . Plasma urea is inversely related to uterine luminal pH and sequential measurements in lactating cows have demonstrated that uterine pH is dynamically attuned to changes in plasma urea with a time lag of
Ž .
several hours Fig. 3 from Butler, 1998 . As a result of feeding diets high in crude protein, increased plasma urea concentrations may interfere with the normal inductive actions of progesterone on the microenvironment of the uterus and, thereby, cause
Ž .
suboptimal conditions for support of embryo development Butler, 2000 .
In vitro studies of bovine endometrial cell cultures have shown that urea alters both the pH gradient across the polarized cells and increases secretion of prostaglandin F2a
Ž .
that may interfere with embryo development and viability Butler, 1998 . Embryo quality and development was reduced in lactating cows fed excess rumen degradable
Ž .
protein Butler, 1998 , but embryo transfer and superovulation experiments in beef Ž .
heifers found no detrimental effect of high dietary crude protein urea on embryo
Ž .
viability, fertilization rate, or embryo quality Gath et al., 1999 . Since the energy balance status of the cattle in the various studies was different, the effects of high dietary protein in lactating cows may exacerbate metabolic or hormonal mediated processes that would result in impaired embryo development. For example, the long-term effect of NEBAL might be to impair the health of preovulatory oocytes and follicles and reduce
Ž .
Ž . Ž .
Fig. 3. The time course of inverse changes in plasma urea or urea nitrogen PUN and uterine pH open bars
Ž .
in a lactating cow cow 5776 . Feeding occurred at the times indicated by arrows during the 40-h period of
Ž Ž . .
study Butler, 1998, by permission of J. Dairy Sci. 81 1998 2533–2539 .
metabolism that may impact embryo developmental processes should further aid our understanding of poor fertility in high producing dairy cows.
In conclusion, the interactions of nutrition on reproductive performance in dairy cattle involve the most important dietary components, energy and protein, and their adequacy relative to requirements for high milk yield. The observed decline in fertility may be attributed to the combined effects of a uterine environment that is dependent on progesterone, but has been rendered suboptimal for embryo development by antecedent effects of NEBAL and may be further compromised by the effects of urea resulting from
Ž .
intake of high dietary protein Butler, 2000 .
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