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Impaired reproduction in heat-stressed cattle:
basic and applied aspects
D. Wolfenson
), Z. Roth, R. Meidan
Department of Animal Science, Faculty of Agriculture, The Hebrew UniÕersity, RehoÕot 76100, Israel
Abstract
Ž .
Summer heat stress HS is a major contributing factor in low fertility in lactating dairy cows in hot environments. Although modern cooling systems are used in dairy farms, fertility remains low. This review summarizes the ways in which the functioning of various parts of the reproductive system of cows exposed to HS is impaired. The dominance of the large follicle is suppressed during HS, and the steroidogenic capacity of theca and granulosa cells is compro-mised. Progesterone secretion by luteal cells is lowered during summer, and in cows subjected to chronic HS, this is also reflected in lower plasma progesterone concentration. HS has been reported to lower plasma concentration of LH and to increase that of FSH; the latter was associated with a drastic reduction in plasma concentration of inhibin. HS impairs oocyte quality and embryo development, and increases embryo mortality. High temperatures compromise endometrial function and alter its secretory activity, which may lead to termination of pregnancy. In addition to the immediate effects, delayed effects of HS have been detected as well. Among them, altered follicular dynamics, suppressed production of follicular steroids, and low quality of oocytes and developed embryos. These may explain the low fertility of cattle during the cool autumn months. Hormonal treatments improve low summer fertility to some extent but not sufficiently for it to equal winter fertility. A limiting factor is the inability of the high-yielding dairy cow to maintain normothermia. A hormonal manipulation protocol, which induces timed insemination, has been found to improve pregnancy rate and to reduce the number of days open during the summer.q2000 Elsevier Science B.V. All rights reserved.
Keywords: Hyperthermia; Cattle; Fertility; Reproduction
)Corresponding author. Tel.:q972-8-948-9393; fax:q972-8-946-5763.
Ž .
E-mail address: wolf@agri.huji.ac.il D. Wolfenson .
0378-4320r00r$ - see front matterq2000 Elsevier Science B.V. All rights reserved. Ž .
1. Introduction
Ž .
Summer heat stress HS is a major contributing factor in low fertility among
lactating dairy cows. It is a worldwide problem, which inflicts heavy economic losses and affects about 60% of the world cattle population. Conception rates drop from about 40–60% in cooler months to 10–20% or lower in summer, depending on the severity of
Ž .
the thermal stress Cavestany et al., 1985 . The most prominent characteristic of summer infertility is its multifactorial nature, since hyperthermia directly alters and impairs the
cellular functions of various partsrtissues of the reproductive system. Furthermore,
exposure of cattle to thermal stress elicits indirect responses, which may also have an impact on reproductive processes. Such responses include redistribution of blood flow among body organs, reduction in food intake, respiratory alkalosis, etc. Although the impact of the various direct and indirect effects of HS on reproductive processes has never been quantified, it is believed that the direct effect of hyperthermia in impairing cellular functions is the predominant one. The substantial rise in milk yield in recent years has aggravated the low summer fertility syndrome, because of the concurrent rise in metabolic heat production. The various cooling procedures used on farms have not been able to improve fertility substantially, and the conception rate of lactating cows in the summer, even in farms equipped with cooling systems, is still pronouncedly below
Ž .
that in the winter Hansen, 1997 .
Traditionally, low summer fertility is associated mainly with the warm months of the
Ž .
year usually June, July, August and September in the northern hemisphere . However,
Ž .
fertility remains lower in autumn October and November , than in winter, although ambient temperatures drop and the cows are no longer exposed to HS. A delayed effect of summer HS on autumn fertility is evident, and it accounts for about one-third or more of the low summer fertility syndrome.
In the last decade, considerable efforts have been dedicated to shedding light on the HS-induced impairment of processes in the reproductive system, and of the functioning of various parts of it. Ultrasonography, cell culture, in vitro oocyte maturation and fertilization are among the means of achieving improved understanding of mechanisms by which thermal stress negatively influences bovine fertility. This review focuses basically on immediate and delayed effects of HS on follicular development, dynamics of follicular waves, steroidogenic capacity of theca and granulosa cells, corpus luteum
ŽCL development and function, and secretion of progesterone and gonadotrophins, and.
briefly reviews oocyte quality, embryonic development and uterine function under HS. In the second part of the review, several hormonal strategies are discussed, which aim to optimize reproductive functioning and to improve fertility of cattle under HS conditions.
2. Follicular dynamics
HS-induced alterations in follicular dynamics have been monitored by ultrasonogra-phy. Heat exposure of lactating cows during the entire estrous cycle induced a 50%
Ž .
increase in the number of large )10 mm follicles during the first follicular wave
ŽWolfenson et al., 1995 . A similar response was monitored during the follicular phase.
Ž .
Ž .
during days 17–21 of the cycle Wilson et al., 1998b . This response resulted from HS-induced reduction in the dominance of the large follicle, which permitted the growth of an additional large follicle, and it provides at least a partial explanation of the marked rise in twinning in cows calving during May–July in hot countries such as Saudi Arabia ŽRyan and Boland, 1991 , or of the 50% rise in the twinning rate of mature cows during.
Ž .
May–July in Israel Herd Book data . This rise is probably due to insemination of cows, which had double ovulations during the hot months of August and September.
Another sensitive indication of HS-induced attenuation of dominance is the lack of a decline in the number of medium-size follicles during the period of dominance of the
Ž . Ž .
first-wave Badinga et al., 1993 or preovulatory follicle Wolfenson et al., 1995 . Similarly, in a seasonal study in which follicular dynamics was studied in April, June,
Ž
August and November, a larger first-wave dominant follicle in April non-heat-stressed .
season was associated with an earlier regression of the largest subordinate follicle and a
Ž .
sharper decrease in the number of medium-size follicles Badinga et al., 1994 . A slower decline in size of the second-largest, subordinate follicle was also found in studies of
Ž .
acute HS in cows and heifers Roth et al., 1997; Wilson et al., 1998b .
HS-induced depression of dominance was also found to be associated with a 2–3-day Ž
earlier emergence of the second-wave dominantrpreovulatory follicle Wolfenson et al.,
.
1995 . This may have an important physiological significance, because earlier emer-gence of the preovulatory follicle may result in ovulation of older follicles. The duration of dominance of the preovulatory follicle was found to be negatively correlated with
Ž .
fertility of cattle Mihm et al., 1994 . It is worth noting, however, that the day of the cycle on which the second-wave dominant follicle was first detected did not differ
Ž .
between replicate months in a seasonal study Badinga et al., 1994 . Earlier emergence of the second follicular wave was also detected, in terms of number of medium-size
Ž .
follicles, in HS lactating cows Roth et al., 1997 . Emergence was noted a day earlier and the number of follicles declined 2 days later than in control cows. This was associated with the earlier appearance of a wider surge in plasma FSH concentration
ŽRoth, 1998 . Moreover, plasma FSH concentrations were also higher during the.
periovulatory period in HS cows; this rise in FSH was associated with a pronounced
Ž .
decrease in the concentration of immunoreactive inhibin in plasma Roth, 1998 . In agreement with these findings, a reduction of plasma inhibin concentration in summer
Ž .
was found in cyclic buffaloes in India Palta et al., 1997 and a tendency for reduction in Ž
plasma concentration of the hormone was also noted in HS cows Wolfenson et al., .
1995 . The latter findings suggest that depression of dominance during HS involves suppression of inhibin secretion by granulosa cells and subsequent alterations in FSH secretion.
Ž Conflicting findings on the effect of HS on the development of small follicles class
.
1; 2–5 mm are evident. A reduction in the number of small follicles was documented
Ž . Ž .
by Wolfenson et al. 1995 and Wilson et al. 1998a,b ; whereas an increase in the
Ž .
number of small follicles was found by Trout et al. 1998 . Discrepancies between studies could be related to differences in experimental design, or in the severity of the HS.
resulting in a number of changes in follicular growth. Among them, at least two Ž .
responses standout in their physiological importance: 1 development of a larger
number of large follicles probably increases the rate of double ovulation and hence of Ž .
twin calving; and 2 early emergence of the preovulatory follicle lengthens the
dominance period, and this has been shown to be associated with lower fertility in
Ž .
spontaneously cyclic dairy cows Bleach et al., 1998 or in heifers induced to ovulate
Ž .
persistent dominant follicles Mihm et al., 1994; Austin et al., 1999 .
3. Steroidogenic capacity
Earlier studies were inconsistent in their findings concerning plasma concentrations Ž
of estradiol under HS no change — Roman-Ponce et al., 1981; increase — Rosenberg .
et al., 1982; decrease — Gwazdauskas et al., 1981 . However, most recent studies indicated that plasma estradiol concentration was lowered during HS. Lactating cows
Ž
and dairy heifers that were heat-stressed during the second half of the cycle Wilson et
. Ž .
al., 1998a,b or during the entire cycle Roth, 1998 had a reduced preovulatory surge in plasma estradiol concentration. Likewise, plasma estradiol was lower during the first
Ž .
follicular wave in HS cows than in non-HS ones Wolfenson et al., 1995 , and a pronounced reduction in plasma estradiol was noted during the first follicular wave in
Ž .
HS cows in September, compared with those heat-stressed in July Badinga et al., 1993 . The difference between the two replicate months is the much longer period of exposure
Ž .
to daily HS in late summer September , which may severely impair follicular function.
Ž .
In contrast, a seasonal study Badinga et al., 1994 detected a higher and faster
Ž .
preovulatory rise of plasma estradiol concentration in August hottest month in Florida than in April, June or November.
The decreased steroidogenic capacity of follicles under HS involved a lower aro-matase activity in the granulosa cells and a lower estradiol concentration in the follicular fluid of dominant follicles on day 8 of the estrous cycle, in late vs. early summer ŽBadinga et al., 1993 . A seasonal study comparing first-wave dominant follicles on day.
Ž .
7 of the cycle Wolfenson et al., 1997 showed lower follicular fluid estradiol in summer than in winter. This decrease was due primarily to a drastic reduction of androstenedione
Ž 5 .
production by theca cells during the summer 4.1 vs. 1.1 ngr10 viable cells . Estradiol production by granulosa cells decreased in summer to about 50% of that in winter, but the difference was barely significant. Furthermore, the percentage of viable granulosa
Ž
cells in follicles collected in summer had fallen to 60% of its winter value Wolfenson .
and Meidan, unpublished data , contributing to the reduction in in vivo secretion of estradiol to the circulation. Reduced androstenedione production by theca cells was also found in cells incubated at high temperature in vitro, and in follicles collected in winter
Ž
from cows previously exposed to 3 days of acute HS in a hot chamber Wolfenson et al., .
1997 .
In an attempt to characterize the molecular events leading to the decrease in plasma
estradiol, the expression of mRNA encoding cytochrome P450 aromatase, cytochrome
P450 sidechain cleavage, 17a-hydroxylase, FSHr, and steroid acute regulatory protein
Ž .
by HS. 17a-Hydroxylase activity is rate-limiting in the biosynthesis of androgens, serving as the substrates for estradiol synthesis by the granulosa cells. The reason why theca cells are susceptible to HS is unclear; it may be related to the fact that theca cells differentiate earlier than granulosa cells.
4. The corpus luteum
The effects of HS on CL function have been examined mainly by measuring plasma concentrations of progesterone. This is an important measure because the hormone is delivered to the uterus via the circulation, to maintain pregnancy. However, plasma progesterone concentration depends not only on its rate of production by the CL, but also on the rate of secretion to the circulation; the latter depends on ovarian luteal blood
Ž .
flow, which was found to be lower by 30% in HS rabbits Lublin and Wolfenson, 1996 . Furthermore, possible adrenal release of progesterone, metabolism in the liver, haemodi-lution or haemoconcentration, the degree of hyperthermia, the type of heat exposure Žacute vs. chronic , the age of the cows, their stage of lactation, and the type of feeding. all contribute to the wide variation among findings on the observed effect of HS on
Ž .
plasma progesterone concentration Jonsson et al., 1997; Trout et al., 1998 . Earlier results were controversial: some show decreased plasma concentration of progesterone
Ž .
during HS Wise et al., 1988b; Wolfenson et al., 1988 , others report no change or
Ž .
increased concentration Thatcher and Collier, 1986; Wise et al., 1988a .
More recent works also vary in their findings on the effect of HS on plasma
Ž .
progesterone. Exposure of cows Trout et al., 1998; Wilson et al., 1998a or heifers
ŽWilson et al., 1998b to HS during the second half of the cycle has been reported to.
result in a rise in plasma progesterone concentration that was associated with delayed
Ž .
luteolysis. Roth 1998 reported no change in plasma progesterone in lactating cows exposed to direct solar radiation in summer. Contrary responses have also been
Ž .
recorded. Younas et al. 1993 found increased luteal progesterone secretion in cows
Ž .
exposed to fan cooling in summer. Howell et al. 1994 , in a seasonal study, showed a decrease in plasma progesterone concentration in cows in summer, which was not associated with any change in cross-sectional area of the CL or with the presence of
Ž .
luteal cavities. Another seasonal study Jonsson et al., 1997 found a lower concentration of plasma progesterone in cows in summer than in winter during the life of the second CL after calving, and the difference was not associated with any differences between seasons, in dry matter intake, body condition score or milk yield. The latter indicates that the decreased progesterone concentration in plasma was directly related to the heat load and not necessarily to HS-induced nutritional or metabolic changes. It has been suggested that plasma progesterone concentration decreased in cows subjected to chronic HS, typical of the natural summer environment, and rose in cows subjected to a more acute HS such as exposure to direct solar radiation or heat exposure in a hot
Ž .
chamber Howell et al., 1994 .
Evidence for direct suppression of progesterone production by high temperature has
Ž .
incubation at 388C, and cell viability was lower than that of cells collected from cows in winter. Also, luteal cells collected in winter and incubated at 408C produced 30% less progesterone than similar cells incubated at 388C. In order to differentiate between the
Ž .
effects of the season on progesterone production by small theca derived and large
Žgranulosa derived luteal cells, theca and granulosa cells obtained from first-wave.
dominant follicles from cows in summer and winter were luteinized in vitro for 9 days at
Ž . Ž .
388C in the presence of forskolin 10mM and insulin 2 mgrml; Sonego, 1995 . These
cells collected from follicles on day 6 of the estrous cycle in each season were similar, in terms of diameter, number of granulosa cells and viability of granulosa and theca cells. Progesterone production by granulosa-derived, large luteal cells was only slightly lower in summer than in winter, though the rate of increase in progesterone production was higher in winter than in summer. In contrast, progesterone production by theca-de-rived, small luteal cells, dropped markedly in summer to one-fifth of the corresponding winter value.
In summary, chronic exposure to summer HS suppressed progesterone production. This was evident in in vitro studies in which progesterone production by luteal cells obtained from cows in summer was lower than that by cells obtained in winter. Under certain physiological states, HS lowers plasma progesterone concentration. Inadequate progesterone secretion may have adverse effects during two physiological periods, before and after insemination. Low plasma progesterone concentration can cause aberrant follicular development, which leads to abnormal oocyte maturation in the
Ž .
ovulatory follicle and early embryo death Ahmad et al., 1995 . Low plasma proges-terone affects steroidogenesis in the dominant follicle and in the subsequently formed CL, and it also altered endometrial morphology and function in the subsequent cycle
ŽShaham-Albalancy et al., 1996a,b . Low plasma progesterone following AI may also.
contribute to increased embryo losses. However, the effectiveness of increasing post-in-semination plasma progesterone in improving the fertility of cattle is debatable:
Robin-Ž . Ž .
son et al. 1989 found a rise in fertility, whereas Breuel et al. 1990 found no effect.
5. Gonadotrophins
The effect of HS on secretion of gonadotrophins in cattle is poorly documented despite the important roles of LH and FSH in regulating follicular growth, ovulation,
and CL function. The available information regarding LHrFSH secretion is limited to
concentrations of these hormones in peripheral blood; there are no data on either GnRH
content of the hypothalamus or LHrFSH content of the pituitary under HS.
Plasma concentrations of tonic LH during the estrous cycle of HS cows have been
Ž .
reported, in earlier studies, to be unchanged Gwazdauskas et al., 1981 or increased ŽRoman-Ponce et al., 1981 . Similarly, the preovulatory surge of plasma LH concentra-.
Ž .
tion decreased in HS heifers Madan and Johnson, 1973 but not in HS cows
ŽGwazdauskas et al., 1981; Rosenberg et al., 1982 . Wise et al. 1988a reported a. Ž .
Ž .
fully functional CL Peters et al., 1994 . The pattern of tonic LH secretion also
Ž influenced the rate of growth and turnover of dominant follicles in cyclic cows Savio et
.
al., 1993 . The effects of HS on tonic LH as well as on GnRH-induced preovulatory surge concentrations were found to be dependent on the concentration of estradiol in
Ž .
plasma Gilad et al., 1993 . Chronic HS during summer decreased the mean and amplitude of tonic LH as well as of GnRH-induced preovulatory plasma LH concentra-tion surge in cows with low concentraconcentra-tions of plasma estradiol. In contrast, neither tonic LH concentration nor GnRH-induced LH concentration surge was altered in cows with high concentrations of plasma estradiol. Similar responses were recorded in cows
Ž .
acutely heat-stressed for 16 h in a hot chamber during the winter Gilad et al., 1993 . GnRH-induced plasma FSH surge was lower in lactating cows during both chronic exposure to HS in summer and an acute 16 h exposure to thermal stress in a hot
Ž . Ž .
chamber Gilad et al., 1993 . These reductions were evident as with LH only in cows
Ž .
with low concentrations of plasma estradiol. In contrast as discussed above , in HS cows that were not treated with GnRH, there was a pronounced increase in plasma concentrations in the FSH surge that preceded the second-wave dominant follicle, and in the preovulatory FSH surge that was associated with decreased plasma inhibin
concen-Ž .
trations Roth, 1998 . In agreement with the latter study, serum FSH concentrations and content of GnRH in the hypothalmus have been found higher in summer than in winter
Ž .
in primiparous sows Armstrong et al., 1986 . The reason for the discrepancy in
Ž .
responses to HS between cows treated with GnRH lower plasma FSH and intact cows Žhigher plasma FSH is unclear..
6. Delayed effects of HS
Autumn fertility of dairy cows is lower than in winter, although ambient temperatures drop and cows are no longer exposed to thermal stress. For example, in Florida, the
Ž .
autumn conception rate October–November of Holstein cattle was found to be around
Ž .
35–40%, compared with above 50% in winter January–March; Badinga et al., 1985 .
Ž .
Conception rates of high-yielding dairy cows in Israel Herd Book data, 1992–1997 drop from 45% in winter to around 20% during the summer, and to 23% and 29% in October and November, respectively. These figures clearly show a delayed influence of summer HS on autumn fertility.
Follicular dynamics was altered in lactating cows that had been heat-stressed by
Ž .
direct solar radiation during the preceding estrous cycle Roth et al., 1997 . During the
Ž .
first wave of the subsequent cycle, fewer medium-size class 2 follicles developed in previously HS cows than in the controls, and the rate of decline in their number was slower. Another study showed that cows heat-stressed for 7 days in a hot chamber had an increased proportion of small and large follicles just after the heat exposure ŽGuzeloglu, 1998 ..
Ž .
androstene-dione, which serves as substrate for estradiol synthesis by the granulosa cells. Impaired functioning of theca cells in the autumn may be due to previous exposure of the animals to HS in the preceding summer. In contrast, aromatase activity of granulosa cells in the autumn was unaffected by HS. The hypothesis that changes in follicular steroidogenesis in the autumn were due to a delayed effect of HS on follicular function was reinforced by a study in which cows were heat-stressed during days 2–6 of the cycle and
Ž
medium-size follicles were examined on day 3 of the subsequent cycle Roth et al., .
1997 . In previously HS cows, granulosa and theca cells obtained from medium follicles produced one-third and one-fourth of the quantities of estradiol and androstenedione, respectively, compared with non-HS cows. Collectively, the above results show im-paired steroidogenic capacity of follicles from cows previously subjected to HS.
Low autumn fertility could be related to a delayed effect of HS on oocyte function in
Ž .
cows previously heat-stressed during the summer. In a recent study Roth et al., 1999 ,
Ž .
follicles 3–8 mm were aspirated during four consecutive estrous cycles in the autumn from lactating cows previously subjected to summer HS. The percentage of grade I Žbest oocytes was low in the first cycle early autumn; 28% and rose later in cycles 3. Ž .
Ž .
and 4 late autumn; 55% . The percentage of eight-cell-stage embryos developed in vitro following oocyte maturation and activation, rose by 50% in late autumn compared with early autumn. Furthermore, enhanced removal of impaired follicles by frequent follicle
Ž .
aspiration days 4, 7, 11 and 15 of the cycle led to a more rapid emergence of healthy
Ž .
oocytes in the autumn Roth et al., 1999 .
7. Oocyte quality, embryonic development and uterine function
Various aspects of the effects of HS on oocyte quality and embryonic development Ž .
include the following: 1 the deleterious effects of heat exposure during different stages of oocyte maturation and early embryo development, on the impaired function of
Ž .
oocytes and embryos, in both in vitro and in vivo systems; 2 the increase in the heat Ž .
tolerance of the embryo with age; 3 the production of heat-shock proteins by the Ž . embryo, and their potential function in protecting the embryo during HS; and 4 the possible use of antioxidants to increase embryo resistance to thermal stress. Relevant Ž . aspects of the effect of HS on uterine environment and endometrial function include: 1 production of heat-shock proteins by the endometrium during HS, and its implications; Ž .2 reduced production of interferon-g by the conceptus; and 3 increased productionŽ .
and release of PGF2a from the endometrium during HS, and its implications for
pregnancy recognition and CL maintenance. The reader is referred to recent studies
ŽEdwards and Hansen, 1997; Rocha et al., 1998 and reviews that cover these subjects.
ŽThatcher and Collier, 1986; Thatcher and Hansen, 1992; Hansen, 1997; Hansen et al.,
. 1992; Zavi, 1994 .
8. Fertility studies
or severe hyperthermia, depending on HS intensity, milk yield and efficiency of the cooling system used. During the last two decades, new cooling systems have been introduced in dairy farms. They are based on wetting the cow with water to cool it directly by evaporation from the skin, or on evaporative cooling of the air surrounding
Ž
the cows under shades Bucklin et al., 1991; Berman and Wolfenson, 1992; Armstrong, .
1994; Huber, 1996 . Collectively, most studies show that such systems achieve some improvement of fertility in commercial farms, compared with non-cooled controls, but the improvement does not match winter fertility. The reason for this is the inability of the various cooling procedures totally to eliminate hyperthermia during the summer. Not surprisingly, however, complete elimination of HS by intensive and frequent use of the sprinkling and ventilation cooling system under experimental farm conditions was able
Ž
to restore the summer conception rate to that recorded in winter Wolfenson et al.,
. Ž .
1988 . The following describes hormonal and other treatment strategies that were tested during summer HS as means to improve fertility.
Administration of GnRH during early stages of estrus, timed to coincide with the endogenous LH surge, may induce an enhanced LH surge, and may also improve the synchronization of the time intervals between estrus, LH surge, ovulation and insemina-tion. Injection of 100mg of GnRH into lactating cows at detection of estrus during late
Ž
summer in Mississippi, increased their conception rate from 18% to 29% Ullah et al., .
1996 . The rise in fertility was suggested to be related to an increase in concentration of plasma progesterone during the first 30 days after AI. In agreement with this result, conception rate of lactating cows that were injected with GnRH at the first signs of standing estrus during summer and autumn months in Israel, increased by about 16.6%
Ž .
above that of untreated control cows Kaim et al., unpublished data .
Ž .
In contrast to the findings of Ullah et al. 1996 , two other studies did not show improvement of fertility following post-AI supplementation of progesterone: induction of an accessory CL by a single injection of 3000 IU of hCG on day 5 or 6 after insemination in summer in Florida, did not improve the fertility of heifers or lactating
Ž .
cows Schmitt et al., 1996 ; and exogenous supplementation of progesterone by insertion of a progesterone-containing CIDR into lactating cows on day 7 post-AI for 11 days in
Ž .
summer in Israel also failed to improve fertility Wolfenson et al., 1994 . Since post-AI treatment with progesterone has been shown to be effective in improving the fertility of
Ž .
non-HS cattle Robinson et al., 1989; Sianangama and Rajamahendran, 1992 , it has been suggested that the increases in progesterone in HS studies might have occurred after day 7, whereas most of the damage to the conceptus in severely HS cattle occurs
Ž .
between estrus and day 7 of pregnancy Putney et al., 1988; Ealy et al., 1993 .
Free radicals have been suggested to be partly responsible for the detrimental effect of elevated temperature on cellular membrane integrity, and for compromising the cellular function of steroidogenic tissues and embryos, since these have been found to be
Ž .
sensitive to free radical damage Hansen, 1997; Arechiga et al., 1998b . Administration
Ž . Ž
of the antioxidant, vitamin E 3000 IU at the time of AI, or injection of vitamin E 500
. Ž .
mg and selenium 50 mg at 30 days postpartum, had no beneficial effect on pregnancy
Ž .
rate during summer or winter in Florida Ealy et al., 1994; Arechiga et al., 1998b .
Ž .
Similarly, cows supplemented with b-carotene 400 mgrday starting 15 days or more
Ž .
A different approach that has been tested recently is the incorporation of the timed-AI program in the system of summer fertility management. Injection of GnRH induces a
programmed recruitment of an ovulatory follicle; 7 days later, a PGF2a injection
regresses the CL and permits final maturation of the ovulatory follicle; 48 h later, a Ž
second GnRH injection induces ovulation and 16 h later, cows are inseminated Burke et .
al., 1996; Pursley et al., 1998 . This program eliminates the need for estrus detection. Ž
The timed-AI program was tested during summer condition in Florida de la Sota et al., .
1998 . Overall pregnancy rate at 120 days postpartum was greater for treated than for
Ž .
control cows inseminated at estrus 27% and 16.5%, respectively , and the number of days open was less and the number of services per conception was greater for timed-AI than for control cows. The timed-AI protocol improved reproductive management, but it does not protect the embryo from the detrimental effects of high temperatures.
9. Conclusions
During the last decade, a considerable amount of information has been published regarding the impairment of the mechanisms of reproductive processes under HS conditions. Most components of the reproductive system have been found to be susceptible to HS. These include: the oocyte, granulosa and, particularly, theca cells within the preovulatory follicle; the developing embryo during early stages of develop-ment; the corpus luteum; the uterine endometrium; and the anterior pituitary. Studies on the delayed effect of HS show that, practically speaking, cows need to be cooled as efficiently as possible during the entire summer in order to raise summer fertility. Currently, summer fertility remains low and various hormonal treatments are limited in their ability to improve conception rate. The use of the timed-AI procedure improves pregnancy rate and reduces the number of days open.
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