- Email: [email protected]
Factors Affecting the Reproductive Performance of the Weaned Sow
0749-0720/92 $0.00
SWINE REPRODUCTION
+ .20
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW Glen W. Almond, DVM, MSc, PhD
The majority of sows return to estrus within 3 to 14 days following weaning. 24.35 Sows that fail to resume estrous cyclicity are either culled from the herd or return to estrus at highly variable times. 9,27 The average interval from weaning to first detected estrus increases during the summer and is substantially longer in primiparous sows than in multiparous SOWS. 12,31 The weaning-to-estrus interval (WEI) often exceeds 30 days during the summer in sows affected with the anestrous condition. 9 Factors influencing WEI include boar exposure,30,56 lactation length,12,55 nutrition during and after lactation,17,36,54 stress, environmental temperature,52 and photoperiod. 28 ,51 Although seasonal influences are inherent to swine reproduction, they have only recently been regarded as significant factors affecting the reproductive efficiency of swine herds. This article is intended to illustrate the interactions between the physiologic events and the factors affecting WEI. In addition, the negative role of season on the WEI, pregnancy loss, abortion, farrowing rates, and irregular returns to estrus after breeding is discussed. ECONOMIC SIGNIFICANCE OF THE WEI AND POSTWEANING ANESTRUS
Most reports have indicated that reproductive failure was the most common cause of culling sows from commercial swine farms.9,27 Postweaning anestrus is cited as a common cause of reproductive failure, thereby contributing to excessive culling of sows prior to reaching their reproductive potential. Reports indicate that between 5 and 30% of sows are culled for failing to return to estrus following weaning. Consequently, swine producers are required to maintain an adequate gilt
From the Department of Food Animal and Equine Medicine, North Carolina State University College of Veterinary Medicine, Raleigh, North Carolina
VETERINARY CUNICS OF NORTH AMERICA: FOOD ANIMAL PRACTICE VOLUME 8. NUMBER 3· NOVEMBER 1992
503
504
ALMOND
replacement pool owing to the high incidence of anestrous sows during the summer months. Delayed returns to estrus following weaning interfere with a producer's ability to keep sufficient animals in designated breeding groups. In addition, it is obvious that prolonged WEIs contribute to excessive nonproductive sow days and additional costs of production. Treatment of the anestrous sow with exogenous hormones has proved beneficial under certain circumstances;32,35 however, cost, commercial availability, and federal restrictions have limited their use by swine producers and veterinarians. In summary, anestrous sows are common in most commercial swine farms, and they contribute to high culling rates and production costs during the summer and early autumn months. PHYSIOLOGIC EVENTS IN RELATION TO THE ONSET OF ESTRUS Relationship Between Lactation and Postweaning Endocrine Events
It has been demonstrated that length of lactation affects reproductive events following weaning. The average number of days from weaning to estrus increases as lactation length is decreased. Furthermore, the duration and intensity of suckling may also influence rate of return to estrus following weaning.ll,I7 Apparently, the removal of piglets for a period of time each day or decreasing litter sizes prior to weaning will cause a more rapid return to estrus following weaning. 50 Weaning the heaviest piglets in a litter 2 days early, commonly referred to as split-weaning, increases the proportion of sows returning to estrus by 10 days after weaning. The relationship between endocrinologic events during lactation and postweaning estrus remains poorly understood. Modest follicular development is accompanied by inhibition of hypophyseal secretion of gonadotropins during lactation. 49 The suppressed serum luteinizing hormone (LH) concentrations and the infrequent episodic release of gonadotropins during lactation25 are followed by a rise in basal and episodic LH secretion following weaning. 48 It has been suggested that LH and follicle-stimulating hormone (FSH) secretion are controlled by different mechanisms during lactation. Suckling modulates gonadotropin-releasing hormone (GnRH) synthesis and secretion, thereby controlling LH release. In contrast, FSH secretion is most likely regulated by an ovarian factor, namely, inhibin. The persistence of these suppressive lactational effects after weaning and their ultimate influence in sows that fail to return to estrus have not been elucidated. Endocrinologic Changes Following Weaning Sows Returning to Estrus
The dynamics and control of folliculogenesis in the sow appear to be complex. Following weaning, follicle size increases with a concomitant increase in ovarian production of estrogens;I6,25,50 however, marked variability in follicular development occurs between sows. These follicular changes are associated with an increased pulsatile secretion of LH and culminate in estrus, a preovulatory surge of LH, and ovulation. I8 The FSH concentrations do not increase until the postweaning FSH surge. 25 Presumably, the initiation of estrus and ovulation after weaning are associated with changes in production of GnRH. These observations indicate that weaning contributes to the removal of inhibitory influences on the hypothalamus and pituitary gland, thereby permitting increased secretory activity of the hypothalamo- hypophyseal axis, gonadotropin stimulation of ovarian activity, and, ultimately, estrus and ovulation.
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW
505
Failure to Resume Reproductive Activity Following Weaning
Few follicles are greater than 5 mm in diameter, corpora lutea are absent, and corpora albicantia are well regressed in ovaries of anestrous sows. 2 Obviously, inadequate stimulation of follicle growth occurs following weaning in sows destined to become anestrous. Although the mechanisms responsible for this failure of ovarian cyclicity are poorly understood, studies have shown an absence of cyclical changes in estradiol (E2) and LH concentrations in sows that remain persistently anestrus. 2 Evidently, E2 has the potential to inhibit hypothalamic release of GnRH and pituitary gland secretion of LH in anestrous sOWS. 2,3 It is apparent that the hypothalamo-hypophyseal-ovarian axis of the anestrous sow potentially is functional; however, the failure to commence increased pulsatile LH secretion is reflected by inadequate follicular development following weaning. Thus, the failure of increased follicular secretion of estrogen precludes the preovulatory surge of LH required for final follicle maturation and ovulation. FACTORS AFFECTING THE ONSET OF POSTWEANING ESTRUS Temperature
Elevated ambient temperature is frequently thought to influence the onset and severity of the postweaning anestrus condition. 12,31 Estrus is detected less frequently during periods of elevated environmental temperatures; however, the onset of the seasonal increase in delayed returns to estrus commences in March to April and has its highest incidence in August to September. Thus, the decline in reproductive performance typically begins in advance of the onset of hot weather. Furthermore, one study 17 indicated that the incidence of anestrous primiparous sows was 40% greater in September than in March, despite similar average daily temperatures in the farrowing facilities during both months. In addition, a similar incidence of the postweaning anestrus condition occurs in animals housed in the presence or absence of evaporative cooling systems. 31 One indirect effect of temperature is decreased feed intake and accompanying energy and protein deficits that frequently occur during hot weather. Prolonged periods of elevated temperatures may cause significant weight loss in the lactating sow, thereby predisposing her to the postweaning anestrus condition. In summary, it is difficult to evaluate the role of elevated environmental temperatures in isolation from other factors on the occurrence of anestrous sows. Photoperiod
Previous investigations have demonstrated that photoperiod affects the onset of maturation of the boar10 and the gilt. 20 It was suspected that photoperiod may influence the time from weaning until the initiation of estrus. 28,39,41,51 Despite speculation that a temporal relationship exists between photoperiod and seasonal postweaning anestrus, studies on the influence of light on the mature sow have yielded conflicting results. The exposure of sows to supplemental lighting (16 h light: 8 h dark) 3 to 9 days prior to farrowing and during lactation resulted in a higher percentage of sows that returned to estrus within 5 days postweaning. 51 In contrast, the exposure of sows to a similar photoperiod only during lactation had no influence on return to estrus following weaning. 39,41 Lastly, an extended photoperiod of 24 h light: 0 h dark following weaning failed to alter the weaning-to-service interval. 45
506
ALMOND
It is not surprising that altering photoperiod for a relatively brief duration does not alter the ability of sows to return to estrus following weaning. Abrupt alterations in photoperiod do not effectively mimic the gradual changes in natural photoperiod. Recent reports have indicated that the seasonal reproductive activity of the SOW 14 and boar 15 were dramatically reversed concomitant with a gradual reversal of photoperiod for a respective season. Length of time allowed for photoperiodic entrainment, the rate of change of photoperiod, the wavelength of light, the intensity of illumination, and the duration of illumination influence the response of mammalian species to photoperiod. Thus, conflicting results have been observed in sows exposed to altered photoperiods.
Facility
Extensive (pasture) systems, group housing, and individual housing in stalls or tethers are the three basic housing systems for weaned sows. The influence of facility design on sow performance is confounded by variations in swine housing systems, competence of personnel, and suitability of a genetic line or breed of sow for a particular housing system. Furthermore, it is evident that the influence of farrowing facilities on lactation performance may indirectly alter the productivity of the weaned sow. Although the different systems of sow housing have been thoroughly reviewed,42 the optimal system for the weaned sow has not been clearly defined. The individual stall housing system, albeit expensive, eliminates fighting between sows, ensures adequate feed consumption and utilization, and provides easy access to and identification of animals. The most commonly cited problem of individual stalls is abnormal behavior of sows. Pen and extensive systems allow social interaction, thereby making sows more responsive to the boar; however, excessive fighting is common between sows in pens or on pasture. Furthermore, feed consumption is difficult to regulate, and identification of sows is awkward in the latter systems. Lastly, estrous detection and boar exposure require less effort in most stall housing systems. A previous study47 revealed that WEIs were 4.25 and 4.5 days in sows penned in groups (4-5Jgroup) and in sows placed into individual stalls, respectively. Evidently, housing system had minimal influence on WEI; however, it has been our experience that placement of sows into individual stalls at weaning reduces the WEI, permits multiple matings, improves farrowing rates, and increases the percentage of sows bred within 7 days after weaning (Fig. 1). Owing to implications of elevated ambient temperatures in seasonal infertility, producers use evaporative cooling devices, such as drippers and misters, in conjunction with fans to increase evaporative cooling in farrowing rooms and breeding/gestation barns. It has been our experience that evaporative cooling improves feed consumption and consequently decreases lactational weight losses and WEI. It is the responsibility of the practitioner to compare the cost of evaporative cooling to the potential of improved production during and subsequent to the summer months. In summary, it is apparent that additional research is required to identify the most cost-effective and productive housing system for weaned sows. Nutrition
Nutrition and body condition of sows at the time of weaning are commonly cited as factors that influence the onset of postweaning estrus. Excessive weight loss during lactation is correlated with postweaning infertility problems. 29,54 Sows
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW
507
that lactate at a high rate and consume insufficient quantities of energy tend to lose weight during lactation and frequently fail to gain weight quickly following weaning. 54 A higher incidence of delayed returns to estrus has been reported in sows experiencing large weight and backfat losses during lactation compared to those that maintain their body condition. In contrast, various investigators22 ,23 suggested that changes in body condition typically observed in sows housed in commercial production units were too subtle to have an effect on reproductive performance. Some researchers 17 have reported that sows fed high-energy diets have increased rates of return to estrus following weaning relative to those fed normal or energy-deficit rations. Other investigators I3 ,22,23 have proposed that energy and feed intake during lactation has no effect on the number of days from weaning until estrus, provided that energy levels meet or exceed the National Research Council requirements for lactating sows. Energy intake during lactation may not be as significant as previously believed, because recent studies36,37 have indicated that protein intake during lactation exerts a greater influence on the WEI in first-litter sows. These studies demonstrated that the effect of protein intake was independent of energy intake; increasing daily protein intakes to a least 700 g crude protein, either alone or in combination with an increase in energy intake, increased the proportion of sows exhibiting estrus within 8 days of weaning. Furthermore, there was a positive association between estimated daily nitrogen loss during lactation and WEI. 43 Possibly, substantial nitrogen loss sustained by lactating sows with low protein intake is the primary nutritional factor responsible for the prolonged WEI in primiparous sows. Protein intake is required for growth as well as milk production in primiparous sows, whereas older sows require minimal protein for growth. First-litter sows mobilize muscle mass during lactation, whereas the weight loss in older sows is caused by regression of fat tissue. 37 These observations may account for the higher incidence of postweaning anestrus in primiparous than in multiparous sows. The influence of feed intake during the WEI is controversial. Some investigators have observed that feed consumption from weaning until estrus does not affect the rate of return to estrus,13,54 whereas others have demonstrated that low levels of feed intake (1.8 kg/day) cause a delayed return to estrus following weaning in primiparous females. It has been suggested that fasting following weaning stimulates an earlier onset of estrus,40 but other reports34 have indicated that fasting has no influence on postweaning reproductive performance. Stress
Stress is commonly defined as an environmental condition that is adverse to the well-being of an animal. This includes factors such as climate, nutrition, pathogens, or physiologic disorders. Therefore, the "stressed" animal often is considered abnormal, and the condition is regarded as undesirable. Adrenal secretion, as measured by serum concentrations of glucocorticoids, is difficult to interpret as an index of stress at anyone time. Because cortisol is the predominant active adrenal steroid produced in sows, most researchers have tended to measure concentrations of cortisol in serially collected serum samples. Administration of exogenous adrenocorticotropic hormone (ACTH) or corticosteroids prevents the preovulatory LH surge and blocks ovulation. 38 Although serum cortisol concentrations have been used to measure stress responses, stress-induced release of endogenous opioid peptides (EOP) has recently received considerable attention. It has been suggested that elevated levels of EOP influence the hypothalamus and pituitary gland during lactation and the
508
ALMOND
7.5 7.0 6.5
en ~
0
6.0
5.5
t
5.0 4.5 4.0
L..&....&....L-.........a...........................-'-...a.-....................-'-...a.-............................
Jan Mar May July Sept Nov Jan Mar May July Sept Nov
A
Mo~h 105~------------------------------------
__
100
--
95
......
a5
90
U
'-
~
85
80 75
% Mu~atings % Bre.?t:Y.1. Days
....................-'-...a.-......~~--~~~~~......- -......- ' - - -
70~
Jan Mar May July Sept Nov Jan Mar May July Sept Nov
B
Mo~h
Figure 1. A, Weaning-to-estrus intervals (WEI; days) over 2 years in a GSO-sow farm. The arrow indicates a management change from weaning sows into pens (4-S sows/pen) to weaning into individual sow crates (stalls). Note the reduction in WEI after the change in weaning procedures. S, The percent multiple matings and percent of sows bred by 7 days after weaning. These production parameters pertain to the GSO-sow farm indicated in A. The arrow represents the change from weaning sows into pens to weaning into crates. Both production parameters increased, and this improvement was evident for the subsequent 18 months.
Illustration continued on opposite page
luteal phase of the estrous cycle. 6,7 Treatment with naloxone, an opioid antagonist, increased serum LH concentrations, thereby indirectly indicating that EOP may influence LH release. 6,7 Therefore, it has been suggested that stress-related EOP release plays a physiologic role in suppressing ovarian activity in sows. The significance of stress in relation to the onset of estrus following weaning has been controversial. Undoubtedly, the removal of piglets and increased sow-tosow interactions after weaning exert stress on sows, and many producers believe that these stressors hasten the return to estrous activity. In view of the aforementioned discussion, it is difficult to relate increased stress to improved rates of return to estrus. In contrast, a minimization of stress occurs when females are moved
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW
509
100~------------------------------------'
en
80
~
~
Cl
'-
NPSD
~ 60 C
Q)
~
Q)
a..
40
t
20~~~~~~~~~~~~~~~--~"~
Jan Mar May July Sept Nov Jan Mar May July Sept Nov
C
Month
Figure 1. (Continued) C, Farrowing rates (FR) (%) and number of nonproductive sow days (NPSD) for 2 years in a 650-sow farm. These production parameters pertain to the farm indicated in A and B. Increased farrowing rates and a reduction in NPSD followed the change (indicated by the arrow) in procedures.
from farrowing crates to breeding crates rather than into groups in pens or pastures. The use of breeding crates has been shown to increase the percentage of sows that return to estrus. 31 ,40 Conversely, other researchers have demonstrated that cortisol concentrations are increased by tethering or individually penning gilts. 8 The reproductive performance of gilts used in the latter study 8 was not recorded. Transportation, relocation, or changes in environment have been reported to successfully facilitate the onset of estrus in SOWS. 46 Presently, the mechanism of estrus induction by these techniques is unknown but presumably involves an alteration in the hypothalamo-hypophyseal-ovarian axis by acute stress and related endocrine modifications. Genetics
A genetic predisposition to seasonal postweaning anestrus has been proposed, because some breeds of sows have been found to have a shorter WEI than other breeds,21,24 and the occurrence of postweaning anestrus was greatest in purebred sows. s Because the heritability of the WEI has been estimated to be 0.25,24 it is apparent that postweaning anestrus can be decreased through genetic selection and crossbreeding programs. INFLUENCE OF SEASON ON WEANED AND PREGNANT SOWS
The severity of seasonal infertility varies from year to year and from farm to farm. Under most circumstances, the diagnosis occurs after the detrimental effects of seasonal infertility have decreased performance, and insufficient time is available to institute therapeutic or management changes. Because changes in reproductive performance occur over several months, it is not uncommon to overlook seasonal patterns in reproductive activity in commercial swine farms.
510
ALMOND
Weaning-to-Estrus
As previously mentioned, elevated ambient temperature and photoperiod play potential roles in seasonal infertility. A common seasonal change in productivity is the failure of sows to return to estrus within 2 weeks following weaning (Fig. 2). During the winter months, most sows return to estrus within 7 days.12,31 In contrast, it is not unusual for less than 50% of the primiparous sows and less than 75 % of the multiparous sows to show estrus within 7 days following weaning during July, August, and September. s,31 Fortunately, recent improvements in management of the weaned sow have increased the percentage of sows returning to estrus within 7 days after weaning. It is evident that swine producers and veterinarians must be cognizant of the adverse affect of season on the WEI. Because numerous factors, described in the aforementioned discussion, influence a sow's ability to return to estrus, practitioners must consider the relative significance of each factor on a farm-by-farm basis. Establishment and Maintenance of Pregnancy
Seasonal changes in conception and farrowing rates are evident in most swine herds. The precise cause(s) of these seasonal alterations is poorly understood; however, it has been demonstrated that heat stress disrupts implantation and decreases embryo development. 44 Consequently, an increased proportion of bred sows return to estrus at 18 to 24 days or at irregular intervals in the summer months. Farrowing rates, as measured by most record systems, are significantly lower in the subsequent winter months (Fig. 3). Loss of embryos/fetuses after the release of the blastocysts' luteotrophic signal for pregnancy maintenance (days 12 - 13 postbreeding) often results in pseudopregnancy or prolonged periods of anestrus in affected sows. Because fetal or embryonic remnants usually are read-
cn10---------------------------------~ ~
co 2:
~
oS en
9 8
2 7
00
~ 6 ~ C> .~ 5
.......... ........... ,
,.\
.... " , ' \ ........ ".... " \,
•••• ••••••••••• ~!'~~ .. -"',..f.~
....·······..................,~ . \
co Q)
3:
4 _
J M
A-J
J-S
0-0 J-M
A-J
J-S
0-0
Quarter Figure 2. Weaning-to-estrus intervals (WEI) in sows over 2 years in a 1000-sow farm. The months of January to March, April to June, July to September, and October to December are represented by J-M, A-J, J-S, and 0-0, respectively. The increased WEI was most evident in primiparous sows during July to September. Seasonal changes in WEI were less apparent in second-parity females and not detected in the third- to sixth-parity sows.
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW
511
100 95
~ 90 co a: 85 Q)
...
...
C>
c
.§ 0
~ ~
al U.
80 75 70 65J-M
A-J
J-S 0-0 J-M Quarter
A-J
J-S 0-0
Figure 3. Farrowing rates of sows over 2 years in a 1000-sow farm. The months of January to March, April to June, July to September, and October to December are represented by J-M, A-J, J-S, and 0-0, respectively. Note the decreased farrowing rates in primiparous sows during the winter months, subsequent to mating during the summer. The seasonal change in farrowing rate was not evident in multiparous sows.
sorbed, pseudopregnant animals are identified as not-in-pig or failing-to-farrow sows in the fall or early winter months. It has been demonstrated that heat stress results in decreased numbers of embryos and/or fetuses and subsequent decreases in litter size. 44 In contrast, heat stress exerts minimal influence on pregnancy after implantation, although seasonal variations in total pigs born and pigs born alive have been observed in some studies. 53 It has been suggested that when sows are exposed to elevated ambient temperatures in late gestation, death of the sow is more likely than death of the litter. 44
Autumn Abortion Syndrome
The autumn abortion syndrome (AAS) is another reproductive disorder that evidently is part of the seasonal infertility complex. 1 The most common clinical feature of AAS is an increased incidence of noninfectious abortion in sows during the months of September through December. The stage of gestation when abortion occurs ranges from 30 to 110 days postbreeding. 1 Clinical signs and pathologic lesions are absent in the affected sows and fetuses, respectively. In addition, serologic evidence of an infectious agent is lacking. It is evident that a combination of environmental, nutritional, and managerial factors predispose or contribute to the AAS. Marginal energy intake and failure to maintain ambient temperatures in the gestation house when environmental temperatures fall drastically after a preceding warm day, and stressors caused by rapid and vast fluctuations in autumn temperatures, may be involved. 1 In addition, decreasing LH and/or progesterone concentrations in sows, associated with reduced daylight hours encountered in the autumn, may playa significant role in the AAS.57
512
ALMOND
CLINICAL EVALUATION OF PROLONGED WEI
The prevalence of anestrous sows is often over- or underestimated by swine producers. This is especially common when producers use suboptimal estrous detection techniques. Consequently, producers attribute prolonged WEI to seasonal infertility when the major problem is suboptimal management. Because the occurrence of anestrous sows varies from year to year and from farm to farm, the economic impact of prolonged WEI is easily overlooked by producers and veterinarians. Techniques to diagnose and identify anestrous sows include record analysis, slaughterhouse evaluation of ovaries, and analysis of plasma or serum progesterone concentrations. Obviously, estrus is not detected in affected sows, but accurate records are necessary to determine the economic significance of prolonged WEI. Records can be used to compare rates of return to estrus following weaning during the summer months to those of the winter months. If records are not available or if management is suspect, the ovarian morphology may be assessed in representative sows. The ovaries of anestrous sows typically have no corpora lutea in accompaniment with follicles less than 5 mm in diameter.2 The presence of corpora lutea is indicative of ovarian cyclical activity, thereby revealing that estrus did occur but was not observed. Paired samples of blood can be obtained at to-day intervals from anestrous sows and used to assess the percentage of females having cyclical and acyclical ovaries. An elevation in serum P4 concentrations in either or both of the two samples is suggestive of cyclical ovarian activity. Low P4 concentrations «2 ng/mL) in sows is representative of the anestrus condition. 2 To appropriately assess anestrous sows, identification of affected animals must be followed by confirmation of ovarian acyclicity.
POTENTIAL TREATMENTS OF ANESTROUS SOWS
Numerous medical and management treatments have been used in attempts to eliminate postweaning anestrous sows and to reduce the WEI. In some instances, the use of exogenous hormones has been effective in stimulating a resumption of ovarian cyclicity in sows that fail to return to estrus following weaning. Pregnant mare serum gonadotropin (PMSG) combined with human chorionic gonadotropin (hCG) has been used therapeutically in the persistently anestrous sow and prophylactically in the weaned sow to improve postweaning reproductive performance. 32 Treatment of the anestrous sow with PMSG/hCG induces a fertile estrus in sows having acyclic ovaries. 19 When administered at weaning, PMSG decreases the WEI and the proportion of sows experiencing postweaning anestrus. These observations suggest that PMSG is potentially effective for treatment of postweaning anestrus. Unfortunately, the commercial PMSG/hCG product (PG 600, Intervet America, DE) is not federally licensed for use in weaned sows. Other hormonal treatments do not appear as efficacious as PMSG in treatment of postweaning anestrous sows. Treatment with hCG consistently induces ovulation in the anestrous sow but is relatively ineffective in causing estrus. 19 The administration of a single dose of GnRH induces hypophyseal release of endogenous gonadotropins but does not cause estrus or ovulation. 19 The pulsatile administration of GnRH at hourly intervals to anestrous sows induces estrus and ovulation,4 but is impractical for commercial application. Exogenous estradiol t7P (E2) consistently induced estrus but sporadically induced ovulation. 19 The combination
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW
513
of E2 and heG induces estrus and ovulation in anestrous sows but results in poor pregnancy rates and small litter size. 26 The administration of a prostaglandin analogue to primiparous sows on the day of weaning increases the percentage of females returning to estrus within 10 days after weaning and decreases the mean number of days from weaning until estrus. 33 Additional research, however, is needed to confirm the efficacy of prostaglandins in the prophylaxis of postweaning anestrus and in the therapy of persistently anestrous sows. SUMMARY
The majority of sows return to estrus within 2 weeks after weaning. Swine practitioners attempt to optimize production by reducing the WEI. Some sows fail to resume estrous cyclicity after weaning; however, the endocrinologic pathogenesis of these anestrous sows is speculative. The average WEI is influenced by numerous factors, including season, environmental temperature, photoperiod, nutrition, stress, facility design, lactation length, and management practices. It is evident that the majority of these factors have a more profound influence on primiparous sows than on multiparous sows. Optimum protein and energy consumption by sows during lactation and after weaning and effective utilization of breeding facilities reduce the WEI. The precise roles of photoperiodic changes, elevated environmental temperatures, and stress in seasonal infertility remain poorly understood. Fortunately, current management techniques have reduced the WEI on most farms without instituting therapeutic measures. References 1. Almond GW, Friendship RM, Bosu WTK: Autumn abortions in sows. Can Vet J 26:162, 1985 2. Almond GW, Dial GD: Steroid hormone and luteinizing hormone concentrations in the anestrous sow. Can J Vet Res 54:209, 1990 3. Almond GW, Dial GD: Estradiol feedback inhibition of luteinizing hormone concentrations in the anestrous sow. J Anim Sci 68:1077, 1990 4. Armstrong JD, Britt JH: Pulsatile administration of gonadotropin-releasing hormone to anestrous sows: Endocrine changes associated with GnRH-induced and spontaneous estrus. BioI Reprod 33:375, 1985 5. Aumaitre A, Dagorn J, Legault C, et al: Influence of farm management and breed type on sows' conception-weaning interval and productivity in France. Livestock Prod Sci 3:75, 1976 6. Barb CR, Kraeling RR, Rampacek GB, et al: Opioid inhibition of luteinizing hormone secretion in the postpartum lactating sow. BioI Reprod 35:368, 1986 7. Barb CR, Kraeling RR, Rampacek GB, et al: Influence of stage of the estrous cycle on endogenous opioid modulation of luteinizing hormone, prolactin, and cortisol secretion in the gilt. BioI Reprod 35:1162, 1986 8. Becker BA, Ford H, Christenson RK, et al: Cortisol response of gilts in tether stalls. J Anim Sci 60:264, 1985 9. Benjaminsen E, Karlberg K: Post weaning oestrus and luteal function in primiparous and pluriparous sows. Res Vet Sci 30:318, 1981 10. Brandt KE, Diekman MA: Influence of supplemental lighting on serum LH, testosterone and semen quality in prepubertal and post-pubertal boars. Anim Reprod Sci 8:287, 1985 11. Britt JH, Levis DG: Effect of altering suckling intervals of early-weaned pigs on rebreeding performance of sows. Theriogenology 18:201, 1982 12. Britt JH, Szarek VE, Levis DG: Characterization of summer infertility of sows in large confinement units. Theriogenology 20:133, 1983
514
ALMOND
13. Brooks PH, Cole DJA, Rowlinson P, et al: Studies in sow reproduction. 3. The effect of nutrition between weaning and remating on the reproductive performance of multiparous sows. Anim Prod 20:407, 1975 14. Claus R, Weiler U: Influence of light and photoperiodicity on pig prolificacy. J Reprod Fertil Suppl 33:185, 1985 15. Claus R, Schopper 0, Wagner HG, et al: Photoperiodic influences on reproduction of domestic boars. Zbl Vet Med A 32:86, 1985 16. Cox NM, Britt JH: Relationships between endogenous gonadotropin-releasing hormone, gonadotropins, and follicular development after weaning in sows. BioI Reprod 27:70, 1982 17. Cox NM, Britt JH, Armstrong WD, et al: Effect of feeding fat and altering weaning schedule on rebreeding performance in primiparous sows. J Anim Sci 56:21, 1983 18. DeRensis F, Hunter MG, Grant SA, et al: Effect of estrogen administration on endogenous and luteinizing hormone-releasing-hormone-induced luteinizing hormone secretion and follicular development in the lactating sow. BioI Reprod 44:975, 1991 19. Dial GO, BeVier GW, Hixon JE, et al: Endocrine pathogenesis of postweaning anestrus in swine: Response of the persistently anestrous sow to hormonal stimuli. Am J Vet Res 45:1737, 1984 20. Diekman MA, Hoagland TA: Influence of supplemental lighting during periods of increasing or decreasing daylength on the onset of puberty in gilts. J Anim Sci 57:1235, 1983 21. Dyck GW: Puberty, postweaning estrus and estrous cycle length in Yorkshire and Lacombe swine. Can Anim Sci 51:135, 1971 22. Esbenshade KL, Britt JH, Armstrong JD, et al: Body condition of sows across parities and relationship to reproductive performance. J Anim Sci 62:1187, 1986 23. Fahmy MH, Dufour JJ: Effects of postweaning stress and feeding management on return to oestrus and reproductive traits during early pregnancy in swine. Anim Prod 23:102, 1976 24. Fahmy MH, Holtmann WB, Baker RD: Failure to recycle after weaning, and weaning to oestrus interval in crossbred sows. Anim Prod 29:193, 1979 25. Foxcroft GR, Shaw HJ, Hunter MG, et al: Relationships between luteinizing hormone, follicle-stimulating hormone and prolactin secretion and ovarian follicular development in the weaned sow. BioI Reprod 36:175, 1987 26. Friendship RM, Bosu WTK, King GJ: Reproductive performance in sows treated with estradiol benzoate/human chorionic gonadotropin combination at weaning. Can J Comp Med 46:410, 1982 27. Friendship RM, Wilson MR, Almond GW, et al: Sow wastage: Reasons for and effect on productivity. Can J Vet Res 50:205, 1986 28. Greenberg LG, Mahone JP: Failure of a 16 h L: 8 h 0 or an 8 h L: 16 h 0 photoperiod to influence lactation or reproductive efficiency in sows. Can J Anim Sci 62:141, 1982 29. Hays VW, Krug JL, Cromwell GL, et al: Effect of lactation length and dietary antibiotics on reproductive performance of sows. J Anim Sci 46:884, 1978 30. Hemsworth PH, Salden NTCJ, Hoogerbrugge A: The influence of the post-weaning social environment on the weaning to mating interval of the sow. Anim Prod 35:41, 1982 31. Hurtgen JP, Leman AD, Crabo B: Seasonal influence on estrous activity in sows and gilts. J Am Vet Med Assoc 176:119, 1980 32. Hurtgen JP, Leman AD: Use of PMSG in the prevention of seasonal postweaning anestrus in sows. Theriogenology 12:207, 1979 33. Jochle W, Ceme F: Clinical evaluation of a new prostaglandin analog in pigs: 2. Prophylaxis and therapy of anestrus after weaning in sows and first litter gilts. Theriogenology 19:481, 1983 34. King GJ: Effects of several weaning procedures on the interval of estrus in sows. Can J Anim Sci 54:251, 1974 35. King RH, Williams IH, Barker I: Induction of oestrus in anestrous, first litter sows with pregnant mare's serum gonadotropin. Anim Reprod Sci 5:41, 1982 36. King RH, Williams IH: The effect of nutrition on the reproductive performance of first-litter sows. 2. Feeding level during lactation, and between weaning and mating. Anim Prod 38:241, 1984 37. King RH, Dunkin AC: The effect of nutrition on the reproductive performance of
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW
38. 39. 40. 41. 42. 43. 44. 45. 46. 47. 48. 49. 50. 51. 52. 53. 54. 55. 56. 57.
515
first-litter sows. 4. The relative effects of energy and protein intakes during lactation on the performance of sows and their piglets. Anim Prod 42:319, 1986 Liptrap RM: Effect of corticotropin and corticosteroids on oestrus, ovulation and oestrogen excretion in the sow. J Endocrinol 47:197, 1970 Mabry JW, Coffey MT, Seerley RW: Comparison of an 8- versus 16-hour photoperiod during lactation on suckling frequency of the baby pig and maternal performance of the sow. J Anim Sci 57:292, 1983 MacLean CW: Observations on noninfectious infertility in sows. Vet Rec 85:675, 1969 McGlone H, Stansbury WF, Tribble LF, et al: Photoperiod and heat stress influence on lactating sow performance and photoperiod effects on nursery pig performance. J Anim Sci 66:1915, 1988 Muirhead MR: A comparison of different systems of sow housing and management. Pig Vet Soc Proc 8:18, 1981 Noblet J, Etienne M: Metabolic utilization of energy and maintenance requirements in lactating sows. J Anim Sci 64:774, 1987 Omtvedt IT, Nelson RE, Edwards RL, et al: Influence of heat stress during early, mid and late pregnancy of gilts. J Anim Sci 32:312, 1971 Perera ANM, Hacker RR: The effects of different photoperiods on reproduction in the sow. J Anim Sci 58:1418, 1984 Renaud G, Guay P, Beauregard M, et al: Anoestrus dans un troupeau de truies: Etude conico-pathologique. Can Vet J 13:94, 1972 Schmidt WE, Stevenson JS, Davis DL: Reproductive traits of sows penned individually or in groups until 35 days after breeding. J Anim Sci 60:755, 1985 Shaw HJ, Foxcroft GR: Relationships between LH, FSH and prolactin and reproductive activity in the weaned sow. J Reprod Fertil 75:17, 1985 Stevenson JS, Cox NM, Britt JH: Role of the ovary in controlling luteinizing hormone, follicle stimulating hormone, and prolactin secretion during and after weaning in sows. BioI Reprod 24:341, 1981 Stevenson JS, Britt JH: Interval to estrus in sows and performance of pigs after alteration of litter size during late lactation. J Anim Sci 53:177, 1981 Stevenson JS, Pollman DS, Davis DL, et al: Influence of supplemental light on sow performance during and after lactation. J Anim Sci 56:1282, 1983 Teague HS, Roller WL, Grifo AP: Influence of high temperatures and humidity on the reproductive performance of swine. J Anim Sci 27:408, 1968 Tomes GJ, Nielson HE: Seasonal variations in the reproductive performance in sows under different climatic conditions. World Review Anim Prod 15:9-19, 1979 Varley MA, Cole DJA: Studies in sow reproduction. 4. The effect of level of feeding in lactation and during the interval from weaning to remating on the subsequent reproductive performance of the early weaned sow. Anim Prod 22:71, 1976 Walker N, Watt D: The effect of weaning at 10, 25, or 40 days on the reproductive performance of sows from the first to the fifth parity. J Agric Sci Camb 92:449, 1979 Walton JS: Effect of boar presence before and after weaning on estrus and ovulation in sows. J Anim Sci 62:9, 1986 Wrathall AE, Wells DE, Jones PC, et al: Seasonal variations in serum progesterone levels in pregnant sows. Vet Rec 118:685, 1986
Address reprint requests to Glen W. Almond, DVM, MSc, PhD Department of Food Animal and Equine Medicine North Carolina State University College of Veterinary Medicine 4700 Hillsborough Street Raleigh, NC 27606
SWINE REPRODUCTION
+ .20
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW Glen W. Almond, DVM, MSc, PhD
The majority of sows return to estrus within 3 to 14 days following weaning. 24.35 Sows that fail to resume estrous cyclicity are either culled from the herd or return to estrus at highly variable times. 9,27 The average interval from weaning to first detected estrus increases during the summer and is substantially longer in primiparous sows than in multiparous SOWS. 12,31 The weaning-to-estrus interval (WEI) often exceeds 30 days during the summer in sows affected with the anestrous condition. 9 Factors influencing WEI include boar exposure,30,56 lactation length,12,55 nutrition during and after lactation,17,36,54 stress, environmental temperature,52 and photoperiod. 28 ,51 Although seasonal influences are inherent to swine reproduction, they have only recently been regarded as significant factors affecting the reproductive efficiency of swine herds. This article is intended to illustrate the interactions between the physiologic events and the factors affecting WEI. In addition, the negative role of season on the WEI, pregnancy loss, abortion, farrowing rates, and irregular returns to estrus after breeding is discussed. ECONOMIC SIGNIFICANCE OF THE WEI AND POSTWEANING ANESTRUS
Most reports have indicated that reproductive failure was the most common cause of culling sows from commercial swine farms.9,27 Postweaning anestrus is cited as a common cause of reproductive failure, thereby contributing to excessive culling of sows prior to reaching their reproductive potential. Reports indicate that between 5 and 30% of sows are culled for failing to return to estrus following weaning. Consequently, swine producers are required to maintain an adequate gilt
From the Department of Food Animal and Equine Medicine, North Carolina State University College of Veterinary Medicine, Raleigh, North Carolina
VETERINARY CUNICS OF NORTH AMERICA: FOOD ANIMAL PRACTICE VOLUME 8. NUMBER 3· NOVEMBER 1992
503
504
ALMOND
replacement pool owing to the high incidence of anestrous sows during the summer months. Delayed returns to estrus following weaning interfere with a producer's ability to keep sufficient animals in designated breeding groups. In addition, it is obvious that prolonged WEIs contribute to excessive nonproductive sow days and additional costs of production. Treatment of the anestrous sow with exogenous hormones has proved beneficial under certain circumstances;32,35 however, cost, commercial availability, and federal restrictions have limited their use by swine producers and veterinarians. In summary, anestrous sows are common in most commercial swine farms, and they contribute to high culling rates and production costs during the summer and early autumn months. PHYSIOLOGIC EVENTS IN RELATION TO THE ONSET OF ESTRUS Relationship Between Lactation and Postweaning Endocrine Events
It has been demonstrated that length of lactation affects reproductive events following weaning. The average number of days from weaning to estrus increases as lactation length is decreased. Furthermore, the duration and intensity of suckling may also influence rate of return to estrus following weaning.ll,I7 Apparently, the removal of piglets for a period of time each day or decreasing litter sizes prior to weaning will cause a more rapid return to estrus following weaning. 50 Weaning the heaviest piglets in a litter 2 days early, commonly referred to as split-weaning, increases the proportion of sows returning to estrus by 10 days after weaning. The relationship between endocrinologic events during lactation and postweaning estrus remains poorly understood. Modest follicular development is accompanied by inhibition of hypophyseal secretion of gonadotropins during lactation. 49 The suppressed serum luteinizing hormone (LH) concentrations and the infrequent episodic release of gonadotropins during lactation25 are followed by a rise in basal and episodic LH secretion following weaning. 48 It has been suggested that LH and follicle-stimulating hormone (FSH) secretion are controlled by different mechanisms during lactation. Suckling modulates gonadotropin-releasing hormone (GnRH) synthesis and secretion, thereby controlling LH release. In contrast, FSH secretion is most likely regulated by an ovarian factor, namely, inhibin. The persistence of these suppressive lactational effects after weaning and their ultimate influence in sows that fail to return to estrus have not been elucidated. Endocrinologic Changes Following Weaning Sows Returning to Estrus
The dynamics and control of folliculogenesis in the sow appear to be complex. Following weaning, follicle size increases with a concomitant increase in ovarian production of estrogens;I6,25,50 however, marked variability in follicular development occurs between sows. These follicular changes are associated with an increased pulsatile secretion of LH and culminate in estrus, a preovulatory surge of LH, and ovulation. I8 The FSH concentrations do not increase until the postweaning FSH surge. 25 Presumably, the initiation of estrus and ovulation after weaning are associated with changes in production of GnRH. These observations indicate that weaning contributes to the removal of inhibitory influences on the hypothalamus and pituitary gland, thereby permitting increased secretory activity of the hypothalamo- hypophyseal axis, gonadotropin stimulation of ovarian activity, and, ultimately, estrus and ovulation.
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW
505
Failure to Resume Reproductive Activity Following Weaning
Few follicles are greater than 5 mm in diameter, corpora lutea are absent, and corpora albicantia are well regressed in ovaries of anestrous sows. 2 Obviously, inadequate stimulation of follicle growth occurs following weaning in sows destined to become anestrous. Although the mechanisms responsible for this failure of ovarian cyclicity are poorly understood, studies have shown an absence of cyclical changes in estradiol (E2) and LH concentrations in sows that remain persistently anestrus. 2 Evidently, E2 has the potential to inhibit hypothalamic release of GnRH and pituitary gland secretion of LH in anestrous sOWS. 2,3 It is apparent that the hypothalamo-hypophyseal-ovarian axis of the anestrous sow potentially is functional; however, the failure to commence increased pulsatile LH secretion is reflected by inadequate follicular development following weaning. Thus, the failure of increased follicular secretion of estrogen precludes the preovulatory surge of LH required for final follicle maturation and ovulation. FACTORS AFFECTING THE ONSET OF POSTWEANING ESTRUS Temperature
Elevated ambient temperature is frequently thought to influence the onset and severity of the postweaning anestrus condition. 12,31 Estrus is detected less frequently during periods of elevated environmental temperatures; however, the onset of the seasonal increase in delayed returns to estrus commences in March to April and has its highest incidence in August to September. Thus, the decline in reproductive performance typically begins in advance of the onset of hot weather. Furthermore, one study 17 indicated that the incidence of anestrous primiparous sows was 40% greater in September than in March, despite similar average daily temperatures in the farrowing facilities during both months. In addition, a similar incidence of the postweaning anestrus condition occurs in animals housed in the presence or absence of evaporative cooling systems. 31 One indirect effect of temperature is decreased feed intake and accompanying energy and protein deficits that frequently occur during hot weather. Prolonged periods of elevated temperatures may cause significant weight loss in the lactating sow, thereby predisposing her to the postweaning anestrus condition. In summary, it is difficult to evaluate the role of elevated environmental temperatures in isolation from other factors on the occurrence of anestrous sows. Photoperiod
Previous investigations have demonstrated that photoperiod affects the onset of maturation of the boar10 and the gilt. 20 It was suspected that photoperiod may influence the time from weaning until the initiation of estrus. 28,39,41,51 Despite speculation that a temporal relationship exists between photoperiod and seasonal postweaning anestrus, studies on the influence of light on the mature sow have yielded conflicting results. The exposure of sows to supplemental lighting (16 h light: 8 h dark) 3 to 9 days prior to farrowing and during lactation resulted in a higher percentage of sows that returned to estrus within 5 days postweaning. 51 In contrast, the exposure of sows to a similar photoperiod only during lactation had no influence on return to estrus following weaning. 39,41 Lastly, an extended photoperiod of 24 h light: 0 h dark following weaning failed to alter the weaning-to-service interval. 45
506
ALMOND
It is not surprising that altering photoperiod for a relatively brief duration does not alter the ability of sows to return to estrus following weaning. Abrupt alterations in photoperiod do not effectively mimic the gradual changes in natural photoperiod. Recent reports have indicated that the seasonal reproductive activity of the SOW 14 and boar 15 were dramatically reversed concomitant with a gradual reversal of photoperiod for a respective season. Length of time allowed for photoperiodic entrainment, the rate of change of photoperiod, the wavelength of light, the intensity of illumination, and the duration of illumination influence the response of mammalian species to photoperiod. Thus, conflicting results have been observed in sows exposed to altered photoperiods.
Facility
Extensive (pasture) systems, group housing, and individual housing in stalls or tethers are the three basic housing systems for weaned sows. The influence of facility design on sow performance is confounded by variations in swine housing systems, competence of personnel, and suitability of a genetic line or breed of sow for a particular housing system. Furthermore, it is evident that the influence of farrowing facilities on lactation performance may indirectly alter the productivity of the weaned sow. Although the different systems of sow housing have been thoroughly reviewed,42 the optimal system for the weaned sow has not been clearly defined. The individual stall housing system, albeit expensive, eliminates fighting between sows, ensures adequate feed consumption and utilization, and provides easy access to and identification of animals. The most commonly cited problem of individual stalls is abnormal behavior of sows. Pen and extensive systems allow social interaction, thereby making sows more responsive to the boar; however, excessive fighting is common between sows in pens or on pasture. Furthermore, feed consumption is difficult to regulate, and identification of sows is awkward in the latter systems. Lastly, estrous detection and boar exposure require less effort in most stall housing systems. A previous study47 revealed that WEIs were 4.25 and 4.5 days in sows penned in groups (4-5Jgroup) and in sows placed into individual stalls, respectively. Evidently, housing system had minimal influence on WEI; however, it has been our experience that placement of sows into individual stalls at weaning reduces the WEI, permits multiple matings, improves farrowing rates, and increases the percentage of sows bred within 7 days after weaning (Fig. 1). Owing to implications of elevated ambient temperatures in seasonal infertility, producers use evaporative cooling devices, such as drippers and misters, in conjunction with fans to increase evaporative cooling in farrowing rooms and breeding/gestation barns. It has been our experience that evaporative cooling improves feed consumption and consequently decreases lactational weight losses and WEI. It is the responsibility of the practitioner to compare the cost of evaporative cooling to the potential of improved production during and subsequent to the summer months. In summary, it is apparent that additional research is required to identify the most cost-effective and productive housing system for weaned sows. Nutrition
Nutrition and body condition of sows at the time of weaning are commonly cited as factors that influence the onset of postweaning estrus. Excessive weight loss during lactation is correlated with postweaning infertility problems. 29,54 Sows
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW
507
that lactate at a high rate and consume insufficient quantities of energy tend to lose weight during lactation and frequently fail to gain weight quickly following weaning. 54 A higher incidence of delayed returns to estrus has been reported in sows experiencing large weight and backfat losses during lactation compared to those that maintain their body condition. In contrast, various investigators22 ,23 suggested that changes in body condition typically observed in sows housed in commercial production units were too subtle to have an effect on reproductive performance. Some researchers 17 have reported that sows fed high-energy diets have increased rates of return to estrus following weaning relative to those fed normal or energy-deficit rations. Other investigators I3 ,22,23 have proposed that energy and feed intake during lactation has no effect on the number of days from weaning until estrus, provided that energy levels meet or exceed the National Research Council requirements for lactating sows. Energy intake during lactation may not be as significant as previously believed, because recent studies36,37 have indicated that protein intake during lactation exerts a greater influence on the WEI in first-litter sows. These studies demonstrated that the effect of protein intake was independent of energy intake; increasing daily protein intakes to a least 700 g crude protein, either alone or in combination with an increase in energy intake, increased the proportion of sows exhibiting estrus within 8 days of weaning. Furthermore, there was a positive association between estimated daily nitrogen loss during lactation and WEI. 43 Possibly, substantial nitrogen loss sustained by lactating sows with low protein intake is the primary nutritional factor responsible for the prolonged WEI in primiparous sows. Protein intake is required for growth as well as milk production in primiparous sows, whereas older sows require minimal protein for growth. First-litter sows mobilize muscle mass during lactation, whereas the weight loss in older sows is caused by regression of fat tissue. 37 These observations may account for the higher incidence of postweaning anestrus in primiparous than in multiparous sows. The influence of feed intake during the WEI is controversial. Some investigators have observed that feed consumption from weaning until estrus does not affect the rate of return to estrus,13,54 whereas others have demonstrated that low levels of feed intake (1.8 kg/day) cause a delayed return to estrus following weaning in primiparous females. It has been suggested that fasting following weaning stimulates an earlier onset of estrus,40 but other reports34 have indicated that fasting has no influence on postweaning reproductive performance. Stress
Stress is commonly defined as an environmental condition that is adverse to the well-being of an animal. This includes factors such as climate, nutrition, pathogens, or physiologic disorders. Therefore, the "stressed" animal often is considered abnormal, and the condition is regarded as undesirable. Adrenal secretion, as measured by serum concentrations of glucocorticoids, is difficult to interpret as an index of stress at anyone time. Because cortisol is the predominant active adrenal steroid produced in sows, most researchers have tended to measure concentrations of cortisol in serially collected serum samples. Administration of exogenous adrenocorticotropic hormone (ACTH) or corticosteroids prevents the preovulatory LH surge and blocks ovulation. 38 Although serum cortisol concentrations have been used to measure stress responses, stress-induced release of endogenous opioid peptides (EOP) has recently received considerable attention. It has been suggested that elevated levels of EOP influence the hypothalamus and pituitary gland during lactation and the
508
ALMOND
7.5 7.0 6.5
en ~
0
6.0
5.5
t
5.0 4.5 4.0
L..&....&....L-.........a...........................-'-...a.-....................-'-...a.-............................
Jan Mar May July Sept Nov Jan Mar May July Sept Nov
A
Mo~h 105~------------------------------------
__
100
--
95
......
a5
90
U
'-
~
85
80 75
% Mu~atings % Bre.?t:Y.1. Days
....................-'-...a.-......~~--~~~~~......- -......- ' - - -
70~
Jan Mar May July Sept Nov Jan Mar May July Sept Nov
B
Mo~h
Figure 1. A, Weaning-to-estrus intervals (WEI; days) over 2 years in a GSO-sow farm. The arrow indicates a management change from weaning sows into pens (4-S sows/pen) to weaning into individual sow crates (stalls). Note the reduction in WEI after the change in weaning procedures. S, The percent multiple matings and percent of sows bred by 7 days after weaning. These production parameters pertain to the GSO-sow farm indicated in A. The arrow represents the change from weaning sows into pens to weaning into crates. Both production parameters increased, and this improvement was evident for the subsequent 18 months.
Illustration continued on opposite page
luteal phase of the estrous cycle. 6,7 Treatment with naloxone, an opioid antagonist, increased serum LH concentrations, thereby indirectly indicating that EOP may influence LH release. 6,7 Therefore, it has been suggested that stress-related EOP release plays a physiologic role in suppressing ovarian activity in sows. The significance of stress in relation to the onset of estrus following weaning has been controversial. Undoubtedly, the removal of piglets and increased sow-tosow interactions after weaning exert stress on sows, and many producers believe that these stressors hasten the return to estrous activity. In view of the aforementioned discussion, it is difficult to relate increased stress to improved rates of return to estrus. In contrast, a minimization of stress occurs when females are moved
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW
509
100~------------------------------------'
en
80
~
~
Cl
'-
NPSD
~ 60 C
Q)
~
Q)
a..
40
t
20~~~~~~~~~~~~~~~--~"~
Jan Mar May July Sept Nov Jan Mar May July Sept Nov
C
Month
Figure 1. (Continued) C, Farrowing rates (FR) (%) and number of nonproductive sow days (NPSD) for 2 years in a 650-sow farm. These production parameters pertain to the farm indicated in A and B. Increased farrowing rates and a reduction in NPSD followed the change (indicated by the arrow) in procedures.
from farrowing crates to breeding crates rather than into groups in pens or pastures. The use of breeding crates has been shown to increase the percentage of sows that return to estrus. 31 ,40 Conversely, other researchers have demonstrated that cortisol concentrations are increased by tethering or individually penning gilts. 8 The reproductive performance of gilts used in the latter study 8 was not recorded. Transportation, relocation, or changes in environment have been reported to successfully facilitate the onset of estrus in SOWS. 46 Presently, the mechanism of estrus induction by these techniques is unknown but presumably involves an alteration in the hypothalamo-hypophyseal-ovarian axis by acute stress and related endocrine modifications. Genetics
A genetic predisposition to seasonal postweaning anestrus has been proposed, because some breeds of sows have been found to have a shorter WEI than other breeds,21,24 and the occurrence of postweaning anestrus was greatest in purebred sows. s Because the heritability of the WEI has been estimated to be 0.25,24 it is apparent that postweaning anestrus can be decreased through genetic selection and crossbreeding programs. INFLUENCE OF SEASON ON WEANED AND PREGNANT SOWS
The severity of seasonal infertility varies from year to year and from farm to farm. Under most circumstances, the diagnosis occurs after the detrimental effects of seasonal infertility have decreased performance, and insufficient time is available to institute therapeutic or management changes. Because changes in reproductive performance occur over several months, it is not uncommon to overlook seasonal patterns in reproductive activity in commercial swine farms.
510
ALMOND
Weaning-to-Estrus
As previously mentioned, elevated ambient temperature and photoperiod play potential roles in seasonal infertility. A common seasonal change in productivity is the failure of sows to return to estrus within 2 weeks following weaning (Fig. 2). During the winter months, most sows return to estrus within 7 days.12,31 In contrast, it is not unusual for less than 50% of the primiparous sows and less than 75 % of the multiparous sows to show estrus within 7 days following weaning during July, August, and September. s,31 Fortunately, recent improvements in management of the weaned sow have increased the percentage of sows returning to estrus within 7 days after weaning. It is evident that swine producers and veterinarians must be cognizant of the adverse affect of season on the WEI. Because numerous factors, described in the aforementioned discussion, influence a sow's ability to return to estrus, practitioners must consider the relative significance of each factor on a farm-by-farm basis. Establishment and Maintenance of Pregnancy
Seasonal changes in conception and farrowing rates are evident in most swine herds. The precise cause(s) of these seasonal alterations is poorly understood; however, it has been demonstrated that heat stress disrupts implantation and decreases embryo development. 44 Consequently, an increased proportion of bred sows return to estrus at 18 to 24 days or at irregular intervals in the summer months. Farrowing rates, as measured by most record systems, are significantly lower in the subsequent winter months (Fig. 3). Loss of embryos/fetuses after the release of the blastocysts' luteotrophic signal for pregnancy maintenance (days 12 - 13 postbreeding) often results in pseudopregnancy or prolonged periods of anestrus in affected sows. Because fetal or embryonic remnants usually are read-
cn10---------------------------------~ ~
co 2:
~
oS en
9 8
2 7
00
~ 6 ~ C> .~ 5
.......... ........... ,
,.\
.... " , ' \ ........ ".... " \,
•••• ••••••••••• ~!'~~ .. -"',..f.~
....·······..................,~ . \
co Q)
3:
4 _
J M
A-J
J-S
0-0 J-M
A-J
J-S
0-0
Quarter Figure 2. Weaning-to-estrus intervals (WEI) in sows over 2 years in a 1000-sow farm. The months of January to March, April to June, July to September, and October to December are represented by J-M, A-J, J-S, and 0-0, respectively. The increased WEI was most evident in primiparous sows during July to September. Seasonal changes in WEI were less apparent in second-parity females and not detected in the third- to sixth-parity sows.
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW
511
100 95
~ 90 co a: 85 Q)
...
...
C>
c
.§ 0
~ ~
al U.
80 75 70 65J-M
A-J
J-S 0-0 J-M Quarter
A-J
J-S 0-0
Figure 3. Farrowing rates of sows over 2 years in a 1000-sow farm. The months of January to March, April to June, July to September, and October to December are represented by J-M, A-J, J-S, and 0-0, respectively. Note the decreased farrowing rates in primiparous sows during the winter months, subsequent to mating during the summer. The seasonal change in farrowing rate was not evident in multiparous sows.
sorbed, pseudopregnant animals are identified as not-in-pig or failing-to-farrow sows in the fall or early winter months. It has been demonstrated that heat stress results in decreased numbers of embryos and/or fetuses and subsequent decreases in litter size. 44 In contrast, heat stress exerts minimal influence on pregnancy after implantation, although seasonal variations in total pigs born and pigs born alive have been observed in some studies. 53 It has been suggested that when sows are exposed to elevated ambient temperatures in late gestation, death of the sow is more likely than death of the litter. 44
Autumn Abortion Syndrome
The autumn abortion syndrome (AAS) is another reproductive disorder that evidently is part of the seasonal infertility complex. 1 The most common clinical feature of AAS is an increased incidence of noninfectious abortion in sows during the months of September through December. The stage of gestation when abortion occurs ranges from 30 to 110 days postbreeding. 1 Clinical signs and pathologic lesions are absent in the affected sows and fetuses, respectively. In addition, serologic evidence of an infectious agent is lacking. It is evident that a combination of environmental, nutritional, and managerial factors predispose or contribute to the AAS. Marginal energy intake and failure to maintain ambient temperatures in the gestation house when environmental temperatures fall drastically after a preceding warm day, and stressors caused by rapid and vast fluctuations in autumn temperatures, may be involved. 1 In addition, decreasing LH and/or progesterone concentrations in sows, associated with reduced daylight hours encountered in the autumn, may playa significant role in the AAS.57
512
ALMOND
CLINICAL EVALUATION OF PROLONGED WEI
The prevalence of anestrous sows is often over- or underestimated by swine producers. This is especially common when producers use suboptimal estrous detection techniques. Consequently, producers attribute prolonged WEI to seasonal infertility when the major problem is suboptimal management. Because the occurrence of anestrous sows varies from year to year and from farm to farm, the economic impact of prolonged WEI is easily overlooked by producers and veterinarians. Techniques to diagnose and identify anestrous sows include record analysis, slaughterhouse evaluation of ovaries, and analysis of plasma or serum progesterone concentrations. Obviously, estrus is not detected in affected sows, but accurate records are necessary to determine the economic significance of prolonged WEI. Records can be used to compare rates of return to estrus following weaning during the summer months to those of the winter months. If records are not available or if management is suspect, the ovarian morphology may be assessed in representative sows. The ovaries of anestrous sows typically have no corpora lutea in accompaniment with follicles less than 5 mm in diameter.2 The presence of corpora lutea is indicative of ovarian cyclical activity, thereby revealing that estrus did occur but was not observed. Paired samples of blood can be obtained at to-day intervals from anestrous sows and used to assess the percentage of females having cyclical and acyclical ovaries. An elevation in serum P4 concentrations in either or both of the two samples is suggestive of cyclical ovarian activity. Low P4 concentrations «2 ng/mL) in sows is representative of the anestrus condition. 2 To appropriately assess anestrous sows, identification of affected animals must be followed by confirmation of ovarian acyclicity.
POTENTIAL TREATMENTS OF ANESTROUS SOWS
Numerous medical and management treatments have been used in attempts to eliminate postweaning anestrous sows and to reduce the WEI. In some instances, the use of exogenous hormones has been effective in stimulating a resumption of ovarian cyclicity in sows that fail to return to estrus following weaning. Pregnant mare serum gonadotropin (PMSG) combined with human chorionic gonadotropin (hCG) has been used therapeutically in the persistently anestrous sow and prophylactically in the weaned sow to improve postweaning reproductive performance. 32 Treatment of the anestrous sow with PMSG/hCG induces a fertile estrus in sows having acyclic ovaries. 19 When administered at weaning, PMSG decreases the WEI and the proportion of sows experiencing postweaning anestrus. These observations suggest that PMSG is potentially effective for treatment of postweaning anestrus. Unfortunately, the commercial PMSG/hCG product (PG 600, Intervet America, DE) is not federally licensed for use in weaned sows. Other hormonal treatments do not appear as efficacious as PMSG in treatment of postweaning anestrous sows. Treatment with hCG consistently induces ovulation in the anestrous sow but is relatively ineffective in causing estrus. 19 The administration of a single dose of GnRH induces hypophyseal release of endogenous gonadotropins but does not cause estrus or ovulation. 19 The pulsatile administration of GnRH at hourly intervals to anestrous sows induces estrus and ovulation,4 but is impractical for commercial application. Exogenous estradiol t7P (E2) consistently induced estrus but sporadically induced ovulation. 19 The combination
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW
513
of E2 and heG induces estrus and ovulation in anestrous sows but results in poor pregnancy rates and small litter size. 26 The administration of a prostaglandin analogue to primiparous sows on the day of weaning increases the percentage of females returning to estrus within 10 days after weaning and decreases the mean number of days from weaning until estrus. 33 Additional research, however, is needed to confirm the efficacy of prostaglandins in the prophylaxis of postweaning anestrus and in the therapy of persistently anestrous sows. SUMMARY
The majority of sows return to estrus within 2 weeks after weaning. Swine practitioners attempt to optimize production by reducing the WEI. Some sows fail to resume estrous cyclicity after weaning; however, the endocrinologic pathogenesis of these anestrous sows is speculative. The average WEI is influenced by numerous factors, including season, environmental temperature, photoperiod, nutrition, stress, facility design, lactation length, and management practices. It is evident that the majority of these factors have a more profound influence on primiparous sows than on multiparous sows. Optimum protein and energy consumption by sows during lactation and after weaning and effective utilization of breeding facilities reduce the WEI. The precise roles of photoperiodic changes, elevated environmental temperatures, and stress in seasonal infertility remain poorly understood. Fortunately, current management techniques have reduced the WEI on most farms without instituting therapeutic measures. References 1. Almond GW, Friendship RM, Bosu WTK: Autumn abortions in sows. Can Vet J 26:162, 1985 2. Almond GW, Dial GD: Steroid hormone and luteinizing hormone concentrations in the anestrous sow. Can J Vet Res 54:209, 1990 3. Almond GW, Dial GD: Estradiol feedback inhibition of luteinizing hormone concentrations in the anestrous sow. J Anim Sci 68:1077, 1990 4. Armstrong JD, Britt JH: Pulsatile administration of gonadotropin-releasing hormone to anestrous sows: Endocrine changes associated with GnRH-induced and spontaneous estrus. BioI Reprod 33:375, 1985 5. Aumaitre A, Dagorn J, Legault C, et al: Influence of farm management and breed type on sows' conception-weaning interval and productivity in France. Livestock Prod Sci 3:75, 1976 6. Barb CR, Kraeling RR, Rampacek GB, et al: Opioid inhibition of luteinizing hormone secretion in the postpartum lactating sow. BioI Reprod 35:368, 1986 7. Barb CR, Kraeling RR, Rampacek GB, et al: Influence of stage of the estrous cycle on endogenous opioid modulation of luteinizing hormone, prolactin, and cortisol secretion in the gilt. BioI Reprod 35:1162, 1986 8. Becker BA, Ford H, Christenson RK, et al: Cortisol response of gilts in tether stalls. J Anim Sci 60:264, 1985 9. Benjaminsen E, Karlberg K: Post weaning oestrus and luteal function in primiparous and pluriparous sows. Res Vet Sci 30:318, 1981 10. Brandt KE, Diekman MA: Influence of supplemental lighting on serum LH, testosterone and semen quality in prepubertal and post-pubertal boars. Anim Reprod Sci 8:287, 1985 11. Britt JH, Levis DG: Effect of altering suckling intervals of early-weaned pigs on rebreeding performance of sows. Theriogenology 18:201, 1982 12. Britt JH, Szarek VE, Levis DG: Characterization of summer infertility of sows in large confinement units. Theriogenology 20:133, 1983
514
ALMOND
13. Brooks PH, Cole DJA, Rowlinson P, et al: Studies in sow reproduction. 3. The effect of nutrition between weaning and remating on the reproductive performance of multiparous sows. Anim Prod 20:407, 1975 14. Claus R, Weiler U: Influence of light and photoperiodicity on pig prolificacy. J Reprod Fertil Suppl 33:185, 1985 15. Claus R, Schopper 0, Wagner HG, et al: Photoperiodic influences on reproduction of domestic boars. Zbl Vet Med A 32:86, 1985 16. Cox NM, Britt JH: Relationships between endogenous gonadotropin-releasing hormone, gonadotropins, and follicular development after weaning in sows. BioI Reprod 27:70, 1982 17. Cox NM, Britt JH, Armstrong WD, et al: Effect of feeding fat and altering weaning schedule on rebreeding performance in primiparous sows. J Anim Sci 56:21, 1983 18. DeRensis F, Hunter MG, Grant SA, et al: Effect of estrogen administration on endogenous and luteinizing hormone-releasing-hormone-induced luteinizing hormone secretion and follicular development in the lactating sow. BioI Reprod 44:975, 1991 19. Dial GO, BeVier GW, Hixon JE, et al: Endocrine pathogenesis of postweaning anestrus in swine: Response of the persistently anestrous sow to hormonal stimuli. Am J Vet Res 45:1737, 1984 20. Diekman MA, Hoagland TA: Influence of supplemental lighting during periods of increasing or decreasing daylength on the onset of puberty in gilts. J Anim Sci 57:1235, 1983 21. Dyck GW: Puberty, postweaning estrus and estrous cycle length in Yorkshire and Lacombe swine. Can Anim Sci 51:135, 1971 22. Esbenshade KL, Britt JH, Armstrong JD, et al: Body condition of sows across parities and relationship to reproductive performance. J Anim Sci 62:1187, 1986 23. Fahmy MH, Dufour JJ: Effects of postweaning stress and feeding management on return to oestrus and reproductive traits during early pregnancy in swine. Anim Prod 23:102, 1976 24. Fahmy MH, Holtmann WB, Baker RD: Failure to recycle after weaning, and weaning to oestrus interval in crossbred sows. Anim Prod 29:193, 1979 25. Foxcroft GR, Shaw HJ, Hunter MG, et al: Relationships between luteinizing hormone, follicle-stimulating hormone and prolactin secretion and ovarian follicular development in the weaned sow. BioI Reprod 36:175, 1987 26. Friendship RM, Bosu WTK, King GJ: Reproductive performance in sows treated with estradiol benzoate/human chorionic gonadotropin combination at weaning. Can J Comp Med 46:410, 1982 27. Friendship RM, Wilson MR, Almond GW, et al: Sow wastage: Reasons for and effect on productivity. Can J Vet Res 50:205, 1986 28. Greenberg LG, Mahone JP: Failure of a 16 h L: 8 h 0 or an 8 h L: 16 h 0 photoperiod to influence lactation or reproductive efficiency in sows. Can J Anim Sci 62:141, 1982 29. Hays VW, Krug JL, Cromwell GL, et al: Effect of lactation length and dietary antibiotics on reproductive performance of sows. J Anim Sci 46:884, 1978 30. Hemsworth PH, Salden NTCJ, Hoogerbrugge A: The influence of the post-weaning social environment on the weaning to mating interval of the sow. Anim Prod 35:41, 1982 31. Hurtgen JP, Leman AD, Crabo B: Seasonal influence on estrous activity in sows and gilts. J Am Vet Med Assoc 176:119, 1980 32. Hurtgen JP, Leman AD: Use of PMSG in the prevention of seasonal postweaning anestrus in sows. Theriogenology 12:207, 1979 33. Jochle W, Ceme F: Clinical evaluation of a new prostaglandin analog in pigs: 2. Prophylaxis and therapy of anestrus after weaning in sows and first litter gilts. Theriogenology 19:481, 1983 34. King GJ: Effects of several weaning procedures on the interval of estrus in sows. Can J Anim Sci 54:251, 1974 35. King RH, Williams IH, Barker I: Induction of oestrus in anestrous, first litter sows with pregnant mare's serum gonadotropin. Anim Reprod Sci 5:41, 1982 36. King RH, Williams IH: The effect of nutrition on the reproductive performance of first-litter sows. 2. Feeding level during lactation, and between weaning and mating. Anim Prod 38:241, 1984 37. King RH, Dunkin AC: The effect of nutrition on the reproductive performance of
FACTORS AFFECTING THE REPRODUCTIVE PERFORMANCE OF THE WEANED SOW
38. 39. 40. 41. 42. 43. 44. 45. 46. 47. 48. 49. 50. 51. 52. 53. 54. 55. 56. 57.
515
first-litter sows. 4. The relative effects of energy and protein intakes during lactation on the performance of sows and their piglets. Anim Prod 42:319, 1986 Liptrap RM: Effect of corticotropin and corticosteroids on oestrus, ovulation and oestrogen excretion in the sow. J Endocrinol 47:197, 1970 Mabry JW, Coffey MT, Seerley RW: Comparison of an 8- versus 16-hour photoperiod during lactation on suckling frequency of the baby pig and maternal performance of the sow. J Anim Sci 57:292, 1983 MacLean CW: Observations on noninfectious infertility in sows. Vet Rec 85:675, 1969 McGlone H, Stansbury WF, Tribble LF, et al: Photoperiod and heat stress influence on lactating sow performance and photoperiod effects on nursery pig performance. J Anim Sci 66:1915, 1988 Muirhead MR: A comparison of different systems of sow housing and management. Pig Vet Soc Proc 8:18, 1981 Noblet J, Etienne M: Metabolic utilization of energy and maintenance requirements in lactating sows. J Anim Sci 64:774, 1987 Omtvedt IT, Nelson RE, Edwards RL, et al: Influence of heat stress during early, mid and late pregnancy of gilts. J Anim Sci 32:312, 1971 Perera ANM, Hacker RR: The effects of different photoperiods on reproduction in the sow. J Anim Sci 58:1418, 1984 Renaud G, Guay P, Beauregard M, et al: Anoestrus dans un troupeau de truies: Etude conico-pathologique. Can Vet J 13:94, 1972 Schmidt WE, Stevenson JS, Davis DL: Reproductive traits of sows penned individually or in groups until 35 days after breeding. J Anim Sci 60:755, 1985 Shaw HJ, Foxcroft GR: Relationships between LH, FSH and prolactin and reproductive activity in the weaned sow. J Reprod Fertil 75:17, 1985 Stevenson JS, Cox NM, Britt JH: Role of the ovary in controlling luteinizing hormone, follicle stimulating hormone, and prolactin secretion during and after weaning in sows. BioI Reprod 24:341, 1981 Stevenson JS, Britt JH: Interval to estrus in sows and performance of pigs after alteration of litter size during late lactation. J Anim Sci 53:177, 1981 Stevenson JS, Pollman DS, Davis DL, et al: Influence of supplemental light on sow performance during and after lactation. J Anim Sci 56:1282, 1983 Teague HS, Roller WL, Grifo AP: Influence of high temperatures and humidity on the reproductive performance of swine. J Anim Sci 27:408, 1968 Tomes GJ, Nielson HE: Seasonal variations in the reproductive performance in sows under different climatic conditions. World Review Anim Prod 15:9-19, 1979 Varley MA, Cole DJA: Studies in sow reproduction. 4. The effect of level of feeding in lactation and during the interval from weaning to remating on the subsequent reproductive performance of the early weaned sow. Anim Prod 22:71, 1976 Walker N, Watt D: The effect of weaning at 10, 25, or 40 days on the reproductive performance of sows from the first to the fifth parity. J Agric Sci Camb 92:449, 1979 Walton JS: Effect of boar presence before and after weaning on estrus and ovulation in sows. J Anim Sci 62:9, 1986 Wrathall AE, Wells DE, Jones PC, et al: Seasonal variations in serum progesterone levels in pregnant sows. Vet Rec 118:685, 1986
Address reprint requests to Glen W. Almond, DVM, MSc, PhD Department of Food Animal and Equine Medicine North Carolina State University College of Veterinary Medicine 4700 Hillsborough Street Raleigh, NC 27606