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Stress and its influence on reproduction in pigs: a review
Acta Veterinaria Scandinavica volume 50, Article number: 48 (2008)
The manifestations of stress, defined as a biological response to an event that the individual perceives as a threat to its homeostasis, are commonly linked to enhanced activity of the hypothalamo-pituitary-adrenal (HPA) axis and the activation of the sympathetic adreno-medullary (SA) system. Activation of the HPA system results in the secretion of peptides from the hypothalamus, principally corticotropin releasing hormone (CRH), which stimulates the release of adrenocorticotropic hormone (ACTH) and beta-endorphin. ACTH induces the secretion of corticosteroids from the adrenal cortex, which can be seen in pigs exposed to acute physical and/or psychological stressors. The present paper is a review of studies on the influence of stressors on reproduction in pigs. The effects of stress on reproduction depend on the critical timing of stress, the genetic predisposition to stress, and the type of stress. The effect of stress on reproduction is also influenced by the duration of the responses induced by various stressors. Prolonged or chronic stress usually results in inhibition of reproduction, while the effects of transient or acute stress in certain cases is stimulatory (e.g. anoestrus), but in most cases is of impairment for reproduction. Most sensitive of the reproductive process are ovulation, expression of sexual behaviour and implantation of the embryo, since they are directly controlled by the neuroendocrine system.
Definition of stress
Stress can be defined in many ways, but one of the most accepted definitions is a biological response to an event that the individual perceives as a threat to its homeostasis . Perception of stressful stimuli leads e.g. to activation of the hypothalamo-pituitary-adrenal (HPA) system, which in turn results in the release of a variety of peptides, principally corticotropin releasing hormone (CRH) and vasopressin from the hypothalamus . CRH stimulates the release of adrenocorticotrophic hormone (ACTH) and other proopiomelanocortin (POMC) derived peptides, such as β-endorphin from the anterior lobe of the pituitary gland. ACTH acts on the adrenal glands and causes secretion of glucocorticoid hormones, e.g. cortisol. ACTH also causes the release of other hormones from the adrenal glands, e.g. progesterone, possibly prostaglandin F2α metabolite  and even inhibin α . Stress also involves the activation of the sympathetic nervous system and the adrenal medulla. This causes the release of catecholamines e.g. adrenaline and noradrenaline into the bloodstream, leading to an increase in the glucose supply by accelerating the degradation of glycogen in the liver . The glucocorticoids also stimulate lipolysis and gluconeogenesis (the conversion of amino acids to glucose), which leads to an increased metabolism that promotes the ability to cope with stress .
Assessment of stress
There are many difficulties involved in evaluation of, and comparing how different types of stress affect animal welfare in general, especially in long-term stressful situations. Stress response can be assessed by determining the activation of the HPA-axis and/or the sympathetic adreno-medullay (SA) system, by measuring the level of secreted peptides in the peripheral blood plasma, urine, cerebrospinal fluid, saliva, etc. Behavioural responses such as heart rate, blood pressure and stereotypical behaviour, as well as the effects on the immune response can also be used for the assessment of stress response [7–10]. However meaningful evaluation of these responses requires a detailed knowledge of the normal physiological and behaviour patterns of the animal studied, because the response to stress is influenced by several factors such as the metabolic condition, health status, age, sexual maturity. The stress response is equally dependant on the nature, intensity and duration of the stressful event. Also, there is a large individual variation between pigs in their ability to cope with stress and the fact that each stressor both has a non-specific effect (stimulation of the HPA-axis) and a specific effect. The latter is the "biological target" for the stressor. Heat stress, for example, leads to hyperthermia of the sow, food deprivation to a catabolic metabolism. For this reason, there is no stressor that can be used as a standard stressor to evaluate stress response in general. The specific response of each stressor has to be evaluated separately.
The present paper is a review of some studies on the influence of stressors on reproduction in pigs in terms of environment, management and housing like lactation, weaning, transportation/relocation, grouping. Also, in a series of experimental studies from our own group, stress was simulated with fasting or repeated ACTH treatments for approximately 48 hours.
Temperature and humidity
Pigs have a low capacity for increased sweating when the ambient temperature increases e.g. from 23 to 34°C, which contributes to the close relationship between environmental temperature and scrotal and testicular temperatures during such periods . Lowered fertility and/or lowered total sperm counts (TSC) and decreased ejaculate volume have been found in boars during or shortly after the warm summer period in several countries with temperate areas such as Europe and North America [12–15]. In tropical areas such as Thailand temperature has a significant negative effect on both the ejaculate volume, TSC and the morphology of the spermatozoa [16–18].
In recent years, a new housing system, called an evaporative cooling system (EVAP) or tunnel ventilation, has been introduced to improve the microclimate for livestock production in regions with hot climate . The EVAP system is a closed housing system, which aims to reduce the temperature via humidification process. In a comprehensive Swedish/Thai study sperm production and sperm morphology was recorded in boars kept in EVAP system vs conventional housing system (CONV) [16–18]. Temperature and humidity were recorded on a daily basis during one calender year. There was a higher diurnal variation and range over the year for both temperature and humidity in the CONV system compared to the EVAP system. The average maximum temperature was lower and the average minimum humidity was higher in the EVAP system, than in the CONV system. There was no overall difference in sperm production and sperm morphology between boars kept in the CONV and the EVAP housing systems. However, during parts of the year, differences between systems in sperm production and sperm morphology were observed. Elevated temperature had a significant negative effect on both the ejaculate volume and TSC in both housing systems. Elevated humidity had a significant negative effect on both the ejaculate volume and TSC in the EVAP system. To further minimize the negative impact of high temperature and high humidity on sperm production of boars under tropical conditions, further investigations on economically competetive technologies that can decrease both temperature and humidity are needed.
In several experiments the effect of elevated temperature (in terms of heat stress) on the spermatogenesis of boars has been investigated using a climatic chamber. McNitt and First  found a reduced TSC and an increased percentage of abnormal spermatozoa around two weeks after placing boars in a climatic chamber at 33°C and 50% RH (% relative humidity) for 72 hours. Exposure of boars for 35°C and 40% RH for 100 hours resulted in decreased sperm quality, in terms of an increased percentage of abnormal spermatozoa; the ejaculate volume and TSC per ejaculate remained unaltered . Additionally, local heating of the scrotum has caused similar disturbances in spermatogenesis [21, 22]. In most studies, an increased proportion of abnormal spermatozoa has been found after heat treatment, but the results vary among boars, and are also related to the different regimes for causing heat stress [20, 23–25]. An acute rise in rectal temperature related to the detrimental effects on the testes was observed in some heat exposed boars . This indicates that the stress, imposed by elevated ambient temperature, may not be of the same magnitude for all boars.
Gilts and sows
Heat stress has been reported to reduce implantation and impair embryo development in pig. Edwards et al  found that gilts are more sensitive to heat stress before day 15 of pregnancy, than during days 15–30 post-breeding. Omtvedt et al.  illustrated a greater reduction in the number of viable embryos among gilts exposed to elevated temperatures during days 8–16 post-breeding than days 0–8, indicating that the time of implantation would be the most sensitive stage of pregnancy to stress.
High ambient temperature leading to heat stress has been associated with seasonal infertility. This is especially true not only in tropical areas, for example in Thailand, where the temperature exceeds 30°C for several months of the year , but also in temperate areas, for example in countries in northern Europe and the USA [29–31]. In the referred comprehensive Swedish/Thai field study performed in Thailand, there was a significant influence by climate, maximum temperature and heat index on litter size, farrowing rate and weaning to first service interval . Several experimental studies have been performed using two or more temperature levels kept constant over the day at a low or moderate relative humidity [32–34]. In these studies a prolonged weaning-to-service interval was recorded at the high temperatures; this prolongation has been reported to associate partly with a reduced appetite [33, 35]. Suriyasomboon et al.  collected daily climatic (temperature, relative humidity) data within a number of herds in Thailand during one calender year. They found a seasonal variation in reproductive performance of the sows, but there was no indication that high temperature and humidity at previous weaning/mating or at farrowing had negative effects on litter size.
Short lactation and weaning
Several technical improvements have made it possible to carefully study e.g. follicles, cysts and corpora lutea in the ovaries  and their relationship to husbandry practice like short lactation, weaning and housing. Before introduction of transrectal ultrasonography [38, 39] the only possible ways to study the ovaries in pigs were either to inspect and make morphological examinations after slaughter , or to carry out laborious laparoscopic examinations [41, 42].
Kunavongkrit  performed comparative clinical and endocrine studies of sows, when all piglets were removed from their dams within 12 hours of farrowing, called "zero-weaning". Using repeated laparoscopic examination, he could endocrinologically compare sows that showed oestrus within 2 weeks after parturition and developed ovarian cysts (anovulatory) with sows that ovulated regularly . None of the anovulatory sows had a well defined pre-ovulatory LH surge. The peripheral plasma concentration of cortisol was significantly higher in the anovulatory than in the ovulatory sows , indicating that elevated cortisol might be one factor inhibiting the LH surge. It is noteworthy that some pairs of full sibs behaved similarly following zero-weaning. Hereditary factors may thus play a role in the development of ovarian cysts in pigs.
A husbandry practice like weaning seems to be a stressful stimulus for the sow. Thus, weaning after five weeks of lactation resulted in a concomitant increase of plasma concentrations of cortisol and β-endorphin [45, 46]. Sows in good nutritional status, which failed to resume oestrous activity after weaning had significantly higher plasma concentrations of cortisol and β-endorphin and lower LH concentrations around weaning than sows that resumed oestrous activity .
There are a few reports of acute stressors stimulating various aspects of reproduction. Thus, Hughes  showed that transport of female pigs advanced the onset of puberty. Combined clinical and endocrinological studies have been performed on the effect of transportation and/or relocation on gilts with delayed puberty  and anoestrous sows [50, 51]. Approximately 75% of the gilts with delayed puberty and 75% of the anoestrous sows showed ovulatory oestrus within one week, after approximately one hour of transportation. The pulse frequency of LH increased significantly right after transportation, and increased oestradiol-17β concentrations were detected in utero-ovarian vein plasma 8–16 hours after transportation, or 24–36 hours earlier than in jugular blood. The increased LH activity following transportation indicates that the hypothalamus and/or the higher brain centre of these animals responded by increased activity to this short-term stress. In a subsequent study, Dalin et al.  showed that the plasma concentrations of both cortisol and catecholamines are elevated in pigs that are transported. Transportation/relocation might therefore act as a positive stressor on hypothalamus in anoestrous female pigs.
The release of catecholamines occurs very rapidly after stress exposure [52, 53], and the plasma half-life of the amines is extremely short, which makes it difficult to determine an accurate and yet comparable timing in different treatments. Moreover, the validity of measurement of venous blood plasma noradrenaline has been questioned, because regional or general differences in sympathetic activity may not be reflected accurately in venous blood samples taken from a single site . Therefore, cortisol is still considered a more valid blood parameter reflecting stress in clinical studies of adult pigs.
The management procedures in modern pig production include a number of events, which might act as stressors on the animals, e.g. high stocking densities, barren environments, transportation, poor or aggressive human-animal interactions and heat stress. Due to welfare consideration, systems with loose-housed sows instead of system with crates/stalls for the sows have become common, at least for non-lactating sows. These systems have several advantages: i.e. the animals have possibility to perform their natural behaviour. However, there are factors in these systems causing problems. In systems with loose-housed sows, the number of sows are in most cases much higher than in groups formed in the wild. The female pigs form family units of one or several sows and their offsprings , and the individuals in the family unit avoid contact with other unfamiliar sows . Therefore, in wild pigs (Sus scrofa) confrontation between unfamiliar female pigs happens very rarely. In commercial group housing systems, however, mixing of unfamiliar sows is difficult to avoid. A drawback with the group-housing system is also the difficulty to avoid regrouping. In most lactation units the sows are housed individually, and grouping of unfamiliar sows usually takes place at least once after weaning. A new social grouping in a limited space results in aggressive behaviour among the animals. Depending on the social status of the animal, i.e. dominant or subordinate, different individuals have various capabilities in competing situations such as feeding and watering. An animal that does not cope with these situations may have a reduced well-being and impaired reproductive performance. High ranked sows in oestrus will also mount submissive sows, and will rise to periods of stress . Elevated stress levels in a newly formed small group of sows may persist for approximately two days until a ranking order is established among the animals , and even continue for additional 10–12 days in large groups of sows .
Peltoniemi et al.  found that rebreeding was performed more often after an irregular oestrus-to-oestrus interval, i.e. 25–37 days in group housed sows than in sows kept in individual stalls, particularly during summer and autumn. Kongsted  described the impaired reproduction in group housed sows as a growing problem in many herds. Group housing conditions resulted in fewer born piglets per litter when comparing with individually housed sows [61, 62]. Moreover, Pedersen et al.  reported that group housing may result in the impairment of heat detection and response to boar stimulation. In a comprehensive study by Karlén et al.  on welfare including reproduction of gestating sows in conventional stalls and large groups on deep litter, sows on deep litter had a higher return to oestrus after mating (13% versus 7 %, p < 0.01) and there was a tendency (p = 0.06) for higher salivary cortisol concentrations in week one of gestation in deep litter sows (the sows were recently mated when they entered respective treatment). However, measurement of cortisol in saliva is not always a reliable method to monitor stress in pigs . Altogether, the reproductive parameters recorded show that sows in stalls weaned the equivalent of 39 more piglets per 100 mated sows than sows in large groups. The results suggest that sows in large groups on deep litter faced greater welfare challenges in the early stages of gestation, all possibly a consequence of aggression. In contrast, sows in stalls faced greater welfare challenges later in gestation based on a higher incidence of feet and leg problems. In addition, the evidence of stereotypical behaviour may indicate some disadvantages for sows kept in stalls for the whole gestation. On the other hand, Cassar et al. , investigating mixed-parity sows assigned to be housed individually or in groups of 15 from the time of insemination and for 5 weeks, found no effect of grouping per se on farrowing rate or subsequent litter sizes.
Recently an excellent study was presented by Munsterhjelm et al.  investigating in 12 replicates of 40 sows the effects of housing on pregnancy rate 28 days post-service, early disruption of pregnancy and behaviour. Half of the dry sows were kept in stalls, and half were group-housed on 5 m2 deep litter per sow. Stall-housing was associated with signs of stress caused by the lack of exercise and a rootable substrate. Behavioural indicators proposed a lower welfare level in stalled animals compared with group-housed ones. This type of stress – or the level thereof – did affect reproduction in terms of weaning-to-oestrus interval, rebreeding rate and irregular rebreeding (% of rebreedings) significantly less than the social stress experienced by group-housed sows.
Soede et al.  investigated hormone patterns, oestrus, ovulation and early embryo development in multiparous sows that had been tethered during lactation, and after weaning were either tethered by neck chain, or individually housed in a pen of approximately 6 m2. The registration of above mentioned parameters started at two months after weaning (the sows were not mated in the post-wening oestrus, and altrenogest treatment was given for oestrous synchronization). The profiles of oestradiol-17β, LH and progesterone around oestrus were similar for both treatment groups, while the duration of oestrus was shorter in the tethered sows. The sows were euthanised day 5 after ovulation; ovulation rate, fertilization rate, embryo development and embryo diversity were similar for the two groups. The results from this study indicate that sows that had been tethered during lactation, and were housed loose or were tethered again at weaning, differed in stereotypic behaviour and in duration of oestrus, without effects on reproductive hormones, two months later.
In a recent study Soede et al.  investigated the effect of repeated stress treatments during the follicular phase and early pregnancy on reproductive performance of gilts. All gilts were housed individually. The animals given a stressful treatment were grouped for half an hour at the start of the treatment and during the treatment period nose-sling and an unpredictable feeding scheme were applied regularly. Despite this rather harsh treatment, saliva cortisol levels and even the reproductive performance were not disturbed. A possible reason for lack of changes in cortisol levels might be related to findings that measurement of cortisol in saliva is not always an accurate method to monitor stress in pigs . It is also plausible that gilts used by Soede et al.  were particularly resistant to imposed negative handling treatment.
Stress simulated by ACTH treatment during pro-oestrus/oestrus
High doses of ACTH (daily intramuscular injections) administered for several days during the follicular phase during the oestrous cycle (from days 16–18 until the end of oestrus)  caused a delay in the onset of oestrus and development of cystic follicles in sows. In an earlier study Liptrap  had clearly demonstrated that cystic follicles were induced in adrenal intact sows by treatment with high doses of ACTH, but not in adrenalectomized sows. These results indicate that the disruption of the ovarian function was caused by cortisol, released from the adrenal glands by exogenous ACTH.
To simulate "stressful" events after weaning and around pro-oestrus/oestrus like aggressive behaviour among sows after grouping/mixing, competetive situations at feeding and drinking, riding etc. repeated injections of small doses of ACTH were given for approximately 48 hours to multiparous healthy sows in a series of experiments (performed by our own research group). Follicular growth and ovulation were monitored using ultrasonography. Blood samples were collected frequently before, during and after treatment.
ACTH given for 48 hours during pro-oestrus
Onset of oestrus was predicted based upon the individual progesterone profile and the time for reaching a progesterone concentration < 8 nmol/L . The interval between the time when progesterone reached a level of < 8 nmol/L and onset of oestrus was prolonged with 2.5 days in the ACTH-cycles vs the control-cycles. At onset of oestrus, the follicles were larger in the ACTH sows than in the control sows. In some sows, ovulation was disturbed.
Administration of ACTH for up to 48 hours from onset of oestrus to ovulation
Cortisol and progesterone were significantly elevated in jugular blood samples [3, 10]. The display of signs of standing oestrus went away more rapidly after ovulation due to the rise in progesterone concentrations, but there was no effect on the time of ovulation.
When insemination was performed once, approximately 18 hours before ovulation and the sows were anesthetized/killed at 4–8 hours after ovulation, there was a tendency towards a larger number of spermatozoa in the UTJ and oviduct among the ACTH sows compared with the control sows [10, 73]. The majority of spermatozoa seemed to have intact membranes. A majority of sows in the ACTH group had moderately to exaggerated amounts of mucus in the intraluminal environment of the sperm reservoir, which might be due to the higher progesterone concentrations than the control group [10, 74].
In a subsequent study the sows were killed at 48 or 60 hours after ovulation and retrieval rate of embryos and oocytes and their localization were investigated [10, 75]. Fewer oocytes/embryos were retrieved from the ACTH group than from the control group (51% vs 81%, P < 0.05). There was also a tendency towards faster embryo transportation to the uterus in the ACTH group, perhaps due to the high progesterone concentrations during treatment.
Stress induced by food deprivation or ACTH treatment for 48 hours during two periods of the early pregnancy
Multiparous sows were deprived of food (FD), but had free access of drinking water, or were treated with ACTH for 48 hours after ovulation. There was a delayed embryonic cleavage rate and a decreased number of spermatozoa attached to zona pellucida (ZP) in FD sows, reflecting a change in the oviductal environment [76, 77]. Postovulatory food deprivation also delayed the oviductal ova transport rate [6, 78], which may be due to a prostaglandin-associated prolonged contraction of the isthmic muscle [79, 80]. ACTH had no effect on the oviductal transport rate of the embryos, but a negative effect on the embryo development in terms of cleavage rate and a lower number of spermatozoa attached to the ZP compared with the controls [6, 81, 82].
Food deprivation during days 10 and 11 of pregnancy did not cause any effect on embryo recovery rate at day 17 of pregnancy [45, 83]. When the treatments (FD or ACTH) were performed during days 13 and 14 of pregnancy, there was a significant effect on endocrine status of the sows during the treatment period. Both FD and ACTH sows had increased levels of cortisol, but only FD sows had increased levels of progesterone and PGF2α-metabolite [6, 83]. There were no effects on total number of foetuses or foetal survival rate, observed at day 30 of pregnancy [6, 84, 85]. However, the progesterone concentration of the allantoic fluid of FD sows at day 30 was increased compared with controls and also correlated to the size of the placentas. ACTH stimulation caused a two-day delay in the increase of plasma oestrone concentration, seen at day 19 of pregnancy in control sows. In gilts, injected with hydrocortisone acetate at 12-hour intervals from day 11 to day 20 of pregnancy, a two-day delay of the peak of oestrone sulphate was also observed [86, 87]. The absence of effects on the embryo survival at day 30 might be due to: (1) large individual variation in the ability to cope with stress in combination with relatively small groups, (2) the degree of stress was not severe enough, or the sows were not exposed to the treatments for a long enough period of time. It must also be taken into account that the sows used in the study were in very good nutritional and physical condition, and as reproduction is the most important activity of any species, the capacity to compensate for the effects of stress is very well developed.
The effects of stress on reproduction depend on the critical timing of stress, the genetic predisposition to stress, and the type of stress. The effect of stress on reproduction is also influenced by the duration of the responses induced by various stressors. Prolonged or chronic stress usually results in inhibition of reproduction, while the effects of transient or acute stress in certain cases is stimulatory (e.g. anoestrus), but in most cases is of impairment for reproduction. Most sensitive of the reproductive process are ovulation, expression of sexual behaviour and implantation of the embryo, since they are directly controlled by the neuroendocrine system.
Moberg GP: A review – developing management strategies to reduce stress in pigs: a new approach utilizing the biological cost of stress. Manipulating Pig Production IV. 1993, Australiaasian Pig Science Association, Attwood, ES Batterham, 116-126.
Buckingham JC, Cowell A-M, Gillies GE, Herbison AE, Steel JH: The neuroendocrine system: anatomy, physiology and responses to stress. Stress, stress hormones and the immune system. Edited by: Buckingham JC, Gillies GE, Cowell A-M. 1997, John Wiley & Sons, Ltd, Chichester, 9-47.
Madej A, Mwanza A, Kindahl H, Einarsson S: Effect of ACTH and CRH on plasma levels of cortisol and prostaglandin F2α metabolite in cycling gilts and castrated boars. Acta Vet Scand. 2005, 46: 249-256. 10.1186/1751-0147-46-249.
Brandt Y, Lundeheim N, Madej A, Rodriguez-Martinez H, Einarsson S: Effects of ACTH injections during estrus on concentrations and patterns of progesterone, estradiol, LH, and inhibin α and time of ovulation in the sow. Domestic Animal Endocrinology. 2007, 32: 122-137. 10.1016/j.domaniend.2006.02.002.
Vellucci SV: The autonomic and behavioural response to stress. Stress, stress hormones and the immune System. Edited by: Buckingham JC, Gillies GE, Cowell A-M. 1997, John Wiley & Sons, Ltd, Chichester, 49-70.
Razdan P: Stress and early pregnancy in sows. Effects on endocrinology, ova transport and embryo development. Doctoral thesis, Veterinaria 153, Acta Universitatis Agriculturae. 2003, Sueciae, Swedish University of Agricultural Sciences Uppsala
Kelley KW: Cross-talk between the immune and endocrine systems. J Anim Sci. 1988, 66: 2095-2108.
Broom DM: Animal Welfare: Consepts and measurements. J Anim Sci. 1991, 69: 4167-4175.
Vellucci SV: Assessment of the autonomic and behavioural effects of stress. Stress, stress hormones and the immune System. Edited by: Buckingham JC, Gillies GE, Cowell A-M. 1997, John Wiley & Sons, Ltd, Chichester, 157-171.
Brandt Y: The effect of ACTH during oestrus on the reproduction in the sow with special reference to duration of oestrus, ovulation, hormonal patterns, gametes and early embryo development. Doctoral thesis, number14, Acta Universitatis Agriculturae Sueciae. 2006, Faculty of Veterinary Medicine and Animal Science
Stone BA: Therma characteristics of the testis and epididymis of the boar. J Reprod Fertil. 1981, 63 (2): 551-557.
Thibault C, Courot M, Martinet L, Mauleon P, Du Mesnil du Buisson F, Ortavant R, Pelletier J, Signoret JP: Regulation of breeding season and oestrous cycles by light and external stimuli in some mammals. Environmental influences on reproductive processes. J Anim Sci. Edited by: Hansel W, Dutt RH. 1966, 25 (Suppl): 119-142.
Einarsson S: Factors affecting fertility in artificial insemination of swine. Nordisk Veterinaermedicin. 1968, 20: 622-629.
Stone BA: Between and within herd variations in conception rates in pig herds in the lower North of South Australia. Agric Rec S Aust. 1977, 4: 22-25.
Colenbrander B, Feitsma H, Grooten HJ: Optimizing semen production for artificial insemination in swine. J Reprod Fertil Suppl. 1993, 48: 207-215.
Suriyasomboon A: Herd investigations on sperm production in boars and sow fertility under tropical conditions, with special reference to season, temperature, and humidity. Doctoral thesis, number 72, Acta Universitatis Agriculturae Sueciae. 2005, Faculty of Veterinary Medicine and Animal Science
Suriyasomboon A, Lundeheim N, Kunavongkrit A, Einarsson S: Effect of temperature and humidity on sperm production in Duroc boars under different housing systems in Thailand. Livestock Production Science. 2004, 89: 19-31. 10.1016/j.livprodsci.2003.12.008.
Suriyasomboon A, Lundeheim N, Kunavongkrit A, Einarsson S: Effect of temperature and humidity on sperm morphology in Duroc boars under different housing systems in Thailand. The Journal of Veterinary Medical Science. 2005, 67: 777-785. 10.1292/jvms.67.777.
McNitt JL, First NL: Effects of 72-hour heat stress on semen quality in boars. Int J Biometerol. 1970, 14: 373-380. 10.1007/BF01462914.
Larsson K, Einarsson S: Seminal changes in boars after heat stress. Acta Vet Scand. 1984, 25: 57-66.
Malmgren L: Experimentally induced testicular alterations in boars: morphology changes in mature and peripubertal boars. Zentralbl Veterinarmed A. 1989, 36 (6): 411-420.
Malmgren L, Larsson K: Experimentally induced testicular alterations in boars: histological and ultrastrucural findings. Zentralbl Veterinarmed A. 1989, 36 (1): 3-14.
Wettemann RP, Wells ME, Omstvedt IP, Pope CE, Turman EJ: Influence of elevated ambient temperature on reproductive performance of boars. J Anim Sci. 1976, 42: 664-669.
Cameron RD, Blackshow AW: The effect of elevated ambient temperature on spermatogenesis in the boar. J Reprod Fertil. 1980, 59 (1): 173-179.
Malmgren L: Induced testicular alterations in peripubertal and mature boars: with special reference to the attainment of spermatogenesis, structure of seminiferous epithelium, sperm morphology and fertility. Docoral thesis. 1993, Department of Obstetrics and Gynaecology, Faculty of Veterinary Medicine, Swedish University of Agricultural Sciences, Uppsala
Edwards RL, Omtvedt IT, Turman EJ, Stephens DF, Mahoney GWA: Reproductive performance of gilts following heat stress prior to breeding and in early gestation. J Reprod Fertil. 1968, 52 (Suppl): 47-61.
Omtvedt IT, Nelson RE, Edwards RL, Stephens DF, Turman EJ: Influence of heat stress during early, mid and late pregnancy of gilts. J Anim Sci. 1971, 32: 312-317.
Tantasuparuk W, Lundeheim N, Dalin AM, Einarsson S: Reproductive performance of purebred Landrace and Yorkshire sows in Thailand with special reference to seasonal influence and parity number. Theriogenology. 2000, 54: 481-496. 10.1016/S0093-691X(00)00364-2.
Peltoniemi OA, Love RJ, Heinonen M, Tuovinen , Saloniemi H: Seasonal and management effects on fertility of the sow: a descriptive study. Anim Reprod Sci. 1999, 55: 47-61. 10.1016/S0378-4320(98)00159-6.
Tummaruk P, Lundeheim N, Einarsson S, Dalin AM: Reproductive performance of purebred Swedish landrace and Swedish Yorkshire sows: I. Seasonal variation and parity influence. Acta Agric Scand Sect A Anim Sci. 2000, 50: 205-216. 10.1080/090647000750014331.
Wettemann RP, Bazer FW: Influence of environmental temperature on prolificacy of pigs. J Reprod Fertil Suppl. 1985, 33: 199-208.
Prunier A, Dourmad JY, Etienne M: Effect of light regimen under various ambient temperatures on sow and litter performance. J Anim Sci. 1994, 72: 1461-1466.
Prunier A, Messias de Braganca M, Le Dividich L: Influence of high ambient temperature on performance of reproductive sows. Livestock Production Science. 1997, 52: 123-133. 10.1016/S0301-6226(97)00137-1.
Wettemann RP, Bazer FW, Thatcher WW, Caton D, Roberts RM: Conceptus development, uterine response, blood gases and endocrine function of gilts exposed to increased ambient temperature during early pregnancy. Theriogenology. 1988, 30: 57-74. 10.1016/0093-691X(88)90263-4.
Koketsu Y, Dial GD, Pettigrew JE, Marsh WE, King VL: Characterization of feed intake patterns during lactation in commercial swine herds. J Anim Sci. 1996, 74: 1202-1210.
Suriyasomboon A, Lundeheim N, Kunavongkrit A, Einarsson S: Effect of temperature and humidity on reproductive performance of crossbred sows in Thailand. Theriogenology. 2006, 65: 606-628. 10.1016/j.theriogenology.2005.06.005.
Madej A, Brandt , Einarsson S: Endocrine dynamics associated with follicle development in pigs: a review. Animal Reproduction. 2009, 6: 135-143.
Soede NM, Nordhuizen JPTM, Kemp B: The duration of ovulation in pigs, studied by transrectal ultrasonography, is not related to early embryonic diversity. Theriogenology. 1992, 38: 653-666. 10.1016/0093-691X(92)90028-P.
Dalin A-M, Nanda T, Hultén F, Einarsson S: Ovarian activity at naturally attained oestrus in the sow. An ultrasonographic and LH study. Acta Vet Scand. 1995, 36: 377-382.
Kunavongkrit A, Einarsson S, Settergren I: Follicular development in primiparous lactating sows. Anim Reprod Sci. 1982, 5: 47-56. 10.1016/0378-4320(82)90036-7.
Kunavongkrit A: Clinical, morphological and endocrinological studies in primiparous post patum sows. Doctoral thesis. 1984, Departments of Obstetrics and Gynaecology, Clinical Chemistry, Faculty of Veterinary Medicine, Swedish University of Agricultural Sciences, Uppsala
Kunavongkrit A, Kindahl H, Andersson AM: Laparoscopy in post partum sows with special emphasis on the effects of uterine manipulation on the release of prostaglandin F2α. Res Vet Sci. 1984, 36: 66-70.
Kunavongkrit A, Edqvist LE, Einarsson S: Clinical and endocrinological studies in primiparous zero-weaned sows. 3. Hormonal patterns of ovarian disorders due to zero-weaning. Zentralbl Veterinarmed A. 1983, 30 (8): 625-636.
Kunavongkrit A, Madej A, Einarsson S: Plasma levels of cortisol in zero-weaned and lactating sows during the first two weeks post partum. Domestic Animal Endocrinology. 1984, 1: 217-223. 10.1016/0739-7240(84)90002-X.
Tsuma VT: Clinical and endocrine studies in primiparous sows. Effects of weaning during lactation and of group housing and fasting during early pregnancy. Doctoral thesis. 1995, Departments of Obstetrics and Gynaecology, Physiology, Clinical Chemistry, Faculty of Veterinary Medicine, Swedish University of Agricultural Sciences, Uppsala
Tsuma VT, Einarsson S, Madej A, Lundeheim N: Cortisol and β-endorphin levels in peripheral circulation around weaning in primiparous sows. Anim Reprod Sci. 1995, 37: 175-182. 10.1016/0378-4320(94)01330-O.
Tsuma VT, Einarsson S, Madej A, Lundeheim N: Hormone profiles around weaning in cyclic and anoestrous sows. Zentralbl Veterinarmed A. 1995, 42 (2): 153-163.
Hughes PE: Factors affecting the natural attainment of puberty in the gilt. Control of Pig Reproduction. Edited by: Cole DJA, Foxcroft GR. 1982, Butterworths London, 117-138.
Dalin AM, Nyberg L, Eliasson L: The effect of transportation on cortisol, CBG and induction of puberty in gilts with delayed puberty. Acta Vet Scand. 1988, 29 (2): 207-218.
Rojanasthien S: Clinical, morphological and endocrinological studies in lactating and post-weaning sows. Doctoral thesis. 1988, Department of Obstetrics and Gynaecology, Faculty of Veterinary Medicine, Swedish University of Agricultural Sciences, Uppsala
Rojanasthien S, Einarsson S: Clinical, morphological and endocrinological studies in post-weaning anoestrous sows. Acta Vet Scand Suppl. 1988, 83: 117-127.
Dalin AM, Magnusson U, Häggendal J, Nyberg L: The effect of transport stress on plasma levels of catecholamines, cortisol, corticosteroid-binding globulin, blood cell count, and lymphocyte proliferation in pigs. Acta Vet Scand. 1993, 34: 59-68.
Roozen AWM, Tsuma VT, Magnusson U: Effects of short-term stress on plasma concentrations of catecholamines, β-endorphin, and cortisol in gilts. Am J Vet Res. 1995, 56 (9): 1225-1227.
Graves HB: Behavior and ecology og wild and feral swine (sus scrofa). J Anim Sci. 1984, 58: 482-492.
Meynhardt H: Schwarzwild-report. Mein leben unter Wildschweinen. 1990, Neumann Verlag, Leigzig, Radebeul, 221pp-
Pedersen LJ, Rydhmer L, Neil M, Dalin AM: Oestrus behaviour of group housed sows in relation to individual competitive success. Proceeding 32nd Congress International Society of Applied Ethology, Clermont-Ferrand, France. 1998, 53-
Tsuma VT, Einarsson S, Madej A, Lundeheim N, Rojkittikhun T: Endocrine changes during group housing of primiparous sows in early pregnancy. Acta Vet Scand. 1996, 37: 481-490.
Stookey JM, Gonyou HW: The effects of regrouping on behavioral and production parameters in finishing swine. J Anim Sci. 1994, 72: 2804-2811.
Peltoniemi OAT, Love RJ, Heinonen M, Tuovinen V, Saloniemi H: Seasonal and management effetcs on fertility of the sow: a descriptive study. Anim Reprod Sci. 1999, 55: 47-61. 10.1016/S0378-4320(98)00159-6.
Kongsted AG: Stress and fear as possible mediations of reproduction problems in group housed sows. A review. Acta Agric Scand Sect A, Anim Sci. 2004, 54: 58-66. 10.1080/09064700410032031.
Fisker BN: Management procedures for group housing of pregnant sows (in Danish). Landsudvalget for svin. Den rullende afproevning Meddelelse. 1995, 311: 1-7.
Hansen LU: Mating stables for individually and group housed sows (in Danish). Den rullende afproevning Meddelelse. 2004, 6: 1-6.
Pedersen LJ, Heiskanen T, Damm BI: Sexual motivation in relation to social rank in pair-housed sows. Anim Reprod Sci. 2003, 75: 39-53. 10.1016/S0378-4320(02)00208-7.
Karlen GAM, Hemsworth PH, Gonyou HW, Fabrega E, Strom AD, Smits RJ: The welfare of gestating sows in conventional stalls and large groups on deep litter. Applied Animal Behaviour Science. 2007, 105: 87-101. 10.1016/j.applanim.2006.05.014.
Lundeheim N, Dalin AM, Hansson Stehn AS, Madej A: Cortisol level in saliva and plasma of growing pigs. Proceeding 18th IPVS Congress Hamburg, Germany. 2004, 1: 277-
Cassar G, Kirkwood RN, Seguin MJ, Widowski TM, Farzan A, Zanella AJ, Friendship RM: Influence of stage of gestation at grouping and presence of boars on farrowing rate and litter size of group-housed sows. Journal of Swine Health and Production. 2008, 16: 81-85.
Munsterhjelm C, Valros A, Heinonen M, Hälli O, Peltoniemi OAT: Housing during early pregnancy affects fertility and behaviour sows. Reprod Dom Anim. 2008, 43: 584-591. 10.1111/j.1439-0531.2007.00956.x.
Soede NM, Helmond FA, Schouten WGP, Kemp B: Oestrus, ovulation and peri- ovulatory hormone profiles in tethered and loose-housed sows. Anim Reprod Sci. 1997, 46: 133-148. 10.1016/S0378-4320(96)01609-0.
Soede NM, Roelofs JB, Verheijen RJE, Schouten WPG, Hazeleger W, Kemp B: Effect of repeated stress treatments during the follicular phase and early pregnancy on reproductive performance of gilts. Reprod Dom Anim. 2007, 42: 135-142. 10.1111/j.1439-0531.2006.00742.x.
Liptrap RM, Doble E: Relationship of prostaglandin F2α to cystic ovarian follicles in the sow. Br vet J. 1981, 137: 289-299.
Liptrap RM: Oestrogen excretion by sows with induced cystic ovarian follicles. Res Vet Sci. 1973, 15: 215-219.
Einarsson S, Ljung A, Brandt Y, Häger M, Madej A: Impact of exogenous ACTH during pro-oestrus on endocrine profile and oestrous cycle characteristics in sows. Reprod Dom Anim. 2007, 42: 100-104. 10.1111/j.1439-0531.2006.00739.x.
Brandt Y, Lang A, Madej A, Rodriguez-Martinez H, Einarsson S: Impact of ACTH administration on the oviductal sperm reservoir in sows: The local endocrine environment and distribution of sperma to zoa. Anim Reprod Sci. 2006, 92: 107-122. 10.1016/j.anireprosci.2005.04.011.
Brandt Y, Lang A, Madej A, Rodriguez-Martinez H, Einarsson S: Impact of ACTH during oestrus on the ultrastructure of the spermatozoa and their environment in the tubal reservoir of the postovulatory sow. Anim Reprod Sci. 2006, 93: 231-245. 10.1016/j.anireprosci.2005.06.031.
Brandt Y, Madej A, Rodriguez-Martinez H, Einarsson S: Effects of exogenous ACTH during oestrus on early embryo development and oviductal transport in the sow. Reprod Dom Anim. 2007, 42: 118-125. 10.1111/j.1439-0531.2006.00698.x.
Mburu JN: Sperm distribution in the porcine oviduct in relation to spontaneous ovulation and stress. Doctoral thesis, Veterinaria 28, Acta Universitatis Agriculturae Sueciae. 1995, Swedish University of Agricultural Sciences, Uppsala
Mburu JN, Einarsson S, Kindahl H, Madej A, Rodriguez-Martinez H: Effects of post-ovulatory food deprivation on oviductal sperm concentration, embryo development and hormonal profiles in the pig. Anim Reprod Sci. 1998, 52: 221-234. 10.1016/S0378-4320(98)00103-1.
Razdan P, Mwanza A, Kindahl H, Hultén F, Einarsson S: Effects of post-ovulatory food deprivation on ova transport, hormonal profiles and metabolic changes in sows. Acta Vet Scand. 2001, 42: 45-55. 10.1186/1751-0147-42-45.
Mwanza AM: Oviductal isthmic motility and the effect of stress thereupon and on the endocrine status and ova transport of recently ovulated pigs. Doctoral thesis, Veterinaria 80, Acta Universitatis Agriculturae Sueciae. 2000, Swedish University of Agricultural Sciences, Uppsala
Mwanza AM, Englund P, Kindahl H, Lundeheim N, Einarsson S: Effects of post- ovulatory food deprivation on the hormonal profiles, activity of the oviduct and ova transport in sows. Anim Reprod Sci. 2000, 59: 185-199. 10.1016/S0378-4320(00)00095-6.
Mwanza AM, Madej A, Kindahl H, Lundeheim N, Einarsson S: Postovulatory effect of repeated administration of ACTH on the contractile activity of the oviduct, ova transport and endocrine status of recently ovulated and unrestrained sows. Theriogenology. 2000, 54: 1305-1316. 10.1016/S0093-691X(00)00437-4.
Razdan P, Mwanza A, Kindahl H, Rodriguez-Martinez H, Hultén F, Einarsson S: Effect of repeated ACTH-stimulation on early embryonic development and hormonal profiles in sows. Anim Reprod Sci. 2002, 70: 127-137. 10.1016/S0378-4320(01)00182-8.
Tsuma VT, Einarsson S, Madej A, Lundeheim N, Rojkittikhun T: Effect of food deprivation during early pregnancy on endocrine changes in primiparous sows. Anim Reprod Sci. 1996, 41: 267-278. 10.1016/0378-4320(95)01456-X.
Razdan P, Tummaruk P, Kindahl H, Rodriguez-Martinez H, Hultén F, Einarsson S: Hormonal profiles and embryo survival of sows subjected to induced stress during days 13 and 14 of pregnancy. Anim Reprod Sci. 2004, 81: 295-312. 10.1016/j.anireprosci.2003.09.005.
Razdan P, Tummaruk P, Kindahl H, Rodriguez-Martinez H, Hultén F, Einarsson S: The impact of induced stress during days 13 and 14 of pregnancy on the composition of allantoic fluid and conceptus development in sows. Theriogenology. 2004, 61: 757-767. 10.1016/S0093-691X(03)00252-8.
Madej A, Romanowicz K, Einarsson S, Forsberg M, Barcikowski B: Urinary excretion of oestrone sulphate and cortisol in early pregnant gilts treated with glucocorticoids. Acta Vet Scand. 1998, 39: 61-70.
Madej A, Madsen MT, Brandt Y, Kindahl H, Einarsson S: Stress-related effects on reproductive capacity of pigs. J Anim Feed Sci. 2005, 14 (Suppl 1): 205-212.
The authors own research during the last 15 years was supported by The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Formas), The Swedish Farmers Foundation for Agricultural Research (SLF), The Swedish Foundation for International Cooperation in Research and Higher Education (STINT) and The Danish Pig Production.
The authors declare that they have no competing interests.
Stig Einarsson has been involved in most of the studies performed in Sweden and reviewed in this manuscript. He has also drafted the major part of this review. Ylva Brandt has performed some of the studies reviewed in this manuscript, and helped to draft the manuscript. Nils Lundeheim has participated in several of the studies and also made the statistics in many of the studies reviewed in this manuscript. He has helped to draft the manuscript. Andrzej Madej has been involved in many of the studies reviewed in this manuscript, and also helped to draft the manuscript.
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Einarsson, S., Brandt, Y., Lundeheim, N. et al. Stress and its influence on reproduction in pigs: a review. Acta Vet Scand 50, 48 (2008). https://doi.org/10.1186/1751-0147-50-48
- Heat Stress
- Corticotropin Release Hormone
- Housing System
- Sperm Morphology
- ACTH Group