Pain and discomfort caused by parturition in cows and sows

Applied Animal Behaviour Science 135 (2011) 241–251

Contents lists available at SciVerse ScienceDirect

Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim

Pain and discomfort caused by parturition in cows and sows Eva Mainau ∗ , Xavier Manteca Department of Animal and Food Science, School of Veterinary Science, Universitat Autònoma de Barcelona, 08193 Bellaterra (Barcelona), Spain

a r t i c l e

i n f o

Article history: Available online 8 November 2011 Keywords: Parturition Pain Cows sows

a b s t r a c t This review focuses on parturition as a painful process in cows and sows. Firstly, the different stages of parturition associated to the origin and transmission of pain stimuli are described. Hypoalgesia during the late pregnancy and parturition has been shown, perhaps as an endogenous defence against the pain of parturition. The principal factors affecting parturition pain are parity and dystocia, which are more likely in cases of long parturition, feto-pelvic disproportion and/or foetal malpresentation. The main consequences of pain caused by parturition are reviewed; parturition is an intrinsically risky process for both mother and young and can cause a stress response, health problems and maternal mortality, in addition to decreased food intake and production. The assessment of parturition pain has tended to use one of three approaches: measures of general indices, physiological and behavioural indicators. Finally, the impact of analgesia after parturition in cows and sows is reviewed. It is concluded that pain caused by parturition in animals deserves more research in order to optimize the parturition process and reduce its negative consequences on health, welfare and productivity. © 2011 Elsevier B.V. All rights reserved.

1. Parturition as a painful process 1.1. Introduction It is generally accepted that animal welfare comprises physical and mental health (Dawkins, 2004) and includes several aspects such as absence of thirst, hunger, discomfort, disease, pain, injuries and stress, as well as the expression of normal behaviour (FAWC, 1992). In consequence, one of the essential components of good welfare is the recognition and control of pain. Pain is defined by the International Association for the Study of Pain (IASP) as an unpleasant sensory and emotional experience normally associated with tissue damage or described in terms of such damage (Merskey, 1979). Pain serves a useful function because it is closely linked to some of the

∗ Corresponding author. Present address: IRTA, Finca Camps i Armet s/n, 17121 Monells (Girona), Spain. Tel.: +34 9726300521493; fax: +34 972630373. E-mail address: [email protected] (E. Mainau). 0168-1591/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2011.10.020

neurohumoral responses that are necessary for inflammation, and it can modify physiological responses, which in turn help the subject cope with an injury (Gregory, 2004). Labour pain is recognized as acute pain with at least two dimensions, a sensory and an affective component (Chapman and Nakamura, 1999). As a result of this, in humans, labour pain has received a great deal of scientific interest. However, most studies in animals concern endocrine changes associated with gestation, parturition and lactation, but there are only few studies of pain associated with the parturition process. According to a survey of 2,700 parturient women, 15% reported no or little pain, 35% reported moderate pain, 30% reported intense pain, and 20% reported very intense pain (Bonica, 1994). Melzack et al. (1981) found that mean labour pain scores were higher in both primiparous and multiparous women than in patients with other pain syndromes such as arthritic pain, back pain or toothache and concluded that labour pain ranks among the most intense pains recorded with the McGill Pain Questionnaire (Melzack, 1975).

242

E. Mainau, X. Manteca / Applied Animal Behaviour Science 135 (2011) 241–251

There are many similarities between animals and humans in anatomical and chemical pathways of pain perception (Morton and Griffiths, 1985). An animal can feel pain at a conscious level if the following criteria are met: (1) it possesses receptors sensitive to noxious stimuli, (2) its brain has structures analogous to the human cerebral cortex, (3) nervous pathways link the receptors to the higher brain and (4) painkillers modify the response to noxious stimuli. Additionally, some criteria related to behaviour in response to noxious stimuli would be as follows: (1) the animal responds to noxious stimuli by consistently avoiding them, (2) the animal can learn to associate neutral events with noxious stimuli and (3) it chooses a pain killer if given access to one, when pain is otherwise unavoidable (Gregory, 2004). In consequence, it is generally accepted that the perception of pain is similar in human beings and other mammals; therefore it can be assumed that what is painful in humans is also painful in animals (Morton and Griffiths, 1985). In consequence, from the maternal perspective, parturition in any species is generally accepted to be a painful process. Additionally, births associated with difficult parturitions or dystocia may cause unacceptably high levels of pain in the mother. For instance, in a questionnaire survey in the UK, dystocia was ranked by cattle practitioners as one of the most painful conditions of cattle obtaining a score of 7 in a scale from 1 to 10. Only claw amputation, caesarean section and left displaced abomasal surgery were considered more painful processes (Huxley and Whay, 2006). 1.2. Stages of parturition: origin and transmission of parturition pain stimuli Traditionally, the process of parturition has been divided into three separate stages. The first stage includes dilation of the cervix, the onset of myometrial contractions and the placement of the foetus for expulsion (Noakes et al., 2001a). In cows and sows, the dilation of the cervix starts gradually during the last stage of gestation and occurs more rapidly just prior to parturition (Taverne, 1992). The initial preparation of the birth canal takes places without uterine contractions, but in presence of the typical prepartum endocrine changes (relaxin release, withdrawal of progesterone and enhanced oestrogen and prostaglandin production) (Challis and Lye, 1986). At least in sows, oestrogens and relaxin induce the dilation of the cervix through modifying the activity of collagen. In cows, the role of endogenous relaxin remains uncertain (Taverne, 1992). The myometrial contractions vary from species to species and individual to individual. In general, their duration, frequency and amplitude increase and become more regular approximately 12 h before the onset of the second stage. Finally, foetal movements occur in response to increased uterine pressure caused by the myometrial contractions of the first stage (Noakes et al., 2001a). During the dilatation phase, visceral pain predominates, with pain stimuli arising from mechanical distention of the lower uterine segment and cervical dilation. In women, these nociceptive stimuli of the dilation phase are predominantly transmitted to the posterior nerve root ganglia at

T10 (spinal nerve of the thoracic segment that originates from the spinal column from below the thoracic vertebra 10) through L1 (spinal nerve of the lumbar segment that originates from the spinal column from below lumbar vertebra 1). Similar to other types of visceral pain, parturition pain may be progressively referred to the abdominal wall, lumbosacral region, iliac crests, gluteal areas and thighs (Lowe, 2002). The second stage is characterized by the appearance of abdominal contractions, allantochorionic sac rupture and expulsion of the foetus. This phase includes the final widening of the cervix which is accomplished by the propulsive forces of the regular uterine contractions during parturition (Taverne, 1992). As parturition advances, the distension of the maternal birth canal causes great increases in the release of oxytocin from the posterior pituitary and this, in turn, accentuates the myometrial contractions (Noakes et al., 2001a). In sows as well as in women, the number of oxytocin receptors in the uterus is elevated, which explains the greater sensitivity to exogenous oxytocin at this stage, relative to the response seen during gestation (Fuchs, 1987; Gorodeski et al., 1990; Soloff, 1975). In cows, increased oxytocin release, rather than a changed oxytocin binding capacity, is involved in the pattern of myometrial contractions (Taverne, 1992). In this stage, somatic pain predominates due to distention and traction on pelvic structures surrounding the vagina and from distention of the pelvic floor and perineum. In women, sharp and generally well localized, stimuli are transmitted via the pudendal nerve through the anterior rami of S2 (spinal nerve of the sacral segment that originates from the spinal column from below the second body of the sacrum) through S4 (spinal nerve of the sacral segment that originates from the spinal column from below the fourth body of the sacrum) (Lowe, 2002). The third stage includes the expulsion of the foetal membranes. In polytocous species (such as sow) the foetal membranes are sometimes voided together with the foetuses, but only the expulsion of the last afterbirth simulates the third stage in monotocous species (such as cow). During this stage, myometrial contractions persist, decreasing in amplitude but becoming more frequent and less regular. When a large portion of the afterbirth becomes detached and inverted it forms a mass within the maternal pelvis which stimulates reflex contractions of the abdominal muscles (Noakes et al., 2001a). 1.3. Hypoalgesia during parturition An increase in nociceptive threshold has been shown during the late pregnancy and parturition not only in women (Cogan and Spinnato, 1986; Whipple et al., 1990) and rats (Gintzler, 1980; Wardlaw and Frantz, 1983), but also in cattle (Aurich et al., 1990) and sows (Jarvis et al., 1997), perhaps as an endogenous defence against the pain of parturition. This pregnancy-induced hypoalgesia is mediated via endogenous opioids (Gintzler, 1980; Sander and Gintzler, 1987). It is well known that endogenous opioids are released in response to nociception and have potent analgesic properties (Dalayeun et al., 1993). Both neuronal and hormonal factors may be involved in the

E. Mainau, X. Manteca / Applied Animal Behaviour Science 135 (2011) 241–251

activation of pregnancy-induced hypoalgesia. The uterine distension and cervical stretching, stimulates the afferents in the hypogastric and pelvic nerves, which constitutes a major sensory pathway in the uterus, cervix and vaginal canal (Berkley et al., 1993; Steinman et al., 1992).This mechanism is mediated, at least in part, by the activation of spinal cord Kappa opioid receptors using dynorphin as the major opioid substrate (Medina et al., 1993a). Pregnancyinduced hypoalgesia is also caused by changes in the plasma concentration of sexual steroids (increases in progesterone and decreases in estrone) during the end of gestation (Edqvist et al., 1978). These hormones modulate an opioid analgesic system (Dawson-Basoa and Gintzler, 1993) and also activate a dynorphin system in the lumbar spinal cord (Medina et al., 1993b). A further accentuation of hypoalgesia has also been shown after ingestion of placenta (Kristal et al., 1985) and amniotic fluids (Kristal et al., 1990) in rats. In cows, the analgesic effect has been shown after ingestion of amniotic fluids, but not after ingestion of placenta (Machado et al., 1997). Cows ingest the placenta about 4 h after calving, whereas rats ingest the placenta immediately after every pup. It is therefore possible that placenta ingestion occurs too late in cows to mediate analgesia (Aurich et al., 1990; Machado et al., 1997). The molecule that promotes hypoalgesia through the ingestion of placenta and amniotic fluids is Placental Opioid-Enhancing Factor (POEF) (Kristal et al., 1988). Ingested POEF does not generate antinociception by itself, but rather potentiates the antinociception that is already present (Kristal, 1991). The strategy of producing more opioid effect without adding more opioids is particularly effective because a low opiate concentration at the time of parturition is essential for maternal behaviour and increasing the concentration of opiates after pregnancy termination would disrupt the maternal behaviour (Bridges and Grimm, 1982; Rubin and Bridges, 1984). It is well known that opioids inhibit oxytocin release, which plays a key role in triggering the parturition process. POEF potentiates ␦- and ␬-opioid antinociception, but attenuates ␮-opioid antinociception. In consequence, POEF not only enhances pain relief without suppression of maternal care, but also decreases ␮- mediated side effects such as constipation (DiPirro and Kristal, 2004). Apart from its analgesic effects, placentophagia may have other functions such as protection against predators, nutrient supply and immunological protection (Kristal, 1980).

243

2.1. Duration of parturition In sows, total farrowing time from first to last piglet may average 2.5 h and parturitions longer than 3 (Borges et al., 2005) or 4 h (Lucia et al., 2002) are considered potentially problematic and more painful. In sows, longer duration of farrowing is influenced by breed (e.g. Farmer and Robert, 2002; Van Dijk et al., 2005) and is more likely when there is a short gestation length (e.g. Van Dijk et al., 2005; Van Rens and van der Lende, 2004), increased litter size (e.g. Fahmy and Friend, 1981; Van Dijk et al., 2005; Van Rens and van der Lende, 2004), increased the number of stillborns (e.g. Fraser et al., 1997; Holm et al., 2004; Van Dijk et al., 2005), higher birth weight, thicker placenta (Van Rens and van der Lende, 2004) and lack of exercise (Vestergaard and Hansen, 1984). Contrary to this, Fahmy and Friend (1981) found that gestation length was positively related to the duration of farrowing. Moreover, several authors did not find any relationship between duration of farrowing and litter size (e.g. Friend et al., 1962), number of stillborn (e.g. Zaleski and Hacker, 1993) or exercise (Fraser et al., 1997). In cows, calving normally occurs between 30 min and 4 h from the appearance of the amnion to the birth of the calf (Noakes et al., 2001a). Most studies in this species have focused on the two main causes that can produce calving longer than normal: feto-pelvic disproportion and foetal malpresentation (see Sections 2.2 and 2.3). Several factors explain why primiparous dams have a priori more painful parturitions than multiparous ones. Apart from the lack of experience of the dams at first parturition, the majority of studies confirm that primiparous females have longer durations of parturitions and the degree of effort associated with it is usually greater than in multiparous females (Noakes et al., 2001a). In women, consistent findings indicate that during early and active labour (defined as cervical dilatation from 0 to 3 cm and from 4 to 7 cm respectively), nulliparous women experience on average greater sensory pain than multiparous women. However, as labour progresses, these differences are less pronounced, except for a possible increase in pain intensity during the pelvic phase of labour (deceleration and second phase) in multiparous women (Lowe, 1987, 1992; Ranta et al., 1996). The possible explanation is that, during the first stage, the cervix and lower uterine segment of multiparous women may actually transmit fewer noxious stimuli. During the second phase, the typically quicker foetal descent characteristic of multiparous births may produce more intense pain as a result of the sudden stimulation of nociceptors surrounding the vaginal vault, vulva and perineum (Lowe, 1996).

2. Factors affecting pain caused by parturition 2.2. Feto-pelvic disproportion (FPD) As previously reviewed, parturition itself it is a cause of pain. Several factors such as parity and parturition difficulties may modify the degree of pain caused by parturition. Dystocia may be defined as parturition difficulty resulting from prolonged spontaneous parturition or prolonged or severe assisted extraction (Mee, 2004), and is associated with unacceptably high levels of pain. In general, the dystocia rate is higher in primiparous than in multiparous dams (e.g. Nix et al., 1998).

In dairy cows, feto-pelvic disproportion (FPD) is the most common type of dystocia, particularly in primiparous cows. A large number of factors (e.g. foetal gender, twins or climate) may predispose to FPD (see Mee, 2008 for review). Controllable factors such as sire and dam breed or strain (e.g. Hansen et al., 2004; Heins et al., 2006; McGuirk et al., 1999), maternal feeding and body condition score at calving (e.g. Freetly et al., 2000; Hoffman et al., 1996) can be

244

E. Mainau, X. Manteca / Applied Animal Behaviour Science 135 (2011) 241–251

important aspects to consider in order to improve animal welfare. For instance, different strategies of maternal feeding can avoid the adverse effect of under or over feeding during the last trimester of pregnancy, which can affect birth weight and adipose deposition in the birth canal with consequent dystocia and stillbirth. In general, the strategies used to reduce FPD are based on reducing calf birth weight rather than increasing maternal pelvic area or by culling small heifers (Mee, 2008). Moreover, FPD causes more painful parturitions and is the main reason why veterinarians perform caesarean operations (Mee, 2008; Meijering, 1984). Caesarean section (CS) is potentially indicated in cases of dystocia (not only FPD, but also in cervical stenosis or uterine torsion; Bouchard et al., 1994) in order to reduce the probability of cow and calf death. From a survey of 133 cases of CS, 95% of the calves alive in utero and 91% of the dams survived, although 30% of the dams suffered ill-health afterwards (Cattell and Dobson, 1990). There is a general believe that CS causes more pain and discomfort than natural delivery. For instance, different authors reported behavioural and physiological pain indicators for a maximum of 48 h after calving (Kolkman et al., 2008; Watts, 2001). Despite this, the success rate of CS and its impact on animal welfare mainly depends on the operation technique (Kolkman et al., 2007). In women, data from Melzack et al. (1984) suggests an association between increased foetal weight and increased pain. Greater foetal weight is often correlated with increased maternal weight, although a positive correlation between pre-pregnancy weight for height and labour pain has not been found consistently (Lowe, 1991; Melzack et al., 1984). In addition, a foetus heavier than 4500 g is associated with an increased risk of CS because of cephalopelvic disproportion (Liao et al., 2005). In sows, FPD is not a risk factor for dystocia due to the obvious difference in size between the sow and piglet. 2.3. Foetal malpresentation In cows, another source of problematic or more painful calving is foetal malpresentation, especially in multiparous cows that are twice as likely as heifers to suffer from this condition (Holland et al., 1993). Foetal malpresentation is influenced by the presence of twins (Echternkamp and Gregory, 1999), breed of sire, sex of calf (males have twice the risk as females) and foetal mortality (see Mee, 2008 for review). In sows, the posterior presentation of piglets is relatively common, ranging from 25 to 52% of the farrowings (e.g. Herpin et al., 1996; Jones, 1966; Mainau et al., 2010). The effect of the anterior or posterior presentation on the progress of farrowing is controversial. Randall (1972) showed that posterior piglet presentation at birth had little or no effect on the ease of farrowing and was not related to abnormal delivery. On the other hand, van Dijk et al. (2005) demonstrated that posteriorly presented piglets were born after significantly longer birth interval than anteriorly presented ones. An anterior presentation of piglets at birth was related to an increased total time lying down of the sow during farrowing and in consequence appears

advantageous in terms of easy of farrowing (Mainau et al., 2010). Moreover, piglets with posterior presentation at birth and/or piglets that showed a high birth interval were more likely to be stillborn (Mainau et al., 2010), perhaps due to increased risk of hypoxia (Herpin et al., 1996). 2.4. Other factors affecting parturition pain Vulval stenosis (especially in primiparous cows) and uterine inertia, uterine torsion or cervical stenoses (especially in multiparous cows) are causes of difficult parturition that produce a higher degree of discomfort and pain around parturition (Mee, 2008; Metz and Metz, 1987). 3. Consequences of pain caused by parturition Parturition is an intrinsically risky process for both the mother and young. Injury, trauma and inflammation associated with parturition (particularly in dystocia parturitions) can have important negative effects on health, welfare and productivity in all farm species. 3.1. Consequences for the mother 3.1.1. Stress As with other species including humans, the parturition phase in sows (e.g. Meunier-Salaün et al., 1991) and cows (e.g. Hydbring et al., 1999) is also associated with increased plasma cortisol concentrations irrespective of the parturition environment. Increases in plasma cortisol could be a response to the intrinsically stress-inducing aspects of birth such as pain or novelty (e.g. neonate movements) (sows: Lawrence et al., 1994; cows: Hydbring et al., 1999). Additionally, sows kept in farrowing crates may experience physiological stress as a result of physical interference with behaviour around and during farrowing. Lawrence et al. (1994) found that crated primiparous sows increased their cortisol levels from 24 h before parturition and spent more time interacting with the floor or allocation fixtures (e.g. bars) during the 12 to 6 h preceding the start of parturition than primiparous sows kept in pens. Moreover, Oliviero et al. (2008) found higher cortisol concentrations during the early lactation (from day+2 to day+5) in sows kept in crates without enrichment material compared with sows kept in enriched pens. These facts cannot be related to the parturition process itself but seem to be a response to the crate environment which induces stress and interferes in the expression of maternal behaviour, such as nestbuilding behaviour or the inability to avoid piglet requests for nursing (Lawrence et al., 1994; Oliviero et al., 2008). Moreover, primiparous sows that are housed for the first time in farrowing crates may respond more strongly to the stress of crating due to their lack of experience with such a restrictive environment (Pedersen and Jensen, 2008). Stress can disrupt farrowing in sows through an opioid mediated inhibition of oxytocin secretion (Lawrence et al., 1992). Sows confined in crates show lower values of oxytocin than sows in pens (Lawrence et al., 1994; Oliviero et al., 2008). As oxytocin plays a key role in sustaining an optimal level of myometrial contractility, lower levels of oxytocin might result in prolonged delivery of piglets

E. Mainau, X. Manteca / Applied Animal Behaviour Science 135 (2011) 241–251

(Oliviero et al., 2008; Van Dijk et al., 2005). In order to decrease the sensitivity of oxytocin neurones to opioidinhibition, a recommended management practice would be confining the sows from 2 weeks to 5 days before farrowing (Lawrence et al., 1994; Oliviero et al., 2008). In relation to management practices in cows, a survey of beef producers in United States reported that only 39.6% of calvings took place in a specialized calving area (Dargatz et al., 2004). Mee (2004) suggests moving cows to a specialized maternity unit within 1 or 2 days prior to calving in order to give an adequate environment for calving and to detect abnormal calving early. At the same time, scientists have been investigating the phenomenon of pain suppression by stressful stimuli, commonly known as stress-induced analgesia. Stress-induced analgesia is mediated by activation of the descending inhibitory pain pathway (see Butler and Finn, 2009 for review). Individual sensitivity to stress-induced analgesia can vary greatly and it is coupled to many different phenotypes including the degree of opioid sensitivity and startle response. Furthermore, stress-induced analgesia is influenced by age and prior experience to stressful, painful or other environmental stimuli. Again, the environment during parturition and parity influence the degree of pain suffered during parturition.

3.1.2. Body weight, feed intake and milk production A reduction in food intake and the consequent weight loss is commonly seen in cows and sows after parturition, especially in primiparous dams. Some reduction in water intake is probably normal as well (Fraser and Phillips, 1989). Increasing food intake after parturition can minimize metabolic disorders, minimize weight loss and improve reproductive performance. For instance, the odds of a sow being removed from the herd before another farrowing decreased by approximately 30% with a 1-kg increase in average daily lactation feed intake (Anil et al., 2006). Cows that experience partum and postpartum disorders (e.g. dystocia, retained placenta or parturient paresis), reduced their dry matter intake (DMI) by 20% after calving (Zamet et al., 1979). In contrast, Proudfoot et al. (2009) compared cows with dystocia and eutocia calving, and did not find any differences in DMI during the 24-h and 48-h period after calving. Moreover, during the 24 h after calving, cows that had dystocia tended to consume more water probably because they tried to compensate for deficits in water intake before calving. Similarly, on day 3 after calving (when food was available), eating time was higher in CS cows than in naturally calving cows, perhaps in an attempt to compensate for the period of food deprivation, since one day after surgery cows did not have access to food in order to prevent adhesions (Kolkman et al., 2008). Feed intake and milk production are closely related. Cows calving in a higher body condition score produced more milk and more fat and protein in the first 90 days of lactation (Markusfeld et al., 1997). Dystocic calving significantly reduced milk production (e.g. Berry et al., 2007; Rajala and Gröhn, 1998; Thompson et al., 1983) and fat and protein yields (Dematawewa and Berger, 1997). In addition, milk production was reduced by an estimated 12% of

245

the potential yield in cows that needed CS at parturition (Cattell and Dobson, 1990). 3.1.3. Health, fertility and maternal mortality Health problems and maternal mortality peak around parturition in cows and in sows. The peripartum period is critically important to health and production and its effects can extend into the following lactation. In a retrospective study, Farhoodi et al. (2000), showed that 10.3% of cows have rectovaginal injuries after calving, including fistula, lacerations, pneumovagina and urovagina. The risk factors were parity (heifers had a higher risk than multiparous cows), male calves and dystocic calvings. Perineal laceration and rectovaginal fistula lead to fecal contamination of the vestibule, vagina and the uterus, which may result in endometritis. Pneumovagina may introduce fecal material, urine and air into the vagina leading to vaginitis, cervicitis and endometritis. Such inflammation can lead to lower fertility (Divers and Peek, 2008; Dreyfuss et al., 1990). Other possible consequences of calving, especially dystocic calving, are vulval discharges (Peeler et al., 1994), metritis (Benzaquen et al., 2007) and retained placenta (Erb et al., 1985). Other complications of parturition in cows and sows are prolapse of the uterus, hernia and rupture of the pelvic or abdominal organs and metabolic diseases (Noakes et al., 2001b). In sows, extended duration of farrowing and post-partum pyrexia appears to be a risk factor for mastitis-metritis-agalactya syndrome (MMA) (Papatsiros et al., 2007). Parturition may result in death of the dam. For example, in one study, 42% of all sow deaths occurred during the peripartum period, with heart failure, torsions and lesions in abdominals organs, cystitis-pyelonephritis, endometritis and uterine prolapses being the major causes (Chagnon et al., 1991). Moreover, vulval discharges can cause early culling of sows and impaired fertility (Oravainen et al., 2006). On the other hand, cow deaths increased about 4% for all parity groups in cows with very difficult calvings compared with cows needing no assistance (Dematawewa and Berger, 1997). 3.2. Consequences for the offspring Prolonged or difficult deliveries (without including caesarean section) are associated with increased offspring mortality in cows (Lombard et al., 2007) and in sows (Alonso-Spilsbury et al., 2005). Perinatal mortality in calves ranges from 4% to 13.2% and half of all preweaning casualties occur within the first day of life (e.g. Berglund et al., 2003; Berry et al., 2007; Johanson and Berger, 2003; Steinbock et al., 2003). The percentage of stillborn piglets ranges from 3 to 12% (e.g. Borges et al., 2005; Leenhouwers et al., 2003; Lucia et al., 2002; Van der Lende et al., 2001; Zaleski and Hacker, 1993) and accounts for 30–40% of the total neonatal mortality (Edwards, 2002). Stillbirth is commonly defined as a newborn that dies just prior to, during, or within 12 h of parturition. Newborn requiring assistance at parturition might incur in severe acidosis because of oxygen deprivation, with subsequent effects on the function of vital organs and

246

E. Mainau, X. Manteca / Applied Animal Behaviour Science 135 (2011) 241–251

overall vitality. Reduced vigor, poor thermoregulation, failure of passive transfer of immunity, poor performance and greater susceptibility to infections are also important secondary problems associated with neonatal asphyxia and acidosis (Alonso-Spilsbury et al., 2005). This occurs in most if not all mammal species, but some clear examples in sows and cows are: (1) Piglets born late on in the birth order, or with a long cumulative farrowing period, are more likely to be stillborn (Baxter et al., 2008) and (2) malpresented calves are five times as likely as normally presented calves to be stillborn (Mee, 2008). In sows, savaging (aggression towards their newborn offspring) contributes to increased piglet mortality. The incidence of savaging ranges from 1.4% to 14.6% (e.g. Cronin et al., 1996; Chen et al., 2008) and is considered to be higher in primiparous sows (Chen et al., 2008) although this could be as a result of savaging gilts being removed from the breeding herd (Ahlström et al., 2002). Moreover, the savaging rate is higher when gilts are housed in restrictive environments (Cronin et al., 1996) indicating that savaging may not necessarily reflect poor maternal ability but may be related to the individual’s inability to cope with restrictive environments around farrowing (Ahlström et al., 2002). In consequence, although the etiology of savaging in pigs is poorly understood, it may be related to pain sensitivity at farrowing that might be caused by possible interaction between low oxytocin (Gilbert, 2001) and the opioid system (Hansen and Curtis, 1981). 4. Assessment of pain caused by parturition In women, verbal questionnaires or verbal rating scales have been the most commonly used method of labour pain assessment both in clinical practice and research (Lowe, 2002). In these cases, the self-reporting of pain is the gold standard for the assessment of the individual labour pain. In veterinary medicine, pain assessment has tended to use one of three approaches: measures of general indices, physiological indicators and behavioural indicators (Weary et al., 2006). General indices or productive measures reflect what is happening over the interval between observations. Although physiological indices may be particularly useful in laboratory animals and in prey species such as cattle that are considered stoic (Weary et al., 2006), behavioural indices are the most commonly used parameters to assess ˜ pain in farm animals (Vinuela-Fernández et al., 2007). Normal deliveries show changes in the three indicators of pain, dystocic deliveries showing the most marked differences. 4.1. Measures of general indices A reduction in food intake is commonly seen in cows and sows before parturition. For instance, in cows DMI decreased 32% during the final 3 weeks of gestation, and 89% of that decline occurred in the final week of gestation (Hayirli et al., 2002). In addition, changes in DMI during the periparturient have been used as to identify cows at risk of postpartum complications (Drackley, 1999; Grummer et al., 2004). For example, Zamet et al. (1979) found that DMI in cows that experienced partum and postpartum disorders such

as dystocia retained foetal membranes or parturient paresis was 18% lower than for healthy cows prepartum. Also, Proudfoot et al. (2009) reported that cows with dystocia consumed 1.9 kg less during the 48 h before calving compared with cows with eutocia, and this difference increased to 2.6 kg in the 24 h before calving. These differences could be the result of several factors. First, because dystocia is often caused by FPD, larger calves could reduce the amount of space available in the rumen and, thus, reduce feed intake in cows (Stanley et al., 1993). Second, reductions in intake could be the result of pain associated with a large or malpositioned calf. Finally, cows that ended up having CS produced less milk at the same stage of gestation than cows that subsequently calved normally and were, therefore, able to produce heavier foetuses than the controls (Barkema et al., 1992). 4.2. Physiological indicators Physiological indicators include responses of the sympathetic-adrenomedullary system (for example changes in heart rate or rectal temperature) and responses of the hypothalamic-pituitary-adrenocortical system (for example changes in cortisol) (Weary et al., 2006). During the period around parturition, cows and sows have increased cardiac frequency, respiratory rates and rectal temperature (Noakes et al., 2001a). The hormonal changes during labour (e.g. cortisol, adrenaline, noradrenaline, ␤-endorphin, met-enkephalin, vasopressin and oxytocin) are related to the phase of labour regardless of its duration. Hormonal peaks are reached around the time of delivery, indicating that they are associated with muscle work, stress and pain rather than metabolic effects (Hydbring et al., 1999). In cows, higher levels of progesterone and lower levels of estrogens have been found in relation to dystocia a few days precalving (Zhang et al., 1999). Cows with twins have a significantly higher mean plasma cortisol concentration on the day of parturition than cows with single calves (Patel et al., 1996). The differences in the cortisol levels of singleton and twin-bearing cows on the day of parturition could be a direct result of added strain and trauma experienced by the dam in expelling two foetuses. Similar differences at delivery are also reported in women carrying twins (Ikeno and Takahashi, 1985). Also, throughout pregnancy, mean concentrations of bPSPB and estrogens are higher in twin than in single pregnancies (Dobson et al., 1993). Knowing which cows are bearing twins might allow us to increase their supervision and careful management practices around calving, and consequently minimize unnecessary pain and distress frequently associated with foetal malpresentation or FPD. In addition, vasopressin shows higher plasma concentration in heifers that needed assistance than in those that did not. Although the role of vasopressin during parturition is still largely unknown, high vasopressin levels during parturition could be explained by stress (Kendrick et al., 1991), intense muscular work and exercise (e.g. Lawrence et al., 1995), increased plasma osmolality (Landgraf et al., 1983) and/or haemorrhage (Olsson et al., 1987). Since increases of vasopressin in assisted heifers became apparent when

E. Mainau, X. Manteca / Applied Animal Behaviour Science 135 (2011) 241–251

intervention started, Hydbring et al., 1999 suggested that they were associated with muscle work, stress and pain rather than metabolic effects. As previously reviewed (see Section 3.1.1) the general increase in cortisol in the early post-partum period in sows could be a response to the intrinsically stressful aspects of birth such as pain or novelty (Lawrence et al., 1994). In the time around parturition there are significant changes in the concentration of acute phase proteins. Haptoglobin and Serum Amyloid A increases around calving and are higher in heifers than in multiparous cows, indicating a higher inflammation or trauma around calving which can cause higher levels of pain (Mainau et al., 2009; Murata et al., 2004). Schönfelder et al. (2005) observed higher levels of haptoglobin concentrations in cows with dystocia after uterine torsion compared to cows with natural parturition after 5 days postpartum. In pigs, C-reactive protein (CRP) and Hp are considered to be the best markers of inflammatory lesions (Eckersall et al., 1996). A higher than average concentration of Hp, as well as CRP, has been reported in sows 1 week after farrowing (Kováˇc et al., 2008). Moreover, primiparous sows have higher values of Hp than multiparous sows (Verheyen et al., 2007). A study by Kostro et al., 2003 showed that CRP reflects inflammation of the reproductive tract and mammary glands in sows with MMA. Other physiological indicators such as bovine pregnancy-specific protein B (bPSPB) in cows and pregnancy associated glycoproteins (PAGs) in cows and sows are used to indicate foetal well-being (Beckers et al., 1999). For instance, the pattern of PAGs in cows (PGF2␣ metabolite, cortisol and progesterone patterns also) change in cases of calving difficulty and stillbirth after induction of parturition with PGF2␣ (Kornmatitsuk et al., 2002). Finally, physiological indicators evaluated in the neonate can also provide information on the degree of parturition difficulty and, in consequence, on the pain suffered by the dam. It is well documented that with the increase of tractive force on the foetus, levels of cortisol in the plasma of the foetus rise and death of the foetus becomes likely (e.g. Hoyer et al., 1990). Moreover, Bellows and Lammoglia (2000) concluded that severe dystocia (use of mechanical calf puller) not only resulted in reduced serum cortisol, but also in lower calf rectal temperature and increased serum glucose. In the latter case, the highest concentration of serum cortisol in eutocial calves was attributed to cold stress because these calves were born outside (±4 ◦ C) compared with assisted calves delivered in an obstetrical barn (±22 ◦ C). 4.3. Behavioural indicators The activity of cows and sows increases quite dramatically prior to parturition. It has been suggested that this increased restlessness may be due to discomfort (e.g. cows: von Keyserlingk and Weary, 2007; sows: Damm et al., 2002), but this behavioural element might also be a part of the normal calving situation. However, Proudfoot et al. (2009) found that cows with dystocia changed position from standing to lying more frequently than cows without dystocia beginning 24 h before calving. Moreover, although

247

Wehrend et al. (2006) did not find differences in feeding or standing behaviour related to difficulty at calving, they showed a higher proportion of rubbing against the wall, discharge of urine and scraping on the floor in cows with dystocia compared to cows with eutocia. An association between difficult parturition and delayed standing of the dam after parturition has been reported in cows (Edwards and Broom, 1982). However, more research is needed in this area because the management practice of placing the newborn in front of the dam following an assisted delivery may contribute to longer periods of recumbency (Houwing et al., 1990). In sows, Mainau et al. (2010) develop an ease of farrowing score (EFS) based on behavioural indicators. Shorter duration of farrowing, sow posture (lying down) and sow activity (lower number of position changes) during the day before and the day of farrowing appear to be important ease of farrowing indicators. Moreover, savaging sows show a different pattern of behaviour compared with nonsavaging sows during the farrowing period. The behaviour of savaging sows includes increased time spent lying ventrally, increased posture changes, increased walking and a higher responsiveness index (Ahlström et al., 2002). Also, a higher frequency of sitting position and teeth grinding behaviour is reported (Chen et al., 2008). Vocalizations can be useful welfare indicators in conditions involving pain in cows (Watts and Stookey, 2000) and pigs (Weary et al., 1998). However, vocalizations during parturition are not always present, perhaps to avoid attracting predators (Lefebvre and Carli, 1985). Moreover, it must be taken into account that vocal responses show high individual variability and can indicate states other than pain, including hunger, isolation, separation or fear (cows: Watts and Stookey, 2000; sows: Weary et al., 1996). The behaviour of the newborn reflects the difficulty of delivery. In cows, calves stand and suckle later after difficult calving (Metz and Metz, 1987). In sows, high percentage of piglets born with a high viability, also showed shorter total time standing or sitting on the day of farrowing, associated with ease of farrowing (Mainau et al., 2010). 5. Treatment of pain caused by parturition There is limited work on the impact of analgesia after parturition in species reviewed. Theoretically, the administration of a non-steroidal anti-inflammatory drugs (NSAIDs) after parturition should reduce the associated inflammation and pain, improve the dam’s health and welfare, and help to maintain or even improve subsequent fertility and milk yield (Richards et al., 2009). Many cows undergoing painful procedures or suffering from painful conditions often receive no or inadequate pain control (Barrett, 2004) despite the fact that different analgesic agents are currently licensed for use in cows. In the UK, practitioners used NSAIDs, ␣2-agonist and/or local anaesthetic to control pain in case of caesarean section (68.1%, 60.3% and 98.4%, respectively) and dystocia (66%, 11.8% and 37.1%, respectively). Some practitioners did not use any painkiller treatment in these situations (0.3% of caesarean section cases and a 23% of dystocia cases). The most frequently used NSAIDs were flunixin, meloxicam and

248

E. Mainau, X. Manteca / Applied Animal Behaviour Science 135 (2011) 241–251

ketoprofen. Moreover, xylazine (an ␣2-agonist), and procaine and lignocaine (local anaesthetics) were the others drugs most frequently cited (Whay and Huxley, 2005). Although the license to use these drugs in farm animals varies between countries, there is a general consensus that there is an urgent need to approve anaesthetic and analgesic drugs for ruminants and swine in order to provide veterinarians and producers with appropriate withdrawal time for these drugs. The cost of providing the analgesia and/or the unwillingness or inability to appreciate the level of pain that cattle are suffering may be limiting factors (Huxley and Whay, 2006). In addition, most analgesics are not licensed for use around parturition. For instance, NSAIDs are licensed in cattle and sows for respiratory disease, diarrhoea, mastitis, locomotor disorders, post-operative surgery and MMA. Only ketoprofen is licensed for problems associated with calving in cows such as parturient paresis and oedema of the udder. Daily flunixin meglumine experimentally administrated to cows for the first 3 days after calving did not improve production during the first 35 days in milk (DIM), and dry matter intake was reduced from 1 to 7 DIM (Shwartz et al., 2009). Moreover, the administration of flunixin meglumine to cows after caesarean section is associated with a high probability of retained placenta (Waelchli et al., 1999). However, treatment with ketoprofen immediately after calving and 24 h later tended to reduce the incidence of retained placenta (Richards et al., 2009). In sows, Haussmann et al. (1999) found a reduced number of body position changes 48 h after farrowing in sows treated with butorphanol and hypothesized that this fact may lead to a decrease in crushing rates. In sows with mamitis-metritis-agalactya syndrome, both meloxicam and flunixin meglumine with adequate antibiotic drug were found to be equally efficacious, however, the mortality rate in piglets of affected litters was reduced in the meloxicam group (Hirsch et al., 2003).

6. Conclusions There is limited published research in relation to parturition pain in cows and sows. The origin and transmission of parturition pain is mainly described in women and rats. There are few publications in relation to the optimal management practices around parturition, and inadequate or absent pain control during this process has been noted. Causes and consequences of parturition pain are focused primarily on dystocia or problematic parturition. Parturition is associated with high levels of stress that can alter normal processes and trigger abnormal maternal behaviours. Management practices such as providing an adequate environment during parturition could reduce the negative impact of stress. It is concluded that parturition pain in animals should receive more scientific interest. In this way, it will be possible to optimize the parturition process and in consequence to reduce impacts on health, welfare and productivity.

Conflict of interest statement We have no financial or other relationship with other people or organizations within three years of submitting this paper that may inappropriately influence our work.

References Ahlström, S., Jarvis, S., Lawrence, A.B., 2002. Savaging gilts are more restless and more responsive to piglets during the expulsive phase of parturition. Appl. Anim. Behav. Sci. 76, 83–91. Alonso-Spilsbury, M., Mota-Rojas, D., Villanueva-García, D., MartínezBurnes, J., Orozco, H., Ramírez-Necoechea, R., Mayagoitia, A.L., Trujillo, M.E., 2005. Perinatal asphyxia pathophysiology in pig and human: a review. Anim. Reprod. Sci. 90, 1–30. Anil, S.S., Anil, L., Deen, J., Baidoo, S.K., Walker, R.D., 2006. Association of inadequate feed intake during lactation with removal of sows from the breeding herd. J. Swine Health Prod. 14, 296–301. Aurich, J.E., Dobrinski, I., Hoppen, H.-O., Grunert, E., 1990. ␤-Endorphin and met-enkephalin in plasma of cattle during pregnancy, parturition and the neonatal period. J. Reprod. Fert. 89, 605–612. Barkema, H.W., Schukken, Y.H., Guard, C.L., Brand, A., van der Weyden, G.C., 1992. Cesarean section in dairy cattle: a study of risk factors. Theriogenology 37, 489–506. Barrett, D.C., 2004. Non-steroidal anti-inflammatory drugs in cattle should we use them more? Cattle Practice 12, 69–73. Baxter, E.M., Jarvis, S., D’Eath, R.B., Ross, D.W., Robson, S.K., Farish, M., Nevison, I.M., Lawrence, A.B., Edwards, S.A., 2008. Investigating the behavioural and physiological indicators of neonatal survival in pigs. Theriogenology 69, 773–783. Beckers, J.F., Drion, P.V., Garbayo, J.M., Perényi, Z.S., Zarrouk, A., Sulon, J., Remy, B., Szenci, O., 1999. Pregnancy associated glycoproteins in ruminants: inactive members of the aspartic proteinase family. Acta Vet. Hung. 47, 461–469. Bellows, R.A., Lammoglia, M.A., 2000. Effects of severity of dystocia on cold tolerance and serum concentrations of glucose and cortisol in neonatal beef calves. Theriogenology 53, 803–813. Benzaquen, M.E., Risco, C.A., Archbald, L.F., Melendez, P., Thatcher, M.-J., Thatcher, W.W., 2007. Rectal temperature, calving-related factors, and the incidence of puerperal metritis in postpartum dairy cows. J. Dairy Sci. 90, 2804–2814. Berglund, B., Steinbock, L., Elvander, M., 2003. Causes of stillbirth and time of death in Swedish Holstein calves examined post mortem. Acta Vet. Scand. 44, 111–120. Berkley, K.J., Robbins, A., Sato, Y., 1993. Functional differences between afferent fibers in the hypogastric and pelvic nerves innervating female reproductive organs in the rat. J Neurophysiol. 69, 533–544. Berry, D.P., Lee, J.M., Macdonald, K.A., Roche, J.R., 2007. Body condition score and body weight effects on dystocia and stillbirths and consequent effects on postcalving performance. J. Dairy Sci. 90, 4201–4211. Bonica, J.J., 1994. Textbook of Pain, 5th ed. Churchill Livingstone, London UK. Borges, V.F., Bernardi, M.L., Bortolozzo, F.P., Wentz, I., 2005. Risk factors for stillbirth and foetal mummifications in four Brazilian swine herds. Prev. Vet. Med. 70, 165–176. Bouchard, E., Daignault, D., Bélanger, D., Couture, Y., 1994. Césarienne chez la vache laitière: 159 cas. Can. Vet. J. 35, 770–774. Bridges, R.S., Grimm, C.T., 1982. Reversal of morphine disruption of maternal behaviour by concurrent treatment with the opiate antagonist naloxone. Science 218, 166–168. Butler, R.K., Finn, D.P., 2009. Stress-induced analgesia. Prog. Neurobiol. 88, 184–202. Cattell, J.H., Dobson, H., 1990. A survey of caesarean operations on cattle in general veterinary practice. Vet. Rec. 127, 395–399. Chagnon, M., D’Allaire, S., Drolet, R., 1991. A prospective study of sow mortality in breeding herds. Can. J. Vet. Res. 55, 180–184. Challis, J.R.G., Lye, S.J., 1986. Parturition. Oxf. Rev. Reprod. Biol. 8, 61–129. Chapman, C.R., Nakamura, Y., 1999. A passion of the soul: an introduction to pain for consciousness researchers. Conscious. Cogn. 8, 391–422. Chen, C., Gilbert, C.L., Yang, G., Guo, Y., Segonds-Pichon, A., Ma, J., Evans, G., Brenig, B., Sargent, C., Affara, N., Huang, L., 2008. Maternal infanticide in sows: incidence and behavioural comparisons between savaging and non-savaging sows at parturition. Appl. Anim. Behav. Sci. 109, 238–248. Cogan, R., Spinnato, J.A., 1986. Pain and discomfort thresholds in late pregnancy. Pain 27, 63–68.

E. Mainau, X. Manteca / Applied Animal Behaviour Science 135 (2011) 241–251 Cronin, G.M., Simpson, G.J., Hemsworth, P.H., 1996. The effects of the gestation and farrowing environments on sow and piglet behaviour and piglet survival and growth in early lactation. Appl. Anim. Behav. Sci. 62, 175–192. Dalayeun, J.F., Nores, J.M., Bergal, S., 1993. Physiology of ␤-endorphin. A close up view and a review of the literature. Biomed. Pharmacother. 47, 311–320. Damm, B.I., Bildsøe, M., Gilbert, C., Ladewig, J., 2002. The effects of confinement on periparturient behaviour and circulating prolactin, prostaglandin F2␣ and oxytocin in gilts with access to a variety of nest materials. Appl. Anim. Behav. Sci 76, 135–156. Dargatz, D.A., Dewell, G.A., Mortimer, R.G., 2004. Calving and calving management of beef cows and heifers on cow-calf operations in the United States. Theriogenology 61, 997–1007. Dawkins, M.S., 2004. Using behaviour to assess animal welfare. Anim. Welf. 13, 3–7. Dawson-Basoa, M.B., Gintzler, A.R., 1993. 17- Beta-estradiol and progesterone modulate an intrinsic opioid analgesic system. Brain Res. 601, 241–245. Dematawewa, C.M.B., Berger, P.J., 1997. Effect of dystocia on yield, fertility and cow losses and an economic evaluation of dystocia scores for Holsteins. J. Dairy Sci. 80, 754–761. DiPirro, J.M., Kristal, M.B., 2004. Placenta ingestion by rats enhances (and (-opioid antinociception, but suppresses (-opioid antinociception. Brain Res. 1014, 22–33. Divers, T.J., Peek, S.F., 2008. Reproductive diseases. In: Rebhun’s Diseases of Dairy Cattle. Elsevier Inc, pp. 395–446. Dobson, H., Rowan, T.G., Kippax, I.S., Humblot, P., 1993. Assessment of fetal number, and fetal and placental viability throughout pregnancy in cattle. Theriogenology 40, 411–425. Drackley, J.K., 1999. Biology of dairy cows during the transition period: the final frontier? J. Dairy Sci. 82, 2259–2273. Dreyfuss, D.J., Tulleners, E.P., Donawick, W.J., Ducharme, N.G., 1990. Thirddegree perineal lacerations and rectovestibular fistulae in cattle: 20 cases (1981–1988). J. Am. Vet. Med. Assoc. 196, 768–770. Echternkamp, S.E., Gregory, K.E., 1999. Effects of twinning on gestation length, retained placenta and dystocia. J. Anim. Sci. 77, 39–47. Eckersall, P.D., Saini, P.K., McComb, C., 1996. The acute phase response of acid soluble glycoprotein ␣1 -acid glycoprotein, ceruloplasmin, haptoglobin and C-reactive protein, in the pig. Vet. Immunol. Immunopathol. 51, 377–385. Edqvist, L.-E., Kindahl, H., Stabenfeldt, G., 1978. Release of prostaglandin F2␣ during the bovine peripartal period. Prostaglandins 16, 111–119. Edwards, S.A., 2002. Perinatal mortality in the pig: environmental or physiological solutions? Livest. Prod. Sci. 78, 3–12. Edwards, S.A., Broom, D.M., 1982. Behavioural interactions of dairy cows with their newborn calves and the effects of parity. Anim. Behav. 30, 525–535. Erb, H.N., Smith, R.D., Oltenacu, P.A., Guard, C.L., Hillman, R.B., Powers, P.A., Smith, M.C., White, M.E., 1985. Path model of reproductive disorders and performance, milk fever, mastitis, milk yield, and culling in Holstein cows. J. Dairy Sci. 68, 3337–3349. Fahmy, M.H., Friend, D.W., 1981. Factors influencing, and repeatability of the duration of farrowing in Yorkshire sows. Can. J. Anim. Sci. 61, 17–22. Farhoodi, M., Nowrouzian, I., Hovareshti, P., Bolourchi, M., Nadalian, M.Gh., 2000. Factors associated with rectovaginal injuries in Holstein dairy cows in a herd in Tehran, Iran. Prev. Vet. Med. 46, 143–148. Farm Animal Welfare Council, 1992. FAWC updates the five freedoms. Vet. Rec. 17, 357. Farmer, C., Robert, S., 2002. Hormonal, behavioural and performance characteristics of meishan sows during pregnancy and lactation. Can. J. Anim. Sci. 83, 1–12. Fraser, D., Phillips, P.A., 1989. Lethargy and low water intake by sows during early lactation: a cause of low piglet weight gains and survival? Appl. Anim. Behav. Sci. 24, 13–22. Fraser, D., Phillips, P.A., Thompson, B.K., 1997. Farrowing behaviour and stillbirth in two environments: An evaluation of the restraint-stillbirth hypothesis. Appl. Anim. Behav. Sci. 55, 51–66. Freetly, H.C., Ferrell, C.L., Jenkins, T.G., 2000. Timing of realimentation of mature cows that were feed-restricted during pregnancy influences calf birth weights and growth rates. J. Anim. Sci. 78, 2790–2796. Friend, D.W., Cunningham, H.M., Nicholson, J.W.G., 1962. The duration of farrowing in relation to the reproductive performance of Yorkshire sows. Can. J. Comp. Vet. Med. Sci. 26, 127–130. Fuchs, A.R., 1987. Prostaglandin F2 alpha and oxytocin interactions in ovarian and uterine function. J. Steroid. Biochem. 27, 1073–1080. Gintzler, A.R., 1980. Endorphin-mediated increases in pain threshold during pregnancy. Science 210, 193–195.

249

Gilbert, C.L., 2001. Endocrine regulation of periparturient behaviour in pigs. Reprod. Suppl. 58, 263–266. Gorodeski, G.I., Sheean, L.A., Utian, W.H., 1990. Myometrial oxytocin receptors levels in the pregnant rat higher in distal than in proximal portions of the horn and correlate with disparate oxytocin responsive myometrial contractility in these segments. Endocrinology 127, 1136–1143. Gregory, N.G., 2004. Physiology and behaviour of animal suffering, third ed. Blackwell Science, Universities Federation for Animal Welfare, Oxford, UK. Grummer, R.R., Mashek, D.G., Hayirli, A., 2004. Dry matter intake and energy balance in the transition period. Vet. Clin. Food Anim. 20, 447–470. Hansen, K.E., Curtis, S.E., 1981. Prepartal activity of sows in stall or pen. J. Anim. Sci. 51, 456–460. Hansen, M., Misztal, I., Lund, M.S., Pedersen, J., Christensen, L.G., 2004. Undesired phenotypic and genetic trend for stillbirth in Danish Holsteins. J. Dairy Sci. 87, 1477–1486. Haussmann, M.F., Lay, D.C., Buchanan, H.S., Hopper, J.G., 1999. Butorphanol tartrate acts to decrease sow activity, which could lead to reduced pig crushing. J. Anim. Sci. 77, 2054–2059. Hayirli, A., Grummer, R.R., Nordheim, E.V., Crump, P.M., 2002. Animal and dietary factors affecting feed intake during the prefresh transition period in Holsteins. J. Dairy Sci. 85, 3430–3443. Heins, B.J., Hansen, L.B., Seykora, A.J., 2006. Calving difficulty and stillbirths of pure Holsteins versus crossbreds of Holstein with Normande, Montbeliarde, and Scandinavian Red. J. Dairy Sci. 89, 2805–2810. Herpin, P., Le Dividich, J., Hulin, J.C., Fillaut, M., De Marco, F., Bertin, R., 1996. Effects of the level of asphyxia during delivery on viability at birth and early postnatal vitality of newborn pigs. J. Anim. Sci. 74, 2067–2075. Hirsch, A.C., Philipp, H., Kleemann, R., 2003. Investigation on the efficacy of meloxicam in sows with mastitis–metritis–agalactia syndrome. J. Vet. Pharmacol. Therap. 26, 355–360. Hoffman, P.C., Brehm, N.M., Price, S.G., Prill-Adams, A., 1996. Effect of accelerated postpubertal growth and early calving on lactation performance on primiparous Holstein heifers. J. Dairy Sci. 79, 2024–2031. Holland, M.D., Speer, N.C., LeFever, D.G., Taylor, R.E., Field, T.G., Odde, K.G., 1993. Factors contributing to dystocia due to fetal malpresentation in beef cattle. Theriogenology 39, 899–908. Holm, B., Bakken, M., Vangen, O., Rekaya, R., 2004. Genetic analysis of litter size, parturition length, and birth assistance requirements in primiparous sows using a joint linear-threshold animal model. J. Anim. Sci. 82, 2528–2533. Houwing, H., Hurnik, J.F., Lewis, N.J., 1990. Behaviour of periparturient dairy cows and their calves. Can. J. Anim. Sci. 70, 355–362. Hoyer, C., Grunert, E., Jöchle, W., 1990. Plasma glucocorticoid concentrations in calves as an indicator of stress during parturition. Am. J. Vet. Res. 51, 1882–1884. Huxley, J.N., Whay, H.R., 2006. Current attitudes of cattle practitioners to pain and the use of analgesics in cattle. Vet. Rec. 159, 662–668. Hydbring, E., Madej, A., MacDonald, E., Drugge-Boholm, G., Berglund, B., Olsson, K., 1999. Hormonal changes during parturition in heifers and goats are related to the phases and severity of labour. J. Endocrinol. 160, 75–85. Ikeno, N., Takahashi, K., 1985. Investigation of changes in serum estrone, estradiol, estriol, DHA-S, and cortisol and urinary estriol excretion. Acta Obstet. Gynaecol. Jap. 37, 99–106. Jarvis, S., McLean, K.A., Chirnside, J., Deans, L.A., Calvert, S.K., Molony, V., Lawrence, A.B., 1997. Opioid-mediated changes in nociceptive threshold during pregnancy and parturition in the sow. Pain 72, 153–159. Johanson, J.M., Berger, P.J., 2003. Birth weight as a predictor of calving ease and perinatal mortality in Holstein cattle. J. Dairy Sci. 86, 3745–3755. Jones, J.E.T., 1966. Observations on parturition in the sow Part II: The parturient and post-parturient phases. Brit. Vet. J. 122, 471–478. Kendrick, K., Keverne, E., Hinton, M., Goode, J., 1991. Cerebrospinal fluid and plasma concentrations of oxytocin and vasopressin during parturition and vaginocervical stimulation in the sheep. Brain Res. Bull. 26, 803–807. Kolkman, I., Aerts, S., Vervaecke, H., Vicca, J., Vandelook, J., de Kruif, A., Opsomer, G., Lips, D., 2008. Assessment of differences in some indicators of pain in double muscled Belgian Blue cows following naturally calving vs caesarean section. Reprod. Dom. Anim. 45, 160–167. Kolkman, I., De Vliegher, S., Hoflack, G., Van Aert, M., Laureyns, J., Lips, D., de Kruif, A., Opsomer, G., 2007. Protocol of the caesarean section as performed in daily bovine practice in Belgium. Reprod. Dom. Anim. 42, 583–589. Kornmatitsuk, B., Veronesi, M.C., Madej, A., Dahl, E., Ropstad, E., Beckers, J.F., Forsberg, M., Gustafsson, H., Kindahl, H., 2002. Hormonal

250

E. Mainau, X. Manteca / Applied Animal Behaviour Science 135 (2011) 241–251

measurements in late pregnancy and parturition in dairy cows – possible tools to monitor foetal well being. Anim. Reprod. Sci. 72, 153–164. ´ Z., 2003. Kostro, K., Wawron, W., Szczubial, M., Luft-Deptula, D., Glinski, C-reactive protein in monitoring and evaluation of effects of therapy of the MMA syndrome of sows. Pol. J. Vet. Sci. 6, 235–238. Kováˇc, G., Tóthová, C.S., Nagy, O., Seidel, H., 2008. Acute phase proteins during the reproductive cycle of sows. Acta Vet. Beograd. 58, 459–466. Kristal, M.B., 1980. Placentophagia: a biobehavioral enigma (or De gustibus non disputandum est). Neurosci. Biobehav. Rev. 4, 141–150. Kristal, M.B., 1991. Enhancement of opioid-mediated analgesia: a solution to the enigma of placentophagia. Neurosci. Biobehav. Rev. 15, 425–435. Kristal, M.B., Abbott, P., Thompson, A.C., 1988. Dose-dependent enhancement of morphine-induced analgesia by ingestion of amniotic fluid and placenta. Pharmacol. Biochem. Behav. 31, 351–356. Kristal, M.B., Tarapacki, J.A., Barton, D., 1990. Amniotic fluid ingestion enhances opioid-mediated but not non-opioid mediated analgesia. Physiol. Behav. 47, 79–81. Kristal, M.B., Thompson, A.C., Grishkat, H.L., 1985. Placenta ingestion enhances opiate analgesia in rats. Physiol. Behav. 35, 481–486. Landgraf, R., Schulz, J., Eulenberger, K., Wilhelm, J., 1983. Plasma levels of oxytocin and vasopressin before, during and after parturition in cows. Exp. Clin. Endocrinol. 81, 321–328. Lawrence, A.B., Petherick, J.C., McLean, K.A., Deans, L.A., Chirnside, J., Vaughan, A., Clutton, E., Terlouw, E.M.C., 1994. The effect of environment on behaviour, plasma cortisol and prolactin in parturient sows. Appl. Anim. Behav. Sci. 39, 313–330. Lawrence, A., Petherick, J., McLean, K., Deans, L., Chirnside, J., Vaughan, A., Gilbert, C., Forsling, M., Russel, J., 1995. The effects of chronic environmental stress on parturition and on oxytocin and vasopressin secretion in the pig. Anim. Reprod. Sci. 38, 251–264. Lawrence, A.B., Petherick, J.C., McLean, K.A., Gilbert, C.L., Chapman, C., Russell, J.A., 1992. Naloxone prevents interruption of parturition and increases plasma oxytocin following environmental disturbance in parturient sows. Physiol. Behav. 52, 917–923. Leenhouwers, J.I., Wissink, P., van der Lende, T., Paridaans, H., Knol, E.F., 2003. Stillbirth in the pig in relation to genetic merit for farrowing survival. J. Anim. Sci. 81, 2419–2424. Lefebvre, L., Carli, G., 1985. Parturition in non-human primates: pain an auditory concealment. Pain 21, 315–327. Liao, J.B., Buhimschi, C.S., Norwitz, E.R., 2005. Normal labor: mechanism and duration. Obstet. Gynecol. Clin. N. Am. 32, 145–164. Lombard, J.E., Garry, F.B., Tomlinson, S.M., Garber, L.P., 2007. Impacts of dystocia on health and survival of dairy calves. J. Dairy Sci. 90, 1751–1760. Lowe, N.K., 1987. Parity and pain during parturition, Journal of Obstetric. Gynecol. Neonatal. Nurs. 16, 340–346. Lowe, N.K., 1991. Critical predictors of sensory and affective pain during four phases of labor. J. Psychosom. Obstet. Gynaecol. 12, 193–208. Lowe, N.K., 1992. Differences in first and second stage labor pain between nulliparous and multiparous women. J. Psychosom. Obstet. Gynaecol. 13, 243–253. Lowe, N.K., 1996. Pain and discomfort of labor and birth. J. Obstet. Gynecol. Neonatal. Nurs. 25, 82–92. Lowe, N.K., 2002. The nature of labor pain. Am. J. Obstet. Gynecol. 186, 16–24. Lucia Jr.T., Corrêa, M.N., Deschamps, J.C., Bianchi, I., Donin, M.A., Machado, A.C., Meincke, W., Matheus, J.E.M., 2002. Risk factors for stillbirths in two swine farms in the south of Brazil. Prev. Vet. Med. 53, 285–292. Machado, F.P., Hurnik,.L.C., Burton, J.F.J.H., 1997. The effect of amniotic fluid ingestion on the nociception of cows. Physiol. Behav. 62, 1339–1344. Mainau, E., Cuevas, A., Ruiz-de-la-Torre, J.L., Manteca, X., 2009. Effect of parity on acute phase proteins and general activity in dairy cows during the puerperal period. Proc. ISAE2009 Cairns, 171. Mainau, E., Dalmau, A., Ruiz-de-la-Torre, J.L., Manteca, X., 2010. A behavioural scale to measure ease of farrowing in sows. Theriogenology 74, 1279–1287. Markusfeld, O., Galon, N., Ezra, E., 1997. Body condition score, health, yield and fertility in dairy cows. Vet. Rec. 141, 67–72. McGuirk, B.J., Going, I., Gilmour, A.R., 1999. The genetic evaluation of UK Holstein Friesian sires for calving ease and related traits. Anim. Sci. 68, 413–422. Medina, V.M., Dawson-Basoa, M.E., Gintzler, A.R., 1993b. 17 beta-estradiol and progesterone positively modulate spinal cord dynorphin: relevance to the analgesia of pregnancy. Neuroendocrinology 58, 310–315.

Medina, V.M., Wang, L., Gintzler, A.R., 1993a. Spinal cord dynorphin: positive region-specific modulation during pregnancy and parturition. Brain Res. 623, 41–46. Mee, J.F., 2004. Managing the dairy cow at calving time. Vet. Clin. Food Anim. 20, 521–546. Mee, J.F., 2008. Prevalence and risk factors for dystocia in dairy cattle: a review. Vet. J. 176, 93–101. Meijering, A., 1984. Dystocia and stillbirth in cattle – a review of causes, relations and implications. Livest. Prod. Sci. 11, 143–177. Melzack, R., 1975. The McGill Pain Questionnaire: major properties and scoring methods. Pain 1, 277–299. Melzack, R., Kinch, R., Dobkin, P., Lebrun, M., Taenzer, P., 1984. Severity of labour pain: Influence of physical as well as psychologic variables. Can. Med. Assoc. J. 230, 579–584. Melzack, R., Taenzer, P., Feldman, P., Kinch, R.A., 1981. Labour is still painful after prepared childbirth training. Can. Med. Assoc. J. 125, 357–363. Merskey, H., 1979. Pain terms: a list with definitions and a note on usage Recommended by the International Association for the Study of Pain (IASP) Subcommittee on Taxonomy. Pain 6, 249–252. Metz, J., Metz, J.H.M., 1987. Behavioural phenomena related to normal and difficult deliveries in dairy cows. Neth. J. Agric. Sci. 35, 87–101. Meunier-Salaün, M.C., Gort, F., Prunier, A., Schouten, W.P.G., 1991. Behavioural patterns and progesterone, cortisol and prolactin levels around parturition in European (Large-White) and Chinese (Meishan) sows. Appl. Anim. Behav. Sci. 31, 43–59. Morton, D.B., Griffiths, P.H.M., 1985. Guidelines on the recognition of pain, distress and discomfort in experimental animals and an hypothesis for assessment. Vet. Rec. 116, 431–436. Murata, H., Shimada, N., Yoshioka, M., 2004. Current research on acute phase proteins in veterinary diagnosis: an overview. Vet. J. 168, 28–40. Nix, J.M., Spitzer, J.C., Grimes, L.W., Burns, G.L., Plyler, B.B., 1998. A retrospective analysis of factors contributing to calf mortality and dystocia in beef cattle. Theriogenology 49, 1515–1523. Noakes, D.E., Parkinson, T.J., England, G.C.W., Arthur, G.H., 2001a. Parturition and the care of parturient animals. In: Arthur’s Veterinary Reproduction and Obstetrics, pp. 155–187. Noakes, D.E., Parkinson, T.J., England, G.C.W., Arthur, G.H., 2001b. Injuries and diseases incidental to parturition. In: Arthur’s Veterinary Reproduction and Obstetrics, pp. 319–332. Oliviero, C., Heinonen, M., Valros, A., Hälli, O., Peltoniemi, O.A.T., 2008. Effect of the environment on the physiology of the sow during late pregnancy, farrowing and early lactation. Anim. Reprod. Sci. 105, 365–377. Olsson, K., Andén, N.-E., Johansson, K., Thornström, U., 1987. Effects of acute haemorrhagic hypotension during pregnancy and lactation in conscious goats. Acta Physiol. Scand. 129, 479–487. Oravainen, J., Heinonen, M., Seppä-Lassila, L., Orro, T., Tast, A., Virolainen, J.V., Peltoniemi, O.A.T., 2006. Factors affecting fertility in loosely housed sows and gilts: vulvar discharge syndrome, environment and acute-phase proteins. Reprod. Dom. Anim. 41, 549–554. Papatsiros, V.G., Alexopoulos, C., Kyriakis, S.C., 2007. Latest information in relation to postpartum dysgalactia syndrome of sows. Hell. Vet. Med. Soc. 58, 61–75. Patel, O.V., Takahashi, T., Takenouchi, N., Hirako, M., Sasaki, N., Domekis, I., 1996. Peripheral cortisol levels throughout gestation in the cow: effect of stage of gestation and foetal number. Br. Vet. J. 152, 425–432. Pedersen, L.J., Jensen, T., 2008. Effects of late introduction of sows to two farrowing environments on the progress of farrowing and maternal behaviour. J. Anim. Sci. 86, 2730–2737. Peeler, E.J., Otte, M.J., Esslemont, R.J., 1994. Inter-relationships of periparturient diseases in dairy cows. Vet. Rec. 134, 129–132. Proudfoot, K.L., Huzzey, J.M., von Keyserlingk, M.A.G., 2009. The effect of dystocia on the dry matter intake and behaviour of Holstein cows. J. Dairy Sci. 92, 4937–4944. Rajala, P.J., Gröhn, Y.T., 1998. Effects of dystocia, retained placenta and metritis on milk yield in dairy cows. J. Dairy Sci. 81, 3172–3181. Randall, G.C.B., 1972. Observations on parturition in the sow I. Factors associated with the delivery of the piglets and their subsequent behaviour. Vet. Rec. 90, 178–182. Ranta, P., Jouppila, P., Jouppila, R., 1996. The intensity of labor pain in grand multiparas. Acta Obster. Gynecol. Scand. 75, 250–254. Richards, B.D., Black, D.H., Christley, R.M., Royal, M.D., Smith, R.F., Dobson, H., 2009. Effects of the administration of ketoprofen at parturition on the milk yield and fertility of Holstein-Friesian cattle. Vet. Rec. 165, 102–106. Rubin, B.S., Bridges, R.S., 1984. Disruption of ongoing maternal responsiveness in rats by central administration of morphine sulfate. Brain Res. 307, 91–97.

E. Mainau, X. Manteca / Applied Animal Behaviour Science 135 (2011) 241–251 Sander, H.W., Gintzler, A.R., 1987. Spinal cord mediation of the opioid analgesia of pregnancy. Brain Res. 408, 389–393. Schönfelder, A., Schrödl, W., Krüger, M., Richter, A., Sobiraj, A., 2005. The change of acute phase protein haptoglobin in cattle during spontaneous labor and Caesarean section with or without torsio uteri intrapartum. Berl. Munch. Tierarztl. Wochenschr. 118, 240–246. Shwartz, G., Jill, K.L., vanBaale, M.J., Baumgard, L.H., 2009. Effects of flunixin meglumine on pyrexia and bioenergetic variables in postparturient dairy cows. J. Dairy Sci. 92, 1963–1970. Soloff, M., 1975. Uterine receptor for oxytocin: effects of estrogen. Biochem. Biophys. Res. Commun. 65, 205–212. Stanley, T.A., Cochran, R.C., Vanzant, E.S., Harmon, D.L., Corah, L.R., 1993. Periparturient changes in intake, ruminal capacity, and digestive characteristics in beef cows consuming alfalfa hay. J. Anim. Sci. 71, 788–795. Steinbock, L., Näsholm, A., Berglund, B., Johansson, K., Philipsson, J., 2003. Genetic effects on stillbirth and calving difficulty in Swedish Holsteins at first and second calving. J. Dairy Sci. 86, 2228–2235. Steinman, J.L., Carlton, S.M., Willis, W.D., 1992. The segmental distribution of afferent fibers from the vaginal cervix and hypogastric nerve in rats. Brain Res. 575, 25–31. Taverne, M.A.M., 1992. Physiology of parturition. Anim. Prod. Sci. 28, 433–440. Thompson, J.R., Pollak, E.J., Pelissier, C.L., 1983. Interrelationships of parturition problems, production of subsequent lactation, reproduction, and age at first calving. J. Dairy Sci. 66, 1119–1127. Van der Lende, T., Knol, E.F., Leenhouwers, J.I., 2001. Prenatal development as a predisposing factor for perinatal losses in pigs. Reprod. Suppl. 58, 247–261. Van Dijk, A.J., van Rens, B.T.T.M., van der Lende, T., Taverne, M.A.M., 2005. Factors affecting duration of the expulsive stage of parturition and piglet birth intervals in sows with uncomplicated, spontaneous farrowings. Theriogenology 64, 1573–1590. Van Rens, B.T.T.M., van der Lende, T., 2004. Parturition in gilts: duration of farrowing, birth intervals and placenta expulsion in relation to maternal, piglet and placental traits. Theriogenology 62, 331–352. Verheyen, A.J.M., Maes, D.G.D., Mateusen, B., Deprez, P., Janssens, G.P.J., de Lange, L., Counotte, G., 2007. Serum biochemical reference values for gestating and lactating sows. Vet. J. 174, 92–98. Vestergaard, K., Hansen, L.L., 1984. Tethered versus loose sows: ethological observations and measures of productivity I. Ethological observations during pregnancy and farrowing. Ann. Rech. Vet. 15, 245–256.

251

˜ Vinuela-Fernández, I., Jones, E., Welsh, E.M., Fleetwood-Walker, S.M., 2007. Pain mechanisms and their implication for the management of pain in farm and companion animals. Vet. J. 174, 227–239. von Keyserlingk, M.A.G., Weary, D.M., 2007. Maternal behavior in cattle. Horm. Behav. 52, 106–113. Waelchli, R.O., Thun, R., Stocker, H., 1999. Effect of flunixin meglumine on placental expulsion in dairy cattle after a caesarean. Vet. Rec. 144, 702–703. Wardlaw, S.L., Frantz, A.G., 1983. Brain beta-endorphin during pregnancy, parturition, and the postpartum period. Endocrinology 113, 1664–1668. Watts, S., 2001. Aspects of Analgesia in Cattle. Phd. University of London, pp. 1–264. Watts, J.M., Stookey, J.M., 2000. Vocal behaviour in cattle: the animal’s commentary on its biological processes and welfare. Appl. Anim. Behav. Sci. 67, 15–33. Weary, D.M., Braithwaite, L.A., Fraser, D., 1998. Vocal response to pain in piglets. Appl. Anim. Behav. Sci. 56, 161–172. Weary, D.M., Lawson, G., Thompson, B.K., 1996. Sows show stronger responses to isolation calls of piglets associated with greater levels of piglet need. Anim. Behav. 52, 1247–1253. Weary, D.M., Niel, L., Flower, F.C., Fraser, D., 2006. Identifying and preventing pain in animals. Appl. Anim. Behav. Sci. 100, 64–76. Wehrend, A., Hofman, E., Failing, K., Bostedt, H., 2006. Behaviour during the first stage of labour in cattle: influence of parity and dystocia. Appl. Anim. Behav. Sci. 100, 164–170. Whay, H.R., Huxley, J.N., 2005. Pain relief in cattle: a practioner’s perspective. Cattle Practice 13, 81–85. Whipple, B., Josimovich, J.B., Komisaruk, B.R., 1990. Sensory thresholds during the antepartum, intrapartum and postpartum periods. Int. J. Nurs. Stud. 27, 213–221. Zaleski, H.M., Hacker, R.R., 1993. Effect of oxygen and neostigmine on stillbirth and pig viability. J. Anim. Sci. 71, 298–305. Zamet, C.N., Colenbrander, V.F., Callahan, C.J., Chew, B.P., 1979. Variables associated with peripartum traits in dairy cows I. Effect of dietary forages and disorders on voluntary intake of feed, body weight and milk yield. Theriogenology 11, 229–244. Zhang, W.C., Nakao, T., Moriyoshi, M., Nakada, K., Ribadu, A.Y., Ohtaki, T., Tanaka, Y., 1999. Relationship of maternal plasma progesterone and estrone sulfate to dystocia in Holstein-Friesian heifers and cows. J. Vet. Med. Sci. 61, 909–913.