Review
Open Access

Causes, consequences and biomarkers of stress in swine: an update

  • Silvia Martínez-Miró1Email author,
  • Fernando Tecles2Email author,
  • Marina Ramón1,
  • Damián Escribano2,
  • Fuensanta Hernández1,
  • Josefa Madrid1,
  • Juan Orengo1,
  • Silvia Martínez-Subiela2,
  • Xavier Manteca3 and
  • José Joaquín Cerón2
BMC Veterinary ResearchBMC series – open, inclusive and trusted201612:171

https://doi.org/10.1186/s12917-016-0791-8

©  The Author(s). 2016

Received: 28 January 2016

Accepted: 3 August 2016

Published: 19 August 2016

Abstract

Background

In recent decades there has been a growing concern about animal stress on intensive pig farms due to the undesirable consequences that stress produces in the normal physiology of pigs and its effects on their welfare and general productive performance. This review analyses the most important types of stress (social, environmental, metabolic, immunological and due to human handling), and their biological consequences for pigs. The physio-pathological changes associated with stress are described, as well as the negative effects of stress on pig production. In addition an update of the different biomarkers used for the evaluation of stress is provided. These biomarkers can be classified into four groups according to the physiological system or axis evaluated: sympathetic nervous system, hypothalamic-pituitary-adrenal axis, hypothalamic-pituitary-gonadal axis and immune system.

Conclusions

Stress it is a process with multifactorial causes and produces an organic response that generates negative effects on animal health and production. Ideally, a panel of various biomarkers should be used to assess and evaluate the stress resulting from diverse causes and the different physiological systems involved in the stress response. We hope that this review will increase the understanding of the stress process, contribute to a better control and reduction of potential stressful stimuli in pigs and, finally, encourage future studies and developments to better monitor, detect and manage stress on pig farms.

Keywords

Stress Pigs Biomarkers

Background

The worldwide increase in the demand for animal products in recent decades has led to the use of intensive systems that have been demonstrated to produce stress in animals [1]. Since Hans Selye first introduced the concept of stress as “the non-specific response of the body to any demand for change” [2], the concept has received several definitions, so that nowadays its meaning can vary depending of the biological field in which it is used. According to Fink [3], stress in behavioral sciences is regarded as the perception of threat, with resulting anxiety, discomfort, emotional tension, and difficulty in adjustment. In terms of pure neuroendocrinology, stress is any stimulus that provokes release of the adrenocorticotropic hormone (ACTH) and adrenal glucocorticoids; and for the sociologists, it is any social disequilibrium that produces disturbances in the social structure within which a population lives [3]. Despite this variability in meaning, one of the most accepted definitions of stress is “the biological response elicited when an individual perceives a threat to its homeostasis” [4] which can apply to both humans and animals. In this review we will study the main types of stress that can affect pigs in intensive farming conditions, its consequences and the main biomarkers that can be used to detect whether the pigs are enduring stressful conditions.

Various classifications of stress have been described in the literature. From a practical point of view, it is of interest to classify the stress according to its duration and also to its causes. Regarding the duration of the stress, it can be acute (short in duration; lasting minutes or various days) or chronic (lasting weeks, months or even years). In addition, depending of its cause, the stress can be classified as social, environmental, metabolic, immunological or due to human practices and manipulation of animals.

Main causes of stress

In the following lines we will study the main causes of stress, as well the situations in the current intensive production systems where the pigs can be more exposed to these causes. It is important to point out that different external factors can produce a similar stress response, but on the other hand, the same stressful stimulus can produce a different response in the animal depending on its age, genetics, production system or previous exposure to the stimulus.

Social stress

Pigs are regrouped with unfamiliar conspecifics at different times of their productive cycle such as during gestation or after weaning, during the fattening period or before transport to slaughter. In these situations, pigs may fight in order to establish a new dominance hierarchy and this generates stress [5]. Such social stress can be acute, immediately following regrouping, or chronic, when the animals are socially subordinate or isolated [6], or as a result of repeated social regrouping [7].

Social stress can vary depending of the group size, space available and gender and genetic of the pig. Larger groups seem to have less social stress than smaller groups, reflecting a lower probability of monopolizing resources as the group size increases [8]. Intensive housing involves a reduction in the space per animal, which causes stress because of restricted movements and freedom to feed themselves [9]. It has been demonstrated that the frequency of social interactions and aggressive behaviour increases as the space allowance decreases in group-housed sows [10, 11] and the growth rate decreases linearly as the space allowance per pig decreases [12]. Response to social stress is higher in males than in females [13]. Aggressive behavior after regrouping varies between individuals and to some extent such individual differences have a genetic basis. As a result, some lines of pigs seem to fight less than other when unacquainted individuals are mixed [14].

Environmental stress

Intensive pig farming requires control of the temperature, humidity, light, concentration of dust and gases, ammonia levels and sound intensity [15–20]. For example, ambient temperature should be as close as possible to the thermal neutrality for the age of the pig being housed, (i.e. for prenursery pigs between 28 and 32 °C, for nursery pigs between 22 and 28 °C (depending on live weight, with lower live weight requiring higher temperature), for growing animals close to 20 °C, for finishing pigs between 16 and 18 °C, for pregnant sows between 15 and 18 °C, and for lactating sows and boars close to 16 °C) [15]. However, sometimes optimal environmental conditions cannot be maintained in farms producing stress in animals. For example, in areas where there are extreme hot or cold seasons, in farms located in areas of high noise or in the case of equipment failure. It is important to bear in mind that the effects of the thermal environment on pigs do not depend solely on ambient temperature, but on the so-called effective temperature, which depends on ambient temperature, ventilation and flooring, among other factors.

It should also be pointed out that the barren environments of modern production systems have a negative effect on animal welfare due to the lack of bedding material and/or slatted pen floors. They create a poor environment where pigs cannot develop their natural behaviour [21]. Inability to perform highly motivated behaviors may lead to a stress response. This is the case, for example, when sows are prevented from showing nest-building behavior before farrowing [22].

Metabolic stress

This stress results from food and/or water restriction or deprivation [23–25]. Although most studies in the literature induce metabolic stress by means of experimental models, metabolic stress can also appear in intensive farming conditions when pregnant sows are subjected to restrict feeding, which has been shown to result in chronic hunger [26]. Likewise, in the process of mixing pregnant sows, it is usual for the more submissive animals to have less or no access to food [27].

In any case, the negative effects of food deprivation will depend on the length of the fasting period. When an animal is food-deprived, its glucose levels in blood drop and enters in a catabolic state that requires the use and production of alternative fuels such as non-esterified fatty acids (NEFA), beta-hydroxybutyrate and glycerol for energetic needs [28, 29]. These analytes could be used as indicators of metabolic stress [29].

Immunological stress

Immunological stress is produced when an animal is challenged by infectious agents [30], which may occur due to the presence of disease or after vaccination. Stress can be considered as a possible cause but also a consequence of infectious disseases. A situation of stress produces changes in numbers and proportions of blood leukocytes [31], mitogen-induced cell proliferation, natural killer cell cytotoxicity and circulating inflammatory factors [32], which can result in increased susceptibility to any infectious disease [33]. And in the case of an existing disease, the stress associated may predispose pigs to the emergence of a different disease that complicates the process [13, 34].

Stress by animal handling

On commercial farms, pigs are subjected to handling practices which can cause acute stress. Some of these practices such as snaring or vena cava blood sampling produce a high stress, whereas others such as tattoing or electric shocks induced a more moderate stress in a previous study [35]. Similarly, castration, a common operation on some farms, has been shown to cause stress when carried out without anesthetics or analgesics [36].

Situations in intensive production systems where pigs are more exposed to stressors

There are two particular situations in the productive system, namely weaning and transport, when animals are more exposed to the causes of stress described above, and which generate a high degree of stress in the animals. Weaning is a period full of challenges to the piglet such as abrupt separation from the sow, transportation to a new physical environment, a different food source, commingling with pigs from other litters, greater exposition to pathogens and dietary or environmental antigens and handling practices such as vaccination and drug administration [37].

Transport either to another holding or slaughterhouse also includes exposure to different stressful events such as departure from the usual room, truck loading and unloading, fasting, different temperature and humidity, noise, vibration of the vehicle or inappropriate stocking densities [16, 38].

Therefore, special care should be taken in weaning, providing high-quality diets to minimize the risk of diarrhoea and reinforce immune system. Highly digestible animal proteins and feed additives such as enzymes and dietary acids may be used to improve the digestibility of the diet. Another option would be to offer low-protein and amino acid-fortified diets to limit the amount of fermentable protein presented to the gut and the use of pre- and probiotics, n-3 long chain polyunsaturated fatty acids and n-6 linoleic acid. Moreover, special attention should be paid to environmental and sanitary conditions in the post weaning stage, and an all-in, all-out management system should be used to minimize disease exposure [37, 39].

In addition, there are published reports and official documents with guidelines to improve the welfare and production of pigs during transport [16, 40]. These guidelines include avoiding extreme temperatures and the overloading of trucks, minimizing the time the pigs are on the truck, using non-slip flooring on loading ramps and providing an adequate handling to the pigs by well-trained people [16, 40].

Consequences of stress in pigs

Biological response

The stressors mentioned above are perceived by pigs as a threat to their homeostasis, which trigger a variety of biological responses (behavioural, neuroendocrine and immunological).

Behavioural responses

Avoiding a threat, facing up to it or hiding from it can be described as normal behaviour, whereas stereotypes (a repetitive, invariant behaviour pattern with no obvious goal or function) are considered as abnormal behaviours that can appear after a stress [41]. In addition, frequent defecation can be an indicator of fear and stress, and excessive aggressive behaviour as well as tail and ear biting are considered abnormal behaviours [42, 43]. A behavioural ethogram to evaluate the external response of pigs to stress has been proposed by Ruis et al. [44], which covers exploring, defecation/urination, inactive (sleeping, lying, sitting and standing), ingestive (feeding and drinking), vocalizing and walking behaviours.

Sympathetic-adrenal-medullary axis response (SAM)

Catecholamines (epinephrine and norepinephrine) are released by the chromaffin cells of the adrenal medulla when the sympathetic nervous system is activated by a stress stimulus. An increase in heart rate and blood pressure is one of the consequences of this activation. Other changes, such as constriction of the intestine and skin vessels, dilatation of skeletal muscle vessels, dilatation of the pupils, or release of glucose and lipids from the liver are also observed. All these short-term changes prepare the animal to face the stressful stimulus or to escape from it [45].

Hypothalamic-pituitary-adrenal axis response (HPA)

Corticotropin-releasing factor is released by the hypothalamus once the stressful stimulus is detected. As a consequence of this, the adrenocorticotropic hormone (ACTH) is released by the anterior pituitary gland. Finally, glucocorticoids are produced and released by the adrenal cortex to increase the catabolism of tissues rich in protein and fat to produce glucose [45].

Hypothalamic-pituitary-gonadal axis response (HPG)

Stress is generally accompanied by both an increase in the HPA activity and a decrease in HPG [46]. Glucocorticoids inhibit the release of luteizing hormone (LH) from the pituitary and estradiol and progesterone secretion by the ovary [47], as well testosterone from the testes [48], decreasing blood concentrations of these hormones. Prolonged or chronic stress usually results in inhibition of reproduction, while the effect of transient or acute stress in certain cases may be stimulatory [49].

Immune system response

This response depends on the mediator released in the process of stress: catecholamines or glucocorticoids [50]. Catecholamines, which are usually produced at the beginning of stress or during a short-term stressful stimulus, produce an increase in leukocytes (mainly granulocytes and lymphocytes), which are released into the systemic circulation. On the other hand, cortisol which predominates when stressful stimuli are prolonged, mainly decreases the number of lymphocytes in blood. Glucocorticoids can also suppress the production of cytokines and immunoglobulins [50–52].

Consequences for pig production

Pigs in intensive systems have to cope with long-term and intense short-term stressful stimuli that affect their welfare. High levels of stress and poor welfare have negative effects on five main factors related with pig production: pig performance, reproduction, behaviour, immunity and meat quality [53]. The magnitude of these effects will vary depending on stress duration and intensity, and on the early experience, age and genetics of the animal [4]. Some representative examples of these negative effects are provided below.

Any stressful condition can produce a decrease in performance parameters of pigs such as feed intake, daily gain or body weight (Table 1). For example, pigs housed at 32.2 °C had a 32.3 % decrease in average daily feed intake, 39.3 % lower average daily gain, 9.8 % lower final body weight and a 16.3 % lower gain:feed ratio compared with pigs housed at 23.9 °C [17]. Indeed, feed intake can decrease by up to 47 % in pigs housed at temperatures above the thermoneutral zone [19]. Similarly, Hyung et al. [54] found that growth rates were reduced by 15.7 and 7.1 % as a result of crowding and mixing, respectively, and showed a decrease in daily gain and gain:feed ratio of about 15 and 10 %, respectively, when the space available per pig was reduced from 0.56 to 0.25 m2/pig. Similarly, Lee et al. [55] showed that weaner pigs housed in a clean environment consumed about 8 % more feed and grew faster (about 10 %) than those housed in a dirty environment, and Hicks et al. [56] described that shipping by 4 h in weaner pigs produced a loss of 2.9 % body weight.
Table 1

Summary of stressful stimuli that produce a decreased in pig performance

Parameter affected

Stressful stimuli

Decrease, %

Reference

ADFI

Heat stress

32.3

White et al. [17]

47.0

Pearce et al. [19]

Dirty environment

8.0

Lee et al. [55]

ADG

Heat stress

39.3

White et al. [17]

Crowding

15.7

Hyung et al. [54]

Mixing

7.1

Hyung et al. [54]

Decreasing space availability

15.0

Hyung et al. [54]

Dirty environment

10.0

Lee et al. [55]

BW

Heat stress

9.8

White et al. [17]

Shipping (4 h)

2.9

Hicks et al. [56]

G:F

Heat stress

16.3

White et al. [17]

Decreasing space availability

10.0

Hyung et al. [54]

ADFI average daily feed intake, ADG average daily gain, BW body weight, G:F Gain:Feed ratio

A negative effect on the reproductive system has been described in boars in situations of stress, with a reduction in both ejaculate volume and semen quality, while gilts and sows may show fewer born piglets per litter and reduced rebreeding rate, as well as irregular rebreeding, higher weaning-to-oestrus interval [49], leading to a fall in farm production parameters.

In stressful situations there may be a reduction in the normal function of the immune system [31, 34], which may even suppress the response after vaccination [13]. This will result in an increase in the presence of diseases [57], with a subsequent increase in costs and decrease in production.

In addition, stress affects meat quality and an increase in incidence of pale, soft and exudative (PSE) and dark, firm and dry (DFD) meats, and reduced meat quality was found when stressful handling systems were used [16].

Biomarkers of stress studied in pigs

There is no a “gold standard” procedure to determine with accuracy the degree of animal welfare and the level of stress of an animal. Methodologies frequently used to quantify stress in animals include: (1) direct behavioural observations using behaviour scoring systems [44, 53, 58] or automated behaviour recognition video analysis [59, 60], and (2) biomarkers that can reflect the pathophysiological responses to stress [61–63]. There is a tendency to evaluate a panel of various biomarkers representing the different body systems involved: SAM, HPA axis, HPG axis and immune system.

Sympathetic Nervous System: alpha-amylase and chromogranin A

Alpha-amylase

This enzyme is used in humans as a stress biomarker because it increases after both physical and psychological stress [64]. It is measured in saliva and its activity is correlated with plasma catecholamine concentrations, being a marker of SAM activation [64–66]. In pigs alpha-amylase activity increases after 1 min of immobilization with nasal snares, however, high inter-individual variability in the responses was observed and some pigs did not present evident changes after this stressful stimulus [67]. Further studies would be necessary to clarify the role of this enzyme in porcine stress.

Chromogranin A

Chromogranin A (CgA) is an acidic soluble protein belonging to the granins family [68]. It was initially detected in chromaffin granules of the adrenal medulla, [69]. Later, CgA was found in secretory vesicles of endocrine, neuroendocrine and neuronal cells [70, 71]. During stress CgA is secreted into the blood by the adrenal medulla and anterior pituitary gland, with a smaller amount also released from sympathetic nerve endings [68]. In addition, CgA has been detected in salivary glands of humans and various animal species [72–74]. The release of CgA in saliva is mediated by the secretion of catecholamines [75], and has been related to the activation of SAM [76]. In humans, the measurement of CgA in saliva has been used as a reliable marker of SAM activation as an alternative to adrenaline and noradrenaline [77], which have high variability in results and low stability in saliva [78–80].

In pig, CgA has been used as a marker of SAM activation in different situations such as immobilization with a nasal snare [80], after refeeding following a period of food deprivation [25] and after isolation or regrouping [63]. CgA is not affected by age, gender or circadian rhythms [81]. This could be considered as an advantage compared with other stress biomarkers such as cortisol [82, 83], or Ig A [84] which are both influenced by these factors.

Hypothalamic-Pituitary-Adrenal Axis: Glucocorticoids

Cortisol is one of the most widely used biomarkers to detect stress in pigs, and is the main glucocorticoid in this species [85]. Its increase is related with HPA axis activation [86–88].

Despite its wide use, cortisol is influenced by factors such as circadian rhythm and genetics that could limit its use as a stress biomarker [89, 90]. Cortisol concentrations follow a circadian rhythm, with morning levels being up to 40 % higher than afternoon levels [91, 92], although a peak during the afternoon has been observed by several authors [83, 93, 94]. Furthermore, the average concentration of cortisol in pigs decrease with age, reaching a stable profile around 20 weeks of age, when levels were about 37 % lower than at 12 weeks of age [91, 95]. In addition, gender is another source of variation, with concentration in barrows being about 15 % higher than in gilts [91].

Plasma or serum has been the most widely used samples to measure cortisol in pigs and they reflect both the fraction of protein-bound cortisol and the free cortisol [91, 96]. However, there is a growing tendency to use saliva for cortisol measurements because it can be obtained by non-invasive techniques and reflects only the free cortisol which is the active fraction [43, 83, 97].

Although most stress stimuli tend to increase cortisol, in some situations cortisol such levels remain unchanged and show a large variability between individuals. For example, after 24 and 48 h transport, cortisol concentrations were not modified [98], and similarly, cortisol concentrations were not affected by feed deprivation or isolation, with a large variability between individual pigs [25, 63]. Likewise, McGlone et al. [99] found no significant change in plasma cortisol levels after shipping.

Hypothalamic-pituitary-gonadal axis: testosterone

Testosterone is a circulating androgen produced by the testes in males and by the ovaries in females, with a small amount being produced by the adrenal gland. The production of testosterone depends on the secretion of gonadotropin releasing hormone (GnRH) by the hypothalamus. GnRH binds to the gonadotrophs of the anterior pituitary to stimulate the secretion of luteinizing hormone (LH) and follicle stimulating hormone (FSH). FSH acts on Sertoli cells to aid spermatogenesis while LH induces the secretion of testosterone by Leydig cells in testes and by Theca cells in ovaries [100].

Although chronic stress has an inhibitory effect testosterone secretion [101], acute stress has been seen to increase testosterone levels in blood [102] and saliva [103]. For example, in pigs, an increase in salivary testosterone was detected after immobilization with a nose-snare or after short road transport [103]. The cause of this increase of testosterone in stress conditions is unclear, but could be due to increased sensitivity of the testes to LH, as a result of the activation of the SAM axis [102]. In addition, the administration of ACTH to boars induced a rapid increase in testosterone levels and adrenals could be a source of testosterone in stress situations [104].

Immune System: acute phase proteins, immunoglobulin A and interleukin-18

Acute phase proteins

Acute phase proteins (APPs) are blood proteins whose concentration is modified in response to inflammation, infection, and physical or psychological stress [105]. They are primarily synthesized by the liver [106] and released into the systemic circulation to restore the homeostasis of the organism [107]. They serve as a tool for disease diagnosis in pigs, especially to detect acute inflammation, but they have also been studied as stress biomarkers in plasma [105, 108, 109] and saliva [110].

A hypothesis was developed by Murata [111] to explain the link between APP and stress. This hypothesis starts with the SAM and HPA axis activation. The release of catecholamines by the SAM leads to the induction of pro-inflammatory cytokines such as interleukin-6 [112], which is known to be a strong inducer of hepatic APP production in pigs [113]. In swine, numerous studies have measured APP in stressful conditions; however, there is no clear pattern of APP response in stress situations and in some cases contradictory results were obtained. For example, while haptoglobin levels increased after 20 min of transport and 3 h lairage [114], 45 min transport or social isolation produced no significant changes in this APP [110]. Another example is the case of serum amyloid A, which increased in isolated animals [110] but did not change after stress induced by changes in the pattern of food administration [115]. So, further studies would be needed to clarify to the link between stress and the acute phase response.

Immunoglobulin A

Immunoglobulin A (IgA) is the most abundant antibody in mucous membranes, where it has a protective role against infectious agents, allergens and foreign proteins [116]. IgA has been described as a stress biomarker in rats [117], dogs [118] and humans [119]. In pigs, an increase in saliva IgA has been reported after immobilization [84, 120], in endotoxemia [121], and after isolation [63]. In the case of isolation, IgA was more strongly affected than other markers such as cortisol and testosterone [63].

Interleukin-18

Interleukin-18 (IL-18) is a proinflammatory cytokine initially detected in Kupffer cells in mice, although it has been located in other sites such as adrenal cortex, astrocytes, microglia or keratinocytes [122, 123]. It is as an interferon-gamma inducing factor [122], and also has antitumor and antimicrobial activity [124, 125].

Based on its increase in rats after ACTH administration [126], IL-18 has been proposed as a stress biomarker. Although studies in domestic animals are very scarce, an increase in IL-18 concentration in saliva has been described in pigs after 1 h of immobilization [120].

Conclusions

In this paper the main causes and consequences of stress in pigs, as well as the biomarkers that can be used for its evaluation are reviewed. Stress is a process with multifactorial causes, producing an organic response that generates negative effects in the health and production of the animals affected. Due to the diverse causes that can produce stress and the various physiological systems involved in the stress response, ideally a panel of various biomarkers should be used to assess the stress response in animals. We hope that this review can increase the understanding of the stress process, contribute to a better control and reduction of potential stressful stimuli in pigs, and encourage further studies and developments to better monitor, detect and manage stress on pig farms.

Abbreviations

ACTH, adrenocorticotropic hormone; ADFI, average daily feed intake; ADG, average daily gain; APPs, acute phase proteins; BW, Body weight; CgA, chromogranin A; DFD, dark, firm, dry; FSH, follicle stimulating hormone; G:F, gain:feed ratio; GnRH, gonadotropin-releasing hormone; HPA, hypothalamic-pituitary-adrenal axis; HPG, hypothalamic-pituitary-gonadal axis; IgA, immunoglobulin A; IL-18, interleukin-18; LH, luteinizing hormone; PSE, pale, soft, exudative; SAM, Sympathetic-adrenal-medullary axis

Declarations

Acknowledgements

This study was funded by the Spanish Ministry of Economy and Competitiveness (AGL 2012–33612) and by the Seneca Foundation of Murcia Region (project 19894/GERM/15).

Authors’ contributions

All authors participated in the design and helped to draft the manuscript and to include updated information in it. Once completed, all authors read and approved the final manuscript. SMM, FT and JJC conceptualized the review. JJC coordinated the process of writing the manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Not applicable.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Animal Production, Campus of Excellence Mare Nostrum, Universidad de Murcia
(2)
Department of Animal Medicine and Surgery, Campus of Excellence Mare Nostrum, Universidad de Murcia
(3)
Department of Animal and Food Science, Universitat Autònoma de Barcelona

References

  1. Barnett JL, Hemsworth PH, Cronin GM, Jongman E, Hutson GD. A review of the welfare issues for sows and piglets in relation to housing. Aust J Agric Res. 2001;52:1–28.View ArticleGoogle Scholar
  2. Selye H. A syndrome produced by diverse nocuous agents. Nature. 1936;138:32.View ArticleGoogle Scholar
  3. Fink G. Stress: definition and history. In: Squire LR, editor. Encyclopaedia of Neuroscience. London: Elsevier; 2009. p. 549–55.View ArticleGoogle Scholar
  4. Moberg GP. Biological response to stress: implications for animal welfare. In: Moberg GP, Mench JA, editors. The biology of animal stress: Basic Principles and Implications for Animal Welfare. USA: CABI Publishing; 2000. p. 1–22.View ArticleGoogle Scholar
  5. Pitts AD, Weary DM, Pajor EA, Fraser D. Mixing at young ages reduces fighting in unacquainted domestic pigs. Appl Anim Behav Sci. 2000;68:191–7.PubMedView ArticleGoogle Scholar
  6. Arnone M, Dantzer R. Does frustration induce aggression in pig? Appl Anim Ethol. 1980;6:351–62.View ArticleGoogle Scholar
  7. Coutellier L, Arnould C, Boissy A, Orgeur P, Prunier A, Veissier I, Meunier-Salaün MC. Pig’s responses to repeated social regrouping and relocation during the growing-finishing period. Appl Anim Behav Sci. 2007;105:102–15.View ArticleGoogle Scholar
  8. Andersen IL, Naevdal E, Bakken M, Boe KE. Aggression and group size in domesticated pigs, Sus scrofa: ‘When the winner takes it all and the loser is standing small’. Anim Behav. 2004;68:965–75.View ArticleGoogle Scholar
  9. Verdon M, Hansen CF, Rault JL, Jongman E, Hansen LU, Plush K, Hemsworth PH. Effects of group housing on sow welfare: a review. J Anim Sci. 2015;93:1999–2017.PubMedView ArticleGoogle Scholar
  10. Weng RC, Edwards SA, English PR. Behaviour, social interactions and lesion scores of group-housed sows in relation to floor space allowance. Appl Anim Behav Sci. 1998;59:307–16.View ArticleGoogle Scholar
  11. Remience V, Wavreille J, Canart B, Meunier-Salau MC, Prunier A, Bartiaux-Thill N, Nicks B, Vandenheede M. Effects of space allowance on the welfare of dry sows kept in dynamic groups and fed with an electronic sow feeder. Appl Anim Behav Sci. 2008;112:284–96.View ArticleGoogle Scholar
  12. Randolph JH, Cromwell GL, Stahly TS, Kratzer DD. Effects of group size and space allowance on performance and behaviour of swine. J Anim Sci. 1981;53(4):922–7.View ArticleGoogle Scholar
  13. de Groot J, Ruis MAW, Scholten JW, Koolhaas JM, Boersma WJA. Long-term effects of social stress on antiviral immunity in pigs. Physiol Behav. 2001;73:145–58.PubMedView ArticleGoogle Scholar
  14. Muráni E, Ponsuksii S, D’Eath RB, Turner SP, Kurt E, Evans G, Thölking L, Klont R, Foury A, Mormède P, Wimmers K. Association of HPA axis related genetic variation with stress reactivity and aggressive behaviour in pigs. BMC Genet. 2010;11:74.PubMedPubMed CentralView ArticleGoogle Scholar
  15. Wathes C, Whittemore C. Environmental management of pigs. In: Kyriazakis I, Whittemore C, Whittemore CT, editors. Whitemore’s science and practice of pig production. Oxford: Blackwell Publishing; 2006. p. 533–90.View ArticleGoogle Scholar
  16. Warriss PD. The welfare of slaughter pigs during transport. Anim Welfare. 1998;7:365–81.Google Scholar
  17. White HM, Richert BT, Schinckel AP, Burgess JR, Donkin SS, Latour MA. Effects of temperature stress on growth performance and bacon quality in grow-finish pigs housed at two densities. J Anim Sci. 2008;86:1789–98.PubMedView ArticleGoogle Scholar
  18. O’Connor EA, Parker MO, McLeman MA, Demmers TG, Lowe JC, Cui L, Davey EL, Owen RC, Wather CM, Abeyesinghe SM. The impact of chronic environmental stressors on growing pigs, sus scrofa (Part 1): Stress physiology, production and play behaviour. Animal. 2010;4:1899–909.PubMedView ArticleGoogle Scholar
  19. Pearce SC, Gabler NK, Ross JW, Escobar J, Patience JF, Rhoads RP, Baumgard LH. The effects of heat stress and plane of nutrition on metabolism in growing pigs. J Anim Sci. 2013;91:2108–18.PubMedView ArticleGoogle Scholar
  20. Sanz MV, Johnson JS, Abuajamieh M, Stoakes SK, Seibert JT, Cox L, Kahl S, Elsasser TH, Ross JV, Isom SC. Effects of heat stress on carbohydrate and lipid metabolism in growing pigs. Physiol Rep. 2015;3(2):e12315.View ArticleGoogle Scholar
  21. Beattie VE, O'Connell NE, Kilpatrick DJ, Moss BW. Influence of environmental enrichment on welfare-related behavioural and physiological parameters in growing pigs. J Anim Sci. 2000;70(3):443–50.View ArticleGoogle Scholar
  22. Oczak M, Maschat K, Berckmans D, Vranken E, Baumgartner J. Classification of nest-building behaviour in non-crated farrowing sows on the basis of accelerometer data. Biosyst Eng. 2015;140:48–58.View ArticleGoogle Scholar
  23. Toscano MJ, Lay DC, Craig BA, Pajor EA. Assessing the adaptation of swine to fifty-seven hours of feed deprivation in terms of behavioural and physiological responses. J Anim Sci. 2007;85:441–51.PubMedView ArticleGoogle Scholar
  24. Lallès JP, David JC. Fasting and refeeding modulate the expression of stress proteins along the gastrointestinal tract of weaned pigs. J Anim Physiol Anim Nutr. 2011;95:478–88.View ArticleGoogle Scholar
  25. Ott O, Soler L, Moons CPH, Kashiha MA, Bahr C, Vandermeulen J, Janssens S, Gutiérrez AM, Escribano D, Cerón JJ, Berckmans D, Tuyttens FAM. Different stressors elicit different responses in the salivary biomarkers cortisol, haptoglobin, and chromogranin A in pigs. Res Vet Sci. 2014;97:124–8.PubMedView ArticleGoogle Scholar
  26. Arellano PE, Pijoan C, Jacobson ID, Algers B. Stereotyped behaviour, social interactions and suckling pattern of pigs housed in groups or in single crates. Appl Anim Behav Sci. 1992;2:157–66.View ArticleGoogle Scholar
  27. Brouns F, Edwards SA. Social rank and feeding behaviour of group-housed sows fed competitively or ad libitum. Appl Anim Behav Sci. 1994;39:225–35.View ArticleGoogle Scholar
  28. Razdan P, Mwanza AM, Kindahl H, Hultén F, Einarsson S. Impact of postovulatory food deprivation on the ova transport, hormonal profiles and metabolic changes in sows. Acta Vet Scand. 2001;42:45–55.PubMedPubMed CentralView ArticleGoogle Scholar
  29. Tucker AL, Atkinson JL, Millman ST, Widowski TM. Metabolic indicators of nutritional stress are not predictive of abnormal oral behavior in piglets. Physiol Behav. 2010;100(4):277–83.PubMedView ArticleGoogle Scholar
  30. Song C, Jiang J, Han X, Yu G, Pang Y. Effect of immunological stress to neuroendocrine and gene expression in different swine breeds. Mol Biol Rep. 2014;41:3569–76.PubMedView ArticleGoogle Scholar
  31. Tuchscherer A, Kanitz E, Puppe B, Tuchscherer A, Viergutz T. Changes in endocrine and immune responses of neonatal pigs exposed to a psychosocial stressor. Res Vet Sci. 2009;87:380–8.PubMedView ArticleGoogle Scholar
  32. Wrona D, Trojniar W, Borman A, Ciepielewski Z, Tokarski J. Stress induced changes in peripheral natural killer cell cytotoxicity in pigs may not depend on plasma cortisol. Brain Behav Immun. 2001;15:54–64.PubMedView ArticleGoogle Scholar
  33. Wirtz PH, von Känel R, Emini L, Suter T, Fontana A, Ehlert U. Variations in anticipatory cognitives stress appraisal and differential proinflammatory cytokine expression in response to acute stress. Brain Behav Immun. 2007;21:851–9.PubMedView ArticleGoogle Scholar
  34. Morrow-Tesch JL, McGlone JJ, Salak-Johnson JL. Heat and social stress effects on pig immune measures. J Anim Sci. 1994;72(10):2599–609.PubMedGoogle Scholar
  35. Merlot E, Mounier AM, Prunier A. Endocrine response of gilts to various common stressors: A comparison of indicators and methods of analysis. Physiol Behav. 2011;102:259–65.PubMedView ArticleGoogle Scholar
  36. Prunier A, Mounier AM, Hay M. Effects of castration, tooth resection, or tail docking on plasma metabolites and stress hormones in young pigs. J Anim Sci. 2005;83:216–22.PubMedView ArticleGoogle Scholar
  37. Campbell JM, Crenshaw JD, Polo J. The biological stress of early weaned piglets. J Anim Sci Biotechnol. 2013;4:19–23.PubMedPubMed CentralView ArticleGoogle Scholar
  38. Brown SN, Knowles TG, Wilkins LJ, Chadd SA, Warriss PD. The response of pigs to being loaded or unloaded onto commercial animal transporters using three systems. Vet J. 2005;170:91–100.PubMedView ArticleGoogle Scholar
  39. Goodband B, Tokach M, Dritz S, de Rouchey J, Woodworth J. Practical starter pig amino acid requirements in relation to immunity, gut health and growth performance. J Anim Biotechnol. 2014;5:12–23.View ArticleGoogle Scholar
  40. Council Regulation (EC) No 1/2005 of 22 December 2004. on the protection of animals during transport and related operations and amending Directives 64/432/EEC and 93/119/EC and Regulation (EC) No 1255/97. Official Journal of European Union. 5.1.2005.Google Scholar
  41. Squires EJ. Effects on Animal Behaviour. Health and Welfare. In: Squires EJ, editor. Applied Animal Endocrinology. Cambridge: CABI Publishing; 2003. p. 192–225.View ArticleGoogle Scholar
  42. Sonoda LT, Fels M, Oczak M, Vranken E, Ismayilova G, Guarino M, Viazzi S, Bahr C, Berckmans D, Hartung J. Tail biting in pigs-causes and management intervention strategies to reduce the behavioural disorder. A review. Berl Munch Tierarztl Wochenschr. 2013;126:104–12.PubMedGoogle Scholar
  43. Valros A, Munsterhjelm C, Puolanne E, Ruusunen M, Heinonen M, Peltoniemi OAT, Pösö AR. Physiological indicators of stress and meat and carcass characteristics in tail bitten slaughter pigs. Acta Vet Scand. 2013;55:75.PubMedPubMed CentralView ArticleGoogle Scholar
  44. Ruis MA, Brake JH, Engel B, Buist WG, Blokhuis HJ, Koolhaas JM. Adaptation to social isolation. Acute and long-term stress responses of growing gilts with different coping characteristics. Physiol Behav. 2001;73:541–51.PubMedView ArticleGoogle Scholar
  45. Dallman MF, Hellhammer D. Regulation of the hypothalamo-pituitary-adrenal axis, chronic stress, and energy: The role of the brain and networks. In: Contrada RJ, Baum A, editors. The Handbook of Stress Science: Biology, Psychology, and Health. New York: Springer Publishing Company; 2011. p. 11–36.Google Scholar
  46. Rivier C, Rivest S. Effect of stress on the activity of the hypothalamic-pituitary-gondal axis: Peripheral and central mechanisms. Biol Reprod. 1991;45:523–32.PubMedView ArticleGoogle Scholar
  47. Chrousos GP, Torpy DJ, Gold PW. Interactions between the hypothalamic-pituitary-adrenal axis and the female reproductive system: clinical implications. Ann Intern Med. 1998;129:229–40.PubMedView ArticleGoogle Scholar
  48. Norman RL, Smith CJ. Restraint inhibits luteinizing hormone and testosterone secretion in intact male rhesus macaques: effects of concurrent naloxone administration. Neuroendocrinol. 1992;55:405–15.View ArticleGoogle Scholar
  49. Einarsson S, Brandt Y, Lundeheim N, Madej A. Stress and its influence on reproduction in pigs: a review. Acta Vet Scand. 2008;50:48.PubMedPubMed CentralView ArticleGoogle Scholar
  50. Dhabhar FS. Enhancing versus suppressive effects of stress on immune function: Implications for immunoprotection and immunopathology. Neuroimmunomodulat. 2009;16:300–17.View ArticleGoogle Scholar
  51. Dhabhar FS, Miller AH, McEwen BS, Spencer RL. Effects of stress on inmune cell distribution-dynamics and hormonal mechanisms. J Immunol. 1995;154:5511–27.PubMedGoogle Scholar
  52. Dhabhar FS, McEwen BS. Bidirectional effects of stress and glucocorticoid hormones on immune function: possible explanations for paradoxical observartions. In: Ader R, Felten DL, Cohen N, editors. Psychoneuroimmunology. San Diego: Elsevier Academic Press; 2001. p. 301–38.Google Scholar
  53. Smulders D, Verbeke G, Mormède P, Geers R. Validation of a behavioural observation tool to assess pig welfare. Physiol Behav. 2006;89:438–47.PubMedView ArticleGoogle Scholar
  54. Hyung Y, Ellis M, Johnson RW. Effects of feeder type, space allowance, and mixing on the growth performance and feed intake pattern of growing pigs. J Anim Sci. 1998;76(11):2771–8.View ArticleGoogle Scholar
  55. Lee C, Gilesc LR, Brydena WL, Downing JL, Owense PC, Kirby AC, Wynn PC. Performance and endocrine responses of group housed weaner pigs exposed to the air quality of a commercial environment. Livest Prod Sci. 2005;93:255–62.View ArticleGoogle Scholar
  56. Hicks TA, McGlone JJ, Whisnant CS, Kattesh HG, Norman RL. Behavioural, endocrine, immune and performance measures for pigs exposed to acute stress. J Anim Sci. 1998;76:474–83.PubMedView ArticleGoogle Scholar
  57. Proudfoot K, Habing G. Social stress as a cause of diseases in farm animals: current knowledge and future directions. Vet J. 2015;206:15–21.PubMedView ArticleGoogle Scholar
  58. O’Driscoll K, Teixeirab DL, O’Gormana D, Taylora S, Boyle LA. The influence of a magnesium rich marine supplement on behaviour, salivary cortisol levels, and skin lesions in growing pigs exposed to acute stressors. Appl Anim Behav Sci. 2013;145:92–101.View ArticleGoogle Scholar
  59. Ott S, Moons CPH, Kashiha MA, Bahr C, Tuyttens FAM, Berckmans D, Niewold TA. Automated video analysis of pig activity at pen level highly correlates to human observations of behavioural activities. Livest Sci. 2014;160:132–7.View ArticleGoogle Scholar
  60. Nilsson M, Herlin AH, Ardö H, Guzhva O, Åström K, Bergsten C. Development of automatic surveillance of animal behaviour and welfare using image analysis and machine learned segmentation technique. Animal. 2015;9(11):1859–65.PubMedView ArticleGoogle Scholar
  61. Ayala I, Martos N, Silvan G, Gutierrez-Panizo C, Clavel J, Illera J. Cortisol, adrenocorticotropic hormone, serotonin, adrenaline, and noradrenaline serum concentrations in relation to disease and stress in the horse. Res Vet Sci. 2012;93:103–7.PubMedView ArticleGoogle Scholar
  62. Hart KA. The use of cortisol for the objective assessment of stress in animals: pros and cons. Vet J. 2012;192(2):137–9.PubMedView ArticleGoogle Scholar
  63. Escribano D, Tvarijonaviciute A, Tecles F, Cerón JJ. Serum paraoxonase type-1 activity in pigs: Assay validation and evolution after an induced experimental inflammation. Vet Immunol Immunop. 2015;163(3–4):210–5.View ArticleGoogle Scholar
  64. Nater UM, Rohleder N. Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: Current state of research. Psychoneuroendocrino. 2009;34:486–96.View ArticleGoogle Scholar
  65. Granger DA, Kivlighan KT, El-Sheikh M, Gordis EB, Stroud LR. Salivary alpha-amylase in biobehavioural research: recent developments and applications. Ann NY Acad Sci. 2007;1098:122–44.PubMedView ArticleGoogle Scholar
  66. DeCaro JA. Methodological considerations in the use of salivary a-amylase as a stress marker in field research. Am J Hum Biol. 2008;20:617–9.PubMedView ArticleGoogle Scholar
  67. Fuentes M, Tecles F, Gutiérrez A, Otal J, Martínez-Subiela S, Cerón JJ. Validation of an automated method for salivary alpha-amylase measurements in pigs (Sus Scrofa Domesticus) and its application as a stress biomarker. J Vet Diagn Invest. 2011;23:282–7.PubMedView ArticleGoogle Scholar
  68. Taupenot L, Harper KL, O'Connor DT. Mechanisms of disease: The chromogranin-secretogranin family. N Engl J Med. 2003;348:1134–49.PubMedView ArticleGoogle Scholar
  69. Takiyyuddin MA, Cervenka JH, Sullivan PA, Pandian MR, Parmer RJ, Barbosa JA, O'Connor DT. Is physiologic sympathoadrenal catecholamine release exocytotic in human? Circulation. 1990;81(1):185–95.PubMedView ArticleGoogle Scholar
  70. Winkler H, Fischer-Colbrie R. The chromogranins A and B: The first 25 years and future perspectives. Neuroscience. 1992;49:497–528.PubMedView ArticleGoogle Scholar
  71. Hendy GN, Bevan S, Mattei MG, Mouland AJ. Chromogranin A. Clinical and investigative. Medicine. 1995;18(1):47–65.Google Scholar
  72. Sato F, Kanno T, Nagasawa S, Yanaihara N, Ishida N, Hasegawa T, Iwanaga T. Immunohistochemical localization of chromogranin A in the acinar cells of equine salivary glands contrasts with rodent glands. Cells Tissues Organs. 2002;172:29–36.PubMedView ArticleGoogle Scholar
  73. Saruta J, Tsukinoki K, Sasaguri K, Ishii H, Yasuda M, Osamura YR, Watanabe Y, Sato S. Expression and localization of chromogranin A gene and protein in human submandibular gland. Cells Tissues Organs. 2005;180:237–44.PubMedView ArticleGoogle Scholar
  74. Huang Y, Liu W, Yin C, Zhao R, Yang X. Response to lipopolysaccharide in salivary components and the submandibular gland of pigs. Livest Sci. 2014;167:323–30.View ArticleGoogle Scholar
  75. Kanno T, Asada N, Yanase H, Iwanaga T, Nishikawa Y, Hoshino M, Yanaihara N. Autonomic control of submandibular chromogranin A secretion in the anaesthetized rat. Biomed Res. 1998;19:411–4.View ArticleGoogle Scholar
  76. Akiyoshi H, Aoki M, Shimada T, Noda K, Kumagai D, Saleh N, Sugii S, Ohashi F. Measurement of plasma chromogranin A concentrations for assessment of stress responses in dogs with insulin-induced hypoglycemia. Am J Vet Res. 2005;66:1830–5.PubMedView ArticleGoogle Scholar
  77. Dimsdale JE, O’Connor DT, Ziegler M, Mills P. Chromogranin A correlates with norepinephrine release rate. Life Sci. 1992;51:519–25.PubMedView ArticleGoogle Scholar
  78. Gallina S, Di Mauro M, D’Amico MA, D’Angelo E, Sablone A, Di Fonso A, Bascelli A, Izzicupo P, Di Baldassarre A. Salivary chromogranin A, but not a-amylase, correlates with cardiovascular parameters during high-intensity exercise. Clin Endocrinol. 2011;75:747–52.View ArticleGoogle Scholar
  79. Kennedy B, Dillon E, Mills PJ, Ziegler MG. Catecholamines in human saliva. Life Sci. 2001;69:87–99.PubMedView ArticleGoogle Scholar
  80. Escribano D, Soler L, Gutiérrez AM, Martínez-Subiela S, Cerón JJ. Measurement of chromogranin A in porcine saliva: Validation of a time-resolved immunofluorometric assay and evaluation of its application as a marker of acute stress. Animal. 2013;7:640–7.PubMedView ArticleGoogle Scholar
  81. Escribano D, Gutiérrez AM, Fuentes-Rubio M, Cerón JJ. Saliva chromogranin A in growing pigs: A study of circadian patterns during daytime and stability under different storage conditions. Vet J. 2014;199(3):355–9.PubMedView ArticleGoogle Scholar
  82. Gallangher NL, Giles LR, Wynn PC. The development of a circadian pattern of salivary cortisol secretion in the neonatal piglet. Biol Neonate. 2002;81:113–8.View ArticleGoogle Scholar
  83. Hillmann E, Schrader L, Mayer C, Gygax L. Effects of weight, temperature and behaviour on the circadian rhythm of salivary cortisol in growing pigs. Animal. 2008;2:405–9.PubMedView ArticleGoogle Scholar
  84. Muneta Y, Yoshikawa T, Minagawa Y, Shibahara T, Maeda R, Omata Y. Salivary IgA as a useful non-invasive marker for restraint stress in pigs. J Vet Med Sci. 2010;72:1295–300.PubMedView ArticleGoogle Scholar
  85. Bottoms GD, Roesel OF, Rausch FD, Akins EL. Circadian variation in plasma cortisol and corticosterone in pigs and mares. Am J Vet Res. 1972;33(4):785–90.PubMedGoogle Scholar
  86. Lawrence AB, Petherick JC, McLean KA, Dean LA, Chirnside J, Vaughan A, Clutton E, Terlouw EMC. The effects of environment on behaviour, plasma cortisol and prolactin in parturient sows. Appl Anim Behav Sci. 1994;39:313–30.View ArticleGoogle Scholar
  87. Barnett JL, Cronin GM, McCallum TH. Effects of grouping unfamiliar adults pigs after dark, after treatment with amperozide and by using pens with stalls, on aggression, skin lesions and plasma cortisol concentrations. Appl Anim Behav Sci. 1996;50:121–33.View ArticleGoogle Scholar
  88. Pol F, Courboulay V, Cotte J, Martrenchar A, Hay M, Mormède P. Urinary cortisol as an additional tool to assess the welfare of pregnant sows kept in two types of housing. Vet Res. 2002;33:13–22.PubMedView ArticleGoogle Scholar
  89. Mormède P, Andanson S, Aupérin B, Beerda B, Guémené D, Malmkvist J, Manteca X, Manteuffel G, Prunet P, Van Reenen CG, Richard S, Veissier I. Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiol Behav. 2007;92:317–39.PubMedView ArticleGoogle Scholar
  90. Désautés C, Bidanel JP, Mormède P. Genetic study of behavioural and pituitary-adrenocortical reactivity in response to an environmental challenge in pigs. Physiol Behav. 1997;62:337–45.PubMedView ArticleGoogle Scholar
  91. Ruis MAW, Brake JHA, Engel B, Ekkel ED, Buist WG, Blokhuis HJ, Koolhaas JM. The circadian rhythm of salivary cortisol in growing pigs: effects of age, gender, and stress. Physiol Behav. 1997;62:623–30.PubMedView ArticleGoogle Scholar
  92. Möstl E, Palme R. Hormones as indicators of stress. Domest Anim Endocrin. 2002;23:67–74.View ArticleGoogle Scholar
  93. de Jong IC, Prelle TI, van De Burgwal JA, Lambooij E, Korte SM, Blokhuis HJ, Koolhaas JM. Effects of environmental enrichment on behavioural responses to novelty, learning, and memory, and the circadian rhythm in cortisol in growing pigs. Physiol Behav. 2000;68:571–8.PubMedView ArticleGoogle Scholar
  94. de Leeuw JA, Ekkel ED. Effects of feeding level and the presence of a foraging substrate on the behaviour and stress physiological response of individually housed gilts. Appl Anim Behav Sci. 2004;86:15–25.View ArticleGoogle Scholar
  95. Ekkel ED, Dieleman SJ, Schouten WGP, Portela A, Corni-Lissen G, Tielen MJM, Halberg F. The circadian rhythm of cortisol in the saliva of young pigs. Physiol Behav. 1996;60:985–9.PubMedView ArticleGoogle Scholar
  96. Evans FD, Christopherson RJ, Aherne FX. Development of the cyrcadian rhythm of cortisol in the gilt from weaning until puberty. Can J Anim Sci. 1988;68:1105–11.View ArticleGoogle Scholar
  97. Escribano D, Fuentes-Rubio M, Cerón JJ. Validation of an automated chemiluminescent immunoassay for salivary cortisol measurements in pigs. J Vet Diagn Invest. 2012;24:918–23.PubMedGoogle Scholar
  98. Piñeiro M, Piñeiro C, Carpintero R, Morales J, Campbell FM, Eckersall PD, Toussaint MJM, Lampreave F. Characterisation of the pig acute phase protein response to road transport. Vet J. 2007;173:669–74.PubMedView ArticleGoogle Scholar
  99. McGlone JJ, Salak JL, Lumpkin EA, Nicholson RI, Gibson M, Norman RL. Shipping stress and social status effects on pig performance, plasma cortisol, natural killer cell activity, and leukocyte numbers. J Anim Sci. 1993;71(4):888–96.PubMedGoogle Scholar
  100. Nargund VH. Effects of psychological stress on male fertility. Nat Rev Urol. 2015;12:373–82.PubMedView ArticleGoogle Scholar
  101. Toufexis D, Rivarola MA, Lara H, Viau V. Stress and the reproductive axis. J Neuroendocrinol. 2014;26(9):573–86.PubMedPubMed CentralView ArticleGoogle Scholar
  102. Chichinadze K, Chichinadze N. Stress-induced increase of testosterone: Contributions of social status and sympathetic reactivity. Physiol Behav. 2008;94:595–603.PubMedView ArticleGoogle Scholar
  103. Escribano D, Fuentes-Rubio M, Cerón JJ. Salivary testosterone measurements in growing pigs: validation of an automated chemiluminescent immunoassay and its possible use as an acute stress marker. Res Vet Sci. 2014;97(1):20–5.PubMedView ArticleGoogle Scholar
  104. Bilandzic N, Simic B, Kmetic I. Effect of three-day ACTH administration on concentrations of cholesterol, cortisol, progesterone, testosterone and LH in the boars. Slov Vet Res. 2012;49(3):123–32.Google Scholar
  105. Murata H, Shimada N, Yoshioka M. Current research on acute phase proteins in veterinary diagnosis: an overview. Vet J. 2004;168:28–40.PubMedView ArticleGoogle Scholar
  106. Baumann H, Gauldie J. The acute phase response. Immunol Today. 1994;15:74–80.PubMedView ArticleGoogle Scholar
  107. Cray C, Zaias J, Altman NH. Acute phase response in animals: a review. Comparative Med. 2009;59(6):517–26.Google Scholar
  108. Eckersall PD. Recent advances and future prospects for the use of acute phase proteins as markers of disease in animals. Rev Med Vet-Toulouse. 2000;151(7):577–84.Google Scholar
  109. Piñeiro C, Piñeiro M, Morales J, Andrés M, Lorenzo E, Pozo MD, Álava MA, Lampreave F. Pig-MAP and haptoglobin concentration reference values in swine from commercial farms. Vet J. 2009;179:78–84.PubMedView ArticleGoogle Scholar
  110. Soler L, Gutiérrez A, Escribano D, Fuentes M, Cerón JJ. Response of salivary haptoglobin and serum amyloid A to social isolation and short road transport stress in pigs. Res Vet Sci. 2013;95:298–302.PubMedView ArticleGoogle Scholar
  111. Murata H. Stress and acute phase protein response: An inconspicuous but essential linkage. Vet J. 2007;173:473–4.PubMedView ArticleGoogle Scholar
  112. Johnson JD, Campisi J, Sharkey CM, Kennedy SL, Nickerson BN, Greenwood BN, Fleshner M. Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience. 2005;135:1295–307.PubMedView ArticleGoogle Scholar
  113. González-Ramón N, Hoebe K, Álava MA, Van Leengoed L, Piñeiro M, Carmona S, Iturralde M, Lampreave F, Piñeiro A. Pig MAP/ITIH4 and haptoglobin are interleukin-6-dependent acute phase serum proteins in porcine primary cultured hepatocytes. Eur J Biochem. 2000;267:1878–85.PubMedView ArticleGoogle Scholar
  114. García-Celdrán M, Ramis G, Quereda JJ, Armedo E. Reduction of transport-induced stress on finishing pigs by increasing lairage time at the slaughter house. J Swine Health Prod. 2012;20(3):118–22.Google Scholar
  115. Piñeiro C, Piñeiro M, Morales J, Carpintero R, Campbell FM, Eckersall PD, Toussaint MJM, Álava MA, Lampreave F. Pig acute-phase protein levels after stress induced by changes in the pattern of food administration. Animal. 2007;1:133–9.PubMedView ArticleGoogle Scholar
  116. Zaine L, Ferreira C, Gomes Mde O, Monti M, Tortola L, Vasconcellos RS, Carciofi AC. Faecal IgA concentration is influenced by age in dogs. Brit J Nutr. 2011;106:183–6.View ArticleGoogle Scholar
  117. Guhad FA, Hau J. Salivary IgA as a marker of social stress in rats. Neurosci Lett. 1996;216:137–40.PubMedView ArticleGoogle Scholar
  118. Kikkawa A, Uchida Y, Nakade T, Taguchi K. Salivary secretory IgA concentrations in beagle dogs. J Vet Med Sci. 2003;65(6):689–93.PubMedView ArticleGoogle Scholar
  119. Wetherell MA, Hyland ME, Harris JE. Secretory immunoglobulin A reactivity to acute and cumulative acute multi-tasking stress: relationships between reactivity and perceived workload. Biol Psychol. 2004;66:257–70.PubMedView ArticleGoogle Scholar
  120. Muneta Y, Minagawa Y, Nakane T, Shibahara T, Yoshikawa T, Omata Y. Interleukin-18 expression in pig salivary glands and salivary content changes during acute immobilization stress. Stress. 2011;14:549–56.PubMedView ArticleGoogle Scholar
  121. Escribano D, Campos PHRF, Gutiérrez AM, Le Floc N, Cerón JJ, Merlot E. Effect of repeated administration of lipopolysaccharide on inflammatory and stress markers in saliva of growing pigs. Vet J. 2014;200(3):393–7.PubMedView ArticleGoogle Scholar
  122. Conti B, Jahng JW, Tinti C, Son JH, Joh TH. Induction of interferon-γ inducing factor in the adrenal cortex. J Biol Chem. 1997;272:2035–7.PubMedView ArticleGoogle Scholar
  123. Stoll S, Müller G, Kurimoto M, Saloga J, Tanimoto T, Yamauchi H, Okamura H, Knop J, Enk AH. Production of IL-18 (IFN-gamma-inducing factor) messenger RNA and functional protein by murine keratinocytes. J Immunol. 1997;159(1):298–302.PubMedGoogle Scholar
  124. Kawakami K, Qureshi MH, Zhang T, Okamura H, Kurimoto M, Saito A. IL-18 protects mice against pulmonary and disseminated infection with Cryptococcus neoformans by inducing IFN-gamma production. J Immunol. 1997;159(11):5528–34.PubMedGoogle Scholar
  125. Micallef MJ, Yoshida K, Kawai S, Hanaya T, Kohno K, Arai S, Tanimoto T, Torigoe K, Fuji M, Ikeda M, Kurimoto M. In vivo antitumor effects of murine interferon-gamma-inducing factor/interleukin-18 in mice bearing syngeneic Meth A sarcoma malignant ascites. Cancer Immunol Immun. 1997;43:361–7.View ArticleGoogle Scholar
  126. Conti B, Sugama S, Kim Y, Tinti C, Kim H, Baker H, Volpe B, Attardi B, Joh T. Modulation of IL-18 production in the adrenal cortex following acute ACTH or chronic corticosterone treatment. Neuroimmunomodulation. 2000;8(1):1–7.PubMedView ArticleGoogle Scholar

Copyright

© The Author(s). 2016

Advertisement